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Reward and punishment differentially recruit cerebellum and medial temporal lobe to facilitate skill memory retention

View ORCID ProfileAdam Steel, Edward H. Silson, Charlotte J. Stagg, Chris I. Baker
doi: https://doi.org/10.1101/243899
Adam Steel
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, OX3 9DU, UK
2Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, 20814
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Edward H. Silson
2Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, 20814
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Charlotte J. Stagg
1Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, OX3 9DU, UK
3Oxford Centre for Human Brain Activity (OHBA), Wellcome Centre for Integrative Neuroimaging, University Department of Psychiatry, University of Oxford, Oxford, UK, OX3 9DU, UK
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Chris I. Baker
2Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, 20814
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Abstract

Reward and punishment shape behavior, but the neural mechanisms underlying their effect on skill learning are not well understood. The premotor cortex (PMC) is known to play a central role in sequence learning and has a diverse set of structural and connections with cortical (e.g. medial temporal/parietal lobes) and subcortical (caudate/cerebellum) memory systems that might be modulated by valenced feedback. Here, we tested whether the functional connectivity of PMC immediately after training with reward or punishment predicted memory retention across two different tasks. Resting-state fMRI was collected before and after 72 participants trained on either a serial reaction time or force-tracking task with reward, punishment, or control feedback. Training-related change in PMC functional connectivity was compared across feedback groups. Reward and punishment differentially affected PMC functional connectivity: PMC-cerebellum connectivity increased following training with reward, while PMC-medial temporal lobe connectivity increased after training with punishment. Moreover, feedback impacted the relationship between PMC-caudate connectivity and 24–48hour skill memory. These results were consistent across the tasks, suggestive of a general, non-task-specific mechanism by which feedback modulates skill learning. These findings illustrate dissociable roles for the medial temporal lobe and cerebellum in skill memory retention and suggest novel ways to optimize behavioral training.

Footnotes

  • ↵$ Joint Senior Authors

  • Competing financial interests: The authors declare no competing financial interests.

  • Acknowledgements: The authors would like to thank Matthew Rushworth for his helpful comments on the manuscript.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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Posted January 05, 2018.
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Reward and punishment differentially recruit cerebellum and medial temporal lobe to facilitate skill memory retention
Adam Steel, Edward H. Silson, Charlotte J. Stagg, Chris I. Baker
bioRxiv 243899; doi: https://doi.org/10.1101/243899
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Reward and punishment differentially recruit cerebellum and medial temporal lobe to facilitate skill memory retention
Adam Steel, Edward H. Silson, Charlotte J. Stagg, Chris I. Baker
bioRxiv 243899; doi: https://doi.org/10.1101/243899

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