Benis Damien, Haegelen Claire, Voruz Philippe, Pierce Jordan, Milesi Valérie, Houvenaghel Jean-François, Vérin Marc, Sauleau Paul, Grandjean Didier, Péron Julie
Clinical and Experimental Neuropsychology Laboratory, Department of Psychology and Educational Sciences, University of Geneva, Switzerland; Neuroscience of Emotion and Affective Dynamics laboratory, Department of Psychology and Swiss Center for Affective Sciences, Campus Biotech, University of Geneva, Switzerland; Swiss Center for Affective Sciences, Campus Biotech, University of Geneva, Switzerland.
Neurosurgery Department, Pontchaillou Hospital, Rennes University Hospital, France; INSERM, LTSI U1099, Faculty of Medicine, University of Rennes, France.
Neuroimage. 2020 Nov 15;222:117215. doi: 10.1016/j.neuroimage.2020.117215. Epub 2020 Aug 1.
The subthalamic nucleus (STN) is involved in different aspects of emotional processes and more specifically in emotional prosody recognition. Recent studies on the behavioral effects of deep brain stimulation (DBS) in patients with Parkinson's disease (PD) have uncovered an asymmetry in vocal emotion decoding in PD, with left-onset PD patients showing deficits for the processing of happy voices. Whether and how PD asymmetry affects STN electrophysiological responses to emotional prosody, however, remains unknown. In the current study, local field potential activity was recorded from eight left- and six right-lateralized motor-onset PD patients (LOPD/ROPD) undergoing DBS electrodes implantation, while they listened to angry, happy and neutral voices. Time-frequency decomposition revealed that theta (2-6 Hz), alpha (6-12 Hz) and gamma (60-150 Hz) band responses to emotion were mostly bilateral with a differential pattern of response according to patient's sides-of onset. Conversely, beta-band (12-20 Hz and 20-30 Hz) emotional responses were mostly lateralized in the left STN for both patient groups. Furthermore, STN theta, alpha and gamma band responses to happiness were either absent (theta band) or reduced (alpha and gamma band) in the most affected STN hemisphere (contralateral to the side-of onset), while a late low-beta band left STN happiness-specific response was present in ROPD patients and did not occur in LOPD patients. Altogether, in this study, we demonstrate a complex pattern of oscillatory activity in the human STN in response to emotional voices and reveal a crucial influence of disease laterality on STN low-frequency oscillatory activity.
底丘脑核(STN)参与情绪过程的不同方面,更具体地说是参与情绪韵律识别。最近关于帕金森病(PD)患者深部脑刺激(DBS)行为效应的研究发现,PD患者在声音情绪解码方面存在不对称性,左侧发病的PD患者在处理快乐声音时表现出缺陷。然而,PD的不对称性是否以及如何影响STN对情绪韵律的电生理反应仍不清楚。在本研究中,对8例左侧和6例右侧运动性发病的PD患者(左侧发病PD/右侧发病PD)在植入DBS电极时记录局部场电位活动,同时让他们聆听愤怒、快乐和中性的声音。时频分解显示,θ(2-6赫兹)、α(6-12赫兹)和γ(60-150赫兹)频段对情绪的反应大多是双侧的,且根据患者发病侧呈现出不同的反应模式。相反,两个患者组的β频段(12-20赫兹和20-30赫兹)情绪反应大多集中在左侧STN。此外,在受影响最严重的STN半球(与发病侧对侧),STN对快乐的θ、α和γ频段反应要么缺失(θ频段),要么减弱(α和γ频段),而右侧发病PD患者左侧STN存在晚期低β频段快乐特异性反应,左侧发病PD患者则未出现。总之,在本研究中,我们证明了人类STN对情绪声音的振荡活动模式复杂,并揭示了疾病侧别对STN低频振荡活动的关键影响。