Disgust and happiness recognition correlate with anteroventral insula and amygdala volume respectively in preclinical Huntington's disease

Patients with Huntington's disease (HD) can show disproportionate impairments in recognizing facial signals of disgust, but the neural basis of this deficit remains unclear. Functional imaging studies have implicated the anterior insula in the ability to recognize disgust, but have identified other structures as well, including the basal ganglia. In view of variable insula and basal ganglia volume changes in HD, we used voxel-based morphometry to map regional variations in gray matter (GM) volume in participants carrying the mutation for HD, and correlated this with their performance on a test of facial emotion recognition for six basic emotions (disgust, fear, anger, happiness, sadness, surprise). The volume of the anteroventral insula was strongly correlated with performance on the disgust recognition task. The amygdala volume (bilaterally) correlated with the ability to recognize happy facial expressions. There was marked specificity of the regional correlations for the emotion involved. Recognition of other emotion expressions, or more general cognitive or motor performance as measured by a standardized rating scale, did not correlate with regional brain volume in this group. Control participants showed no effect for any measure. The strong linear correlations for disgust and happiness recognition imply direct involvement of the anterior insula in disgust appreciation, and a similar role for the amygdala in recognizing happy facial expressions. The absence of a significant correlation with the basal ganglia suggests a less critical role for these structures in disgust recognition than has previously been suggested. The findings also highlight the role of neurodegenerative diseases combined with statistical imaging techniques in elucidating the brain basis of behavior and cognition.     

Number processing and basal ganglia dysfunction: a single case study

Numerical processing has never been investigated in a case of Fahr's disease (FD) and only rarely in cases of basal ganglia dysfunction. The study describes the cognitive decline of a pre-morbidly high-functioning patient (medical doctor) affected by FD and his difficulties in number processing. A MRI scan revealed bilateral calcifications in the basal ganglia and a brain PET showed a massive reduction of glucose metabolism in the basal ganglia and both frontal lobes, but no other brain abnormalities. The patient's cognitive deficits included impairments in problem solving, in cognitive set shifting and in mental flexibility, as well as in verbal memory. These deficits are attributed to the disruption of the dorsolateral prefrontal circuit involving the basal ganglia. In number processing, the patient showed a severe deficit in the retrieval of multiplication facts, deficits in all tasks of numerical problem solving and in the execution of complex procedures. Importantly, he also showed a dense deficit in conceptual knowledge, which concerned all test conditions and all operations. The findings confirm the predictions of the triple code model in so far, as a disruption of cortico-subcortical loops involving the basal-ganglia may lead to specific deficits in fact retrieval. However, no verbal deficit, as assumed in the triple code model and reported in similar cases, could be observed. The present findings further add to current knowledge on numerical processing, showing how fronto-executive dysfunction may disrupt conceptual understanding of arithmetic. This study shows that not only parietal lesions may lead to severe deficits in conceptual understanding, but that basal ganglia lesions leading to frontal dysfunction may have a devastating effect.     

Impairment of recognition of disgust in Chinese with Huntington's or Wilson's disease

The selective involvement of the basal ganglia in recognition of the facial expression of disgust was investigated by examining a group of six symptomatic Huntington's disease patients and 32 Wilson's disease patients in China. Morphed photographs of facial expressions covering happiness-surprise-fear-sadness-disgust-anger were used and the patients were asked to label each photo. Other measures assessed basic cognitive functions and perception of non-emotion facial information, such as perception of gender, age, gaze direction, and recognition of unfamiliar as well as famous people. There was dissociation between the perception of emotions and other facial information, and between impairment of recognition of disgust and other emotions. The basal ganglia are the overlapping substrate involved in both Huntington's and Wilson's disease, although each has its own other lesions. The differentially severe impairment of recognition of disgust in the Chinese Huntington's disease and Wilson's disease patients strengthens the view that basal ganglia are selectively involved in processing the emotion of disgust.     

