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.
Highlights
Precise control of flow in biological systems allows efficient transportation of critical molecules throughout an organism
We show that the cerebrospinal fluid (CSF) flows unidirectionally from the diencephalic/mesencephalic ventricle to the entrance of the central canal, and that in vivo two-photon ablation of this connection leads to a reduction in size of embryos
As no significant difference in the central canal (CC) diameter was detected during the muscle contractions, we propose that the reported enhancement of CSF flow is not due to a local variation of the CC diameter, but instead due to a change in the volume of the brain ventricles that occurs during muscle contraction at larval stage (Olstad et al, 2018)
Summary
Precise control of flow in biological systems allows efficient transportation of critical molecules throughout an organism. For organisms larger than a few hundreds of microns, diffusion alone is too slow to achieve supply of nutrients or signaling molecules to all cells in the body. Organisms have developed a large variety of flows to accelerate and orient the transport of key molecules. Other flows involve asymmetric beating of motile cilia or flagella, which are efficient motors that generate directional flows at small scales and mix fluids in biological systems (Ferreira et al, 2017; McGrath et al, 2003; Shields et al, 2010; Supatto and Vermot, 2011). Cilia-driven flows are critical for left/right asymmetry in the developing embryos of many species including humans (Baker and Beales, 2009), in Thouvenin et al eLife 2020;9:e47699.
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