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Uncovering 2-D toroidal representations in grid cell ensemble activity during 1-D behavior

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  • Erik Hermansen

    (NTNU)

  • David A. Klindt

    (NTNU
    Cold Spring Harbor Laboratory)

  • Benjamin A. Dunn

    (NTNU)

Abstract

Minimal experiments, such as head-fixed wheel-running and sleep, offer experimental advantages but restrict the amount of observable behavior, making it difficult to classify functional cell types. Arguably, the grid cell, and its striking periodicity, would not have been discovered without the perspective provided by free behavior in an open environment. Here, we show that by shifting the focus from single neurons to populations, we change the minimal experimental complexity required. We identify grid cell modules and show that the activity covers a similar, stable toroidal state space during wheel running as in open field foraging. Trajectories on grid cell tori correspond to single trial runs in virtual reality and path integration in the dark, and the alignment of the representation rapidly shifts with changes in experimental conditions. Thus, we provide a methodology to discover and study complex internal representations in even the simplest of experiments.

Suggested Citation

  • Erik Hermansen & David A. Klindt & Benjamin A. Dunn, 2024. "Uncovering 2-D toroidal representations in grid cell ensemble activity during 1-D behavior," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49703-1
    DOI: 10.1038/s41467-024-49703-1
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    References listed on IDEAS

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    1. Nathaniel J. Killian & Michael J. Jutras & Elizabeth A. Buffalo, 2012. "A map of visual space in the primate entorhinal cortex," Nature, Nature, vol. 491(7426), pages 761-764, November.
    2. Michael W. Dorrity & Lauren M. Saunders & Christine Queitsch & Stanley Fields & Cole Trapnell, 2020. "Dimensionality reduction by UMAP to visualize physical and genetic interactions," Nature Communications, Nature, vol. 11(1), pages 1-6, December.
    3. Hanne Stensola & Tor Stensola & Trygve Solstad & Kristian Frøland & May-Britt Moser & Edvard I. Moser, 2012. "The entorhinal grid map is discretized," Nature, Nature, vol. 492(7427), pages 72-78, December.
    4. Steffen Schneider & Jin Hwa Lee & Mackenzie Weygandt Mathis, 2023. "Learnable latent embeddings for joint behavioural and neural analysis," Nature, Nature, vol. 617(7960), pages 360-368, May.
    5. Dmitry Kobak & Philipp Berens, 2019. "The art of using t-SNE for single-cell transcriptomics," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    6. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
    7. James J. Jun & Nicholas A. Steinmetz & Joshua H. Siegle & Daniel J. Denman & Marius Bauza & Brian Barbarits & Albert K. Lee & Costas A. Anastassiou & Alexandru Andrei & Çağatay Aydın & Mladen Barbic &, 2017. "Fully integrated silicon probes for high-density recording of neural activity," Nature, Nature, vol. 551(7679), pages 232-236, November.
    8. Richard J. Gardner & Erik Hermansen & Marius Pachitariu & Yoram Burak & Nils A. Baas & Benjamin A. Dunn & May-Britt Moser & Edvard I. Moser, 2022. "Toroidal topology of population activity in grid cells," Nature, Nature, vol. 602(7895), pages 123-128, February.
    9. Soledad Gonzalo Cogno & Horst A. Obenhaus & Ane Lautrup & R. Irene Jacobsen & Claudia Clopath & Sebastian O. Andersson & Flavio Donato & May-Britt Moser & Edvard I. Moser, 2024. "Minute-scale oscillatory sequences in medial entorhinal cortex," Nature, Nature, vol. 625(7994), pages 338-344, January.
    10. Pierre-Yves Jacob & Fabrizio Capitano & Bruno Poucet & Etienne Save & Francesca Sargolini, 2019. "Path integration maintains spatial periodicity of grid cell firing in a 1D circular track," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    11. Alon Rubin & Liron Sheintuch & Noa Brande-Eilat & Or Pinchasof & Yoav Rechavi & Nitzan Geva & Yaniv Ziv, 2019. "Revealing neural correlates of behavior without behavioral measurements," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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