Impaired disgust processing following left posterior insular and SII cortices lesion

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Impaired emotional processing in a patient with a left

posterior insula-SII lesion

Journal: Neurocase

Manuscript ID: NCS-OA 11-072.R1

Manuscript Type: Original Article

Date Submitted by the Author: n/a

Complete List of Authors: BORG, CELINE; CHU NORD Saint-Etienne, Neuropsychology/neurology Bedoin, Nathalie; UMR CNRS 5596, Peyron, Roland; INSERM U879, Bogey, Soline; CHU Saint-Etienne nord, laurent, bernard; CHU Nord, Thomas-Anterion, C.; CHU Saint-Etienne nord,

Keywords: insula, emotion, disgust, implicit processing, explicit processing

URL: http:/mc.manuscriptcentral.com/nncs Email: [email protected]

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Impaired emotional processing in a patient with a left posterior insula-SII lesion

Running head: emotion and insula.

Céline Borg1, Nathalie Bedoin

2, Roland Peyron

1,3, Soline Bogey

1, Bernard Laurent

1, and

Catherine Thomas-Antérion1

1 Neurology/Neuropsychology, CMRR Unit, Hospital Nord, 42270 Saint-Priest-en-Jarez, France

2 Laboratoire Dynamique du Langage, UMR CNRS 5596 and University of Lyon 2, France

3 INSERM U879; University of Lyon; UJM St-Etienne, France

Corresponding author:

Céline Borg

Neurology/Neuropsychology, CMRR Unit

Hospital Nord

Avenue Albert Raimond

42270 Saint-Priest-en-Jarez, France.

Tel: +33 (0)477128882

Fax: +33 (0)477120543

E-mail: [email protected]

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Abstract

The present case-report investigated the influence of a lesion in the left posterior insula-SII

cortices on the processing of emotions. MB and 16 normal controls explicitly rated the

valence and the intensity of both facial expressions and emotional words. In addition, they

had to perform a number comparison task and a lexical decision task without focusing their

attention on emotional components of stimuli. MB identified the valence of emotional words

as well as the control group. Nevertheless, she provided higher intensity scores for disgusted

words and her responses in the lexical decision task were significantly delayed for these

stimuli. In addition, MB’s response times were not differently influenced by the presence of

irrelevant emotional faces. However, she explicitly identified fewer facial expressions of

disgust and she assessed them as significantly less intense. This pattern of results contributes

to highlight the psychological and behavioural disorders observed after a left posterior insular

stroke.

Key words: insula, emotion, disgust, implicit processing, explicit processing.

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1. Introduction

Although the insula cortex is clearly associated with the processing of disgust (Calder, Keane,

Manes, Antoun, & Young, 2000; Hennenlotter et al., 2004; Jabbi, Bastiaansen, & Keysers,

2008; Krolak-Salmon, Hénaff, Bretrand, Mauguière, & Vighetto, 2006; Krolak-Salmon et al.,

2003; Phillips et al., 1997, 2004; Shapira et al., 2003; Sprengelmeyer et al., 1998; Stark et al.,

2007; Wicker et al., 2003), the specificity of its relation to the processing of this emotion is

debated. This cerebral area has been found to respond to other emotions such as fear, anger or

sadness (Damasio et al., 2000; Lane, Reiman, Ahern, Schwartz, & Davidson, 1997; Liotti et

al., 2000; Schienle et al., 2002). In a magnetoencephalography study, a strong activation has

been observed in the right insula 200 msec after the presentation of the stimulus, regardless of

whether it induced disgust or happiness. However, a second discriminative response occurred

about 350 msec after the stimulus, and it was stronger for disgust than for happy faces (Chen

et al., 2009). Therefore, it seems likely that the insula is specifically involved in disgust

processes, but it also seems crucial for a more general “interoceptive awareness” that may

contribute to decode our bodily states (Craig, 2009; Phan, Wager, Taylor, & Liberzon, 2002).

Accordingly, an anatomical posterior-to-anterior gradient has been described in the insula

cortex (Craig, 2009) from the primary interoceptive representations (posterior) to the ultimate

representation of one’s feeling (anterior).

Assuming that the insula contributes to the regulation of emotions, the present study

investigated a unique patient (MB) complaining about emotional disturbance after a brain

lesion involving the left posterior insular and SII cortices. The emotional dysfunction reported

by the patient in her daily life could be explained by the existence of two kinds of emotional

processes: integration and reactivity (Coan & Alleen, 2007; Levenson & Miller, 2007).

