Subliminal fear priming potentiates negativefacial reactions to food pictures in women withanorexia nervosa

R. Soussignan1*, T. Jiang1, D. Rigaud1, J. P. Royet2 and B. Schaal1

1 Centre Europeen des Sciences du Gout, CNRS (UMR 5170), Universite de Bourgogne, Dijon, France2 Laboratoire de Neurosciences Sensorielles, Comportement, Cognition, CNRS (UMR 5020), Universite Claude Bernard Lyon 1, France

Background. To investigate hedonic reactivity and the influence of unconscious emotional processes on the low

sensitivity to positive reinforcement of food in anorexia nervosa (AN).

Method. AN and healthy women were exposed to palatable food pictures just after a subliminal exposure to facial

expressions (happy, disgust, fear and neutral faces), either while fasting or after a standardized meal (hunger versus

satiety). Both implicit [facial electromyographic (EMG) activity from zygomatic and corrugator muscles, skin conduct-

ance, heart rate, and videotaped facial behavior] and explicit (self-reported pleasure and desire) measures of affective

processes were recorded.

Results. In contrast to healthy women, the AN patients did not display objective and subjective indices of pleasure

to food pictures when they were in the hunger states. Pleasure to food cues (liking) was more affected than the desire

to eat (wanting) in AN patients. Subliminal ‘ fear faces ’ increased corrugator muscle reactivity to food stimuli in

fasting AN patients, as compared to controls.

Conclusions. The results suggest that unconscious fear cues increase the negative appraisal of alimentary stimuli in

AN patients and thus contribute to decreased energy intake.

Received 5 November 2008 ; Revised 18 May 2009 ; Accepted 19 May 2009

Key words : Anorexia nervosa, emotion, facial electromyography, facial expressions, fear, liking, pleasure, unconscious

process, wanting.

Introduction

Anorexia nervosa (AN) is a disorder that occurs

mainly in females during adolescence or young adult-

hood. AN is associated with a self-induced excessive

weight loss, an intense fear of gaining weight, and a

disturbance in the perception of one’s body shape

(DSM-IV; APA, 1994). Current aetiological models

emphasize a multifactorial origin involving genetic,

psychobiological and sociocultural factors (Polivy &

Herman, 2002 ; Connan et al. 2003 ; Bergen et al. 2005).

Although a biopsychosocial approach can account for

the key symptoms of AN, current explanations have

largely neglected the potential role of reward/hedonic

processes as contributing factors to the decline in food

intake. Such a perspective has been advocated recently,

leading to several proposals suggesting the dysfunc-

tion of brain reward systems as a possible cause of AN

(Davis & Woodside, 2002 ; Berridge, 2007 ; Zandian

et al. 2007). Others have stressed the value of hedonic/

positive incentive theory to guide future research on

this eating disorder (Pinel et al. 2000). According to

this framework, the anticipated pleasure of eating is

a strong motivating factor of consumption: people

are driven to eat less by energy stores declining

below homeostatic set points than by nutritional needs

and sensory/cognitive expectations modulating the

hedonic/incentive value of foods (Pinel et al. 2000 ;

Berridge, 2004a). Thus, when laboratory animals or

humans have ad libitum access to high-energy palat-

able food, overconsumption or obesity is relatively

common (Rothwell & Stock, 1979 ; Sorensen et al. 2003;

Berthoud, 2004). Conversely, according to the positive

incentive perspective, AN develops because it is in-

itially rewarding to eat less food, and self-starvation is

strengthened by the low reinforcing or hedonic value

of perceived food cues (Pinel et al. 2000 ; Zandian et al.

2007). This hypothesis is consistent with the fact that

excessive food restriction (i) activates neural sub-

strates of reward (i.e. dopamine and endogenous

* Address for correspondence : Dr R. Soussignan, Centre Europeen

des Sciences du Gout, CNRS, 15 rue Picardet, 21000 Dijon, France.

(Email : soussignan@cesg.cnrs.fr)

Psychological Medicine, Page 1 of 12. f Cambridge University Press 2009doi:10.1017/S0033291709990377 Printed in the United Kingdom

ORIGINAL ARTICLE

opioid systems), more particularly when it is as-

sociated with increased physical exercise (Heubner,

1993 ; Bergh & Sodersten, 1996; Sodersten et al. 2006),

(ii) may induce symptoms associated with AN (e.g.

depression, obsession) (Keys et al. 1950 ; Zandian et al.

2007) and (iii) produces adverse physiological effects

and taste aversion following food intake (Capaldi &

Myers, 1982 ; Pinel et al. 2000). Findings consistent with

this perspective have also been documented by

studies using food cueing paradigms in AN patients.

Compared to controls, AN patients (restricting and/or

binge-purge subtypes) displayed a dislike for the taste

or the sight of high-energy food (Drewnowski et al.

1987 ; Sunday & Halmi, 1990 ; Bossert et al. 1991 ; Santel

et al. 2006), less salivation to olfactory food stimuli

(LeGoff et al. 1988), a reduced pleasantness to sucrose

(Sunday & Halmi, 1990), no palatability priming effect

(Roefs et al. 2005), and highly anhedonic scores on self-

reported scales (Davis & Woodside, 2002 ; Eiber et al.

2002).

Despite the potential relevance of the reward/

pleasure deficit hypothesis in AN, not all attempts

to replicate previous results have been successful.

