Subthalamic nucleus oscillations during vocal emotion processing are dependent of the motor asymmetry of Parkinson's disease
Damien Benis,
Claire Haegelen,
Philippe Voruz,
Jordan Pierce,
Valérie Milesi,
Jean-François Houvenaghel,
Marc Vérin,
Paul Sauleau,
Didier Grandjean,
Julie Péron
Affiliations
Damien Benis
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
Claire Haegelen
Neurosurgery Department, Pontchaillou Hospital, Rennes University Hospital, France; INSERM, LTSI U1099, Faculty of Medicine, University of Rennes, France
Philippe Voruz
Clinical and Experimental Neuropsychology Laboratory, Department of Psychology and Educational Sciences, University of Geneva, Switzerland
Jordan Pierce
Clinical and Experimental Neuropsychology Laboratory, Department of Psychology and Educational Sciences, University of Geneva, Switzerland
Valérie Milesi
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
Jean-François Houvenaghel
Neurology Department, Pontchaillou Hospital, Rennes University Hospital, France; Behavior and Basal Ganglia's research unit (EA 4712), University of Rennes 1, Rennes University Hospital, France
Marc Vérin
Neurology Department, Pontchaillou Hospital, Rennes University Hospital, France; Behavior and Basal Ganglia's research unit (EA 4712), University of Rennes 1, Rennes University Hospital, France
Paul Sauleau
Neurology Department, Pontchaillou Hospital, Rennes University Hospital, France; Behavior and Basal Ganglia's research unit (EA 4712), University of Rennes 1, Rennes University Hospital, France
Didier Grandjean
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
Julie Péron
Clinical and Experimental Neuropsychology Laboratory, Department of Psychology and Educational Sciences, University of Geneva, Switzerland; Neuropsychology Unit, Neurology Department, University Hospitals of Geneva, Switzerland; Corresponding author.
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.
