Disgust Processing Research Articles

Altered Insula Response to Sweet Taste Processing in Recovered Anorexia and Bulimia Nervosa: a Matter of Disgust Sensitivity?

To the Editor: In the June issue, the Journal published aninteresting study on recovered anorexia nervosa and bulimianervosa (1). The authors of this research used sweet tastes,with (sucrose) and without (sucralose) caloric content, to in-terrogate gustatory neurocircuitry involving the anterior insulaand related regions that modulate sensory-interoceptive-rewardsignals in response to palatable foods. In particular, the rightanterior insula response to sucrose was diminished in anorexianervosa and exaggerated in bulimia nervosa relative to com-parison subjects.This abnormal insula response associated with the ex-posure to sweet compounds led the authors to concludethat there may be a failure to accurately recognize hungersignals. This conclusion is consistent with the suggestionthat an altered interoceptive awareness may be a pre-cipitating and reinforcing factor in both populations, al-though this altered awareness leads to antithetical feedingbehaviors.The neural pattern observed by the authors suggestsanother, not mutually exclusive, interpretation of the result,whichreferstothehypothesisofanaltereddisgustsensitivity.AssuggestedbyChapmanandAnderson(2),disgustmaybeparticularly strongly associated with visceral changes, consis-tent with its apparent origins in defending against the ingestionof contaminated foods. Given the key role of the anteriorinsula in interoception (3) and disgust processing (4), onecould argue that the reported abnormal activity of this neuralregion in response to sweet tastes may reflect an altereddisgust processing at the visceral level.Thissuggestionissupportedbyresearchexamining disgustsensitivity in these clinical populations before recovery. Forexample, Aharoni and Hertz (5) reported that anorexia nervosapatients scored consistently higher on all domains of disgustsensitivity,with a particularregard to the fooddomain. Moreover,Troop et al. (6) reported higher levels of disgust sensitivity tofood in bulimia nervosa. On the other hand, Houben andHavermans (7) reported lower disgust sensitivity in over-weight individuals.Given the evidence of this relationship between disgustsensitivity and feeding behavior, an assessment of disgustsensitivity could provide important clues for interpreting thepattern of neural activity reported by Oberndorfer et al. (1) intheanterior insulaof recovered anorexianervosa and bulimianervosa patients.References

Examining the relationship between lateralisation for processing emotional faces, depression, and sex

It is now relatively well established that the right hemisphere is specialised for processing facial emotion; however, there is variability in this pattern of lateralisation. One factor that has been examined is atypical lateralisation in individuals diagnosed with clinical psychological conditions. To date the evidence regarding the neuropsychological processing of emotional stimuli in individuals with depression is contradictory. In this study 160 participants completed the Beck Depression Inventory and the chimeric faces test, a test of lateralisation for the processing of facial expressions of each of the six basic emotions. A negative relationship between depression and lateralisation was found for females only, showing that women with higher depression scores tend to be less strongly lateralised to the right hemisphere, or even lateralised to the left hemisphere, for processing facial emotion. The strength of this relationship also varied across the different emotions with the clearest results for the processing of anger, disgust, and fear. There were no significant findings for males. The possible reasons for there being a sex difference in our findings and an attempt to reconcile the disparate findings within this area of research are discussed.

