Coordinated human prefrontal dynamics sustain task-state representations during learning

Abstract

Making decisions in complex, real-world environments is challenging. Biologically plausible strategies like reinforcement learning (RL) require attention toward reward-predictive stimuli to define task states, yet how attention and decision processes coordinate in the human brain remains unclear. We hypothesized this arises through interactions between orbitofrontal (OFC) value-based mechanisms and lateral prefrontal (LPFC) attention filtering. To test this, we combined behavioral modeling with local field potential (LFP) and single-unit recordings in 22 subjects performing a multidimensional RL task. Reward expectations were encoded in OFC and LPFC, as reflected in high-frequency LFP and OFC single-unit spiking, but modulated by attention only in LPFC. Theta LFPs encoded reward expectations and indexed attention-dependent LPFC-OFC coordination, with value-related coupling emerging pre-choice in high-attention subjects and post-choice in low-attention subjects. These findings show that prefrontal circuits dynamically coordinate to encode attention-weighted value signals, shaping state representations and providing a tractable solution to learning in complex environments.