Alternative hypotheses, and also crucial method-

ological issues, must be considered before favouring

this perspective. First, the finding of a reduced hedonic

response to sucrose in AN patients was not reported

in some studies when sweet solutions were not

swallowed (Eiber et al. 2002), suggesting that an ex-

cessive fear of gaining weight rather than a decreased

ability to experience pleasure might be causal. Second,

if dysfunction of reward processes is involved in AN,

it is unclear which component is affected in AN per-

sons exposed to palatable food. Berridge (2003, 2007)

relied on animal findings to argue that two separable

brain systems underlie food incentives and hedonics :

the first, involving mesolimbic dopaminergic sub-

strates, mediates a motivational component (termed

‘wanting’, that is the desire to get a food) ; and the

second, involving a distributed network of brain

islands (e.g. opioidergic hotspots in the shell of nu-

cleus accumbens and in the ventral pallidum), me-

diates a hedonic/affective component (termed ‘ liking’,

that is the pleasure resulting from orosensory stimu-

lation of food). In humans, the role of endogenous

opioids in ingestive behavior and food pleasantness

has also been aptly reviewed (Yeomans & Gray, 2002),

and pharmacological and genetic evidence suggests

that both dopamine and opioid systems might con-

tribute to the pathophysiology of AN with possible

consequences in the reduction of desire or pleasure for

food (Yeomans & Gray, 2002 ; Frank et al. 2005 ; Brown

et al. 2007). Thus, because of their theoretical implica-

tions, experimental studies on wanting and liking are

needed to determine whether they are both altered in

AN. Third, self-ratings of food likes and dislikes were

most often used in AN studies, but whether subjective

report is the most appropriate to probe core hedonic

processes in this eating disorder is unclear. ANpatients

were often shown to display disturbances in the accu-

rate perception of internal states or feelings and in

their verbalization (i.e. alexithymia). This could affect

self-evaluation of hunger and satiety, of interocep-

tive awareness and of emotional states (Garfinkel,

1974 ; Nakai & Koh, 2001 ; Bydlowski et al. 2005 ;

Montebarocci et al. 2006). An approach based on

implicit measures of hedonic processes is therefore

needed. Such measures are currently used in psycho-

physiological research in both healthy and clinical

samples, relying on facial electromyography (EMG)

and autonomic variables as sensitive markers of

valence and arousal dimensions of affective processes

(e.g. Cacioppo et al. 1992; Lang et al. 1993). The use of

facial EMG and autonomic measures of emotional

bodily changes is further justified by the fact that

they may be dissociated from conscious experi-

ence in brain-damaged or emotionally disordered

patients (Luminet et al. 2004 ; Soussignan et al. 2005 ;

Zonnevylle-Bender et al. 2005) and are less susceptible

to demand characteristics and social desirability ef-

fects than are self-report data. Finally, it remains to be

clarified whether avoidance of food in AN may be in-

fluenced by dislike/fear cues independent of inten-

tionally controlled processes and without awareness

of the underlying affective response (Berridge &

Winkielman, 2003 ; Berridge, 2004b ; Winkielman et al.

2005). This issue can be investigated with affective

priming paradigms that have the potential to examine

whether (i) automatic/unconscious processes influ-

ence negative reactivity to food and (ii) AN patients

are more sensitive than healthy controls to emotional

primes related to food (i.e. disgust and fear cues).

Although there is some evidence that AN patients

make relatively automatic associations with foods

based on their palatability (Roefs et al. 2005), to the best

of our knowledge there are no studies that have

assessed whether unconscious emotional processes

potentiate facial, autonomic and subjective reactivity

to food cues in AN patients, and whether such pre-

attentive processing depends on their motivational

state (hungry versus satiated states).

The current study addresses the following ques-

tions. First, do distinct measures of hedonic processing

(facial EMG, videotaped facial behavior, verbal

ratings) differentiate AN women from healthy control

(HC) women while exposed to food pictures, regard-

less of the potential impact of affective primes?

Second, do subliminal positive and negative primes

influence facial EMG, autonomic and subjective re-

sponses to food pictures as a function of their valence,

2 R. Soussignan et al.

and does the motivational state (hunger versus satiety)

bear a differential impact on the effect of affective

primes in AN and healthy individuals? Third, are

subjective measures of liking and wanting dissociated

in AN patients?

These issues were addressed in a two-session ex-

periment in healthy and AN women, one run before

and the other after a standardized lunch, using a

backward masking procedure (exposure to subliminal

disgust, fear, happy, and neutral faces). Meanwhile,

EMG (activity of corrugator and zygomatic muscles),

autonomic (skin conductance and heart rate), video-

taped (smiles and negative expressions) and self-

reported (hedonic and wanting ratings) responses

were recorded in participants viewing pictures of

palatable foods. Disgust and fear expressions were

chosen as negative primes based on the importance of

these emotions in food hedonics and eating disorders

(Davey et al. 1998 ; Ellison et al. 1998), and on neuro-

imaging studies reporting that subliminal presen-

tations of fear and disgust expressions can activate

brain substrates underlying emotional processing

(Whalen et al. 1998 ; Phillips et al. 2004). The following

predictions were proposed: first, AN patients should

display higher negative reactivity (corrugator activity,

negative expressions and subjective ratings) to food

pictures as compared to HC subjects, and this dif-

ferential effect should be more pronounced during

hunger states to avoid food intake ; conversely, HC

participants should express a stronger positive reac-

tivity (zygomatic activity, smiles and subjective

ratings) during this motivational state. Second, sub-

liminal fear and disgust faces should potentiate nega-

tive and autonomic reactivity to food pictures in AN

patients during hunger states, whereas subliminal

happy faces should potentiate positive hedonic reac-

tivity in controls. Third, if AN involves a dysfunction

in hedonic processing, self-report measures of liking

and wanting should be dissociable in AN patients as

compared to HC subjects.