Emotional integration or explicit processing of emotions refers to elaborate responses

occurring at late post-perceptual stages and results from the explicit recognition of emotions

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in self and others. Impaired emotional integration is considered as inducing errors in the

identification and naming of facial or vocal expressions (Calder et al., 2000; Lavenu,

Pasquier, Lebert, Petit, & Van der Linden, 1999) or yet as generating a lack of self-conscious

emotions (Evers, Kilander, & Lindau, 2007). Emotional reactivity or implicit processing of

emotions is defined as a standardized and automatic reaction to unexpected emotional stimuli.

The finality of this automatic vigilance process is to provide a defensive reaction and is

considered to interrupt the ongoing cognitive activity. Typically, emotional reactivity induces

a slowdown in response latencies when participants had to ignore the emotional content and

to explicitly direct their attention to other features of the stimulus. The classical methods that

have been used to assess this emotional bias are the emotional Stroop task and the lexical

decision task (e.g., Algom, Chajut, & Ley, 2004; Estes & Verges, 2008; MacKay et al., 2004).

Emotional reactivity increases response times when the central task is performed in the

context of emotion inducing stimuli (particularly negative emotions), although the emotional

content has not to be explicitly processed (Larsen, 2009; Vuilleumier, 2002). Disturbance in

emotional reactivity may result in the increase or the disappearance of such a negative bias.

Therefore, emotional functioning encompasses explicit and implicit processes, which

may be differently impaired by specific pathologies. For instance, patients with fronto-

temporal dementia (FTD) produce intact physiological and behavioural responses in reaction

to emotional contexts. For instance, they correctly reacted to unexpected loud noises (Sturm,

Levenson, Rosen, Allison, & Miller, 2006). In contrast, they exhibited reduced performance

when the task explicitly required higher level of emotional processes. For example, they failed

to identify negative emotions (Rosen et al., 2004) and did not exhibit the usual signs of

embarrassment (e.g., nervous laughter, embarrassment smiling), which typically follow

irrelevant emotional reactivity (Sturm et al., 2006). In addition, Wieser et al. (2006) showed

that patients with Parkinson’s disease (PD) explicitly rated the emotional content of pictures

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as less exciting than healthy controls did. However, ERPs provided evidence for an automatic

reactivity to the emotional content of the pictures. Therefore, emotional deficits in patients

with PD may reflect blunted emotional responses, which could be partly due to disturbance in

executive functioning, whereas the automatic emotional sensitivity of the patients is spared.

In this research, we investigated the implicit and explicit emotional processes. We

used experimental tests to specifically assess each aspect of emotional processing for disgust,

fear and happiness, with the aim to characterize the consequences of a lesion in the left

posterior insula in MB. In accordance with the literature, we expected atypical emotional

effects of disgust, and deficiencies were also suspected regarding other emotions.

Additionally, this issue was addressed through both facial expressions and printed words.

Emotional responses could be genetically predetermined for facial expressions, but not for

words, which probably entail more sophisticated emotional understanding and higher cortical

processing. Therefore, in a series of experiments, we aimed to examine if MB shows selective

impairments from emotions conveyed by facial expressions and emotional words.

In order to investigate the explicit emotional functioning, participants were required to

indicate the valence of facial expressions and emotional words. Then, they had to rate the

intensity of the emotional content of the stimuli on a five-point scale. According to our first

hypothesis, the patient may be impaired in recognizing emotions, due to her lesion in the

insular cortex and to the crucial role for this cortical area in “interoceptive awareness” and

decoding of bodily states (Craig, 2009; Phan et al., 2002). This may reflect dysfunctions in

emotional integration. In other words, the percentage of incorrect responses especially in

labelling emotions was expected to be higher in MB than in control participants. In addition,

impaired emotional awareness may result in inaccurate explicit evaluation of the intensity of

emotions induced by the stimuli. Therefore, we also predicted that MB would rate emotional

stimuli as less intense than control participants.

