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      Few-shot learning: temporal scaling in behavioral and dopaminergic learning

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          Abstract

          How do we learn associations in the world (e.g., between cues and rewards)? Cue-reward associative learning is controlled in the brain by mesolimbic dopamine 1- 4 . It is widely believed that dopamine drives such learning by conveying a reward prediction error (RPE) in accordance with temporal difference reinforcement learning (TDRL) algorithms 5 . TDRL implementations are “trial-based”: learning progresses sequentially across individual cue-outcome experiences. Accordingly, a foundational assumption—often considered a mere truism—is that the more cue-reward pairings one experiences, the more one learns this association. Here, we disprove this assumption, thereby falsifying a foundational principle of trial-based learning algorithms. Specifically, when a group of head-fixed mice received ten times fewer experiences over the same total time as another, a single experience produced as much learning as ten experiences in the other group. This quantitative scaling also holds for mesolimbic dopaminergic learning, with the increase in learning rate being so high that the group with fewer experiences exhibits dopaminergic learning in as few as four cue-reward experiences and behavioral learning in nine. An algorithm implementing reward-triggered retrospective learning explains these findings. The temporal scaling and few-shot learning observed here fundamentally changes our understanding of the neural algorithms of associative learning.

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          A neural substrate of prediction and reward.

          The capacity to predict future events permits a creature to detect, model, and manipulate the causal structure of its interactions with its environment. Behavioral experiments suggest that learning is driven by changes in the expectations about future salient events such as rewards and punishments. Physiological work has recently complemented these studies by identifying dopaminergic neurons in the primate whose fluctuating output apparently signals changes or errors in the predictions of future salient and rewarding events. Taken together, these findings can be understood through quantitative theories of adaptive optimizing control.
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            Pingouin: statistics in Python

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              Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval.

              The hippocampus is required for the encoding, consolidation and retrieval of event memories. Although the neural mechanisms that underlie these processes are only partially understood, a series of recent papers point to awake memory replay as a potential contributor to both consolidation and retrieval. Replay is the sequential reactivation of hippocampal place cells that represent previously experienced behavioral trajectories and occurs frequently in the awake state, particularly during periods of relative immobility. Awake replay may reflect trajectories through either the current environment or previously visited environments that are spatially remote. The repetition of learned sequences on a compressed time scale is well suited to promote memory consolidation in distributed circuits beyond the hippocampus, suggesting that consolidation occurs in both the awake and sleeping animal. Moreover, sensory information can influence the content of awake replay, suggesting a role for awake replay in memory retrieval.
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                Author and article information

                Journal
                bioRxiv
                BIORXIV
                bioRxiv
                Cold Spring Harbor Laboratory
                31 March 2023
                : 2023.03.31.535173
                Affiliations
                [1 ]Department of Neurology, University of California, San Francisco, CA, USA
                [2 ]University of California, Berkeley, CA, USA
                [3 ]Neuroscience Graduate Program, University of California, San Francisco, CA, USA
                [4 ]Weill Institute for Neurosciences, Kavli Institute for Fundamental Neuroscience, Center for Integrative Neuroscience, University of California, San Francisco, CA, USA
                Author notes

                Author contributions

                D.A.B. and V.M.K.N. conceived the project. D.A.B., H.J., B.W., S.L., and J.R.F. performed experiments. D.A.B. performed analyses. H.J. performed simulations. V.M.K.N. oversaw all aspects of the study. D.A.B. and V.M.K.N. wrote the manuscript with help from all authors.

                Article
                10.1101/2023.03.31.535173
                10081323
                37034619
                7ce576ce-f694-457a-8de2-3d36d4ee6872

                This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.

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