An independent coding scheme for idiothetic distance in the hippocampus

Self-location and navigation are crucial to daily life, and their disruption is particularly disabling. The hippocampus is central to this process as well as episodic memory. Hippocampal place cells are spatially selective, increasing their activity in specific locations. When external landmarks are...

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Veröffentlicht in:Current biology Jg. 35; H. 17; S. 4199
Hauptverfasser: Nordlund, Mathilde, Levernier, Nicolas, Trippa, Massimiliano, Bourboulou, Romain, Marti, Geoffrey, Monasson, Rémi, Rouault, Hervé, Epsztein, Jérôme, Koenig-Gambini, Julie
Format: Journal Article
Sprache:Englisch
Veröffentlicht: England 08.09.2025
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ISSN:1879-0445, 1879-0445
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Abstract Self-location and navigation are crucial to daily life, and their disruption is particularly disabling. The hippocampus is central to this process as well as episodic memory. Hippocampal place cells are spatially selective, increasing their activity in specific locations. When external landmarks are scarce, place cells use self-motion (idiothetic) information to track location based on distance traveled (distance coding). Distance coding may be particularly relevant to episodic memory. However, the determinants of distance coding are poorly understood. Here, we used virtual reality, electrophysiological recordings in mice, and local cue manipulations to isolate and characterize hippocampal distance coding. In cue-poor conditions, a global distance coding scheme dominated hippocampal activity with high distance indices in all place cells, including both superficial and deep CA1 pyramidal cells. The mapping of distance onto a low-dimensional manifold and rigid distance relationships between place fields are compatible with attractor dynamics similar to those observed for grid cells. Inactivation of the medial septum (MS), which disrupts grid cells, significantly reduced both distance coding and rigid distance dynamics, suggesting an alteration (but not complete abolition) of the underlying attractor. By contrast, place cell coding was also influenced by local visual cues in cue-rich environments, notably deep CA1 pyramidal cells, and this persisted under MS inactivation. We propose that grid cells and associated rigid attractor dynamics predominantly contribute to hippocampal distance coding.
AbstractList Self-location and navigation are crucial to daily life, and their disruption is particularly disabling. The hippocampus is central to this process as well as episodic memory. Hippocampal place cells are spatially selective, increasing their activity in specific locations. When external landmarks are scarce, place cells use self-motion (idiothetic) information to track location based on distance traveled (distance coding). Distance coding may be particularly relevant to episodic memory. However, the determinants of distance coding are poorly understood. Here, we used virtual reality, electrophysiological recordings in mice, and local cue manipulations to isolate and characterize hippocampal distance coding. In cue-poor conditions, a global distance coding scheme dominated hippocampal activity with high distance indices in all place cells, including both superficial and deep CA1 pyramidal cells. The mapping of distance onto a low-dimensional manifold and rigid distance relationships between place fields are compatible with attractor dynamics similar to those observed for grid cells. Inactivation of the medial septum (MS), which disrupts grid cells, significantly reduced both distance coding and rigid distance dynamics, suggesting an alteration (but not complete abolition) of the underlying attractor. By contrast, place cell coding was also influenced by local visual cues in cue-rich environments, notably deep CA1 pyramidal cells, and this persisted under MS inactivation. We propose that grid cells and associated rigid attractor dynamics predominantly contribute to hippocampal distance coding.Self-location and navigation are crucial to daily life, and their disruption is particularly disabling. The hippocampus is central to this process as well as episodic memory. Hippocampal place cells are spatially selective, increasing their activity in specific locations. When external landmarks are scarce, place cells use self-motion (idiothetic) information to track location based on distance traveled (distance coding). Distance coding may be particularly relevant to episodic memory. However, the determinants of distance coding are poorly understood. Here, we used virtual reality, electrophysiological recordings in mice, and local cue manipulations to isolate and characterize hippocampal distance coding. In cue-poor conditions, a global distance coding scheme dominated hippocampal activity with high distance indices in all place cells, including both superficial and deep CA1 pyramidal cells. The mapping of distance onto a low-dimensional manifold and rigid distance relationships between place fields are compatible with attractor dynamics similar to those observed for grid cells. Inactivation of the medial septum (MS), which disrupts grid cells, significantly reduced both distance coding and rigid distance dynamics, suggesting an alteration (but not complete abolition) of the underlying attractor. By contrast, place cell coding was also influenced by local visual cues in cue-rich environments, notably deep CA1 pyramidal cells, and this persisted under MS inactivation. We propose that grid cells and associated rigid attractor dynamics predominantly contribute to hippocampal distance coding.
Self-location and navigation are crucial to daily life, and their disruption is particularly disabling. The hippocampus is central to this process as well as episodic memory. Hippocampal place cells are spatially selective, increasing their activity in specific locations. When external landmarks are scarce, place cells use self-motion (idiothetic) information to track location based on distance traveled (distance coding). Distance coding may be particularly relevant to episodic memory. However, the determinants of distance coding are poorly understood. Here, we used virtual reality, electrophysiological recordings in mice, and local cue manipulations to isolate and characterize hippocampal distance coding. In cue-poor conditions, a global distance coding scheme dominated hippocampal activity with high distance indices in all place cells, including both superficial and deep CA1 pyramidal cells. The mapping of distance onto a low-dimensional manifold and rigid distance relationships between place fields are compatible with attractor dynamics similar to those observed for grid cells. Inactivation of the medial septum (MS), which disrupts grid cells, significantly reduced both distance coding and rigid distance dynamics, suggesting an alteration (but not complete abolition) of the underlying attractor. By contrast, place cell coding was also influenced by local visual cues in cue-rich environments, notably deep CA1 pyramidal cells, and this persisted under MS inactivation. We propose that grid cells and associated rigid attractor dynamics predominantly contribute to hippocampal distance coding.
Author Nordlund, Mathilde
Bourboulou, Romain
Monasson, Rémi
Koenig-Gambini, Julie
Trippa, Massimiliano
Marti, Geoffrey
Epsztein, Jérôme
Levernier, Nicolas
Rouault, Hervé
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  givenname: Nicolas
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  organization: Institute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems, Aix-Marseille University, INSERM UMR1249, Parc Scientifique de Luminy, 163 route de Luminy, 13273 Marseille, France; Aix-Marseille University, Université de Toulon, CNRS, CPT (UMR 7332), Parc Scientifique de Luminy, 163 route de Luminy, 13273 Marseille, France
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– sequence: 8
  givenname: Jérôme
  surname: Epsztein
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  organization: Institute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems, Aix-Marseille University, INSERM UMR1249, Parc Scientifique de Luminy, 163 route de Luminy, 13273 Marseille, France; Institut Universitaire de France, 1 rue Descartes, 75231 Paris, France. Electronic address: julie.koenig@inserm.fr
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Issue 17
Keywords hippocampus
path integration
place cells
grid cells
distance coding
medial septum
cognitive map
Language English
License Copyright © 2025 The Authors. Published by Elsevier Inc. All rights reserved.
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Snippet Self-location and navigation are crucial to daily life, and their disruption is particularly disabling. The hippocampus is central to this process as well as...
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SubjectTerms Animals
CA1 Region, Hippocampal - physiology
Cues
Grid Cells - physiology
Hippocampus - physiology
Male
Mice
Mice, Inbred C57BL
Place Cells - physiology
Pyramidal Cells - physiology
Septal Nuclei - physiology
Spatial Navigation - physiology
Virtual Reality
Title An independent coding scheme for idiothetic distance in the hippocampus
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