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However, emotional reactivity can be spared in spite of obvious impairment of

emotional integration, for instance in fronto-temporal dementia with extreme self-neglect

(Bedoin, Thomas-Antérion, Dorey, & Lebert, 2009; Sturm et al., 2006; Werner et al., 2007) or

in PD (Wieser et al., 2006). In the present research, emotional reactivity was investigated by a

number comparison task in which participants had to compare two numbers and to ignore the

emotional facial expressions. In this condition, emotional processing could be considered as

implicit and automatic. We also used a lexical decision task in which participants had to

classify words and pseudo-words while ignoring the emotional content of the words. The

maintenance of emotional reactivity in the patient would result in longer response times for

stimuli with emotional content than for neutral stimuli in both experiments. In contrast, if MB

suffered from a decrease in emotional reactivity, response times should not differ between

emotional and neutral stimuli, contrary to the pattern of results in the control group. Finally, a

potential exaggerated emotional reactivity in MB could be reflected by an excessive slow

down in response times for emotional stimuli as compared to controls, because impaired

ability to modulate emotional reactivity.

2. Methods

All participants gave their written informed consent before participation and this research was

conducted in accordance with the Helsinki Declaration.

2.1 Case-report

At onset, this 36-year-old right handed patient (MB) had, on February 2007, an acute

idiopathic stroke in the left sylvian artery, with a right hemiparesia and a partial conduction

aphasia. MRI was performed two days later, showing a recent infarct located in the left

posterior insula and extended to the adjacent operculum, including SII. This lesion was unique

and of small size as shown on figure 1. However, on the delayed MRI the lesion appeared as

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bifocal, involving the posterior portion of the insular cortex and the lower and medial part of

SII.

(Figure 1 about here)

She was examined one year later in February 2008 at the University Hospital of Saint-

Etienne, France. She had a deficit of motor strength in the right hand, mainly for the

prehension of objects (Jamar scale equal 4 for the right and 22 for the left hand) and a right

hemianesthesia to warmth, heat, pinprick, including the right face. She had severe chronic

neuropathic pain with permanent spontaneous burning sensations, paresthesiae and electrical

discharges, mainly on the right upper limb. In addition, she had a severe allodynia with a

withdrawal reaction to brush, contact and non-noxious cold stimuli. She did not have any

disturbance for taste. She spontaneously reported emotional disturbance resulting in changes

in her behaviour: she was still able to identify emotions but she evaluated their intensity as

less intense compared with what she had been used to feel before her lesion. For example,

when she visited her family three months after the stroke, everybody was crying at the airport,

she understood her family’s emotion, but she was unable to feel happy herself, even though

she was able to correctly identify an emotionally happy situation. In the same way, she

realized that during the travel, her fear of takeoff disappeared and she was not affected by the

fact of leaving her five-year old son behind. She also reported a decrease of her libido and a

complete change of activity occurred with a compulsive drive to paint while she was never

interested in art before the stroke (Thomas-Antérion, Créac’h, Dionet, Borg, & Peyron, 2010).

MB’s overall cognitive abilities were normal with only minor executive and verbal

working memory dysfunctions (Table 1). A facial processing test battery (the Benton Facial

Recognition Test) was also administered. MB’s score indicated that she could successfully

process the perceptual features of faces.

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(Table 1 about here)

2.2. Controls

We compared MB’s performance with that of a control group of 16 healthy adult females,

who were matched for age (mean age: 29.8 years +/- 1.9).

2.3. Materials for emotional investigations

Behavioural symptoms were objectively assessed in MB with the IOWA Scale of Personality

Changes (ISPC, Barrash, Anderson, Jones, & Tranel, 1997; French translation from Juillerat

& Peter-Favre, 1999). This 7-level scale consists in 26 aspects of emotional behaviours and

personality. Actual behaviour (after the lesion) is compared with premorbid behaviour (before

the lesion) (Meulemans, Van der Linden, Seron, & Juillerat, 2000). A quotation of 3 points

corresponds to a “normal” behaviour and higher quotations suggest behavioural dysfunctions.

The ISPC contains four additional dimensions of control (avarice, manipulation, vanity and

behaviour of type “A”) allowing to detect possible biases (e.g., exaggeration or minimization

of the troubles). The IOWA Scale of Personality was filled by a patient’s family member

before carrying out experiments with MB.

