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

Author:

Hoy Colin W.1ORCID,de Hemptinne Coralie23ORCID,Wang Sarah S.1ORCID,Harmer Catherine J.4ORCID,Apps Matthew A. J.567ORCID,Husain Masud58ORCID,Starr Philip A.9ORCID,Little Simon1ORCID

Affiliation:

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

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

3. Department of Neurology, University of Florida, Gainesville, FL 32608

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

5. Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom

6. Institute for Mental Health, School of Psychology, University of Birmingham, Birmingham UK B15 2TT, United Kingdom

7. Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham B15 2TT, United Kingdom

8. Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom

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

Abstract

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.

Funder

Wellcome Trust

HHS | NIH | National Institute of Neurological Disorders and Stroke

HHS | NIH | National Institute of Mental Health

UKRI | Biotechnology and Biological Sciences Research Council

Publisher

Proceedings of the National Academy of Sciences

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