Basal ganglia lesions and the theory of fronto-subcortical loops: neuropsychological findings in two patients with left caudate lesions

Basal ganglia lesions have a high prevalence for associated behavioural impairments. However, the exact pattern of cognitive impairments and its relationship to individual basal ganglia lesion have rarely been investigated by means of a detailed neuropsychological and lesion study. Furthermore, different mechanisms have been proposed as relevant for the observed cognitive deficits; among these, the hypothesis of fronto-subcortical loops (Alexander et al., 1986) has made predictions regarding the relationship between the damage of particular striato-frontal circuits and the resulting behavioural impairment which await clinical confirmation. We present a study of two subjects who suffered a MRI-documented focal left basal ganglia hematoma. The two patients differed in their lesions; in one patient (PJ) large parts of the caudate nucleus were destroyed whereas in the other (AS) mainly the pallidum and putamen were lesioned and the caudate suffered only minor damage. In the acute phase, the behavioural and neuropsychological abnormalities were similar in both cases and included mainly abulia, an impairment of executive and attentional functions, and a severe amnestic syndrome. After several months many functions were restored in AS, whereas PJ's abilities remained largely defective. Based on these data and on previous case studies several conclusions are drawn. Left caudate lesions induce marked and long-lasting behavioural and neuropsychological impairments comprising predominantly drive, executive control, attention, and memory. The extent of lesion in the head of the caudate nucleus is the critical factor regarding the severity and the outcome of the syndrome, whereas damage to the putamen and pallidum is less crucial for cognitive functions. A subset of behavioural alterations, among them abulia, attentional and frontal-executive dysfunctions, can well be attributed to lesions of the anterior cingulate circuit and the dorsolateral-frontal circuit at the basal ganglia level. Other impairments, most importantly the prominent amnestic syndrome, are more difficult to interpret on the grounds of this hypothesis and may be related to other pathomechanisms.     

Basal Ganglia Lesions and the Theory of Fronto-Subcortical Loops: Neuropsychological Findings in Two Patients with Left Caudate Lesions

Basal ganglia lesions have a high prevalence for associated behavioural impairments. However, the exact pattern of cognitive impairments and its relationship to individual basal ganglia lesion have rarely been investigated by means of a detailed neuropsychological and lesion study. Furthermore, different mechanisms have been proposed as relevant for the observed cognitive deficits; among these, the hypothesis of fronto-subcortical loops (Alexander et al., 1986) has made predictions regarding the relationship between the damage of particular striato-frontal circuits and the resulting behavioural impairment which await clinical confirmation. We present a study of two subjects who suffered a MRI-documented focal left basal ganglia hematoma. The two patients differed in their lesions; in one patient (PJ) large parts of the caudate nucleus were destroyed whereas in the other (AS) mainly the pallidum and putamen were lesioned and the caudate suffered only minor damage. In the acute phase, the behavioural and neuropsychological abnormalities were similar in both cases and included mainly abulia, an impairment of executive and attentional functions, and a severe amnestic syndrome. After several months many functions were restored in AS, whereas PJ’s abilities remained largely defective. Based on these data and on previous case studies several conclusions are drawn. Left caudate lesions induce marked and long-lasting behavioural and neuropsychological impairments comprising predominantly drive, executive control, attention, and memory. The extent of lesion in the head of the caudate nucleus is the critical factor regarding the severity and the outcome of the syndrome, whereas damage to the putamen and pallidum is less crucial for cognitive functions. A subset of behavioural alterations, among them abulia, attentional and frontal-executive dysfunctions, can well be attributed to lesions of the anterior cingulate circuit and the dorsolateral-frontal circuit at the basal ganglia level. Other impairments, most importantly the prominent amnestic syndrome, are more difficult to interpret on the grounds of this hypothesis and may be related to other pathomechanisms.     

