Topography of emotional valence and arousal within the motor part of the subthalamic nucleus in Parkinson\u2019s disease

Tereza Serranová,Filip Růžička,Eduard Bakštein,Petr Dušek,Evžen Růžička,Daniel Novák,Dušan Urgošík,Robert Jech,Tomáš Sieger,Pavel Vostatek

doi:10.1038/s41598-019-56260-x

Abstract

Clinical motor and non-motor effects of deep brain stimulation (DBS) of the subthalamic nucleus (STN) in Parkinson's disease (PD) seem to depend on the stimulation site within the STN. We analysed the effects of the position of the stimulation electrode within the motor STN on subjective emotional experience, expressed as emotional valence and arousal ratings to pictures representing primary rewards and aversive fearful stimuli in 20 PD patients. Patients’ ratings from both aversive and erotic stimuli matched the mean ratings from a group of 20 control subjects at similar position within the STN. Patients with electrodes located more posteriorly reported both valence and arousal ratings from both the rewarding and aversive pictures as more extreme. Moreover, posterior electrode positions were associated with a higher occurrence of depression at a long-term follow-up. This brain–behavior relationship suggests a complex emotion topography in the motor part of the STN. Both valence and arousal representations overlapped and were uniformly arranged anterior-posteriorly in a gradient-like manner, suggesting a specific spatial organization needed for the coding of the motivational salience of the stimuli. This finding is relevant for our understanding of neuropsychiatric side effects in STN DBS and potentially for optimal electrode placement.

Highlights

Deep brain stimulation (DBS) of the subthalamic nucleus (STN), which has become a standard treatment for motor complications in Parkinson's disease (PD)[3,4] has provided a unique opportunity to study the functional architecture of the basal ganglia in humans
Considering the functional anatomy of the STN, in this study we further analysed the relationship between the electrode position within the STN and individual affective ratings in PD patients treated with bilateral STN DBS
The electrode position-related effect on the subjective emotional experience was present in both the DBS ON and the OFF conditions which could be a consequence of several mechanisms: (i) surgical intervention, or (ii) due to the long-term structural effects of the DBS electrodes within the brain parenchyma, or (iii) due to the long-term effects of chronic STN DBS34,35

Summary

Introduction

Deep brain stimulation (DBS) of the subthalamic nucleus (STN), which has become a standard treatment for motor complications in Parkinson's disease (PD)[3,4] has provided a unique opportunity to study the functional architecture of the basal ganglia in humans. Despite the high rate of neuropsychiatric side effects and changes in emotional processes found in patients successfully treated by STN DBS for motor complications[20], the effect of the electrode position on subjective emotional experience has not been studied so far. We found the effects of the STN DBS on subjective valence and arousal ratings from affective pictures representing primary rewards and aversive fearful stimuli. Emotional valence and arousal ratings from pictures representing primary rewards (visual sexual stimuli) and aversive fearful stimuli were recorded postoperatively in OFF-medicated PD patients with the stimulation ON and OFF and in matched control subjects. Each STN was transformed into the standardized stereotactic space (Montreal Neurological Institute – MNI)[24] and both the active electrode contacts and the positions of the neurons responding to either emotional valence or arousal from our previous study were plotted together to compare the functional anatomy of emotional valence and arousal on large and small scales

Methods

Results

Discussion

Conclusion