Jessica L Bowersock, Scott A Wylie, Ahmad Alhourani, Ajmal Zemmar, Victoria Holiday, Peter Hedera, Travis Stewart, Elizabeth Bridwell, Isabelle Hattab, Beatrice Ugiliweneza, Joseph S Neimat, Nelleke C van Wouwe
{"title":"Theta and beta power in the subthalamic nucleus responds to conflict across subregions and hemispheres.","authors":"Jessica L Bowersock, Scott A Wylie, Ahmad Alhourani, Ajmal Zemmar, Victoria Holiday, Peter Hedera, Travis Stewart, Elizabeth Bridwell, Isabelle Hattab, Beatrice Ugiliweneza, Joseph S Neimat, Nelleke C van Wouwe","doi":"10.1093/braincomms/fcaf021","DOIUrl":null,"url":null,"abstract":"<p><p>The subthalamic nucleus is thought to play a crucial role in controlling impulsive actions. Networked among the basal ganglia and receiving input from several cortical areas, the subthalamic nucleus is well positioned to influence action selection when faced with competing and conflicting action outcomes. The purpose of this study was to test the dissociable roles of the dorsal and ventral aspects of the subthalamic nucleus during action conflict in patients with Parkinson's disease undergoing intraoperative neurophysiological recording and to explore a potential mechanism for this inhibitory control. We hypothesized that modulations of neurophysiological activity during action conflict would be more pronounced in the dorsal subthalamic nucleus compared with the ventral subthalamic nucleus, due to the dissociation of cortical afferents to subthalamic nucleus subregions and previous findings of deep brain stimulation targeting subthalamic nucleus subregions in Parkinson's disease. We recorded neurophysiological activity while 10 participants with Parkinson's disease performed the Simon task during deep brain stimulation surgery. Response-locked local field potentials in the theta and beta band (associated with conflict control and movement inhibition, respectively) were analysed across subthalamic nucleus subregions and hemispheres relative to the motor response (ipsilateral/contralateral). In the presence of action conflict, the dorsal subthalamic nucleus, connected to cortical motor regions, exhibited larger theta power relative to the ventral subthalamic nucleus subregion, which is linked to the limbic circuits (<i>P</i> < 0.05). This evidence supports independent subregion function in conflict control. However, both subregions had relatively increased beta power for conflict trials compared with non-conflict in the hemisphere ipsilateral to the motor response. The conflict-related beta modulation was not present in the contralateral hemisphere. This indicates the importance of the ipsilateral hemisphere in the inhibition of incorrect action impulses. Additionally, higher intertrial beta power in the ventral subregion correlated with reduced accuracy on conflict trials, which we propose, could serve as a biomarker for impaired task performance. The results of the study support the existence of a functional dissociation within subthalamic nucleus subregions, emphasizing the role of the dorsal subthalamic nucleus in modulating action conflict.</p>","PeriodicalId":93915,"journal":{"name":"Brain communications","volume":"7 1","pages":"fcaf021"},"PeriodicalIF":4.1000,"publicationDate":"2025-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11775628/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/braincomms/fcaf021","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The subthalamic nucleus is thought to play a crucial role in controlling impulsive actions. Networked among the basal ganglia and receiving input from several cortical areas, the subthalamic nucleus is well positioned to influence action selection when faced with competing and conflicting action outcomes. The purpose of this study was to test the dissociable roles of the dorsal and ventral aspects of the subthalamic nucleus during action conflict in patients with Parkinson's disease undergoing intraoperative neurophysiological recording and to explore a potential mechanism for this inhibitory control. We hypothesized that modulations of neurophysiological activity during action conflict would be more pronounced in the dorsal subthalamic nucleus compared with the ventral subthalamic nucleus, due to the dissociation of cortical afferents to subthalamic nucleus subregions and previous findings of deep brain stimulation targeting subthalamic nucleus subregions in Parkinson's disease. We recorded neurophysiological activity while 10 participants with Parkinson's disease performed the Simon task during deep brain stimulation surgery. Response-locked local field potentials in the theta and beta band (associated with conflict control and movement inhibition, respectively) were analysed across subthalamic nucleus subregions and hemispheres relative to the motor response (ipsilateral/contralateral). In the presence of action conflict, the dorsal subthalamic nucleus, connected to cortical motor regions, exhibited larger theta power relative to the ventral subthalamic nucleus subregion, which is linked to the limbic circuits (P < 0.05). This evidence supports independent subregion function in conflict control. However, both subregions had relatively increased beta power for conflict trials compared with non-conflict in the hemisphere ipsilateral to the motor response. The conflict-related beta modulation was not present in the contralateral hemisphere. This indicates the importance of the ipsilateral hemisphere in the inhibition of incorrect action impulses. Additionally, higher intertrial beta power in the ventral subregion correlated with reduced accuracy on conflict trials, which we propose, could serve as a biomarker for impaired task performance. The results of the study support the existence of a functional dissociation within subthalamic nucleus subregions, emphasizing the role of the dorsal subthalamic nucleus in modulating action conflict.