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THESE DE DOCTORAT DE L’UNIVERSITE LUMIERE LYON 2 Ecole Doctorale de Sciences Cognitives Doctorat de Sciences Cognitives - mention Neurosciences présentée par Jane PLAILLY La mémoire olfactive humaine : Neuroanatomie fonctionnelle de la discrimination et du jugement de la familiarité Soutenue publiquement le 16 septembre 2005 devant le jury composé de : Dr. Sylvie Issanchou INRA, Dijon, France Rapporteur Pr. David A. Kareken IUPUI, Indianapolis, USA Examinateur Dr. Jean-Pierre Royet CNRS 5020, Lyon, France Directeur de thèse Pr. Rémy Versace Univ. Lyon2, Lyon, France Examinateur Pr. Robert J. Zatorre McGill Univ., Montréal, Canada Examinateur Laboratoire d’accueil : Laboratoire Neurosciences & Systèmes Sensoriels, UMR CNRS 5020, Université Claude Bernard Lyon1, 50 av. Tony Garnier, 69366 Lyon cedex 07, France. Rapporteurs : Dr. Driss Boussaoud, INCM, CNRS 6193, Marseille, France et Dr. Sylvie Issanchou, INRA, Dijon, France

La mémoire olfactive humaine : Neuroanatomie fonctionnelle de la

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THESE DE DOCTORAT DE L’UNIVERSITE LUMIERE LYON 2

Ecole Doctorale de Sciences Cognitives

Doctorat de Sciences Cognitives - mention Neurosciences

présentée par

Jane PLAILLY

La mémoire olfactive humaine : Neuroanatomie fonctionnelle de la discrimination

et du jugement de la familiarité

Soutenue publiquement le 16 septembre 2005 devant le jury composé de :

Dr. Sylvie Issanchou INRA, Dijon, France Rapporteur

Pr. David A. Kareken IUPUI, Indianapolis, USA Examinateur

Dr. Jean-Pierre Royet CNRS 5020, Lyon, France Directeur de thèse

Pr. Rémy Versace Univ. Lyon2, Lyon, France Examinateur

Pr. Robert J. Zatorre McGill Univ., Montréal, Canada Examinateur

Laboratoire d’accueil : Laboratoire Neurosciences & Systèmes Sensoriels, UMR CNRS 5020, Université Claude Bernard Lyon1, 50 av. Tony Garnier, 69366 Lyon cedex 07, France.

Rapporteurs : Dr. Driss Boussaoud, INCM, CNRS 6193, Marseille, France et Dr. Sylvie Issanchou, INRA, Dijon, France

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Remerciements

Mes remerciements vont en premier lieu à Jean-Pierre Royet, avec qui je travaille depuis

maintenant 6 ans. Jean-Pierre m’a formée à la recherche en toute rigueur, me laissant une vraie liberté

de pensée et me donnant toute sa confiance. Depuis le début, il a aussi cherché à préparer mon avenir

professionnel. Il m’a permis de rencontrer les chercheurs importants dans notre domaine, afin de me

faire connaître de notre communauté scientifique. Rares sont les directeurs de thèse ayant aussi bien

assumé leur fonction de formateur. Il a accepté ces dernières années, sans ciller, de me voir débarquer

dans son bureau, parfaitement convaincue que ce qu’il avançait était faux et que j’avais la vérité. Il

en a suivi de nombreuses discussions scientifiques enrichissantes, se soldant par l’existence d’une

centaine de versions d’un même article… Il a accepté mes choix personnels avec respect, en étant

toujours à mes côtés, dans les moments difficiles comme dans les moments de grandes joies. Il n’a cessé

de me proposer son aide durant toutes ces années, aide dont j’ai grandement abusé dans l’élaboration

de cette thèse. Il est peu de dire que ce manuscrit est né de notre entière collaboration…

Je remercie Barbara Tillmann pour les discussions exigeantes que nous avons eues. J’ai aimé cette

volonté de décortiquer jusqu’au bout chaque processus de façon à faire émerger mille autres questions

qui n’auront jamais de réponse ! J’ai aimé l’atmosphère honnête, attentive et amitieuse de ces

discussions. Ce furent de très bons moments.

Je remercie profondément David Kareken pour m’avoir accueillie si gentiment pendant 6 mois

dans son équipe de recherche, et dans sa famille… En sa compagnie, j’ai approfondi mes

connaissances scientifiques, assisté au 5 hundred miles, goûté mes premiers ‘vrais’ hamburgers, discuté

politique en buvant un Martini… David m’a fait l’honneur d’être aussi présent pendant la

soutenance de ma thèse, et je le remercie du soutient qu’il m’a toujours apporté. Je tiens aussi à

remercier toute son équipe pour m’avoir fait une place en leur sein pendant ce séjour : Judy, Alex,

Merav, Regat, Leigh, Cami et Lyn.

Je tiens à remercier Robert Zatorre d’avoir accepté de traverser l’atlantique pour participer à ma

soutenance de thèse. Je le remercie de la pertinence de ses critiques ainsi que des échanges amicaux que

nous avons eu durant son séjour.

Je veux remercier aussi les Sylvie Issanchou et Driss Boussaoud pour m’avoir accordé un peu de

leur temps en étant les rapporteurs de ma thèse. Ces critiques ont égrené dans mon manuscrit de

nouvelles questions et de nouvelles réflexions. Elles m’ont donné envie d’aborder des questions sous un

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angle nouveau, ont aiguisé ma curiosité… Merci !

Je remercie le Pr. Rémy Versace d’avoir présidé mon jury de thèse. J’ai bon espoir que, à l’avenir,

nous rediscutions des différents théoriques qui nos opposent afin qu’ils puissent alors nous enrichir.

Je veux remercier les psychiatres Thierry d’Amato et Mohamed Saoud pour l’opportunité qu’ils

m’ont offerte de travailler avec les patients qu’ils suivaient. J’ai grandement apprécié leur vision

tolérante de la maladie, ainsi que l’approche respectueuse des patients et désireuse de leur bien-être.

Merci à Bruno Wicker pour notre collaboration enrichissante.

Je remercie Lionel Collet pour m’avoir accueillie au Laboratoire Neurosciences & Systèmes

Sensoriels.

Cette thèse est l’aboutissement de 4 années de travail dont le quotidien a été embelli par mon ami

Samy, la bouille en face de moi avec un grand sourire, mon acolyte du 217. Je garde en souvenir les

goûters en tête à tête, l’émerveillement devant les couchers de soleil, les discussions sur l’opposition

entre hasard et rationalité, les joies quotidiennes, les moments de doutes, de mal-être… Il a apporté

un esprit festif, et moi un esprit studieux. Plutôt que de nous opposer, ce cocktail nous a épanouis.

Merci de cette amitié riche en confiance et en respect.

Et merci à Alex bien sûr ! Elle m’a fait partager sa passion pour la science, m’obligeant alors à

m’impliquer un peu plus dans mon travail, exigeant de moi une plus grande curiosité. Il en est né une

chère amitié.

Merci enfin à tous ceux qui ont permis que mon travail au labo se fasse dans une si bonne

ambiance : Catherine, Nico, Fabien, Etienne, Tristan, Alex, Samuel, Moustafa et les anciens : TTD,

Gaëtan, Damien et Jeanne.

Ce travail n’aurait pu aboutir sans l’aide de l’équipe technique de notre laboratoire, Vincent

Farget, Bernard Bertrand, Michel Vigouroux et Samuel Garcia ; de Chantal Delon-Martin, Mathilde

Pachot-Clouard et Christoph Segebarth, de l’UM594 de l’UJF (Grenoble) ; de Nicolas Costes, Franck

Lavenne, et des infirmières Christine et Martine du Cermep (Lyon) ; et enfin de Jean-Luc Anton,

Muriel Roth et de Bruno Nazarian du Centre IRMf du CHU La Timone (Marseille).

Mes profonds remerciements vont enfin à tous les sujets qui ont participé aux expériences, et qui

ont accepté de sentir des odeurs parfois pour le moins ‘surprenantes’ … : les étudiants de Lyon, ceux

de Marseille, ceux d’Indianapolis, les Parfumeurs, les étudiants de l’ISIPCA et les patients du CH le

Vinatier (Lyon).

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References

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www.elsevier.com/locate/ynimg

NeuroImage 24 (2005) 1032–1041

Involvement of right piriform cortex in olfactory

familiarity judgments

Jane Plailly,a,* Moustafa Bensafi,a Mathilde Pachot-Clouard,b Chantal Delon-Martin,b

David A. Kareken,c Catherine Rouby,a Christoph Segebarth,b and Jean-P. Royeta,d

aNeurosciences et Systemes Sensoriels, Universite Claude Bernard Lyon 1, UMR CNRS 5020, IFR 19, Institut Federatif des Neurosciences de Lyon,

50 Avenue Tony Garnier, 69366 Lyon Cedex 07, FrancebUnite mixte INSERM/Universite Joseph Fourier U594, LRC-CEA, Hopital Michallon, 38043 Grenoble, FrancecNeuropsychology Section, Department of Neurology, Indiana University School of Medicine, Indianapolis, IN 46202, USAdCERMEP, 69003 Lyon, France

Received 16 April 2004; revised 12 October 2004; accepted 26 October 2004

Available online 9 December 2004

Previous studies have shown activation of right orbitofrontal cortex

during judgments of odor familiarity. In the present study, we sought to

extend our knowledge about the neural circuits involved in such a task

by exploring the involvement of the right prefrontal areas and limbic/

primary olfactory structures. Fourteen right-handed male subjects

were tested using fMRI with a single functional run of two olfactory

conditions (odor detection and familiarity judgments). Each condition

included three epochs. During the familiarity condition, subjects rated

whether odors were familiar or unfamiliar. During the detection

condition, participants decided if odors were present. When contrasting

the familiarity with the detection conditions, activated areas were found

mainly in the right piriform cortex (PC) and hippocampus, the left

inferior frontal gyrus and amygdala, and bilaterally in the mid-fusiform

gyrus. Further analyses demonstrated that the right PC was more

strongly activated than the left PC. This result supports the notion that

the right PC is preferentially involved in judgments of odor familiarity.

D 2004 Elsevier Inc. All rights reserved.

Keywords: Olfaction; Familiarity judgment; Recognition memory; Piriform

cortex; fMRI

Introduction

Hemispheric asymmetry is well-established for high-level brain

functions such as language and spatial attention (e.g., Broca, 1863;

Weintraub and Mesulam, 1987). Hemispheric predominance also

exists in sensory functions such as hand somatosensory represen-

tation (Soros et al., 1999) and temporal and spectral auditory

resolution (Zatorre et al., 2002). Studies in olfaction lead to similar

conclusions. Early cerebral imaging studies showed functional

1053-8119/$ - see front matter D 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.neuroimage.2004.10.028

* Corresponding author. Fax: +33 4 37 28 76 01.

E-mail address: [email protected] (J. Plailly).

Available online on ScienceDirect (www.sciencedirect.com).

95

lateralization of olfactory processes in the right hemisphere,

especially in orbitofrontal cortex (OFC) (Zatorre et al., 1992);

most subsequent studies confirm this result (Dade et al., 1998;

Sobel et al., 1998; Yousem et al., 1997). However, Zald and

colleagues reported stronger activation in the left OFC and

amygdala for very aversive odors, pointing to these areas as being

important in the emotional processing of olfactory information

(Zald and Pardo, 1997; Zald et al., 1998). Using positron emission

tomography (PET), Royet et al. (1999, 2001) found that judgments

of odor familiarity preferentially activated right OFC, whereas

hedonic judgments principally activated left OFC.

Beyond OFC, recent cerebral imaging data have extended these

observations to piriform cortex (PC). In a functional magnetic

resonance imaging (fMRI) study, we showed that left piriform–

amygdala region activation was associated with subjects’ ratings of

the odorants’ emotional intensities (Royet et al., 2003), a result

consistent with Gottfried et al.’s (2002) and Anderson et al.’s

(2003) findings. Convergent results from Dade et al.’s (2002)

lesion and PET studies further show that the piriform region

mediates olfactory long-term recognition memory, giving support

to the notion that this area may be more than primary sensory

cortex (e.g., Schoenbaum and Eichenbaum, 1995). Specifically,

Dade et al. (2002) found that the extent of piriform activity

corresponded with different cognitive demands, in which PC

activity followed a continuum between mnemonic encoding (no

significant activity), to short-term recognition (weak bilateral

activity), to long-term recognition (strong bilateral activity). These

authors further suggested that piriform activity could be related to

odor familiarity, which would require that subjects compare odors

with previously stored olfactory representations, and thus represent

a type of long-term olfactory reference memory.

In the present study, we explored that question by specifically

asking whether PC is involved in the processing of odor familiarity,

and if so, whether familiarity-evoked activations are lateralized, as

previously suggested (Royet et al., 1999, 2001). We studied

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J. Plailly et al. / NeuroImage 24 (2005) 1032–1041 1033

familiarity judgments and their relation to PC activation with fMRI

using a classical block paradigm design. Familiar and unfamiliar

odors were presented in a same epoch allowing subjects to rate

familiarity in a binary fashion by pressing one of two buttons. A

control condition was employed in which subjects had to judge the

presence or absence of an odor. The contrast between both

conditions allowed us to identify the areas specifically involved

in the familiarity judgment of odors.

Materials and methods

Subjects

Fourteen healthy right-handed men (18–32 years old) partici-

pated in the study. Participation required a medical screening.

Exclusion criteria were rhinal disorders (colds, active allergies,

history of nasal-sinus surgery, or asthma), neurologic disease,

ferrous implants (e.g., pacemakers, cochlear implants), or claus-

trophobia. Participants scored at least 87% correct in a forced-

choice suprathreshold detection test, and had a breathing cycle

mean duration of 3.88 s (F0.72). All participants provided written

informed consent as approved by the local Institutional Review

Board, and according to French regulations on biomedical experi-

ments on healthy volunteers.

Odorous stimuli

One hundred and eight stimuli were used, 27 of which were

employed before imaging sessions and 81 of which were used

Table 1

List of odorants selected for the Da, Db, Dc, Fa, Fb, and Fc epochs

Da Db Dc

1 Plum Sage Acacia

2 Turpentine

3

4 Tarragon Orange

5 Parsley Acetophenone

6 Guaiacol

7 Jonquil Camphor

8 Neroli

9 Musk

10 Carrot Pine needle

11 EBA

12 1,4-Dichlorobutane Butanol

13 Eglantine

14

15 Cherry 2-Bromopheno

16 Acetol Liqueur wine Tangerine

17 2-Octanol

18 Liquorice Blackcurrant

Unfamiliar odors

Mean (SD) 4.00 (0.72) 4.11 (0.87) 4.29 (0.92)

Range 3.14–5.11 3.19–5.16 3.09–5.17

Familiar odors

Mean (SD)

Range

Note. EBA, ethyl benzoyl acetate; PPA, phenyl propionaldehyde; SD, standard d

scale, with 1 representing low familiarity, and 10 representing high familiarity (s

96

during scanning. For fMRI, 54 odorants were used for the

familiarity (F) condition and 27 odorants for the detection (D)

condition (Table 1). For F conditions, three sets (Fa, Fb, Fc)

contained nine familiar and nine unfamiliar odorants selected so as

to provide high- and low-familiarity scores from data as derived

from previous work (Royet et al., 1999). Analysis of variance

(ANOVA) indicated that familiarity scores were significantly

higher for familiar than for unfamiliar odorants [F(1,48) =

129.173, P b 0.0001]. For D conditions, three sets (Da, Db, Dc)

contained nine odorants with low familiarity and nine bottles with

odorless air. Odors with low familiarity were selected to avoid

implicit familiarity judgments. For training, three sets of nine low

familiarity odorants and nine bottles with odorless air were used. In

each set, the presentation order of stimuli was pseudorandomized,

but identical for all subjects. Odorants were diluted to a concen-

tration of 10% using mineral oil (Sigma Aldrich, France). For

presentation, 5 ml of this solution was absorbed into compressed

polypropylene filaments inside of a 100 ml white polyethylene

squeeze-bottles equipped with a dropper (Osi, France).

Stimulating and recording materials

Odors were presented using an airflow olfactometer, which

allowed synchronizing stimulation with breathing. The stimulation

equipment was essentially the one used in a previous PET study

(Royet et al., 1999), but adapted so as to avoid interference with

the static magnetic field of the scanner (Royet et al., 2003). Briefly,

the apparatus was split into two modules: the electronic part of the

olfactometer positioned outside the magnet room (shielded with a

Faraday cage), and the nonferrous (DuraluminR) air-dilution

Fa Fb Fc

Apricot Raspberry Citronella

Bergamot Orange Tetralin trans-2-Hexenal

Diethyl ether Mint Cypress

Pine Honey Geranium

Bornyl acetate Patchouli Vienna bread

Caramel Jasmine Anise

Grass Basil Iris

Strawberry Toluene Incense

Pepper Green lily Lavender

Oyster Banana Gingerbread

Gardenia Vanilla Apple

Celery Lily Garlic

Hazelnut Bitter almond PPA

Tar Caprylic aldehyde Rose

l Methyl acetate Passion fruit Thyme

Biscuit Eucalyptus Lime

Tobacco Coconut 1-Octen-3-ol

3-Methyl anisol Clove Camomile

4.56 (0.28) 4.38 (0.39) 4.37 (0.23)

4.03–4.91 3.41–4.69 3.89–4.61

6.53 (0.75) 6.28 (0.67) 6.24 (0.23)

5.13–7.27 4.89–7.24 4.96–6.91

eviation. Italic, familiar odorants. Odorants were rated on a 10-point rating

ee Royet et al., 1999).

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J. Plailly et al. / NeuroImage 24 (2005) 1032–10411034

injection head placed within the stray-field of the magnet.

Compressed air (10 l/min) was pumped into the olfactometer,

and delivered continuously through a standard anesthesia mask. A

detailed description was recently given (Vigouroux et al., in press).

The ventral breathing rhythm of the subject was recordedwith the

aid of a foot bellows in polyvinyl chloride (Herga Electric Limited,

Suffolk, UK) held on the stomach with a weaved cotton belt.

Movements of the abdominal wall produced variations in the internal

volume of the foot bellows. The flow was transformed into an

electrical signal that was amplified, and then successively trans-

mitted to the acquisition system and to a headphone via a voltage-to-

frequency converter. The experimenter could therefore listen to the

progressive frequency variations that accompanied respiration (high

frequency during inspiration and low frequency during expiration).

This method made respiration easily detected for the experimenter

and allowed easy timing of the stimulus delivery. During scanning,

the subject was instructed to avoid sniffing or blocking his breathing,

but instead to breathe regularly, thus allowing the experimenter to

anticipate the beginning of an inspiration phase. One stimulus was

then injected into the olfactometer by squeezing one bottle into the

injection head, so that the odor (or odorless air) was carried to the

subject’s anesthesia mask.

Subjects rated familiarity or judged odor presence by pressing

one of two buttons. The response signal was then transmitted

outside the radiofrequency shielded room by fiber optics to analog-

to-digital converters powered by nickel–cadmium batteries.

Behavioral data were recorded on line (100 Hz sampling rate)

using a NEC PC computer equipped with a digital acquisition

board DAQCard-500 (National Instruments, USA). LabView 5.0

software (National Instruments) was used to acquire, store, and

read data. Data analysis was performed with the WinDaq Wave-

form Browser 1.91 software (DataQ Instruments, USA).

Experimental procedure

A single functional run was presented in blocks that consisted

of two olfactory conditions (F and D) alternating with odorless rest

(R) epochs (Fig. 1). Each epoch lasted 60 s. Both F and D

conditions were presented three times each, either three F followed

by three D conditions or vice versa. Within the same condition, the

presentation order of the three sets (a, b, c) was counterbalanced

across subjects according to a balanced experimental (Latin square)

design. For olfactory conditions, subjects were asked to judge

whether or not they smelled an odor (D condition) or whether the

odor was familiar or unfamiliar (F condition). Subjects were then

asked to make a dyesT or dnoT rating using the two buttons with

Fig. 1. Experimental procedure showing the functional run including 12

epochs of 60 s each. Two olfactory conditions were performed: one

detection condition with three epochs (Da, Db, Dc) and one familiarity

condition with three epochs (Fa, Fb, Fc). Example of an epoch (Da) for

which 15 stimuli (from S1 to S15) were delivered. R, rest.

97

their dominant hand. For half of the subjects, dyesT and dnoTresponses were obtained with the index and the middle fingers,

respectively. For the other half of the subjects, the meaning of the

two key-press buttons was reversed. For the R condition, no

stimulation was provided and the subjects were instructed not to

use the key-press buttons.

General instructions were provided to subjects before the

functional run. During the run, and 3 s before each experimental

condition (F, D or R), subjects were instructed orally by means of

specific keywords (dfamiliarity,T ddetection,T and drestT) which task

was to be performed next. Subjects wore earplugs to protect

hearing from excessive scanner noise and kept their eyes closed

during scanning. The day before the fMRI examination, subjects

were trained outside the MR facility to breathe regularly, to detect

odorants without sniffing during normal inspiration, and to give the

most rapid possible response (odor vs. no odor) using the buttons.

Imaging parameters

Functional MR imaging was performed on a 1.5-T MR imager

(Philips NT). Twenty-five adjacent 5-mm-thick axial slices were

imaged. The imaging volume covered the whole brain and was

oriented parallel to the bicommissural plane. The image planes

were positioned from scout images acquired in the sagittal plane. A

3D three-shot PRESTO MR imaging sequence (Liu et al., 1993)

was used with the following parameters: TR = 26 ms, TE = 38 ms,

flip angle = 148, field-of-view = 256 � 205 mm2, imaging matrix =

64 � 51 (voxel size of 4 � 4 � 5 mm3). This sequence is less

prone to magnetic susceptibility artifacts than the usual echo planar

imaging (EPI) sequence (Van Gelderen et al., 1995), particularly in

the OFC and mesial temporal region (Zald and Pardo, 2000).

During the functional run, the volume of interest was scanned 144

times successively. The signal was averaged three times, leading to

an acquisition time per volume of 5 s. A high-resolution anatomical

3D T1-weighted MR scan was acquired before the functional run.

Data processing and statistical analyses

Functional images were analyzed using SMP99 (Wellcome

Department of Cognitive Neurology, London, UK). Image process-

ing included interscan realignment, spatial normalization to stereo-

tactic space as defined by the Montreal Neurological Institute

(MNI) reference brain template, and image smoothing with a three-

dimensional Gaussian kernel (FWMH: 8 � 8 � 10 mm3) to

overcome residual anatomical variability during group analysis,

increase the signal-to-noise ratio and conform to Random Field

Theory assumptions underlying the statistical analysis (Friston et

al., 1995a). A boxcar reference function was convolved with

SPM99’s dcanonical hemodynamicT response function. A high-pass

filter (cutoff frequency of 1/720 Hz) was used to eliminate

instrumental and physiological very low frequency signal fluctua-

tions. Global differences in BOLD signal were covaried out from all

voxels, and comparisons across conditions were effected with t

tests. The statistical significance of signal differences was assessed

through Z scores in an omnibus sense, using an uncorrected height

threshold (P b 0.001). Only clusters of more than 10 adjacent

activated voxels were taken into account as a significant hemody-

namic response (Z N 3.20 at voxel level). Duvernoy’s (1991) and

Mai et al.’s (1997) anatomic atlases were used to localize and

describe activated anatomic regions as the often used Talairach’s

atlas (Talairach and Tournoux, 1988) describes subcortical and

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Table 2

Behavioral data recorded for the three sets of odors (a, b, c) during the detection and familiarity judgment tasks

Parameter Task Response Set a Set b Set c

Mean number of stimulations Detection 13.33 F 1.87 14.11 F 3.02 13.89 F 1.96

Familiarity 12.89 F 2.20 13.33 F 2.24 13.44 F 2.65

Response accuracy Detection 0.962 F 0.050 0.857 F 0.104 0.930 F 0.078

Reaction time Detection Yes 1.597 F 0.462 1.698 F 0.624 1.625 F 0.487

No 2.125 F 0.602 2.092 F 0.758 2.033 F 0.620

Familiarity Yes 2.141 F 0.668 1.985 F 0.540 2.153 F 0.635

No 2.220 F 0.652 2.346 F 0.730 2.359 F 0.819

Proportion of familiar odors Familiarity 0.545 F 0.214 0.520 F 0.188 0.509 F 0.180

For reaction time, data are given according to whether the odors were detected or not (Yes or No), or whether they were recognized as being familiar or not (Yes

or No).

J. Plailly et al. / NeuroImage 24 (2005) 1032–1041 1035

limbic olfactory regions with much less detail. Activated areas were

indicated using the MNI coordinate system.

Specific effects for the familiarity judgment task were calculated

by comparing the signals during the F and D conditions using the

general linear model (Friston et al., 1995b). Intrasubject analyses

were first performed, followed by a random effects analysis which

extent statistical inferences into the healthy population. This two-

stage analysis accounted first for intrasubject variance (scan-to-

scan), and second for intersubject variance. In the first step, scan-to-

scan variance was separately modeled for each subject by creating a

summary contrast image from weighted parameter estimates that

represented each scan condition. In the second step, these contrast

images were then analyzed using a basic model one-sample t tests

to assess the F–D contrast against a null hypothesis.

A cluster analysis was further performed to compare activation

between the right and left PC. A region of interest (ROI)

corresponding to the right PC was defined by selecting an 8-

mm-diameter sphere centered on coordinates (30, 2, �16) of the

activation cluster obtained in the F–D contrast image from the

group analysis. An identical ROI was centered on the contralateral

coordinate in the left hemisphere (�30, 2, �16). Using the

MarsBar SPM toolbox (Brett et al., 2002), we then obtained a

mean activity level within both ROIs for each one of 12 subjects. A

statistical analysis was then performed to compare the activity

levels of left and right PC.

Fig. 2. Reaction times represented as a function of the olfactory task

(Detection vs. Familiarity) and of the type of response (Yes vs. No). Data

were normalized with respect to the number of stimulations per epoch. The

vertical bars show the standard errors of the means. *, significant difference

(P b 0.007).

Results

Behavioral data

Response accuracy was determined for the detection task only,

since the familiarity judgment depends on personal experience.

During the scanning day, two subjects scored very low response

accuracy (65% and 68%, respectively), due to a very small number

of odors detected (29% and 41%, respectively). The aberration of

both these values was rated with the Grubbs’ test (Dagnelie, 1975),

which indicated that they were indeed outliers (t = 5.414 and t =

5.052, respectively, for a theoretical value of t0.99815 = 3.663). One

of these subjects also did not provide behavioral responses during

the three epochs of the familiarity task. These two subjects were

therefore excluded from further analysis. For the 12 remaining

subjects, the mean numbers and response accuracies of odors

delivered per epoch for the three odor sets (Da, Db, Dc) of the

detection task are given in Table 2. A one-way ANOVA with

repeated measurements performed on response accuracy showed a

significant main effect of set factor [F(2,22) = 5.985, P = 0.0084],

98

indicating that odors of the Da and Dc sets were more easily

detected than those of the Db set.

For the F condition, the number of odorants judged as being

familiar or unfamiliar by the subjects was determined for the three

odor sets (Fa, Fb, and Fc). For each subject, data were normalized

with respect to the number of stimulations per epoch. The mean

number of stimulations and the mean ratios of familiar odorants

delivered per epoch are given in Table 2. A one-way ANOVAwith

repeated measurements performed on the ratios of familiar odor-

ants showed no significant effect of set factor [F(2,22) = 0.455, P =

0.640], indicating that the same proportion of familiar odorants was

found in the three odor sets.

Subjects’ reaction times for odor detection and familiarity

judgments were also calculated (Table 2). The number of

stimulations delivered per epoch depended on the subject’s

breathing rhythm. As this factor could affect reaction times by

creating a shorter interstimulus response period in those who

breathe more rapidly, the data were normalized with respect to the

number of stimulations, and analyzed as a function of task, odor

sets, and response (Yes or No) factors. A three-way ANOVA with

repeated measurements showed a significant effect of the judgment

task [F(1,11) = 33.380, P b 0.0001], of response [F(1,11) =

65.965, P b 0.0001], but no significant effect of odor set factor

[F(2,22) = 1.020, P = 0.3772]. Significant task � response

[F(2,22) = 10.153, P = 0.0087] (see Fig. 2) and task � set �

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Table 3

Areas activated in the F–D contrast

Brain region L/R k Z value MNI coordinates

x y z

Amygdala L 54 4.29 �24 �6 �12

Cingulate gyrus L 67 4.21 �8 16 40

Mid-fusiform gyrus R 432 3.93 40 �40 �16

Amygdala R 3.85 20 �16 �10

Hippocampal

region (CA3)

R 3.84 22 �20 �8

Temporal

piriform cortex

R 3.75 30 2 �16

Parahippocampal

gyrus

R 3.61 42 �16 �10

Posterior Insula R 3.29 46 �10 �6

Superior occipital

gyrus

L 62 3.79 �16 �100 14

Inferior frontal gyrus,

pars orbitalis

L 13 3.27 �50 28 2

Note. F, familiarity; D, detection; L, left; R, right; k, size of the cluster in

number of connected voxels; x, y, z, MNI coordinates in mm of the

maximum in the Montreal Neurological Institute Brain template; CA,

Cornu Ammonis.

J. Plailly et al. / NeuroImage 24 (2005) 1032–10411036

response [F(2,22) = 3.833, P = 0.0373] interactions were noted.

Mean comparisons indicated that reaction times in the D condition

were longer when no odor was detected (P b 0.0001), longer in the

F condition when odors were perceived as more unfamiliar (P b

0.0070), and longer with unfamiliar odors during familiarity

judgments (as compared to detection judgments; P b 0.0001).

Breathing data

Breathing changes could be expected as a function of epoch, as

during F-epochs odors were delivered at each inspiration, and

during D epochs odors were delivered on 50% of inspirations.

Inspiratory airflow measures were therefore analyzed as a function

of task (Detection and Familiarity), three epochs (a, b, and c), and

subject responses (Yes and No) (Fig. 3). A three-way ANOVAwith

repeated measurements showed no significant effect of task

[F(1,22) = 2.169, P = 0.169], epochs [F(2,22) = 0.415, P =

0.665], and response [F(1,22) = 1.409, P = 0.260] factors.

fMRI data

F–D contrast

Familiarity-specific responses (F–D) were present in the right

temporal piriform area (30, 2, �16; Z = 3.75), spanning the

cortico-amygdaloid transition area, the preamygdalar claustrum,

the periamygdalar area, and the lateral amygdaloid nucleus (22,

�16, �10; Z = 3.85; Table 3 and Fig. 4A). PC activation was not

detected in the left hemisphere (using the same statistical

significance threshold), but strong activation was present in the

amygdala (�24, �6, �12; Z = 4.29) spanning approximate areas

for the basomedial, basolateral, central, lateral and medial

amygdaloid nuclei, and the anterior amygdaloid area. Familiarity-

related activation in the right PC extended into the right mid-

fusiform gyrus (40, �40, �16; Z = 3.93) and hippocampal region

(Fig. 4B; 22, �22, �8; Z = 3.84). The familiarity judgment task

also activated the left cingulate gyrus (�8, 16, 40; Z = 4.21) and

the left inferior frontal gyrus in its opercular part (�50, 28, 2; Z =

3.27), as depicted in Fig. 4C. Finally, we noted significant

activation in the left occipital gyrus (�16, �100, 14; Z = 3.79)

and the right middle frontal gyrus (44, 20, �18; Z = 3.40).

Fig. 3. Inspiratory airflow as a function of the olfactory task (Detection vs.

Familiarity) and of the type of response (Yes vs. No). Data were normalized

with respect to the number of stimulations per epoch. The vertical bars

show the standard errors of the means.

99

Comparison of activations between the right and left PC

Mean activity levels were measured in the right and left PC

using ROIs. A one-way ANOVA with repeated measurements on

these data showed significantly higher right than left PC activation

[F(1,11) = 4.846, P = 0.0499].