Differential deficits in expression recognition in gene-carriers and patients with Huntington's disease

Previous studies in symptomatic patients and asymptomatic gene-carriers of Huntington's disease (HD) reported a differential deficit in the recognition of facial expressions of disgust. This impairment may point to involvement of the basal ganglia in the recognition of disgust. In this study, we compared the performance of 20 patients with symptoms of HD, 20 gene-carriers of HD and 20 healthy controls on two tests of facial expressions in order to further investigate the role of the basal ganglia in disgust recognition. Recognition of fear, rather than disgust, was most severely impaired in the patients, who were also impaired at recognising expressions of anger, disgust and sadness. Direct testing for a differential deficit in disgust at the group level (and at the level of individual HD cases) revealed that the patients were in fact significantly more impaired on the other negative expressions than on disgust. The gene-carriers were not impaired on any expression, although there was a trend for the gene-carriers to be poorer at recognising fearful faces than the controls. We argue that the expression recognition performance of the patients and gene-carriers simply reflects differences in task difficulty, rather than dysfunction of any mechanisms dedicated to specific emotions. In contrast to previous studies in patients or gene-carriers of HD, our findings provide no evidence for a role of the basal ganglia in the recognition of disgust and cast doubt on whether results from HD patients and gene-carriers can be used in support of a double dissociation between recognition of disgust and fear.     

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.     

No disgust recognition deficit in obsessive-compulsive disorder

BACKGROUND: Patients with basal ganglia abnormalities misclassify facial expressions of disgust as expressions of anger when asked to identify the emotion depicted in photographs of individuals displaying different emotions. Sprengelmeyer, Young, Pundt et al. (1997) reported a similar disgust recognition deficit in patients with obsessive-compulsive disorder (OCD)--an anxiety disorder associated with basal ganglia abnormality. METHODS: In the present experiment, we attempted to replicate Sprengelmeyer, Young, Pundt et al.'s (1997) findings. RESULTS: We failed to replicate Sprengelmeyer, Young, Pundt et al.'s finding of disgust recognition deficits in OCD patients relative to healthy control subjects. One patient with especially severe OCD did, however, exhibit impairment by misclassifying disgust expressions as anger expressions. DISCUSSION: These data do not confirm the presence of disgust recognition deficits in individuals with OCD. In light of the deficits exhibited by one subject with severe OCD, disgust recognition deficits may be confined to an unidentified subset of people with OCD.     

Wilson病患者心理理论障碍的研究

目的探讨Wilson病(WD)患者的心理理论(ToM)障碍。方法对32例WD患者(WD组)以及29名健康人(NC组)进行认知功能及失言识别和眼区基本情绪辨别(喜、惊、恐、悲、厌、怒)评分,并对结果进行比较。结果与NC组比较,WD组的简易精神状态检查量表、智商、言语流畅性测试和数字广度评分差异无统计学意义。与NC组比较,WD组失言识别及心理状态判断评分显著降低(均P<0.01);眼部情绪辨别中的怒、恐和厌的评分显著降低(P<0.05～0.01),而喜、悲和惊的评分差异无统计学意义。结论 WD患者存在明显的ToM障碍,可能与其基底节损害有关。     

Wilson病患者眼区情绪认知障碍的研究

目的探讨Wilson病(Wilson disease,WD)患者是否存在眼区情绪认知障碍,了解基底节有无参与眼区情绪认知加工过程。方法将32例WD患者以及29名与其人口学资料相匹配的健康人(healthy control,HC)作为被试,采用眼区的6种基本情绪(喜、惊、恐、悲、厌、怒)任务,对两组进行测试。结果与HC组比较,WD组在在眼区情绪认知任务对怒(17.53±1.39分,P<0.05),恐(15.88±1.21分,P<0.05)和厌(18.00±1.85分,P<0.001)眼区情绪认知存在明显障碍;而对于喜、惊、悲的眼区情绪认知任务识别却无障碍(均P>0.05)。结论WD患者存在明显的怒、恐及厌眼区情绪认知障碍,基底节可能参与眼区情绪认知任务的加工过程。     