For the present study, we used photographs of facial expressions (happiness, fear,

disgust and neutral), most of them were taken from the standardized test battery (Nim

Tottenham, The MacBrain Face Stimulus Set, John D. and Catherine T. MacArthur

Foundation Research Network on Early Experience and Brain Development). The remainder

of the pictures came from a standardized battery elaborated by Baudoin (see Baudoin &

Humphreys, 2006). All photographs, 20 male and 20 female Caucasian actors, were adjusted

to the same size and presented on a white background. This assortment of pictures has been

previously validated in a pilot study conducted with 20 young adults to ensure that each

emotion was identified according to the batteries’ norms. Therefore, a first selection of facial

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expressions was made among 120 pictures (30 for each emotion): only those with a score of

identification that was shared by at least 80% of the participants were considered. Then, to

adjust the intensity of the emotions, we used a five level scale (1: low intensity to 5: high

intensity) and selected expressions with a similar score of intensity (mean intensity for

disgust: 3.5 (± 0.8); 3.5 (± 0.6) for fear; 3.3 (± 0.5) for happiness; 2.7 (± 0.2) for neutral

expressions).

We also used a set of 64 French words, which were divided into four emotional

valence conditions: 16 were pleasant (e.g., humour), 16 were fear-inducing (e.g., scary), 16

were disgust-inducing (e.g., spit) and 16 were neutral. Emotional and neutral words were

matched for lexical frequency from the data base BRULEX (Content, Mousty, & Radeau,

1990). The number of their letters, phonemes and syllables was also equated. Additionally,

the list contained 64 pseudo-words, which were paired with the words according to the

number of their letters, phonemes and syllables. The 20 participants of the pilot study for the

pictures were also required to categorize and evaluate the intensity of the emotions induced by

the words. As aforementioned for facial expressions, the same rule was used to select 16

words for each emotion among a data base of 120 emotional words (mean intensity for disgust

3.1 (± 0.5); 3.4 (± 0.6) for fear; 3.3 (± 0.3) for happiness; 1.7 (± 0.2) for neutral words).

2.4. Procedure

2.4.1. Explicit processing of emotion

The 40 facial expressions were displayed in a pseudo-randomized order in one block and the

64 words in another block. The order of presentation of the blocks was counterbalanced

between participants. The same timing and sequence of events was used for words and

pictures. Each target was preceded by a fixation cross during 500 msec and lasted until the

participant’s response. Firstly, the participant indicated the valence of the stimulus by

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choosing one of the proposed labels: happiness, fear, disgust, neutral or “others” (i.e., anger,

surprise…). Then, the participant rated the intensity of the emotional content of the stimulus

on a five-point scale. The list of labels and the scale remained on the screen until the response.

In order to exclude an experimental bias, this explicit task was systematically performed after

the implicit experiments had been completed.

For the explicit task, we carried out analyses on the percentages of correct valence

identification of emotional faces and words and on the mean intensity rating scores. The case-

controls comparisons were carried out using the Q’ test (Michael, 2007; Michael, Garcia,

Bussy, Lion-François, & Guibaud, 2009), with the sole factor being the tested valence

(disgust, fear, happy and neutral items). The Q’ test offers the possibility to investigate the

main effects and interactions by comparing a single case with the control group. This test

requires the transformation of the mean percentage of correct responses and the mean scores

of each condition into z values on the basis of the mean and SD of the controls and the

submitting of the corresponding points to estimate an analysis of proportions.

2.4.2. Implicit processing of emotions with a number comparison task

The same pictures of facial expressions as in the explicit experiment were used here.

Two digits were displayed 18 cm far from each other, one on the right and the other on the

left side of the screen. Each trial started with a centred fixation point displayed for 500 msec

and immediately followed by the presentation of a facial expression at the center of the

screen. The digits were displayed on either side of the picture 100 msec later. Participants

were instructed to focus on the digits and to detect the largest by pressing the corresponding

right or left key. They were asked to perform the task as quickly and accurately as possible

and had no instructions regarding the facial expressions. The inter-stimulus-interval (ISI) was

1500 msec.

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2.4.3. Implicit processing of emotions with a lexical decision task

The same words as in the explicit experiment were used here. Each trial began with a

500 msec-centred fixation cross, immediately followed either by a letter string or a word.

Participants had to decide whether it was a word or a pseudo-word by pressing on the

corresponding button, as quickly and accurately as possible. The ISI was 1500 msec. The

assignment of the number comparison task and the lexical decision task as the first to be

performed was counterbalanced across participants.

