Within- and across-trial dynamics of human EEG reveal cooperative interplay between reinforcement learning and working memory

Proceedings of the National Academy of Sciences of the United States of America
Anne G E Collins, Michael J Frank

Abstract

Learning from rewards and punishments is essential to survival and facilitates flexible human behavior. It is widely appreciated that multiple cognitive and reinforcement learning systems contribute to decision-making, but the nature of their interactions is elusive. Here, we leverage methods for extracting trial-by-trial indices of reinforcement learning (RL) and working memory (WM) in human electro-encephalography to reveal single-trial computations beyond that afforded by behavior alone. Neural dynamics confirmed that increases in neural expectation were predictive of reduced neural surprise in the following feedback period, supporting central tenets of RL models. Within- and cross-trial dynamics revealed a cooperative interplay between systems for learning, in which WM contributes expectations to guide RL, despite competition between systems during choice. Together, these results provide a deeper understanding of how multiple neural systems interact for learning and decision-making and facilitate analysis of their disruption in clinical populations.

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Citations

Jun 8, 2018·Journal of Cognitive Neuroscience·Harrison RitzAmitai Shenhav
Jun 13, 2019·Cognitive, Affective & Behavioral Neuroscience·Cameron D HassallOlave E Krigolson
Jul 4, 2020·Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology·Quentin J M HuysMichael J Frank
Sep 10, 2020·PLoS Computational Biology·Charley M WuNicolas W Schuck
May 10, 2020·Nature Communications·Christopher W LynnDanielle S Bassett
Sep 3, 2020·Nature Reviews. Neuroscience·Anne G E Collins, Jeffrey Cockburn
May 18, 2019·Translational Neuroscience·Xiaomei Zheng
Aug 20, 2020·Cognitive, Affective & Behavioral Neuroscience·Franz WurmMarco Steinhauser
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Sep 7, 2020·Cortex; a Journal Devoted to the Study of the Nervous System and Behavior·Christian N L Olivers, Pieter R Roelfsema
Jan 28, 2021·ELife·Steven MiletićAndrew Heathcote
Nov 27, 2019·Developmental Cognitive Neuroscience·Kate Nussenbaum, Catherine A Hartley
Dec 13, 2019·Developmental Cognitive Neuroscience·Sarah L MasterAnne G E Collins
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Jul 8, 2021·Cerebral Cortex·Samuel D McDougleAnne G E Collins
Aug 29, 2021·Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology·Anne G E Collins, Amitai Shenhav

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