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Research Articles, Behavioral/Cognitive

Neural index of reinforcement learning predicts improved stimulus-response retention under high working memory load

Rachel Rac-Lubashevsky, Anna Cremer, Anne Collins, Michael J Frank and Lars Schwabe
Journal of Neuroscience 17 March 2023, JN-RM-1274-22; DOI: https://doi.org/10.1523/JNEUROSCI.1274-22.2023
Rachel Rac-Lubashevsky
1Department of Cognitive, Linguistic & Psychological Sciences, Brown University, Providence, Rhode Island, United States of America
2Carney Institute for Brain Science, Brown University, Providence, Rhode Island, United States of America
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Anna Cremer
3Department of Cognitive Psychology, Universitat Hamburg 20146, Germany
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Anne Collins
4Department of Psychology, University of California, Berkeley, United States
5Helen Wills Neuroscience Institute, University of California, Berkeley, United States
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Michael J Frank
1Department of Cognitive, Linguistic & Psychological Sciences, Brown University, Providence, Rhode Island, United States of America
2Carney Institute for Brain Science, Brown University, Providence, Rhode Island, United States of America
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Lars Schwabe
3Department of Cognitive Psychology, Universitat Hamburg 20146, Germany
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Abstract

Human learning and decision making is supported by multiple systems operating in parallel. Recent studies isolating the contributions of reinforcement learning (RL) and working memory (WM) have revealed a trade-off between the two. An interactive WM-RL computational model predicts that while high WM load slows behavioral acquisition, it also induces larger prediction errors in the RL system that enhance robustness and retention of learned behaviors. Here we tested this account by parametrically manipulating WM load during RL in conjunction with EEG, in both male and female participants, and administered two surprise memory tests. We further leveraged single trial decoding of EEG signatures of RL and WM to determine whether their interaction predicted robust retention. Consistent with the model, behavioral learning was slower for associations acquired under higher load but showed parametrically improved future retention. This paradoxical result was mirrored by EEG indices of RL, which were strengthened under higher WM loads and predictive of more robust future behavioral retention of learned stimulus-response contingencies. We further tested whether stress alters the ability to shift between the two systems strategically to maximize immediate learning versus retention of information and found that induced stress had only a limited effect on this trade-off. The present results offer a deeper understanding of the cooperative interaction between WM and RL and show that relying on WM can benefit the rapid acquisition of choice behavior during learning but impairs retention.

SIGNIFICANCE STATEMENT:

Successful learning is achieved by the joint contribution of the dopaminergic reinforcement learning (RL) system and working memory (WM). The cooperative WMRL model was productive in improving our understanding of the interplay between the two systems during learning, demonstrating that reliance on RL computations is modulated by WM load. However, the role of WM/RL systems in the retention of learned stimulus-response associations remained unestablished. Our results show that increased neural signatures of learning, indicative of greater RL computation, under high WM load also predicted better stimulus-response retention. This result supports a trade-off between the two systems, where degraded WM increases RL processing which improves retention. Notably, we show that this cooperative interplay remains largely unaffected by acute stress.

Footnotes

  • The authors declare no competing interests.

  • This research was funded by a grant of the Landesforschungsfoerdung Hamburg, Germany (LFF FV 38) to L.S and by R01 MH084840-08A1 to MJF.

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Neural index of reinforcement learning predicts improved stimulus-response retention under high working memory load
Rachel Rac-Lubashevsky, Anna Cremer, Anne Collins, Michael J Frank, Lars Schwabe
Journal of Neuroscience 17 March 2023, JN-RM-1274-22; DOI: 10.1523/JNEUROSCI.1274-22.2023

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Neural index of reinforcement learning predicts improved stimulus-response retention under high working memory load
Rachel Rac-Lubashevsky, Anna Cremer, Anne Collins, Michael J Frank, Lars Schwabe
Journal of Neuroscience 17 March 2023, JN-RM-1274-22; DOI: 10.1523/JNEUROSCI.1274-22.2023
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