Origin and role of the cerebrospinal fluid bidirectional flow in the central canal
- Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France
- École Polytechnique Fédérale de Lausanne, Switzerland
- Institute of Psychiatry and Neuroscience of Paris, Hôpital Saint-Anne, Université Descartes, INSERM U1266, France
- Norwegian University of Science and Technology, Norway
Abstract
Circulation of the cerebrospinal fluid (CSF) contributes to body axis formation and brain development. Here, we investigated the unexplained origins of the CSF flow bidirectionality in the central canal of the spinal cord of 30 hpf zebrafish embryos and its impact on development. Experiments combined with modeling and simulations demonstrate that the CSF flow is generated locally by caudally-polarized motile cilia along the ventral wall of the central canal. The closed geometry of the canal imposes the average flow rate to be null, explaining the reported bidirectionality. We also demonstrate that at this early stage, motile cilia ensure the proper formation of the central canal. Furthermore, we demonstrate that the bidirectional flow accelerates the transport of particles in the CSF via a coupled convective-diffusive transport process. Our study demonstrates that cilia activity combined with muscle contractions sustain the long-range transport of extracellular lipidic particles, enabling embryonic growth.
Data availability
The data enabling to plot all graphs for figures and supplemental videos have been deposited to the Dryad Digital Repository doi:10.5061/dryad.4mj3pv1.The full MATLAB script can be found on Github https://github.com/wyartlab/eLife_2019_OriginAndRole
-
Data from: Origin of bidirectionality of cerebrospinal fluid flow and impact on long range transport between brain and spinal cordDryad Digital Repository, doi:10.5061/dryad.4mj3pv1.
Article and author information
Author details
Nathalie Jurisch-Yaksi
Funding
Human Frontier Science Program (RGP00063/2018)
- Francois Gallaire
- Claire Wyart
NIH Blueprint for Neuroscience Research (U19NS104653)
- Martin Carbo-Tano
- Claire Wyart
European Research Council (311673)
- Yasmine Cantaut-Belarif1
- Martin Carbo-Tano
- Claire Wyart
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All procedures were performed on zebrafish embryos before 2 days post fertilization in accordance with the European Communities Council Directive (2010/63/EU) and French law (87/848) and approved by the Brain and Spine Institute (Institut du Cerveau et de la Moelle épinière).
Copyright
© 2020, Thouvenin 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
-
- 4,922
- views
-
- 574
- downloads
-
- 56
- 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)
Origin and role of the cerebrospinal fluid bidirectional flow in the central canal
eLife 9:e47699.
https://doi.org/10.7554/eLife.47699
Further reading
-
- Physics of Living Systems
Vertebrates have evolved great diversity in the number of segments dividing the trunk body, however, the developmental origin of the evolvability of this trait is poorly understood. The number of segments is thought to be determined in embryogenesis as a product of morphogenesis of the pre-somitic mesoderm (PSM) and the periodicity of a molecular oscillator active within the PSM known as the segmentation clock. Here, we explore whether the clock and PSM morphogenesis exhibit developmental modularity, as independent evolution of these two processes may explain the high evolvability of segment number. Using a computational model of the clock and PSM parameterised for zebrafish, we find that the clock is broadly robust to variation in morphogenetic processes such as cell ingression, motility, compaction, and cell division. We show that this robustness is in part determined by the length of the PSM and the strength of phase coupling in the clock. As previous studies report no changes to morphogenesis upon perturbing the clock, we suggest that the clock and morphogenesis of the PSM exhibit developmental modularity.
-
- Physics of Living Systems
Bacterial biofilms are communities of bacteria usually attached to solid strata and often differentiated into complex structures. Communication across biofilms has been shown to involve chemical signaling and, more recently, electrical signaling in Gram-positive biofilms. We report for the first time, community-level synchronized membrane potential dynamics in three-dimensional Escherichia coli biofilms. Two hyperpolarization events are observed in response to light stress. The first requires mechanically sensitive ion channels (MscK, MscL, and MscS) and the second needs the Kch-potassium channel. The channels mediated both local spiking of single E. coli biofilms and long-range coordinated electrical signaling in E. coli biofilms. The electrical phenomena are explained using Hodgkin-Huxley and 3D fire-diffuse-fire agent-based models. These data demonstrate that electrical wavefronts based on potassium ions are a mechanism by which signaling occurs in Gram-negative biofilms and as such may represent a conserved mechanism for communication across biofilms.