Discussion

The aim of this fMRI study was to determine the cerebral

regions that mediate judgments of odor familiarity. With such an

approach, we identified odor-evoked neural responses in several

olfactory and limbic regions, including piriform cortex, amygdala,

hippocampus, the pars orbitalis of the inferior frontal gyrus, and

the mid-fusiform gyrus.

Activation of the mesial temporal region

Olfactory-related activation of mesial temporal regions remains

inconsistent across studies. Whereas some authors have reported

activation in PC in PET studies (e.g., Kareken et al., 2001, 2003,

2004; Savic et al., 2000; Small et al., 1997; Zatorre et al., 1992),

we did not find any mesial temporal activation in our previous

studies (Royet et al., 1999, 2001). Piriform cortex activation has

also been inconsistently detected across fMRI studies (e.g., Sobel

et al., 1998; Yousem et al., 1999). A well-known problem with the

EPI pulse sequence usually applied in fMRI is magnetic

susceptibility artefact, which induces signal loss in these regions

(Zald and Pardo, 2000). The PRESTO sequence used in the current

study appears to reduce these artifacts and to provide stronger

signal in the regions affected by susceptibility differences.

Habituation may also contribute to signal loss in these ventral

regions, particularly with blocked designs and the use of only one

or two odorants (Poellinger et al., 2001; Sobel et al., 2000). Since

we used a different odorant on each breathing cycle (from 12 to 20

different odorants per 60-s epoch, depending on the duration of

breathing cycle of the subject), we minimized both self-adaptation

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Fig. 4. Localization of task-specific activations in the F–D contrasts. (A) Piriform cortex; (B) hippocampus; (C) inferior frontal gyrus. Neural responses are

overlaid on coronal and axial sections from a subject’s normalized T1-weighted brain image. Clusters were thresholded at t = 3.10.

J. Plailly et al. / NeuroImage 24 (2005) 1032–1041 1037

(Engen, 1982) and sensory habituation (Demonet et al., 1993). As

in our previous fMRI study (Royet et al., 2003), the present data

suggest that the pulse sequence and stimulation paradigm provided

sufficient sensitivity to detect activation in primary olfactory areas.

A PC activation that is stronger in the F than D condition could

be explained by different factors. A possible confound lies first of

all in the higher proportion of odorous stimulations delivered in

the F than D condition. We decided for this particular design

because we considered it was important to keep the subjects’

attention focused during the detection task (in which they had to

respond dyesT and dnoT equivalently). At the same time, if we had

presented blanks during the familiarity task, this might have

confused the subjects and this would have introduced a third type

of event (no odor in addition to the familiar and the unfamiliar

100

odors). Further experiments are therefore needed to rule out this

specific confound. It would be of interest, in particular, to design

an event-related fMRI study in which familiar and unfamiliar

odors would be distinguished as discrete events in both conditions.

Unfamiliar odors of the F and D conditions could then be

contrasted and any PC activation could then be specifically

associated with the F task. It should nevertheless be noted that the

piriform cortex may become activated in retrieving odor associ-

ations alone, without any direct chemosensory stimulation

(Gottfried et al., 2004). This strongly suggests that the task

performed by subjects may be a decisive factor in activating the

piriform cortex.

A second source of potential confound may lie in the

different respiratory patterns across conditions, as it has

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J. Plailly et al. / NeuroImage 24 (2005) 1032–10411038

previously been shown that sniffing alone can induce piriform

activation (Sobel et al., 1998; but also see Kareken et al., 2004

for contradictory results), and that odor imagery alone can lead

to breathing differences (Bensafi et al., 2003). In the present

study, however, inspiratory airflow was not higher in the F

condition than in the D condition. Finally, a third source of

potential confound is identified in the differences in odor

familiarity, since odors selected a priori as being familiar were

only delivered in the F condition. Nevertheless, the same number

of a priori unfamiliar odors were presented in both conditions.

We then noted that reaction times were much longer when the

unfamiliar odors were presented in the F condition, and even

longer than reaction times of familiar odors presented in this

same condition. This suggests that subjects performed different

judgments across conditions, and that activation differences in

PC could be better explained by the type of task than by

perceptual differences in odor familiarity. This could also explain

why Savic and Berglund (2004) did not find differential

activation in PC when subjects passively smelled familiar or

unfamiliar odorants. It nevertheless stands to reason, however,

that the task (when not explicitly required by the experiment)

should be facilitated by the intrinsic properties of the odors

themselves: That is, highly familiar odors would more easily

facilitate familiarity judgments, and highly pleasant or unpleasant

odors would more easily encourage emotional judgments.

Involvement of piriform cortex in recognition memory

Recognition memory is known to involve two different

processes: familiarity and recollection (Bogacz et al., 2001;

Mandler, 1980; Rajaram, 1998). According to the ddual processtheoryT, processes underlying familiarity are perceptual in nature,

and those subserving recollection include the retrieval of con-

textual information. Lehrner et al. (1999) demonstrated that these

two forms of recognition memory processes also exist in olfaction.

In other words, familiarity judgments are made on the basis of

feelings devoid of specific information about the encoding

episode, and thus relate to implicit memory. By contrast,

recollection is more directly tied to specific events, and thus

relates to explicit memory. To illustrate these concepts, Bogacz

et al. (2001) note that, b. . .it is not uncommon to be able to

recognize that a person is familiar to us even though we cannot

immediately recollect anything more about the person or our

previous encounters with themQ (Bogacz et al., 2001). Since

familiarity judgments are inherent in recognition memory, our

results relate to previous findings in humans indicating that PC is

involved in long-term odor recognition memory (Dade et al.,

2002). More recently, Gottfried et al. (2004) further reported that

PC responds to non-olfactory stimuli with which odors were

previously associated.

Further experiments are needed to compare activation

produced by different memory processes. Familiarity and

recollection could involve slightly different neural networks,

but the present experimental design cannot distinguish between

them. Our findings nevertheless cohere with a large body of

research using animal models, and lend support to the theory that

the piriform cortex is involved in learning- and memory-related

processes (e.g., Datiche et al., 2001; Schoenbaum and Eichen-

baum, 1995). For instance, synaptic potentiation has been shown

to occur in rat PC in vitro (e.g., Jung et al., 1990; Saar et al.,

2002) and in vivo at the conclusion of learning (Litaudon et al.,

101

1997; Roman et al., 1993). These findings are thus consistent

with models demonstrating that the primary olfactory cortex is a

parallel-distributed architecture characteristic of associative mem-

ory systems (e.g., Bower, 1991; Haberly, 2001; Haberly and

Bower, 1989).

Lateralization of familiarity judgment process

The current study shows that activation of the right PC was

stronger than that of the left PC. This is in line with the results of a

large body of other research. In a monorhinal odor recognition

task, Savic et al. (2000) noted significant right, but not left,

piriform activity. Although Dade et al. (2002) did not explicitly

report hemispheric asymmetry for long-term olfactory memory,

their results distinctly indicated strong activation in right OFC, and

more activation in right than left PC. Interestingly, Gottfried et al.’s

study of cross-modal visual–olfactory associations also showed

unilateral right PC activation, and in this case without direct

olfactory stimulation. Using behavioral measures, Broman et al.

(2001) finally observed that odors presented to the right nostril

were rated as more familiar than odors presented to the left nostril.

They also reported that episodic recognition via the right nostril

tended to nominally have more dknowT responses and fewer

drememberT responses than did odors recognized via the left nostril,which is in keeping with the right-nostril advantage for familiarity.

Taken together, these findings are consistent with the notion that

left temporal lobe structures mediate processing of distinctiveness

(i.e., what clearly distinguishes one percept from another), whereas

right temporal lobe structures subserve processes underlying

perceptual fluency (i.e., what involves perceptual analysis of the

surface features of an item; Blaxton and Theodore, 1997; Rajaram,

1998). Such a perceptual analysis of surface features is especially

observed for odors which are intrinsically difficult to name

(Lawless and Engen, 1977).

Findings in brain-damaged patients and results from neuro-

imaging studies converge with these data. For instance, epilepsy

patients with left temporal lobe lesions who were asked to

recognize previously seen abstract designs provided more dknowTthan drememberT responses, whereas right temporal lesioned

patients showed the opposite pattern (Blaxton and Theodore,

1997). Along the same line, Henson et al. (1999) explored word

recognition with fMRI and showed a dissociation whereby a

dknowT judgment induced right frontal activation, and a

drememberT judgment induced left frontal activation.

In conclusion, the present data, which are consistent with our

previous work in PET, indicate a preferential involvement of the

right hemisphere in familiarity judgments (Royet et al., 1999,

2001). An intriguing result in the present study is the lack of

activation in right OFC. When specifically examining activation

resulting from familiarity versus rest, and from detection versus

rest, we nevertheless saw activation in the right OFC for both

contrasts (44, 32, �16; Z = 3.62 and 46, 30, �12; Z = 2.79,

respectively). This could explain the lack of activation when we

compared images in the familiarity versus detection contrast.

Participation of the hippocampal region, inferior frontal and

mid-fusiform gyri in modality-independent mnemonic and semantic

processing

Since only a few authors have previously reported hippocampal

activations in olfaction studies (e.g., Kareken et al., 2003; Suzuki

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J. Plailly et al. / NeuroImage 24 (2005) 1032–1041 1039

et al., 2001), the right hippocampal activation during the familiarity

judgment task was not anticipated in the present study. Inconsistent

activation of the hippocampal formation is not specific to olfaction,

and has been characteristic of other studies of memory (Andreasen

et al., 1995; Shallice et al., 1994; Tulving et al., 1996). Our data are

nevertheless consistent with a recent finding showing hippocampal

activation during the retrieval of olfactory episodic memories

(Gottfried et al., 2004).

Lesion studies recently examined whether the brain structures

that comprise the medial temporal lobe memory system (i.e., the

hippocampal and parahippocampal regions) differ in how they

support recollective and familiarity components (Manns et al.,

2003; Yonelinas et al., 2002). Our data do not permit distinguish-

ing these aspects of memory, as the subjects may well have had

consciously evoked memories from the odorants. They are,

however, consistent with the idea that both regions probably

contribute to olfactory recognition memory.

Activation of the left inferior frontal gyrus, in the pars

orbitalis, during familiarity judgments further supports the

hypothesis that this region is involved in the selection and

integration of semantic information in a modality-independent

manner (Homae et al., 2002; Kareken et al., 2003). In a recent

study, Savic and Berglund (2004) found that left frontal and right

parahippocampal region activation positively correlated with

familiarity ratings, showing the engagement of semantic circuits

during passive smelling of familiar odorants. Along the same line,

the mid-fusiform gyrus activation in the current study might lead

to similar interpretations, since it has further been associated with

visual, tactile and auditory recognition and categorization of

objects (Adams and Janata, 2002; Joseph and Gathers, 2003;

Stoeckel et al., 2003). Its involvement in olfactory object

recognition therefore reinforces the idea of the polymodal nature

of this area (Adams and Janata, 2002) and its role in semantic

processing (Price, 2000; Wagner et al., 1998).

Conclusion

Complementing previous PET studies that demonstrate right

OFC involvement in odor familiarity judgments, the present fMRI

study shows that right PC is also activated during this task, an

activation that may be related to olfactory recognition memory. In

previous fMRI and PET studies, we demonstrated that a neural

network in the left hemisphere, involving the OFC and primary

olfactory areas, mediated olfactory hedonic perception (Royet et al.,

2000, 2003). It thus appears that odor processing activates a large

neural network involving both hemispheres. Nevertheless, this

network possesses hemispheric predominance depending on the

type of olfactory task performed (see Royet and Plailly, 2004, for

review). The present data provide further evidence that the right

hippocampal region, left inferior frontal gyrus and mid-fusiform

gyrus take part in recognition memory, likely cross-modally to

assist in gathering relevant associations to enable identification of

olfactory percepts.

Acknowledgments

We thank the technical team (M. Vigouroux, B. Bertrand, and

V. Farget) for designing and building the stimulation and recording

materials and J.P. Lomberget and M.B. Sanglerat for medical

102

examinations of subjects participating in the study. We are grateful

to the companies Givaudan, International Flavors and Fragrances,

Lenoir, Davenne, and Perlarom for supplying the odorants used in

this study. This work was supported by research grants from the

dRegion Rhone-AlpesT and the dGIS Sciences de la Cognition,T thedCentre National de la Recherche Scientifique,T and the dUniversiteClaude-Bernard de Lyon.T

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Page 133: La mémoire olfactive humaine : Neuroanatomie fonctionnelle de la

ARTICLE IN PRESS

www.elsevier.com/locate/ynimg

YNIMG-03326; No. of pages: 12; 4C: 7

DTD 5

NeuroImage xx (2005) xxx – xxx

Left temporo-limbic and orbital dysfunction in schizophrenia

during odor familiarity and hedonicity judgments

Jane Plailly,a,* Thierry d’Amato,b Mohamed Saoud,b and Jean-P. Royet a,c

aLaboratoire Neurosciences & Systemes Sensoriels, Universite Claude Bernard Lyon1, UMR CNRS 5020, IFR 19,

Institut Federatif des Neurosciences de Lyon, 50 avenue Tony Garnier, 69366 Lyon cedex 07, FrancebFVulnerabilite a la schizophrenie: de la prediction a la prevention_, Universite Claude Bernard Lyon1 (EA3092),

Centre hospitalier FLe Vinatier_, 69677 Bron, FrancecCERMEP, 69003 Lyon, France

Received 29 April 2005; revised 27 June 2005; accepted 28 June 2005

Impairments of olfactory processing in patients with schizophrenia (SZ)

have been reported in various olfactory tasks such as detection,

discrimination, recognition memory, identification, and naming. The

purpose of our study was to determine whether impairments in odor

familiarity and hedonicity judgments observed in SZ patients during a

previous behavioral study are associated with modifications of the

activation patterns in olfactory areas. Twelve SZ patients, and 12 healthy

comparison (HC) subjects, were tested using the H215O-PET technique

and 48 different odorants delivered during 8 scans. In addition to an

odorless baseline condition, they had either to detect odor, or to judge

odor familiarity or hedonicity, giving their responses by pressing a

button. Regional cerebral blood flows during olfactory conditions were

compared with those for baseline condition. Between-group analyses

were then performed, and completed by regions of interest analyses.

Both groups had equivalent ability for the detection of suprathreshold

odorants, but patients found odors less familiar, and pleasant odors less

pleasant than HC subjects. These behavioral results were related to

functional abnormalities in temporo-limbic and orbital olfactory regions

lateralized in the left hemisphere: the posterior part of the piriform

cortex and orbital regions for familiarity judgments, the insular gyrus

for hedonicity judgments, and the left inferior frontal gyrus and anterior

piriform cortex/putamen region for the three olfactory tasks. They

mainly resulted from a lack of activation during task conditions in the SZ

patients. These data could explain olfactory disturbances and other

clinical features of schizophrenia such as anhedonia.

D 2005 Elsevier Inc. All rights reserved.

Keywords: Schizophrenia; activation deficit; odor familiarity judgment;

odor hedonicity judgment; PET

1053-8119/$ - see front matter D 2005 Elsevier Inc. All rights reserved.

doi:10.1016/j.neuroimage.2005.06.056

* Corresponding author. Fax: +33 4 37 28 76 01.

E-mail address: [email protected] (J. Plailly).

Available online on ScienceDirect (www.sciencedirect.com).

133

Introduction

Schizophrenia is a chronic, severe, and disabling brain disease

that presents impairments of cognitive and emotional functions,

such as perception, inferential thinking, motivation, thought, and

speech (Schultz and Andreasen, 1999). The processing of olfactory

information is a cognitive function which is disturbed in patients

with schizophrenia (SZ), and behavioral evidence of this dysfunc-

tion is found with odor discrimination, recognition memory,

identification, and naming tasks (Kohler et al., 2001; Kopala et al.,

1993, 1994; Moberg et al., 1999; Saoud et al., 1998; Stedman and

Clair, 1998; Wu et al., 1993). Although abnormalities were found at

the level of the peripheral olfactory pathways (Arnold et al., 2001;

Turetsky et al., 2000), several studies reported no decrease in the

olfactory sensitivity of patients (Geddes et al., 1991; Good et al.,

1998; Kohler et al., 2001; Kopala et al., 1989, 1993), suggesting that

deficits in suprathreshold olfactory tasks partly arise from dysfunc-

tion of the central olfactory areas.

Over the last 10 years, our knowledge of olfactory neural

networks in healthy subjects has been increasing through the use of

cerebral imaging. It has been shown that the temporo-limbic

(piriform cortex, amygdala, insular gyrus) and inferior frontal

(orbitofrontal and inferior frontal gyri) regions are strongly

involved in odor discrimination, recognition memory, and identi-

fication tasks (for review, Kobal and Kettenmann, 2000; Royet and

Plailly, 2004; Savic, 2001, 2002, 2005; Zald and Pardo, 2000;

Zatorre and Jones-Gotman, 2000). It has also been shown that the

anatomy and metabolism of these neural networks are disturbed in

SZ patients, particularly with a reduction in grey matter volume

(Turetsky et al., 2003b) and a lower rate of cerebral glucose

metabolism (Bertollo et al., 1996; Clark et al., 1991).

Despite the behavioral, structural, and metabolic clues asso-

ciated with olfactory deficits in schizophrenia, only three previous

studies have focused on the functional bases of such olfactory

impairments. Turetsky et al. (2003a) showed abnormalities in the

amplitude and latency of the evoked potentials obtained from

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ARTICLE IN PRESS

Table 1

Demographic and clinical data for HC subjects and SZ patients

HC subjects SZ Patients

Demographic variables

Age 32.83 T 5.78 29.67 T 7.06

Education (years) 10.63 T 1.76 10.50 T 1.86

Smoking history (cigarettes/day) 4.71 T 6.95 11.67 T 10.52

Personal psychiatric history

Length of psychiatric history (months) – 66.33 T 46.13

Medication

Antipsychotic (mg/day CPZ Eq.) – 429.17 T 216.83

PANSS scores

Negative symptoms score – 22.83 T 4.91

Positive symptoms score – 16.00 T 4.33

Mean T standard deviations.

J. Plailly et al. / NeuroImage xx (2005) xxx–xxx2

passive odor presentation, and explained them by impaired odor

sensitivity and identification. Evoked potentials were nevertheless

obtained from the scalp and these data only indirectly allowed

them to infer which neural networks were presenting a disturbance.

Using single photon emission computed tomography, Malaspina et

al. (1998) demonstrated that schizophrenia patients did not increase

activation of their hippocampus and visual association areas for the

odor identification test compared to a picture matching task, as did

the control group, and showed hypometabolism in right-sided

cortical areas for odor identification. Thus, the only regions

disclosed were those where activation differed between both tasks

but did not evidence any specific dysfunction of the olfactory

networks. Finally, Crespo-Facorro et al. (2001) studied the loss of

the capacity to experience pleasure in SZ patients and investigated

the specific neural systems underlying olfactory emotional

disturbances. Participants experienced a pleasant odor and an

unpleasant odor, and the authors then found that patients failed to

activate several limbic and paralimbic regions during the experi-

ence of an unpleasant odor.

An olfactory experience involves not only an emotional

response but also perceptual processes associated with recognition

memory and related to identification. In our work, we currently use

several olfactory tasks such as the detection task and intensity,

hedonicity, familiarity, and edibility judgments, and have shown

through cerebral imaging in healthy subjects that several areas of

the limbic and paralimbic regions participate in these processes

(Plailly et al., 2005; Royet et al., 1999, 2000, 2001, 2003). The

purpose of examining functional abnormalities in these various

structures as a function of the different olfactory tasks performed

by patients therefore appears crucial if we are to better understand

the psychopathology of schizophrenia. Recent behavioral studies

have proved that, in addition to the hedonicity judgment, that of

familiarity but not intensity is impaired in SZ patients (Hudry et al.,

2002; Moberg et al., 2003).

The current study was undertaken to investigate whether

activation patterns specifically associated with the odor supra-

threshold detection task and the odor familiarity and hedonicity

judgment tasks in healthy subjects are modified in SZ patients.

Twelve SZ patients and 12 healthy comparison (HC) subjects were

tested, using positron emission tomography (PET) to compare

regional cerebral blood flow (rCBF) patterns between both groups.

Four different conditions were tested twice: an odorless baseline

(B) condition, a detection (D) task, and familiarity (F) and

hedonicity (H) judgment tasks.

Material and methods

Subjects

Twelve SZ patients and 12 HC subjects, all male and right-

handed, participated in this study (Table 1). HC subjects were

recruited by local newspaper advertisement. Patients were recruited

from the Vinatier Hospital (Lyon, France) and met the DSM-IV

criteria for schizophrenia (American Psychiatric Association,

1994). Psychiatric diagnoses were established, by consensus of

the two psychiatrists involved in the current study, in accordance

with the Schedule for Affective Disorders and Schizophrenia

(SADS) (Fyer et al., 1985) and included an in depth review of the

patients’ medical records. The Positive And Negative Syndrome

Scale (PANSS; Kay et al., 1987) was then used to assess the

134

patients’ psychopathology (Table 1). Patients were clinically stable

with no change in medication for at least 1 month before the study.

Through SADS evaluations, selected HC subjects had neither

current DSM-IV Axis I psychiatric diseases nor schizophrenia

spectrum personality disorders, i.e. schizotypal, schizoid and

paranoid personality disorders. Furthermore, none of them had

any family history of psychopathology. Both groups were paired in

age (F(1,22) = 1.445, P = 0.2422), educational level (F(1,22) = 0.029,

P = 0.8672), and smoking history (F(1,22) = 3.657, P = 0.0690).

Subjects were all selected on the basis of their olfactory ability

with a forced-choice suprathreshold detection test (at least 75%

correct) and on the mean duration of their breathing cycle (from

2.5 to 6 s/cycle). The exclusion criteria for all subjects included

possible brain damage, major medical problems, current sub-

stance abuse, lithium medication, known anosmia, rhinal disor-

ders (colds, active allergies, history of nasal–sinus surgery, or

asthma), and anxiety. Participation required medical screening

and written informed consent. The study was approved by the

local Institutional Review Board and conducted according to

French regulations on biomedical experiments on healthy

volunteers and out-patients.

Odorous stimuli

Seventy odorants and 14 odorless stimuli were used during the

scans: 28 odorants for each of the F and H conditions, and 14

odorants and 14 odorless stimuli for the D condition (Table 2). For

the F condition, each of the 2 sets was composed of 7 familiar and

7 unfamiliar odorants to respectively provide the highest or lowest

familiarity scores (rated from 0 to 10 with a rating scale) from data

previously obtained by Royet et al.’s (1999) study (set 1: 5.99 T0.79 and 3.48 T 0.49, respectively; set 2: 5.56 T 1.21 and 3.59 T0.90, respectively). For the H condition, 2 sets were each

composed of 7 pleasant and 7 unpleasant odorants, to provide

the highest or lowest hedonicity scores (set 1: 6.48 T 0.45 and

1.77 T 0.72, respectively; set 2: 6.25 T 0.56 and 2.00 T 0.55,

respectively). For the D condition, 2 sets were composed of 7

neutral odorants and 7 bottles with odorless air. For training, 14

odorants and 14 odorless stimuli were used, split into 2 sets of 7

neutral odorants and 7 bottles with odorless air. In each set, the

presentation order of the stimuli was pseudorandomized but

identical for all subjects. Odorants were diluted to a concentration

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Table 2

Lists of odorants used for the three olfactory conditions (D, F, and H)

during the two scans (Scan1 and Scan2)

Olfactory conditions

D F H

Scan1 Cypress Pine needle Honeysuckle

3-Methyl anisol Isopropylacetate Lemon

NO Liquorice Tetralin

NO Violet Tetrahydrofurane*

Geranium Citronella Passion fruit

NO White spirit Lavender

Basil Diethyl ether Butyric acid

NO Parsley 2-Heptanol

Eucalyptus Vervain Tetrahydrothiophene*

Chamomile Guaıacol Apricot

NO Hexyl cinnamaldehyde Pear

Tarragon Anise Garlic

NO trans-2-Hexenal Gardenia

NO Hexanal Ethyl diglycol

Scan2 Toluene Ethyl benzoyl acetate 1,4-Dichlorobutane

NO 2-Octanol Lilac

Green lily Ethyl acetate Heptanal

NO Banana Isovaleric acid*

Coffee Tar Caramel

Patchouli Blackcurrant Rose

NO h-Caryophyllene Furfuryl mercaptan*

NO Bitter almond Coconut

Carrot Diethyl maleate Wild Strawberry

NO Thyme 2-Bromophenol

Smoked salmon Acetophenone Mint

NO Cedar Ethylmercaptan*

NO Garrigue 2,5-Dimethyl pyrrole

Turpentine Hazelnut Jasmine

D, detection; F, familiarity; H, hedonicity; NO, no odor; italics, odorants

selected as familiar for the F condition, and unpleasant for the H condition

* 1% diluted odorant.

J. Plailly et al. / NeuroImage xx (2005) xxx–xxx 3

of 10% using mineral oil (Sigma Aldrich, France). The

concentration of the products with very high potency was limited

to 1%. Five milliliters of this solution was absorbed into

compressed polypropylene filaments inside 100-ml white poly-

ethylene squeeze bottles with a dropper (Osi, France).

Stimulating material

The stimulating material used allowing synchronization of the

stimulation with breathing has been described in a previous paper

(Vigouroux et al., 2005). Briefly, vector air is pumped with a

compressor, treated with a charcoal filter, and flows into an air-

dilution olfactometer. At the end of expiration, the stimulus is

injected into the olfactometer by squeezing the bottle and delivered

into a commercially available anesthesia mask (Respiron, Europe

Medical, France). Breathing is recorded with a thermal probe close

to the right nostril, and controlled by stereo headphones. Our

subjects were stimulated during every other breathing cycle. For a

mean respiratory cycle of about 3–4 s, about 13 (13.3 T 1.8)

stimulations were performed per scan.

Experimental procedure

During scanning, each subject underwent a total of 8 PET scans,

with two scans (Scan1 and Scan2) for each of the following 4

135

conditions: B, D, F, and H. To control the cognitive processing

performed by the subjects, tasks were conducted in an invariant

order. The odorless B condition was the first one to avoid the

influence of the olfactory conditions. The D condition preceded the

F and H conditions to prevent subjects from performing high-level

processing. The H condition, that included highly aversive odors,

was performed last to avoid inducing a strong emotional reaction in

SZ patients who may then have refused to continue the experiment.

A scan was performed approximately every 10 min. To avoid

surprising the subjects and to optimize data acquisition, the

stimulations started 30 s before the beginning of the scan.

General instructions were provided at the beginning of the

experiment, and specific task instructions were given before each

scan to limit contamination between the different cognitive tasks.

During olfactory conditions, the subjects were asked to rate whether

they smelled an odor or not (D condition) or whether the odor was

familiar or not (F condition), or unpleasant or not (H condition).

They had to answer by pressing a one-key press button with the

index finger of their right hand only when the response was Fyes_,but not to press it at all if the response was Fno_. The use of the onekey instead of the usual two-key press button box was in response to

experimental observation during the preliminary study; patients

mixed up the two buttons and had much better abilities using only a

one-button response-box. During the B condition, the subjects were

requested to press the button at random. The Fyes_ judgments and the

reaction times were recorded with a Macintosh PowerBook G3

computer (Apple Computers, Cupertino, CA). The experimental

design was programmed using FPsyScope_ software (Cohen et al.,

1993). Scans were performed while the subjects kept their eyes

closed and the room lighting was dimmed. Prior to scanning,

subjects performed a training session in which they were trained to

breath regularly without sniffing, to detect (odor vs. no odor)

stimulations during inspiration and to give a manual response as

quickly as possible with the one-key press button before the

following breath.

PET imaging

Subjects were imaged with a whole-body tomograph (Siemens

EXACT HR+) in 3-D mode, with a transaxial resolution of 4.5 mm

(FWHM). Sixty-three slices of 2.43 mm with an axial field of view

of 15.2 mm were acquired during each scan. Subjects were

positioned using a thermoplastic facemask (Tru-Scan Imaging Inc.,

Annapolis, MD, USA) that reduced head movement and allowed

reproducible positioning. The effects of radiation self-attenuation

were corrected by an initial 10-min transmission scan of each

subject using an external positron-emitting isotope (68Ge). An i.v.

bolus injection of 333 MBq H215O was given for each run in the

brachial vein of the left forearm through an indwelling catheter.

The scan to record rCBF began when the radioactive counts

exceeded the background activity by 200% and lasted 60 s. The

images were attenuation-corrected and reconstructed with filtered

back projection using a Hanning filter.

Image analysis

Statistical Parametric Mapping (SPM) 99 (Wellcome Depart-

ment of Cognitive Neurology, London, UK) was used for image

preprocessing and analysis. The steps included interscan realign-

ment, spatial normalization (default 7 � 8 � 7 basis function, 12

nonlinear iterations) to stereotactic space defined by the Montreal

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ARTICLE IN PRESSJ. Plailly et al. / NeuroImage xx (2005) xxx–xxx4

Neurological Institute’s (MNI) reference brain, and smoothing of

the images using a 12-mm isotropic 3-D Gaussian kernel. The

localization of activation clusters was given with reference to the

MNI MRI template and the atlas produced by Mai et al. (1997).

Random effects analyses were performed on the whole brain

using the Fsingle-subject: conditions and covariates_ PET model to

average task conditions into a single contrast image. Three contrasts

were performed by comparing brain responses obtained in olfactory

conditions to those obtained in the B condition: D–B, F–B, H–B.

Activations related to the use of the one-key press button could be

suppressed in the olfactory conditions since participants also used it

in the B condition. In a second step, contrast images were then

analyzed in separate Fbasic model_ two-sample t tests to highlight

between-group differences (SZ vs. HC), using an uncorrected height

threshold (P < 0.001), a cluster of more than 15 adjacent voxels, and

a Z � 3.40 at voxel level. Since the aim of the study was to

investigate differences between the two groups, only results from the

between-group analyses were examined. We limited our statistical

inferences to principal olfactory regions (temporo-limbic and

inferior frontal areas), and will report here only those activation

foci that fell within these areas.

Firstly, to evidence the brain areas significantly activated in the

three contrasts (D–B, F–B, and H–B), an analysis of conjunction

was performed. Contrast images were transformed into true-false

maps of significant and nonsignificant voxels (using the threshold

of P < 0.001 uncorrected and an extent threshold of k > 5), and

voxels with Ftrue_ values in the three contrasts were considered as

being part of the overlap.

Secondly, to determine activation levels as a function of the

different conditions (groups � tasks), we extracted, from the

random effects analyses, the activation levels found for each of the

12 HC subjects and the 12 SZ patients and for both conditions of a

given contrast at the level of the peak voxel coordinates. The

presence of significant activation in the regions controlateral to

those observed in the piriform and insular areas of the left

hemisphere was tested by measuring the activation levels in the

right hemisphere at the level of controlateral coordinates of the

maximum peak voxel of these activation clusters.

Lastly, to test the task-specificity of the between-group differ-

ences in the piriform region and the left inferior frontal gyrus, we

performed functional ROI analyses in contrasts comparing the

olfactory conditions with themselves (D, F, and H). Anatomical

ROIs of the amygdalae were finally defined and the mean

activation levels within these ROIs were extracted for each of

the 24 participants and for the different conditions. Analyses of

variance (ANOVA) and mean comparisons were then performed to

compare the activation levels as a function of the groups and tasks.

The MarsBar SPM toolbox (http://marsbar.sourceforge.net/) was

used to define ROIs and to perform all analyses, except for the

anatomical ROIs of the amygdala which were defined using

MARINA software (http://www.bion.de/Marina.htm).

Fig. 1. Percentages in HC subjects and SZ patients of odors judged (A)

familiar among all odors, and (B) unpleasant among odors considered

pleasant (left) and unpleasant (right) by most of the HC subjects. Vertical

bars, standard errors of the mean; *P < 0.05; **P < 0.01.

