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
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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).
Reviewing Editor
- Julien Vermot, Institut de Génétique et de Biologie Moléculaire et Cellulaire, France
Publication history
- Received: April 15, 2019
- Accepted: January 7, 2020
- Accepted Manuscript published: January 9, 2020 (version 1)
- Version of Record published: January 29, 2020 (version 2)
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.
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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
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- Medicine
- Physics of Living Systems
Background:
Postoperative knee instability is one of the major reasons accounting for unsatisfactory outcomes, as well as a major failure mechanism leading to total knee arthroplasty (TKA) revision. Nevertheless, subjective knee instability is not well defined clinically, plausibly because the relationships between instability and implant kinematics during functional activities of daily living remain unclear. Although muscles play a critical role in supporting the dynamic stability of the knee joint, the influence of joint instability on muscle synergy patterns is poorly understood. Therefore, this study aimed to understand the impact of self-reported joint instability on tibiofemoral kinematics and muscle synergy patterns after TKA during functional gait activities of daily living.
Methods:
Tibiofemoral kinematics and muscle synergy patterns were examined during level walking, downhill walking, and stair descent in eight self-reported unstable knees after TKA (3M:5F, 68.9 ± 8.3 years, body mass index [BMI] 26.1 ± 3.2 kg/m2, 31.9 ± 20.4 months postoperatively), and compared against 10 stable TKA knees (7M:3F, 62.6 ± 6.8 years, 33.9 ± 8.5 months postoperatively, BMI 29.4 ± 4.8 kg/m2). For each knee joint, clinical assessments of postoperative outcome were performed, while joint kinematics were evaluated using moving video-fluoroscopy, and muscle synergy patterns were recorded using electromyography.
Results:
Our results reveal that average condylar A-P translations, rotations, as well as their ranges of motion were comparable between stable and unstable groups. However, the unstable group exhibited more heterogeneous muscle synergy patterns and prolonged activation of knee flexors compared to the stable group. In addition, subjects who reported instability events during measurement showed distinct, subject-specific tibiofemoral kinematic patterns in the early/mid-swing phase of gait.
Conclusions:
Our findings suggest that accurate movement analysis is sensitive for detecting acute instability events, but might be less robust in identifying general joint instability. Conversely, muscle synergy patterns seem to be able to identify muscular adaptation associated with underlying chronic knee instability.
Funding:
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
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- Microbiology and Infectious Disease
- Physics of Living Systems
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