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A brainstem integrator for self-localization and positional homeostasis

View ORCID ProfileEn Yang, View ORCID ProfileMaarten F. Zwart, View ORCID ProfileMikail Rubinov, View ORCID ProfileBenjamin James, View ORCID ProfileZiqiang Wei, View ORCID ProfileSujatha Narayan, View ORCID ProfileNikita Vladimirov, View ORCID ProfileBrett D. Mensh, View ORCID ProfileJames E. Fitzgerald, View ORCID ProfileMisha B. Ahrens
doi: https://doi.org/10.1101/2021.11.26.468907
En Yang
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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  • For correspondence: yange@janelia.hhmi.org ahrensm@janelia.hhmi.org
Maarten F. Zwart
2School of Psychology and Neuroscience, Centre for Biophotonics, University of St Andrews, UK
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Mikail Rubinov
3Department of Biomedical Engineering, Vanderbilt University, TN, USA
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Benjamin James
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Ziqiang Wei
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Sujatha Narayan
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Nikita Vladimirov
4Brain Research Institute, University of Zurich, Switzerland
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Brett D. Mensh
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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James E. Fitzgerald
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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Misha B. Ahrens
1Janelia Research Campus, Howard Hughes Medical Institute, USA
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  • For correspondence: yange@janelia.hhmi.org ahrensm@janelia.hhmi.org
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Abstract

To accurately track self-location, animals need to integrate their movements through space. In amniotes, representations of self-location have been found in regions such as the hippocampus. It is unknown whether more ancient brain regions contain such representations and by which pathways they may drive locomotion. Fish displaced by water currents must prevent uncontrolled drift to potentially dangerous areas. We found that larval zebrafish track such movements and can later swim back to their earlier location. Whole-brain functional imaging revealed the circuit enabling this process of positional homeostasis. Position-encoding brainstem neurons integrate optic flow, then bias future swimming to correct for past displacements by modulating inferior olive and cerebellar activity. Manipulation of position-encoding or olivary neurons abolished positional homeostasis or evoked behavior as if animals had experienced positional shifts. These results reveal a multiregional hindbrain circuit in vertebrates for optic flow integration, memory of self-location, and its neural pathway to behavior.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 27, 2021.
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A brainstem integrator for self-localization and positional homeostasis
En Yang, Maarten F. Zwart, Mikail Rubinov, Benjamin James, Ziqiang Wei, Sujatha Narayan, Nikita Vladimirov, Brett D. Mensh, James E. Fitzgerald, Misha B. Ahrens
bioRxiv 2021.11.26.468907; doi: https://doi.org/10.1101/2021.11.26.468907
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A brainstem integrator for self-localization and positional homeostasis
En Yang, Maarten F. Zwart, Mikail Rubinov, Benjamin James, Ziqiang Wei, Sujatha Narayan, Nikita Vladimirov, Brett D. Mensh, James E. Fitzgerald, Misha B. Ahrens
bioRxiv 2021.11.26.468907; doi: https://doi.org/10.1101/2021.11.26.468907

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