Abstract

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.

Highlights

  • The subthalamic nucleus (STN) has been shown to be involved in vocal emotion recognition by neuroimaging studies (Fruhholz et al, 2012; Péron et al, 2016), and impairments have been observed following disruption of STN functioning during deep brain stimulation (DBS) in patients with Parkinson’s disease (PD) (Péron et al, 2015; J. 2010)

  • No behavioral differences were detected between left-onset PD patients (LOPD) and right-onset PD patients (ROPD) patients in terms of successful one-back trials (t(1) =0.012, p = 0.99) and false-alarms (t(1) =0.058, p = 0.95)

  • STN and eight right STN for LOPD, six left STN and six right STN for ROPD patients) were analyzed in order to evaluate the pattern of oscillatory activity in different frequency bands during presentation of angry, happy and neutral voices

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Summary

Introduction

The subthalamic nucleus (STN) has been shown to be involved in vocal emotion recognition by neuroimaging studies (Fruhholz et al, 2012; Péron et al, 2016), and impairments have been observed following disruption of STN functioning during deep brain stimulation (DBS) in patients with Parkinson’s disease (PD) (Péron et al, 2015; J. 2010). Vocal emotion recognition includes processing of emotional prosody, which refers to changes in different segmental and supra-segmental aspects ∗ †. These authors contributed to this work of voice such as rhythm and intonation that convey emotions during speech (Grandjean et al, 2005). For vocal emotion recognition in the cortex, Schirmer and Kotz proposed a model with sequential processing of the emotional percept in three steps (Schirmer and Kotz, 2006).

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