Results

Behavioral results

For the detection task, the mean scores for the accuracy of the

responses in both repetitions (Scan1 and Scan2) were 0.863 T0.158 and 0.871 T 0.108 in HC subjects, and 0.858 T 0.149 and

0.878 T 0.076 in SZ patients. A two-way ANOVA with repeated

136

measurements did not show any significant difference between

groups (F(1,22) = 0.003, P = 0.954) and repetitions (F(1,22) = 0.291,

P = 0.595), and no significant interaction (F(1,22) = 0.029, P =

0.8663) between these two factors, indicating that both groups

detected suprathreshold odors with the same accuracy.

To analyze the accuracy of behavioral responses, and since

familiarity and hedonicity judgments depend on personal experi-

ence, familiar/unfamiliar, and pleasant/unpleasant odorants were

selected as a function of the HC subjects’ responses rather than

simply using the initial selection chosen by the experimenters. The

percentage of odors judged familiar and unpleasant in both groups

of subjects is illustrated in Fig. 1. For the familiarity judgment task,

a two-way ANOVA indicated a significant effect for group

(F(1,22) = 5.961, P = 0.0231), and familiarity judgment (F(1,22) =

125.34, P < 0.0001) factors, but no significant task � group

interaction (F(1,22) = 1.112, P = 0.3031).

For the hedonicity judgment task, a two-way ANOVA indicated

a significant effect for the hedonicity task factor (F(1,22) = 193.26,

P < 0.0001), but not for the group factor (F(1,22) = 2.734, P =

0.1124). A significant hedonicity judgment � group interaction

was also noted (F(1,22) = 20.106, P = 0.0002), further showing that

the patients judged pleasant odors less pleasant than the HC

subjects (P = 0.0050). No difference between either group was

observed for unpleasant odors (P = 0.4430).

Reaction times were analyzed for detection, familiarity, and

hedonicity judgment tasks as a function of group (HC and SZ) and

repetition (Scan1 and Scan2) factors. A three-way ANOVA

showed a significant effect for group (F(1,22) = 12.624, P =

0.0018), task (F(2,44) = 44.632, P < 0.0001), and repetition

(F(1,22) = 9.017, P = 0.0066) factors, and a significant task �repetition interaction (F(2,44) = 6.402, P = 0.0036). No other

interaction was significant. The group effect was due to longer

reaction times in SZ patients than HC subjects (Fig. 2). Multiple

mean comparisons indicated that reaction times, all the subjects

considered together, were longer for the hedonicity judgment task

than for detection (P < 0.0001) and longer for the familiarity than

the hedonicity judgment task (P < 0.0001).

PET results

Significant rCBF differences between HC subjects and SZ

patients groups (HC minus SZ, and SZ minus HC) for olfactory

minus B contrasts were extracted and are listed in Table 3.

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Fig. 3. rCBF differences found in the D–B contrast between HC subjects

and SZ patients in the piriform cortex and inferior frontal gyrus. The SPMs

are superimposed on coronal sections of a T1-weighted scan (thresholded at

P = 0.0001). Graphs: levels of activation in the B and D conditions in these

two areas in HC subjects and SZ patients inferred from functional ROIs.

Vertical bars, standard errors; ***P < 0.001.

Fig. 2. Mean reaction times in ms to detect odors, and judge them

unpleasant and familiar in HC subjects and SZ patients. Vertical bars,

standard errors; ***P < 0.001.

J. Plailly et al. / NeuroImage xx (2005) xxx–xxx 5

HC minus SZ contrast

For the D–B contrast, significant rCBF variations were

detected in the left anterior part of the frontal piriform cortex

(�24, 10, �14), and the left inferior frontal gyrus in its orbital part

(�46, 40, �8) (Fig. 3). Detailed examination of data for the

piriform cortex showed that the significant group � task interaction

(F(1,22) = 21.266, P < 0.0001) resulted from a higher activation

level in the HC subjects (P < 0.0001) in the D than B condition.

For the inferior frontal gyrus, the significant group � task

interaction (F(1,22) = 17.340, P = 0.0004) resulted from a lower

activation level in the SZ patients (P < 0.0001) in the D than B

condition. No activation levels difference was noted in the B

condition between groups (piriform cortex: P = 0.1999; inferior

frontal gyrus: P = 0.9002).

For the F–B contrast, differences in rCBF were observed in the

left inferior part of the putamen extending ventrally to the posterior

part of the frontal piriform cortex (�20, 2, �6), left superior

temporal gyrus (�48, 8, �16), right gyrus rectus (10, 36, �24), left

medial orbital gyrus (�18, 30, �18), and left orbital part of the

inferior frontal gyrus (�42, 32, �4). For the putamen/piriform

cortex region, the between-group difference [group � task

interaction: F(1,22) = 32.959, P < 0.0001] was due to an rCBF

Table 3

Brain regions with significant rCBF differences when comparing the contrast ima

Contrasts Anatomic regions L/R

HC-SZ

D–B Frontal piriform cortex, anterior part L

Inferior frontal gyrus, orbital part L

F–B Putamen/frontal piriform cortex, posterior part L

Superior temporal gyrus L

Gyrus rectus R

Medial orbital gyrus L

Inferior frontal gyrus, orbital part L

H–B Insular gyrus, anterior and ventral part L

Inferior frontal gyrus, orbital part L

SZ-HC

D–B Insular gyrus R

Note. D, detection; F, familiarity; H, hedonicity; B, baseline; HC, healthy compari

k, cluster of voxels size; Z, Z value; x, y, z, MNI co-ordinates in left – right (x),

137

increase in HC subjects (P < 0.0001) and an rCBF decrease in SZ

patients (P = 0.0080) in the F condition when compared with the B

condition (Fig. 4). The rCBF was also significantly higher in SZ

patients than HC subjects (P = 0.0090) in the B condition.

Significant group � task interactions noted for the four other areas

[superior temporal gyrus: F(1,22) = 21.010, P = 0.0001; gyrus

rectus: F(1,22) = 19.551, P = 0.0002; medial orbital gyrus: F(1,22) =

17.542, P = 0.0004; inferior frontal gyrus: F(1,22) = 15.781, P =

0.0006] resulted from a higher activation level in the HC subjects

(P = 0.0047, P < 0.0001, P < 0.0001, and P < 0.0001,

respectively) in the F than B condition. No activation level

ges of both groups (FHC–SZ_ and FSZ–HC_ contrasts)

k Z MNI

x y z

101 4.13 �24 10 �14

64 3.54 �46 40 �8

95 4.44 �20 2 �6

25 3.80 �48 8 �16

57 3.70 10 36 �24

41 3.55 �18 30 �18

19 3.41 �42 32 �4

218 4.13 �26 20 �6

43 3.58 �46 34 �8

44 4.65 40 2 12

son subjects; SZ, patients with schizophrenia; L/R, left or right hemisphere;

posterior–anterior ( y), and inferior– superior (z) planes.

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Fig. 4. rCBF differences found in the F–B contrast between HC subjects and SZ patients in the piriform cortex, inferior frontal gyrus, medial orbital gyrus, and

gyrus rectus. The SPMs are superimposed on coronal and horizontal sections of a T1-weighted scan (thresholded at P = 0.0001). Graphs: levels of activation in

the B and F conditions in these four areas in HC subjects and SZ patients inferred from functional ROIs. White arrow, activation for which a ROI was

performed; vertical bars, standard errors; **P < 0.01; ***P < 0.001.

J. Plailly et al. / NeuroImage xx (2005) xxx–xxx6

difference in the B condition was found between groups (P =

0.2458; P = 0.8271; P = 0.9580; and P = 0.2748, respectively).

For the H–B contrast, significant variations in rCBF were

detected in the left anterior ventral insular gyrus (�26, 20, �6)

extending laterally and posteriorly to the anterior part of the frontal

piriform cortex, and in the left inferior frontal gyrus, in its orbital

part (�46, 34, �8) (Fig. 5). Significant group � task interactions

found for the insular gyrus (F(1,22) = 26.490, P < 0.0001) and the

inferior frontal gyrus (F(1,22) = 17.833, P = 0.0004) were due to a

higher activation level in the H than B condition in the HC subjects

(P < 0.0001 and P = 0.0010, respectively). The second interaction

was also explained by a lower activation level in the H than B

condition in the SZ patients (P = 0.0394). No activation difference

was found in the B condition between groups for both areas (P =

0.5113, and P = 0.4346, respectively).

The conjunction analysis showed an overlap between the three

olfactory conditions when compared to the B condition in a region

Fig. 5. rCBF differences found in the H–B contrast between HC subjects and SZ

The SPMs are superimposed on a horizontal section of a T1-weighted scan (thresh

in these two areas in HC subjects and SZ patients inferred from functional ROIs

138

between the left anterior part of the temporal piriform cortex and

the lower part of the putamen (�25, 11, �12), and in the left

inferior frontal gyrus (�45, 32, �5) (Fig. 6).

Comparing olfactory conditions among themselves, ROI

analyses on the functional clusters overlapping at the level of the

left piriform/putamen region (clusters centered on �20, 2, �6

coordinates in the F–B contrast, and on �26, 20, �6 coordinates

in the H–B contrast) showed significant activation differences in

the piriform/putamen region in the F–D and F–H contrasts (t =

2.56, uncorrected P = 0.0089; and t = 2.14, uncorrected P =

0.0216, respectively), and an activation difference which tended to

be significant in the insular/piriform region in the H–D (t = 1.44,

uncorrected P = 0.0816), but not in the H–F (t = 1.15, uncorrected

P = 0.1315) contrast. ROI analyses on the functional clusters

overlapping at the level of the left inferior frontal gyrus (clusters

centered on �42, 32, �4 coordinates in the F–B contrast, and on

�46, 34, �8 coordinates in the H–B contrast) showed significant

patients in the anterior insular gyrus (AIG) and inferior frontal gyrus (IFG).

olded at P = 0.0001). Graphs: levels of activation in the B and H conditions

. Vertical bars, standard errors; *P < 0.05; ***P < 0.001.

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Fig. 6. Overlap of the rCBF differences found in the D–B (blue color), F–B (green color), and H–B (red color) contrasts between HC subjects and SZ patients

in the left piriform cortex/putamen region (top) and left inferior frontal gyrus (bottom). The overlap between D–B and F–B contrasts is represented in yellow;

the overlap between D–B and H–B contrasts is represented in pink; the overlap between F–B and H–B are represented in orange; and the overlap between

the three contrasts is represented in white. The contrast images are superimposed on coronal (left) and sagittal (right) sections of a T1-weighted scan

(thresholded at P = 0.001).

Fig. 7. Interaction between groups (HC vs. SZ) and hemispheres (right vs.

left) of rCBF differences found in the piriform cortex in the D–B and F–B

contrasts (peak coordinates: 24, 10, �14 and 20, 2, �6, respectively), and

in the anterior ventral insula in the H–B contrast (26, 20,�6). Vertical bars,

standard errors; *P < 0.05; ***P < 0.001.

J. Plailly et al. / NeuroImage xx (2005) xxx–xxx 7

activation differences for the first cluster, in the F–D and F–H

contrasts (t = 3.91, uncorrected P = 0.0003; and t = 2.91,

uncorrected P = 0.004, respectively), and for the second cluster, in

the H–D and H–F contrasts (t = 2.73, uncorrected P = 0.006; and

t = 1.98, uncorrected P = 0.0300, respectively).

SZ minus HC contrasts

Only comparisons between D and B conditions showed a

significant rCBF difference (Table 3). This was detected in the right

medial part of the insular gyrus (40, 2, 12) and resulted from a higher

activation level in the D than B condition in the SZ patients (P <

0.0001), but not in the HC subjects (P = 0.0793). No difference in

between-group activationwas found in the B condition (P = 0.2003).

Activations in other olfactory areas

To test lateralization of cerebral dysfunction in SZ patients in

the temporo-limbic olfactory areas, we performed analyses in areas

controlateral to those found to be activated in our study.

Comparing HC subjects minus SZ patients, we thus measured

activation in the piriform cortex in the D–B contrast (24, 10, �14),

the putamen/piriform cortex region in the F–B contrast (20, 2,

�6), and the anterior insula in the H–B contrast (26, 20, �6). A

four-way ANOVA with repeated measurements on hemisphere,

region, and task factors showed a significant effect of group

(F(1,22) = 23.894, P < 0.0001), but not hemisphere (F(1,22) =

0.037, P < 0.8501) or region (F(2,44) = 0.050, P = 0.9516), and

task (F(2,44) = 0.531, P = 0.5918) factors. Only the group �hemisphere interaction (Fig. 7) was found to be significant

(F(1,22) = 11.477, P = 0.0026) and was explained by higher

activation in HC subjects than SZ patients in the left (P <

0.0001), but not right (P = 0.4744) hemisphere, and higher

139

activation in the left than right hemisphere in HC subjects (P =

0.0190).

Since differences of activation levels between the olfactory and B

conditions could be similar for the HC subjects and SZ patients,

between-group comparisons could consequently equal zero. To test

this, and since the amygdala has been shown to be involved in

emotional intensity processing (Zald and Pardo, 1997; Royet et al.,

2003), we examined the H–B contrast in the two groups combined

(HC + SZ) and observed bilateral activation clusters centered in the

temporal claustrum, just beside the amygdala, but spreading over its

lateral part (�28, 2, �18; k = 317; Z = 4.93; and 24, 4, �24; k =

64; Z = 3.59). These results were reinforced by ROI analyses of

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Fig. 8. Levels of activation evoked in the HC subject and SZ patient groups

and in the B and H conditions in the left and right amygdalae inferred from

ROIs. Vertical bars, standard errors; ***P < 0.001.

J. Plailly et al. / NeuroImage xx (2005) xxx–xxx8

the amygdalae performed with the H–B contrast in the two

groups. A three-way ANOVA applied to these data showed

significant differences in the H–B contrast as a function of

groups (F(1,22) = 8.917, P = 0.0068) and tasks (F(1,22) = 22.664,

P < 0.0001), but not of brain side (F(1,22) = 0.088, P = 0.7696).

Activation was thus higher in SZ patients than HC subjects and

higher in the H than B condition (Fig. 8). No significant

interaction between the three factors was noted.

Discussion

The current study was undertaken to determine whether impair-

ments in odor familiarity and hedonicity judgments in SZ patients

are associated with modification of activation patterns in their

olfactory areas. Our results are consistent with other findings

suggesting that schizophrenia is a neurobehavioral disorder resulting

partly from a dysfunction in the temporo-limbic brain areas. In

contrast to HC subjects, patients evidenced functional abnormalities

in the olfactory areas during detection of odors as well as during

familiarity and hedonicity judgment tasks. Major functional

disturbances were observed in the left frontal piriform cortex, the

left inferior frontal, anterior ventral insular, medial orbital, superior

temporal gyri, and the right gyrus rectus. They resulted from a lack

of activation in brain areas during olfactory tasks in all cases but one.

Central olfactory impairments in SZ patients

In the current study, patients had the same acuity for detecting

suprathreshold odors as healthy subjects. This leads us to speculate

that the olfactory deficits observed in the SZ patients during more

complex tasks such as familiarity or hedonicity judgments (both in

terms of correct responses and reaction times) could be associated

with central impairments. However, despite the same detection

accuracy observed in both groups during the suprathreshold

detection task, patients exhibited activation patterns different from

those in healthy subjects. They had a relative lack of activation in

the left piriform cortex and inferior frontal gyrus, and showed

hyperactivation in the right insular gyrus, compared to the HC

group. It could be hypothesized that, when subjects and patients

detected an odor, they performed minimal cognitive judgments that

differed between populations.

Since no breathing data were recorded in this study, a source of

potential confound may lie in the different breathing patterns across

140

conditions and groups, as it has previously been shown that sniffing

alone can induce piriform activation (Sobel et al., 1998). However,

subjects in the present studywere trained to breathe regularly and not

to sniff. In previous studies, when breathing data were recorded and

analyzed (Plailly et al., 2005; Royet et al., 2003), we did not

evidence respiratory flow differences between experimental con-

ditions when subjects were asked to breath in the same way.

Furthermore, Kareken et al. (2004) recently compared piriform

activation induced by either the sniffing or the velopharyngeal

closure method, which prevents subject-induced airflow through the

nasal passage. They did not show any difference in piriform

activation between the two conditions, a result leading to the view

that sniffing, in the absence of odorants, does not activate the

piriform cortex.

Since SZ patients performed less well on the familiarity and

hedonicity judgment tasks, it may be suggested that the lack of

brain area activation in the present study was not the direct result of

temporo-limbic dysfunction, but the consequence of the patients’

inability to perform the tasks. In other words, temporo-limbic

structures could be functionally intact in SZ patients, but may not

be activated due to the behavioral impairment. This hypothesis is

nevertheless unlikely because most studies indicate sizeable

cytoarchitectural abnormalities in these regions with grey matter

volume reductions or a deficit of the cortical surface size in the

orbitofrontal, insular, entorhinal, perirhinal and temporopolar

cortices, the amygdala, the hippocampus, and the gyrus rectus

(Ananth et al., 2002; Arnold et al., 1991; Crespo-Facorro et al.,

2000a,b; Goldstein et al., 1999; Gur et al., 2000; Shenton et al.,

2001; Turetsky et al., 2003b; Wright et al., 1999). Furthermore, we

and others have shown (Hudry et al., 2002; Moberg et al., 2003)

that SZ patients can give appropriate intensity judgments and

correct hedonic responses for unpleasant odors, demonstrating

their fundamental ability to perform tasks. Consequently, behav-

ioral impairments observed in the current study were probably

caused by structural and functional abnormalities, and the lack of

activation observed during the olfactory judgment tasks probably

reflected this dysfunction.

Disturbance of familiarity judgments

Patients judged odors less familiar than HC subjects, replicat-

ing the results of our previous behavioral study (Hudry et al.,

2002). Recognition memory implies two different processes

known as familiarity, which is perceptual in nature, and

recollection, which includes the retrieval of contextual informa-

tion (Mandler, 1980). It has been shown that SZ patients have

reduced recollection abilities, yet intact familiarity judgments

(Achim and Lepage, 2003; Huron and Danion, 2002; Tendolkar

et al., 2002), but also that the recollection deficits could be

compensated by an increased proportion of familiarity judgments

(Edelstyn et al., 2003). The dissociation between both kinds of

processing was not specifically addressed in the current study and

participants could have performed recollection processing while

they were requested only to perform familiarity judgments.

Although related to familiarity deficits, our results could therefore

partly reflect a weak ability to recollect memories associated with

previously encountered odors. However, it could also be

suggested that the familiarity judgments of odors have distinct

neural bases from those observed for the familiarity judgments of

other sensory modalities, and that previously observed results

from visual and verbal items cannot be compared with our

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ARTICLE IN PRESSJ. Plailly et al. / NeuroImage xx (2005) xxx–xxx 9

results. The impairment found in the temporo-limbic and orbital

regions of our patients could thus reflect a deficit in the

familiarity judgment specific to the olfactory modality.

The piriform cortex has been implicated in odor recognition

memory in healthy subjects (Dade et al., 2002; Gottfried et al.,

2004) and more specifically in familiarity judgments (Plailly et al.,

2005). The decreased activation observed in the piriform cortex

when patients judged odor familiarity could therefore mirror their

low familiarity judgment scores. We must nevertheless note that

the decrease in this activation in patients is combined with an

abnormally high activation in the baseline condition in patients, an

unusual finding suggesting that schizophrenia could show itself in

hypermetabolism in the resting state. Along the same lines, Friston

et al. (1992) showed that deterioration in the psychopathology was

associated with an increased rCBF in the left medio-temporal

regions. It could thus be hypothesized that patients in the baseline

condition were not in the same cognitive state as the HC subjects.

This hyperactivation, however, concerned only a small part of the

brain (a subregion of the piriform cortex) and was observed only

for this comparison (out of 11 comparisons). It is therefore not

possible to generalize the result and interpretation of hyper-

metabolism indicated above. The fact remains that activation

differences found between the baseline and odor familiarity

judgment conditions in HC subjects were not observed in SZ

patients. In addition, we demonstrated that this difference was task-

specific, since activation differences were also found in the

familiarity judgment task when compared with the detection task

or with the hedonicity judgments condition.

During odor familiarity ratings, SZ patients did not exhibit

activation in the left medial orbital gyrus. Although slightly more

lateral and dorsal, this region was previously observed in the

familiarity judgment of odors (Royet et al., 2001). This impairment

in patients, related to behavioral response deficits, could reinforce

the role of this region in odor familiarity judgments. Nevertheless,

this region was also observed in hedonicity judgments of various

emotional odors (Royet et al., 2000, 2001), suggesting that it could

be involved in the common cognitive demands of the two olfactory

judgment tasks.

Finally, we noted an rCBF decrease in the opercular part of the

left inferior frontal gyrus, and right gyrus rectus in patients. The

conjunction analysis also demonstrated differences in the activa-

tion of the inferior frontal gyrus for patients and healthy subjects in

the two other olfactory tasks when compared with the baseline

condition. This difference was more marked in the familiarity and

hedonicity judgment tasks than the detection task, since differences

between the two groups persisted with the F–D or H–D contrasts.

This region was found to be activated during odor identification

(Kareken et al., 2003; Royet et al., 1999; Savic and Berglund,

2004), and involved in the selection and integration of semantic

information in a modality-independent manner (Homae et al.,

2002). The lack of activation in this area in patients could therefore

indicate their widely reported inability to gather evidence to

identify odors. (Hudry et al., 2002; Kopala et al., 1989; Serby et al.,

1990; Stedman and Clair, 1998). Regarding the gyrus rectus,

corresponding regions in the macaque receive projections from

lower olfactory areas such as the agranular orbital cortex and

anterior olfactory nucleus (Carmichael and Price, 1996). No

activation associated with olfactory stimulation has been reported

in these low orbitofrontal regions in previous fMRI studies, but

they are particularly sensitive to susceptibility artifacts, and only

Kareken et al. (2003), using PET, found them to be activated

141

during odor discrimination and identification. Although the role of

this region in odor processing is unclear, white matter abnormal-

ities have been shown both in it, in the inferior frontal gyrus and in

the medial orbital gyrus (Spalletta et al., 2003), leading to the

hypothesis that the lack of activation found in the present study

could be partly inferred from connection defaults.

Disturbance of hedonicity judgments

Although patients had appropriate hedonicity judgments with

unpleasant odorants, they estimated pleasant odorants less pleasant

than HC subjects, as has already been observed (Crespo-Facorro et

al., 2001; Moberg et al., 2003). In Hudry et al.’s (2002) study,

patients found odors more neutral than HC subjects, but scores

were not compared as a function of hedonic valence. Reanalyzing

these data, we found a reduction in the scores for pleasant odors

only, patients then finding pleasant odors more neutral than healthy

comparison subjects (P = 0.0021). This inability to judge pleasant

stimuli in an appropriate manner has also been observed with

visual stimuli (Quirk et al., 1998; Paradiso et al., 2003). Cacioppo

and Gardner (1999) argued that, from an evolutionary standpoint, it

is much more important to quickly detect facial expressions that

signal unpleasant or threatening events than expressions that signal

positive events, but they also emphasized that a patients’ inability

to recognize a positive valence for pleasant pictures is reflective of

the suffering they experienced during survival. The loss of the

capacity to subjectively experience pleasure is a typical clinical

feature of SZ patients and has been referred to as the anhedonia

state (Becker et al., 1993).

The amygdala is well known to play a central role in the

emotional processing of stimuli, but we did not observe any

difference in activation of the amygdala using a between-group

analysis. Focusing on this region, we demonstrated that hedonicity

judgments induced activation in both groups thereby explaining the

fact that no differential amygdalar activation was observed. This

finding is surprising since patients had inappropriate judgments of

pleasant odors during the experiment, and that abnormalities have

been found in this structure in previous studies (Shenton et al.,

2001). Two explanations can account for these data. Firstly,

amygdala activation in patients may explain either their appropriate

judgments of unpleasant odors or the higher proportion of odors

perceived as unpleasant relative to the HC subjects. These data are

consistent with previous results indicating that there is more

activation of the amygdala during exposure to aversive than

positively valenced stimuli and that the responses of the amygdala

are modulated by the hedonic strength of the stimuli (Royet et al.,

2003; Zald, 2003; Zald and Pardo, 1997; Zald et al., 1998). They

further corroborate Cacioppo and Gardner’s (1999) hypothesis

described above and the assertion that describes the amygdala as ‘‘a

router that permits a rapid and adaptive response to dangerous

stimuli’’ (Paradiso et al., 2003). Secondly, it has been suggested that

an unmodified response of the amygdala to affective stimuli could be

due to active neuroleptic medication in patients during task

performance (Paradiso et al., 2003). Since our patients were not

drug naıve, this hypothesis could also explain our activation results

in the amygdala.

The question is why pleasant odors are perceived as more

neutral or less pleasant by patients, and which cerebral structures

code pleasant experiences. Whereas aversive stimuli need not

reach conscious awareness to engage the amygdala in processing

(Zald, 2003), pleasant stimuli can induce conscious processing

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that must then engage neural substrates other than the amygdala.

The orbitofrontal cortex has for instance been shown to be

involved in affective processing. In olfaction, Zald and Pardo

(1997) observed that exposure to mildly aversive, so rather

neutral odorants, only activated the left orbitofrontal cortex (�42,

35, �14), and not the amygdala, and we have already shown that

the left orbitofrontal (�44, 32, �6) could mediate conscious

assessment of emotional odorants (Royet et al., 2003). This

region, described in both the above studies, was also found to be

activated during the present study in healthy subjects (�46, 34,

�8), and was called the left inferior frontal gyrus. The decrease

in the activation of this area in SZ patients during the hedonicity

judgments could thus be related to their poor performance for

pleasant odors.

The weakened pleasantness judgments of the patients in our

study could also be associated with the lack of activation

observed in the anterior part of the left frontal piriform cortex.

This assumption would corroborate Gottfried et al.’s (2002)

assertions that this subdivision is receptive to hedonic quality, and

findings in animals showing a functional dissociation in the

piriform cortex (Litaudon et al., 1997; Mouly et al., 1998).

Crespo-Facorro et al. (2001) studying the emotional response to

odor in SZ patients did not demonstrate any functional

disturbance of this structure. However, they directly compared

unpleasant and pleasant odors, which is a more restrictive contrast

than our analysis which compared olfactory conditions with an

odorless condition. In addition, by using a single odor repetitively

in each condition, they might have limited the signal strength by

increasing habituation (Poellinger et al., 2001). Further experi-

ments are needed to determine whether this part of the piriform

cortex participates in the coding of hedonicity judgments with

pleasant odors.

A lack of activation was also noted in the anterior ventral insula

during hedonicity judgments. This result can be associated with

previously observed reductions of cortical surface size and grey

matter volume in SZ patients (Crespo-Facorro et al., 2000a). The

insular cortex is known to be a multimodal integration region

linking sensory experiences with their appropriate emotional

response (Paradiso et al., 2003; Peyron et al., 2000; Royet et al.,

2003), but no clear data have been reported regarding its

involvement as a function of hedonic valence. Considering the

design of our experiment, brain activation depending on hedonic

valence could not be distinguished in the present study, but Crespo-

Facorro et al. (2001) found that SZ patients failed to activate the

insula only when experiencing an unpleasant, but not a pleasant

odor. This result agrees with hypotheses suggesting that it may

serve as an internal alarm center that alerts individuals to

potentially distressing interoceptive sensory stimuli, and may be

involved in both the perception and the feelings of disgust

produced by very unpleasant odors (Wicker et al., 2003). However,

it is inconsistent with both their and our behavioral results which

showed that subjective hedonicity judgments in SZ patients were

altered only for pleasant odors.

A functional disturbance lateralized in the patients’ left hemisphere

In our study, medio-temporal dysfunction in patients was

lateralized in the left hemisphere while normal cerebral activation

was found in the right side. This could be related to structural

abnormalities found on the left side in most studies performed

with SZ patients and schizotypal subjects. Volume reductions of

142

grey matter and white matter abnormalities have mainly been

observed in the left temporal lobe and prefrontal cortices (Dickey

et al., 1999; Shenton et al., 2001; Spalletta et al., 2003; Woodruff

et al., 1997). Since we previously demonstrated the strong

involvement of the left hemisphere in emotional odor processing

(Royet et al., 2000; Royet and Plailly, 2004), we suggest that this

dysfunction could explain the frequent anhedonia associated with

this illness.

Conclusion

SZ patients had inappropriate familiarity and hedonicity

judgments of odors. They judged odors less familiar and pleasant

odors less pleasant than HC subjects. These results were related

to functional abnormalities in temporo-limbic and orbital olfac-

tory areas. These dysfunctions were mainly lateralized in the left

hemisphere and concerned the left piriform cortex, inferior

frontal, and medial orbital gyri, but also the right gyrus rectus,

for the familiarity judgments and the left piriform cortex/insular

gyrus and inferior frontal gyrus for the hedonicity judgments.

They resulted almost exclusively from a lack of activation during

task conditions. Our results clearly show that schizophrenia is a

neurobehavioral disorder resulting partly from a dysfunction in

the temporo-limbic and orbital regions of the brain and including

those core areas involved in olfactory processing.

Acknowledgments

We thank the technical and medical staff of CERMEP as well as

the department of psychiatry (Pr. J. Dalery) at the Centre

Hospitalier Fle Vinatier_, for their valuable assistance. The authors

are indebted to the participants who have supported and

participated in the present study. We also thank the perfume and/

or aroma companies (Davenne, Givaudan-Roure, International

Flavors and Fragrances, Lenoir, Perlarom) for supplying the

odorants used in this study. This research was supported by the

Conseil Scientifique de la Recherche du Centre Hospitalier FleVinatier_, l’Universite Claude Bernard de Lyon (BQR), and the

Centre National de la Recherche Scientifique.

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CHAPITRE 3 : DISCUSSION GENERALE

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ANNEXES

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ANNEXE 1

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Journal of Neuroscience Methods 142 (2005) 35–44

A stimulation method using odors suitable for PET and fMRI studieswith recording of physiological and behavioral signals

M. Vigourouxa, B. Bertranda, V. Fargeta, J. Plaillya, J.P. Royeta,b,∗a Neurosciences and Sensory Systems Laboratory, CNRS UMR 5020, IFR 19, Neuroscience Federative Institute of Lyon,

Claude-Bernard University Lyon1, 50, Avenue Tony Garnier, 69366 Lyon Cedex 07, Franceb CERMEP, 69003 Lyon, France

Received 11 May 2004; received in revised form 12 July 2004; accepted 16 July 2004

Abstract

A design for a semi-automatic olfactometric system is described for PET and fMRI experiments. The olfactometer presents severaladvantages because it enables the use of an ‘infinite’ number of odorants and the synchronization of stimuli with breathing. These advantagesmean that the subject is recorded while breathing normally during olfactory judgment tasks. In addition, the design includes a system forr iven by thes he Faradayc©

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ecording the behavioral (rating scale) and physiological (breathing, electrodermal reaction (ED), plethysmography (PL)) signals gubject. Both systems present the advantage of being compatible with fMRI magnetic fields since no ferrous material is used in tage and signals are transmitted via an optical transmission interface to an acquisition system.2004 Elsevier B.V. All rights reserved.

eywords: Olfactometric system; PET; fMRI; Breathing; Electrodermal reaction; Plethysmography

. Introduction

Several methods of odorant stimulation have been used inresearch context. The easiest way to present odorants is tose a piece of odorant saturated cotton. Whereas this method

s directly usable in PET (Zatorre et al., 1992), the length ofhe tunnel in an fMRI imager means that a plastic rod at thend of which the cotton is placed must be used (Levy et al.,997). This method, however, is not very reliable, because itoes not allow the odor concentrations to be controlled, the

ime-course of the odors is imprecise and it can induce tactiletimulations if the experimenter touches the subject’s nose.more sophisticated method is that of dynamic olfactometry

e.g.,Dravnieks, 1974; Kobal and Plattig, 1978; Doty, 1991;arren et al., 1992; De Wijk et al., 1996). It is based on the

se of a deodorized vector gas which conveys the odorantapor towards the subject’s nose after activating a solenoidalve. Several authors have employed this method in cere-

∗ Corresponding author. Tel.: +33 4 37 28 74 95; fax: +33 4 37 28 76 01.E-mail address:[email protected] (J.P. Royet).

bral imaging studies (Yousem et al., 1997; Sobel et al., 191998a,b; Lorig et al., 1999; Gottfried et al., 2002a,busingLorig’s olfactometer). The main problem of olfactometdesigned using this principle is that they use only a limnumber of stimulation channels, giving rise to limited expmental designs, habituation, and then potential weakeniconcentrations due to repeated sampling of the sameor gas. Olfactometers made in the laboratory can cost frfew thousand Euros to close to 100 KEuros dependingthe specific design and number of channels.

