Distributed Intracranial Activity Underlying Human Decision-making Behavior

Abstract

Value-based decision–making involves multiple cortical and subcortical brain areas, but the distributed nature of neurophysiological activity underlying economic choices in the human brain remains largely unexplored. Specifically, the nature of the neurophysiological representation of reward-guided choices, as well as whether they are represented in a subset of reward-related regions or in a more distributed fashion, is unknown. Here, we hypothesize that reward choices, as well as choice-related computations (win probability, risk), are primarily represented in high-frequency neural activity reflecting local cortical processing and that they are highly distributed throughout the human brain, engaging multiple brain regions. To test these hypotheses, we used intracranial recordings from multiple areas (including orbitofrontal, lateral prefrontal, parietal, cingulate cortices as well as subcortical regions such as the hippocampus and amygdala) from neurosurgical patients of both sexes playing a decision-making game. We show that high-frequency activity (HFA; ɣ and HFA) represents both individual choice-related computations (e.g., risk, win probability) and choice information with different prevalence and regional representation. Choice-related computations are locally and unevenly present in multiple brain regions, whereas choice information is widely distributed and more prevalent and appears later across all regions examined. These results suggest brain-wide reward processing, with local HFA reflecting the coalescence of choice-related information into a final choice, and shed light on the distributed nature of neural activity underlying economic choices in the human brain.