Organization of hippocampal CA3 into correlated cell assemblies supports a stable spatial code

Liron Sheintuch; Nitzan Geva; Daniel Deitch; Alon Rubin; Yaniv Ziv

Organization of hippocampal CA3 into correlated cell assemblies supports a stable spatial code

Liron Sheintuch, Nitzan Geva, Daniel Deitch, Alon Rubin^*, Yaniv Ziv^*

^*Corresponding author for this work

Department of Brain Sciences

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

4 Citations (Scopus)

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Abstract

Hippocampal subfield CA3 is thought to stably store memories in assemblies of recurrently connected cells functioning as a collective. However, the collective hippocampal coding properties that are unique to CA3 and how such properties facilitate the stability or precision of the neural code remain unclear. Here, we performed large-scale Ca2+ imaging in hippocampal CA1 and CA3 of freely behaving mice that repeatedly explored the same, initially novel environments over weeks. CA3 place cells have more precise and more stable tuning and show a higher statistical dependence with their peers compared with CA1 place cells, uncovering a cell assembly organization in CA3. Surprisingly, although tuning precision and long-term stability are correlated, cells with stronger peer dependence exhibit higher stability but not higher precision. Overall, our results expose the three-way relationship between tuning precision, long-term stability, and peer dependence, suggesting that a cell assembly organization underlies long-term storage of information in the hippocampus.

Original language	English
Article number	112119
Number of pages	13
Journal	Cell reports (Cambridge)
Volume	42
Issue number	2
Early online date	17 Feb 2023
Publication status	Published - 28 Feb 2023

Bibliographical note

Y.Z. is Head of the Mike and Valeria Rosenbloom Center for Positive Neuroscience and is supported by grants from the Belle S. and Irving E. Meller Center for the Biology of Aging, European Research Council (ERC-CoG 101001226), Human Frontier Science Program (RGY0069/2017), and Israel Science Foundation (2113/19). We thank Nachum Ulanovsky, Misha Tsodyks, Ofer Yizhar, Tamir Eliav, David Omer, Shaked Palgi, and Natalie Page for helpful advice and comments on the manuscript.
Author contributions : L.S., A.R., and Y.Z. conceived the project. L.S., N.G., and D.D. conducted the experiments. L.S. analyzed the data. L.S., A.R., and Y.Z. wrote and revised the manuscript with input from D.D. and N.G. Y.Z. and A.R. supervised the research. Y.Z. obtained funding.

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title = "Organization of hippocampal CA3 into correlated cell assemblies supports a stable spatial code",

abstract = "Hippocampal subfield CA3 is thought to stably store memories in assemblies of recurrently connected cells functioning as a collective. However, the collective hippocampal coding properties that are unique to CA3 and how such properties facilitate the stability or precision of the neural code remain unclear. Here, we performed large-scale Ca2+ imaging in hippocampal CA1 and CA3 of freely behaving mice that repeatedly explored the same, initially novel environments over weeks. CA3 place cells have more precise and more stable tuning and show a higher statistical dependence with their peers compared with CA1 place cells, uncovering a cell assembly organization in CA3. Surprisingly, although tuning precision and long-term stability are correlated, cells with stronger peer dependence exhibit higher stability but not higher precision. Overall, our results expose the three-way relationship between tuning precision, long-term stability, and peer dependence, suggesting that a cell assembly organization underlies long-term storage of information in the hippocampus.",

author = "Liron Sheintuch and Nitzan Geva and Daniel Deitch and Alon Rubin and Yaniv Ziv",

note = "Y.Z. is Head of the Mike and Valeria Rosenbloom Center for Positive Neuroscience and is supported by grants from the Belle S. and Irving E. Meller Center for the Biology of Aging, European Research Council (ERC-CoG 101001226), Human Frontier Science Program (RGY0069/2017), and Israel Science Foundation (2113/19). We thank Nachum Ulanovsky, Misha Tsodyks, Ofer Yizhar, Tamir Eliav, David Omer, Shaked Palgi, and Natalie Page for helpful advice and comments on the manuscript. Author contributions : L.S., A.R., and Y.Z. conceived the project. L.S., N.G., and D.D. conducted the experiments. L.S. analyzed the data. L.S., A.R., and Y.Z. wrote and revised the manuscript with input from D.D. and N.G. Y.Z. and A.R. supervised the research. Y.Z. obtained funding.",

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AU - Sheintuch, Liron

AU - Geva, Nitzan

AU - Deitch, Daniel

AU - Rubin, Alon

AU - Ziv, Yaniv

N1 - Y.Z. is Head of the Mike and Valeria Rosenbloom Center for Positive Neuroscience and is supported by grants from the Belle S. and Irving E. Meller Center for the Biology of Aging, European Research Council (ERC-CoG 101001226), Human Frontier Science Program (RGY0069/2017), and Israel Science Foundation (2113/19). We thank Nachum Ulanovsky, Misha Tsodyks, Ofer Yizhar, Tamir Eliav, David Omer, Shaked Palgi, and Natalie Page for helpful advice and comments on the manuscript. Author contributions : L.S., A.R., and Y.Z. conceived the project. L.S., N.G., and D.D. conducted the experiments. L.S. analyzed the data. L.S., A.R., and Y.Z. wrote and revised the manuscript with input from D.D. and N.G. Y.Z. and A.R. supervised the research. Y.Z. obtained funding.

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N2 - Hippocampal subfield CA3 is thought to stably store memories in assemblies of recurrently connected cells functioning as a collective. However, the collective hippocampal coding properties that are unique to CA3 and how such properties facilitate the stability or precision of the neural code remain unclear. Here, we performed large-scale Ca2+ imaging in hippocampal CA1 and CA3 of freely behaving mice that repeatedly explored the same, initially novel environments over weeks. CA3 place cells have more precise and more stable tuning and show a higher statistical dependence with their peers compared with CA1 place cells, uncovering a cell assembly organization in CA3. Surprisingly, although tuning precision and long-term stability are correlated, cells with stronger peer dependence exhibit higher stability but not higher precision. Overall, our results expose the three-way relationship between tuning precision, long-term stability, and peer dependence, suggesting that a cell assembly organization underlies long-term storage of information in the hippocampus.

AB - Hippocampal subfield CA3 is thought to stably store memories in assemblies of recurrently connected cells functioning as a collective. However, the collective hippocampal coding properties that are unique to CA3 and how such properties facilitate the stability or precision of the neural code remain unclear. Here, we performed large-scale Ca2+ imaging in hippocampal CA1 and CA3 of freely behaving mice that repeatedly explored the same, initially novel environments over weeks. CA3 place cells have more precise and more stable tuning and show a higher statistical dependence with their peers compared with CA1 place cells, uncovering a cell assembly organization in CA3. Surprisingly, although tuning precision and long-term stability are correlated, cells with stronger peer dependence exhibit higher stability but not higher precision. Overall, our results expose the three-way relationship between tuning precision, long-term stability, and peer dependence, suggesting that a cell assembly organization underlies long-term storage of information in the hippocampus.

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Organization of hippocampal CA3 into correlated cell assemblies supports a stable spatial code

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