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      Reinforcement learning with associative or discriminative generalization across states and actions: fMRI at 3 T and 7 T

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          Abstract

          The model‐free algorithms of “reinforcement learning” (RL) have gained clout across disciplines, but so too have model‐based alternatives. The present study emphasizes other dimensions of this model space in consideration of associative or discriminative generalization across states and actions. This “generalized reinforcement learning” (GRL) model, a frugal extension of RL, parsimoniously retains the single reward‐prediction error (RPE), but the scope of learning goes beyond the experienced state and action. Instead, the generalized RPE is efficiently relayed for bidirectional counterfactual updating of value estimates for other representations. Aided by structural information but as an implicit rather than explicit cognitive map, GRL provided the most precise account of human behavior and individual differences in a reversal‐learning task with hierarchical structure that encouraged inverse generalization across both states and actions. Reflecting inference that could be true, false (i.e., overgeneralization), or absent (i.e., undergeneralization), state generalization distinguished those who learned well more so than action generalization. With high‐resolution high‐field fMRI targeting the dopaminergic midbrain, the GRL model's RPE signals (alongside value and decision signals) were localized within not only the striatum but also the substantia nigra and the ventral tegmental area, including specific effects of generalization that also extend to the hippocampus. Factoring in generalization as a multidimensional process in value‐based learning, these findings shed light on complexities that, while challenging classic RL, can still be resolved within the bounds of its core computations.

          Abstract

          This “generalized reinforcement learning” (GRL) model, a frugal extension of RL, parsimoniously retains the single reward‐prediction error (RPE), but the scope of learning goes beyond the experienced state and action. Aided by structural information but as an implicit rather than explicit cognitive map, GRL provided the most precise account of human behavior and individual differences in a reversal‐learning task with hierarchical structure that encouraged inverse generalization across both states and actions. With high‐resolution high‐field fMRI targeting the dopaminergic midbrain, the GRL model's RPE signals (alongside value and decision signals) were localized within not only the striatum but also the substantia nigra and the ventral tegmental area, including specific effects of generalization that also extend to the hippocampus.

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                Author and article information

                Contributors
                jcolas@ucsb.edu
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                21 July 2022
                15 October 2022
                : 43
                : 15 ( doiID: 10.1002/hbm.v43.15 )
                : 4750-4790
                Affiliations
                [ 1 ] Department of Psychological and Brain Sciences University of California Santa Barbara California USA
                [ 2 ] Division of the Humanities and Social Sciences California Institute of Technology Pasadena California USA
                [ 3 ] Computation and Neural Systems Program, California Institute of Technology Pasadena California USA
                [ 4 ] Department of Child and Adolescent Psychiatry, Psychotherapy, and Psychosomatics University of Freiburg Freiburg im Breisgau Germany
                [ 5 ] Department of Psychology Columbia University New York New York USA
                [ 6 ] Zuckerman Mind Brain Behavior Institute, Columbia University New York New York USA
                [ 7 ] Center for Science and Society Columbia University New York New York USA
                [ 8 ] Department of Psychology New York University New York New York USA
                [ 9 ] Department of Psychology University of California Los Angeles California USA
                [ 10 ] Department of Bioengineering University of Pennsylvania Philadelphia Pennsylvania USA
                [ 11 ] Department of Psychology University of California Berkeley California USA
                [ 12 ] Department of Psychology University of Pennsylvania Philadelphia Pennsylvania USA
                [ 13 ] Neuroscience Graduate Group University of Pennsylvania Philadelphia Pennsylvania USA
                [ 14 ] Laboratory of Neuro Imaging USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California Los Angeles California USA
                [ 15 ] Department of Neuroscience University of Pennsylvania Philadelphia Pennsylvania USA
                [ 16 ] Department of Electrical and Systems Engineering University of Pennsylvania Philadelphia Pennsylvania USA
                [ 17 ] Department of Neurology University of Pennsylvania Philadelphia Pennsylvania USA
                [ 18 ] Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA
                [ 19 ] Department of Physics and Astronomy University of Pennsylvania Philadelphia Pennsylvania USA
                [ 20 ] Santa Fe Institute Santa Fe New Mexico USA
                [ 21 ] Center for Neural Science New York University New York New York USA
                [ 22 ] Kavli Institute for Brain Science Columbia University New York New York USA
                Author notes
                [*] [* ] Correspondence

                Jaron T. Colas, Department of Psychological and Brain Sciences, University of California, Santa Barbara, CA, USA.

                Email: jcolas@ 123456ucsb.edu

                Author information
                https://orcid.org/0000-0003-1872-7614
                https://orcid.org/0000-0001-6246-1775
                https://orcid.org/0000-0001-9782-1005
                https://orcid.org/0000-0002-4493-6113
                https://orcid.org/0000-0003-1822-0688
                https://orcid.org/0000-0003-3563-6781
                https://orcid.org/0000-0001-9342-9014
                https://orcid.org/0000-0002-4948-5550
                https://orcid.org/0000-0003-1904-1753
                https://orcid.org/0000-0001-7902-3755
                https://orcid.org/0000-0002-6018-0483
                https://orcid.org/0000-0002-6183-4493
                https://orcid.org/0000-0003-0177-7295
                https://orcid.org/0000-0003-4239-4960
                https://orcid.org/0000-0003-4015-3151
                https://orcid.org/0000-0003-0016-3531
                Article
                HBM25988
                10.1002/hbm.25988
                9491297
                35860954
                cc11da19-1036-4f9c-9ed1-69f1de8bf5c3
                © 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 May 2022
                : 19 January 2022
                : 10 June 2022
                Page count
                Figures: 11, Tables: 3, Pages: 41, Words: 41184
                Funding
                Funded by: Army Research Office , doi 10.13039/100000183;
                Award ID: W911NF‑18‑1‑0244
                Award ID: W911NF‑16‑1‑0474
                Award ID: W911NF‑19‑2‑0026
                Funded by: Klingenstein‑Simons Neuroscience Fellowship
                Funded by: National Institute for Mathematical and Biological Synthesis , doi 10.13039/100008947;
                Funded by: National Institute of Biomedical Imaging and Bioengineering , doi 10.13039/100000070;
                Award ID: P41 EB015922
                Funded by: National Institute of Mental Health , doi 10.13039/100000025;
                Award ID: P50 MH094258
                Award ID: R01 MH115557
                Funded by: National Institute on Drug Abuse , doi 10.13039/100000026;
                Award ID: R01 DA040011
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                October 15, 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.8 mode:remove_FC converted:21.09.2022

                Neurology
                cognitive map,counterfactual learning,dopaminergic midbrain,generalization,hippocampus,individual differences,model‐free and model‐based,multifield fmri,reinforcement learning,striatum

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