Perceiving disgust affects cortico-bulbar excitability. A TMS study

Perceiving disgust affects cortico-bulbar excitability. A TMS study

Morality and disgust: insights from obsessive compulsive disorder

A commentary on Neural correlates of moral sensitivity in obsessive compulsive disorder by Harrison, B. J., Pujol, J., Soriano-Mas, C., Hernandez-Ribas, R., Lopez-Sola, M., Ortiz, H., et al. (2012). Arch. Gen. Psychiatry 69, 741–749. In a recent issue of Archives of General Psychiatry, Harrison et al. (2012) provided the first evidence of neural correlates on moral sensitivity in Obsessive Compulsive Disorder (OCD), which is believed to be heightened in this clinical population. This study aimed to explore whether subjects with OCD showed increased ventromedial prefrontal and orbitofrontal cortex responses in a functional magnetic resonance imaging study of difficult moral decision-making. These brain areas were found to be active on healthy humans experiencing moral emotions such as indignation or moral disgust (see Moll et al., 2005 for a complete review). The results are striking in so far as they show that patients with OCD demonstrated significantly increased activation of the ventral frontal cortex, particularly of the medial orbitofrontal cortex. Moreover, significant positive associations were documented between the patients' DY-BOCS ratings of total symptom severity and the activation of the anterior insula (Harrison et al., 2012). The evidence from this study offers the opportunity to discuss two emerging related issues. First, it adds further support on a clinical model to the view that visceral and moral disgust share, at least in part, common neural and cognitive mechanisms (Jones, 2007). In fact, OCD is also characterized by an altered representation of disgust at sensory (Tsao and McKay, 2004) and affective (Shapira et al., 2003) level. Thus, their heightened moral sensitivity might reflect an enhanced disgust for immoral outcomes. This hypothesis is supported by previous evidence coming from neuroimaging studies. For instance, an overlapped recruitment of ventromedial prefrontal and orbitofrontal cortices have already been reported during the processing of both sensorial and moral disgust (Moll et al., 2005). A similar result was announced for the insula. For example, Wicker et al. (2003) have discovered that the anterior insula was activated both during the observation of disgusted facial expressions and during the feeling of disgust evoked by unpleasant odors. Moreover, Sanfey et al. (2003) found an activation of this region in healthy subjects who received unfair monetary offers, which are known to elicit moral disgust. All these findings suggest that, the heightened moral sensitivity in OCD can be grounded on the same neural mechanisms responsible for their altered sensitivity to outcomes which can induce sensory and emotional disgust (Shapira et al., 2003; Tsao and McKay, 2004). Another remarkable aspect deserving some discussion is that OCD participants were not different from healthy control subjects in the subjective rating of the moral dilemmas, despite the difference reported in neural activation. This result, which probably argues some distinction between the patients' increased neural responses and their perceived emotional experience during a moral dilemma (Harrison et al., 2012), can be discussed calling into question the interoceptive awareness which might be deranged in this clinical population. This suggestion is supported by the recent evidence of a negative correlation between interoception and anxiety (Pollatos et al., 2009), which is known to affects OCD. Moreover, Zaki et al. (2012) have recently found a common cluster of activation for interoception and emotional experience in the anterior insula, a region clearly deranged in this clinical population (Song et al., 2011).

Voxel-based morphometry of disgust proneness

This voxel-based morphometry study investigated whether the personality trait disgust proneness is associated with gray matter volume (GMV) of distinct brain regions implicated in disgust processing. We analyzed brain structural data from 99 healthy women, who had rated their tendency to experience disgust for different disgust domains (offensive food, death, poor hygiene, decay, and body secretions). Food-related disgust proneness was positively correlated with insula volume. The disgust domains decay and death showed negative correlations with GMV of the dorsomedial and the dorsolateral prefrontal cortex (DMPFC, DLPFC). Our data implicate that only core disgust shows an association with the GMV of the gustatory cortex, whereas the reactivity to other disgust areas is linked with cognitive control areas.

Differential effects of escitalopram challenge on disgust processing in obsessive–compulsive disorder

Introduction Literature on the ability of patients with obsessive–compulsive disorder (OCD) to recognize static facial expressions of disgust is not consistent. We aimed to investigate whether OCD is associated with deficits in the recognition of disgust in a dynamic task, and if so, whether the acute administration of the selective serotonin reuptake inhibitor (SSRI) escitalopram would result in the normalization of such deficits. Methods OCD patients ( n = 20) and matched healthy controls ( n = 20) received a single dose of escitalopram 20 mg on one day, and a single dose of placebo on another day, in randomized order, under double-blind conditions. Accuracy (i.e. the percentage of correct answers) and sensitivity to disgust stimuli (defined as the lowest level of emotional intensity expressed on the photo image after which no errors were made in the recognition of disgust for subsequent trials of increasing intensity) were compared in OCD patients and controls, with a repeated measures analysis of variance using a mixed model approach. Results On placebo, the accuracy of, and sensitivity to, disgust stimuli were similar across groups. OCD patients had more accurate and more sensitive recognition of disgust after acute SSRI administration than after placebo, while controls had less accurate recognition and less sensitive recognition of disgust after acute SSRI administration than after placebo. Conclusions The use of a dynamic facial recognition task demonstrated altered responses to disgust in OCD patients compared to healthy controls after a pharmacological challenge with escitalopram. These findings suggest that the serotonergic system plays a role in disgust recognition.