Method

Participants

The current study involved 16 females (age: mean ¡

S.D.=26.68¡7.30 years) fulfilling the DSM-IV criteria

for AN. They were recruited from the Endocrinology

Service of Dijon University Hospital. All were suffer-

ing from the restricting form of AN. They had a mean

body mass index (BMI) of 14.97¡1.97 kg/m2. The

HC subjects comprised 25 females (aged 24.6¡6.03

years) recruited by local advertisements. They had a

normal BMI (mean¡S.D.=20.52¡1.90 kg/m2) and re-

ported neither food restrictions nor allergies. For all

participants, exclusion criteria were consumption of

psychotropic drugs, hearing and visual impairments

and neurological diseases. Written informed consent

was obtained from all participants, with the an-

nounced aim to conduct a study on feeding behavior

in women.

Timing of experimental sessions

Each participant took part in two experimental

sessions, one before (hunger) and the other after

(satiety) lunch, during two consecutive days at the

Dijon Centre des Sciences du Gout. To control for

order effect, the hunger and satiety conditions were

counterbalanced across participants. Before the

hunger session, each participant was instructed to take

her breakfast before 0730 hours and to avoid eating

and drinking (except water) until the experiment that

began at 1220 hours. All participants complied with

this requirement and reported that they had followed

it. For the satiety session, the participant came to the

laboratory at 1230 hours to take a standard lunch

composed of an entree (100 g steamed semolina, 100 g

ham with parsley and half an egg), meat (60 g), cheese

(35 g), bread (50 g), cake with fruit (75 g), and a bottle

of mineral water (330 ml). The participants were told

to take their lunch ad libitum, and usually spent

15–25 min before terminating their meal. For the

satiety condition, the experimental sessions were

scheduled between 1340 and 1400 hours.

Stimuli

Food stimuli

The food stimuli were composed of 32 color pictures of

meals with a varied energy content drawn from the

International Affective Picture System (Lang et al.

2001) or selected from the Internet. They comprised

four sets of eight food pictures (SF1, SF2, SF3 and SF4),

each including the same food categories : pizza, meals

with a variety of dishes (including potatoes, vege-

tables and chicken), beef, cheese, chocolate, ice-cream,

cake/biscuits, and fruit. The eight pictures of each set

were matched on arousing, liking, and wanting scores

following a pretest conducted on 40 healthy female

undergraduates (aged 21.2¡1.1 years) who reported a

hungry level of 5.15 (S.D. =2.29) on a nine-point scale.

The pictures were shown on a 300r230 cm screen

during 6 s using Superlab software (version 2, Cedrus,

USA). The participants had to rate their arousal (i.e.

whether they felt stimulated/aroused while viewing

the picture) and wanting (i.e. their desire to consume

the food) reactions on a scale ranging from 1 (not at all)

to 9 (extremely), and also their liking reactions (i.e. If

you had to eat this food, what would you feel?) on a

Unconscious fear in anorexia nervosa 3

scale ranging from –4 (extreme dislike) to 4 (extreme

pleasure). Multivariate ANOVA using Wilks’ l distri-

bution revealed that the food pictures were rated as

palatable (pleasure rating : 1.30¡0.86) and that the

four sets of food pictures did not differ either on rat-

ings of arousal [SF1: 4.97¡0.61, SF2 : 4.81¡0.51, SF3:

4.84¡1.05, SF4: 4.68¡0.42, F(3, 37)=2.15, p>0.05], of

wanting [SF1: 5.49¡1.18, SF2: 5.25¡1.26, SF3:

5.51¡1.25, SF4: 5.30¡1.11, F(3, 37)=1.78, p>0.05] or

of liking [SF1 : 1.45¡0.80, SF2: 1.16¡0.92, SF3:

1.32¡0.98, SF4:1.27¡0.74, F(3, 37)=1.58, p>0.05].

Affective primes

Eight neutral faces were selected as masks and 32

stimuli (eight each of happy, fear, disgust and neutral

faces) served as primes. Of these 40 faces, 20 were

female and 20 were male. All except two neutral faces

came from the Pictures of Facial Affect (Ekman &

Friesen, 1976). The slides were digitized as 466r700

pixels resolution to allow presentation on a 17-inch

computer monitor.

Design of the priming procedure

The priming experiment consisted of four blocks, each

containing eight different subliminal facial expressions

of the same emotion (i.e. fear, disgust, happy and

neutral blocks). Each trial began with a warning signal

(the word ‘slide’) presented on the screen for 6 s, in-

dicating to the participant that pictures would be

presented. This condition was included as a baseline

period for the psychophysiological data. This warning

signal was followed by a forward mask (500-ms cross)

that was immediately replaced by a subliminal prime

(30-ms facial expression or neutral face). The prime

was immediately followed by a backward mask

(400-ms neutral female or male face). Following the

mask, the target (food picture) was presented for 6 s.