An attention modulated response to disgust in human ventral anterior insula

The human brain is expert in analyzing rapidly and precisely facial features, especially emotional expressions representing a powerful communication vector. The involvement of insula in disgust recognition has been reported in behavioral and functional imaging studies. However, we do not know whether specific insular fields are involved in disgust processing nor what the processing time course is. Using depth electrodes implanted during presurgical evaluation of patients with drug-refractory temporal lobe epilepsy, we recorded intracerebral event-related potentials to human facial emotional expressions, that is, fear, disgust, happiness, surprise, and neutral expression. We studied evoked responses in 13 patients with insular contacts to specify the insular fields involved in disgust processing and assess the timing of their activation. We showed that specific potentials to disgust beginning 300 milliseconds after stimulus onset and lasting 200 milliseconds were evoked in the ventral anterior insula in four patients. The occurrence and latency of event-related potentials to disgust in the ventral anterior insula were affected by selective attention. The analysis of spatial and temporal characteristics of insular responses to disgust facial expression lead us to underline the crucial role of ventral anterior insula in the categorization of facial emotional expressions, particularly the disgust.     

Facial recognition in primary focal dystonia.

The basal ganglia seem to be involved in emotional processing. Primary dystonia is a movement disorder considered to result from basal ganglia dysfunction, and the aim of the present study was to investigate emotion recognition in patients with primary focal dystonia. Thirty-two patients with primary cranial (n=12) and cervical (n=20) dystonia were compared to 32 healthy controls matched for age, sex, and educational level on the facially expressed emotion labeling (FEEL) test, a computer-based tool measuring a person's ability to recognize facially expressed emotions. Patients with cognitive impairment or depression were excluded. None of the patients received medication with a possible cognitive side effect profile and only those with mild to moderate dystonia were included. Patients with primary dystonia showed isolated deficits in the recognition of disgust (P=0.007), while no differences between patients and controls were found with regard to the other emotions (fear, happiness, surprise, sadness, and anger). The findings of the present study add further evidence to the conception that dystonia is not only a motor but a complex basal ganglia disorder including selective emotion recognition disturbances.     

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.     

Dystonia following head trauma: a report of nine patients and review of the literature.

We report nine patients who developed dystonia following head trauma. The most frequent form was hemidystonia only (six patients). One patient presented with hemidystonia plus torticollis, one with bilateral hemidystonia and one with torticollis only. Seven patients sustained a severe head injury, and two had a mild head injury. At the time of injury, six were younger than 10 years, two were adolescents, and the patient with torticollis only was an adult. Except in the patient with torticollis only, the onset of dystonia varied considerably from months to years. All patients with hemidystonia had posthemiplegic dystonia of delayed onset. Seven out of 8 patients with hemidystonia had lesions involving the contralateral caudate or putamen, as demonstrated by CT and MR. The patient with hemidystonia plus torticollis had no lesion to the basal ganglia, but a contralateral pontomesencephalic lesion. Response to medical treatment was generally poor. Functional stereotactic operations were performed in seven patients. A variety of factors may be responsible for the vascular or nonvascular posttraumatic basal ganglia lesions, which may lead to dystonia. The pathophysiology seems to be more complex than thought previously. We believe that dystonia following head injury is not as rare as is assumed. Awareness of its characteristics and optimized diagnostic procedures will lead to wider recognition of this entity.     

Subacute dementia and imaging correlates in a case of Fahr's disease

We report a case of idiopathic bilateral basal ganglia calcinosis, or Fahr's disease (FD) in a 50 year old patient who developed rapidly progressive behavioural abnormalities and severe neuropsychological impairments, but no movement disorder. Neuropsychological deficits included a severe dysexecutive syndrome, anterograde amnesia, and attentional impairment. Neuropsychiatric features comprised apathy with intermittent disinhibition, anxiety, irritability, frequent mood changes, ritualistic and antisocial behaviour, and psychosis. Fluorodeoxyglucose positron emission tomography showed a massive reduction of glucose metabolism in the basal ganglia and the frontal brain. The observed abnormalities possibly result from a disruption of frontostriatal circuits, presumably at the basal ganglia level. This case indicates that FD may cause exclusively behavioural alterations and that the associated hypometabolism in certain frontal areas is closely related to the clinical picture.     

