Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues

Torgeir Waaga; Haggai Agmon; Valentin A. Normand; Anne Nagelhus; Richard J. Gardner; May Britt Moser; Edvard I. Moser; Yoram Burak

doi:10.1016/j.neuron.2022.03.011

Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues

Torgeir Waaga, Haggai Agmon^*, Valentin A. Normand, Anne Nagelhus, Richard J. Gardner, May Britt Moser, Edvard I. Moser^*, Yoram Burak^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

The representation of an animal's position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, ensuring that they jointly encode a coherent and smooth trajectory.

Original language	American English
Pages (from-to)	1843-1856.e6
Journal	Neuron
Volume	110
Issue number	11
DOIs	https://doi.org/10.1016/j.neuron.2022.03.011
State	Published - 1 Jun 2022

Bibliographical note

Funding Information:
Y.B. is the incumbent of the William N. Skirball Chair in Neurophysics. This study was supported by a Synergy Grant to Y.B. and E.I.M. from the European Research Council (“ KILONEURONS ,” grant agreement no. 951319 ), by grants to Y.B. from the Israel Science Foundation (grant nos. 1319/13 , 1978/13 , and 1745/18 ), by a grant to Y.B. from the German-Israeli Foundation for Scientific Research and Development , a FRIPRO grant to E.I.M., a Centre of Excellence grant to M.-B.M. and E.I.M., and a National Infrastructure grant to E.I.M. and M.-B.M., all from the Research Council of Norway ( FRIPRO , grant number 286225 ; Centre of Neural Computation , grant number 223262 ; NORBRAIN , grant number 295721 ), the Kavli Foundation (M.-B.M. and E.I.M.), and a direct contribution to M.-B.M. and E.I.M. from the Ministry of Education and Research of Norway. Y.B. acknowledges support from the Gatsby Charitable Foundation . The authors are grateful to Christine Lykken for performing the Neuropixels implantation on one of the animals.

Publisher Copyright:
© 2022 The Author(s)

Keywords

entorhinal cortex
grid cells
neural circuits
neural coding
neural decoding
population coding
spatial coding
spatial memory

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10.1016/j.neuron.2022.03.011

Cite this

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title = "Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues",

abstract = "The representation of an animal's position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, ensuring that they jointly encode a coherent and smooth trajectory.",

keywords = "entorhinal cortex, grid cells, neural circuits, neural coding, neural decoding, population coding, spatial coding, spatial memory",

author = "Torgeir Waaga and Haggai Agmon and Normand, {Valentin A.} and Anne Nagelhus and Gardner, {Richard J.} and Moser, {May Britt} and Moser, {Edvard I.} and Yoram Burak",

note = "Funding Information: Y.B. is the incumbent of the William N. Skirball Chair in Neurophysics. This study was supported by a Synergy Grant to Y.B. and E.I.M. from the European Research Council (“ KILONEURONS ,” grant agreement no. 951319 ), by grants to Y.B. from the Israel Science Foundation (grant nos. 1319/13 , 1978/13 , and 1745/18 ), by a grant to Y.B. from the German-Israeli Foundation for Scientific Research and Development , a FRIPRO grant to E.I.M., a Centre of Excellence grant to M.-B.M. and E.I.M., and a National Infrastructure grant to E.I.M. and M.-B.M., all from the Research Council of Norway ( FRIPRO , grant number 286225 ; Centre of Neural Computation , grant number 223262 ; NORBRAIN , grant number 295721 ), the Kavli Foundation (M.-B.M. and E.I.M.), and a direct contribution to M.-B.M. and E.I.M. from the Ministry of Education and Research of Norway. Y.B. acknowledges support from the Gatsby Charitable Foundation . The authors are grateful to Christine Lykken for performing the Neuropixels implantation on one of the animals. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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AU - Agmon, Haggai

AU - Normand, Valentin A.

AU - Nagelhus, Anne

AU - Gardner, Richard J.

AU - Moser, May Britt

AU - Moser, Edvard I.

AU - Burak, Yoram

N1 - Funding Information: Y.B. is the incumbent of the William N. Skirball Chair in Neurophysics. This study was supported by a Synergy Grant to Y.B. and E.I.M. from the European Research Council (“ KILONEURONS ,” grant agreement no. 951319 ), by grants to Y.B. from the Israel Science Foundation (grant nos. 1319/13 , 1978/13 , and 1745/18 ), by a grant to Y.B. from the German-Israeli Foundation for Scientific Research and Development , a FRIPRO grant to E.I.M., a Centre of Excellence grant to M.-B.M. and E.I.M., and a National Infrastructure grant to E.I.M. and M.-B.M., all from the Research Council of Norway ( FRIPRO , grant number 286225 ; Centre of Neural Computation , grant number 223262 ; NORBRAIN , grant number 295721 ), the Kavli Foundation (M.-B.M. and E.I.M.), and a direct contribution to M.-B.M. and E.I.M. from the Ministry of Education and Research of Norway. Y.B. acknowledges support from the Gatsby Charitable Foundation . The authors are grateful to Christine Lykken for performing the Neuropixels implantation on one of the animals. Publisher Copyright: © 2022 The Author(s)

PY - 2022/6/1

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N2 - The representation of an animal's position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, ensuring that they jointly encode a coherent and smooth trajectory.

AB - The representation of an animal's position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, ensuring that they jointly encode a coherent and smooth trajectory.

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KW - grid cells

KW - neural circuits

KW - neural coding

KW - neural decoding

KW - population coding

KW - spatial coding

KW - spatial memory

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DO - 10.1016/j.neuron.2022.03.011

M3 - Article

C2 - 35385698

AN - SCOPUS:85131130748

SN - 0896-6273

VL - 110

SP - 1843-1856.e6

JO - Neuron

JF - Neuron

IS - 11

ER -

Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues

Abstract

Bibliographical note

Keywords

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