Facial Affect Processing in Patients Receiving Opioid Treatment in Palliative Care: Preferential Processing of Threat in Pain Catastrophizers

Context As a multidimensional phenomenon, pain is influenced by various psychological factors. One such factor is catastrophizing, which is associated with higher pain intensity and emotional distress in cancer and noncancer pain. One possibility is that catastrophizing represents a general cognitive style that preferentially supports the processing of negative affective stimuli. Such preferential processing of threat—toward negative facial expressions, for example—is seen in emotional disorders and is sensitive to pharmacological treatment. Whether pharmacological (analgesic) treatment might also influence the processing of threat in pain patients is currently unclear. Objectives This study investigates the effects catastrophizing on processing of facial affect in those receiving an acute opioid dose. Methods In a double-blind crossover design, the performance of 20 palliative care patients after their usual dose of immediate-release opioid was compared with their performance following matched-placebo administration on a facial affect recognition (i.e., speed and accuracy) and threat-pain estimation task (i.e., ratings of pain intensity). The influence of catastrophizing was examined by splitting the sample according to their score on the Pain Catastrophizing Scale (PCS). Results Opioid administration had no effect on facial affect processing compared with placebo. However, the main finding was that enhanced processing of fear, sadness, and disgust was found only in patients who scored highly on the PCS. There was no difference in performance between the two PCS groups on the other emotions (i.e., happiness, surprise, and anger). Conclusion These findings suggest that catastrophizing is associated with an affective information-processing bias in patients with severe pain conditions.

No impairment of recognition and experience of disgust in a patient with a right-hemispheric lesion of the insula and basal ganglia

An influential single case study (Calder, Keane, Manes, Antoun, & Young, 2000, Nature Neuroscience, 3, 1077–1078) recently showed a marked multimodal impairment in the recognition and experience of disgust in a patient with a left-hemispheric lesion of the basal ganglia and the insular cortex. Here, we investigated whether a similar deficit will be observed in a patient with a comparable lesion of the insula and basal ganglia in the right hemisphere. Remarkably, the patient showed no impairments in the recognition or experience of disgust and also no notable impairments in the recognition and experience of other emotions, across a range of stimuli, as compared to healthy comparison subjects. Thus, either deficits in disgust processing are not reliably observed in patients with lesion of the insula and basal ganglia regardless of the laterality of the lesion; or right-hemispheric lesions, in contrast to left-hemispheric lesions, do not seem to induce impairments in the processing of disgust.

Diminished Neural and Cognitive Responses to Facial Expressions of Disgust in Patients with Psoriasis: A Functional Magnetic Resonance Imaging Study

Psoriasis produces significant psychosocial disability; however, little is understood about the neurocognitive mechanisms that mediate the adverse consequences of the social stigma associated with visible skin lesions, such as disgusted facial expressions of others. Both the feeling of disgust and the observation of disgust in others are known to activate the insula cortex. We investigated whether the social impact of psoriasis is associated with altered cognitive processing of disgust using (i) a covert recognition of faces task conducted using functional magnetic resonance imaging (fMRI) and (ii) the facial expression recognition task (FERT), a decision-making task, conducted outside the scanner to assess the ability to recognize overtly different intensities of disgust. Thirteen right-handed male patients with psoriasis and 13 age-matched male controls were included. In the fMRI study, psoriasis patients had significantly (P<0.005) smaller signal responses to disgusted faces in the bilateral insular cortex compared with healthy controls. These data were corroborated by FERT, in that patients were less able than controls to identify all intensities of disgust tested. We hypothesize that patients with psoriasis, in this case male patients, develop a coping mechanism to protect them from stressful emotional responses by blocking the processing of disgusted facial expressions.