CT scan correlates of gesture recognition.

The ability to recognise gestures was studied in 65 left-hemispheric stroke patients whose lesions were located by CT scan. In the acute stage (first month) frontal lobe and basal ganglia were frequently involved in patients showing inability to recognise gestures. In the later (third to fourth month) and chronic stages (greater than 6 months) parietal lobe involvement was important; lesions causing gesture recognition impairment were larger, had more extensive and frequent parietal involvement and produced less temporal lobe damage than those causing aural comprehension defects. These findings are discussed in the light of recent models of cerebral localisation of complex functions.     

Recognition of emotion from facial,prosodic and written verbal stimuli in Parkinson's disease

Although the basal ganglia are thought to be important in recognizing emotion, there is contradictory evidence as to whether patients with Parkinson's disease (PD) have deficits in recognizing facial expressions. In addition, few studies have examined their ability to recognize emotion from non-visual stimuli, such as voices. We examined the ability of PD patients and age-matched controls to recognize emotion in three different modalities: facial, prosodic, and written verbal stimuli. Compared to controls, PD patients showed deficits in recognizing fear and disgust in facial expressions. These impairments were not seen in their recognition of prosodic or written verbal stimuli. This modality-specific deficit suggests that the neural substrates for recognizing emotion from different modalities are not fully identical.     

A selective role for right insula—basal ganglia circuits in appetitive stimulus processing

Hemispheric lateralization of hedonic evaluation (‘liking’) and incentive motivation (‘wanting’) in neural networks connecting the basal ganglia and insula (BG-I) in humans was examined. Participants with brain damage restricted to the BG-I of the right (n = 5) or left (n = 5) hemisphere, and 26 healthy participants matched on age, sex and intelligence quotient were tested on positively and negatively valenced pictures drawn from varied stimulus categories (Vijayaraghavan et al., 2008). Liking was assessed with explicit ratings of pleasantness using a nine-point Likert scale. Wanting was quantified as the amount of work (via repeated keypresses) that participants expended to increase (approach) or decrease (withdraw) viewing time. Right-lesion patients showed abnormally low viewing times and liking ratings for positive images. For a subset of positive images depicting sexual content, right-lesion patients exhibited active withdrawal, while the other two groups approached such stimuli. These results suggest that the right basal ganglia–insula complex plays a greater role than the left in supporting hedonic evaluation and motivational approach to positively valenced stimuli. The finding that active avoidance of stimuli that were not ‘liked’ was spared in both right- and left-sided lesion subjects suggests that unilateral damage to insula/basal ganglia circuits may not be sufficient to affect general incentive motivation independent of preference.     

Core,social and moral disgust are bounded: A review on behavioral and neural bases of repugnance in clinical disorders

Disgust is a multifaceted experience that might affect several aspects of life. Here, we reviewed research on neurological and psychiatric disorders that are characterized by abnormal disgust processing to test the hypothesis of a shared neurocognitive architecture in the representation of three disgust domains: i) personal experience of ‘core disgust’; ii) social disgust, i.e., sensitivity to others’ expressions of disgust; iii) moral disgust, i.e., sensitivity to ethical violations. Our review provides some support to the shared neurocognitive hypothesis and suggests that the insula might be the “hub” structure linking the three domains of disgust sensitivity, while other brain regions may subserve specific facets of the multidimensional experience. Our review also suggests a role of serotonin core and moral disgust, supporting “neo-sentimentalist” theories of morality, which posit a causal role of affect in moral judgment.     

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.