Journal Article Epublish
PubMed: 42846914 DOI: 10.1093/braincomms/fcag325
Hyperdirect projections from the supplementary motor area mediate subthalamic stimulation effects on movement initiation and inhibition in Parkinson's disease.
Brain Commun 8(5):fcag325
Authors: Garance M Meyer, Marion Albares, Guillaume Lio, Alina Beliakova, Gustavo Polo, Brian Lau, Andreas Horn, Stéphane Thobois, Bénédicte Ballanger, Philippe Boulinguez
Affiliations
- Université Lyon 1, CNRS, INSERM, Centre de Recherche en Neurosciences de Lyon CRNL, UMR 5292, UMR S1028, Bron F-69500, France.
- Harvard Medical School, Boston, MA 02138, USA.
- Brigham and Women's Hospital, Department of Neurology, Center for Brain Circuit Therapeutics, Bos, MA 02115, USA.
- iMIND, Center of Excellence for Autism, le Vinatier Hospital, Bron F-69500, France.
- CNRS, UMR 5229, Institute of Cognitive Science Marc Jeannerod, Bron F-69500, France.
- Hospices Civils de Lyon, Hôpital Neurologique Pierre Wertheimer, Neurochirurgie A, Bron F-69500, France.
- Sorbonne Université, Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Paris 75013, France.
- Network Stimulation Institute, Department of Stereotactic and Functional Neurosurgery, University Hospital Cologne 50937, Germany.
- Hospices Civils de Lyon, Hôpital Neurologique Pierre Wertheimer, Neurologie C, Centre Expert Parkinson, Bron F-69500, France.
Abstract
In Parkinson's disease, subthalamic deep brain stimulation improves movement initiation but can induce impulsivity. The origin of these effects remains unclear. Here, we test the hypothesis that modulation of automatic response inhibition, an underrecognized process that governs the ability to refrain from reacting, accounts for both effects. Nineteen Parkinson's disease patients were assessed for (i) behavioural changes in a simple Go/NoGo task, ON versus OFF deep brain stimulation, (ii) structural connectivity between the stimulated subthalamic region and the supplementary motor complex and (iii) a previously established electroencephalographic marker of automatic response inhibition (the DMF170). Under stimulation, patients exhibited faster reaction times and increased commission errors. These changes were accompanied by an increase in DMF170 amplitude, which correlated with reaction times. Finally, behavioural changes were associated with stimulation volume overlap with fibres connecting the subthalamic nucleus to the supplementary motor complex. Our findings link improved movement initiation and increased impulsivity under stimulation of the subthalamic nucleus to a shared anatomical and functional substrate, namely the subthalamic nucleus-supplementary motor cortex loop supporting automatic response inhibition.
MeSH
Parkinson Disease, Brain, Motor Cortex, Reaction Time, Deep Brain Stimulation, Impulsive Behavior, Movement, Subthalamic Nucleus