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Neural landscape diffusion resolves conflicts between needs across time

Animals perform flexible goal-directed behaviours to satisfy their basic physiological needs(1–12). However, little is known about how unitary behaviours are chosen under conflicting needs. Here we reveal principles by which the brain resolves such conflicts between needs across time. We developed a...

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Autores principales: Richman, Ethan B., Ticea, Nicole, Allen, William E., Deisseroth, Karl, Luo, Liqun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10651489/
https://www.ncbi.nlm.nih.gov/pubmed/37938783
http://dx.doi.org/10.1038/s41586-023-06715-z
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author Richman, Ethan B.
Ticea, Nicole
Allen, William E.
Deisseroth, Karl
Luo, Liqun
author_facet Richman, Ethan B.
Ticea, Nicole
Allen, William E.
Deisseroth, Karl
Luo, Liqun
author_sort Richman, Ethan B.
collection PubMed
description Animals perform flexible goal-directed behaviours to satisfy their basic physiological needs(1–12). However, little is known about how unitary behaviours are chosen under conflicting needs. Here we reveal principles by which the brain resolves such conflicts between needs across time. We developed an experimental paradigm in which a hungry and thirsty mouse is given free choices between equidistant food and water. We found that mice collect need-appropriate rewards by structuring their choices into persistent bouts with stochastic transitions. High-density electrophysiological recordings during this behaviour revealed distributed single neuron and neuronal population correlates of a persistent internal goal state guiding future choices of the mouse. We captured these phenomena with a mathematical model describing a global need state that noisily diffuses across a shifting energy landscape. Model simulations successfully predicted behavioural and neural data, including population neural dynamics before choice transitions and in response to optogenetic thirst stimulation. These results provide a general framework for resolving conflicts between needs across time, rooted in the emergent properties of need-dependent state persistence and noise-driven shifts between behavioural goals.
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spelling pubmed-106514892023-11-08 Neural landscape diffusion resolves conflicts between needs across time Richman, Ethan B. Ticea, Nicole Allen, William E. Deisseroth, Karl Luo, Liqun Nature Article Animals perform flexible goal-directed behaviours to satisfy their basic physiological needs(1–12). However, little is known about how unitary behaviours are chosen under conflicting needs. Here we reveal principles by which the brain resolves such conflicts between needs across time. We developed an experimental paradigm in which a hungry and thirsty mouse is given free choices between equidistant food and water. We found that mice collect need-appropriate rewards by structuring their choices into persistent bouts with stochastic transitions. High-density electrophysiological recordings during this behaviour revealed distributed single neuron and neuronal population correlates of a persistent internal goal state guiding future choices of the mouse. We captured these phenomena with a mathematical model describing a global need state that noisily diffuses across a shifting energy landscape. Model simulations successfully predicted behavioural and neural data, including population neural dynamics before choice transitions and in response to optogenetic thirst stimulation. These results provide a general framework for resolving conflicts between needs across time, rooted in the emergent properties of need-dependent state persistence and noise-driven shifts between behavioural goals. Nature Publishing Group UK 2023-11-08 2023 /pmc/articles/PMC10651489/ /pubmed/37938783 http://dx.doi.org/10.1038/s41586-023-06715-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Richman, Ethan B.
Ticea, Nicole
Allen, William E.
Deisseroth, Karl
Luo, Liqun
Neural landscape diffusion resolves conflicts between needs across time
title Neural landscape diffusion resolves conflicts between needs across time
title_full Neural landscape diffusion resolves conflicts between needs across time
title_fullStr Neural landscape diffusion resolves conflicts between needs across time
title_full_unstemmed Neural landscape diffusion resolves conflicts between needs across time
title_short Neural landscape diffusion resolves conflicts between needs across time
title_sort neural landscape diffusion resolves conflicts between needs across time
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10651489/
https://www.ncbi.nlm.nih.gov/pubmed/37938783
http://dx.doi.org/10.1038/s41586-023-06715-z
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