The Reissner fiber under tension in vivo shows dynamic interaction with ciliated cells contacting the cerebrospinal fluid

  1. Celine Bellegarda  Is a corresponding author
  2. Guillaume Zavard
  3. Lionel Moisan
  4. Françoise Brochard-Wyart
  5. Jean-François Joanny
  6. Ryan S Gray
  7. Yasmine Cantaut-Belarif
  8. Claire Wyart  Is a corresponding author
  1. Paris Brain Institute, Sorbonne Université, France
  2. Université Paris Cité, CNRS, MAP5, France
  3. Institut Curie, CNRS UMR168, France
  4. The University of Texas at Austin, United States
  5. Paris Brain Institute (ICM), Sorbonne Université, France

Abstract

The Reissner fiber (RF) is an acellular thread positioned in the midline of the central canal that aggregates thanks to the beating of numerous cilia from ependymal radial glial cells (ERGs) generating flow in the central canal of the spinal cord. RF together with cerebrospinal fluid (CSF)-contacting neurons (CSF-cNs) form an axial sensory system detecting curvature. How RF, CSF-cNs and the multitude of motile cilia from ERGs interact in vivo appears critical for maintenance of RF and sensory functions of CSF-cNs to keep a straight body axis, but is not well-understood. Using in vivo imaging in larval zebrafish, we show that RF is under tension and resonates dorsoventrally. Focal RF ablations trigger retraction and relaxation of the fiber’s cut ends, with larger retraction speeds for rostral ablations. We built a mechanical model that estimates RF stress diffusion coefficient D at 5 mm2/s and reveals that tension builds up rostrally along the fiber. After RF ablation, spontaneous CSF-cN activity decreased and ciliary motility changed, suggesting physical interactions between RF and cilia projecting into the central canal. We observed that motile cilia were caudally-tilted and frequently interacted with RF. We propose that the numerous ependymal motile monocilia contribute to RF's heterogenous tension via weak interactions. Our work demonstrates that under tension, the Reissner fiber dynamically interacts with motile cilia generating CSF flow and spinal sensory neurons.

Data availability

All code are accessible on GitHub and processed data from imaging and ablation experiments are available here:https://doi.org/10.5061/dryad.573n5tbc2

The following data sets were generated

Article and author information

Author details

  1. Celine Bellegarda

    Paris Brain Institute, Sorbonne Université, Paris, France
    For correspondence
    cbellegarda@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4394-295X
  2. Guillaume Zavard

    Paris Brain Institute, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8948-4387
  3. Lionel Moisan

    Université Paris Cité, CNRS, MAP5, Paris, France
    Competing interests
    No competing interests declared.
  4. Françoise Brochard-Wyart

    Institut Curie, CNRS UMR168, Paris, France
    Competing interests
    No competing interests declared.
  5. Jean-François Joanny

    Institut Curie, CNRS UMR168, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6966-3222
  6. Ryan S Gray

    Dell Pediatrics Research Institute, The University of Texas at Austin, Austin, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9668-6497
  7. Yasmine Cantaut-Belarif

    Paris Brain Institute, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
  8. Claire Wyart

    Paris Brain Institute (ICM), Sorbonne Université, Paris, France
    For correspondence
    claire.wyart@icm-institute.org
    Competing interests
    Claire Wyart, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1668-4975

Funding

Human Frontier Science Program (2017/RG0063)

  • Claire Wyart

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Eva Kanso, University of Southern California, United States

Ethics

Animal experimentation: Animal handling and procedures were validated by the Paris Brain Institute (ICM) and the French National Ethics Committee (ComiteNational de Reflexion Ethique sur l'Experimentation Animale; APAFIS # 2018071217081175) in agreement with EU legislation. All experimentswere performed on Danio rerio 3 days old larvae of AB Larvae raised in the same conditions.Experiments were performed at RT on 3 days post fertilization (dpf) larvae based on the protocol of each experiment.

Version history

  1. Received: January 14, 2023
  2. Preprint posted: February 23, 2023 (view preprint)
  3. Accepted: September 28, 2023
  4. Accepted Manuscript published: September 29, 2023 (version 1)
  5. Accepted Manuscript updated: October 3, 2023 (version 2)
  6. Version of Record published: October 31, 2023 (version 3)

Copyright

© 2023, Bellegarda et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 633
    views
  • 137
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Celine Bellegarda
  2. Guillaume Zavard
  3. Lionel Moisan
  4. Françoise Brochard-Wyart
  5. Jean-François Joanny
  6. Ryan S Gray
  7. Yasmine Cantaut-Belarif
  8. Claire Wyart
(2023)
The Reissner fiber under tension in vivo shows dynamic interaction with ciliated cells contacting the cerebrospinal fluid
eLife 12:e86175.
https://doi.org/10.7554/eLife.86175

Share this article

https://doi.org/10.7554/eLife.86175

Further reading

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Taegon Chung, Iksoo Chang, Sangyeol Kim
    Research Article

    Locomotion is a fundamental behavior of Caenorhabditis elegans (C. elegans). Previous works on kinetic simulations of animals helped researchers understand the physical mechanisms of locomotion and the muscle-controlling principles of neuronal circuits as an actuator part. It has yet to be understood how C. elegans utilizes the frictional forces caused by the tension of its muscles to perform sequenced locomotive behaviors. Here, we present a two-dimensional rigid body chain model for the locomotion of C. elegans by developing Newtonian equations of motion for each body segment of C. elegans. Having accounted for friction-coefficients of the surrounding environment, elastic constants of C. elegans, and its kymogram from experiments, our kinetic model (ElegansBot) reproduced various locomotion of C. elegans such as, but not limited to, forward-backward-(omega turn)-forward locomotion constituting escaping behavior and delta-turn navigation. Additionally, ElegansBot precisely quantified the forces acting on each body segment of C. elegans to allow investigation of the force distribution. This model will facilitate our understanding of the detailed mechanism of various locomotive behaviors at any given friction-coefficients of the surrounding environment. Furthermore, as the model ensures the performance of realistic behavior, it can be used to research actuator-controller interaction between muscles and neuronal circuits.

    1. Physics of Living Systems
    Giulio Facchini, Alann Rathery ... Andrea Perna
    Research Article

    Termites build complex nests which are an impressive example of self-organization. We know that the coordinated actions involved in the construction of these nests by multiple individuals are primarily mediated by signals and cues embedded in the structure of the nest itself. However, to date there is still no scientific consensus about the nature of the stimuli that guide termite construction, and how they are sensed by termites. In order to address these questions, we studied the early building behavior of Coptotermes gestroi termites in artificial arenas, decorated with topographic cues to stimulate construction. Pellet collections were evenly distributed across the experimental setup, compatible with a collection mechanism that is not affected by local topography, but only by the distribution of termite occupancy (termites pick pellets at the positions where they are). Conversely, pellet depositions were concentrated at locations of high surface curvature and at the boundaries between different types of substrate. The single feature shared by all pellet deposition regions was that they correspond to local maxima in the evaporation flux. We can show analytically and we confirm experimentally that evaporation flux is directly proportional to the local curvature of nest surfaces. Taken together, our results indicate that surface curvature is sufficient to organize termite building activity and that termites likely sense curvature indirectly through substrate evaporation. Our findings reconcile the apparently discordant results of previous studies.