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Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish

View ORCID ProfileIris Odstrcil, Mariela D. Petkova, Martin Haesemeyer, Jonathan Boulanger-Weill, Maxim Nikitchenko, James A. Gagnon, Pablo Oteiza, Richard Schalek, Adi Peleg, Ruben Portugues, Jeff Lichtman, Florian Engert
doi: https://doi.org/10.1101/2021.05.04.442674
Iris Odstrcil
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
2Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
11Friedrich Miescher Institute for Biomedical Research, Basel, 4056, Switzerland
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  • ORCID record for Iris Odstrcil
  • For correspondence: iris.odstrcil@protonmail.com
Mariela D. Petkova
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
2Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
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Martin Haesemeyer
3The Ohio State University, Department of Neuroscience, Columbus, Ohio, 43210, USA
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Jonathan Boulanger-Weill
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
2Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
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Maxim Nikitchenko
4Duke University School of Medicine, Durham, North Carolina, 27707, USA
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James A. Gagnon
5School of Biological Sciences, University of Utah, Salt Lake City, Utah, 84112, USA
6Center for Cell & Genome Science, University of Utah, Salt Lake City, Utah, 84112, USA
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Pablo Oteiza
7Max Planck Institute for Ornithology, Flow Sensing Research Group, Seewiesen, 82319, Germany
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Richard Schalek
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
2Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
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Adi Peleg
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
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Ruben Portugues
8Institute of Neuroscience, Technical University of Munich, Munich, 80333, Germany
9Max Planck Institute of Neurobiology, Research Group of Sensorimotor Control, Martinsried, 82152, Germany
10Munich Cluster for Systems Neurology (SyNergy), Munich, 81377, Germany
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Jeff Lichtman
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
2Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
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Florian Engert
1Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
2Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, Massachusetts, 02138, USA
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Abstract

All animals need to differentiate between exafferent stimuli, which are caused by the environment, and reafferent stimuli, which are caused by their own movement. In the case of mechanosensation in aquatic animals, the exafferent inputs are water vibrations in the animal’s proximity, which need to be distinguished from the reafferent inputs arising from fluid drag due to locomotion. Both of these inputs are detected by the lateral line, a collection of mechanosensory organs distributed along the surface of the body.

In this study, we characterize in detail how the hair cells, which are the receptor cells of the lateral line, discriminate between such reafferent and exafferent signals in zebrafish larvae. Using dye labeling of the lateral line nerve, we visualize two parallel descending inputs that can influence lateral line sensitivity. We combine functional imaging with ultra-structural EM circuit reconstruction to show that cholinergic signals originating from the hindbrain transmit efference copies that cancel out self-generated reafferent stimulation during locomotion, and that dopaminergic signals from the hypothalamus may have a role in threshold modulation both in response to locomotion and salient stimuli. We further gain direct mechanistic insight into the core components of this circuit by loss-of-function perturbations using targeted ablations and gene knockouts.

We propose that this simple circuit is the core implementation of mechanosensory reafferent suppression in these young animals and that it might form the first instantiation of state-dependent modulation found at later stages in development.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# these authors have jointly supervised the work

  • ↵+ Lead author

  • First name of last author was corrected.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 06, 2021.
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Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish
Iris Odstrcil, Mariela D. Petkova, Martin Haesemeyer, Jonathan Boulanger-Weill, Maxim Nikitchenko, James A. Gagnon, Pablo Oteiza, Richard Schalek, Adi Peleg, Ruben Portugues, Jeff Lichtman, Florian Engert
bioRxiv 2021.05.04.442674; doi: https://doi.org/10.1101/2021.05.04.442674
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Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish
Iris Odstrcil, Mariela D. Petkova, Martin Haesemeyer, Jonathan Boulanger-Weill, Maxim Nikitchenko, James A. Gagnon, Pablo Oteiza, Richard Schalek, Adi Peleg, Ruben Portugues, Jeff Lichtman, Florian Engert
bioRxiv 2021.05.04.442674; doi: https://doi.org/10.1101/2021.05.04.442674

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