Asymmetric right/left encoding of emotions in the human subthalamic nucleus

Renana Eitan,Ovadya Rosenbluh,Hagai Bergman,Eduard Linetsky,Zvi Israel,Shay Moshel,Tamir Ben-Hur,Reuben R Shamir

doi:10.3389/fnsys.2013.00069

Abstract

Emotional processing is lateralized to the non-dominant brain hemisphere. However, there is no clear spatial model for lateralization of emotional domains in the basal ganglia. The subthalamic nucleus (STN), an input structure in the basal ganglia network, plays a major role in the pathophysiology of Parkinson's disease (PD). This role is probably not limited only to the motor deficits of PD, but may also span the emotional and cognitive deficits commonly observed in PD patients. Beta oscillations (12–30 Hz), the electrophysiological signature of PD, are restricted to the dorsolateral part of the STN that corresponds to the anatomically defined sensorimotor STN. The more medial, more anterior and more ventral parts of the STN are thought to correspond to the anatomically defined limbic and associative territories of the STN. Surprisingly, little is known about the electrophysiological properties of the non-motor domains of the STN, nor about electrophysiological differences between right and left STNs. In this study, microelectrodes were utilized to record the STN spontaneous spiking activity and responses to vocal non-verbal emotional stimuli during deep brain stimulation (DBS) surgeries in human PD patients. The oscillation properties of the STN neurons were used to map the dorsal oscillatory and the ventral non-oscillatory regions of the STN. Emotive auditory stimulation evoked activity in the ventral non-oscillatory region of the right STN. These responses were not observed in the left ventral STN or in the dorsal regions of either the right or left STN. Therefore, our results suggest that the ventral non-oscillatory regions are asymmetrically associated with non-motor functions, with the right ventral STN associated with emotional processing. These results suggest that DBS of the right ventral STN may be associated with beneficial or adverse emotional effects observed in PD patients and may relieve mental symptoms in other neurological and psychiatric diseases.

Highlights

Subthalamic nucleus (STN) associated with emotional processing. These results suggest that deep brain stimulation (DBS) of the right ventral STN may be associated with beneficial or adverse emotional effects observed in Parkinson’s disease (PD)
Neuronal responses to emotive stimuli in the ventro-medial non-oscillatory region of the right STN were far larger than the responses at the dorso-lateral oscillatory region
Effective reinforcement learning depends on accurate recognition of the current state of the animal, including the emotional valence of different stimuli

Summary

Introduction

Subthalamic nucleus (STN) deep brain stimulation (DBS) is an established therapy for the management of motor symptoms of advanced Parkinson’s disease (PD; Benazzouz et al, 1993; Benabid et al, 1994; Weaver et al, 2009; Follett et al, 2010; Moro et al, 2010; Bronstein et al, 2011; Lhommée et al, 2012; Odekerken et al, 2013; Schuepbach et al, 2013), and is a promising potential therapy for the management of obsessivecompulsive disorder (OCD) (Mallet et al, 2008; Chabardès et al., 2012).Psychiatric adverse effects such as apathy, depression, emotion recognition and reactivity, hypomania, and suicide have been observed in PD patients before and after STN DBS (Dujardin et al, 2004; Schroeder et al, 2004; Biseul et al, 2005; Temel et al, 2006; Drapier et al, 2008; Witt et al, 2008; Péron et al., Frontiers in Systems Neuroscience2010a). Subthalamic nucleus (STN) deep brain stimulation (DBS) is an established therapy for the management of motor symptoms of advanced Parkinson’s disease (PD; Benazzouz et al, 1993; Benabid et al, 1994; Weaver et al, 2009; Follett et al, 2010; Moro et al, 2010; Bronstein et al, 2011; Lhommée et al, 2012; Odekerken et al, 2013; Schuepbach et al, 2013), and is a promising potential therapy for the management of obsessivecompulsive disorder (OCD) (Mallet et al, 2008; Chabardès et al., 2012) Psychiatric adverse effects such as apathy, depression, emotion recognition and reactivity, hypomania, and suicide have been observed in PD patients before and after STN DBS STN DBS of PD patients in the “off ” medication state was associated with a reduction in www.frontiersin.org

Methods

Results

Discussion

Conclusion