A double Latin square design was used to present the

four priming blocks. This allowed all possible as-

sociations between each of the four blocks of primes

and each of the four sets of food pictures. Once the

prime–target associations were determined for a given

participant (e.g. fear–SF1 ; disgust–SF2 ; happy–SF3;

neutral–SF4), the order in which the eight trials were

presented within each block was randomized for each

participant. The duration of projection of stimuli was

controlled using SuperLab Pro software.

Procedure

On arrival, the participant was seated in a comfortable

chair in a dimly lit, sound-attenuated experimental

room. Two experimenters and the material were

located in an adjacent isolated room. The participant

was asked to relax during the task and avoid any

movement of body parts where the sensors were at-

tached. After attachment of biosensors (see section on

psychophysiological recording), the subject was po-

sitioned 75 cm in front of a 17-inch flat-screen monitor

and a Hi-speed USB Webcam (DigiHoney TM series)

that recorded her facial behavior with a 480r640

video resolution. The first experimenter started the

psychophysiological and video recordings. The sec-

ond experimenter collected data about the partici-

pant’s hunger/satiety state (1=not at all hungry/full,

7=very hungry/full) and then activated pre-recorded

task-specific instructions using both the screen and

headphones. The participant was told that the word

‘slide ’ would be presented in the center of the screen

(warning signal) followed 6 s later by a face picture

and then a food picture. She was informed that the

face picture was included as if the person represented

by this face had to consume the food. The onsets of

primes and food pictures were automatically signaled

by a 60-ms 5-V pulse on a channel of the Chart

Windows software (which displayed psychophysio-

logical data) using a data acquisition and signal

conditioning card (DAQCard-DIO-24, National Instru-

ments Corporation, USA). After each food picture,

the participants used nine-point Likert scales to rate

their liking [from –4 (extreme dislike) to 4 (extreme

pleasure)] and wanting responses [from 1 (no desire

at all) to 9 (extreme desire)]. Prior to the onset of

the experiment, two trials served as practice stimuli.

After the experiment, the participants completed the

shortened 13-item Beck Depression Inventory (BDI ;

Beck et al. 1974), a widely used self-rating with estab-

lished reliability and validity.

Psychophysiological recording

The facial EMG and autonomic measures were moni-

tored using a 16-channel PowerLab system (AD

Instruments Pty Ltd, Australia) connected to a PC. The

bioelectrical signals were filtered and amplified before

being fed into the analog input connector of the

PowerLab unit and sampled at a rate of 200 Hz under

the online control of Chart 5.2 software.

Facial EMG

Muscular activity was detected using five miniature

Ag/AgCl surface electrodes filled with electrolyte gel,

following the guidelines proposed by Fridlund &

Cacioppo (1986) : two were placed over the left corru-

gator supercilii region, two over the left zygomaticus

major region (recording electrodes) and one on the

middle part of the forehead (reference electrode).

Before attaching the electrodes, the target sites of the

4 R. Soussignan et al.

skin were cleaned with alcohol and rubbed slightly to

reduce inter-electrode impedance. The EMG signals

were fed into electronic amplifiers and were band-

pass filtered from 10 to 250 Hz. The raw EMG signals

were rectified and smoothed with a 500-ms time

constant.

Autonomic measures

Skin conductance (SC) was recorded with the ML116

GSR Amplifier of the 16-channel PowerLab system,

which provides a low, constant-voltage AC excitation,

allowing the use of dry electrodes, with no special

electrolytes needed. The electrodes were attached with

a Velcro strap on the palmar surfaces of the distal

phalanges of the second and third fingers of the non-

dominant (usually the left) hand. Measurements

were displayed directly in mS. Heart rate (HR) was

measured using Ag/AgCl electrodes (BB-COM 2,

Comepa, France) and a standard Lead I electrode

configuration. A low-pass filter of 50 Hz was used

with the bioamplifier to eliminate high-frequency

components. A computed input command allowed a

threshold control to detect R wave pulses and to dis-

play HR in beats per minute on a separate channel.

Analysis of physiological and videotaped facial data

Physiological data

Muscular and cardiac data were averaged off-line

for each of the 6-s periods immediately preceding

(baseline) and following (stimulus period) the prime

onset. In accordance with standard practice (Fridlund,

1991), mean facial EMG data were log transformed

[log10(EMG+1)] to minimize skewness and hetero-

scedasticity. The EMG and cardiac scores acquired

during the baseline period were respectively sub-

tracted from those acquired during stimulus presen-

tation. SC response (SCR) was defined as a change in

the amplitude with onset occurring 1–4 s after stimu-

lus presentation. SCR change was calculated by sub-

tracting the 2-s SC level immediately preceding

stimulus onset from the largest value in the 2-s win-

dow after stimulation.

Coding of facial behavior

Videotaped facial behavior was analyzed with the

anatomically based Facial Action Coding System

(FACS; Ekman et al. 2002) by a certified coder (R.S.)

blind to the priming condition, the type of food pic-

tures and the clinical status of each participant

(healthy or AN). The negative expressions to food

pictures were coded in regrouping action units (AU)

indexing disgust [nose wrinkling (AU 9)/upper lip

raising (AU 10)] and those that have been shown to be

associated with negative emotions [brow lowering

(AU 4), lip corners tightening (AU 14), lip corners

lowering (AU 15), chin raising (AU 17), and lips

stretched laterally (AU 20)] (Soussignan et al. 1995,

1999 ; Soussignan & Schaal, 1996). For smiling, lip

corners pulling (AU 12) was coded (Soussignan, 2002).

