Decoding the neural dynamics of free choice in humans

PLoS Biol. 2020 Dec 10;18(12):e3000864. doi: 10.1371/journal.pbio.3000864. eCollection 2020 Dec.

Abstract

How do we choose a particular action among equally valid alternatives? Nonhuman primate findings have shown that decision-making implicates modulations in unit firing rates and local field potentials (LFPs) across frontal and parietal cortices. Yet the electrophysiological brain mechanisms that underlie free choice in humans remain ill defined. Here, we address this question using rare intracerebral electroencephalography (EEG) recordings in surgical epilepsy patients performing a delayed oculomotor decision task. We find that the temporal dynamics of high-gamma (HG, 60-140 Hz) neural activity in distinct frontal and parietal brain areas robustly discriminate free choice from instructed saccade planning at the level of single trials. Classification analysis was applied to the LFP signals to isolate decision-related activity from sensory and motor planning processes. Compared with instructed saccades, free-choice trials exhibited delayed and longer-lasting HG activity during the delay period. The temporal dynamics of the decision-specific sustained HG activity indexed the unfolding of a deliberation process, rather than memory maintenance. Taken together, these findings provide the first direct electrophysiological evidence in humans for the role of sustained high-frequency neural activation in frontoparietal cortex in mediating the intrinsically driven process of freely choosing among competing behavioral alternatives.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain / physiology
  • Brain Mapping / methods
  • Cerebral Cortex / physiology
  • Choice Behavior / physiology*
  • Decision Making / physiology*
  • Electroencephalography / methods*
  • Female
  • Frontal Lobe / physiology
  • Gamma Rhythm / physiology
  • Humans
  • Male
  • Neurons / physiology
  • Parietal Lobe / physiology
  • Personal Autonomy
  • Photic Stimulation
  • Psychomotor Performance / physiology
  • Saccades / physiology

Grants and funding

KJ is supported by funding from the Canada Research Chairs program and a Discovery Grant (RGPIN-2015-04854) from the Natural Sciences and Engineering Research Council of Canada, a New Investigators Award from the Fonds de Recherche du Québec - Nature et Technologies (2018-NC-206005) and an IVADO- Apogée fundamental research project grant. TT was supported by IVADO Excellence Scholarship – PhD. JPL received funding from HBP Grant Agreements No. 785907 (SGA2) and No. 7202070 (SGA1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.