Fear and disgust processing during repeated exposure to threat-relevant stimuli in spider phobia

Although disgust plays a significant role in the etiology of spider phobia, there remains a paucity of research examining the role of disgust in the treatment of spider phobia. Spider fearful participants ( N = 46) were randomly assigned to a disgust (view vomit images) or neutral activation (view inanimate objects) condition. They were then repeatedly exposed to a videotaped tarantula, during which time their fear, disgust, and physiological levels were assessed repeatedly. Growth curve analyses indicated that repeated exposure led to significant declines in fear and disgust with no statistically significant differences between the two conditions. However, there was marginal evidence for decreased physiological arousal during repeated exposure among spider fearful participants in the disgust activation condition compared to those in the neutral condition. Reduction in disgust during exposure in the disgust activation condition remained significant after controlling for change in fear, whereas change in fear was no longer significant after controlling for change in disgust. However, the opposite pattern of relations between change in fear and disgust was observed in the neutral activation condition. Higher fear and disgust activation during exposure was also associated with higher fear and disgust responding on a subsequent behavioral task and higher spider fear and disgust at 3-month follow-up. Baseline trait disgust propensity also predicted fear and disgust parameters during repeated exposure. The implications of these findings for the role of disgust in the treatment of spider phobia are discussed.

Alteration of fractional anisotropy and apparent diffusion coefficient in obsessive–compulsive disorder: A diffusion tensor imaging study

Background Abnormalities of fractional anisotropy (FA) have been reported in previous diffusion tensor imaging (DTI) studies in patients with obsessive–compulsive disorder (OCD). However, there are some inconsistencies in the results and the apparent diffusion coefficient (ADC) has not been investigated. The goal of this study was to investigate white matter abnormalities and water diffusivity, as reflected by FA and ADC, using DTI in patients with OCD. Methods Fifteen patients with OCD and 15 healthy volunteers underwent DTI. Voxelwise analysis was used to compare FA in white matter and ADC in gray matter/white matter of the two groups. Results Compared with healthy volunteers, the patients had higher FA in the bilateral semioval center extending to the subinsular white matter; and a higher ADC in the left medial frontal cortex. There were no areas with a significantly lower FA or ADC in patients compared with healthy volunteers. Conclusions A significantly higher FA was found in regions associated with the emotion of disgust and a trend for a higher ADC was found in a region associated with the regulation of emotions. These findings suggest that neurocircuits involved in disgust processing may play an important role in the pathophysiology of OCD.

Recognition and evaluation of emotional prosody in individuals with generalized social phobia: A pilot study

Studies using facial emotional expressions as stimuli partially support the assumption of biased processing of social signals in social phobia. This pilot study explored for the first time whether individuals with social phobia display a processing bias towards emotional prosody. Fifteen individuals with generalized social phobia and fifteen healthy controls (HC) matched for gender, age, and education completed a recognition test consisting of meaningless utterances spoken in a neutral, angry, sad, fearful, disgusted or happy tone of voice. Participants also evaluated the stimuli with regard to valence and arousal. While these ratings did not differ significantly between groups, analysis of the recognition test revealed enhanced identification of sad and fearful voices and decreased identification of happy voices in individuals with social phobia compared with HC. The two groups did not differ in their processing of neutral, disgust, and anger prosody.

Hemodynamic brain correlates of disgust and fear ratings

Inconsistent findings from several functional magnetic resonance imaging (fMRI) studies on fear and disgust raise the question which brain regions are relatively specialized and which are general in the processing of these basic emotions. Some of these inconsistencies could partially be due to inter-individual differences in the experience of the applied emotional stimuli. In the present study, we therefore correlated the participants' individual online reports of fear and disgust with their hemodynamic responses towards each of the fear- and disgust-inducing scenes. Sixty six participants (32 females) took part in the fMRI study. In an event-related design, they saw 50 pictures with different emotional impact (10 neutral, 20 disgust-inducing, 20 fear-inducing). Pictures were presented for 4 s and participants rated each picture online – just after the presentation – on the dimensions disgust and fear among others. The results indicate that the processing of disgust- and fear-inducing pictures involves similar as well as distinct brain regions. Both emotional stimulus categories resulted in activations in the extended occipital cortex, in the prefrontal cortex, and in the amygdala. However, insula activations were only significantly correlated with subjective ratings of disgust, pointing to a specific role of this brain structure in the processing of disgust.