The frequencies of negative facial expressions and

smiles for each priming block were used as dependent

variables.

Prime recognition task

To verify the validity of our subliminal priming pro-

cedure, participants performed a forced-choice recog-

nition task on a 15-inch laptop computer using

SuperLab Pro software. The task consisted of 32 trials

that were presented randomly across the participants

and that comprised the subliminal primes to which

each participant had been initially exposed. The par-

ticipants were instructed to direct their attention

to successive single pictures of faces (the flash of a

neutral/emotional face followed by a visible face) and

also to the simultaneous presentation of two faces.

Each trial began with a 2-s warning signal (slide) fol-

lowed by a 500-ms central cross and then by a 30-ms

prime (emotional or neutral face). The prime was im-

mediately masked by a 400-ms neutral face. Immedi-

ately afterward, two faces were presented for 1500 ms:

one target face (which corresponded to the neutral or

emotional subliminal prime) on one side of the screen

and another face (an incorrect foil expressing a distinct

emotion) on the other side of the screen. The two faces

were equally distributed at the left (L) and the right

(R) side of the screen. Following this presentation, the

L and R letters were shown on each side of the screen

and the participants had to decide which face was

presented in the flash by pressing the appropriate key

using an RB-730 pad (Cedrus, USA) connected to the

laptop. Three practice trials preceded the task. A three-

way ANOVA (grouprstaterprime) performed on

the percentage of prime recognition yielded no sig-

nificant main effects or interactive effects. The HC

subjects and AN patients had similar performances

during the fasting session (HC: 50.75¡3.96%, AN:

51.36¡4.95%) and after the lunch (HC: 50.0¡3.34%,

AN: 50.97¡4.18%), and the performance of recog-

nition did not vary as a function of the primes

[disgust : 51.92¡2.88%, happy: 48.91¡2.54%, neutral :

49.77¡3.05%, fear : 52.49¡2.98%, F(3, 117)=0.74,

p>0.05]. Performance on the forced-choice test for

each priming condition ranged from 47.9% to

53.9% in the fasting (hunger state) and lunch (satiety

state) sessions, which was not significant different

from chance [t(40), p’s >0.10]. Thus, the results

Unconscious fear in anorexia nervosa 5

suggested that our subliminal priming procedure was

appropriate to investigate the influence of uncon-

scious affective processes on facial, autonomic and

subjective reactivity to food pictures.

Statistical analyses

As AN patients reported higher depression scores

(12.6¡8.3) than the HC subjects [3.2¡3.4, t(39)=5.03,

p < 0.001], the D-Beck score was entered as a co-

variate in repeated-measures ANCOVAs conducted

on subjective, psychophysiological and observational

measures#, with group (AN versus HC) as the be-

tween-subject variable and motivational state (hunger

versus satiety) and priming (fear, disgust, happy,

neutral) as within-subject variables$. A two-way

ANCOVA (grouprmotivational state) was also per-

formed on self-reported scores of motivational state.

Fisher’s least significant difference (LSD) test was used

for making post-hoc comparisons between means.

Partial eta-squared (g2p) and Cohen’s d were reported

as a measure of effect size in ANCOVAs and in the

mean comparisons respectively, where d =(M1 –M2)/

spooled and spooled =p[(s1

2+s22)/2] (Cohen, 1988), where

M1, M2 are the means of samples and s1, s2 their stan-

dard deviations. Cohen (1988) has defined small effect

sizes as d=0.2, medium as d=0.5, and large as d=0.8.

Results

Subjective measures

Ratings of motivational states

All the participants reported a higher hunger level

before than after the lunch [5.23¡1.41 v. 2.79¡1.02,

F(1, 38)=33.24, p<0.00001, g2p=0.466]. A significant

interaction between state and group was found

[F(1, 38)=6.93, p=0.01, g2p=0.154]. The HC women

reported a higher hunger level than the AN patients

during the hunger session only (5.97 v. 4.49, d=0.95).

Liking rating

Significant main effects of group [F(1, 38)=4.33,

p=0.04, g2p=0.102], and hunger state [F(1, 38)=11.05,

p=0.002, g2p=0.225] emerged. These effects were

qualified by an interaction between group and state

[F(1, 38)=5.75, p=0.02, g2p=0.131]. As illustrated in

Fig. 1, the HC women reported higher hedonic reac-

tions to food pictures than AN patients during both

the hunger (p<0.001, d=0.51) and the satiety (p=0.03,

d=0.21) sessions. Furthermore, only the HC subjects

rated the food pictures as more pleasant in the hunger

than in the sated session (p<0.0001). The prime effect

failed to reach significance. Note that the lower sub-

jective rating of pleasure in AN women than in HC

during the pre-prandial condition was not solely due

to hunger differences because the group effect re-

mained significant after including hunger scores as a

covariate in the ANCOVA [F(1, 37)=4.15, p=0.048,

g2p=0.10].

Wanting rating

There were also significant effects of group [F(1, 38)=25.96, p<0.00001, g2

p=0.406] and hunger state

[F(1, 38)=4.69, p=0.037, g2p=0.11], and a significant

grouprstate interaction [F(1, 38)=8.47, p=0.006,

g2p=0.182]. As shown in Fig. 2, this interaction reflects

the fact that the HC responded to the food pictures

with higher wanting scores than did the AN patients

during the hunger state only (p<0.001, d=0.53).

