Face perception enhances insula and motor network reactivity in Tourette syndrome

Rae, Charlotte L, Polyanska, Liliana, Gould van Praag, Cassandra D, Parkinson, Jim, Bouyagoub, Samira, Nagai, Yoko, Seth, Anil K, Harrison, Neil A, Garfinkel, Sarah N and Critchley, Hugo D (2018) Face perception enhances insula and motor network reactivity in Tourette syndrome. Brain, 141 (11). pp. 3249-3261. ISSN 0006-8950

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Abstract

Tourette syndrome is a neurodevelopmental disorder, characterised by motor and phonic tics. Tics are typically experienced as avolitional, compulsive, and associated with premonitory urges. They are exacerbated by stress and can be triggered by external stimuli, including social cues like the actions and facial expressions of others. Importantly, emotional social stimuli, with angry facial stimuli potentially the most potent social threat cue, also trigger behavioural reactions in healthy individuals, suggesting that such mechanisms may be particularly sensitive in people with Tourette syndrome. Twenty-one participants with Tourette syndrome and 21 healthy controls underwent functional magnetic resonance imaging while viewing faces wearing either neutral or angry expressions to quantify group differences in neural activity associated with processing social information. Simultaneous video recordings of participants during neuroimaging enabled us to model confounding effects of tics on task-related responses to the processing of faces. In both Tourette syndrome and control participants, face stimuli evoked enhanced activation within canonical face perception regions, including the occipital face area and fusiform face area. However, the Tourette syndrome group showed additional responses within the anterior insula to both neutral and angry faces. Functional connectivity during face viewing was then examined in a series of psychophysiological interactions. In Tourette syndrome participants, the insula showed functional connectivity with a set of cortical regions previously implicated in tic generation: the pre-supplementary motor area, premotor cortex, primary motor cortex, and the putamen. Furthermore, insula functional connectivity with the globus pallidus and thalamus varied in proportion to tic severity, while supplementary motor area connectivity varied in proportion to premonitory sensations, with insula connectivity to these regions increasing to a greater extent in patients with worse symptom severity. In addition, the occipital face area showed increased functional connectivity in Tourette syndrome participants with posterior cortical regions, including primary somatosensory cortex, and occipital face area connectivity with primary somatosensory and primary motor cortices varied in proportion to tic severity. There were no significant psychophysiological interactions in controls. These findings highlight a potential mechanism in Tourette syndrome through which heightened representation within insular cortex of embodied affective social information may impact the reactivity of subcortical motor pathways, supporting programmed motor actions that are causally implicated in tic generation. Medicinal and psychological therapies that focus on reducing insular hyper-reactivity to social stimuli may have potential benefit for tic reduction in people with Tourette syndrome.

Item Type: Article
Keywords: basal ganglia; movement disorders: imaging; neuropsychiatry: imaging; tic disorder; Tourette’s syndrome
Schools and Departments: School of Psychology > Psychology
Research Centres and Groups: Centre for Computational Neuroscience and Robotics
Sackler Centre for Consciousness Science
Sussex Neuroscience
Subjects: R Medicine > RC Internal medicine > RC0321 Neurosciences. Biological psychiatry. Neuropsychiatry
Depositing User: Alexei Fisk
Date Deposited: 13 Sep 2018 15:37
Last Modified: 02 Jul 2019 14:01
URI: http://sro.sussex.ac.uk/id/eprint/78713

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