In most of the first cerebral imaging studies, subjects wnot asked to perform a specific task during the actual sning period. When subjects need to perform a cognitiveit is recommended that experimenters use different stito avoid the problems associated with sensory habituor the performance of tasks in a routine manner (Demoneet al., 1993), but it is also interesting to record their behioral responses on line. These may for instance be bwhen subjects must judge whether the odor is intense ofamiliar or not, pleasant or unpleasant (Royet et al., 19992001; Gottfried and Dolan, 2003). They can be graduat

165-0270/$ – see front matter © 2004 Elsevier B.V. All rights reserved.oi:10.1016/j.jneumeth.2004.07.010

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36 M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44

when subjects rate the levels of familiarity or the hedonic in-tensity using the visual rating scale principle (De Araujo etal., 2003; Royet et al., 2003). The used method can be thenbased on the finger-span (FS) technique (Cerf-Ducastel andMurphy, 2001; Royet et al., 2003). It may also be pertinentto record any indications of the subject’s physiological ac-tivity inasmuch as this may reflect his reaction to a sensorystimulation. It is usually measurements of the autonomic ner-vous system that are made, such as the electrodermal (ED)reaction, plethysmography (PL), skin temperature and res-piratory frequency (Van Toller et al., 1983; Dittmar, 1989;Vernet-Maury et al., 1999). However, no system adapted forthe strong magnetic fields of an fMRI scanner is commer-cially available.

Our purpose was to perform cerebral imaging studieswhile subjects were performing olfactory judgment tasks. Wepropose a semi-automatic olfactometric system that can beused in both PET and fMRI environments, and that is basedon new concepts. It was conceived to respect three main ex-perimental conditions: the possibility of using an ‘infinite’number of odorants; using the highest possible number ofstimulations per scan or epoch; and synchronizing the stim-uli with the subject’s breathing. The first condition allows usto vary stimuli between olfactory tasks (Royet et al., 1999,2001), and to avoid habituation phenomenona. Subjects canc hilet di-t pira-t ap-t ndM op smell( i-n weret niff-i iorala Thet , ast ma-t dayc

2

be-h s isc ETd theF es ofm esena thet nd/orp com-p Theu aday

cage avoids these problems. Other materials which includemagnetic pieces are then placed in the control room. All theconnections between both kinds of material are made withoptical fibers.

2.1. Odor stimulating material

Odors are presented with an air-flow olfactometer, whichallows synchronization of the stimulations with breathing.Instead of using several channels and solenoid valves thatlead to over complexity, and of which the number is in anycase limited, our stimulation method is based on the princi-ple of directly delivering odors into a rapid airflow (to purgethe system) and then to convey the odorized air to the sub-ject via a tube made of very low adsorbent material (Teflon®

Fluorinated Ethylene Propylene). This can be accomplishedwithout drying the subject’s nose because the odors are notdelivered directly into the nostril, but into a facial mask andbecause a diffuser is used. In methods as used byYousem etal. (1997)andSobel et al. (1997), visual or auditory instruc-tions are presented to the subject asking him to synchronouslyinspire with a stimulation. In the current method, while thesubject is asked to breathe regularly, we locate his inspirationphases and deliver stimuli just at the end of an expiration. Thesubject must avoid sniffing or blocking his breathing. A ses-s bjectt r de-l thef inall thatn ctiono

parts( ces,a rt),a twop mag-n g thea ge.

2sly

f ana par-t ) to-w by am r oft sub-j rilsb idifyt thea

2min

w : an

onsequently concentrate on a given olfactory task wheir brain activity is being recorded. The last two conions involve the stimulation of subjects during each resory cycle, notwithstanding the well-known olfactory adation phenomenon (e.g.,Cain and Engen, 1969; Cain aoskowitz, 1974; Engen, 1982). Rather than using a viderojector to project a visual message asking subjects toSobel et al., 1997; Suzuki et al., 2001), we chose to subordate the odorous stimuli to subject’s breathing. Subjects

hus tested during a regular breathing rhythm, avoiding sng. We have further conceived a system to record behavnd physiological parameters during fMRI experiments.

wo systems are compatible with fMRI magnetic fieldshey do not induce electromagnetic radiation and onlyerials with no ferrous metals are used within the Faraage.

. Methods

The conception of odor stimulating apparatuses andavioral and physiological parameter recording systemonditioned by their more restrictive use in fMRI than Pue to magnetic fields. The use of magnetic material inaraday cage is proscribed for two reasons. Firstly, piecagnetic metal can be attracted into the magnet and prpotential risk for the physical integrity of the subject in

unnel. Secondly, materials including magnetic pieces aroducing electromagnetic wave radiation, such as auter can modify field lines and induce image distortion.se of plastic material or nonmagnetic metals in the Far

t

ion is performed before the scanning day to train the suo keep a regular rhythm of breathing, to detect an odoivered during inspiration, and to give a response beforeollowing stimulation. Odors are presented at a supralimevel and conveyed to the mask with a delay inferior toeeded for an inspiration phase (from 1.5 to 2 s as a funf the subjects).

The stimulating apparatus is composed of threeFig. 1): an air treatment part including the electronic devipneumatic part called the ‘injection head’ (air-dilution pand a facial mask. In the frame of an fMRI study, thesearts can be dissociated in order to keep only the nonetic pneumatic part near the magnet (2 m) while placinir treatment and electronic part outside the Faraday ca

.1.1. The air treatmentVector air (10 l/min) is pumped directly and continuou

rom the Hospital distribution network. It is treated withctivated charcoal filter, conveyed through a submicronic

icle filter (Deltech 115 Leca, New Castle Delaware, USards the olfactometer where its pressure is checkedanometer. Airflow is then fed into the mixing chambe

he injection head, and directed towards the nose of theect. Since airflow is not directly delivered into the nostut into a mask, it is not necessary to warm and humhe air. Airflow temperature and humidity are those ofmbient air.

.1.2. The injection head and odor bottlesThe injection head (50 mm high) is made in duralu

hich is not magnetic. It is composed of two chambers

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M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44 37

Fig. 1. Diagram of an olfactometer including the air treatment part placed outside the Faraday cage, and the injection head and odor mask situated in theFaraday cage. Left picture: box showing the superior part of the injection head and an injection head extracted from the box. Right picture: odor mask.F1,activated charcoal filter; F2, submicronic particle filter; LED, light emitted diode; M, manometer; NV, needle valve; PR, pressure regulator; T, Teflon®.

injection chamber and a chamber to mix the odor with theairflow. Airtightness between both chambers is maintainedwith a check valve made of a 5 mm stainless steel ball bearing(18/10 AISI 316) fitted to the conical superior part of the mix-ing chamber by a calibrated coil spring made of stainless steel(AISI 302, 9.5 spiral, 15 mm length, 0.2 mm wire diameter)(Cochet, France). The injection chamber is made airtight us-ing a butyl (isobutylene isoprene-IIR) rubber seal which actsas an anti-leak valve. During stimulation, the experimenterintroduces the dropper of a polyethylene bottle (Osi, France)into the injection chamber and rapidly squeezes it. The air,now saturated with the odorous product, induces a pressureover the steel ball, and enters the mixing chamber. A pressuregauge situated in the injection chamber allows the detectionof any superpressure produced from the bottle. This signal istransmitted to the optical transmission interface, and thenceto the acquisition system placed outside the Faraday cage.The injection head is enclosed in a die-cast aluminum box222 mm× 146 mm× 106 mm in dimension (Boss, UK). Adetailed scale drawing is given inFig. 2.

2.1.3. The facial maskThe odorized air is delivered into a commercially avail-

able anesthesia mask (Respiron, Europe Medical, France).Different types of mask can be used as a function of the sub-j 1/8B iffu-s voidst en-t g ismn 3 m

Fig. 2. Detailed drawing of the injection head. Dimensions are given in mm;M3, M5, dimensions of threads.

ect’s facial morphology. A brass silencer (Pneumax GSP, Italy) in the mask provides a rapid, homogenous dion of the odors, reduces decompression noise, and aactile stimulation of the subjects. To allow for sufficient vilation and odor elimination, a 15 mm-diameter openinade on the lateral part of the mask. A Teflon® tube (Fluori-ated Ethylene Propylene; 2.4 mm interior diameter and

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38 M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44

Fig. 3. Relative odorous concentration as a function of time for a stimu-lation with n-butanol. No units are given for concentration since the massspectrometer had not been previously calibrated.

in length) links the stimulating apparatus to the mask via acustom-made Teflon® connection. The use of Teflon® allowsus to minimize odor absorption and desorption phenomena.

2.1.4. Shape of the chemosensory stimulusIt is usually recommended that the shape of the concen-

tration curve of a chemosensory stimulus as a function oftime approximates a square wave (Evans et al., 1993). Torate the rise and fall times of odorous stimulation, we mea-sured the concentrations ofn-butanol in the facial mask byusing a mass spectrometer (Agilent MS5973, US). The facialmask was placed over a mannequin head and connected tothe injection head. The end of the mass spectrometer capil-lary was inserted into the mask 10 mm under the nose. Sincethe mass spectrometer filament can be destroyed by oxygennitrogen was used for the vector flow (10 l/min). The massspectrometer allowed acquisition of a spectrum, from whichwe could detect the amount of analyte, every 20 ms.Fig. 3shows data recorded after delivering ann-butanol stimulus.The odor was detected 430 ms after injection. Since the trans-fer time in the capillary is about 250 ms, the actual time forthe odor to reach, then diffuse into the facial mask is thereforeabout 180 ms. The rise time was about 280 ms to reach 70%of maximum (as suggested byEvans et al., 1993). and thetotal stimulation time was approximately 4 s.

2p

l pa-r llicp con-t eticfi tallicp tionsb not be

used because they produce antennas that can pick up electro-magnetic waves from the outside and transmit them into theFaraday cage. The oxygen spin frequency is 100 MHz whichcorresponds to the waveband of commercial frequency mod-ulation transmitters. To avoid this problem, optical fibers orpneumatic pipes can be used. A general schema of the stim-ulating and recording systems is illustrated inFig. 4.

2.2.1. Breathing recordingThe breathing rhythm of the subject is obtained by mea-

suring variations in ventral breathing. It is recorded with theaid of a foot bellows in polyvinyl chloride (Herga ElectricLimited, Suffolk, UK) held on the stomach with a flexiblebelt. Movements of the abdominal wall produce variationsin the internal volume of the foot bellows which is linkedvia a polyethylene tube to a sensitive bi-directional mass air-flow sensor (Honeywell AWM2100, US) transforming theflow into an electrical signal. This signal is amplified, andprovides an image of the airflow during breathing, but not ofbreathing volume (i.e., it is represented by the derivative, notthe integral of breathing). This signal is then transmitted viathe optical transmission interface to the acquisition systemand re-transmitted via the optical transmission interface to aheadphone via a voltage to frequency converter. The experi-menter then listens to the progressive variations in the soundw bassf s res-p thed owst justa

2(size

1 ont f then asp f1 needt thee rtingt micf3 sioni itials n.

2thys-

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.2. Materials of behavioral and physiologicalarameter recording

Devices used to record behavioral and physiologicaameters must satisfy two conditions. Firstly, no metaiece which could conduct electricity must be placed in

act with the subject’s skin as high variations of magneld can induce Foucault’s current that can heat up meieces and burn the subject. Secondly, electrical connecetween the inside and outside of the Faraday cage can

,

ith a treble frequency when the subject inspires and arequency when the subject expires. This method makeiration implicit for the experimenter and easy to controlelivery of an odorous stimulus. A regular respiration all

he experimenter to anticipate and to deliver a stimulust the end of an expiration phase.

.2.2. Electrodermal signalThe ED response is recorded from two electrodes

5 mm× 10 mm) made of Maillechort (Cu, Ni, Zn) placedhe third phalanx of the forefinger and the middle finger oon-dominant hand (Fig. 5A). The measurement method wreviously described byStrong (1970). A direct current o0�A is used to measure ED resistance. To obviate the

o manually check the range of the signal variation duringxperiment, we further compress its dynamic by convehe linear product of the ED resistance into a logarithunction. The resistance is then measured between 68 k� and.3 M�. The signal is transmitted via the optical transmis

nterface to the acquisition system. The dynamics of the inignal is re-obtained by applying an exponential functio

.2.3. Plethysmographic signalChanges in the peripheral blood flow response (Ple

ography) are recorded from an easy to attach sensor pn the third phalanx of the thumb of the non-dominant hFig. 5A). The photoelectric PL reflectance sensor contaight source to illuminate the finger segment and a photector to monitor returning light. Living tissue is transparo red and infrared light while nonhemolyzed blood istively opaque in this spectral range. As the blood vol

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M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44 39

Fig. 4. General setup schema for stimulating the subject and recording his behavioral and physiological signals. See the text for a detailed description. ADC,analog-to-digital converter; B, breath; ED, electrodermal; FS, finger-span; FVC, frequency-to-voltage converter; LED, light emitted diode; PCMCIA, acquisitioncard (National Instrument); PL, plethysmography; VFC, voltage-to-frequency converter.

changes, the amount of light absorbed or reflected changes,and as a consequence, the electrical characteristics of thephotodetector change as well. To reduce artifacts, we use alight source modulated in near infrareds, that is 900 nm. Thereflected radiation is first filtered in the near infrareds be-fore reaching the sensor. The photoelectric signal (processedby synchronous detection) is then amplified and transmit-ted, via the optical transmission interface, to the acquisitionsystem.

2.2.4. Behavioral responseFor a binary response, we use two key-press buttons (see

Royet et al., 1999). For a graduated response requiring theuse of a linear visual rating scale, the subject is instructed torate olfactory sensations, such as hedonic intensity, throughthe distance between the thumb and forefinger according tothe FS method (Berglund et al., 1978; Larson-Powers andPangborn, 1978; Yamamoto et al., 1985) recently usedin fMRI studies on gustation (Cerf-Ducastel and Murphy,2001). Two long rectilinear potentiometers (Piher, Spain) areused with respectively 45 and 63 mm of sliding travel de-pending on a given subject’s actual FS (Fig. 5B). The metal-lic parts of the potentiometers are suppressed and replaced

by a custom-made Plexiglas® support (180 mm× 45 mm×15 mm). Two Plexiglas® stops allow the subject to immobi-lize the thumb and the middle finger of the dominant handwhile the forefinger moves a plastic slide. The potentiome-ter is connected to a 1 Hz low-pass filter, then to the opticaltransmission interface and the acquisition system.

2.3. Optical transmission interface and acquisitionsystem

Transmission of the signal using optical pathways allowsus to satisfy two conditions. Firstly, it avoids introducingradio-electric interference into the Faraday cage. Secondly,it presents a galvanic insulation between the subject andthe acquisition system. The optical transmission interfacesare voltage-to-frequency (VFC) converters fitted with NickelCadmium batteries (750 or 1800 mA/h).

Behavioral and physiological data are recorded on line(100 Hz sampling rate) with a NEC PC computer and a mul-tifunction DAQCard-500 characterized by eight inputs, a flowof 50 kS/s, and 12-bit resolution (National Instruments, US).LabView 5.0 software (National Instruments, USA) is usedto acquire, store, and read these data.

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40 M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44

Fig. 5. (A) ED sensors placed on the third phalanx of the forefinger and themiddle finger, and a PL sensor placed on the third phalanx of the thumb ofthe subject’s non dominant hand. (B) FS device including a rectilinear slidepotentiometer with 63 mm travel. ED, electrodermal; PL, plethysmography;PS, plastic slide; S, Plexiglas® stop.

3. Operational example

3.1. Procedures

The data presented in the current study were collectedfrom a 24-year-old healthy right-handed non-smoking femalesubject. This subject had participated in a previous fMRIstudy in which 28 subjects performed hedonic judgmentswith pleasant and unpleasant odorants presented during onerun of three epochs each (Royet et al., 2003).

Data processing and statistical analysis methods have al-ready been described byRoyet et al. (2003). Briefly, fMRIwas performed using a 1.5-T imager (Philips NT). Twenty-five adjacent, 5 mm thick axial slices were imaged. The imag-ing volume covered the subject’s whole brain and was ori-ented parallel to the bicommissural plane. The image planeswere positioned on scout images acquired in the sagittalplane. A 3D PRESTO, less prone to the magnetic suscepti-bility artifacts than is the echo-planar imaging sequence (Liuet al., 1993), was used with the following parameters: TR =26 ms, TE = 38 ms, flip angle = 14◦, field-of-view = 256 mm2

× 205 mm2, imaging matrix = 64× 51 (voxel size of 4 mm×4 mm× 5 mm). A high-resolution anatomic 3D T1-weightedMR scan was also acquired.

The fMRI runs were analyzed using Statistical ParametricMapping (SMP99, The Wellcome Department of CognitiveNeurology, London, UK;Friston et al., 1995a,b). Image pro-cessing included inter-scan realignment, spatial normaliza-tion to the stereotactic space as defined by the ICBM templateprovided by the Montreal Neurological Institute (MNI), andimage smoothing using a three-dimensional Gaussian ker-nel (FWMH: 8 mm× 8 mm× 10 mm). A boxcar referencefunction was convolved with SPM99’s ‘canonical’ hemody-namic response function. Global differences in blood oxy-genation level dependent (BOLD) signal were covaried outof all voxels, and comparisons across conditions were ef-fected witht-tests. The significance of signal differences wasassessed throughZ-scores in an omnibus sense (Friston et al.,1995b), using an uncorrected probability with a threshold ofP < 0.001.

3.2. Results

A typical example of physiological and behavioral datarecorded for a 60 s epoch when the subject is smelling andjudging unpleasant odors is depicted inFig. 6. Thirteen odor-ous stimulations were delivered in a 60 s epoch indicating thatthe subject’s mean breathing was 4.62 s per cycle. For eachbreath cycle, an odorous stimulation was delivered just be-fs e FS.F thylp larlyu wereo y int e EDr

g tow whenp g in-s veals -r erea t oru be-t rants( un-p ,t ndb0 EDv1 ,r

un-p t per-f LDs sso-c andp

ore an inspiration phase (see the square-box ofFig. 6). Theubject provided a more or less ample response with thor instance, odors of tar, butyl sulfide, pyrrole, 2,5-dimeyrrole, and tetrahydrothiophene were judged as particunpleasant. Systematic variations of the ED responsebserved after each olfactory stimulation. A short dela

he ED response attests to the low time constant of thesponse.

Variations of breathing could be expected accordinhether the subject was recorded during rest epochs orleasant or unpleasant odors were delivered. Comparinpiratory flows between these different epochs did not reignificant differences [F(2, 102) = 0.789,P = 0.457]. Corelations between ED, FS and inspiratory flow values wlso calculated for this subject when smelling pleasannpleasant odorants. A significant correlation was found

ween ED and FS when the subject smelt unpleasant odoFig. 7), indicating that the more odors were rated asleasant, the higher the ED amplitude variations (r = 0.472= 3.124,P = 0.0036). No significant correlation was fouetween ED and FS for pleasant odorants (r = 0.163, t =.964,P = 0.3417), and between inspiratory flow andariations for pleasant and unpleasant odors (r = 0.198,t =.180,P = 0.2461 andr = 0.261, t = 1.554,P = 0.1298espectively).

fMRI activation was determined by contrasting theleasant olfactory and rest conditions when the subjec

ormed the hedonic judgment task. The results show BOignal variations in several brain regions commonly aiated with odor processing, such as the orbitofrontaliriform cortices, amygdala, and insula (Fig. 8).

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M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44 41

Fig. 6. Example of behavioral and physiological measurements recorded during an epoch for which 13 unpleasant odorants were synchronously delivered withthe beginning of each inspiration. Square-box (top) shows two breathing cycles superimposed with stimulations 8 and 9. Inspiration and expiration phases arerespectively represented by the superior and inferior parts of the horizontal reference line. ED, electrodermal; FS, finger-span; PL, plethysmography. Data weredepicted with the WinDaq Waveform Browser 1.91 software (DataQ Instruments, Inc., USA).

Fig. 7. Correlation between FS and ED data obtained during hedonic judg-ment of unpleasant odorants.

4. Discussion

The method of odor stimulation presented in the currentstudy has proved its validity since regions activated in bothour PET as fMRI studies (Royet et al., 1999, 2000, 2001,2003) were reliable and consistent with those obtained byother authors (e.g.,Zatorre et al., 1992; Sobel et al., 1997,1998a; Zald and Pardo, 1997).

By synchronizing odorous stimulation with inspiration,our olfactometer allows the stimulation of the subject using agreat diversity of odorants during the experiment and a highnumber of odorants during a scan or an epoch, which is notthe case of olfactometers proposed by other researchers andbased on a different principle (Sobel et al., 1997; Lorig et al.,1999). For instance, for a mean breath rhythm of about 4–5 sand 1 min of brain activity recording, 12–15 stimulations canbe performed depending on the duration of the breath cy-cle. This advantage allows subjects to satisfactorily performan olfactory task by improving their attention ability and in-creasing the signal by repeating stimulation while avoidingsensory habituation phenomenona. Although this frequency

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42 M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44

Fig. 8. fMRI activations covering regions of interest during hedonic judgment of unpleasant odorants. Activations were superimposed on axial sections (4 mmapart) from an anatomically normalized standard brain. Sections extended from−24 to−8 mm (MNI Z coordinates are given below the image). The gray scaleindicatesT values.

of sensory stimulation is lower than that employed in neu-roimagery for other modalities, it is much higher than thatcurrently used in olfaction when the experimenter wants toavoid the exacerbated phenomenon of odor adaptation (Cainand Moskowitz, 1974; Engen, 1982). However, the high flowof the vector air (10 l/min) avoids odors stagnating in themask, and thus produces a more punctual odorous stimula-tion. When synchronizing odors with breathing, the numberof odorous stimulations per scan or epoch depends on theindividual (since the duration of the breathing cycle can varyfrom 2.5 s to more than 10 s), but can also vary for any onesubject from one scan or epoch to another. To homogenizethe number of stimulations between subjects, it therefore isnecessary to select these subjects as a function of their res-piratory cycle. When the duration of the breathing cycle isvery short, the phenomenon of odor masking is increased.A cycle of long duration (low stimulation frequency) avoidsthese disadvantages, but the subject no longer needs to focushis attention on the task once he has responded, since severalseconds will pass before the following stimulus is delivered.

Compared with other methods of stimulation, our olfac-tometer does, however, present some limitations. Whereaswe can suppose that the control of odor concentration is re-liable with olfactometers in which the airflow is imposed bysolenoid valves, it seems more difficult to precisely control itw uallyd dor-a ther.R ents stim-u thes iono ira-t f ani

thes est-i eyesc toryt d. Thfi them ta tter

concentrated on the olfactory task. It also induces activationpatterns mostly limited to the olfactory neural networks byavoiding systematic activation of perceptual and semantic vi-sual or auditory neural networks. The results clearly indicatethat odors were delivered at the beginning of an inspiration,and that the subjects had time to respond before the followinginspiration. The current study further demonstrates the pos-sibility of simultaneously recording the behavioral responsesof the subject, which is more efficient that re-measuring olfac-tory performance after scanning (Levy et al., 1997, 1998; Zaldand Pardo, 1997; Cerf-Ducastel and Murphy, 2001; Crespo-Facorro et al., 2001; Savic et al., 2002). The present paper fi-nally shows that the physiological parameters, such as breath-ing, ED and PL can be recorded online and the measurementsthen analyzed in different experimental conditions especiallyin studies linked to emotion. The significant correlations be-tween the ED and FS responses testify to the reliability ofthese measurements.

The present olfactometric method was designed to be usedin PET and fMRI experiments where the duration of thescans or epochs was 60 s. This method is, however, suitablefor fMRI studies with shorter epochs (10 s) (Wicker et al.,2003) and in event-related fMRI experiments. Since stimula-tion timing of our olfactometer could be longer than that ob-tained with some other methods (e.g., Lorig et al., 1999), thism ent-r pointi nly tos a ac-q eterc spira-t tro-p thats ap-p undert

A

ithM ria-t the

ith our method, because the quantity of odorant is manelivered by squeezing the odor bottle. The quantity of ont delivered may then vary from one stimulation to anoeliability of stimulation timing was not rated in the prestudy, but it is also dependent on our manual method oflation that was conceived to synchronize stimuli withubject’s breathing. Therefore, reliability is mainly a functf the experimenter’s ability to locate the subject’s insp

ion phases and to deliver the stimuli at the beginning onspiration.

Synchronizing the stimulations with inspiration allowsubject to be firstly in a regular respiration condition for tng without the need to sniff, and secondly, to keep hislosed and his ears plugged while performing the olfacask since no visual or auditory messages are then neederst point avoids the recording of activations related tootor activity of sniffing as previously observed bySobel el. (1998a,b). The second point allows the subject to be be

e

ay preclude its use for psychophysiological or rapid evelated studies. Nevertheless, we think that the crucialn recording these responses in such paradigms is maiynchronise the stimulus with inspiration, and to start datuisition at the beginning of an inspiration. Our olfactoman satisfy such constraints. It thus appears that the inion cue represents the limiting factor for performing elechysiological studies of olfactory evoked potentials, andubordination of the stimulus to inspiration allows suchroaches even when the odorants are presented directly

he nostrils with a bottle (Hudry et al., 2001, 2003).

cknowledgements

We would like to thank S. Garcia for conceiving watlab the software to measure the physiological va

ions, and J.L. Gass and L. Fine for their contribution in

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M. Vigouroux et al. / Journal of Neuroscience Methods 142 (2005) 35–44 43

measuring of odor concentration as a function of time us-ing a mass spectrometer. We are very grateful to anonymousreferees for pertinent comments, and to W. Lipski for cor-recting the English language of the paper. This work wassupported by research grants from the Rhone-Alpes Region,the Groupement d’Interet Scientifique (Sciences de la Cogni-tion), the Centre National de la Recherche Scientifique, andthe Universite Claude-Bernard de Lyon.

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ANNEXE 2

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fMRI of emotional responses to odors:influence of hedonic valence and judgment, handedness, and gender

Jean-P. Royet,a,d,* Jane Plailly,a Chantal Delon-Martin,b David A. Kareken,c

and Christoph Segebarthb

a Neurosciences and Sensory Systems, CNRS UMR 5020, Claude-Bernard University Lyon1, 69007 Lyon, Franceb INSERM/UJF U594 Unity, LRC CEA 30V, 38043 Grenoble, France

c Department of Neurology, Indiana University School of Medicine, Indianapolis, IN 46202, USAd CERMEP, Neurological Hospital, 69003 Lyon, France

Received 4 March 2003; revised 10 June 2003; accepted 26 June 2003

Abstract

Previous positron emission tomography studies of right-handed individuals show that the left orbitofrontal cortex is dominant duringemotional processing of odors. We collected functional magnetic resonance imaging data from 28 subjects to study this network as afunction of odor hedonic valence (pleasant vs. unpleasant), active hedonic judgments versus passive sensation of hedonically charged odors,handedness, and gender. Two functional runs were performed, with pleasant and unpleasant odors presented in different epochs. In the firstrun, subjects passively smelled odorants, whereas in the second run they rated degree of odor pleasantness or unpleasantness by using a“finger-span” technique that simulated a visual rating scale. Electrodermal and plethysmography responses were simultaneously recordedto control for covert, physiological manifestations of the emotional response. The piriform-amygdala area and ventral insula were activatedmore for unpleasant than pleasant odors. More extreme ratings were also associated with higher electrodermal amplitude, suggesting thatactivation stemmed more from emotional or hedonic intensity than valence, and that unpleasant odors induced more arousal than pleasantodors. Unpleasant odors activated the left ventral insula in right-handers and the right ventral insula in left-handers, suggesting lateralizedprocessing of emotional odors as a function of handedness. Active decisions about odor pleasantness induced specific left orbitofrontalcortex activation, implicating the role of this area in the conscious assessment of the emotional quality of odors. Finally, left orbitofrontalcortex was more active in women than men, potentially in relation to women’s well-documented advantage in odor identification.© 2003 Elsevier Inc. All rights reserved.

Keywords: Olfactory emotion; Hedonic valence; Hedonic judgment; Handedness; Gender; fMRI

Introduction

Emotion and hedonic judgment are primary facets ofolfaction (Herz and Engen, 1996). Odors are also knownto influence mood, induce alertness or relaxation, andevoke long-forgotten emotional memories. The close re-lationship between olfaction and emotion is a logicalconsequence of how both processes share several limbicregions. Despite the view espoused by several authors

that negative emotions are associated with the right hemi-sphere (Davidson, 1992; Canli et al., 1998), several re-cent positron emission tomography (PET) studies haveinstead reported strong activations of the left amygdalaand orbitofrontal cortices (OFC) when subjects smellhighly aversive odors (Zald and Pardo, 1997; Zald et al.,1998a), or perform a hedonic judgment task (Royet et al.,2001). We also demonstrated that emotional judgmentsshare similar left hemispheric networks, independently ofwhether emotions are induced via olfactory, visual, orauditory sensory modalities (Royet et al., 2000). Otherneuroimaging studies have similarly indicated strong in-volvement of the left hemisphere in emotional processing(Pardo et al., 1993; Morris et al., 1998).

* Corresponding author. Neurosciences and Sensory Systems, Claude-Bernard University Lyon1, CNRS UMR 5020, 50 Avenue Tony Garnier,69007 Lyon, France. Fax: �33-4-37-28-76-01.

E-mail address: [email protected] (J.-P. Royet).

NeuroImage 20 (2003) 713–728 www.elsevier.com/locate/ynimg

1053-8119/$ – see front matter © 2003 Elsevier Inc. All rights reserved.doi:10.1016/S1053-8119(03)00388-4

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Nevertheless, there are limitations to this corpus of work.First, in studies on hedonic judgment, the activity specific toa given hedonic valence could not be determined sincepleasant (P) and unpleasant (U) odors were intermingledduring the same scan. Thus, it remains an open question asto whether P and U odors activate the same neural network.Second, our previous PET studies were conducted in right-handers (RH) only, begging the question as to whether theresults generalize to left-handers (LH). In some behavioralstudies on olfaction, lateralized differences as a function ofhandedness have been reported, but the data conflict andother studies reveal no differences (Koelega, 1979; Youn-gentob et al., 1982; Zatorre and Jones-Gotman, 1990; Fryeet al., 1992; Hummel et al., 1998). Third, our previous studyof cross-modal emotional activation revealed a large neuralnetwork stretching from the amygdala to the superior frontalgyrus. However, these regions might participate in differentlevels of emotional processing. For example, Reiman et al.(1997) suggested that the superior frontal gyrus might playa role in the conscious experience of emotion. Finally,behavioral studies show that women clearly outperformmen in odor identification (Cain, 1982; Doty et al., 1985;Engen, 1987). Nevertheless, neuroimaging studies of odorperception have not shown consistent gender differences incerebral activation (Levy et al., 1997, 1999; Yousem et al.,1999; Bengtsson et al., 2001).

The purpose of this fMRI experiment was to study brainregions associated with odor hedonic valence, and the effectof handedness on the lateralization of emotionally inducedactivation. P and U odors were presented in different epochswhile subjects rated their degree of pleasantness or unpleas-antness. Electrodermal (ED) and plethysmography (PL) re-sponses were also recorded to control for covert, physio-logical manifestations of the emotional response. The studyfurther examined the extent to which different neural net-works were engaged by explicit hedonic judgments, andincluded a sufficiently large sample of men and women toenable a robust comparison between activation patternsacross genders.

