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Dynamic modulation of subthalamic nucleus activity facilitates adaptive behavior.

Authors :
Herz, Damian M.
Bange, Manuel
Gonzalez-Escamilla, Gabriel
Auer, Miriam
Muthuraman, Muthuraman
Glaser, Martin
Bogacz, Rafal
Pogosyan, Alek
Tan, Huiling
Groppa, Sergiu
Brown, Peter
Source :
PLoS Biology; 6/1/2023, Vol. 21 Issue 6, p1-32, 32p, 1 Color Photograph, 1 Diagram, 4 Graphs
Publication Year :
2023

Abstract

Adapting actions to changing goals and environments is central to intelligent behavior. There is evidence that the basal ganglia play a crucial role in reinforcing or adapting actions depending on their outcome. However, the corresponding electrophysiological correlates in the basal ganglia and the extent to which these causally contribute to action adaptation in humans is unclear. Here, we recorded electrophysiological activity and applied bursts of electrical stimulation to the subthalamic nucleus, a core area of the basal ganglia, in 16 patients with Parkinson's disease (PD) on medication using temporarily externalized deep brain stimulation (DBS) electrodes. Patients as well as 16 age- and gender-matched healthy participants attempted to produce forces as close as possible to a target force to collect a maximum number of points. The target force changed over trials without being explicitly shown on the screen so that participants had to infer target force based on the feedback they received after each movement. Patients and healthy participants were able to adapt their force according to the feedback they received (P < 0.001). At the neural level, decreases in subthalamic beta (13 to 30 Hz) activity reflected poorer outcomes and stronger action adaptation in 2 distinct time windows (P<subscript>cluster-corrected</subscript> < 0.05). Stimulation of the subthalamic nucleus reduced beta activity and led to stronger action adaptation if applied within the time windows when subthalamic activity reflected action outcomes and adaptation (P<subscript>cluster-corrected</subscript> < 0.05). The more the stimulation volume was connected to motor cortex, the stronger was this behavioral effect (P<subscript>corrected</subscript> = 0.037). These results suggest that dynamic modulation of the subthalamic nucleus and interconnected cortical areas facilitates adaptive behavior. This study shows that activity in the subthalamic nucleus reflects action outcomes and consequent adaptation in humans. This can be modified through bursts of electrical stimulation, with the potential to restore healthy brain function in people with neurological disorders like Parkinson's disease. [ABSTRACT FROM AUTHOR]

Details

Language :
English
ISSN :
15449173
Volume :
21
Issue :
6
Database :
Complementary Index
Journal :
PLoS Biology
Publication Type :
Academic Journal
Accession number :
164067046
Full Text :
https://doi.org/10.1371/journal.pbio.3002140