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Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex

Competing accounts propose that working memory (WM) is subserved either by persistent activity in single neurons or by dynamic (time-varying) activity across a neural population. Here, we compare these hypotheses across four regions of prefrontal cortex (PFC) in an oculomotor-delayed-response task,...

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Autores principales: Cavanagh, Sean E., Towers, John P., Wallis, Joni D., Hunt, Laurence T., Kennerley, Steven W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6115433/
https://www.ncbi.nlm.nih.gov/pubmed/30158519
http://dx.doi.org/10.1038/s41467-018-05873-3
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author Cavanagh, Sean E.
Towers, John P.
Wallis, Joni D.
Hunt, Laurence T.
Kennerley, Steven W.
author_facet Cavanagh, Sean E.
Towers, John P.
Wallis, Joni D.
Hunt, Laurence T.
Kennerley, Steven W.
author_sort Cavanagh, Sean E.
collection PubMed
description Competing accounts propose that working memory (WM) is subserved either by persistent activity in single neurons or by dynamic (time-varying) activity across a neural population. Here, we compare these hypotheses across four regions of prefrontal cortex (PFC) in an oculomotor-delayed-response task, where an intervening cue indicated the reward available for a correct saccade. WM representations were strongest in ventrolateral PFC neurons with higher intrinsic temporal stability (time-constant). At the population-level, although a stable mnemonic state was reached during the delay, this tuning geometry was reversed relative to cue-period selectivity, and was disrupted by the reward cue. Single-neuron analysis revealed many neurons switched to coding reward, rather than maintaining task-relevant spatial selectivity until saccade. These results imply WM is fulfilled by dynamic, population-level activity within high time-constant neurons. Rather than persistent activity supporting stable mnemonic representations that bridge subsequent salient stimuli, PFC neurons may stabilise a dynamic population-level process supporting WM.
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spelling pubmed-61154332018-08-31 Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex Cavanagh, Sean E. Towers, John P. Wallis, Joni D. Hunt, Laurence T. Kennerley, Steven W. Nat Commun Article Competing accounts propose that working memory (WM) is subserved either by persistent activity in single neurons or by dynamic (time-varying) activity across a neural population. Here, we compare these hypotheses across four regions of prefrontal cortex (PFC) in an oculomotor-delayed-response task, where an intervening cue indicated the reward available for a correct saccade. WM representations were strongest in ventrolateral PFC neurons with higher intrinsic temporal stability (time-constant). At the population-level, although a stable mnemonic state was reached during the delay, this tuning geometry was reversed relative to cue-period selectivity, and was disrupted by the reward cue. Single-neuron analysis revealed many neurons switched to coding reward, rather than maintaining task-relevant spatial selectivity until saccade. These results imply WM is fulfilled by dynamic, population-level activity within high time-constant neurons. Rather than persistent activity supporting stable mnemonic representations that bridge subsequent salient stimuli, PFC neurons may stabilise a dynamic population-level process supporting WM. Nature Publishing Group UK 2018-08-29 /pmc/articles/PMC6115433/ /pubmed/30158519 http://dx.doi.org/10.1038/s41467-018-05873-3 Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Cavanagh, Sean E.
Towers, John P.
Wallis, Joni D.
Hunt, Laurence T.
Kennerley, Steven W.
Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
title Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
title_full Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
title_fullStr Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
title_full_unstemmed Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
title_short Reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
title_sort reconciling persistent and dynamic hypotheses of working memory coding in prefrontal cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6115433/
https://www.ncbi.nlm.nih.gov/pubmed/30158519
http://dx.doi.org/10.1038/s41467-018-05873-3
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