Neuronal birthdate reveals topography in a vestibular brainstem circuit for gaze stabilization

Across the nervous system, neurons with similar attributes are topographically organized. This topography reflects developmental pressures. Oddly, vestibular (balance) nuclei are thought to be disorganized. By measuring activity in birthdated neurons, we revealed a functional map within the central vestibular projection nucleus that stabilizes gaze in the larval zebrafish. We first discovered that both somatic position and stimulus selectivity follow projection neuron birthdate. Next, with electron microscopy and loss-of-function assays, we found that patterns of peripheral innervation to projection neurons were similarly organized by birthdate. Finally, birthdate revealed spatial patterns of axonal arborization and synapse formation to projection neuron outputs. Collectively, we find that development reveals previously hidden organization to the input, processing, and output layers of a highly conserved vertebrate sensorimotor circuit. The spatial and temporal attributes we uncover constrain the developmental mechanisms that may specify the fate, function, and organization of vestibulo-ocular reflex neurons. More broadly, our data suggest that, like invertebrates, temporal mechanisms may assemble vertebrate sensorimotor architecture. •Vestibular projection neurons are topographically organized by birthdate•Projection neuron subtypes (up/down) follow birthdate-related topography•Sensory inputs and motor outputs to projection neurons are similarly organized Goldblatt et al. use development to uncover previously hidden functional topography in the vestibular system. Nose-up/nose-down subtypes of vestibular projection neurons, their sensory inputs, and their motor outputs share a common spatial and temporal organization. This suggests a role for conserved temporal mechanisms in circuit assembly.