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Evolutionary origin of the neural tube in basal deuterostomes

Journal

CURRENT BIOLOGY
Volume 33, Issue 8, Pages R319-R331

Publisher

CELL PRESS
DOI: 10.1016/j.cub.2023.03.045

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The evolutionary origin of the hollow tube-like central nervous system (CNS) in chordates remains mysterious as most animals in the animal kingdom have ganglionic-type nervous systems without epithelialized tubes or liquid-filled cavities. Recent findings suggest that nerve cords in other deuterostomes may provide insights into the homologies, histology, and anatomy of the chordate neural tube. These findings inspire new hypotheses about the evolutionary scenarios explaining the tubular structure of the CNS, including the role of directional olfaction and the biomechanical support provided by a liquid-filled tube. These hypotheses challenge previous explanations and shed light on the development of the CNS in chordates.
The central nervous system (CNS) of chordates, including humans, develops as a hollow tube with ciliated walls containing cerebrospinal fluid. However, most of the animals inhabiting our planet do not use this design and rather build their centralized brains from non-epithelialized condensations of neurons called ganglia, with no traces of epithelialized tubes or liquid-containing cavities. The evolutionary origin of tubetype CNSs stays enigmatic, especially as non-epithelialized ganglionic-type nervous systems dominate the animal kingdom. Here, I discuss recent findings relevant to understanding the potential homologies and scenarios of the origin, histology and anatomy of the chordate neural tube. The nerve cords of other deuterostomes might relate to the chordate neural tube at histological, developmental and cellular levels, including the presence of radial glia, layered stratification, retained epithelial features, morphogenesis via folding and formation of a lumen filled with liquid. Recent findings inspire a new view of hypothetical evolutionary scenarios explaining the tubular epithelialized structure of the CNS. One such idea suggests that early neural tubes were key for improved directional olfaction, which was facilitated by the liquid-containing internal cavity. The later separation of the olfactory portion of the tube led to the formation of the independent olfactory and posterior tubular CNS systems in vertebrates. According to an alternative hypothesis, the thick basiepithelial nerve cords could provide deuterostome ancestors with additional biomechanical support, which later improved by turning the basiepithelial cord into a tube filled with liquid - a hydraulic skeleton.

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