Beta and theta oscillations track effort and previous reward in the human basal ganglia and prefrontal cortex during decision making.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
30 Jul 2024
Historique:
medline: 26 7 2024
pubmed: 26 7 2024
entrez: 24 7 2024
Statut: ppublish

Résumé

Choosing whether to exert effort to obtain rewards is fundamental to human motivated behavior. However, the neural dynamics underlying the evaluation of reward and effort in humans is poorly understood. Here, we report an exploratory investigation into this with chronic intracranial recordings from the prefrontal cortex (PFC) and basal ganglia (BG; subthalamic nuclei and globus pallidus) in people with Parkinson's disease performing a decision-making task with offers that varied in levels of reward and physical effort required. This revealed dissociable neural signatures of reward and effort, with BG beta (12 to 20 Hz) oscillations tracking effort on a single-trial basis and PFC theta (4 to 7 Hz) signaling previous trial reward, with no effects of net subjective value. Stimulation of PFC increased overall acceptance of offers and sensitivity to reward while decreasing the impact of effort on choices. This work uncovers oscillatory mechanisms that guide fundamental decisions to exert effort for reward across BG and PFC, supports a causal role of PFC for such choices, and seeds hypotheses for future studies.

Identifiants

pubmed: 39047043
doi: 10.1073/pnas.2322869121
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2322869121

Subventions

Organisme : Wellcome Trust (WT)
ID : 226645/Z/22/Z
Organisme : HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : K23NS120037
Organisme : HHS | NIH | National Institute of Mental Health (NIMH)
ID : F32MH132174
Organisme : UKRI | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/R010668/2

Déclaration de conflit d'intérêts

Competing interests statement:M.H. has received honoraria from Eli Lilley, Otsuka and Sumitomo Pharma for lectures/participation in advisory panels, and is a founding member of the Oxford University spin-out NeuHealth. P.A.S. receives grant support from Medtronic. S.L. has honoraria from Medtronic and is a consultant for Iota Biosciences. All other authors declare no competing interests.

Auteurs

Colin W Hoy (CW)

Department of Neurology, University of California, San Francisco, CA 94143.

Coralie de Hemptinne (C)

Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, FL 32608.
Department of Neurology, University of Florida, Gainesville, FL 32608.

Sarah S Wang (SS)

Department of Neurology, University of California, San Francisco, CA 94143.

Catherine J Harmer (CJ)

Department of Psychiatry, University of Oxford, Oxford OX3 7JX, United Kingdom.

Matthew A J Apps (MAJ)

Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom.
Institute for Mental Health, School of Psychology, University of Birmingham, Birmingham UK B15 2TT, United Kingdom.
Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham B15 2TT, United Kingdom.

Masud Husain (M)

Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom.
Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom.

Philip A Starr (PA)

Department of Neurological Surgery, University of California, San Francisco, CA 94143, United Kingdom.

Simon Little (S)

Department of Neurology, University of California, San Francisco, CA 94143.

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