Subthalamic nucleus oscillations during facial emotion processing and apathy in Parkinson's disease

Jun Li; Linbin Wang; Yixin Pan; Peng Huang; Lu Xu; Yuyao Zhang; Dirk De Ridder; Valerie Voon; Dianyou Li

doi:10.1016/j.jad.2025.01.005

Subthalamic nucleus oscillations during facial emotion processing and apathy in Parkinson's disease

J Affect Disord. 2025 Jan 4:373:314-324. doi: 10.1016/j.jad.2025.01.005. Online ahead of print.

Authors

Jun Li¹, Linbin Wang², Yixin Pan³, Peng Huang³, Lu Xu³, Yuyao Zhang⁴, Dirk De Ridder⁵, Valerie Voon⁶, Dianyou Li⁷

Affiliations

¹ Center for Functional Neurosurgery, Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; School of Information Science and Technology, ShanghaiTech University, Shanghai, China.
² Center for Functional Neurosurgery, Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.
³ Center for Functional Neurosurgery, Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁴ School of Information Science and Technology, ShanghaiTech University, Shanghai, China.
⁵ Unit of Neurosurgery, Department of Surgical Sciences, University of Otago, Dunedin, Otago, New Zealand.
⁶ Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom; Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China.
⁷ Center for Functional Neurosurgery, Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Electronic address: ldy11483@rjh.com.cn.

PMID: 39761756
DOI: 10.1016/j.jad.2025.01.005

Abstract

Background: Parkinson's disease (PD) is primarily characterized by motor symptoms, but patients also experience a relatively high prevalence of non-motor symptoms, including emotional and cognitive impairments. While the subthalamic nucleus (STN) is a common target for deep brain stimulation to treat motor symptoms in PD, its role in emotion processing is still under investigation. This study examines the subthalamic neural oscillatory activities during facial emotion processing and its association with affective characteristics.

Methods: Twenty PD patients who underwent subthalamic deep brain stimulation surgery performed a facial-expression-recognition task while STN local field potential (LFP) and frontal electroencephalography (EEG) were recorded. The facial-emotion-induced time-frequency decomposition of the STN-LFP and the frontal EEG, as well as the LFP-EEG coherence, were analyzed. Furthermore, the correlation between STN activities and affective characteristics was examined.

Results: Facial expressions elicited increased delta-theta-band and decreased alpha-beta-band activities in STN-LFP. Reduced alpha-beta-band LFP desynchronization was correlated with the severity of apathy. Increased theta-band and decreased alpha-beta-band EEG activities responded to facial emotion. Notably, lower coherence between STN-LFP and frontal EEG in delta-theta-band activity and alpha-band activity correlated with the degree of anhedonia.

Conclusion: These results indicate that subthalamic activities during facial emotion processing are associated with apathy and anhedonia, emphasizing the cognitive-limbic function of STN and its role as a physiological target for apathy neuromodulation in PD.

Keywords: Anhedonia; Apathy; Electroencephalography; Facial emotion; Local field potential; Parkinson's disease; Subthalamic nucleus.