Materials and methods

Subjects

Twenty-eight subjects (20–30 years of age) participated,comprising 4 groups of 7 subjects classified by handedness(as determined by the Edinburgh Handedness Inventory)and gender. Subjects were selected on the basis of theirolfactory ability with a forced-choice suprathreshold detec-tion test (at least 91% correct) and of the mean duration oftheir breathing cycle (4.08 � 1.12 s). Subjects with rhinaldisorders (colds, active allergies, history of nasal-sinus sur-gery, or asthma), neurologic disease, ferrous implants (e.g.,pacemakers, cochlear implants, etc and so on), or claustro-phobia were excluded. Subjects with anhedonia, as rated

with the Physical Anhedonia Scale (score � 29; Chapmanet al., 1976), were also excluded. Participation required amedical screening and written informed consent. Sevenfemale subjects were on contraceptive medication and 7other females not on contraceptive medication tested nega-tive for pregnancy. The study was approved by the localInstitutional Review Board and conducted according toFrench regulations on biomedical experiments on healthyvolunteers.

Odorous stimuli

One hundred twenty-six odorants were used. Ninetyodorants were used for both functional runs. They were splitinto 6 sets of 15 odorants as a function of perceived hedo-nicity and intensity ratings (Table 1) from data obtained inprevious work (Royet et al., 1999). For pleasant (P) condi-tions, 3 sets (Pa, Pb, and Pc) contained P odorants selectedso as to provide the highest scores. Similarly, in the un-pleasant (U) condition 3 sets (Ua, Ub, and Uc) contained Uodorants selected for their lowest scores. Odorants were alsoselected such that mean intensity scores were identical be-tween hedonic conditions and between sets. Accordingly,analyses of variance (ANOVA) showed that hedonicity, butnot intensity scores, significantly differed between P and Uconditions [F(1,84) � 503.433, P � 0.0001 and F(1,84) �2.016, P � 0.1593, respectively], and that neither hedonic-ity nor intensity scores differed between sets within thesame hedonic condition [F(2,84) � 0.103, P � 0.9026 andF(2,84) � 0.660, P � 0.5164, respectively]. No hedonicvalence � set interaction was present for hedonicity andintensity scores [F(2,84) � 0.001, P � 0.9991 and F(2,84)� 0.595, P � 0.5540]. In each set the order of presentationof P or U odors was pseudorandomized but identical for allsubjects. For training, 36 neutral odorants (score range of4–5) and 9 bottles with odorless air were used. Odorantswere diluted to a concentration of 10% using mineral oil.For presentation, 5 ml of this solution was absorbed intocompressed polypropylene filaments inside of 100-ml whitepolyethylene squeeze bottles with a dropper (Osi, France).

Stimulating and recording materials

Odors were presented with an airflow olfactometer,which allowed synchronization of stimulation with breath-ing. The stimulation equipment was essentially the one usedin a previous PET study (Royet et al., 1999), but adapted soas to avoid interference with the static magnetic field of thescanner. Specifically, the apparatus was split into two parts:the electronic part of the olfactometer positioned outside themagnet room (shielded with a Faraday cage), and the non-ferrous (aluminum) air-dilution injection head installed nearthe magnet. Compressed air (10 l/min) was pumped into theolfactometer, and delivered continuously through a com-mercially available anesthesia mask. At the beginning ofeach inspiration, odor was injected into the olfactometer,

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which carried it to the subject’s anesthesia mask. Breathing(B) was recorded with the aid of a PVC foot bellows (HergaElectric Ltd, Suffolk, UK) held on the stomach with a judobelt. An operator monitored breathing and squeezed theodor bottle so as to flush the odor into the injection headduring inspiration. The ED signal was recorded from twostainless steel electrodes placed on the tips of the index andmiddle fingers of the nondominant hand. PL responses wererecorded from a sensor fixed to the tip of the thumb of thenondominant hand.

Subjects rated hedonic intensity in Run2 (and respondedrandomly in Run1) by using the “finger-span” (FS) tech-nique (Berglund et al., 1978; Larson-Powers and Pangborn,1978; Yamamoto et al., 1985; Cerf-Ducastel and Murphy,2001), which simulated a visual rating scale by havingsubjects vary the distance between the thumb and forefingerto approximate a linear scale. Two long rectilinear potenti-ometers (4.5 and 6.3 cm of sliding travel) were used de-pending on a given subject’s actual finger span. The thumbof the dominant hand was fixed to one end of the potenti-ometer while the forefinger moved a slide. The potentiom-eter was connected to a 1-Hz low-pass filter and then to ananalog-to-digital converter.

ED, PL, FS, B, and odor stimulation signals were trans-mitted by means of optical fibers to AD converters poweredby nickel-cadmium batteries. Behavioral and physiologicaldata were recorded online (100 Hz sampling rate) using anNEC PC computer equipped with a digital acquisition boardDAQCard-500 (National Instruments, USA). LabView 5.0software (National Instruments) was used to acquire, store,and read data. Data analysis was performed with the

WinDaq Waveform Browser 1.91 software (DataQ Instru-ments, USA).

Experimental procedure

Two functional runs (Run1 and Run2) were performed(Fig. 1) in a single fMRI session. A block paradigm wasapplied and consisted of hedonic odor conditions (P and Uepochs) alternating with odorless rest (R) epochs. Eachepoch lasted 60 s. This relatively large epoch was employedto compensate for slight asynchronies in the beginning andend of each epoch and the subject’s inspiratory phase, whichis concomitant with odorant stimulation. For each run, bothP and U conditions were presented three times each, so as topermit a balanced experimental design (Latin square). Theorder of conditions/odor sets for a given subject in Run1was repeated in Run2. For olfactory stimulation in Run1,subjects passively smelled the odorants and responded ran-domly with the FS apparatus. For olfactory stimulation inRun2, subjects made a hedonic judgment by moving the FSslide according to their perceived level of pleasantness orunpleasantness. For P, ratings ranged from neutral, whichrequired very little movement, to very pleasant at the ex-treme of FS. For U, ratings similarly ranged from neutral tovery unpleasant Subjects were asked not to move the slidein the absence of perceived odors in either of the hedonicconditions. For R, subjects were requested not to respond atall. The “passive smelling” condition (Run1) always pre-ceded the “hedonic judgment” condition (Run2) to not biasthe subject during the passive condition with the explicitknowledge of the hedonic judgment task.

Table 1List of odors selected for epoch of Pa, Pb, Pc, Ua, Ub, and Uc conditions

Pa Pb Pc Ua Ub Uc

1 Apricot Pear Citronella Garlic Onion Santalol2 Lemon Raspberry Apple Tar Mustarda 4-pentanoic acid3 Lavender Violet Rose Ethyl phenyl acetate Furfuryl mercaptan Pine needle4 Sage Honeysuckle Lime Butyl bromide Beer Butyl sulfide5 Coconut Jonquil Mint IAPAb Butyric acid 2-Bromophenol6 Wild rose Orange Strawberry Hexane Nonyl acetate Guaiacol7 Caramel Chewing-gum Biscuit Pyrrole Isovaleric acida Ethylmercaptana

8 Lis Chocolate Bread Mushroom Caproic acid Valeraldehyde9 Melon Tobacco Grapefruit 2-Heptanol Acetone Tetrahydrofurane

10 Anise Banana Carnation 2,5-Dimethyl pyrrole Methyl isonicotinate Butanol11 Ethyl nitrite Hazel Bitter almond Tetrahydrothiophenea Heptanal Wine12 Nutmeg Jasmine Gardenia Tetralin 2-Octanol Ethyl acetate13 Passion fruit Fennel Bergamote Ethyl propionate Amyl valerate Methyl-2-furoate14 Lilac Vervain Cinnamon Hexanal Pizza 1,4-Dichlorobutane15 Vanilla Iris Garrigue Ethyl pyrazine Ethyl diglycol ValerolactoneHedonicityMean score (SD) 5.85 (0.86) 5.75 (0.68) 5.82 (0.85) 2.13 (0.71) 2.05 (0.76) 2.10 (0.84)Score range 4.55–7.24 4.51–6.65 4.59–7.04 0.79–3.01 0.80–2.85 0.45–3.04IntensityMean score (SD) 5.46 (0.67) 5.47 (0.80) 5.80 (0.51) 6.07 (0.88) 5.70 (1.48) 5.91 (1.28)Score range 4.30–6.62 4.14–6.65 4.70–6.48 1.55–7.92 3.35–7.73 1.20–8.25

a Underlined name, odorant with high potency and of which the concentration was limited to 1%.b iso-Amylphenyl acetate.

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General instructions were provided to subjects beforeeach run. During each run, and 3 s before each experimentalcondition (P, U, or R), the subjects were instructed orally bymeans of specific key words (“pleasant,” “unpleasant,” and“rest”) which task was to be performed next. Subjects woreearplugs as protection from the scanner noise and kept theireyes closed during scanning. The day before fMRI, subjectswere trained outside the MR facility to breathe regularly, todetect odorants without sniffing during normal inspiration,and to rate odor intensity using the FS technique duringexpiration.

Imaging parameters

Functional MR imaging was performed on a 1.5-T MRimager (Philips NT). Twenty-five adjacent, 5-mm-thick ax-ial slices were imaged. The imaging volume covered thesubjects’ whole brain and was oriented parallel to the bi-

commissural plane (Fig. 2). The image planes were posi-tioned on scout images acquired in the sagittal plane. A 3DPRESTO three-shot MR imaging sequence (Liu et al., 1993)was used with the following parameters: TR � 26 ms, TE� 38 ms, flip angle � 14°, field-of-view � 256 � 205 mm2,imaging matrix � 64 � 51 (pixel size of 4 � 4 � 5 mm3).The PRESTO sequence is less prone to the artifacts inducedby susceptibility differences between brain tissue and theunderlying bone and air than is the echoplanar imaging(EPI) sequence usually applied in fMRI (Frahm et al.,1988). These susceptibility artifacts induce MR signal loss,particularly in the OFC and mesial temporal region (Zaldoand Pardo, 2000). To illustrate the typical image qualityfrom the PRESTO sequence, three orthogonal slices from anaveraged 3D functional image from one subject are depictedin Fig. 2. During each functional scan, the volume of inter-est was scanned 144 times successively. The signal wasaveraged three times, leading to an acquisition time per

Fig. 1. Experimental procedure including two runs (Run1 and Run2) with 12 epochs of 60 s each. Two hedonic conditions were performed with P odorantspresented for 3 epochs (Pa, Pb, Pc), and U odorants presented for 3 epochs (Ua, Ub, Uc). Each run provided 144 temporal volumes of 12 slices each. R, rest.Fig. 2. Three orthogonal slices from an averaged 3D functional three-shot PRESTO image from one of the subjects. The signal-to-noise ratio in the OFC werecomputed using the approach of Parrish et al. (2000), and ranged from approximately 80 to 200. The minimum value of 80 allowed detection of a 1% BOLDsignal change with a detection rate (beta) of 95% in case of a t test with an alpha of 1%. Axial (A), coronal (B), and sagittal (C) orientations.

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volume of 5 s. A high-resolution anatomic 3D T1-weightedMR scan was acquired between both functional runs. In LH,an additional gradient-recalled echo EPI MR pulse sequence(GRE-EPI) functional scan was run during a verbal fluencytask (Pujol et al., 1999) to assess hemispheric dominance forlanguage. Our results indicated that 10 subjects (71.4%)were left lateralized, 2 (14.3%) had right hemispheric lan-guage dominance, and 2 had bilateral involvement.

Data processing and statistical analyses

fMRI runs were analyzed using Statistical ParametricMapping (SMP99, The Wellcome Department of CognitiveNeurology, London, UK; Friston et al., 1995a, 1995b).Image processing included interscan realignment, spatialnormalization to stereotactic space as defined by the ICBMtemplate provided by the Montreal National Institute(MNI), and image smoothing with a three-dimensionalGaussian kernel (FWMH: 8 � 8 � 10 mm) to overcomeresidual anatomical variability and increase signal-to-noise.A boxcar reference function was convolved with SPM99’s“canonical” hemodynamic response function. Global differ-ences in BOLD signal were covaried out of all voxels, andcomparisons across conditions were effected with t tests.The significance of signal differences was assessed throughZ scores in an omnibus sense (Friston et al., 1995b), using

an uncorrected probability with a threshold of P � 0.001.An MRI template and Duvernoy’s (1991) anatomic nomen-clature were used to localize and describe anatomic regionsof activation.

Olfactory main effects were calculated by contrasting theolfactory and rest conditions (e.g., U1-R). Specific effectswere calculated by comparing unpleasant (U1 and U2) withpleasant (P1 and P2) conditions for both functional runs (U1vs. P1, U2 vs. P2, and U1U2 vs. P1P2), and by comparingpassive smelling (Run1) and hedonic judgment (Run2) withU2 vs. U1, P2 vs. P1, and U2P2 vs. U1P1 contrasts. Ran-dom effects analyses (SPM99, Wellcome Foundation, Lon-don) were applied to extrapolate statistical inferences intothe healthy population. This two-stage analysis accountedfirst for intrasubject (scan-to-scan) variance, and second forbetween-subject variance. During the first step, scan-to-scanvariance was modeled for each subject individually by cre-ating a summary contrast image from weighted parameterestimates that reflected each scan condition. These contrastimages were then used in a second, between-subjects levelof analysis that employed basic model t tests to assess thecondition effects. Four kinds of groups were consideredaccording to handedness and gender. Since random effectsanalyses require large subject samples, analyses could notbe performed on 4 groups of 7 subjects each. Therefore,males and females with the same handedness were re-

Fig. 3. Recording of behavioral and physiologic measures. Example of an epoch of 60 s for which 12 U odorous stimulations were synchronously deliveredat the beginning of inspiration. Finger-span (FS), plethysmography (PL), and electrodermal (ED) responses were recorded for each odorant.

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grouped either into the RH or LH groups. Similarly, RH andLH of the same sex were regrouped into the male or femalegroups. Separate analyses by subject group were then per-formed using basic model, one-sample t tests. Between-groups analyses were also performed using two-sample ttests to compare patterns of activation as a function ofhandedness and gender. However, these direct comparisonswere hampered by the fact that we were forced to analyzeonly relative olfactory differences, as our rest condition didnot involve motor activity. The signal strength of the rela-tive differences between groups is thus a more difficultphenomenon to test in a between-groups model. For thisreason, we compared groups on the basis of their thresh-olded activation.

Results

Behavioral and physiological data

A typical example of the physiological and behavioraldata recorded during a 60-s epoch of olfactory stimulation isdepicted in Fig. 3. From 12 to 20 odor stimulations weredelivered per epoch, depending on the subject’s respiratoryrate.

Mean FS, ED, and PL measurements per epoch wereanalyzed as a function of Handedness (RH vs. LH), Run(Run1 vs. Run2, i.e., random response vs. explicit hedonicjudgment), and Hedonic (Pa, Pb, Pc, Ua, Ub, Uc) conditions(Fig. 4). FS data were normalized with respect to bothpotentiometer sizes. Multivariate ANOVA of these sets ofdependent measures showed significant main effects forHandedness [Wilks’ �(3,310) � 10.45; P � 0.001], Run[Wilks’ �(3,310) � 13.96; P � 0.001], and Hedonicity[Wilks’ �(15,856) � 2.69; P � 0.001], but no significantinteractions between these factors. We then performedthree-way ANOVAs separately on FS, ED, and PL, withHandedness as a between-groups factor, and Run and He-donicity conditions as repeated measures. For FS, therewere significant main effects for Run and Hedonicity[F(1,26) � 17.87, P � 0.0003, and F(5,130) � 5.62, P �0.001, respectively], and a significant Run � Hedonicityinteraction [F(5,130) � 3.70, P � 0.0035]. The main effectof Run reflects higher FS ratings during Run1 than duringRun2, likely secondary to the subjects’ random responsesduring Run1. The main effect for Hedonicity reflects sig-nificantly more extreme FS ratings for U odors (Fig. 4), andsuggests that these odors were hedonically more intense.For ED, there was a significant main effect of Hedonicity[F(5,130) � 6.08, P � 0.001] and a significant interaction-between Handedness and Hedonicity [F(5,130) � 3.57, P �0.005]. This interaction was due to the LH’s higher EDresponses in U than P conditions for both runs, irrespectiveof explicit hedonic analysis. For PL, there was a significantmain effect of Run [F(1,26) � 22.67, P � 0.001] andHedonicity [F(5,130) � 14.78, P � 0.001], as well as a

significant Run � Hedonicity interaction [F(5,130) � 3.15,P � 0.010]. Thus, while cardiac rhythm was clearly relatedto hedonic intensity, it declined generally over the course ofthe imaging period, suggesting progressive habituation dur-ing the experiment.

Fig. 4. Behavioral and physiological scores as a function of Handedness(Right-hander vs. Left-hander), Run (Run1 vs. Run2), and Hedonic valence(Pa, Pb, Pc vs. Ua, Ub, Uc) for finger-span (FS, top), electrodermal (ED,middle), and plethysmography (PL, bottom). The vertical bars (plus orminus directions) show the SEM. The y-axis for FS represents both P andU odors, spanning the range from “neutral” to the extreme of P or U.

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Table 2Correlations (Fischer’s r test) between FS and ED values in different conditions

Subject Run1 Run2

P U P U

r p r p r p r p

1 0.102 0.6375 0.368 0.0765 0.378 0.0225 0.636 0.00012 0.151 0.3828 0.396 0.0162 0.069 0.6904 0.430 0.00833 0.168 0.3303 0.3327 0.0511 0.009 0.9590 0.431 0.00804 �0.082 0.7068 0.247 0.4486 0.579 0.0001 0.635 <0.00015 0.481 0.0035 0.387 0.0229 0.169 0.3348 0.472 0.00326 0.385 0.0195 0.337 0.0440 0.081 0.6409 0.209 0.2267 0.034 0.8462 0.379 0.0219 0.640 <0.0001 0.378 0.02238 �0.065 0.7102 �0.125 0.4689 0.043 0.8068 0.471 0.00339 0.364 0.0284 0.344 0.0392 0.097 0.5769 0.395 0.0164

Note. Bold, significant probability wtih p � 0.05.

Table 3Areas activated in P and U conditions of both runs relative to the R condition in RH and LH

Handedness Contrast Brain region Size voxels T values MNI coordinates

x y z

RH P1-R Insula 212 6.39 46 18 �10U1-R Hypothalamus 35 5.27 10 �6 �10P2-R Insula 1317 10.28 �40 14 0

Insula 9.61 �36 18 �6OFC 7.16 �42 42 �12OFC 763 9.30 40 28 �8Hypothalamus 24 5.90 �10 �2 �10

U2-R Insula 852 7.58 �38 16 �6Insula 7.14 �46 20 �6OFC 6.31 �30 28 �16Insula 399 6.68 38 16 �10OFC 6.36 38 28 �8Limen insulae 4.78 30 10 �12Amygdala 67 5.19 �22 �2 �12

P1U1P2U2-4R Insula 1233 9.91 �42 24 �4Insula 7.77 �44 10 �2Precentral gyrus 6.36 �54 14 8OFC 933 7.31 58 18 12OFC 7.30 40 28 �8OFC 6.73 48 22 �6OFC 149 7.18 �42 46 �12

LH P1-R OFC 369 8.16 44 18 �2Precentral gyrus 6.43 58 10 10Precentral gyrus 4.77 46 8 2

U1-R Insula 53 6.61 �42 8 �12OFC 281 6.06 �26 38 �18Insula 5.59 �34 20 0

P2-R OFC 77 5.02 �40 50 6OFC 4.46 �36 42 14OFC 4.04 �34 44 22Lateral sulcus 44 4.40 44 14 �10

U2-R Insula 146 5.10 �42 6 �8Insula 4.77 �48 14 �8Insula 96 4.82 40 8 �12Insula 3.97 40 16 �4

P1U1P2U2-4R Insula 309 7.09 �34 18 0Insula 6.82 �40 4 �8Insula 215 6.05 42 18 �4Insula 4.66 38 8 �12OFC 78 5.69 �40 50 6Hypothalamus 40 5.05 �10 �6 �14

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ED amplitude showed high intersubject variability:whereas a few subjects did not show any response, 9subjects exhibited clear changes with olfactory stimula-tion. Correlation coefficients between ED and FS valueswere calculated for these 9 subjects as a function of bothRun and Hedonic valence (Table 2). ED and FS werecorrelated mainly in the U condition of both runs. Sig-nificant correlations in the U condition for Run1 showthat behavioral responses from these 9 subjects were notcompletely random, but influenced by the odorants’ he-donic intensity.

fMRI activations

Olfactory conditions vs. restWhen the images from the P and U conditions were

contrasted with those from the rest (R) condition (U1-R,P1-R, U2-R, P2-R, U1U2P1P2-4R), significant activationswere found in a neural network encompassing the insula,OFC, cingulate gyrus, piriform cortex, amygdala, hypothal-amus, and superior temporal gyrus (Table 3 and Fig. 5). Inboth RH and LH, there were significant activations bilater-ally, but predominantly in the left insular and inferior frontal

Fig. 5. Localization of task-specific activations (P1U1P2U2-4R) as a function of handedness. Activations were superimposed on horizontal sections (2 mmapart) from an anatomically normalized standard brain. Sections extended from �20 to 0 mm (MNI Z coordinates provided below the image), the zero valuedefining the horizontal plane passing through the anterior and posterior commissures. Clusters were thresholded at T � 3.1. Color scales indicate T values.Fig. 6. Localization of activations as a function of hedonic valence and hedonic judgment task in RH and LH. Sagittal and horizontal sections showingolfactory activations in hedonic valence (U1U2-P1P2) and hedonic judgment task (P2U2-P1U1) conditions. Z indicates the coordinate along the vertical linepassing through the intercommisural plane. See Fig. 4 for details.

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cortices. In addition, more areas were activated in Run2(U2-R, P2-R) than in Run1 (U1-R, P1-R), with particularlystrong OFC activation during hedonic judgments (Run2).Since FS was not used during the rest period, motor areaactivation was evident when contrasting the olfactory andresting conditions.

Hedonic valence and handedness effectsTo reveal activations specific to hedonic valence, we

compared images acquired in the P condition with thoseacquired in the U condition (Table 4 and Fig. 6A). Wefound many more activations for the U-P contrasts (U1-P1,U2-P2, U1U2-P1P2) than for the P-U (inverse) contrasts.The former contrasts led to activations in the piriform cor-tex, the amygdala, and the ventral insula in the left hemi-sphere in RH, and only in the right ventral insula in LH. Wealso observed cingulate activation in RH and left superiortemporal gyrus activation in LH.

Hedonic judgment taskActivations due to explicit hedonic judgments were ob-

tained by subtracting images acquired in Run1 from thoseacquired in Run2 (P2-P1, U2-U1, P2U2-P1U1). Significantactivations were found mainly in the insula and the OFC inRH (Table 4, Fig. 6B). No significant activation was ob-served in LH.

Gender effectsThe 28 subjects were divided into 2 groups according to

gender (14 males and 14 females). In men, contrasting theolfactory conditions with the resting conditions led to acti-vation principally in the bilateral insula and in the leftpiriform-amygdala region. In women, activations were lo-

cated in these same areas, as well as in the left OFC (Table5 and Fig. 7).

Discussion

This study of the neural correlates of emotionally va-lenced olfactory stimuli shows that the same left hemisphereneural network was engaged, regardless of the odors’ he-donic valence. Nevertheless, parts of this network, includ-ing the ventral insula and piriform-amygdala region, weremore active in RH with U odors, which according to FS andED data, were hedonically more intense. The hemisphericpredominance of this response appears to depend on hand-edness, with the left ventral insula responding most in RHand the right ventral insula responding most in LH. Further,active hedonic judgments recruited additional areas in theinsula and caudal OFC—areas that did not activate whensubjects only passively smelled the hedonically chargedodors. Finally, the OFC was more strongly activated inwomen than men.

Olfactory network as a function of hedonic valence

A similar neural network was activated by P and Uodorants when contrasting olfactory against rest conditions.This included the piriform-amygdala region, the hypothal-amus, the superior temporal gyrus, the insula, the OFC, andthe anterior cingulate gyrus. This network includes areasdescribed in our previous studies (Royet et al., 2000, 2001),and appears to be similar in RH and LH, albeit with weakeractivations in the latter. It is well known, however, thatcognitive function is less lateralized in LH (Laeng and

Fig. 7. Localization of olfactory activations as a function of gender. Horizontal sections depicting olfactory activations (P1U1P2U2-4R) in males and femalesfor every 2 mm in z coordinates from �20 to 0 mm. The clusters were thresholded at T � 3.1. See Fig. 4 for details.

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Peters, 1995), consistent with our language data showingonly 70% of the LH to be left-dominant for language. Apossible confound also exists in that parts of this putativenetwork might have been obscured by FS-related activation.For example, we cannot rule out the possibility that someprefrontal areas might mediate both the planning of an FSresponse and explicit hedonic analysis. By contrasting the Pand U conditions directly, such confounds may be avoided,but those contrasts provide only relative differences be-tween U and P odors and not the overall network involvedin more general decisions about hedonic perception. ForU-P contrasts, we mainly observed amygdala-piriform andventral insula activations, while no activation was observedwith the P-U contrasts.

Zald and Pardo (1997) previously found substantial ac-tivation in both amygdalae and the left OFC during expo-sure to highly aversive odors, but only in left OFC duringexposure to less aversive odorants. Gottfried et al. (2002)found that unpleasant odors also activated the left OFC, butonly the right amygdala. By contrast, no activation in bothamygdalae was found with pleasant odors. Zald and Pardo(1997) suggest that the more aversive an odor, the more itevokes activity in the amygdala. In the current study, more

activation in the amygdala for U compared to P odorantscannot be related to perceived intensities since the odorswere selected to be of identical intensity on the basis ofpsychophysical ratings (Royet et al., 1999). The behavioraland physiological data acquired during active hedonic judg-ments further revealed that hedonic reaction was strongerwith U than with P odors, and that individual subject vari-ations in ED amplitude were significantly correlated withFS ratings in a few subjects, especially in U conditions. Theremaining subjects who did not show this correlation maynot typically express autonomic activity via ED responses.For example, Vernet-Maury and colleagues (1991, 1999)studied 6 different autonomic nervous system parametersand found that subjects typically reacted through a specific,preferential channel.

From these findings, we speculate that activation in theamygdala-piriform area is mostly from the strength of theperceived emotion (emotional or hedonic intensity), ratherthan from the type of emotion per se (hedonic valence). Thatis, our U stimuli induced a stronger emotional response thanour P stimuli, independently of perceived intensity. Thisformulation is consistent with Rolls’ (1999) hypothesis thatthe amygdala mediates both negative and positive emotions,

Table 4Areas activated in hedonic valence and hedonic judgment task conditions in RH and LH from contrasts applied between olfactory conditions

Condition Handedness Contrast Brain region Size voxel T values MNI coordinates

x y z

Hedonic Valence RH U1-P1 Piriform/amygdala 46 5.53 �30 4 �24Piriform/amygdala 5.21 �22 2 �24

P1-U1 Cingulate gyrus 116 4.76 �12 �30 32P2-U2 Middle temporal gyrus 60 7.18 �44 �38 �2

Insula 79 5.64 36 12 14U1U2-P1P2 Piriform/amygdala 19 5.03 �20 0 �24

Amygdala 5.03 �14 �8 �22Insula 4.12 �44 �2 �8

LH U1U2-P1P2 Ventral insula 56 4.99 38 6 �16Hedonic Judgment Task RH P2-P1 Insula 93 5.85 �36 20 �10

OFC 72 4.89 �42 40 �6OFC 4.59 �36 40 �14

U2-U1 Insula 145 6.59 38 16 �6OFC 5.68 36 22 �16OFC 5.59 40 28 �4OFC 37 5.27 �34 28 �14OFC 59 4.51 54 30 8OFC 3.89 54 28 18

P2U2-P1U1 OFC 66 6.24 40 30 �6Middle temporal gyrus 35 6.07 �44 �28 �8Insula 32 5.71 34 �14 0Middle temporal gyrus 63 5.21 �52 �4 �6Insula 4.32 �44 �6 �4Insula 86 5.19 �34 20 �10OFC 4.73 �34 30 �14OFC 34 4.75 �42 40 �8OFC 4.24 �44 32 �6Insula 21 4.30 36 6 �2Insula 4.06 36 16 �6

LH No significant results

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Table 5Areas activated in P and U conditions relative to the R condition in male and female subjects

Gender Contrast Brain region Size voxels T values MNI coordinates

x y z

Male P1-R Insula 748 6.93 44 16 �2Insula 6.41 42 4 0OFC 6.10 56 12 16Superior temporal gyrus 214 5.95 �52 10 0Insula 5.51 �40 16 �4

U1-R OFC 63 8.32 54 14 14Insula 302 6.40 �38 12 �12Insula 6.14 �40 4 �8OFC 5.61 �40 20 �14Precentral gyrus 65 6.33 �56 10 26OFC 4.50 �60 6 16Insula 104 5.87 40 6 �12

P2-R Insula 361 7.28 �44 8 �4OFC 6.75 �44 20 �12OFC 4.66 �32 20 0Lateral sulcus 311 6.53 48 20 �8OFC 6.41 38 24 �8OFC 4.50 32 28 �14Hypothalamus 89 5.54 �12 �6 �12

U2-R Insula 270 9.15 �50 12 �8Insula 4.86 �42 20 �6Superior temporal gyrus 731 7.77 46 4 �10OFC 7.28 38 22 �12Lateral sulcus 7.06 50 14 �10Piriform/amygdala 141 5.86 �22 0 �18

P1U1P2U2-4R Insula 766 10.85 �40 4 �6Insula 8.51 �40 20 �4OFC 6.41 �44 20 �12OFC 999 6.79 38 24 �10Insula 6.59 38 16 �6Lateral sulcus 6.55 48 20 �8Piriform/amygdala 203 6.27 �20 0 �18Amygdala/hypothalamus 6.24 �12 �6 �12

Female P1-R Precentral gyrus 45 7.53 �54 4 34OFC 180 6.09 50 22 0Precentral gyrus 5.02 58 12 10

U1-R OFC 122 7.12 24 34 4OFC 373 6.58 �20 28 8

P2-R OFC 394 8.56 �50 26 2Precentral gyrus 6.94 �46 20 6OFC 5.83 �44 40 �2Insula 109 6.34 �32 18 �4Insula 801 9.97 �36 14 �6

U2-R OFC 6.67 �28 30 �16OFC 6.18 �44 44 �10

P1U1P2U2-4R OFC 538 9.05 �28 34 �14Insula 7.07 �32 20 �4Insula 5.32 �50 18 �4OFC 68 6.70 44 22 �6Insula 146 6.45 �38 4 �12Insula 3.99 �40 16 �12Insula 71 5.87 36 8 �12OFC 283 5.64 �42 40 �2OFC 5.59 �40 46 �14OFC 4.77 �38 38 10Hypothalamus 28 5.21 �6 �8 �16Hypothalamus 3.87 �10 �2 �10

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and that differences in activity of this area stem from theintensity of the induced emotion. Whereas amygdala acti-vation has been observed principally for negative stimuli(e.g., the current study, Zald and Pardo, 1997; Gottfried etal., 2002), this can be explained by the level of arousal thatthese stimuli induce (Zald, 2003). For example, it has beendemonstrated that arousal correlates with valence intensity:in stimuli ranging from neutral to highly unpleasant, there isalmost always a strong correlation between arousal ratingsand ratings of unpleasantness (Lang et al., 1993). By con-trast, the relationship between valence intensity for pleas-antness and arousal appears more complex, since highlypleasant stimuli can be experienced as arousing, but also asextremely relaxing and calming (Zald, 2003).

