Brain expansion in the chick embryo initiated by experimentally produced occlusion of the spinal neurocoel

Abstract

The brain expands in the early chick embryo from pressure generated by accumulation of cerebrospinal fluid (CSF) in a closed neural tube. The sealing of the neural tube occurs as the result of occlusion of the spinal neurocoel rostral to and before closure of the posterior neuropore. We have previously demonstrated the dependence of normal brain expansion upon intraluminal pressure.We had yet to demonstrate, however, that brain expansion actually depends upon natural occlusion of the spinal neurocoel. To demonstrate such dependence, we experimentally occluded the spinal neurocoels of embryos 5 hr younger than stage 11 embryos (in which occlusion of the neurocoel occurs naturally). The stage 10 chick embryos were cultured ex ovo and critically staged, and their spinal neurocoels were occluded using microcautery. All embryos were photographed immediately and at 5, 12, and 24 hr after cautery. Serial sections were made of selected embryos, in which the areas of both the brain and the head were measured. Wilcoxon-Mann-Whitney rank-sum nonparametric tests, Hodges-Lehmann estimators, bootstrapping techniques, and resampling randomization tests were used to determine whether the increases in the brain and head areas for the experimental embryos were significantly different from those of the control embryos during three distinct intervals of expansion: 0 -5, 5-12, and 0 -12 hr. From 0 to 5 hr, the brains of the precociously occluded embryos expanded significantly more than the brains of the nonoccluded controls. From 5 to 12 hr, the brains of the embryos with naturally occluded neurocoels grew significantly larger than the brains of the embryos with precociously occluded neurocoels. At 12 hr, there appeared to be no difference in brain size for these two groups. We conclude that the data support the hypothesis that brain expansion is directly dependent upon occlusion of the spinal neurocoel. Anat Rec 268: 147-159, 2002.

Initial formation of zebrafish brain ventricles occurs independently of circulation and requires thenagie okoandsnakehead/atp1a1a.1gene products

“…It was therefore suggested that zebrafish brain ventricle defects developed secondarily to the circulation defect (Schier et al, 1996). This reasoning also stemmed from studies in chick, which showed that after the onset of circulation a positive CSF pressure inside the brain ventricles is necessary for brain ventricle expansion (Desmond, 1985;Desmond and Jacobson, 1977;Desmond and Levitan, 2002).…”

“…This dilation pattern is highly conserved in all vertebrates. Elegant studies in chick embryos have shown that intraluminal pressure resulting from the accumulation of CSF inside the brain ventricles is necessary for normal brain ventricle expansion and cell proliferation (Desmond, 1985;Desmond and Levitan, 2002), and levels of proteoglycans such as chondroitin sulfate affect this process (Alonso et al, 1998; The mechanisms by which the vertebrate brain develops its characteristic three-dimensional structure are poorly understood. The brain ventricles are a highly conserved system of cavities that form very early during brain morphogenesis and that are required for normal brain function.…”

Functional antagonism of voltage-gated K+ channel α-subunits in the developing brain ventricular system

“…It is thought that this is achieved by a combination of increased production of eCSF by neuroepithelial (ependymal) cells, which also function as neural stem cells (Desmond and Levitan, 2002;Johansson et al, 1999;Lowery and Sive, 2005;Mirzadeh et al, 2008;Meletis et al, 2008;Hamilton et al, 2009;Guo et al, 2011) and/or restriction of neuroepithelial permeability (Chang et al, 2012;Fossan et al, 1985;Lowery and Sive, 2009;Whish et al, 2015). While the mechanisms regulating the ventricular lining remain unclear, the expression of voltage-gated potassium (K v ) channels by ependymal cells might be essential due to their role in cell proliferation (Smith et al, 2008).…”

Focal adhesion kinase as a mechanotransducer during rapid brain growth of the chick embryo

“…As the tube is closed it also forms three vesicles anterior to posterior: the prosencepalon/forebrain, the mesencephalon/midbrain and the rhombencephalon/hindbrain. Expansion of the brain now rapidly occurs regulated by an increase in intraluminal pressure created by an increase in CSF (Desmond & Jacobson, 1977;Pacheco et al, 1986;Desmond & Levitan, 2002). At the same time that the brain suggest that intraluminal pressure regulates cell proliferation which immediately leads us to ask how mechanistically this might come about.…”