Disgust and Huntington's disease

The disproportionate impairment for the recognition of facial expressions of disgust in patients with Huntington's disease (HD) forms a double dissociation with the impaired recognition of fear that has been reported in amygdala patients. The dissociation has generated discussion regarding the potential existence of neural substrates dedicated to the recognition of facial signals of specific emotions. The aim of this study was to establish whether the impairment for disgust in HD was restricted solely to the domain of facial perception, or whether HD patients also demonstrate impairment in other kinds of disgust. Fourteen HD patients and fourteen age and education matched healthy controls participated in seven disparate emotion processing tasks. (1) A measure of knowledge for the situational determinants of distinct emotions; (2) recognition of emotion expressed in nonverbal vocalisations; (3) recognition of the emotional content of explicit lexical stimuli; (4) recognition of emotional content in pictures of emotion scenes; (5) a disgust experience questionnaire; (6) a measure of olfactory hedonic responsiveness; (7) a measure of gustatory perception. While verbal aspects of disgust processing were preserved, parallel impairments were revealed for olfactory disgust, vocal disgust expressions, the classification of disgusting pictures, and declarative knowledge of disgust elicitors. The finding of impaired perception of disgust signalled through different input domains suggests that the inability to recognise the facial expression in this population reflects a fundamental problem with disgust processing.

Preferential responses in amygdala and insula during presentation of facial contempt and disgust

Some authors consider contempt to be a basic emotion while others consider it a variant of disgust. The neural correlates of contempt have not so far been specifically contrasted with disgust. Using functional magnetic resonance imaging (fMRI), we investigated the neural networks involved in the processing of facial contempt and disgust in 24 healthy subjects. Facial recognition of contempt was lower than that of disgust and of neutral faces. The imaging data indicated significant activity in the amygdala and in globus pallidus and putamen during processing of contemptuous faces. Bilateral insula and caudate nuclei and left as well as right inferior frontal gyrus were engaged during processing of disgusted faces. Moreover, direct comparisons of contempt vs. disgust yielded significantly different activations in the amygdala. On the other hand, disgusted faces elicited greater activation than contemptuous faces in the right insula and caudate. Our findings suggest preferential involvement of different neural substrates in the processing of facial emotional expressions of contempt and disgust.

Neurocircuitry of disgust and anxiety in obsessive-compulsive disorder: A positron emission tomography study

Disgust and fear are basic emotions that have different elicitors and expressions, and that appear to be mediated by different neurocircuits. Although obsessive-compulsive disorder (OCD) is classified as an anxiety disorder, disgust may be involved in its pathogenesis. Functional magnetic resonance imaging (fMRI) studies of disgust-inducing visual stimuli in OCD have suggested disorder specific alterations in brain activation during these tasks. Subjects with OCD and healthy controls (HC) underwent positron emission tomography (PET) brain scanning after injection of H(2) (15)O. During PET, subjects either watched slides designed to evoke feelings of disgust (OCD = 5, HC = 11), expected the delivery of an electrical shock (OCD = 11, HC = 13), or rested (OCD = 11, HC = 14). After the anticipatory anxiety and resting tasks, anxiety ratings, heart rate, and electrodermal measures were obtained. Statistical parametric mapping (SPM) was used to analyze regional cerebral blood flow (rCBF) data. Comparison of OCD subjects with controls on differences in rCBF across the disgust-inducing and resting tasks showed that OCD was characterized by greater rCBF in the left insula. In OCD the disgust-inducing task increased right lateral orbitofrontal cortex rCBF compared to resting, whereas in controls there was no difference in rCBF between these tasks. Anxiety ratings, heart rate, and electrodermal activity increased during anticipatory anxiety in both groups, and comparison of rCBF in OCD subjects with controls in anticipatory anxiety versus resting state also found no significant differences. OCD may be characterized by a disruption in disgust processing, such that there is a decrease in appropriate disgust (such as that evoked by observing disgust in others) and an increase in inappropriate disgust (such as that evoked by contamination stimuli). The insula may play a particularly important role in mediating such putative disruptions. The sample studied here was small, and further work is required to determine whether disgust-induced activation patterns in OCD are more apparent in specific subtypes of this disorder, whether they are specific to OCD, and whether they are normalized by treatment.

