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Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task

Hippocampal place cells show position-specific activity thought to reflect a self-localization signal. Several reports also point to some form of goal encoding by place cells. We investigated this by asking whether they also encode the value of spatial goals, which is crucial information for optimiz...

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Autores principales: Duvelle, Éléonore, Grieves, Roddy M., Hok, Vincent, Poucet, Bruno, Arleo, Angelo, Jeffery, Kate J., Save, Etienne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6435828/
https://www.ncbi.nlm.nih.gov/pubmed/30696727
http://dx.doi.org/10.1523/JNEUROSCI.1578-18.2018
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author Duvelle, Éléonore
Grieves, Roddy M.
Hok, Vincent
Poucet, Bruno
Arleo, Angelo
Jeffery, Kate J.
Save, Etienne
author_facet Duvelle, Éléonore
Grieves, Roddy M.
Hok, Vincent
Poucet, Bruno
Arleo, Angelo
Jeffery, Kate J.
Save, Etienne
author_sort Duvelle, Éléonore
collection PubMed
description Hippocampal place cells show position-specific activity thought to reflect a self-localization signal. Several reports also point to some form of goal encoding by place cells. We investigated this by asking whether they also encode the value of spatial goals, which is crucial information for optimizing goal-directed navigation. We used a continuous place navigation task in which male rats navigate to one of two (freely chosen) unmarked locations and wait, triggering the release of reward, which is then located and consumed elsewhere. This allows sampling of place fields and dissociates spatial goal from reward consumption. The two goals varied in the amount of reward provided, allowing assessment of whether the rats factored goal value into their navigational choice and of possible neural correlates of this value. Rats successfully learned the task, indicating goal localization, and they preferred higher-value goals, indicating processing of goal value. Replicating previous findings, there was goal-related activity in the out-of-field firing of CA1 place cells, with a ramping-up of firing rate during the waiting period, but no general overrepresentation of goals by place fields, an observation that we extended to CA3 place cells. Importantly, place cells were not modulated by goal value. This suggests that dorsal hippocampal place cells encode space independently of its associated value despite the effect of that value on spatial behavior. Our findings are consistent with a model of place cells in which they provide a spontaneously constructed value-free spatial representation rather than encoding other navigationally relevant but nonspatial information. SIGNIFICANCE STATEMENT We investigated whether hippocampal place cells, which compute a self-localization signal, also encode the relative value of places, which is essential information for optimal navigation. When choosing between two spatial goals of different value, rats preferred the higher-value goal. We saw out-of-field goal firing in place cells, replicating previous observations that the cells are influenced by the goal, but their activity was not modulated by the value of these goals. Our results suggest that place cells do not encode all of the navigationally relevant aspects of a place, but instead form a value-free “map” that links to such aspects in other parts of the brain.
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spelling pubmed-64358282019-04-17 Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task Duvelle, Éléonore Grieves, Roddy M. Hok, Vincent Poucet, Bruno Arleo, Angelo Jeffery, Kate J. Save, Etienne J Neurosci Research Articles Hippocampal place cells show position-specific activity thought to reflect a self-localization signal. Several reports also point to some form of goal encoding by place cells. We investigated this by asking whether they also encode the value of spatial goals, which is crucial information for optimizing goal-directed navigation. We used a continuous place navigation task in which male rats navigate to one of two (freely chosen) unmarked locations and wait, triggering the release of reward, which is then located and consumed elsewhere. This allows sampling of place fields and dissociates spatial goal from reward consumption. The two goals varied in the amount of reward provided, allowing assessment of whether the rats factored goal value into their navigational choice and of possible neural correlates of this value. Rats successfully learned the task, indicating goal localization, and they preferred higher-value goals, indicating processing of goal value. Replicating previous findings, there was goal-related activity in the out-of-field firing of CA1 place cells, with a ramping-up of firing rate during the waiting period, but no general overrepresentation of goals by place fields, an observation that we extended to CA3 place cells. Importantly, place cells were not modulated by goal value. This suggests that dorsal hippocampal place cells encode space independently of its associated value despite the effect of that value on spatial behavior. Our findings are consistent with a model of place cells in which they provide a spontaneously constructed value-free spatial representation rather than encoding other navigationally relevant but nonspatial information. SIGNIFICANCE STATEMENT We investigated whether hippocampal place cells, which compute a self-localization signal, also encode the relative value of places, which is essential information for optimal navigation. When choosing between two spatial goals of different value, rats preferred the higher-value goal. We saw out-of-field goal firing in place cells, replicating previous observations that the cells are influenced by the goal, but their activity was not modulated by the value of these goals. Our results suggest that place cells do not encode all of the navigationally relevant aspects of a place, but instead form a value-free “map” that links to such aspects in other parts of the brain. Society for Neuroscience 2019-03-27 /pmc/articles/PMC6435828/ /pubmed/30696727 http://dx.doi.org/10.1523/JNEUROSCI.1578-18.2018 Text en Copyright © 2019 Duvelle et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Duvelle, Éléonore
Grieves, Roddy M.
Hok, Vincent
Poucet, Bruno
Arleo, Angelo
Jeffery, Kate J.
Save, Etienne
Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task
title Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task
title_full Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task
title_fullStr Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task
title_full_unstemmed Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task
title_short Insensitivity of Place Cells to the Value of Spatial Goals in a Two-Choice Flexible Navigation Task
title_sort insensitivity of place cells to the value of spatial goals in a two-choice flexible navigation task
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6435828/
https://www.ncbi.nlm.nih.gov/pubmed/30696727
http://dx.doi.org/10.1523/JNEUROSCI.1578-18.2018
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