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A brainstem integrator for self-location memory and positional homeostasis in zebrafish

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Yang_2022_Cell_Brainstem_integrator_CC.pdf (13.60Mb)
Date
22/12/2022
Author
Yang, En
Zwart, Maarten F.
James, Ben
Rubinov, Mikail
Wei, Ziqiang
Narayan, Sujatha
Vladimirov, Nikita
Mensh, Brett D.
Fitzgerald, James E.
Ahrens, Misha B.
Keywords
Neuroscience
Memory
Neural circuits
Motor control
Brainstem
Navigation
Path integration
Hippocampus
Zebrafish
Inferior olive
Cerebellum
RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
DAS
MCC
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Abstract
To track and control self-location, animals integrate their movements through space. Representations of self-location are observed in the mammalian hippocampal formation, but it is unknown if positional representations exist in more ancient brain regions, how they arise from integrated self-motion, and by what pathways they control locomotion. Here, in a head-fixed, fictive-swimming, virtual-reality preparation, we exposed larval zebrafish to a variety of involuntary displacements. They tracked these displacements and, many seconds later, moved toward their earlier location through corrective swimming (“positional homeostasis”). Whole-brain functional imaging revealed a network in the medulla that stores a memory of location and induces an error signal in the inferior olive to drive future corrective swimming. Optogenetically manipulating medullary integrator cells evoked displacement-memory behavior. Ablating them, or downstream olivary neurons, abolished displacement corrections. These results reveal a multiregional hindbrain circuit in vertebrates that integrates self-motion and stores self-location to control locomotor behavior.
Citation
Yang , E , Zwart , M F , James , B , Rubinov , M , Wei , Z , Narayan , S , Vladimirov , N , Mensh , B D , Fitzgerald , J E & Ahrens , M B 2022 , ' A brainstem integrator for self-location memory and positional homeostasis in zebrafish ' , Cell , vol. 185 , no. 26 , e20 , pp. 5011-5027 . https://doi.org/10.1016/j.cell.2022.11.022
Publication
Cell
Status
Peer reviewed
DOI
https://doi.org/10.1016/j.cell.2022.11.022
ISSN
0092-8674
Type
Journal article
Rights
Copyright © 2022 The Authors. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Description
Funding: This work was supported by the Howard Hughes Medical Institute and by the Simons Foundation (Simons Collaboration on the Global Brain #542943SPI).
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/26685

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