Abstract

A growing body of evidence suggests a role of the insular cortex (IC) and the basal ganglia (BG) in the experience, expression, and recognition of disgust. However, human lesion research, probing this structure-function link, has yielded rather disparate findings in single cases of unilateral and bilateral damage to these areas. Comparative group approaches are needed to elucidate whether disgust-related deficits specifically follow damage to the IC-BG system, or whether there might be a differential hemispheric contribution to disgust processing. We examined emotional processing by means of a comprehensive emotional test battery in four patients with left- and four patients with right-hemispheric lesions to the IC-BG system as well as in 19 healthy controls. While single tests did not provide clear-cut separations of patient groups, composite scores indicated selective group effects for disgust. Importantly, left-lesioned patients presented attenuated disgust composites, while right-lesioned patients showed increased disgust composites, as compared to each other and controls. These findings propose a left-hemispheric basis of disgust, potentially due to asymmetrical representations of autonomic information in the human forebrain. The present study provides the first behavioral evidence of hemispheric lateralization of a specific emotion in the human brain, and contributes to neurobiological models of disgust.

Highlights

  • The insular cortex (IC) and the basal ganglia (BG) have been attributed a pivotal role in the functional neurocircuitry of disgust (Chapman and Anderson, 2012)

  • Inclusion criteria were: (1) unilateral lesions due to an ischaemic or haemorrhagic middle cerebral artery stroke, centrally affecting the IC-BG complex, as corroborated by highresolution structural MRI data and neuroradiological report; (2) stable lesions; (3) no cognitive deficits compromising understanding of instructions and task performance; (4) no history of neurodegenerative disorders, epilepsy, brain tumors, or brain trauma; (5) no history of substance induced disorders; (6) no history of psychiatric disorders; (7) motor ability to participate in the experimental procedure; (8) male gender, since previous single case findings on disgust processing have been mainly derived from the examination of male patients

  • Significant group differences emerged for the intensity of disgust experience in the daily life, with left-lesioned patients scoring lower than controls (t21 = 2.776, P = 0.011), and the Questionnaire for the Assessment of Disgust Sensitivity (QADS), with right-lesioned patients scoring higher than controls (t21 = 2.376, P = 0.027)

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Summary

Introduction

The insular cortex (IC) and the basal ganglia (BG) have been attributed a pivotal role in the functional neurocircuitry of disgust (Chapman and Anderson, 2012). Another study on epilepsy patients revealed selective activation of depth electrodes in the anterior IC for disgusted rather than for other emotional faces (Krolak-Salmon et al, 2003) While these lines of evidence strongly support the hypothesis of an IC-BG system in disgust, findings from studies of patients with focal lesions in the IC-BG complex are rather inconclusive. In a pioneering case study, selective impairment of recognition and experience of disgust was found in a patient with lefthemispheric infarction impacting both IC and BG (Calder et al, 2000) Another patient with bilateral IC, temporal and frontal damage exhibited disproportionate disgust deficits for dynamic emotional facial expressions and stories describing emotional actions (Adolphs et al, 2003). Another plausible option is distinct hemispheric involvement in disgust processing

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