The ability to respond flexibly to an ever-changing environment relies on the orbitofrontal cortex (OFC). However, how the OFC associates sensory information with predicted outcomes to enable flexible sensory learning in humans remains elusive. Here, we combine a probabilistic tactile reversal learning task with functional magnetic resonance imaging (fMRI) to investigate how lateral OFC (lOFC) interacts with the primary somatosensory cortex (S1) to guide flexible tactile learning in humans. fMRI results reveal that lOFC and S1 exhibit distinct task-dependent engagement: while the lOFC responds transiently to unexpected outcomes immediately following reversals, S1 is persistently engaged during re-learning. Unlike the contralateral stimulus-selective S1, activity in ipsilateral S1 mirrors the outcomes of behavior during re-learning, closely related to top-down signals from lOFC. These findings suggest that lOFC contributes to teaching signals to dynamically update representations in sensory areas, which implement computations critical for adaptive behavior.
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.
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