However, both the AN and the HC women reported

higher wanting scores during the hungry than during

the satiety sessions (p<0.001). No priming effect was

detected.

Facial EMG

Corrugator muscle activity

The ANCOVA did not reveal significant main effects

for group, hunger state or priming. However, sig-

nificant grouprpriming [F(3, 102)=6.00, p=0.0008,

g2p=0.15] and grouprstaterpriming [F(3, 102)=2.91,

p=0.038, g2p=0.08] interactions were detected. Fig. 3

shows that these interactions reflect the fact that only

2

1

0

–1AN HC AN HC

**

*

***

Hunger Satiety

Fig. 1. Mean ratings of self-reported pleasure (liking) and

standard errors bars in response to food pictures during the

hunger and satiety sessions in anorexic (AN) and healthy

control (HC) participants (* p<0.05, ** p<0.01, *** p<0.001).

# The facial EMG data from four healthy controls and the

videotaped facial behavior data from three healthy controls and one

AN patient were not available because of equipment problems.

$ Preliminary analyses revealed that sessions order

(hunger–satiety versus satiety–hunger) did not

influence subjective and psychophysiological measures.

6 R. Soussignan et al.

subliminal fear expressions induced larger activity of

the corrugator muscle region in AN than HC partici-

pants viewing food pictures during the hunger session

(p=0.029, d=0.91). Furthermore, fear primes induced

a larger increase in corrugator activity in AN patients

during the hunger than during the satiety session

(p=0.02, d=0.54), whereas in the HC the effect of fear

primes on corrugator activity to food pictures was

lower in the hunger than in the satiety sessions

(p=0.04, d=0.42). A larger corrugator activity was

also found in response to fear as compared to happy

primes in AN participants during the hunger states

(p=0.048, d=0.57). Note that the effect sizes were

medium to large, suggesting that corrugator activity

differences between the AN and HC participants can

be accepted with confidence.

Zygomatic muscle activity

A significant main effect of group was detected

[F(1, 34)=4.51, p=0.04, g2p=0.12], revealing that, while

viewing food pictures, the controls demonstrated a

higher activity of zygomatic muscle region than the

AN patients (d=0.78) (Fig. 4). There was a trend for a

larger zygomatic activity during the hunger than

during the satiety sessions [F(1, 34)=3.42, p=0.07,

g2p=0.09], more particularly for the HC group as

compared to the AN group [F(1, 34)=2.94, p=0.09,

g2p=0.08, d=0.48]. Note, however, that the groupr

state interaction reached significance when depression

was not entered as a covariate [F(1, 35)=8.15, p=0.007,

g2p=0.19]. This latter finding suggests that depression

modulates positive responsiveness to food pictures in

AN patients. There was no main priming effect, and

no significant interaction effects between priming and

the other factors. Of interest, the group effect on

zygomatic activity persisted after entering the hunger

score as a covariate [F(1, 33)=4.85, p=0.034, g2p=

0.128], suggesting that differences in motivational state

between both groups of participants are not sufficient

to explain the lower zygomatic activity to food

pictures in AN patients.

Autonomic reactivity

SCR changes

The ANCOVA yielded only a main priming effect

[F(3, 111)=3.15, p=0.03, g2p=0.08], revealing that,

while the participants viewed foodpictures, subliminal

0.03

0.02

0.01

–0.01

–0.02

–0.03

–0.04

0

Dis Hap Neu Fea Dis Hap Neu Fea

*

*

**

log

µV

Hunger Satiety

Fig. 3. Mean electromyography (EMG) amplitudes and

standard errors bars of corrugator muscle reactivity to food

pictures primed by the subliminal presentation of emotional

facial expressions (Dis, disgust ; Hap, happy ; Neu, neutral ;

Fea, fear) during the hunger and satiety sessions in anorexic

(AN; –––) and healthy control (HC; – – –) participants

(* p<0.05).

AN HC

0.017

0.012

0.007

0.002

0

–0.003

log

µV

*

Fig. 4. Mean electromyography (EMG) amplitudes and

standard errors bars of zygomatic muscle reactivity to food

pictures in anorexic (AN) and healthy control (HC)

participants (* p<0.05).

8

7

6

5

4

3

2

1AN HC AN HC

Hunger Satiety

***

***

Fig. 2. Mean ratings of self-reported desire (wanting) and

standard errors bars in response to food pictures during the

hunger and satiety sessions in anorexic (AN) and healthy

control (HC) participants (*** p<0.001).

Unconscious fear in anorexia nervosa 7

fear and happy primes elicited a higher increase in

SCR than did the neutral primes (all p<0.05) (Fig. 5).

HR changes

HR was not affected either by motivational state,

group or priming factors, or by their interactions.

Both AN and HC groups evinced an overall decrease

in HR in hunger (AN: x0.40¡0.56, HC:x0.57¡0.43)

and satiety states (AN: x0.17¡0.60, HC: x0.65¡47),

suggesting an orienting response to food pictures in all

participants.

Videotaped facial behavior

Smiling

The ANCOVA revealed a main effect for group

[F(1, 34)=4.31, p=0.045, g2p=0.15] and state [F(1, 34)=

9.03, p=0.005, g2p=0.21]. HC subjects smiled signifi-

cantly more than AN patients while viewing food

pictures (0.61¡0.11 v. 0.18¡0.15, d=0.78) and the

frequency of smiles was higher during hunger

(0.58¡0.22) than during satiety (0.21¡0.16) sessions.