As regard to the number comparison and the lexical decision tasks, we carried out

analysis on the response times (RT). RTs out of 2 standard deviations (SD) were excluded

from the analyses. Discarded trials accounted for less than 5% of the total number of trials, in

the control group as in the patient. The mean error percentage was not considered in the

analysis because it represented less than 2%. The case-controls comparison was carried out

using the Q’ test as aforementioned for the explicit task.

3. Results

3.1. The IOWA Scale of Personality Changes

According to the Wilcoxon test, significant differences appeared in 9 of 26 dimensions of the

IOWA scale (p < .05) for MB. The most striking changes were loss of sensitivity, lack of

resistance, impassiveness, mood changes, irritability, impulsiveness, and also the increased

risk to be easily overwhelmed and to feel emotions in an inadequate way (see table 2).

(Table 2 about here)

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3.2. Explicit processing task

3.2.1. Valence assessment

Facial expressions. The effect of the emotional valence significantly differed between MB

and the control group (Q’ (3) = 40.3; p < .0001), and it was mainly due to a selective

reduction of disgust identification by MB (Q’ = 4.4; p < .0001, Figure 2a). In addition,

multiple corrected q’ comparisons showed that the difference between neutral and disgusted

facial expressions was significantly higher in MB than in controls (q’ = 4.04; p < .001).

Finally, differences between disgusting facial expressions and fear-inducing or pleasant

expressions were also significantly higher in MB than in the control group (respectively, q’ =

6.17; p < .0001 and q’ = 5; p < .0001). In other words, MB was specifically impaired at

recognizing disgust from facial expressions, compared with the controls.

Emotional words. The performance pattern of MB was not significantly different from that of

the control group. MB judged the valence of words as well as the control group.

3.2.2. Intensity assessment

Facial expressions. Intensity rating differed significantly between MB and the control group

(Q’ (3) = 19.69; p < .0002, Figure 2b). The patient scored the facial expressions of disgust (Q’

= 4.45; p < .0001), fear (Q’ = 4.45; p < .0001) and happiness (Q’ = 4.45; p < .0001), as less

intense than controls, while intensity scores were normal for neutral expressions as compared

to controls. Specifically, and compared with controls, a significantly larger decrease in the

intensity score appeared between neutral expressions on the one hand, and happiness, disgust,

or fear expressions on the other hand (respectively, q’ = 4.29; p < .0001, q’ = 4; p < .001, q’ =

4,07; p < .001).

Emotional words. The effects of emotional intensity differed between MB and the control

group (Q’ (3) = 25.97; p < .001, Figure 2c). The intensity of disgust elicited by words was

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judged as significantly higher by MB, than by the healthy controls (Q’ = 4.39; p < .0001). A

similar trend was observed for words suggesting fear and happiness but it did not reach

significance. Intensity scores were normal for neutral words as compared to controls.

Compared to all other emotions, disgusting words resulted in significantly higher intensity

scores in MB performances (disgust vs. neutral: q’ = 4.55; p < .0001, disgust vs. fear: q’ =

4.25; p < .0001, and disgust vs. pleasant: q’ = 5.03; p < .0001).

(Figures 2 a, b and c about here)

3.3. Implicit processing task: Number comparison task

No significant effect of facial expression was observed on MB’s RTs, nor on the RTs of the

control group. Precisely, negative and pleasant pictures did not slow down reaction times

when participants had to detect the highest digit by pressing the corresponding key.

3.4. Implicit processing task: Lexical decision task

The effect of emotional words was significantly different in MB and in the control group (Q’

(3) = 31.44; p < .0001). MB was significantly longer to respond than the control group,

whatever the emotional word (p < .002, Figure 3). However, post hoc multiple corrected q’

comparisons revealed that the specific pattern of MB’s results was mainly due to delayed

responses for disgust-inducing words as compared with neutral (q’ = 4.04; p < .001), fear-

inducing (q’ = 2.96; p < .03) and pleasant (q’ = 4.04; p < .001) words. Therefore, MB mainly

differed from the control group by exhibiting greater reactivity to disgust than to other

emotions elicited by the semantic content of words.

In addition, an analysis of variance was performed on correct RTs of the control group

with the emotion factor (disgust, fear, happy and neutral) as the within-subjects factor and

revealed a significant effect of emotion, F(3,45) = 10.45, p < .0001. Post hoc comparison

showed that RTs were longer in the disgust condition (712 ms) than in the neutral condition

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(664 ms); This suggests that disgusting words induce emotional reactivity in healthy controls,

even if this bias is less important than in MB.

