Human orbitofrontal cortex signals decision outcomes to sensory cortex during flexible tactile learning

Abstract

The ability to respond adaptively to an ever-changing environment relies on the orbitofrontal cortex (OFC). The OFC sends neuroanatomical projections to the primary sensory cortex - yet the contribution of this top-down feedback projection to behavioural flexibility in humans is unknown. Inspired from recent rodent studies, we here combined a probabilistic Go/No-Go tactile reversal learning task with functional magnetic resonance imaging (fMRI) in human participants to investigate how OFC interacts with the primary somatosensory cortex (S1) to promote flexible decision-making. We show a distinct task-dependent engagement of S1 and lateral OFC: while the lateral OFC responds saliently and transiently to rule-switches, activity in S1 reflects initial task learning and persistent engagement after each rule-switch event. Unlike the contralateral S1, which represents the sensory input, activity in ipsilateral S1 mirrors the outcome value during re-learning. Importantly, the implementation of this outcome-selectivity in ipsilateral S1 is dependent on top-down 'teaching' signals from lateral OFC. Overall, as in mice, we show comparable physiological and computational signatures of how dynamic interactions between OFC and sensory cortex support flexible decision-making in humans.