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. Lastly, 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.

When threatened by dangerous or harmful stimuli, animals engage in diverse forms of rapid escape behavior. In Drosophila larvae, escape behavior is characterized by C-shaped bending and lateral rolling, followed by rapid forward crawling. The sensory circuitry that promotes escape has been extensively characterized, but the motor programs underlying escape are unknown. Here, we characterize the neuromuscular basis of escape. We use high-speed, volumetric, Swept Confocally-Aligned Planar Excitation (SCAPE) microscopy to image muscle activity during larval rolling. Unlike the sequential peristaltic muscle contractions from segment to segment that underlie crawling, muscle activity progresses in a circumferential sequence during bending and rolling. Certain muscle subgroups show functional antagonism during bending and rolling. We use EM connectome data to identify premotor to motor connectivity patterns that could drive rolling behavior and test the necessity of specific groups of motor neurons in rolling using neural silencing approaches. Our data reveal body-wide muscle activity patterns and putative premotor circuit organization for escape.