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bioRxiv · 10.1101/2023.12.06.570482

The vestibulospinal nucleus is a locus of balance development

Hamling, K. R.·Harmon, K.·Kimura, Y.·Higashijima, S.-i.·Schoppik, D.
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Abstract

Mature vertebrates maintain posture using vestibulospinal neurons that transform sensed instability into reflexive commands to spinal motor circuits. Postural stability improves across development. However, due to the complexity of terrestrial locomotion, vestibulospinal contributions to postural refinement in early life remain unexplored. Here we leveraged the relative simplicity of underwater locomotion to quantify the postural consequences of losing vestibulospinal neurons during development in larval zebrafish of undifferentiated sex. By comparing posture at two timepoints, we discovered that later lesions of vestibulospinal neurons led to greater instability. Analysis of thousands of individual swim bouts revealed that lesions disrupted movement timing and corrective reflexes without impacting swim kinematics, and that this effect was particularly strong in older larvae. Using a generative model of swimming, we showed how these disruptions could account for the increased postural variability at both timepoints. Finally, late lesions disrupted the fin/trunk coordination observed in older larvae, linking vestibulospinal neurons to postural control schemes used to navigate in depth. Since later lesions were considerably more disruptive to postural stability, we conclude that vestibulospinal contributions to balance increase as larvae mature. Vestibulospinal neurons are highly conserved across vertebrates; we therefore propose that they are a substrate for developmental improvements to postural control. SIGNIFICANCE STATEMENTMany animals experience balance improvements during early life. Mature vertebrates use vestibulospinal neurons to transform sensed instability into postural corrections. To understand if/how these neurons shape postural development, we ablated them at two developmentally important timepoints in larval zebrafish. Loss of vestibulospinal neurons disrupted specific stabilizing behaviors (swim timing, tilt correction, and fin/body coordination) more profoundly in older fish. We conclude that postural development happens in part by changes to vestibulospinal neurons -- a significant step towards understanding how developing brains gain the ability to balance.

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Hamling, K. R., Harmon, K., Kimura, Y., Higashijima, S.-i., Schoppik, D.. 2023-12-07. The vestibulospinal nucleus is a locus of balance development. https://doi.org/10.1101/2023.12.06.570482

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