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Three-dimensional head-direction coding in the bat brain

Author

Listed:
  • Arseny Finkelstein

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Dori Derdikman

    (Weizmann Institute of Science, Rehovot 76100, Israel
    Rappaport Faculty of Medicine and Research Institute, Technion – Israel Institute of Technology, Haifa 31096, Israel)

  • Alon Rubin

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Jakob N. Foerster

    (Weizmann Institute of Science, Rehovot 76100, Israel
    Present address: Department of Engineering, University of Cambridge, Cambridge CB2 1PZ, UK.)

  • Liora Las

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Nachum Ulanovsky

    (Weizmann Institute of Science, Rehovot 76100, Israel)

Abstract

Navigation requires a sense of direction (‘compass’), which in mammals is thought to be provided by head-direction cells, neurons that discharge when the animal’s head points to a specific azimuth. However, it remains unclear whether a three-dimensional (3D) compass exists in the brain. Here we conducted neural recordings in bats, mammals well-adapted to 3D spatial behaviours, and found head-direction cells tuned to azimuth, pitch or roll, or to conjunctive combinations of 3D angles, in both crawling and flying bats. Head-direction cells were organized along a functional–anatomical gradient in the presubiculum, transitioning from 2D to 3D representations. In inverted bats, the azimuth-tuning of neurons shifted by 180°, suggesting that 3D head direction is represented in azimuth × pitch toroidal coordinates. Consistent with our toroidal model, pitch-cell tuning was unimodal, circular, and continuous within the available 360° of pitch. Taken together, these results demonstrate a 3D head-direction mechanism in mammals, which could support navigation in 3D space.

Suggested Citation

  • Arseny Finkelstein & Dori Derdikman & Alon Rubin & Jakob N. Foerster & Liora Las & Nachum Ulanovsky, 2015. "Three-dimensional head-direction coding in the bat brain," Nature, Nature, vol. 517(7533), pages 159-164, January.
    • Handle: RePEc:nat:nature:v:517:y:2015:i:7533:d:10.1038_nature14031
    DOI: 10.1038/nature14031
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    Cited by:

    1. Guillaume Viejo & Thomas Cortier & Adrien Peyrache, 2018. "Brain-state invariant thalamo-cortical coordination revealed by non-linear encoders," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-25, March.
    2. M. Jerome Beetz & Christian Kraus & Basil el Jundi, 2023. "Neural representation of goal direction in the monarch butterfly brain," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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