Recently, Anderson et al. (2003) found that amygdalaactivation was associated with odor intensity, rather thanodor valence. In manipulating two odorants, they observeda greater response in the amygdala from high-intensity va-leric acid than low-intensity valeric acid when these odorswere equated for valence (i.e., both odors about equallyunpleasant). By contrast, they did not observe a greaterresponse to the unpleasant (low-intensity) valeric acid whencompared to the pleasant (low-intensity) citral odor whenthey were equated for subjective intensity. They thereforeconcluded that the amygdala’s response was associated withstimulus intensity, but not valence. However, it so happensthat these authors selected odors in a narrow intensity range(from 4 to 6 for a 9-point visual rating scale) to manipulateodor valence, and also a narrow valence range (from 4 to 5)to manipulate intensity. The authors thus used odors thatwere close to the neutral range, or in other words, odorswith a limited range of emotional intensity. In our study,odors that were clearly at more extremes of unpleasantness(maximum hedonicity of 0.7 for maximum intensity of 8.0)were perceived as more intense and more likely to haveevoked a much stronger emotional reaction than the pleas-ant odors (maximum hedonicity of 7.0 and maximum in-tensity of 6.6). This is probably because very unpleasantodors are well known to induce more violent reactions ofdisgust, whereas rarely do pleasant odors induce an analo-gous reaction (i.e., intense euphoria). It is for this reasonthat we believe that the greater response of the left piriform-amygdala to unpleasant odors most reflected the strength ofthe emotional response. Thus, whereas we agree withAnderson et al. (2003) that the amygdala does not respondto valence per se, we strongly suspect that emotional inten-sity, and not simply perceived psychophysical intensity, isthe decisive factor in activating the amygdala.

Odorous stimulation produced a number of activations inventral insula, a structure into which piriform cortex extendsa limb at the insula’s most anterior and ventral extent(Mesulam and Mufson, 1985). Insular activation has beenreported in response to a large variety of innocuous tactile,electrical, vibratory, and thermal stimulations, as well as toswallowing, urinary retention/micturation, and visceralstimulation (see Peyron et al., 2000, for review). Olfactory

and gustatory stimulations similarly evoke activation withinthe insular cortex (Zatorre et al., 1992; Fulbright et al.,1998; Small et al., 1997, 1999; Sobel et al., 1998; Faurionet al., 1999; Savic et al., 2000; Cerf-Ducastel and Murphy,2001; Kareken et al., 2003), especially when stimuli areunpleasant (Kinomura et al., 1994; Kettenmann et al., 1997;Zald et al., 1998b). Insular activity is also found duringbiological urges, such as dyspnea, hunger, thirst, and nausea(Tataranni et al., 1999; Banzett et al., 2000; Peiffer et al.,2001), as well as during emotional conditions such as hyp-nosis (Rainville et al., 1999), exposure to frightening faces(Phillips et al., 1997; Morris et al., 1998), sadness, anguish,fear, happiness (Damasio et al., 2000), sexual excitation(Stoleru et al., 1999), phobia, obsessive-compulsive urges(Rauch et al., 1995, 1996), and anticipation of anxiety andpain (Chua et al., 1999; Ploghaus et al., 1999), and aversiveconditioning (Buchel et al., 1999). The anterior insula may,in fact, serve as an internal alarm center that alerts individ-uals to potentially distressing interoceptive sensory stimuli,and imbues them with negative emotional significance(Reiman, 1997).

Lateralization of emotional processing as a function ofhandedness

We found evidence of lateralized emotional processing,as the OFC and insula showed stronger activation in the lefthemisphere. The right OFC was also activated, but moreweakly in intensity and spatial extent. We previously re-ported that the right OFC is mainly related to odor famil-iarity judgments (Royet et al., 2001). Interestingly, odorspresented to the right nostril are perceived as more familiarthan when presented to the left (Broman et al., 2001).

Although the data conflict, lateralized differences in ol-factory performances (sensitivity and discrimination) as afunction of handedness have also been reported (e.g., Tou-louse and Vashide, 1899; Youngentob et al., 1982; Cain andGent, 1991; Frye et al., 1992; Hummel et al., 1998). Re-cently, hedonic judgments have further been associated withhandedness (Dijskerhuis et al., 2002), although the effectswere complex due to the interaction between handednessand gender. In the present study, the U-P contrasts showedactivation of the left piriform-amygdala region and the mostventral part of the left insula in RH, and of the right insulaventral part in LH. These results constitute the first neuro-imaging observation of an interaction between lateralizationof olfactory emotional processing and handedness, althoughHirsch et al. (1994) and Faurion et al. (1999) also foundunilateral activation mainly in the ventral insula of thehemisphere contralateral to the dominant hand in subjectswhose tongue was stimulated with various tastes. We didnot find lateralized olfactory emotional processing in theright piriform-amygdala region of LH, perhaps becausetheir cognitive functions are less lateralized in general(Laeng and Peters, 1995), or alternatively, because this areadoes not lateralize strongly in general. Anatomic differences

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as a function of handedness have nevertheless been de-scribed. Szabo et al. (2001) for instance noted that the rightamygdala is larger than the left amygdala in right-handers,but also showed that such an asymmetry is lacking inleft-handers. An olfactory stimulus can include a trigeminalcomponent when the intensity of the stimulus is high. Sincetrigeminal projections are known to be controlateral, acti-vation observed in the present study could be associatedwith the trigeminal (somatosensory) dimension of our stim-uli. It appears, however, that pure somatosensory stimuliactivate the second somatic cortex (SII), and that tempera-ture, pain, and numerous interoceptive modalities stemmingfrom the body instead activate dorsal insular cortex (Craig,2002). The anterior ventral part of insula (closely associatedwith piriform cortex region) activated in the current study,and this finding is more consistent with the emotional con-sequences of stimulation, as reported in other data of thisliterature (e.g., Rauch et al., 1995; Buchel et al., 1999;Morris et al., 1999; Eliott et al., 2000).

Influence of hedonic judgment task

This study is the first to experimentally dissociate cere-bral areas involved in either primary hedonic perception ora conscious hedonic judgment task of P and U odors. Sincethe passive smelling condition systematically preceded thehedonic judgment task condition, comparisons of activationpatterns between these two conditions were confounded byan order effect, but also contaminated by possible centralhabituation from stimulus repetition. Specific activation wasnevertheless observed in the hedonic judgment task despiteof these different effects. Actively performing the hedonicjudgment task specifically induced bilateral activation in theinsula and the OFC, but more so in the left hemisphere inRH. This result is consistent with our previous findings withPET (Royet et al., 2000, 2001). Thus, while the piriform-amygdala region is directly involved in the perception of anodor’s hedonic intensity, the lateral OFC appears to mediateconscious assessment of P and U odorants. We thereforesuspect that the OFC activation in Zald and Pardo’s (1997)subjects, who passively detected mildly aversive or P odor-ants, was evoked by spontaneous hedonic judgments. Theseobservations are consistent with hypotheses that OFC playsa role in evaluating the appetitive or aversive reinforcementvalue of a stimulus (Zald and Kim, 1996; Rolls, 1999),while prefrontal cortex participates in generating behaviorthat is flexible and adaptive, rather than deterministicallydriven by the current sensory input (Elliott et al., 2000).Only a few studies have investigated the effect of taskdemands in other modalities. For instance, Gorno-Tempiniet al. (2001) examined the correlates of incidental and ex-plicit processing of the emotional content of faces express-ing either disgust or happiness. Different structures includ-ing the left amygdala and OFC were activated depending onwhether subjects made explicit judgments either of disgustor happiness, or of either of these emotions compared to a

condition devoid of affect. These data indicate that hedonicdecisions themselves can be a decisive component in acti-vation, which given the nature of our design, we cannotaddress with these data.

Influence of gender

We demonstrated clear differences in brain activationpatterns between males and females when passively smell-ing emotional odors or performing odor hedonic judgments.While males mainly showed bilateral activation of the in-sula, females also activated the left OFC. Cerebral process-ing of odor perception has been compared between thesexes (Levy et al., 1997, 1999; Yousem et al., 1999), al-though these studies compared either percentages of acti-vated pixel area to total brain area (Levy et al., 1997, 1999),or percentages of activated voxels in right and left frontal ortemporal lobe volumes (Yousem et al., 1999). In addition,the findings were inconsistent, since the size of women’sactivated fields was smaller in Levy’s studies, but consid-erably larger in Yousem’s study. In a more recent PETwork, Bengtsson et al. (2001) specifically studied spatialpatterns of cerebral activation with statistical parametricmapping and found no gender differences. One possibleexplanation for the discrepancy between these results is thatsubjects in the Bengtsson et al. (2001) study did not performexplicit olfactory tasks during scanning, and in particular ahedonic judgment task. Further, these authors used only 5stimuli that were either pleasant (vanillin, lavender, cedaroil) or somewhat unpleasant (butanol, eugenol). Repeateduse of this small number of stimuli might have also led tocentral habituation (Demonet et al., 1993). Gender-relateddifferences in the patterns of hypothalamic activation wereobserved by Savic et al. (2001), but they used two odorouspheromone-like steroids as stimuli. Thus, while gender-related differences have been reported in the activationpatterns of word processing, visual stimulation, spatial nav-igation, and working memory (Shaywitz et al., 1995; Levinet al., 1998; Gron et al., 2000; Speck et al., 2000), thepresent study is the first report demonstrating specific, lo-calized gender differences in the processing of commonodors.

Well-known gender differences in olfaction include afemale advantage in odor identification (Cain, 1982; Doty etal., 1985; Engen, 1987). This difference holds for familiar,nonbody odors, and all age categories. Anatomical/physio-logical differences in the structure of the nasal airways,olfactory neural pathways, and endocrine system may ac-count for some of these differences (Doty et al., 1985), butdifferences in socialization, discriminative ability, and moreintentional learning, memory, and verbal facility (Coltheartet al., 1975; Engen, 1987; Schab, 1991) might also contrib-ute. Olfactory hedonic judgments are likely closely relatedto odor identification (Royet et al., 1999, 2001) and requirethe left OFC, close to language areas. Split-brain patientswho have undergone resection of the corpus callosum (but

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not of the anterior commissure) identify odors better whenthey are presented to the left nostril (Risse et al., 1978;Eskenazi et al., 1988). Women may also process lexical-emotional stimuli more accurately than men (Grunwald etal., 1999), and this advantage might generalize to olfactoryperception. Women’s greater left OFC activation duringolfactory hedonic judgments could thus correspond withbetter verbal skills and olfactory identification.

Conclusion

To our knowledge, this is the first functional imagingstudy to examine explicit hedonic processing of olfactorystimuli, and to compare the neural correlates of olfactoryhedonic perception across handedness. The results showthat, compared to passive perception, overt judgments of theodors’ hedonic valence involved a left-dominant networkincluding the insula and orbitofrontal areas. Our results alsosuggest that the left piriform/amygdala/ventral insula regionactivates more strongly with U than P odorants, that is, isstrongly related to the strength of an emotion, but is inde-pendent of perceived subjective intensity and of the emo-tion’s valence. Further studies in which emotional valenceand intensity are systematically varied are however neededto confirm these hypotheses. Women also appear to activateleft OFC more strongly than did the men. Finally, this sameregion also appears to be involved most significantly in RH,while LH activate the contralateral (right) piriform/amyg-dala in response to U odors, suggesting a relationship be-tween olfactory emotional processing and manual domi-nance.

Acknowledgments

This work was supported by research grants from theRegion Rhone-Alpes, the Groupement d’Interet Scientifique(Sciences de la Cognition), the Centre National de la Re-cherche Scientifique, and the Universite Claude-Bernard deLyon. The Laboratoire des Neurosciences et Systemes Sen-soriels belongs to the Institut Federatif des Neurosciencesde Lyon. We thank M. Vigouroux, V. Farget, and B. Ber-trand for conceiving stimulating and recording materials, N.Zaafouri for assistance during the fMRI experiments, andJ.P. Lomberget and M.B. Sanglerat for medical examina-tions of subjects participating in the study. We are gratefulto the companies Givaudan, International Flavour and Fra-grances, Lenoir, Davenne, and Perlarom for supplying theodorants used in this study.

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ANNEXE 3

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Chem. Senses 29: 731–745, 2004 doi:10.1093/chemse/bjh067

Chemical Senses vol. 29 no. 8 © Oxford University Press 2004; all rights reserved.

Correspondence to be sent to J.P. Royet, Neurosciences and Sensory Systems, Claude-Bernard University, Lyon 1, CNRS UMR 5020, IFR 19, Institut Fédératif des Neurosciences, 69366 Lyon cedex 7, France. e-mail: [email protected]

Abstract

Over the last ten years, methods of cerebral imaging have revolutionized our knowledge of cognitive processes in humans. Animpressive number of papers dealing with cerebral imaging for olfaction have been published to date. Whereas the early worksrevealed those structures participating in the processing of odours presented passively to subjects, researchers later recordedbrain activity when subjects performed specific olfactory tasks based on memory, emotion and identification. From theseresults, we suggest that there is a dissociation of olfactory processes, with involvement of the right hemisphere in memoryprocesses and the left hemisphere in emotional processes. The review concludes with a summary of how these lateralizedprocesses are consistent with the gestalt-nature of our olfactory perception.

Key words: emotion, familiarity, fMRI, hedonicity, judgement task, lateralization, olfactory processes, PET

Introduction

Human lesion studies since the 1970s have made a substan-tial contribution to our understanding of the neuralsubstrate participating in the processing of olfaction (e.g.Gordon and Sperry, 1969; Gazzaniga et al., 1975; Mair andEngen, 1976; Risse et al., 1978; Abraham and Mathai, 1983;Eichenbaum et al., 1983; Eskenazi et al., 1983, 1986, 1988;Zatorre and Jones-Gotman, 1991), but it is only since the1990s that functional imaging techniques have revealedlarge-scale activation patterns associated with cognitiveprocesses and have thus allowed the identification of theneural networks specifically activated by odours. Since thefirst studies using cerebral imaging, more than 100 specificpapers and several reviews have been published (Kobal andKettenmann, 2000; Zald and Pardo, 2000; Zatorre andJones-Gotman, 2000; Brand et al., 2001; Kettenmann et al.,2001; Savic, 2001, 2002).

The purpose of the current review is not to present anoverview of this emerging literature, but to focus on a majorfinding of the data: the lateralization of olfactory processesas a function of the kind of task performed by the subjects.After a rapid presentation of the basic anatomical data, and

the various methods of cerebral imaging, we shall presentneuroimaging data acquired at the level of the orbitofrontalcortex (OFC) and amygdala, while attempting to respect thechronological order of both the findings and the evolutionof the concepts and ideas. Briefly, findings indicate thatmost of the first studies showed activation in the right OFC,which has since been associated with the familiarity judge-ment task. Activation of the left OFC was simultaneouslyevidenced during both stimulation with emotional odoursand when subjects performed a hedonicity judgement task.This lateralization of olfactory processes as a function of thetype of olfactory task was further extended to the olfactoryprimary cortex and the amygdala. It was hypothesized thatthe familiarity and hedonicity of odours was consistent withour holistic perception of odours, and that the right–leftdichotomy of olfactory processes facilitated or contributedto increased survival from an evolutionary point of view.

The olfactory system: anatomical data

A great deal of data has been accumulated on the neuralbasis of odour processing, both in humans and animals. We

REVIEW

Lateralization of Olfactory Processes

Jean-Pierre Royet1,2 and Jane Plailly1

1Neurosciences and Sensory Systems, Claude-Bernard University Lyon 1, CNRS UMR 5020, IFR 19, Institut Fédératif des Neurosciences, 69366 Lyon cedex 7, France and 2CERMEP, 69003 Lyon, France

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shall only give a brief report of this anatomical data, becausea detailed description would be beyond the scope of thecurrent paper. The reader may consult the following reviewsfor further information (Scott, 1986; Takagi, 1986; McLeanand Shipley, 1992; Shipley et al., 1995; Shipley and Ennis,1996).

From the olfactory receptors located in the superiorregion of the nasal cavity, axons lead to the olfactory bulbsituated under the ipsilateral cerebral hemisphere. The olfac-tory bulb cells are connected to the primary olfactory cortexby the fibres of the lateral olfactory tract (Shipley and Reyes,1991). The olfactory cortex comprises the anterior olfactorynucleus, tenia tecta, olfactory tubercle, piriform cortex (PC),anterior cortical amygdaloid nucleus, periamygdaloid andentorhinal cortices (Figure 1). These projections are prima-rily ipsilateral. Only a few controlateral connections

between both sides of the olfactory system via the anteriorcommissure have been reported (Shipley and Ennis, 1996).The major subcortical projections of the PC are thethalamus, the hypothalamus and the ventral striatum (Priceand Slotnick, 1983). The lateral entorhinal cortex is themajor source of afferent input to the hippocampus (VanHoesen and Pandya, 1975), and the nuclei of the thalamushas further connections towards the OFC and the insularcortex (Von Bonin and Green, 1949; Nauta, 1960; Mesulamand Mufson, 1985). It has also been reported that the PCpossesses projections connecting directly with the OFC(Potter and Nauta, 1979; Price et al., 1991). A further char-acteristic of the olfactory system is that it has a very richnetwork of centrifugal fibres leading from the PC, the ante-rior olfactory nucleus, the amygdala, the lateral entorhinalcortex, the hypothalamus, the locus coeruleus and the raphe

Figure 1 Schema illustrating the major efferent connections of the main olfactory system, and axial and sagittal sections from an anatomically normalizedstandard brain showing areas of olfactory projection. ACo nucleus, anterior cortical amygdaloid nucleus; Amy, amygdala; AON, anterior olfactory nucleus;hippoc, hippocampus, OFC, orbitofrontal cortex; PC, piriform cortex; Thal, thalamus; x, coordinate in mm along the horizontal line perpendicular to theintercommissural plane; z, coordinate in mm along the vertical line passing through the intercommissural plane (adapted from McLean and Shipley, 1992).

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nuclei to the olfactory bulb (Shipley et al., 1995). Thesefibres enable the brain to control the incoming flow of olfac-tory signals.

The OFC is heterogeneous and contains several distinctregions that deserve to be described because most cerebralimaging studies systematically activated them (Zald andKim, 1996a,b; Öngür and Price, 2000; Petrides and Pandya,2002). Briefly, this description is based on a brain mappingsystem initially proposed by Brodmann (1909), whoparcelled the cerebral hemisphere into more than 50 areas(Brodmann’s area, BA). Cerebral imaging studies often referto these numbered areas to indicate activated areas. Nowa-days, the OFC is considered to be a region of cytoarchitec-tural transition between the agranular and granular corticesof the frontal lobe. Carmichael and Price (1994) proposed adetailed parcellation system to take into account thesecytoarchitectural transitions. Very succinctly, the olfactoryareas in humans were reported as being the anterior andposterior BA 11 areas corresponding to Walker’s areas 11and 13 respectively, described in the monkey (Walker, 1940).The BA 47 area, just lateral to the BA 11 and also implicatedin olfactory processes, was reported to correspond toWalker’s area 12.

Methods of cerebral imaging

Non-invasive functional neuroimaging methods arecommonly classified into two broad groups: electro-magnetic techniques, such as electro-encephalography(EEG), event-related potential (ERP) and magneto-enceph-alography (MEG); and haemodynamic techniques, such aspositron emission tomography (PET) and functionalmagnetic resonance imaging (fMRI).

Electromagnetic techniques

In the field of olfaction, classical methods utilizing EEG andERP recordings in response to olfactory stimuli have been inuse since the 1960s (e.g. Allison and Goff, 1967; Smith et al.,1971; Kobal, 1982; Lorig et al., 1988; Kobal and Hummel,1991a,b; Kobal et al., 1992; Hummel et al., 1995; Pause etal., 1996; Castle et al., 2000). The MEG technique has beenin use since the 1990s (e.g. Kobal and Hummel, 1991b;Tonoike and Kaetsu, 1995; Kettenmann et al., 1996;Sakuma et al., 1997; Kobal and Kettenmann, 2000; Hamadaand Yamaguch, 2001). Electromagnetic techniques haveexcellent temporal resolution (a few milliseconds), but poorspatial resolution (several centimetres). Furthermore,although the magnetic techniques convey information aboutslightly deeper brain structures with less distortion thanusing scalp techniques, electromagnetic methods are mainlydesigned for recording superficial brain activity and aretherefore unsuitable for recording small olfactory areaslocated deep in the brain. This limitation explains the smallnumber of studies devoted to olfaction based on such tech-niques. Another special electrophysiological method is thestereo-EEG (SEEG) technique that consists in recording

intracerebral EEG and ERP activities in epileptic patientsusing deep electrodes prior to surgical treatment for relief ofintractable seizures. Since activity in olfactory areas canthen be directly recorded in deep cerebral structures, thismethod is more suitable for our purposes than the previousones, but only two studies have been performed to date(Hudry et al., 2001, 2003).

Haemodynamic techniques

In addition to the last method described above, haemody-namic techniques of cerebral imaging such as PET andfMRI are quite suitable for studying olfactory informationprocessing. These techniques allow investigation of theneural activity and metabolism by measuring changes in theregional cerebral blood flow (rCBF) (Cabeza and Nyberg,2000). rCBF is a good indicator of neural activity, but theresolution of haemodynamic measurements is limited bothtemporally and spatially. Temporal resolution is limited bythe ‘sluggishness’ of the haemodynamic response: althougha neural event lasts a few milliseconds, the rCBF can last for10 s. In addition, whereas PET cameras possess a relativelygood mapping resolution (5 mm), spatial resolution islimited by smoothing applied to the data to improve thesignal-to-noise ratio (from 10 to 20 mm). Finally, PET doesnot usually allow an adequate signal to noise ratio to beobtained in <1 min, although Silbersweig et al. (1993)demonstrated detection of PET responses in only 30 s. Tostudy cognitive processes, the radioactive tracer H2

15O,which has a half-life of 2 min, is commonly used. Its shorthalf-life allows the planning of several experimental condi-tions in a single session, commonly up to 12 scans of 60 seach.

fMRI measures rCBF changes through changes in bloodoxygenation. When a cerebral region is activated, theconcentration of oxyhaemoglobin increases, while that ofdeoxyhaemoglobin decreases. Deoxyhaemoglobin containsuncoupled electrons responsible for magnetic interactionsthat do not exist in oxyhaemoglobin, causing a dephasing ofthe spins in the brain voxel. During activation, spindephasing is slower and signal intensity is enhanced (a fewpercent) on a T2*-weighted image. This effect is called the‘blood oxygenation level dependent (BOLD) contrast’(Ogawa et al., 1990). The temporal resolution of fMRI islimited by the intrinsic time constant of the haemodynamicresponse, although images can commonly be acquired in 100ms. Although epoch designs from 30 to 60 s (Yousem et al.,1997; Sobel et al., 1998b; Royet et al., 2003) are commonlyused in olfaction, event-related designs may also be used(Gottfried et al., 2002a,b; Anderson et al., 2003; Gottfriedand Dolan, 2003).

Relative to PET scanning, fMRI presents several advan-tages. It is non-invasive and less expensive because it doesnot need an infrastructure with a radionuclide-producingcyclotron with its intendant specialized medical and para-medical personnel. fMRI provides both structural and func-

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tional information and enables event-related paradigms.Subjects can be scanned several times allowing single-subjectanalyses not easily conceivable using PET. Lastly, it isquicker to perform, and more commonly available.However, fMRI also has its disadvantages. It is very noisyand is more sensitive to both motion and susceptibility arte-facts especially in the vicinity of air–tissue interfaces (Frahmet al., 1988). Because these artefacts are located in the olfac-tory regions, several methods have been developed to alle-viate them (e.g. Liu et al., 1993; Yang et al., 1997; Zald andPardo, 2000; Wilson et al., 2002). However, these techniqueshave had varying degrees of success, and at best have shownonly moderate signal quality in the ventromedial prefrontalcortex.

To reveal activation patterns the analysis techniquescommonly applied in PET and block-design fMRI areprimarily based on the principle of the subtraction ofimages; for example, subtracting images obtained in thebaseline condition from those acquired when the subjectperforms a cognitive task. Before performing analyses,several pre-treatment steps are performed on each subjectdata set including realignment, stereotactic normalization,and smoothing. Group statistical analyses based on theGeneralized Linear Model are then performed (Friston etal., 1995a,b). The specific location of the activated regions isoften expressed in the form of three-dimensional coordi-nates as defined in the atlas published by Talairach andTournoux (1988). Other more recent atlases are, however,available to identify activation regions (Duvernoy, 1991;Mai et al., 1997).

Statistical maps of the whole brain are exploratory and areused when no a priori hypothesis has been made concerningthe neural network involved. It is possible to limit analysis tosmall anatomical regions of interest (ROI) such as theamygdala or the PC (Zald and Pardo, 1997; Royet et al.,2000, 2001; Kareken et al., 2001; O’Doherty et al., 2001;Gottfried et al., 2002a,b). The analysis of these ROI is moresensitive than maps from a statistical viewpoint, and notablyovercomes the problem of variability in location and sizeacross subjects, but can more easily give false positiveresponses. Statistical maps and ROI are most often used as acomplement to other methods of data acquisition.

The orbitofrontal cortex

The first noteworthy study using the bolus H2O technique tomeasure rCBF during PET scans in healthy subjects wasdescribed by Zatorre et al. (1992). They found that the twomost significant foci were located at the junction of thetemporal and inferior frontal lobes in both hemispheres,corresponding to the PC. The third focus was located in theright OFC (corresponding roughly to BA 11), and the fourthone in the left inferior medial frontal lobe (BA 25). Theysuggested that ‘the asymmetric activity in OFC is related to

more complex analyses of stimulus properties that preferen-tially recruit right hemisphere mechanisms’.

Activation in the right OFC (or more activation in theright than left OFC) was corroborated in most subsequentstudies using both PET and fMRI techniques (Koizuka etal., 1994; Levy et al., 1997, 1998; Small et al., 1997; Sobel etal., 1997, 1998a, 2000b;Yang et al., 1997; Yousem et al.,1997, 1999; Fulbright et al., 1998; Francis et al., 1999;O’Doherty et al., 2000; Savic and Gulyas, 2000; Zatorre etal., 2000). Such a consensus in results is striking, and isconsistent with most of the data found in behaviouralstudies in healthy subjects and lobectomized patients(Toulouse and Vaschide, 1900; Rausch et al., 1977;Abraham and Mathai, 1983; Zucco and Tressoldi, 1988;Cain and Gent, 1991; Zatorre and Jones-Gotman, 1991,2000; Jones-Gotman and Zatorre, 1993; Kobal et al., 2000;Bratko and Barušic, 2002). It was additionally observed thatthe right OFC was activated independently of the stimulatedside, although the right OFC rCBF was higher during rightnostril stimulations (Savic and Gulyas, 2000; Zatorre et al.,2000). Savic and Gulyas (2000) concluded that ‘odours seemto be processed both ipsi- and controlaterally, with a righthemisphere preponderance irrespective of the stimulatednostril’. Rather than BA 11, it appears that the most likelylocation for the observed activation is a more posteriorregion (within area 13), strongly connected with the PC andamygdala (Zald and Pardo, 2000; Zatorre and Jones-Gotman, 2000). This cytoarchitecturally distinct area is notdescribed in the Talairach and Tournoux atlas, but appearsto be structurally homologous to Walker’s area 13 in themonkey (Walker, 1940) and has been identified as an olfac-tory area in humans by Beck (1949) and Petrides andPandya (1994). If any, such an asymmetry of olfactoryprocesses found in humans can be related to structural,morphological and neurochemical asymmetry previouslyevidenced in olfactory structures in animals (Prasadao Raoand Finger, 1984; Heine and Galaburda, 1986; Dluzen andKreutzberg, 1996; Rodriguez-Gomez et al., 2000). Further-more, it is not unique because lateral asymmetries in percep-tion of complex stimuli have also been reported in theauditory, visual and somesthetic modalities (Bryden andBulman-Fleming, 1994). While a left-hemispheric domi-nance is commonly observed for language function, stimulisuch as musical sounds, faces or visuospatial materialrequire processing mechanisms mainly involving the righthemisphere (McKeever and Hulling, 1971; Rizzolatti et al.,1971; Zatorre, 1979).

Zald and Pardo (1997) reported the first noteworthyexception to the strong asymmetry described above. Meas-uring rCBF with PET when exposing healthy subjects tohighly aversive olfactory stimuli (i.e. dimethyl sulphide,ethanethiol, methanethiol), they observed strong rCBFincreases in the left OFC, but also in both amygdalae. Thisresult was the second outstanding finding in olfactory neuro-imagery.

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Parallel and hierarchical processing of odours

In the first studies using cerebral imaging, odours werepassively presented to subjects. In addition, some authorsselected odorants considered to be the most neutral, difficultto name, unfamiliar, and similar in intensity ratings (Zatorreet al., 1992; Savic et al., 2000). It has however been empha-sized that ‘The presence of a “passive” task in an activationparadigm ignores the nature of the cognitive components ofsuch a task and therefore obscures the interpretation of anyobserved between-task differences in brain activity’(Démonet et al., 1993). From concepts deduced from cogni-tive psychology (Craik and Lockhart, 1972; Craik andTulving, 1975; Kosslyn and Koenig, 1992), we suggested theuse of various olfactory tasks to study different odourprocessings (Royet et al., 1999, 2001). Cognitive studies haveshown that sensory stimuli can be analysed at differentlevels, ranging from simple sensory analysis to deep orsemantic analysis. In his review of the literature on odourmemory, Schab (1991) suggested that the process of olfac-tory identification varies ‘in informational specificity frompleasantness and familiarity judgements to single-label,object-name identification, with various intermediate steps’.We further assumed that the detection task requires a super-ficial judgement not involving stored representations ofodours, that perceptual and semantic odour representationsare stored in separate neural subsystems, and that edibilityjudgements can involve the activation of semantic odourrepresentations. We have thus shown that superficialprocessing of odour detection induced only a weak rCBFincrease in the right OFC of healthy subjects, whereas thefamiliarity task, requiring perceptual processing, showedmore activity in this area. In contrast, activity was signifi-cantly higher in the left OFC during the hedonicity judge-ment task.

Furthermore, we have shown that high-level odourprocessing, namely the edibility and familiarity judgementtasks, involves the left inferior frontal gyrus (BA 47) forsemantic associations (Royet et al., 1999). Given that boththese judgements are strongly correlated with naming, weconcluded that activation of this area is also likely to reflectnaming. This interpretation has been corroborated by morerecent studies showing activation of this area to be correl-ated with familiarity ratings (Savic and Berglund, 2004), andduring odour identification (Kareken et al., 2003). Our workhas further revealed the involvement of the visual cortexwhen subjects performed edibility judgements (Royet et al.,1999, 2001). Activation of visual areas has also been foundby other authors (Qureshy et al., 2000; Suzuki et al., 2001;Gottfried, personal communication). Given the well-knowndifficulty of verbalizing and identifying odours, we claimedthat visual areas might participate in the semanticprocessing of odours, in the sense that subjects might visu-alize the object evoked by the odour and determine, forexample, if the odour evokes an edible item.

From our cerebral imaging data, we suggested that odourprocessing comprises both a serial processing of informationfrom the primary to secondary olfactory cortices, and aparallel, distributed processing depending on the nature ofthe cognitive operations being performed (Royet et al., 1999,2001). The pattern of activation in the left and right OFCsvaried respectively depending on whether the odourprocessing was related to emotional response (hedonicityjudgement) or recognition memory (familiarity judgement).

Other cerebral imaging studies have been based on the useof active tasks such as detection, discrimination, recognitionmemory and identification (Dade et al., 1998, 2002; Qureshyet al., 2000; Savic et al., 2000; Zatorre et al., 2000; Karekenet al., 2001; Suzuki et al., 2001). In many of the aforemen-tioned studies, several structures have also been found to beactivated in addition to the OFC, such as the amygdala,hypothalamus, entorhinal, cingulate gyrus, thalamus, insulaand cerebellum. On the basis of the different olfactory tasks,Savic et al. (2000) thus showed that odour perception acti-vates complex neural networks which include all these struc-tures, but in a variable way depending on the task. Forexample, they showed a significantly higher activity in thelateral OFC, frontal operculum and brainstem during odourquality discrimination and memory than during singleodour exposition and intensity discrimination, whereas allfour tasks activated structures in the olfactory cortex andmore closely related structures. They further showed ahigher activity in the right temporal neocortex and rightparietal cortex during odour memory than in odour qualitydiscrimination. From these findings, Ivanka Savic and hercolleagues suggested that olfactory functions are organizedin both a parallel and hierarchical manner, depending on thecharacter and complexity of the task

A lateralized and extensive emotional circuit

In their pioneer study, Zald and Pardo (1997) demonstratedthat exposure to a highly aversive odorant produced strongrCBF increases in the left OFC and both amygdalae,whereas exposure to less aversive odorants produced rCBFincreases only in the left OFC. Furthermore, the activitywithin the left amygdala was significantly correlated withsubjective ratings of perceived aversiveness, but not withperceived intensity. In a subsequent noteworthy work,applying covariance analyses to their previously acquiredPET data, Zald et al. (1998a) estimated the functionalconnectivity between the amygdala and OFC in both hemi-spheres. They found a significant correlation between rCBFincreases in the left amygdala and OFC in response to aver-sive odorants relative to when attempting only detection ofan odour. Only the left OFC and amygdala operated inunison when exposed to an unpleasant odorant. The authorsinterestingly added that ‘if functional coupling reflects anactive process that facilitates the interaction or communica-tion between regions, functional uncoupling may optimiseneurocognitive functioning by isolating the processing in

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different regions’. These findings stressed for the first timethe dynamic nature of connectivity between the amygdalaeand OFCs in olfaction.

