Subacute alpha frequency (10Hz) subthalamic stimulation for emotional processing in Parkinson's disease

Linbin Wang; Jun Li; Yixin Pan; Peng Huang; Dianyou Li; Valerie Voon

doi:10.1016/j.brs.2023.08.005

Subacute alpha frequency (10Hz) subthalamic stimulation for emotional processing in Parkinson's disease

Brain Stimul. 2023 Sep-Oct;16(5):1223-1231. doi: 10.1016/j.brs.2023.08.005. Epub 2023 Aug 9.

Authors

Linbin Wang¹, Jun Li², Yixin Pan³, Peng Huang³, Dianyou Li⁴, Valerie Voon⁵

Affiliations

¹ Institute of Science and Technology for Brain-Inspired Intelligence (ISTBI), Fudan University, Shanghai, China; Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
² School of Information Science and Technology, ShanghaiTech University, Shanghai, China.
³ Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁴ Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Electronic address: ldy11483@rjh.com.cn.
⁵ Institute of Science and Technology for Brain-Inspired Intelligence (ISTBI), Fudan University, Shanghai, China; Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom. Electronic address: vv247@cam.ac.uk.

PMID: 37567462
DOI: 10.1016/j.brs.2023.08.005

Abstract

Background: Psychiatric comorbidities are common in Parkinson's disease (PD) and may change with high-frequency stimulation targeting the subthalamic nucleus. Numerous accounts indicate subthalamic alpha-frequency oscillation is implicated in emotional processing. While intermittent alpha-frequency (10Hz) stimulation induces positive emotional effects, with more ventromedial contacts inducing larger effects, little is known about the subacute effect of ventral 10Hz subthalamic stimulation on emotional processing.

Objective/hypothesis: To evaluate the subacute effect of 10Hz stimulation at bilateral ventral subthalamic nucleus on emotional processing in PD patients using an affective task, compared to that of clinical-frequency stimulation and off-stimulation.

Methods: Twenty PD patients with bilateral subthalamic deep brain stimulation for more than six months were tested with the affective task under three stimulation conditions (10Hz, 130Hz, and off-stimulation) in a double-blinded randomized design.

Results: While 130Hz stimulation reduced arousal ratings in all patients, 10Hz stimulation increased arousal selectively in patients with higher depression scores. Furthermore, 10Hz stimulation induced a positive shift in valence rating to negative emotional stimuli in patients with lower apathy scores, and 130Hz stimulation led to more positive valence to emotional stimuli in the patients with higher apathy scores. Notably, we found correlational relationships between stimulation site and affective rating: arousal ratings increase with stimulation from anterior to posterior site, and positive valence ratings increase with stimulation from dorsal to ventral site of the ventral subthalamic nucleus.

Conclusions: Our findings highlight the distinctive role of 10Hz stimulation on subjective emotional experience and unveil the spatial organization of the stimulation effect.

Keywords: Alpha frequency stimulation; Emotional processing; Parkinson's disease; Subthalamic nucleus.

Publication types

Randomized Controlled Trial
Research Support, Non-U.S. Gov't

MeSH terms

Apathy*
Arousal
Deep Brain Stimulation*
Emotions / physiology
Humans
Parkinson Disease* / psychology
Parkinson Disease* / therapy
Subthalamic Nucleus* / physiology

Grants and funding

MR/W020408/1/MRC_/Medical Research Council/United Kingdom