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Odstrcil I, Petkova MD, Haesemeyer M, et al. Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish. Curr Biol. 2021;doi: 10.1016/j.cub.2021.11.007.
Odstrcil, I., Petkova, M. D., Haesemeyer, M., Boulanger-Weill, J., Nikitchenko, M., Gagnon, J. A., Oteiza, P., Schalek, R., Peleg, A., Portugues, R., Lichtman, J. W., & Engert, F. (2021). Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish. Current biology : CB, . https://doi.org/10.1016/j.cub.2021.11.007
Odstrcil, Iris, et al. "Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish." Current biology : CB vol. (2021). doi: https://doi.org/10.1016/j.cub.2021.11.007
Odstrcil I, Petkova MD, Haesemeyer M, Boulanger-Weill J, Nikitchenko M, Gagnon JA, Oteiza P, Schalek R, Peleg A, Portugues R, Lichtman JW, Engert F. Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish. Curr Biol. 2021 Nov 17; doi: 10.1016/j.cub.2021.11.007. Epub 2021 Nov 17. PMID: 34822765.
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Curr Biol. 2021 Nov 17; doi: 10.1016/j.cub.2021.11.007. Epub 2021 Nov 17.

Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish.

Current biology : CB

Iris Odstrcil, Mariela D Petkova, Martin Haesemeyer, Jonathan Boulanger-Weill, Maxim Nikitchenko, James A Gagnon, Pablo Oteiza, Richard Schalek, Adi Peleg, Ruben Portugues, Jeff W Lichtman, Florian Engert

Affiliations

  1. Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA; Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA. Electronic address: [email protected].
  2. Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA; Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA.
  3. The Ohio State University, Department of Neuroscience, Columbus, OH 43210, USA.
  4. Duke University School of Medicine, Durham, NC 27707, USA.
  5. School of Biological Sciences, University of Utah, Salt Lake City, UT 84112, USA; Center for Cell & Genome Science, University of Utah, Salt Lake City, UT 84112, USA.
  6. Max Planck Institute for Ornithology, Flow Sensing Research Group, Seewiesen 82319, Germany.
  7. Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA.
  8. Institute of Neuroscience, Technical University of Munich, Munich 80333, Germany; Max Planck Institute of Neurobiology, Research Group of Sensorimotor Control, Martinsried 82152, Germany; Munich Cluster for Systems Neurology (SyNergy), Munich 81377, Germany.
  9. Department of Molecular and Cellular Biology, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA; Center for Brain Science, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA. Electronic address: [email protected].

PMID: 34822765 DOI: 10.1016/j.cub.2021.11.007

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 distinguishable 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 hair cells-the receptor cells of the lateral line-in zebrafish larvae discriminate between such reafferent and exafferent signals. 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 (copies of the motor command 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.

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Keywords: 2-photon calcium imaging; cholinergic modulation; connectomics; dopaminergic modulation; efference copy; hair cells; lateral line; re-afferent modulation; zebrafish

Conflict of interest statement

Declaration of interests The authors declare no competing interests.

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