In a more recent work, we examined the neural correlatesof responses to emotionally valenced olfactory, visual andauditory stimuli using PET and found an extensiveemotional network (Royet et al., 2000). For all three sensorymodalities, emotionally valenced stimuli led to increasedrCBF in the OFC, temporal pole and superior frontal gyrusin the left hemisphere. These findings suggested thatpleasant and unpleasant emotional judgements call upon thesame core network in the left hemisphere regardless of thesensory modality. This core network was, however, acti-vated in addition to a number of circuits specific to indi-vidual sensory modalities. Emotionally valenced olfactoryand visual, but not auditory stimuli thus produced addi-tional rCBF increases in the hypothalamus and the subcal-losal gyrus. Only emotionally valenced olfactory stimuliinduced activation in the left amygdala, suggesting that suchstimuli are more potent activators of the amygdala thanvisual and auditory stimuli.

A major result found in the three PET studies describedabove was the strong involvement of the left hemisphere inemotional processes. This finding was consistent with datafound in other PET or fMRI studies of chemical senses(Zald et al., 1998b; Royet et al., 2001, 2003; Gottfried et al.,2002a; Anderson et al., 2003), but also with other types ofemotional processing such as the subjective experience ofanger, dysphoria and obsessive-compulsive symptoms(Drevets et al., 1992; Pardo et al., 1993; Rauch et al., 1994;Morris et al., 1996, 1998; Dougherty et al., 1999). Interest-ingly, hemispheric lateralization of olfactory-mediatedaffective processes is not restricted to human beings and hasalso been observed in rats. Left bulbectomized rats areimpaired in their response to emotionally negative socialodours (Dantzer et al., 1990). Such a lateralization has,however, never been reported by Rolls and his team in theirnumerous electrophysiological studies on the functions ofthe OFC in monkey (for review, see Rolls, 2004). Overall,this data indicates that left hemisphere structures play amore prominent role in emotional processing than could beexplained by traditional accounts of the lateralization ofemotions. It is indeed noteworthy that studies based onbehavioural, lesion and electrophysical precepts have attrib-uted a decisive role to the right hemisphere in emotion(Ahren and Schwartz, 1985; Gainotti, 1989; Jones and Fox,1992; Wittling and Roschmann, 1993). This does not appeartrue when performing cerebral imaging studies. On the onehand, the previous works on behavioural, lesion and electro-physiological data were not devoted to the study of olfactoryprocesses, and it is possible that the present results reflect aspecific aspect of olfactory function. On the other hand, it isconceivable that methodological bias in neuroimaging couldalso explain the present data.

When a neural network implicated in an emotionalresponse to odours is located in the left hemisphere, then thestructures pertaining to this network do indubitably play aslightly different role. In a recent fMRI study, we demon-strated that actively performing the hedonicity judgementtask for pleasant and unpleasant odorants compared topassively smelling these same odorants specifically inducedmore activation in the left OFC (Royet et al., 2003). Itfollows that this area is implicated in the conscious assess-ment of the emotional quality of odours and that the OFCactivation in Zald and Pardo (1997) subjects, who passivelydetected mildly aversive or pleasant odorants, was probablyevoked by spontaneous hedonicity judgements. In contrast,the piriform–amygdala region did not appear to participatein conscious evaluation but was activated in relation to theemotional intensity (faculty to cause arousal) of the odours.Several recent distinct findings in relation to the primaryolfactory cortex and the amygdala however deserve a moredetailed presentation.

The primary olfactory cortex and the amygdala

Although activation of the PC has been found in severalstudies in humans (Zatorre et al., 1992; Small et al., 1997;Sobel et al., 1998a, 2000b; O’Doherty et al., 2000; Savic etal., 2000; Kareken et al., 2001, 2003), several subsequentstudies reported either no piriform activity (Yousem et al.,1997; Zald and Pardo, 1997; Dade et al., 1998, 2002;Fulbright et al., 1998; Royet et al., 1999, 2000, 2001; Zatorreet al., 2000; Suzuki et al., 2001), showed only inconsistentactivation (Sobel et al., 1998a; Yousem et al., 1999) or asso-ciated these activations with sniffing (Sobel et al., 1998a).These discrepancies were partly explained by the findingthat odorants induce sharp increases in PC activation whichthen rapidly habituates despite continued odorant presenta-tion and detection (Sobel et al., 2000b; Poellinger et al.2001). Since in previous fMRI studies the odorants werepresented for a relatively long time, habituation limitedresponses in the PC. Despite this phenomenon, differentroles were attributed to the piriform–amygdala region. Wewill successively examine the various propositions.

A memory and familiarity judgement processor?

Dade et al. (1998, 2002) examined human brain functionusing PET during different stages of olfactory memoryprocessing: (i) encoding of new odours; (ii) recognition ofodours after a short interval and (iii) recognition of odoursafter a long interval (24 h). They did not find PC activationin the encoding condition, but found a weak bilateralactivity in the short-term recognition condition, and strongbilateral activity in the long-term recognition condition.They added that these findings were in agreement with thetheory developed in several studies (Haberly and Bower,1989; Bower, 1991; Hasselmo and Barkai, 1995), ‘whichsuggests that the primary olfactory cortex serves as a type ofassociative memory system, which allows for the association

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of odour stimuli with memory traces of previously experi-enced events’. Several findings lend support to the theorythat the PC is involved in learning and memory. Forexample, long-term synaptic potentiation was shown tooccur in the rat PC in vitro (e.g. Jung et al., 1990) and in vivoat the conclusion of learning (Roman et al., 1993; Litaudonet al., 1997b). The finding that PC activity changes in ratsafter odour learning may explain the greater piriform activa-tion during recognition than in encoding. In Dade’s study,the greater piriform activity during long-term recognitioncould reflect increases related to memory consolidationprocesses.

It is well established that recognition of a repeated stim-ulus may depend on two different forms of memory pro-cesses (Mandler, 1980; Lehrner et al., 1999; Bogacz et al.,2001). According to the ‘dual process theory’, these formsare called ‘familiarity’, which is based on perceptualprocessing, and ‘recollection’, which includes the retrieval ofcontextual information. Familiarity judgements are madeon the basis of a feeling, without specific information aboutthe encoding episode, and thus relate to implicit or uncon-scious memory. In other terms, familiarity ratings to a largeextent reflect the clarity of perceptual processing (Broman etal., 2001). Recollection is seen as a form of an elaborate orconceptually driven process, and thus relates to explicit orconscious memory. Since a familiarity judgement task isthus clearly associated with a memory recognition task, itwas surprising that we did not observe any activation in thePC in our previous PET studies. In a recent fMRI study(Plailly et al., 2003), we were, however, able to show that theodour familiarity judgement task also specifically activatedprimary olfactory areas such as the right PC.

We further showed activation of the PC only in the righthemisphere. Although Dade et al. (2002) reported bilateralactivation of the PC, careful examination of their data indi-cated a more substantial activation in the right than left PCand showed that the extent of this spread in the right OFCwas fairly wide. Findings with brain-damaged patients areconvergent with these data. For instance, findings on therecognition of abstract visuospatial designs in unilateraltemporal lobe epilepsy patients indicated that left-lesionedpatients give more ‘known’ (familiarity process) than‘remembered’ (recollection process) responses, whereasright-lesioned patients depict the opposite pattern (Blaxtonand Theodore, 1997). Lastly, it has been demonstrated thatthe right prefrontal cortex is specialized for familiarity-based traces, whereas the left prefrontal cortex is specializedfor recollective memories (Kensinger et al., 2003).

A hedonic intensity and arousal processor?

In a recent fMRI work, we examined those networks sepa-rately activated by pleasant and unpleasant odours whilesubjects rated their degree of pleasantness or unpleasantnessby using the ‘finger-span’ technique (Royet et al., 2003).Subjective intensities of odorants perceived by subjects were

checked and found to be identical between pleasant andunpleasant conditions. When we subtracted imagesobtained in the pleasant condition from those obtained inthe unpleasant condition, we mainly observed activation ofthe left amygdala–piriform region and ventral insula. Noactivation was observed with the ‘pleasant–unpleasant’contrast. Electrodermal and plethysmography responseswere also recorded to control for covert physiological mani-festations of the emotional response. We demonstrated thatsubjective hedonic perception (rating of degree of pleasant-ness or unpleasantness) was stronger with unpleasant thanpleasant odours and that individual subject variations inelectrodermal amplitudes were correlated with finger-spanratings. Unpleasant odours therefore induced strongeremotional responses than did pleasant stimuli, independ-ently of perceived subjective intensity. Other concomitantdata have consistently shown that the BOLD signal in boththe amygdala (Anderson et al., 2003) and the PC (Rolls etal., 2003) is related to odour intensity, but not to odourvalence. Interestingly, a similar dissociation of the neuralrepresentation of intensity and affective valuations wasfound in gustation (Small et al., 2003; see also the preview byAnderson and Sobel, 2003). We have emphasized that, tomanipulate odour valence, Anderson et al. (2003) hadselected an intensity range that provided rather neutralodours and that their data then suffered from a restriction ofaffective range (Royet et al., 2003). In our study, the odoursselected to be at the extremes of unpleasantness were there-fore perceived as more intense and were more likely to evokea much stronger emotional reaction than the pleasantodours (Royet et al., 2003). Although we agree withAnderson’s results that amygdala activation is independentof valence, the first point to be underlined is that thestrength of the emotional response, i.e. emotional intensity(even more specific with unpleasant odours), is determinantfor activation of the amygdala. The second point to beemphasized is the preferential involvement of the leftamygdala in the negative emotional processing of olfactorystimuli. This result is consistent with previous findings (Zaldand Pardo, 1997; Zald et al., 1998b) and has also recentlybeen reported by Gottfried et al. (2002a). Specificallyconsidering the PC, these same authors found bilateral acti-vation elicited for all odours regardless of valence. It is alsoworth noting that in the visual domain, the responses of theamygdala to unpleasant stimuli are almost always left later-alized (e.g. Morris et al., 1996; Lane et al., 1997; Phillips etal., 1998; Taylor et al., 1998; Whalen et al., 1998; Pessoa etal., 2002). We explained the activation of the piriform–amygdala region observed for strongly emotional, so rathernegative, stimuli in our study from the level of arousal thatthey induced. ‘Arousal refers to the extent to which stimuliare calming (low arousal) or activating (high arousal) andthis dimension has been described as being orthogonal to thevalence dimension’ (Zald, 2003). Preferential activation ofthe amygdala in response to negatively valenced stimuli

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further appears to be a general principle, since it is observedfar more consistently than activations induced by positivelyvalenced stimuli (Breiter et al., 1996; Hamann, 2003).

Functional heterogeneity within the PC and the amygdala

Attribution of a distinct function to the right and left PC andamygdala is made more complex by the fact that these struc-tures are subdivided from an anatomical point of view, andtherefore can also subtend different functions. Lateraliza-tion of olfactory processes could then involve only one partof these structures. In animals, a functional dissociationbetween the anterior and posterior parts of the PC has beenshown by anatomical as well as optical and electrophysio-logical recording studies (Litaudon et al., 1997a,b; Mouly etal., 1998; Chabaud et al., 2000; Haberly, 2001). Notwith-standing the ‘sniffing versus smelling’ dichotomy evidencedby Sobel et al. (1998a), Gottfried et al. (2002a) were the firstauthors to show functional heterogeneity within the PC inhumans. They showed that the posterior PC mediates basicodour perception (so neutral odour) and detection. In thisregard, the posterior PC activations described in their studywere situated close to those identified in previous imagingexperiments using passive smelling (e.g. Zatorre et al., 1992;Savic et al., 2000; Sobel et al., 2000b; Poellinger et al., 2001).In contrast, they found that the anterior segment of the PCis receptive to hedonic quality, especially at extremes ofodour valence. They also noted a difference in temporalprocessing according to whether odours were pleasant orunpleasant.

Although Anderson et al. (2003) found that the amygdalaresponse is not specifically related to the dimensions of thepositive and negative valences of olfactory experience, theamygdala comprises several subnuclei, and thus a ‘collapse’across these subdivisions could have blurred the segregationof pleasantness coding. To guard against this possibility,they tested this, but did not find any functional hetero-geneity within the amygdala for hedonic valence. The wholeamygdala response profile appeared characteristic of smallersubdivisions. Functional segregation of the posterioramygdala was found by Gottfried et al. (2002b) with appeti-tive, but not aversive olfactory learning. As noted by theauthors, these findings were intriguing and the reversepattern of results could have been predicted. Gottfried et al.(2002b) suggested that the use of unpleasant odours couldcause insufficient arousal to engage amygdala-dependentconditioning and/or that the reactions of disgust provokedby unpleasant odorants could activate the amygdala onlypoorly. These hypotheses, however, appear inconsistentwith findings described in previous sections and data from arecent study in which disgusting odours induced strong acti-vation in the amygdala (Wicker et al., 2003).

Regarding functional heterogeneity within the PC andamygdala, too little data has been published to be able todraw conclusions. The proximity of areas such as the PC andamygdala, and a fortiori of subregions of these areas, can in

addition lead to the misinterpretation of activation patterns.The question is indeed whether the fMRI technique canallow the functional dissociation of small adjacent regions.To date, it seems that the event-related fMRI techniqueassociated with analyses of small ROIs enables the examina-tion of such subregions of the PC and amygdala. Recordingof intracerebral EEG activity in these structures could alsobe an alternative method adapted to evoking responses. Ifsubtle differences in function are implied in subregions ofthe PC and amygdala, it is likely that new investigations willsoon allow us to elucidate their specific role.

Conclusions

Zatorre et al. (2000) claimed that ‘data suggest a need torevise the traditional view of PC as a simple sensory relay ina hierarchy’. However, neurophysiologists have long sinceestablished that the primary olfactory cortex is a cortexinvolved in highly integrated processes (see Haberly, 2001,for review). Cells in the PC do not respond to only olfactoryinput, but also fire vigorously in relation to the non-olfac-tory components of an odour discrimination task (Schoen-baum and Eichenbaum, 1995). The findings described abovefurther subtend this assertion, and prove that the primaryolfactory cortex in humans also participates in high levels ofprocessing. It appears that the primary olfactory cortex hasseveral roles and that these different functions can probablybe ascribed to different subregions. With improvement incerebral imaging techniques, it is likely that we may soon beable to distinguish activation patterns in substructures ofthis cortex such as the anterior olfactory nucleus, olfactorytubercle, frontal and temporal parts of the PC and the diag-onal band nucleus as already shown by Sobel et al. (2000b).In summary, it was found that both odorants and sniffingactivate the PC. This double function is coherent given that‘sniffs may be regarded as the attentional spotlight of olfac-tion’ (Sobel et al., 2000b). In addition to this ‘zoom lens’function, the PC further appears to participate in memoryprocesses such as long-term recognition memory (Dade etal., 2002) and familiarity judgement (Plailly et al., 2003) andto the evaluation of hedonic intensity (Gottfried et al.,2002a; Royet et al., 2003). Furthermore, these processesseem lateralized with the preferential involvement of theright PC in memory processes and the left PC in hedonicintensity. The hedonic aspect (quality) further appears to beprocessed in the anterior part of PC, whereas odour detec-tion seems to be processed in the posterior part (Gottfried etal., 2002a).

Lateralization of odour processing

Several theories have been proposed regarding the hemi-spheric asymmetry of cerebral processing. The HERAmodel, for instance, suggests that the left prefrontal corticalregions are more involved during the learning of newmaterial (encoding), whereas the right prefrontal corticalregions are supposed to be more involved during subsequent

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Lateralization of Olfactory Processes 739

recall or recognition (retrieval) (Tulving et al., 1994; Habibet al., 2003). However, the relevant anatomical regionswithin the extensive prefrontal cortex were not specified. Ithas been hypothesised that the right hemisphere is better at‘holistic’ or ‘global’ processing, and the left hemisphere at‘local’ processing (Fink et al., 1999). Regarding left–rightlateralization of the amygdala activity, other hypotheseshave been suggested such as unconscious versus consciousprocessing of stimuli (Morris et al., 1998), innate versusconditioned fearful stimuli (Dolan and Morris, 2000), andcognitively learned fear versus experimentally learned fear(Phelps et al., 2001), respectively.

Findings reported in the field of olfaction demonstratethat basic perceptual processes appear lateralized betweenthe hemispheres, not only at the level of the OFCs, but alsoin primary olfactory regions including the PC andamygdala. It appears that the right hemisphere participatesin the process of recognition memory, whereas the left hemi-sphere participates in the emotional processing of odours.First, these distinctions probably reflect more functionalasymmetries than fully fledged dissociations. Second, sincethese two processes are closely related and difficult to disso-ciate, most studies simultaneously observe activationpatterns in both hemispheres. Consistent with this, andalthough evidence suggests that each hemisphere can func-tion independently (Gordon and Sperry, 1969), it is theinteraction of the two that allows for optimal performancein more complex olfactory processing. The specificity ofeach hemisphere is all the more difficult to show as theairflow periodically reverses between both nostrils(Hasegawa and Kern, 1977) causing a slightly differentimage of the olfactory world to be conveyed to the brain(Sobel et al., 2000a), and that gender and handedness mayalso interact with hemispheric lateralization (Royet et al.,2003).

Several studies indicate that the right hemisphere isinvolved in the processing of pleasant odours. For instance,Zatorre et al. (2000) studying neural mechanisms involved inodour pleasantness and intensity judgements, demonstratedactivation in the right OFC only. The lack of activation inthe left OFC could, however, be explained by the use ofmoderately familiar odours. Intensity, hedonicity and famil-iarity have indeed been reported to be closely related, andless familiar odorants are rated as rather neutral and notintense (Distel et al., 1999; Royet et al., 1999). With theexception of pyridine, the odorants used in Zatorre’s studywere not very intense and, since activation was summed on60 s, the unpleasant dimension could then be eclipsed to thedetriment of the pleasant dimension. Anderson et al. (2003)corroborated that activation in the left OFC showed greaterresponsiveness to unpleasant than pleasant odours, but alsoclaimed that activation in the right medial OFC was greaterfor pleasant than unpleasant odours, regardless of intensity.The preferential activation of the right caudolateral OFCwas subsequently replicated with pleasant tastes (Small et

al., 2003). Activation of the right PC with pleasant odourswas also reported by Gottfried et al. (2002b). Recent behav-ioural studies have finally indicated that subjects stimulatedthrough the right nostril provided higher hedonic scoresthan those stimulated through the left nostril (Herz et al.,1999; Dijksterhuis et al., 2002) but it appears that theauthors used rather neutral or pleasant odours. Briefly, fromthese data, we suggest that the right hemisphere is activatedby pleasant odours because these are less emotionallyarousing, and that cerebral processing of the familiarityrating is then engaged or prominent. This hypothesis couldbe tested by performing a comparative cerebral imagingstudy, in which subjects judge either hedonicity or famili-arity of the same set of odours selected a priori as beingrather neutral or pleasant. We suppose that activationpatterns would be more lateralized in the right hemispherefor the familiarity than hedonicity judgement task.

The dichotomy of unpleasant versus pleasant emotionalresponses for odorous stimuli is not associated with therespective functions of left and right olfactory systems as hasbeen suggested in several studies. Whereas the specializationof the left hemisphere for higher cognitive processes such aslanguage is indubitably well established (Gazzaniga, 2000),it appears that the basic perceptual processing of odours isalso lateralized between the hemispheres, with hedonicjudgements (and emotional intensity) and familiarity judge-ments being lateralized in the left and right hemispheresrespectively. Objections have been raised that the widenetwork activated in the left hemisphere for processingolfactory emotions (Royet et al., 2000) may be partly due tothe influence of semantic processing. This viewpoint issupported if we refer to the OFC and superior frontal gyrus,but such an explanation cannot be corroborated by dataconcerning activation in the PC/amygdala, temporal poleand insula. Furthermore, it would be surprising that top-down semantic processes activate a wide neural network inthe left hemisphere after stimulation only with emotionalodours. Even when odours are presented passively and arenot emotional, subjects are probably performing an implicittask of semantic processing. Interestingly, Zald (2003) alsobrilliantly pointed out the problem of emotional lateraliza-tion in a wider context by stressing that the neuroimagingdata on the amygdala fails to support traditional modelsgenerally deduced from lesion data. He emphasized that roleof the right amygdala was probably more important to thesuccessful recognition of facial emotion. In other words, itappears that the right amygdala is more involved in recogni-tion than emotional processes.

It appears that lateralization of the olfactory systemhinges on three principles: one being based on ‘analytical’processing (semantic), the second and third based on the‘non-analytical’, basic perceptual processing, i.e. emotionaland familiarity processings. The left brain would participatenot only in analytical processing, but would also beprocessing the hedonic value of odours. The right brain

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would be ‘non-analytical’, ‘holistic’, and would process thefamiliarity of odours. Hedonic value as well as familiaritylevels are crucial, decisive determinants of odour identity. Aright-hemispheric advantage in processing odour familiarityand a left-hemispheric advantage in aversive or unpleasantodour processing enable a better and faster basic reaction ofthe ‘flight/fight/fear type’, because they can contribute toincreased survival from an evolutionary viewpoint. A famil-iarity processing is unaware of the details of a stimulus andinduces a feeling of ‘known’ before more semantic processingcan be performed. Similarly, ‘emotional processing takesplace irrespective of details of a stimulus, often beforedetailed properties can even be perceived or inferred’(Kunst-Wilson and Zajonc, 1980; Zajonc, 1980). The ‘aver-sive’ term includes toxic food odours, stress odours that canbe related to fear, odours of fire, dangerous fumes andpolluted environments and natural gas leaks. If, in all thesesituations, the aversive or unpleasant aspect induces anarousal reaction, it also involves a very rapid decision as towhether or not an odour is familiar. It thus appears thattemporal factor is a key component in hedonicity and famil-iarity judgements. It should be interesting to measureresponse times of subjects and take them into account inanalyses. Activation patterns associated with these dimen-sions could then be strengthened.

Conclusions

To date, cerebral imaging findings have shown that olfac-tory function involves a complex and extensive olfactoryneural network. Odour processing appears to be based ontwo main modes of processing, a serial processing withsuccessive involvement of the primary and secondary olfac-tory areas, and a parallel processing (right hemisphereversus left hemisphere) depending on the nature of thecognitive task. While areas located in the right hemispheresuch as the OFC and PC are more involved in memory andfamiliarity ratings, those located in the left hemisphere, suchas the OFC, insula, PC, amygdala, temporal pole and supe-rior frontal cortex, participate more in the emotionalresponse to odours. These different structures would,however, be involved at different levels of emotional olfac-tory processing. Whereas the piriform–amygdala regionappears to be associated with the evaluation of emotionalintensity and therefore more activated with unpleasant thanpleasant odours, the caudolateral OFC appears to mediate aconscious assessment of these odours. The role of the supe-rior frontal cortex would be to control one’s own emotionalstate in the making of personally relevant decisions.

In humans, our difficulty in verbalizing and/or identifyingodours is consistent with the Gestalt-nature (i.e. unitary) ofour olfactory perception, and the shortened olfactory input-to-cortex pathway of the olfactory system. Wilson andStevenson (2003) claim ‘that early analytical processing ofodors is inaccessible at the behavioral level and that all

odors are initially encoded as “objects” in the piriformcortex’, i.e. that odour percepts are synthetic. Familiarity/novelty and hedonicity perceptions can represent compo-nents of this holistic perception and their rapidity of execu-tion represents an unquestionable advantage for survival.The PC has been reported to involve a detector of novelty(Sobel et al., 2000b), and the familiarity-based signal may besimilar to that required for determining whether an object isnovel (Kensinger et al., 2003). The major finding reported inthe current review from neuroimaging studies is likely right–left lateralization of these processes. Although rarelydescribed in animal studies, this lateralization of perceptualprocesses appears highly consistent with data obtained fromcerebral imaging studies in fields of research other as olfac-tion. In order to formally test these hypotheses that are onlyderived from neuroimaging results, it would nevertheless beof further value to study patients with lateralized lesions inolfactory regions by testing them on specific judgementtasks

AcknowledgementsThe authors would like to thank Chemical Senses’s editorR. Hudson for suggesting this review on cerebral imaging. We arevery grateful to anonymous referees for constructive and pertinentcomments. We thank W. Lipski for correcting the English languageof the paper. This work was supported by the Centre National de laRecherche Scientifique (CNRS) and the Claude Bernard Univer-sity of Lyon.

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Accepted July 5, 2004

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Occupational Medicine 2004;54:000–000DOI: 10.1093/occmed/kqhXXX

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ANNEXE 4

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Neuron, Vol. 40, 655–664, October 30, 2003, Copyright 2003 by Cell Press

Both of Us Disgusted in My Insula:The Common Neural Basis ofSeeing and Feeling Disgust

leads to a propositional representation of the inferredstate of disgust. This representation then determinesour decision not to eat the food. Another interpretationof the phenomenon may be based on a “sensory motorresonance” hypothesis. Observing the facial expression

Bruno Wicker,1 Christian Keysers,2,3

Jane Plailly,4 Jean-Pierre Royet,4

Vittorio Gallese,2 and Giacomo Rizzolatti2,*1Institut de Neurosciences Physiologiques

et CognitivesCNRS of another person evokes a similar facial motor repre-

sentation in the observer (see Hess et al., 1999, for aChemin Joseph Aiguier13402 Marseille cedex 20 review). This motor representation (Lipps, 1907) and its

associated somatosensory consequences (Adolphs etFrance2 Physiology section al., 2000; Adolphs, 2001, 2002) might be sufficient to

understand the meaning of the other’s facial expression.Department for NeuroscienceUniversity of Parma Neither of these hypotheses predicts that the observer

shares the emotion of disgust with the observed individ-Via Volturno 3943100 Parma ual, in that they both—although in different ways—

assign a causal role to mechanisms not directly involvedItaly3 BCN Neuroimaging Center in the experience of emotions. We will refer to them

jointly as “cold hypotheses.” A third possibility is that,University GroningenAntonius Deusinglaan 2 in order to understand the facial expression of disgust

displayed by others, a feeling of disgust must occur also9713 AV GroningenThe Netherlands in the observer. This hypothesis predicts that brain areas

responsible for experiencing this emotion will become4 Laboratoire de Neurosciences etSystemes Sensoriels active during the observation of that emotion in others.

We will refer to this hypothesis as the “hot hypothesis.”UMR CNRS 5020Universite Claude-Bernard LYON 1 Gerland So far, there is only indirect evidence to support the

latter hypothesis. A number of investigations show that,50, Avenue Tony Garnier69007 Lyon cedex 07 among other structures, the insula and the amygdala

are activated when subjects are exposed to disgustingFranceodors or tastes (Royet et al., 2003; Small et al., 2003;Zald and Pardo, 2000; Zald et al., 1998a). Independently,a number of functional imaging studies (Phillips et al.,Summary1997, 1998; Sprengelmeyer et al., 1998; Schienle et al.,2002) and electrophysiological investigations (Krolak-What neural mechanism underlies the capacity to un-

derstand the emotions of others? Does this mecha- Salmon et al., 2003) have suggested that the insula isactivated during the observation of disgusted facial ex-nism involve brain areas normally involved in experi-

encing the same emotion? We performed an fMRI pressions. The aim of the present study will be to directlydetermine whether the same locations in the insula arestudy in which participants inhaled odorants produc-

ing a strong feeling of disgust. The same participants activated during the experience of disgust and the ob-servation of the facial expression of disgust in others.observed video clips showing the emotional facial ex-

pression of disgust. Observing such faces and feeling To this purpose, we performed an fMRI study com-posed of four functional runs. In the first and seconddisgust activated the same sites in the anterior insula

and to a lesser extent in the anterior cingulate cortex. (“visual runs”), participants passively viewed movies ofindividuals smelling the contents of a glass (disgusting,Thus, as observing hand actions activates the observ-

er’s motor representation of that action, observing an pleasant, or neutral) and expressing the facial expres-sions of the respective emotions. In the third and fourthemotion activates the neural representation of that

emotion. This finding provides a unifying mechanism (“olfactory runs”), the same participants inhaled dis-gusting or pleasant odorants through a mask placed onfor understanding the behaviors of others.their nose and mouth. Our core finding is that the anteriorinsula is activated both during the observation of dis-Introductiongusted facial expressions and during the emotion ofdisgust evoked by unpleasant odorants. This result indi-In a natural environment, food poisoning is a substantial

threat. When an individual sees a conspecific looking cates that, for disgust, there is a common substrate forfeeling an emotion and perceiving the same emotiondisgusted after tasting some food, he or she automati-

cally infers that the food is bad and should not be eaten. in others.What happens in the observer’s brain to keep him or

her from eating the potentially damaging food? Ac- Resultscording to a cognitive account, the processing of thefacial expression occurring in the visual cortical areas The experiment was carried out on 14 healthy right-

handed male subjects. As mentioned in the Introduction,all subjects took part in two visual and two olfactory*Correspondence: [email protected]

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the activated structures, two are of particular interestfor the present study: the amygdala and the insula (Fig-ure 2). Amygdala activations were present with bothdisgusting and pleasant odorants, with a clear overlapbetween the two types of activations (Figure 2A). Thefact that the amygdala is activated by both pleasant andunpleasant odorants is in accord with previous findings(Gottfried et al., 2002; Hudry et al., 2001; Anderson et al.,2003; Zald, 2003). In contrast, disgusting and pleasantodorants produced clearly separated activation foci inthe insula. Disgusting odorants activated the anteriorsector of the insula bilaterally, whereas pleasant odor-ants activated a more posterior site of only the rightinsula (Figure 2B).

