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Environment geometry alters subiculum boundary vector cell receptive fields in adulthood and early development

Author

Listed:
  • Laurenz Muessig

    (University College London)

  • Fabio Ribeiro Rodrigues

    (University College London)

  • Tale L. Bjerknes

    (Norwegian University of Science and Technology)

  • Benjamin W. Towse

    (University College London)

  • Caswell Barry

    (University College London)

  • Neil Burgess

    (University College London
    University College London)

  • Edvard I. Moser

    (Norwegian University of Science and Technology)

  • May-Britt Moser

    (Norwegian University of Science and Technology)

  • Francesca Cacucci

    (Physiology and Pharmacology; University College London)

  • Thomas J. Wills

    (University College London)

Abstract

Boundaries to movement form a specific class of landmark information used for navigation: Boundary Vector Cells (BVCs) are neurons which encode an animal’s location as a vector displacement from boundaries. Here we characterise the prevalence and spatial tuning of subiculum BVCs in adult and developing male rats, and investigate the relationship between BVC spatial firing and boundary geometry. BVC directional tunings align with environment walls in squares, but are uniformly distributed in circles, demonstrating that environmental geometry alters BVC receptive fields. Inserted barriers uncover both excitatory and inhibitory components to BVC receptive fields, demonstrating that inhibitory inputs contribute to BVC field formation. During post-natal development, subiculum BVCs mature slowly, contrasting with the earlier maturation of boundary-responsive cells in upstream Entorhinal Cortex. However, Subiculum and Entorhinal BVC receptive fields are altered by boundary geometry as early as tested, suggesting this is an inherent feature of the hippocampal representation of space.

Suggested Citation

  • Laurenz Muessig & Fabio Ribeiro Rodrigues & Tale L. Bjerknes & Benjamin W. Towse & Caswell Barry & Neil Burgess & Edvard I. Moser & May-Britt Moser & Francesca Cacucci & Thomas J. Wills, 2024. "Environment geometry alters subiculum boundary vector cell receptive fields in adulthood and early development," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45098-1
    DOI: 10.1038/s41467-024-45098-1
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    References listed on IDEAS

    as
    1. Julija Krupic & Marius Bauza & Stephen Burton & Caswell Barry & John O’Keefe, 2015. "Grid cell symmetry is shaped by environmental geometry," Nature, Nature, vol. 518(7538), pages 232-235, February.
    2. Øyvind Arne Høydal & Emilie Ranheim Skytøen & Sebastian Ola Andersson & May-Britt Moser & Edvard I. Moser, 2019. "Object-vector coding in the medial entorhinal cortex," Nature, Nature, vol. 568(7752), pages 400-404, April.
    3. Matthias Stangl & Uros Topalovic & Cory S. Inman & Sonja Hiller & Diane Villaroman & Zahra M. Aghajan & Leonardo Christov-Moore & Nicholas R. Hasulak & Vikram R. Rao & Casey H. Halpern & Dawn Eliashiv, 2021. "Boundary-anchored neural mechanisms of location-encoding for self and others," Nature, Nature, vol. 589(7842), pages 420-425, January.
    4. Tor Stensola & Hanne Stensola & May-Britt Moser & Edvard I. Moser, 2015. "Shearing-induced asymmetry in entorhinal grid cells," Nature, Nature, vol. 518(7538), pages 207-212, February.
    5. 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.
    6. 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.
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