There was no significant difference in the frequency of

smiles as a function of primes. Controls also displayed

more smiles than AN participants during the pre-

prandial condition when the hunger level was entered

as a covariate [F(1, 34)=7.51, p=0.009, g2p=0.18], sug-

gesting that differences in the motivational state did

not account for the higher positive facial behavior to

food pictures in the HC than in the AN group.

Negative facial expressions

When the participants were presented with food pic-

tures, no main effects of state, group and priming or

interaction effects of priming and the other factors

were noted with this variable.

Discussion

This research aimed to explore the value of a positive

incentive theoretical framework to further clarify

psychological processes underlying salient symptoms

in anorexia, such as the decline of appetite and food

restriction. More specifically, we investigated hedonic

reactivity to food pictures in AN, and the potential

influence of unconscious emotional processes on the

low sensitivity to the positive reinforcement of food

that characterizes this eating disorder. To reach this

objective, the following issues were addressed.

Do measures of hedonic processing differentiate

between AN and HC women?

Our findings provide clear evidence that both subjec-

tive (verbal ratings) and bodily (facial EMG activity,

videotaped facial expressions) measures of affective

processes induced by food pictures discriminate AN

patients from HC subjects. On the one hand, AN

women reported similar hedonic ratings to food pic-

tures (next to neutrality) during hunger and satiety

whereas the controls declared higher pleasure when

hungry than when sated. Additionally, in both pre-

and post-prandial states, the AN group rated the sight

of food pictures as less pleasant than did the HC

group. Thus, regardless of current interoceptive sig-

nals of hunger/satiation, the present findings confirm

a decline in the positive incentive value of foods in AN

women, in line with the findings in a recent neuro-

imaging study (Santel et al. 2006). On the other hand,

facial measures of positive affect also evidenced a dif-

ferential pattern of responsiveness. Compared to HC

participants, AN patients exhibited lower zygomatic

muscle activity and expressed fewer smiles in re-

sponse to food pictures. This convergence of both im-

plicit and explicit measures of hedonic processing

supports the robustness of our data, and excludes ex-

planations based on social desirability or disturbances

in the accurate perception of internal states in AN

(Garfinkel, 1974). It may be noted that lower declared

pleasure and positive facial behavior in AN do not

simply reflect a difference in prandial state because all

participants obtained higher hunger scores before

than after lunch, and the differences between both

groups persisted after controlling for hunger ratings.

Thus, these findings give credit to the hypothesis of

a diminished capacity to express and experience

pleasure in AN persons while viewing foods, which

could be causal in reduced intake (Davis & Woodside,

2002). This is in accordance with a prior study in AN

0.15

0.10

0.05

0.00Disgust Happy Neutral Fear

*

*

µS

Fig. 5. Mean amplitudes of skin conductance response (SCR)

and standard errors bars to food pictures primed by the

subliminal presentation of emotional facial expressions in

all the participants (* p<0.05).

8 R. Soussignan et al.

patients that used reaction time as an indicator of im-

plicit processes in an affective priming paradigm

(Roefs et al. 2005). The AN group was slower in re-

sponding, suggesting less sensitivity to the palatability

of foods than controls. However, our finding is not

entirely consistent with those of another study using a

startle eyeblink modulation paradigm to gauge ap-

petitive and aversive responses in eating disordered

patients (Friederich et al. 2006). In this study, AN per-

sons showed an EMG startle response to food pictures

that was not significantly different from healthy con-

trols. This lack of difference, which was not in favour

of a dysfunctional appetitive system in AN, may be

due to the lack of subjective (e.g. pleasantness ratings)

or facial (i.e. zygomatic activity) measures of positive

affect, or to several possible biases (e.g. restricting and

purging AN subtypes regrouped, food intake prior to

the experiment not monitored, depression not used as

a covariate) in the Friederich et al. study.

Do subliminal primes influence subjective and

psychophysiological reactivity to food pictures in

AN and HC participants?

The major finding of our study is the differential im-

pact of subliminal fear primes on negative facial EMG

reactions in AN and healthy women. Namely, the

unconscious perception of fear expressions potentiated

the corrugator muscle responses to food pictures

during the hunger state in AN patients only. This

suggests that a social display signaling a potential

threat/danger, which operates outside phenomenal

awareness and controlled processes, can influence an

implicit measure of negative emotion in AN patients

viewing palatable food pictures during a motivational

state (hunger) that usually generates a positive affect

in healthy controls. By contrast, the effect of subliminal

fear primes on corrugator activity was lower in hun-

gry than in sated HC participants. This result is in line

with the positive incentive theory that predicts that an

affective prime presented during a congruent motiva-

tional state facilitates responses to target stimuli.

However, contrary to our prediction, no subliminal

prime effect of the happy faces on zygomatic muscle

activity was found in hungry HC participants. This

did not reflect unresponsiveness to the happy primes

because an increase in the SCR, an indicator of sym-

pathetic arousal, was evidenced in all participants

subliminally exposed to happy faces. Moreover, in all

participants the impact of subliminal fear expressions

on this autonomic measure was higher than the impact

of the other primes. This suggests that valence

(indexed by facial EMG) and arousal (indexed by SCR)

dimensions of affective processes may be dissociated

in AN patients and HC subjects, and partly reflects the

influence of motivational state. Although we have

no clear explanation for the lack of priming effect

of happy faces on an implicit measure of affective

valence, the following proposal may be suggested.