Visual StimulationThe visual runs were analyzed using two contrasts: ob-servation of disgust – neutral and observation of plea-

Figure 1. Frames from Movies Used in the Visual Runssure – neutral. Both contrasts revealed significant BOLD

The demonstrators leaned forward to sniff at the content of a glasssignal changes in various locations (see Table 2). The(top two rows) and then retracted the torso and expressed a facialinsula in particular was only activated in the observationexpression of disgust (left) pleasure (center) or neutral (right column).of disgust – neutral contrast. Most importantly, clustersEach movie lasted 3 s. Six different demonstrators (three are shown

here) expressed the three types of facial expressions, leading to six of overlap were found between the observation of dis-variants of each expression. A vision-of-disgust block, for instance, gust – neutral and the disgusting odorant – rest contrastswas then composed of the six variants of the disgusted emotion (Figure 3 and Table 3). These clusters were located inseparated by 1 s pauses.

the left anterior insula and in the transition zone betweenthe insula and inferior frontal gyrus. A smaller overlapwas also observed in the anterior right cingulate cortex.

functional acquisition sessions. Visual runs containedThe amygdalae were not activated by the observation

three experimental conditions: “observation of disgust,”of disgusted facial expressions. This lack of amygdalar

“observation of pleasure,” and “neutral.” Each conditionactivation is in agreement with previous studies sug-

was composed of blocks of six movies showing individu-gesting a dissociation between the neural basis of the

als leaning forward to smell the content of a glass. De-recognition of fear, in which the amygdala is strongly

pending on the condition, the glass contained an unpleas-involved, and that of disgust, in which the amygdala

ant, pleasant, or neutral odorant, and the individuals in thedoes not appear to play a crucial role (Calder et al., 2001).

movie reacted accordingly with a disgusted, pleased, orTo test if the BOLD signal increases in these zones of

neutral facial expression (see Figure 1). Movies wereoverlap were selective for disgust, we performed direct

used instead of static facial expressions for three rea-comparisons between the disgusting odorants and

sons. First, under ecological conditions, facial expres-pleasant odorants conditions and between the observa-

sions are intrinsically dynamic stimuli. Second, emotionstion of disgust and the observation of pleasure condi-

are recognized better from movies compared to statictions within these regions of interest (see Table 3, last

displays (Wehrle et al., 2000). Third, in a recent neuro-two columns). In all cases, responses were stronger to

imaging study, Kilts et al. (2003) compared the brainthe disgust compared to the pleasure stimuli, be they

activity during the recognition of emotions from staticolfactory or visual (i.e., all t values were positive). For

and dynamic displays of facial expressions and con-two of the insular clusters, both the visual and olfactory

cluded that the encoding of facial expressions of emo-responses were significantly larger for the disgust stim-

tion by static or dynamic displays is associated withuli (p � 0.05). The third cluster of the insula responded

different neural correlates for their decoding.significantly more to the observation of disgust com-

Olfactory runs were composed of two experimentalpared to the observation of pleasure but did not signifi-

conditions separated by periods of rest. Conditionscantly discriminate between the two types of odorants.

were composed of blocks of olfactory stimulation duringFinally, the cluster located in the anterior cingulate cor-

which subjects were exposed to different disgusting ortex showed significantly stronger activations for the ob-

pleasant odorants (“disgusting odorant” and “pleasantservation of disgust versus observation of pleasure con-

odorant” conditions, respectively). Full details of theditions but only showed a nonsignificant trend for

procedures are provided in the Experimental Proce-disgusting odorants versus pleasant odorants.

dures section. The data obtained during the olfactoryTo confirm the presence of the overlaps observed

and visual runs were analyzed separately using random-between the observation of disgust – neutral and the

effect analyses (n � 14 subjects, p � 0.005 uncorrected,disgusting odorant – rest contrast t maps, we performed

and k � 20).a modified conjunction analysis (p � 0.005, k � 20)between these two contrasts (see Experimental Proce-dures). The results confirmed the presence of overlapsOlfactory Stimulation

The results of the disgusting odorant – rest and pleasant between these two conditions, showing a cluster [33voxels with a peak at x � �38, y � 26, z � �6, and aodorant – rest contrasts are reported in Table 1. Among

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Table 1. Olfactory Activations

MNI TALSize

Anatomical Description Hem. x y z x y z t Value (Voxels)

A. Disgusting odorant � rest, random effect,p � 0.005, k � 20, n � 14 s

Amygdala/uncus L �24 �2 �30 �24 �3 �25 6.57 64Amygdala R 20 �4 �16 20 �5 �13 5.82 200Anterior insula/inferior frontal gyrus R 36 28 �2 36 27 �3 4.89 155Anterior insula R 36 10 4 36 10 3 5.78 64Middle frontal gyrus L �44 52 8 44 51 5 4.71 38Anterior insula L �36 22 8 �36 22 6 6.28 149Inferior frontal gyrus R 50 26 14 50 26 12 4.82 32Inferior frontal gyrus R 46 16 18 46 16 16 6.63 66Middle frontal gyrus R 44 36 22 44 36 18 4.59 31Anterior cingulate R � L 4 26 26 4 26 23 5.14 69Precentral sulcus L �34 0 36 �34 2 33 7.43 54Superior parietal lobule R 36 �70 56 36 �65 55 4.53 25

B. Pleasant odorant – rest, random effect,p � 0.005, k � 20, n � 14 s

Cerebellum L �20 �54 �30 �20 �54 �23 5.23 20Amygdala/uncus L �18 �2 �28 �18 �3 �23 6.51 40Brain stem R � L 2 �20 �24 2 �20 �19 5.35 43Amygdala R 26 0 �22 26 �1 �18 8.37 327Inferior frontal gyrus pars orbitalis R 34 34 �12 34 32 �12 4.84 114Cerebellum (culmen) L �2 �42 �6 �2 �41 �3 5.36 64Anterior insula R 38 �2 2 38 �2 2 4.5 48Anterior tip of caudate R 26 28 10 26 28 8 9.31 34Middle frontal gyrus R 48 42 24 48 42 20 5 80Middle frontal gyrus L �46 34 24 �46 34 20 6.52 183Precentral sulcus R 46 8 28 46 9 25 4.77 41Middle frontal gyrus R 40 30 30 40 30 26 5.13 43Rostral inf. parietal lobule R 44 �62 48 44 �58 47 4.48 58Superior parietal lobule R 34 �70 54 34 �65 53 4.83 23

Location in MNI and Talaraich (TAL) coordinates (x, y, z), anatomical description, maximum t value, and number of voxels for all clusters foundto be significantly activated during the olfactory contrasts. Activations are shown in ventrodorsal order. The voxel size was 2 � 2 � 2 mm3.

t(13) � 5.41, p � 0.001] corresponding to the first cluster that are selectively activated during the feeling of dis-gust. This suggests that the understanding of the facialof Table 3. All the three remaining clusters of Table 3

are significant in this conjunction analysis if k is lowered expressions of disgust as displayed by others involvesthe activation of neural substrates normally activatedto the cluster size of these remaining clusters.

Applying the same modified conjunction analysis to during the experience of the same emotion. Theseshared neural substrates are the left anterior insula andthe observation of pleasure – neutral and pleasant odor-

ant – rest conditions revealed no significant clusters of the right anterior cingulate cortex.overlap. Nor did the conjunction analysis between thenonmatching contrasts, i.e., observation of pleasure – The Insulaneutral with disgusting odorants – rest or observation Cytoarchitectonically, the monkey’s insula can be di-of disgust – neutral with pleasant odorants – rest. The vided into three zones (agranular, dysgranular, and gran-lack of overlap between the observation of pleased fa- ular; Mesulam and Mufson, 1982a). Functionally, how-cial expressions and the olfaction of pleasant odorants ever, the insula is formed by two major functionalis probably due to the fact that, in contrast to the emotion sectors: an anterior sector comprising the agranular andof disgust, which is tightly linked to bad odorants/tastes, the anterior dysgranular insula and a posterior sectorthe emotion of pleasure can be triggered by many stim- comprising the posterior dysgranular and the granularuli, only few of which are olfactory or gustatory. There insula (Mesulam and Mufson, 1982b; Mufson and Mesu-is therefore a strong link between bad tastes/smells, the lam, 1982). The anterior sector is an olfactory and gusta-emotion of disgust, and the facial expression of disgust, tory center that appears to control visceral sensationswhile there is a much weaker link between pleasant and the related autonomic responses. Additionally, itodors/smells, the emotion of pleasure, and pleased fa- receives visual information from the anterior sectors ofcial expressions. the ventral bank of the superior temporal cortex, where

cells have been found in the monkey to respond to thesight of faces (Bruce et al., 1981; Perrett et al., 1982,Discussion1984, 1985; Keysers et al., 2001). In contrast, the poste-rior sector of the insula is characterized by connectionsThe main finding of the present study is that the observa-

tion of disgust automatically activates neural substrates with auditory, somatosensory, and premotor areas and

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hemisphere (Zald and Pardo, 1997, 2000; Zald et al.,1998b; Royet et al., 2000, 2001, 2003; Gottfried et al.,2002; Anderson et al., 2003; Zald, 2003). Investigationsusing gustatory stimuli confirm this finding, showing thatthe left anterior insula/opercular region responded pref-erentially to unpleasant compared to pleasant tastes(Zald et al., 1998a; Small et al., 2003).

While unpleasant tastes and smells are often per-ceived as more intense than their pleasant counterparts,recently, Small et al. (2003) showed that the left anteriorinsula preference for unpleasant tastes is maintainedeven if these unpleasant tastes are perceived as lessintense than the pleasant tastes they are comparedagainst. The cluster showing this property included thecoordinates at which we found the overlap between theobservation of disgust and the disgusting odorants.

Finally, Yaxley et al. (1990) and Scott et al. (1991)report the existence of single neurones in the macaqueanterior insula and opercular frontal cortex respondingselectively to particular gustatory stimuli (see also Au-gustine, 1996, and Dolan, 2002, for reviews). None ofFigure 2. Results of the Olfactory Stimulationthese studies, however, addressed the issue of whetherResults of the olfactory stimulation superimposed on the anatomical

image of a standard MNI brain using neurological conventions (right the same area was also activated during the observationis right). (A) Coronal sections focusing on the amygdalae. Note the of facial expressions of disgust. Taken together the ana-large degree of overlap (orange) between the activations determined tomical and functional data indicate that the left anteriorby disgusting (red) and pleasant odorants (green) in the right amyg- insula and neighboring opercular frontal cortex aredala and left parahippocampal cortex. (B) Axial slice showing the

structures strongly involved in the sensation of dis-response to odorants in the insula. The activity is bilateral and ante-gusting stimuli.rior for the disgusting odorants and is confined to a more posterior

location of the right insula for the pleasant odorants. There is no The insula, however, is not only a center for elaborat-overlap in the insula between the activations determined by the two ing olfactory and gustatory stimuli. Electrical stimulationodorants. The color coding is indicated on the bottom right. of the anterior sector of the insula conducted during

neurosurgery (Penfield and Faulk, 1955) evoked nauseaor the sensation of being sick (“Feeling as if she wereis not related to the olfactory or gustatory modalities.going to be sick,” Penfield and Faulk [1955], p. 451). ItA direct comparison between the macaque monkey’salso evoked visceromotor activity (“My stomach wentinsula and the human one showed that, although theup and down like when you vomit,” ibidem, p. 451). More

human insula is substantially larger than the macaque’srecently, Krolak-Salmon and colleagues (2003) showed

counterpart, the general architectonic organization isthat electrically stimulating the anterior insula through

strikingly similar in the two species and shows the sameimplanted depth electrodes produced sensations in the

subdivisions (Mesulam and Mufson, 1982a). throat and mouth that were “difficult to stand.” TakenThe activations observed during the disgusting odor- together, these findings demonstrate a role for the ante-

ant condition of our experiment fall within the anterior rior insula in transforming unpleasant sensory input intohalf of both insulae, most likely corresponding to the visceromotor reactions and the accompanying feelinganterior sectors of Mesulam and Mufson (1982a, 1982b). of disgust.No activations were found in the posterior sectors. An Here we show that the same visceromotor region,activation of the same anterior sector, but restricted to related to such an evolutionary ancient basic emotionthe left insula, was found during the observation of the as disgust, can be directly activated by the observationdisgusted facial expression, a finding in agreement with of the facial expression of disgust displayed by others.the higher-order visual information reaching the insula This finding is in agreement with previous experimentsfrom the superior temporal sulcus. Most interestingly, showing that the vision of disgusted static facial expres-there was a clear overlap between both activations. This sions leads to activations in the anterior insula (Phillipsis, to our knowledge, the first direct neuroimaging dem- et al., 1997, 1998; Sprengelmeyer et al., 1998; Schienleonstration that the same sites in the insula mediate both et al., 2002; Krolak-Salmon et al., 2003). None of thesethe observation and the feeling of disgust. studies, though, evoked the sensation of disgust in the

The activation of the anterior insula during disgusting participants to investigate if the activated locations areolfactory stimulation found in the present experiment is common to both the experience of disgust and the per-in accord with previous neuroimaging findings showing ception of the same emotion in others.its activation during olfactory stimulation. These studies Carr et al. (2003) showed an activation of the anteriorindicate that the transition zone between the anterior insula/inferior frontal gyrus during both the observationinsula and the frontal operculum located in the left hemi- and imitation of facial expressions. In their block design,sphere was preferentially activated for unpleasant com- each block contained examples of all six basic emotionspared to pleasant odors (Zald and Pardo, 2000; Royet in random order: happy, sad, angry, surprised, afraid,et al., 2003). Indeed, emotional responses to disgusting and disgusted. It is important to stress that imitation

usually does not require experiencing the imitated emo-stimuli are generally reported to be stronger in the left

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Table 2. Visual Activations

MNI TAL

Anatomical Description Hem. x y z x y z t Value Size (Voxels)

A. Observation of disgust – neutral, randomeffect, p � 0.005, k � 20, n � 14 s

Fusiform gyrus/declive L �30 �74 �20 �30 �73 �13 5.37 82Middle occipital R 44 �70 �14 44 �68 �8 5.23 107Brain stem L �4 �26 �10 �4 �26 �7 5.77 46Inferior frontal gyrus L �38 26 �6 �38 25 �6 5.41 103Pulvinar/lentiform nucleus R 22 12 0 22 12 �1 5.2 39Anterior insula/inferior frontal gyrus L �24 30 4 �24 29 2 4.03 67Superior temporal sulcus R 62 �44 8 61 �42 9 4.48 43Anterior insula L �24 8 12 �24 8 11 4.59 30Precentral gyrus R 64 12 14 63 12 12 5.11 29Dorsal bank of the silvian fisure L �50 �14 18 �50 �13 17 6.13 60Middle frontal gyrus L �36 56 24 �36 55 19 5.33 23Supramarginal gyrus R 40 �50 28 40 �47 28 4.71 30Cingulate gyrus R 4 24 30 4 25 26 5.59 20Middle frontal R 54 8 40 53 10 36 5.07 51Cingulate/medial frontal gyrus L �4 12 48 �4 14 44 4.22 36Postcentral gyrus L �52 �20 52 �51 �17 49 6.63 33Superior/medial frontal gyrus R 8 12 52 8 14 47 6.12 101

B. Observation of pleasure – neutral, randomeffect, p � 0.005, k � 20, n � 14 s

Cerebellum (declive) L �2 �64 �24 �2 �63 �17 5.90 26Parahippocampal gyrus L �16 �10 �22 �16 �11 �18 4.10 38Fusiform gyrus R 40 �74 �20 40 �73 �13 3.73 34Precentral gyrus L �50 �12 10 �50 �11 10 4.68 28Inferior frontal gyrus R 48 24 18 48 24 15 4.81 46Precuneus R 6 �70 44 6 �66 44 4.40 34

Location in MNI and Talaraich (TAL) coordinates (x, y, z), anatomical description, maximum t value, and number of voxels for all clusters foundto be significantly activates during the visual contrasts. Activations are shown in ventrodorsal order. The voxel size was 2 � 2 � 2 mm3

tion. Their data, therefore, indicate that the insula is we show the anterior insula to respond to disgusted butnot to happy dynamic facial expressions.involved in imitation but not that it is directly involved

in the experience of emotions. However, in the light of The fact that the feeling of disgust and the perceptionof that emotion in others share a common neural sub-our findings, it is possible that, during imitation, some

of their participants felt the imitated emotion—as actors strate confirms previous neuropsychological studies(Calder et al., 2000, and Adolphs et al., 2003). Afterdo when using the “Stanislavsky” method of emotion

induction (Stanislavsky, 1936). The relatively low statisti- lesions affecting the insulae and neighboring structures,two patients were selectively impaired in recognizingcal significance of the activation in the insula reported

by Carr et al. (2003) during the observation of emotions the facial expression of disgust as compared to otherfacial expressions and reported having reduced sensa-(t � 3.02) is probably a consequence of their experimen-

tal design: they used blocks of mixed emotions, while tions of disgust themselves. In those patients, the le-

Table 3. Overlap between Observing and Feeling Disgust

MNI TAL t Value Direct ComparisonsSize

Anatomical Description Hem x y z x y z Vis. Olf. (vox.) Disg. – pleas. odorants Observ. of disgust – pleasure

Anterior insula/inferior L �38 26 �6 �38 25 �6 5.41 4.07 25 t(13) � 2.44, p � 0.01 t(13) � 2, p � 0.03frontal gyrus

Anterior insula/inferior L �34 28 6 �34 27 4 3.92 4.00 12 t(13) � 0.02, p � 0.49 t(13) � 1.64, p � 0.06frontal gyrus

Anterior insula L �34 10 16 �34 10 14 3.55 4.22 2 t(13) � 2, p � 0.03 t(13) � 2.52, p � 0.01Anterior cingulate R 4 24 30 4 25 26 5.59 4.43 6 t(13) � 1.29, p � 0.11 t(13) � 3.63, p � 0.002

cortex

Location in MNI and Talairach space and size of the clusters common to both the disgusting odorants – rest and the observation of disgust– neutral contrasts together with the anatomical description of their location. The maximal t score observed in the clusters of overlap is shownseparately for the visual and olfactory contrasts. The last two columns show the result of a direct comparison between the BOLD signalevoked by disgusting versus pleasant odorants and between the observation of disgusted versus pleased faces. Results that are significantat p � 0.05 are shown in bold. The probability of finding five or more significant t tests with a p � 0.05 criterion is less than 2 � 10�5 accordingto a binomial distribution.

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Figure 3. Illustration of the Overlap

Illustration of the overlap (white) between the brain activation during the observation (blue) and the feeling (red) of disgust. The olfactory andvisual analysis were performed separately as random-effect analysis. The results are superimposed on parasagittal slices of a standardMNI brain.

sions were not restricted to the insula, but our data sence of further imaging studies demonstrating the acti-vation of the anterior cingulate during the observationsuggest that, among the affected structures, the insula

was probably responsible for the symptomatology. of the facial expressions of others, conclusions aboutthe overlapping activation found in our study can onlybe tentative. In the light of the study of Hutchison et al.The Cingulate Cortex

Anatomically, the cingulate cortex is a very heteroge- (1999), our data nevertheless suggest that the anteriorcingulate might be implicated both in the experienceneous structure formed by a large number of cytoarchi-

tectonic areas. It can be divided along the rostrocaudal and the observation of aversive stimuli, be they painfulor disgusting.axis into a posterior granular and an anterior agranular

sector (Brodmann, 1909). Furthermore, it can be dividedalong the dorsoventral dimension into an old periallocor- Understanding Others by Matching Felt

and Observed Emotionstical area, adjacent to the corpus callosum (Brodmannareas, BA 33), a proisocortical region (BA 24, 25), and The idea that we perceive emotions in others by activat-

ing the same emotion in ourselves is not new. It hasa paralimbic region on the upper bank of the cingulatesulcus and in the paracingulate gyrus (BA 32). Our acti- been the explicit content of many theoretical papers and

the tentative conclusion of many experimental studiesvation is located in the anterior sector of the cingulatecortex and is relatively ventral, thus, most likely falling (Phillips et al., 1997; Adolphs, 2002; Goldman and Gal-

lese, 2000; Gallese, 2003; Calder et al., 2000; Carr et al.,within the paracingulate gyrus.The anterior cingulate cortex is considered to be im- 2003). In the present study, by using disgusting olfactory

stimulation, we evoked what is called “core disgust”portant for the processing of painful stimuli. Single neu-ron studies in monkeys (Koyama et al., 1998) and hu- (Rozin et al., 2000)—the most primitive and intimate feel-

ing of disgust. The neural substrate of this core disgustmans (Lozano et al., 1995, and Hutchison et al., 1999)show neurons in the anterior cingulate cortex re- overlapped considerably with the neural activation ob-

tained during the passive viewing of another’s facialsponding to painful stimulation. This finding was con-firmed by neuroimaging studies in humans (Talbot et expression of disgust. This finding is in accord with the

above-mentioned data of Krolak-Salmon et al. (2003)al., 1991; Casey et al., 1996; Vogt et al., 1996; Davis etal., 1997; Peyron et al., 2000, for a review). The anterior showing that that the anterior ventral insula is activated

by the observation of disgusted facial expressions andcingulate has also been shown to participate in the pro-cessing of aversive olfactory and gustative stimuli (Zald that electrical stimulation of the same location causes

unpleasant sensations in the throat and mouth. Takenet al., 1998b; Royet et al., 2000).On the other hand, evidence for the activation of the together, these findings demonstrate that observing

someone else’s facial expression of disgust automati-same structure during the observation of aversive stimulioccurring to others is still very scarce. Only Hutchison cally retrieves a neural representation of disgust. The

fact that the anterior insula is necessary for our abilityet al. (1999) report that a single neuron in the anteriorcingulate cortex of a patient responded both when the to feel disgust and recognize the same emotion in others

is supported by neuropsychological studies (Calder etfinger of the patient was pinpricked and when the patientobserved the surgeon pinpricking himself. In the ab- al., 2000, and Adolphs et al., 2003) showing that lesions

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Experimental Designfocused on the anterior insula lead to selective deficitsThe study was conducted as a block design, with four functionalin experiencing disgust and recognizing that emotiondata acquisition runs: two visual runs followed by two olfactory runs.in others. Thus, the available empirical data strongly

support the hot hypothesis of emotion recognition.Visual RunsOur subjects passively observed the stimuli withoutVisual runs followed a 24 s ON/3 s OFF block design, with three

any explicit task and without being aware of the aim of conditions: observation of neutral, disgusted, and pleased facialthe study. This indicates that the anterior insula/inferior emotional expression (see Figure 1). Each block was repeated three

times in each run and was composed of 3 s movies showing anfrontal gyrus and cingulate cortex activations we ob-actor leaning forward (�1 s) to smell the content of a glass. Theserved are the result of an automatic sharing, by theactor then leaned back slowly with either a neutral (neutral), pleasedobserver, of the displayed emotion. In the context of(pleasure), or disgusted (disgust) facial expression (�2 s) (see Figureeveryday life, this automaticity may explain why it is so1). Actors were recruited from a theater school in Marseille. The

hard to refrain from sharing a visceromotor response glass in front of them contained either pure water (neutral) or water(e.g., vomiting) of others when observing it in them. It with an added disgusting or pleasant odorant. This odorant was the

content of “stinking balls” taken at the local toy store for the disgustis likely, though, that our understanding of the emotionsand perfume for the pleasure condition. They were asked to displayof others depends on multiple systems associated withthe emotion in a natural but clear way. Each emotion was filmeddifferent levels of processing of emotional stimuli. Thethree times for each actor, and the most natural example was se-“hot” activation we found in the present experiment islected by one of the experimenters. Each block contained six movies

likely to be the evolutionary oldest form of emotion un- of the same condition showing six different actors separated by aderstanding. This “primitive” mechanism may protect 1 s pause of black screen. Two consecutive blocks were separated

by a 3 s pause of black screen. The order of the blocks was pseudo-monkeys and young infants from the food poisoningrandomized and mirror imaged between the first and second run.described in the Introduction, even before the evolution/The order of the two runs was inverted from subject to subject.development of sophisticated cognitive skills. In hu-

mans, cognitive routes toward the understanding ofOlfactory Runsemotions are then probably added (see Frith and Frith,Olfactory runs followed a 12 s ON/24 s OFF blocked design, with1999). Thus, the hot hypothesis and the cold hypothesestwo experimental conditions: pleasant odorants (P) and disgusting

we mentioned earlier should be seen as complementary. odorants (D). Each run contained eight blocks of each experimentalOne may speculate, however, that a disturbance of this condition, separated by rest (R). In each run, the order of presenta-

tion of P and D conditions was pseudorandomized but identical forprimitive mechanism might have important implicationsall subjects. The order of both runs was counterbalanced betweenfor social interactions.subjects. Subjects were instructed to breathe regularly and to focusThe mirror-neuron matching system found in monkeystheir attention on the odorants. They had their eyes and mouthand humans shows that our internal representation ofclosed throughout the runs. Since the mean duration of a breath

actions is triggered during the observation or listening cycle was from 3 to 5 s, two to four odorous stimulations wereof someone else’s actions (Gallese et al., 1996; Rizzolatti performed during an ON block. Olfactory stimulation: Odors were

presented with an airflow olfactometer, which allowed synchroniza-et al., 1996; Kohler et al., 2002; see Rizzolatti et al., 2001,tion of stimulation with breathing. The stimulation equipment wasfor a review). The present findings demonstrate thatessentially the one used in a previous PET study (Royet et al., 1999,a similar mechanism may apply to emotions: seeing2001), but adapted so as to avoid interference with the static mag-someone else’s facial emotional expressions triggersnetic field of the scanner (Royet et al., 2003). Briefly, compressed

the neural activity typical of our own experience of the air (10l/min) was pumped into the olfactometer and delivered contin-same emotion—even when, as in our experiment, parti- uously through a commercially available anesthesia mask. This

masked was put in place before the beginning of the experimentcipants are not explicitly instructed to empathize withand was therefore on the subjects face even during the visual runs.the actors they saw.At the beginning of each inspiration, odors were injected into theIn conclusion, the present results suggest that thereolfactometer, which carried it to the subject’s anesthesia mask.is a common mechanism for understanding the emotionBreathing was recorded with the aid of a PVC foot bellows (Herga

in others and feeling the same emotions in ourselves. Electric Ltd, Suffolk, UK) held on the stomach with a judo belt. AnFurthermore, and most importantly, these findings sug- operator monitored breathing and squeezed the odor bottle so as

to flush the odor into the injection head during inspiration. Odorousgest that a similar mechanism allows us to understandstimuli: Twenty odorants were used for both olfactory functionalboth the actions and the emotions of others, thereforeruns. They were split into two sets of ten odorants as a functionproviding a unifying perspective on the neural mecha-of perceived hedonicity and intensity ratings (Table 4) from datanisms underlying our capacity to understand the behav-obtained in previous work (Royet et al., 1999). For the pleasant

ior of others. condition, ten odorants were selected so as to provide the highesthedonicity scores. For the unpleasant condition, ten odorants wereselected for their particularly low hedonicity scores. To avoid anExperimental Proceduresintensity effect, the mean intensity scores between the two condi-tions were kept as similar as possible [F(1,18) � 5.3, p � 0.03], butSubjects

Fourteen healthy right-handed male volunteers (20–27 years of age) as reported previously, odors selected to be the most unpleasantare generally perceived as more intense and more likely to evokescreened for neurological and psychiatric antecedents participated

in the experiment. Handedness was assessed by means of the Edin- a stronger emotional reaction than the odors selected to be themost pleasant (Royet et al., 2003). The hedonicity scores indeedburgh questionnaire (Oldfield, 1971). All subjects had normal olfac-

tion and a mean duration of breath cycle ranging from 3 to 6 s. deviated more from neutral (i.e., 5) for the disgusting compared tothe pleasant odorants. Accordingly, all our subjects described hav-The subjects participating in the study provided informed written

consent, and the experiment was approved by the local ethics com- ing felt strong disgust in reaction to the disgusting odorants butoften reported that the pleasant odorants, while clearly perceived,mittee and conducted according to French regulations on biomedi-

cal experiments on healthy volunteers. Subjects were not informed were not as pleasant as the disgusting odorants were disgusting.Before scanning, subjects were trained not to move their headsabout the aim of the study before the experiment but were informed

after the study. or facial musculature during odorous stimulation. Despite strong

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contrast significantly differed from zero. Clusters were consideredTable 4. List of Odorants Selected for Pleasant and Disgustingsignificant only if they were composed of at least 20 contiguousConditions during Olfactory Runsvoxels, each of which having a p � 0.005 (uncorrected). Overlaps

Pleasant Disgusting between different contrasts were obtained by transforming the fil-tered statistic three-dimensional maps into true-false maps of signif-1 passion fruit valeraldehydeicant and nonsignificant voxels. Voxels were considered to be part2 lavender ethyl-mercaptana

of an “overlap” when they had a “true” value in both contrasts.3 apricot hexaneSince we were considering results from a random-effect analysis4 anise butyric acid(second-order analysis) a reliable estimate of the type I error of5 pear tetrahydrothiophenea

finding voxels of overlap is not currently available.6 caramel ethyl-diglycol7 coconut isovaleric acida

Direct Comparisons8 wild strawberry furfuryl mercaptanOnce we determined clusters activated both by disgusting odorants9 mint onionand by the observation of disgusted facial expressions, we tested10 banana iso amylphenyl acetatewithin these clusters if the activation caused by disgust stimuli (be

Hedonicity they odorants or facial expressions) was significantly larger thanthat determined by pleasure stimuli. Using the toolbox MarsBarMean score (SD) 6.39 (0.55) 1.16 (0.45)(http://marsbar.sourceforge.net; M. Brett, J.-L. Anton, R. Valabregue,Score range 5.58–7.24 0.55–1.93and J.-B. Poline, 2002, Region of interest analysis using an SPM

Intensity toolbox, abstract), for each of the four clusters of Table 3 and foreach subject, we evaluated the GLM used for the group analysisMean score (SD) 5.91 (0.68) 6.88 (1.13)but considered the mean BOLD signal of the voxels composingScore range 4.69–6.62 4.95–8.25each cluster instead of the voxel-by-voxel values used in the groupanalysis. This method yielded a single time series and a single seta Odorant with high potency and of which the concentration wasof GLM parameters for each cluster and subject. We then calculatedlimited to 1%.the contrast values for disgusting odorants – pleasant odorants andfor observation of disgust – observation of pleasure for each subjectseparately. Finally, we tested if these contrast values had a mean

unpleasant and possible trigeminal sensations, the results from the larger than zero using a one-sided t test with df � 13. This analysisrealignment procedures confirm that the subjects did not move their was a random-effect analysis for ROI. The last two columns of Tableheads in reaction to the odorants. Odorants were presented in white 3 show the results.polyethylene squeeze bottles (100 ml) provided with a dropper (Osi,France). They were diluted in mineral oil so that 5 ml of odorous Modified Conjunction Analysessolution (10%) were prepared and adsorbed by compressed fila- Conjunction analyses between two contrasts A and B have beenments of polypropylene. The concentration of the products with described as a method to test if both contrasts are different fromvery high potency was limited to 1%. zero in a particular voxel (Price and Friston, 1997). Due to the imple-

mentation of the conjunction analysis in SPM99 (Price and Friston,fMRI Acquisition 1997), the probability reported by such a conjunction analysis canImages were acquired using a 3T whole-body imager MEDSPEC 30/ pass a certain statistical threshold despite the fact that one of the80 AVANCE (Brucker, Ettlingen, Germany) equipped with a circular contrasts would not be significant if tested alone. To exclude thispolarized head coil. For each participant, we first acquired a high- possibility, we masked the results of the conjunction analysis be-resolution structural T1-weighted anatomical image (inversion- tween A and B (p � 0.005 and k � 20) with the results of the individualrecovery sequence, 1 � 0.75 � 1.22 mm) parallel to the bicommis- t test for the two contrasts A and B at p � 0.01. All these analysessural plane, covering the whole brain. For functional imaging, we were performed at the second level, i.e., on the contrast imagesused a T2*-weighted echo-planar sequence at 30 interleaved 3.5 obtained from the single subject analyses, and were therefore ran-mm thick axial slices with 1 mm gap (TR � 3000 ms, TE � 35 ms, dom-effect analyses.flip angle � 80�, FOV � 19.2 � 19.2 cm, 64 � 64 matrix of 3 � 3mm voxels). Acknowledgments

fMRI Data Preprocessing The research was financed by the Fondation de France, the Fonda-Data were preprocessed and analyzed using Statistical Parametrical tion Lejeune, the Italian MIURST, and the Neuroscience and SensoryMapping (SPM 99, Wellcome Department of Cognitive Neurology, System laboratory of the CNRS. C.K. held a European Union Marie-London, UK; http://www.fil.ion.ucl.ac.uk; Friston et al., 1995a). All Curie fellowship. We wish to thank M. Roth, B. Nazarian, and J.-L.functional volumes for each subject were realigned to the first vol- Anton for their expert help with the fMRI scanning. The Neuroscienceume acquired. Images were then spatially normalized (Friston et al., and Sensory System laboratory belongs to the Institut Federatif des1995b) to the Montreal Neurological Institute (MNI) standard brain Neurosciences de Lyon.and resampled to obtain images with a voxel size of 2 � 2 � 2mm. Allvolumes were then smoothed with a 6 mm full-width half-maximum Received: July 18, 2003isotropic Gaussian kernel. This smoothing is necessary to fulfill the Revised: September 16, 2003statistical assumptions of the random field analysis. Accepted: October 10, 2003

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