Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation

Naeem Muhammad; Saurabh Sonkusare; Qiong Ding; Linbin Wang; Alekhya Mandali; Yi Jie Zhao; Bomin Sun; Dianyou Li; Valerie Voon

doi:10.3389/fnhum.2023.1181635

Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation

Front Hum Neurosci. 2023 Jul 27:17:1181635. doi: 10.3389/fnhum.2023.1181635. eCollection 2023.

Authors

Naeem Muhammad^#^{1

2}, Saurabh Sonkusare^#^{1

2

3}, Qiong Ding¹, Linbin Wang^{1

3

4}, Alekhya Mandali², Yi Jie Zhao^{3

4}, Bomin Sun¹, Dianyou Li¹, Valerie Voon^{1

2

3

4}

Affiliations

¹ Department of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
² Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.
³ Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China.
⁴ Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, Shanghai, China.

^# Contributed equally.

Abstract

Introduction: Deep brain stimulation (DBS) studies in Parkinson's Disease (PD) targeting the subthalamic nucleus (STN) have characterized its spectral properties across cognitive processes. In emotional evaluation tasks, specific alpha frequency (8-12 Hz) event-related de-synchronization (ERD) (reduced power) has been demonstrated. The time-locked stimulation of STN relative to stimuli onset has shown subjective positive valence shifts with 10 Hz but not with 130 Hz. However, neurophysiological effects of stimulation on power modulation have not been investigated. We aim to investigate effects of acute stimulation of the right STN on concurrent power modulation in the contralateral STN and frontal scalp EEG. From our previous study, we had a strong a priori hypothesis that negative imagery without stimulation would be associated with alpha ERD; negative imagery with 130 Hz stimulation would be also associated with alpha ERD given the lack of its effect on subjective valence ratings; negative imagery with 10 Hz stimulation was to be associated with enhanced alpha power given the shift in behavioral valence ratings.

Methods: Twenty-four subjects with STN DBS underwent emotional picture-viewing tasks comprising neutral and negative pictures. In a subset of these subjects, the negative images were associated with time-locked acute stimulation at either 10 or 130 Hz. Power of signals was estimated relative to the baseline and subjected to non-parametric statistical testing.

Results: As hypothesized, in 130 Hz stimulation condition, we show a decrease in alpha power to negative vs. neutral images irrespective of stimulation. In contrast, this alpha power decrease was no longer evident in the negative 10 Hz stimulation condition consistent with a predicted increase in alpha power. Greater beta power in the 10 Hz stimulation condition along with correlations between beta power across the 10 Hz stimulation and unstimulated conditions suggest physiological and cognitive generalization effects.

Conclusion: Acute alpha-specific frequency stimulation presumably was associated with a loss of this expected decrease or desynchronization in alpha power to negative images suggesting the capacity to facilitate the synchronization of alpha and enhance power. Acute time-locked stimulation has the potential to provide causal insights into the spectral frequencies and temporal dynamics of emotional processing.

Keywords: acute stimulation; alpha frequency; deep brain stimulation (DBS); emotion; event related (de)/synchronization.

Abstract

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