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 (gamma and high-frequency activity) 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, more prevalent, and appears later across all regions examined. These results suggest brain-wide reward processing, with local high frequency activity 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.Significance Statement Economic decision-making depends on multiple brain areas. However, how neural activity in the human brain supports choices is not well understood, due to the difficulty of measuring human neural activity. Here, we leveraged the rare opportunity to record electrophysiological activity from several human brain regions implicated in decision-making from neurosurgical patients to study the neurophysiological basis of economic decisions. We show that neural activity supporting human economic choices under uncertainty is highly distributed across brain areas. However, different relevant calculations, such as the probability of a win, or the risk of an uncertain choice, are differentially reflected in across brain regions. This study demonstrates the highly distributed, but regionally specific, nature of choices and reward computations in the human brain.