Disgust and Obsessive–Compulsive Disorder: An Update

In this paper, we review the growing body of literature investigating the association between obsessive–compulsive disorder (OCD) and the emotion of disgust. Initially studied with regard to specific phobias, the potential role of disgust responses in contamination concerns has led researchers to investigate possible associations between disgust and OCD symptoms. The literature on disgust–sensitivity in OCD is reviewed. Studies of disgust recognition in OCD and research using neuroimaging methods are then summarized. We suggest that disgust has a moderate association with OCD symptoms, particularly those which are contamination–based or which have a religious focus. Evidence for a disgust recognition deficit in patients with OCD is lacking; however, neuroimaging findings have confirmed hypothesized associations between contamination–focused OCD and the insula cortex, which has been implicated in disgust processing. Finally, treatment implications are discussed, and suggestions are made for further research.

FMRI responses to pictures of mutilation and contamination

Findings from several functional magnetic resonance imaging (fMRI) studies implicate the existence of a distinct neural disgust substrate, whereas others support the idea of distributed and integrative brain systems involved in emotional processing. In the present fMRI experiment 12 healthy females viewed pictures from four emotion categories. Two categories were disgust-relevant and depicted contamination or mutilation. The other scenes showed attacks (fear) or were affectively neutral. The two types of disgust elicitors received comparable ratings for disgust, fear and arousal. Both were associated with activation of the occipitotemporal cortex, the amygdala, and the orbitofrontal cortex; insula activity was nonsignificant in the two disgust conditions. Mutilation scenes induced greater inferior parietal activity than contamination scenes, which might mirror their greater capacity to capture attention. Our results are in disagreement with the idea of selective disgust processing at the insula. They point to a network of brain regions involved in the decoding of stimulus salience and the regulation of attention.

Increased activation of the anterior cingulate cortex during processing of disgust faces in individuals with social phobia

Researchers have examined the role of differential activation of various brain regions involved in processing emotional information in subjects with social phobia. These studies have focused mostly on the activation of the amygdala. The anterior cingulate cortex (ACC) also has been implicated in processing emotional information, but its role in social phobia has not been examined. We recruited subjects with social phobia and matched them with non-anxious control subjects. Participants viewed facial expressions of disgust ("disgust faces") and neutral facial expressions ("neutral faces"). We measured brain activation, focusing on the ACC, using functional magnetic resonance imaging. We also recorded participants' ratings of emotional valence of faces, as well as response latencies to make these valence judgments. We repeated this procedure using three different sets of facial expressions. Individuals with social phobia exhibited a significant increase in ACC activity compared with non-anxious control subjects when processing disgust versus neutral faces. Additionally, compared with control subjects, subjects with social phobia were faster in their ratings of disgust faces and rated the neutral faces more negatively. Our findings demonstrate that the ACC might be involved in affective processing of negative information in socially phobic subjects.

Relationship between Disgust Sensitivity, Trait Anxiety and Brain Activity during Disgust Induction

We examined the influence of disgust sensitivity and trait anxiety on disgust processing via functional magnetic resonance imaging. Data of 63 healthy females were combined across four studies, where the same disgusting and affectively neutral pictures had been presented. The disgust pictures, rated as highly repulsive, provoked activation in the occipital cortex, the left prefrontal cortex and both amygdalae. Disgust sensitivity and trait anxiety were positively, and independently from each other, correlated with the activation of the right amygdala. This points to the role of the amygdala as an integrative brain structure, whose activation can be modulated by different affective styles.