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The role of the orbitofrontal cortex in creating cognitive maps

Kauê Machado Costa, Robert Scholz, Kevin Lloyd, Perla Moreno-Castilla, Matthew P. H. Gardner, Peter Dayan, Geoffrey Schoenbaum
doi: https://doi.org/10.1101/2022.01.25.477716
Kauê Machado Costa
1National Institute on Drug Abuse Intramural Research Program, National Institutes of Health, Baltimore, MD, 21224, USA
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  • For correspondence: kaue.m.costa@gmail.com geoffrey.schoenbaum@nih.gov
Robert Scholz
2Max Planck Institute for Biological Cybernetics, Tübingen, 72076, Germany
3Max Planck School of Cognition, Leipzig, 04103, Germany
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Kevin Lloyd
2Max Planck Institute for Biological Cybernetics, Tübingen, 72076, Germany
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Perla Moreno-Castilla
4National Institute on Aging Intramural Research Program, National Institutes of Health, Baltimore, MD, 21224, USA
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Matthew P. H. Gardner
5Concordia University, Montreal, QC, 7141, Canada
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Peter Dayan
2Max Planck Institute for Biological Cybernetics, Tübingen, 72076, Germany
6University of Tübingen, Tübingen, 72074, Germany
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Geoffrey Schoenbaum
1National Institute on Drug Abuse Intramural Research Program, National Institutes of Health, Baltimore, MD, 21224, USA
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  • For correspondence: kaue.m.costa@gmail.com geoffrey.schoenbaum@nih.gov
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Abstract

We use internal models of the external world to guide behavior, but little is known about how these cognitive maps are created. The orbitofrontal cortex (OFC) is typically thought to access these maps to support model-based decision-making, but it has recently been proposed that its critical contribution may be instead to integrate information into existing and new models. We tested between these alternatives using an outcome-specific devaluation task and a high-potency chemogenetic approach. We found that selectively inactivating OFC principal neurons when rats learned distinct cue-outcome associations, but prior to outcome devaluation, disrupted subsequent model-based inference, confirming that the OFC is critical for creating new cognitive maps. However, OFC inactivation surprisingly led to generalized devaluation. Using a novel reinforcement learning framework, we demonstrate that this effect is best explained not by a switch to a model-free system, as would be traditionally assumed, but rather by a circumscribed deficit in defining credit assignment precision during model construction. We conclude that the critical contribution of the OFC to learning is regulating the specificity of associations that comprise cognitive maps.

One Sentence Summary OFC inactivation impairs learning of new specific cue-outcome associations without disrupting model-based learning in general.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://colab.research.google.com/drive/1VYRAnvAO8OmzQpVaJe5radKIZnpEn638?usp=sharing

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 26, 2022.
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The role of the orbitofrontal cortex in creating cognitive maps
Kauê Machado Costa, Robert Scholz, Kevin Lloyd, Perla Moreno-Castilla, Matthew P. H. Gardner, Peter Dayan, Geoffrey Schoenbaum
bioRxiv 2022.01.25.477716; doi: https://doi.org/10.1101/2022.01.25.477716
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The role of the orbitofrontal cortex in creating cognitive maps
Kauê Machado Costa, Robert Scholz, Kevin Lloyd, Perla Moreno-Castilla, Matthew P. H. Gardner, Peter Dayan, Geoffrey Schoenbaum
bioRxiv 2022.01.25.477716; doi: https://doi.org/10.1101/2022.01.25.477716

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