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Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model

Navigation is one of the most fundamental skills of animals. During spatial navigation, grid cells in the medial entorhinal cortex process speed and direction of the animal to map the environment. Hippocampal place cells, in turn, encode place using sensory signals and reduce the accumulated error o...

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Autores principales: Fernandez-Leon, Jose A., Uysal, Ahmet Kerim, Ji, Daoyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744848/
https://www.ncbi.nlm.nih.gov/pubmed/36509873
http://dx.doi.org/10.1038/s41598-022-25863-2
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author Fernandez-Leon, Jose A.
Uysal, Ahmet Kerim
Ji, Daoyun
author_facet Fernandez-Leon, Jose A.
Uysal, Ahmet Kerim
Ji, Daoyun
author_sort Fernandez-Leon, Jose A.
collection PubMed
description Navigation is one of the most fundamental skills of animals. During spatial navigation, grid cells in the medial entorhinal cortex process speed and direction of the animal to map the environment. Hippocampal place cells, in turn, encode place using sensory signals and reduce the accumulated error of grid cells for path integration. Although both cell types are part of the path integration system, the dynamic relationship between place and grid cells and the error reduction mechanism is yet to be understood. We implemented a realistic model of grid cells based on a continuous attractor model. The grid cell model was coupled to a place cell model to address their dynamic relationship during a simulated animal’s exploration of a square arena. The grid cell model processed the animal’s velocity and place field information from place cells. Place cells incorporated salient visual features and proximity information with input from grid cells to define their place fields. Grid cells had similar spatial phases but a diversity of spacings and orientations. To determine the role of place cells in error reduction for path integration, the animal’s position estimates were decoded from grid cell activities with and without the place field input. We found that the accumulated error was reduced as place fields emerged during the exploration. Place fields closer to the animal’s current location contributed more to the error reduction than remote place fields. Place cells’ fields encoding space could function as spatial anchoring signals for precise path integration by grid cells.
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spelling pubmed-97448482022-12-14 Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model Fernandez-Leon, Jose A. Uysal, Ahmet Kerim Ji, Daoyun Sci Rep Article Navigation is one of the most fundamental skills of animals. During spatial navigation, grid cells in the medial entorhinal cortex process speed and direction of the animal to map the environment. Hippocampal place cells, in turn, encode place using sensory signals and reduce the accumulated error of grid cells for path integration. Although both cell types are part of the path integration system, the dynamic relationship between place and grid cells and the error reduction mechanism is yet to be understood. We implemented a realistic model of grid cells based on a continuous attractor model. The grid cell model was coupled to a place cell model to address their dynamic relationship during a simulated animal’s exploration of a square arena. The grid cell model processed the animal’s velocity and place field information from place cells. Place cells incorporated salient visual features and proximity information with input from grid cells to define their place fields. Grid cells had similar spatial phases but a diversity of spacings and orientations. To determine the role of place cells in error reduction for path integration, the animal’s position estimates were decoded from grid cell activities with and without the place field input. We found that the accumulated error was reduced as place fields emerged during the exploration. Place fields closer to the animal’s current location contributed more to the error reduction than remote place fields. Place cells’ fields encoding space could function as spatial anchoring signals for precise path integration by grid cells. Nature Publishing Group UK 2022-12-12 /pmc/articles/PMC9744848/ /pubmed/36509873 http://dx.doi.org/10.1038/s41598-022-25863-2 Text en © The Author(s) 2022 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
Fernandez-Leon, Jose A.
Uysal, Ahmet Kerim
Ji, Daoyun
Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
title Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
title_full Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
title_fullStr Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
title_full_unstemmed Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
title_short Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
title_sort place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744848/
https://www.ncbi.nlm.nih.gov/pubmed/36509873
http://dx.doi.org/10.1038/s41598-022-25863-2
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