Medical Scientist Training Program, Mayo Clinic, Rochester, MN 55902, USA.
Department of Neurologic Surgery, Mayo Clinic, Rochester, MN 55902, USA.
Brain. 2023 Oct 3;146(10):4174-4190. doi: 10.1093/brain/awad142.
Tourette syndrome is a childhood-onset neuropsychiatric disorder characterized by intrusive motor and vocal tics that can lead to self-injury and deleterious mental health complications. While dysfunction in striatal dopamine neurotransmission has been proposed to underlie tic behaviour, evidence is scarce and inconclusive. Deep brain stimulation (DBS) of the thalamic centromedian parafascicular complex (CMPf), an approved surgical interventive treatment for medical refractory Tourette syndrome, may reduce tics by affecting striatal dopamine release. Here, we use electrophysiology, electrochemistry, optogenetics, pharmacological treatments and behavioural measurements to mechanistically examine how thalamic DBS modulates synaptic and tonic dopamine activity in the dorsomedial striatum. Previous studies demonstrated focal disruption of GABAergic transmission in the dorsolateral striatum of rats led to repetitive motor tics recapitulating the major symptom of Tourette syndrome. We employed this model under light anaesthesia and found CMPf DBS evoked synaptic dopamine release and elevated tonic dopamine levels via striatal cholinergic interneurons while concomitantly reducing motor tic behaviour. The improvement in tic behaviour was found to be mediated by D2 receptor activation as blocking this receptor prevented the therapeutic response. Our results demonstrate that release of striatal dopamine mediates the therapeutic effects of CMPf DBS and points to striatal dopamine dysfunction as a driver for motor tics in the pathoneurophysiology of Tourette syndrome.
妥瑞氏症候群是一种儿童期发病的神经精神疾病,其特征为侵入性的运动和发声抽搐,可能导致自残和不良的心理健康并发症。虽然纹状体多巴胺神经传递功能障碍被认为是抽搐行为的基础,但证据很少且不确定。丘脑中央中侧旁核复合体(CMPf)的深部脑刺激(DBS)是一种已批准的用于治疗医学难治性妥瑞氏症候群的手术干预治疗方法,它可能通过影响纹状体多巴胺释放来减少抽搐。在这里,我们使用电生理学、电化学、光遗传学、药物治疗和行为测量来从机制上研究丘脑 DBS 如何调节背侧纹状体中的突触和紧张性多巴胺活动。先前的研究表明,在轻度麻醉下,大鼠背外侧纹状体中 GABA 能传递的局部破坏导致重复运动抽搐,重现了妥瑞氏症候群的主要症状。我们在该模型下进行了研究,发现 CMPf DBS 通过纹状体胆碱能中间神经元诱发突触多巴胺释放和升高紧张性多巴胺水平,同时减少运动抽搐行为。抽搐行为的改善被发现是通过 D2 受体激活介导的,因为阻断该受体可防止治疗反应。我们的结果表明,纹状体多巴胺的释放介导了 CMPf DBS 的治疗效果,并指出纹状体多巴胺功能障碍是妥瑞氏症候群病理神经生理学中运动抽搐的驱动因素。