Sackler Centre for Consciousness Science, University of Sussex, UK.
Department of Neuroscience, Brighton and Sussex Medical School, UK.
Brain. 2018 Nov 1;141(11):3249-3261. doi: 10.1093/brain/awy254.
Tourette syndrome is a neurodevelopmental disorder, characterized 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 MRI 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 participants with Tourette syndrome, the insula showed functional connectivity with a set of cortical regions previously implicated in tic generation: the presupplementary 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.
妥瑞氏症候群是一种神经发育障碍,其特征为运动性抽搐和发声性抽搐。抽搐通常是不由自主的、强制性的,与预感冲动有关。它们会因压力而加剧,并可能被外部刺激触发,包括他人的动作和面部表情等社会线索。重要的是,情绪性社会刺激,包括愤怒的面部刺激,可能是最有效的社会威胁线索,也会引发健康个体的行为反应,这表明在妥瑞氏症候群患者中,这些机制可能特别敏感。21 名妥瑞氏症候群患者和 21 名健康对照者在观看戴有中性或愤怒表情的面孔时进行了功能性磁共振成像,以量化与处理社会信息相关的神经活动的组间差异。在神经影像学期间对参与者进行同步视频记录,使我们能够对抽动对处理面孔的任务相关反应的混杂影响进行建模。在妥瑞氏症候群患者和对照组参与者中,面孔刺激均在包括枕叶面孔区和梭状回面孔区在内的典型面孔感知区域内引起了增强的激活。然而,妥瑞氏症候群组在对中性和愤怒面孔时,在前脑岛内显示出了额外的反应。然后,通过一系列心理生理交互作用来检查观看面孔时的功能连接。在妥瑞氏症候群患者中,脑岛与先前与抽动生成有关的一组皮质区域显示出功能连接:补充运动区、运动前区、初级运动皮质和壳核。此外,脑岛与苍白球和丘脑的功能连接与抽动严重程度成正比,而补充运动区的连接与预感感觉成正比,随着患者症状严重程度的增加,脑岛与这些区域的连接程度增加更大。此外,在妥瑞氏症候群患者中,枕叶面孔区与后皮质区域(包括初级体感皮层)之间的功能连接增加,并且在初级体感和初级运动皮质之间,枕叶面孔区的功能连接与抽动严重程度成正比。对照组中没有显著的心理生理交互作用。这些发现突出了妥瑞氏症候群中的一种潜在机制,即脑岛皮层内对具身情感社会信息的增强表示可能会影响皮质下运动通路的反应性,支持程序化的运动动作,这些动作在抽动生成中具有因果关系。专注于减少脑岛对社会刺激的过度反应的医学和心理治疗方法可能对减少妥瑞氏症候群患者的抽动具有潜在益处。