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A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex

Dopamine is required for working memory, but how it modulates the large-scale cortex is unknown. Here, we report that dopamine receptor density per neuron, measured by autoradiography, displays a macroscopic gradient along the macaque cortical hierarchy. This gradient is incorporated in a connectome...

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Autores principales: Froudist-Walsh, Sean, Bliss, Daniel P., Ding, Xingyu, Rapan, Lucija, Niu, Meiqi, Knoblauch, Kenneth, Zilles, Karl, Kennedy, Henry, Palomero-Gallagher, Nicola, Wang, Xiao-Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8571070/
https://www.ncbi.nlm.nih.gov/pubmed/34536352
http://dx.doi.org/10.1016/j.neuron.2021.08.024
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author Froudist-Walsh, Sean
Bliss, Daniel P.
Ding, Xingyu
Rapan, Lucija
Niu, Meiqi
Knoblauch, Kenneth
Zilles, Karl
Kennedy, Henry
Palomero-Gallagher, Nicola
Wang, Xiao-Jing
author_facet Froudist-Walsh, Sean
Bliss, Daniel P.
Ding, Xingyu
Rapan, Lucija
Niu, Meiqi
Knoblauch, Kenneth
Zilles, Karl
Kennedy, Henry
Palomero-Gallagher, Nicola
Wang, Xiao-Jing
author_sort Froudist-Walsh, Sean
collection PubMed
description Dopamine is required for working memory, but how it modulates the large-scale cortex is unknown. Here, we report that dopamine receptor density per neuron, measured by autoradiography, displays a macroscopic gradient along the macaque cortical hierarchy. This gradient is incorporated in a connectome-based large-scale cortex model endowed with multiple neuron types. The model captures an inverted U-shaped dependence of working memory on dopamine and spatial patterns of persistent activity observed in over 90 experimental studies. Moreover, we show that dopamine is crucial for filtering out irrelevant stimuli by enhancing inhibition from dendrite-targeting interneurons. Our model revealed that an activity-silent memory trace can be realized by facilitation of inter-areal connections and that adjusting cortical dopamine induces a switch from this internal memory state to distributed persistent activity. Our work represents a cross-level understanding from molecules and cell types to recurrent circuit dynamics underlying a core cognitive function distributed across the primate cortex.
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spelling pubmed-85710702021-11-06 A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex Froudist-Walsh, Sean Bliss, Daniel P. Ding, Xingyu Rapan, Lucija Niu, Meiqi Knoblauch, Kenneth Zilles, Karl Kennedy, Henry Palomero-Gallagher, Nicola Wang, Xiao-Jing Neuron Article Dopamine is required for working memory, but how it modulates the large-scale cortex is unknown. Here, we report that dopamine receptor density per neuron, measured by autoradiography, displays a macroscopic gradient along the macaque cortical hierarchy. This gradient is incorporated in a connectome-based large-scale cortex model endowed with multiple neuron types. The model captures an inverted U-shaped dependence of working memory on dopamine and spatial patterns of persistent activity observed in over 90 experimental studies. Moreover, we show that dopamine is crucial for filtering out irrelevant stimuli by enhancing inhibition from dendrite-targeting interneurons. Our model revealed that an activity-silent memory trace can be realized by facilitation of inter-areal connections and that adjusting cortical dopamine induces a switch from this internal memory state to distributed persistent activity. Our work represents a cross-level understanding from molecules and cell types to recurrent circuit dynamics underlying a core cognitive function distributed across the primate cortex. 2021-09-17 2021-11-03 /pmc/articles/PMC8571070/ /pubmed/34536352 http://dx.doi.org/10.1016/j.neuron.2021.08.024 Text en https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ).
spellingShingle Article
Froudist-Walsh, Sean
Bliss, Daniel P.
Ding, Xingyu
Rapan, Lucija
Niu, Meiqi
Knoblauch, Kenneth
Zilles, Karl
Kennedy, Henry
Palomero-Gallagher, Nicola
Wang, Xiao-Jing
A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
title A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
title_full A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
title_fullStr A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
title_full_unstemmed A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
title_short A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
title_sort dopamine gradient controls access to distributed working memory in the large-scale monkey cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8571070/
https://www.ncbi.nlm.nih.gov/pubmed/34536352
http://dx.doi.org/10.1016/j.neuron.2021.08.024
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