(Figure 3 about here)

4. Discussion

MB felt a decrease in her emotional feelings, but she did not suffer from abnormalities

in social interactions and she had no frontal lobe dysfunction. The ISPC score confirmed

emotional changes in the fields of irritability, impulsiveness, lability, fatigability,

insensitivity, impassiveness, and pointed out inadequate emotions, which was consistent with

her post-stroke complaint. We investigated these changes by using tasks, which assessed

explicit and implicit processing of various emotions. Taken together, the results of our study

provided arguments for MB’s selective deficit in emotional processing, since the

abnormalities did not concern the recognition of neutral facial expressions and neutral words

but only the emotional ones.

Firstly and as it was suggested, MB was impaired in explicit identification of disgust

from facial expressions, while she did not differ from the control group in identifying this

emotion from the content of words. The involvement of the insula in the processing of facial

expression of disgust has largely been reported (Calder et al., 2000; Hennenlotter et al., 2004;

Jabbi et al., 2008; Krolak-Salmon et al., 2003, 2006; Phillips et al., 1997, 2004; Suzuki,

Hoshini, Shigemasu, & Kawamura, 2006; Wicker et al., 2003). The dissociation observed

between the understanding of disgusted facial expressions and the recognition of disgust from

the semantic content of words is consistent with the neuropsychological study of a patient,

NK, whose brain injury affected the anterior and posterior insula cortices and the putamen

(Calder et al., 2000). NK successfully identified emotions from pictures of scenes, involving

both verbal and non-verbal processing, but he was impaired in recognizing disgust from faces,

and he incorrectly labelled this emotion when it was conveyed by non-verbal emotional

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human sounds or prosodic cues. Accordingly, it appears that a selective impairment in the

identification of social cues of disgust extracted from facial or prosodic speech signals could

be associated with a lesion of the posterior insula. Contrary to the understanding of the

semantic content of emotional words, the understanding of facial emotions may be

phylogenetically predetermined, which may entail the involvement of specific cerebral areas

and produce a selective deficit of emotional integration of facial expressions.

Secondly and as it was hypothesized, MB assessed every expression of emotion as less

intense than the control group did. According to MB’s scores in the valence assessment task,

the decrease in her explicit sensitivity to facial expressions cannot be attributed to the inability

to identify them (except, perhaps, in the case of disgust). She may rather suffer from a general

impairment in interoceptive awareness and had difficulties in evaluating bodily states

associated with emotion feeling, a problem which has been attributed to cerebral damage to

the insula (Craig, 2009; Phan et al., 2002). As expected, cerebral lesion of the insula produces

major, but not exclusive, impairment in disgust processing. Other studies have similarly

reported deficits in the processing of various facial expressions after lesions in SI, SII and

insular areas (Adolph, Damasio, Tranel, Cooper, & Damasio, 2000), that is consistent with the

selective lesions of MB. In addition, a body of studies recently showed that the insula is

involved in the integration of various emotions (Chen et al., 2009) and in the representation of

“interoceptive states” (Craig, 2009). It is finally possible that MB’s neuropathic pain plays a

role in modifying her “interoceptive” sensitivity since the integrity of the somatosensory

system may contribute to the process of facial emotions. For example, a relation between the

intensity of the sensorial deficiencies and the extent of the impairment in recognizing facial

expressions has been documented elsewhere (Olausson et al. 2002). If the sensitivity to facial

expressions partly depends on the ability to simulate the body state associated with the

expression of this emotion, then the integrity of the somatosensory system is decisive for the

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recognition of facial emotions (Keysers et al., 2004). MB’s sensory deficit was not strong

enough to prevent her from identifying facial expressions, but it could be important enough to

attenuate the mechanism of simulation and reduce the intensity of her feelings.

Previous results raise the question of whether alexithymia can explain MB’s inability

to feel different emotions. Functional neuroimaging studies showed that insula is a brain

region associated with alexithymia (e.g., Karlsson, Näätänen, & Stenman, 2008; Reker et al.,

2010) and a deficit in interoceptive awareness has been described in alexithymic individuals

(Herbert, Herbert, & Pollatos, 2011). Furthermore, previous studies have suggested that

alexithymic individuals process facial expressions differently from non-alexithymic

individuals (e.g., Pandey & Mandal, 1997; Parker, Prkachin, & Prkachin, 2005; Taylor &

Bagby, 1988). Therefore, the question whether MB presents an alexithymia can be discussed.

