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      Deliberation and Procedural Automation on a Two-Step Task for Rats

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          Abstract

          Current theories suggest that decision-making arises from multiple, competing action-selection systems. Rodent studies dissociate deliberation and procedural behavior, and find a transition from procedural to deliberative behavior with experience. However, it remains unknown how this transition from deliberative to procedural control evolves within single trials, or within blocks of repeated choices. We adapted for rats a two-step task which has been used to dissociate model-based from model-free decisions in humans. We found that a mixture of model-based and model-free algorithms was more likely to explain rat choice strategies on the task than either model-based or model-free algorithms alone. This task contained two choices per trial, which provides a more complex and non-discrete per-trial choice structure. This task structure enabled us to evaluate how deliberative and procedural behavior evolved within-trial and within blocks of repeated choice sequences. We found that vicarious trial and error (VTE), a behavioral correlate of deliberation in rodents, was correlated between the two choice points on a given lap. We also found that behavioral stereotypy, a correlate of procedural automation, increased with the number of repeated choices. While VTE at the first choice point increased with the number of repeated choices, VTE at the second choice point did not, and only increased after unexpected transitions within the task. This suggests that deliberation at the beginning of trials may correspond to changes in choice patterns, while mid-trial deliberation may correspond to an interruption of a procedural process.

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          Most cited references51

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          Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point.

          Neural ensembles were recorded from the CA3 region of rats running on T-based decision tasks. Examination of neural representations of space at fast time scales revealed a transient but repeatable phenomenon as rats made a decision: the location reconstructed from the neural ensemble swept forward, first down one path and then the other. Estimated representations were coherent and preferentially swept ahead of the animal rather than behind the animal, implying it represented future possibilities rather than recently traveled paths. Similar phenomena occurred at other important decisions (such as in recovery from an error). Local field potentials from these sites contained pronounced theta and gamma frequencies, but no sharp wave frequencies. Forward-shifted spatial representations were influenced by task demands and experience. These data suggest that the hippocampus does not represent space as a passive computation, but rather that hippocampal spatial processing is an active process likely regulated by cognitive mechanisms.
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            Vicarious trial and error.

            A. Redish (2016)
            When rats come to a decision point, they sometimes pause and look back and forth as if deliberating over the choice; at other times, they proceed as if they have already made their decision. In the 1930s, this pause-and-look behaviour was termed 'vicarious trial and error' (VTE), with the implication that the rat was 'thinking about the future'. The discovery in 2007 that the firing of hippocampal place cells gives rise to alternating representations of each of the potential path options in a serial manner during VTE suggested a possible neural mechanism that could underlie the representations of future outcomes. More-recent experiments examining VTE in rats suggest that there are direct parallels to human processes of deliberative decision making, working memory and mental time travel.
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              Hippocampal theta sequences reflect current goals.

              Hippocampal information processing is discretized by oscillations, and the ensemble activity of place cells is organized into temporal sequences bounded by theta cycles. Theta sequences represent time-compressed trajectories through space. Their forward-directed nature makes them an intuitive candidate mechanism for planning future trajectories, but their connection to goal-directed behavior remains unclear. As rats performed a value-guided decision-making task, the extent to which theta sequences projected ahead of the animal's current location varied on a moment-by-moment basis depending on the rat's goals. Look-ahead extended farther on journeys to distant goals than on journeys to more proximal goals and was predictive of the animal's destination. On arrival at goals, however, look-ahead was similar regardless of where the animal began its journey from. Together, these results provide evidence that hippocampal theta sequences contain information related to goals or intentions, pointing toward a potential spatial basis for planning.
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                Author and article information

                Contributors
                Journal
                Front Integr Neurosci
                Front Integr Neurosci
                Front. Integr. Neurosci.
                Frontiers in Integrative Neuroscience
                Frontiers Media S.A.
                1662-5145
                03 August 2018
                2018
                : 12
                : 30
                Affiliations
                [1] 1Graduate Program in Neuroscience, University of Minnesota Twin Cities Minneapolis, MN, United States
                [2] 2Department of Neuroscience, University of Minnesota Twin Cities Minneapolis, MN, United States
                Author notes

                Edited by: Geoffrey Schoenbaum, University of Maryland, Baltimore, United States

                Reviewed by: Peter Bossaerts, École Polytechnique Fédérale de Lausanne, Switzerland; Nandakumar Narayanan, University of Iowa, United States

                *Correspondence: A. David Redish redish@ 123456umn.edu
                Article
                10.3389/fnint.2018.00030
                6085996
                30123115
                da0484ff-da0b-4b43-ac3c-5c8694e03ec5
                Copyright © 2018 Hasz and Redish.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 08 December 2017
                : 02 July 2018
                Page count
                Figures: 7, Tables: 6, Equations: 17, References: 73, Pages: 19, Words: 13025
                Funding
                Funded by: National Institute of Mental Health 10.13039/100000025
                Award ID: R01-MH112688
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: IGERT DGE-1069104
                Categories
                Neuroscience
                Original Research

                Neurosciences
                decision-making,reinforcement learning,model-based,model-free,vicarious trial and error,path stereotypy

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