Abstract
Orbitofrontal cortex (OFC) and secondary motor cortex (M2) are both implicated in flexible reward learning but the conditions that differentially recruit these regions are not fully understood. We imaged calcium activity from single neurons in OFC or M2 during de novo learning of uncertain reward probability schedules. Predictions of choice were decoded from M2 neurons with high accuracy under all certainty conditions, but were more accurately decoded from OFC neurons under greater uncertainty. In M2, the proportion of outcome-selective neurons decreased with uncertainty whereas this proportion remained stable in OFC, due to an increased recruitment of reward-selective neurons across levels of uncertainty. Decoding accuracy of both choice and outcome were predicted by indices of flexible strategy like Win-Stay and Lose-Shift in OFC, but not M2. When schedules were experienced in increasing and then decreasing uncertainty, chemogenetic perturbation of M2 and OFC neurons resulted in opposing roles in certain and uncertain conditions, respectively. Our results indicate that M2 neurons are causally involved in learning of more certain conditions, whereas OFC neurons preferentially encode choices and outcomes that foster greater reliance on adaptive strategies under conditions of uncertainty. This reveals a novel functional heterogeneity within frontal cortex in support of flexible learning.
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