Asymmetric coding of reward prediction errors in human insula and dorsomedial prefrontal cortex

Colin W. Hoy (), David R. Quiroga-Martinez, Eduardo Sandoval, David King-Stephens, Kenneth D. Laxer, Peter Weber, Jack J. Lin and Robert T. Knight
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Colin W. Hoy: University of California, San Francisco
David R. Quiroga-Martinez: University of California, Berkeley
Eduardo Sandoval: University of California, Berkeley
David King-Stephens: California Pacific Medical Center
Kenneth D. Laxer: California Pacific Medical Center
Peter Weber: California Pacific Medical Center
Jack J. Lin: University of California, Davis
Robert T. Knight: University of California, Berkeley

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract The signed value and unsigned salience of reward prediction errors (RPEs) are critical to understanding reinforcement learning (RL) and cognitive control. Dorsomedial prefrontal cortex (dMPFC) and insula (INS) are key regions for integrating reward and surprise information, but conflicting evidence for both signed and unsigned activity has led to multiple proposals for the nature of RPE representations in these brain areas. Recently developed RL models allow neurons to respond differently to positive and negative RPEs. Here, we use intracranially recorded high frequency activity (HFA) to test whether this flexible asymmetric coding strategy captures RPE coding diversity in human INS and dMPFC. At the region level, we found a bias towards positive RPEs in both areas which paralleled behavioral adaptation. At the local level, we found spatially interleaved neural populations responding to unsigned RPE salience and valence-specific positive and negative RPEs. Furthermore, directional connectivity estimates revealed a leading role of INS in communicating positive and unsigned RPEs to dMPFC. These findings support asymmetric coding across distinct but intermingled neural populations as a core principle of RPE processing and inform theories of the role of dMPFC and INS in RL and cognitive control.

Date: 2023
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DOI: 10.1038/s41467-023-44248-1

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