A ceiling effect cannot be ruled out because the food

stimuli induced both a high level of self-reported

pleasure and positive facial behaviors in the controls

during the pre-prandial condition. Thus, it cannot be

excluded that an affective prime potentially interferes

with the strength of affective valence of a target,

accounting for the ongoing facial muscular activity. It

is interesting to note that previous studies using the

backward-masking technique in healthy participants

demonstrated priming effects on zygomatic EMG

activity when the happy faces were associated with

either neutral targets (Rotteveel et al. 2001) or no target

at all (Dimberg et al. 2000). Further research is needed

to clarify this issue.

An unexpected finding of the present study is the

lack of priming effect for the subliminal facial expres-

sions of disgust. Neither psychophysiological nor

subjective evidence was found that the participants

reacted strongly to the covert presentation of disgust

faces when they were associated with food pictures.

Thus, our findings suggest that fear primes are more

powerful than disgust primes to influence arousal and

valence dimensions of affective processes and to dis-

criminate AN from controls. This could be explained

by the fact that fear, as a salient feature in AN

(DSM-IV; APA, 1994), is probably a potent emotion

that influences food restriction.

It can be hypothesized that the fear priming effect

evidenced here probably reflects the involvement of

brain structures, such as the amygdala, that are crucial

for mediating autonomic and behavioral responses to

the threat value of stimuli (Ledoux, 1996 ; Ohman et al.

2007), with attention and awareness having little im-

pact on its reactivity to fear expressions (Whalen et al.

1998 ; Pegna et al. 2005 ; Ohrmann et al. 2007).

Exaggerated amygdala responses may also be induced

by masked presentation of fearful faces in patients

with post-traumatic stress disorder, suggesting that

affective upheavals might lead to an amygdalian hy-

persensitivity to potentially harmful stimuli (Rauch

et al. 2000). A tentative interpretation related to AN

symptoms would be that an irrational fear of food

intake/weight gain, resulting from the amygdalian

hyperactivation, would negatively influence the ap-

praisal of food cues. It can be noted that the supra-

liminal presentation of a high caloric drink to AN

patients has been shown to produce a ‘caloric fear ’,

with activation of limbic/paralimbic regions (i.e.

amygdala, insula, anterior cingulate gyrus) (Ellison

et al. 1998). This leaves the possibility that structures

such as the amygdala react automatically to food

Unconscious fear in anorexia nervosa 9

stimuli evaluated as threatening by AN people.

Additional studies are required to test this hypothesis

in AN individuals exposed to food cues primed by

subliminal fear and disgust faces in using both func-

tional magnetic resonance imaging (fMRI) and back-

ward masking techniques.

Are subjective measures of liking and wanting

dissociated in AN patients?

Our results revealed that subjective measures of desire

(wanting) and pleasure (liking) of food stimuli were

partially dissociated in AN patients as compared to

HC subjects. That is, whereas controls reported higher

wanting and liking scores for the visually presented

foods when hungry than when sated, AN patients ex-

pressed no food pleasure (next to neutrality) during

both states, although their desire or motivation to eat

a food was higher in the hunger than in the sated

condition. Although wanting and liking normally

work together, they can be split apart by neurochemi-

cal manipulations or under certain circumstances

(Berridge, 2004a). Available psychopharmacological

evidence on animal models indicates that both of these

food reward components are mediated by partially

separated brain substrates relying on dopamine or

opioid neurotransmission (Berridge, 2007). Our find-

ing of an apparent dissociation between liking and

wanting in AN patients is consistent with the view

that a lower capacity to experience pleasure than de-

sire to eat foods might be more involved in AN. This

issue should be addressed in future studies using

implicit measures of desire/motivation to eat (e.g.

reaction time to select foods). It further remains to

demonstrate whether candidate genes that have been

hypothesized to be involved in the susceptibility to

AN are differentially related to both components of

food reward. Polymorphisms in both opioid d receptor

(Brown et al. 2007) and D2 dopamine receptor genes

(Bergen et al. 2005) have recently been reported in AN

patients. Given the functional role of the dopamine

and opioid systems in desire and pleasure of foods,

studies using genotyping, neuroimaging and psycho-

physiological measures are needed to clarify the issue

of the differential involvement of these neurochemical

systems in the components of food reward in AN.

In conclusion, our psychophysiological study using

a backward masking paradigm emphasizes the heu-

ristic value of a positive-incentive framework for a

better understanding of some phenotypic features of

AN. First, in contrast to healthy controls, AN patients

did not display objective and subjective indices of

pleasure during the hunger state. Second, the experi-

ence of pleasure to food stimuli seemed to be more

affected than the desire to eat in AN. Third, we

provide the first evidence that unconscious fear cues

potentiated negative facial reactions to food stimuli in

AN patients. This leaves the possibility that a non-

controlled emotional mechanism might bias the ap-

praisal of alimentary cues and contribute to induce

food aversion in persons with AN.

Acknowledgments

We thank C. Serrano for installing the experimental

room, S. Martin for managing the participants during

the experiments, and N. Mutin for her highly effective

logistic and administrative support. We thank the

participants who made this research possible. This

research was funded by a grant from Conseil Regional

de Bourgogne (to T.J.) and by the Centre National de la

Recherche Scientifique.

Declaration of Interest

None.

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