Clinically, it is essential to specify that alexithymic individuals are characterized by an

inability to find words to describe feelings or emotions. When they talk about an emotional

situation, their comments are limited to describe an overall impression of their feelings.

Experimentally speaking, even if alexithymia is associated with impaired verbal and non

verbal recognition of emotional stimuli (Lane et al., 1996), studies strongly suggested an

important role of verbal ability on emotional recognition in alexithymia (Kokkonen et al.,

2003). From a clinical point of view, MB fails to feel if she was sad, disappointed, angry or

guilty but she correctly identified and distinguished emotional situations by verbally

expressing them with a rich vocabulary. Besides, in the present study, MB identified the

correct valence of stimuli (except disgust), regardless of the nature of the stimuli, words or

facial expressions. In addition, she correctly rated the intensity of emotional words, certainly

because she based her responses on semantic cues to properly assess emotion. Knowledge

about emotional events can be derived directly from experience, or indirectly, from general

knowledge. On the contrary, facial expressions brought no semantic cues so that MB tended

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to assign them a low intensity, since she did not feel, herself, the intensity of emotions. MB

seemed to have no physical sensations but she was still able to verbally associate relevant

emotions to events. In addition, alexithymia is an inability to associate one's visual

representations, thoughts and fantasies with a specific emotion. In contrast, MB had rich and

emotional fantasies. She began to paint six months after her stroke. She had never before nor

drawn or painted and had no interest in art. She was, however, a hairdresser with a

specialization as a colorist and loved fashion. She therefore went to buy canvases, brushes and

oil paints and painted her first picture that was reproduced in the paper of Thomas-Antérion

(2009). The composition of her paintings is very rich with a combination of colors and she

varies the themes. Today, she continues to paint. She can paint while emotionally, she feels

blunted. Nevertheless, she finds physical sensations while she paints (Thomas-Antérion,

2009). From all these strong arguments, we cannot conclude that MB is alexithymic.

Regarding the processing of words, we observed two anomalies in MB’s performance.

She explicitly judged disgusting words as more intense than the controls. This result suggests

an atypical increase in her sensitivity to the intensity of this emotion. This effect cannot be

ascribed to lower understanding of the semantic content of words, since the patient did not

differ from the controls in the explicit identification of emotions from words. Nevertheless,

the overestimation of intensity for disgust-inducing words by MB is consistent with the

observed effect exerted by this emotional content on her lexical decisions. In other words, one

of our main results was MB’s very high reactivity to the emotional content of disgusting

words, which yielded delayed responses for these words in the lexical decision task. Such a

result provides evidence for the preservation of emotional reactivity, in spite of difficulties in

regulating the magnitude of emotional responses. Theories of emotion processing suggest that

negative stimuli automatically attract more attention than neutral stimuli (e.g., Carretié et al.,

2001; Huang & Luo, 2006; Smith et al., 2003). This emotional bias is revealed by slower

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responses to negative-inducing stimuli in several cognitive tasks, such as the lexical decision

task (e.g., Algom et al., 2004; Estes & Verges, 2008). This pattern of results was replicated

here in the control group, and it was very pronounced in MB. This means that the patient

reacted to disgust, but with atypically high intensity, which suggests deficiencies in the

emotional regulation of reactions to disgusting words. Unfortunately, we cannot infer any

conclusion about MB’s emotional sensitivity to facial expressions from performance in the

number comparison task, since we failed to show any reactivity to emotions in this task both

in the controls and in the patient (see Pessoa, McKenna, Gutierrez, & Ungerleider, 2002).

Is the role of the insula restricted to the processing of disgust? This issue could depend

on the processing level (emotional reactivity and integration), which is required by the

situation. The present case-report may contribute to the literature on cognitive/behavioural

changes after small brain injury. It confirms the role of the posterior insula-SII in explicit

evaluation of the intensity of emotions expressed by faces, in understanding the social cues

for disgust, and in regulating reactions to this emotion when conveyed by words. It also

provides new evidence for the independence of these emotional mechanisms. These results

are consistent with the emotional changes experienced by MB in social life. Her impairment

in understanding and regulating emotions conveyed by faces could partly explain the changes

that she described in family meeting, her deficit in empathy, and her difficulty in evaluating

the signs of her own feelings. These feeling states are sometimes assumed to involve the

representation of bodily responses. The imbalance of MB’s sensitivity to the intensity of

emotions may be partly associated with the modification of her somatosensory system and her

internal bodily responses.

