The neural code of reward anticipation in human orbitofrontal cortex

TLDR

Reward outcomes must be precisely anticipated for optimal choice, yet single‑cell studies in OFC reveal a heterogeneous coding scheme that differs from fMRI findings and aligns with animal electrophysiology showing distributed, opposing neural populations. The study asks how such anticipated outcomes are represented in the brain. Multivariate fMRI pattern analysis in the OFC revealed that reward value of sensory cues can be decoded, that anticipation patterns resemble those during reward receipt, and that the similarity predicts behavior, thereby aligning human and animal reward coding and showing OFC value representations are independent of anticipation or receipt.

Abstract

An optimal choice among alternative behavioral options requires precise anticipatory representations of their possible outcomes. A fundamental question is how such anticipated outcomes are represented in the brain. Reward coding at the level of single cells in the orbitofrontal cortex (OFC) follows a more heterogeneous coding scheme than suggested by studies using functional MRI (fMRI) in humans. Using a combination of multivariate pattern classification and fMRI we show that the reward value of sensory cues can be decoded from distributed fMRI patterns in the OFC. This distributed representation is compatible with previous reports from animal electrophysiology that show that reward is encoded by different neural populations with opposing coding schemes. Importantly, the fMRI patterns representing specific values during anticipation are similar to those that emerge during the receipt of reward. Furthermore, we show that the degree of this coding similarity is related to subjects’ ability to use value information to guide behavior. These findings narrow the gap between reward coding in humans and animals and corroborate the notion that value representations in OFC are independent of whether reward is anticipated or actually received.