Conflict of interests and financial support

The authors have declared that no conflict of interest exists. The present research protocol has

received no financial support.

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Table 1. MB’ s performances in several neuropsychological tests.

Tests Scale Cutt-off

Mini Mental State 30/30 <27

Token test 32/36 <27

Naming of pictures 78/80 <76

Verbal fluency (category) 25 <21

Benton Facial Recognition 49/54 < 43

Verbal fluency (letter P) 20 <9

Words reading (MT 86) 33/33 <32

Writing to dictation 32/34 <28

Words repetition 33/33 <30

Words comprehension 9/9 <9

Sentences comprehension 32/34 <30

Digit span 4 <5

Digit span forward 3 <5

Visual span 7 <5

Trail Making test A (time) 29 >53

Trail Making test A (errors) 0 0

Trail Making test B (time) 69 >138

Trail Making test B (errors) 0 0

Interference Stroop 41 >76

Six elements Test 6 >2,1

Wisconsin Card Sorting Test (categories) 6 < 5

Wisconsin Card Sorting Test (errors) 2 >9,9

Wisconsin Card Sorting Test (perseverations) 0 >3,7

FCSRT free recall 31/48 24

FCSRT total recall (free and cued recall) 48/48 42

Visual recognition (DMS 48 ; set 1 and 2) 48/48 47

WAIS similarities 13/19 10

Hamilton scale 3 12

DO 80: Naming 80 pictures; MT 86: Montreal-Toulouse 86; FCRST: Free and Cued Selective Recall

Reminding Test; DMS 48: Delayed Matching Sample 48; WAIS: Weschler Adult Intelligence Scale; ISPC:

Iowa Scale of Personality Changes.

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Table 2. Exploration of emotional and behaviour disturbances by means of the IOWA Scale of Personality

(ISPC): items presenting in bold and with ** represent the most significant changes.

items Now Before Change

Irritability ** 6 1 5

Lack of initiative 1 1 0

Perseveration 1 1 0

Depression 3 1 2

Impulsiveness ** 5 1 4

Mania 5 5 0

Moody character ** 5 2 3

Lack of persistence 1 1 0

Lack of resistance ** 5 1 4

Abilities of planning 2 1 1

Obstinacy 1 1 0

Abilities of judgement 1 1 0

Anxiety 4 2 2

Insensitivity ** 7 2 5

Social behavior 1 1 0

Dependence 2 1 1

Impatience 3 3 0

Behavior of type « A » 6 3 3

Impassiveness ** 7 1 6

Social withdrawal 3 1 2

Aggressiveness 3 1 2

Indecision 1 1 0

Vanity 1 1 0

Mistrust 1 1 0

Apathy 1 3 2

Avarice 1 1 0

Inadequate emotions ** 7 1 6

Manipulation 5 5 0

Risk to be overwhelmed ** 5 1 4

Conscience of troubles 3 3 0

Total 97 50 52

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a. Diffusion weighted MRI showing the lesion in the posterior third of the left insular cortex (lower slices), with an extension to the parietal operculum including SII, in its lower and medial portion (upper slices). b & c. A delayed 3D-high resolution MRI (radiological convention) showing the residual lesions in the

posterior third of the left insular cortex (b, red circles), and in the parietal operculum including SII, in its lower and medial portion (c, yellow circles). Please note that on coronal sections the residual two lesions are

not contiguous but separated by apparently normal tissue. 81x60mm (300 x 300 DPI)

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Overall performances of MB, by comparison with normal controls, on the explicit facial expressions recognition showing (a) correct responses in percentage, (b) the mean score of intensity for faces

expressing disgust (DI), fear (FE), happiness (HA) and neutral items (NE) and (c) the mean score of

intensity for words. Variability (mean SEs) appears for the four conditions in the control group. 177x311mm (300 x 300 DPI)

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Mean response times of MB and controls in the lexical decision task for words expressing disgust (DI), fear (FE), happiness (HA) and for neutral items (NE). Variability (mean SEs) appears for the four conditions in

the control group. 62x38mm (300 x 300 DPI)

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Impaired disgust processing following left posterior insular and SII cortices lesion