Birthdate aligns vestibular sensory neurons with central and motor partners across a sensorimotor reflex circuit for gaze stabilization

Developing populations of connected neurons often share spatial and/or temporal features that anticipate their assembly. A unifying spatiotemporal motif might link sensory, central and motor populations that comprise an entire circuit. In the sensorimotor reflex circuit that stabilizes vertebrate gaze, central and motor partners are paired in time (birthdate) and space (dorsoventral). To determine if birthdate and/or dorsoventral organization could align the entire circuit, we measured the spatial and temporal development of the sensory circuit node: the vestibular ganglion neurons. We discovered that progressive dorsal-to-ventral organization closely predicts vestibular ganglion development, with additional organization along its functional (rostrocaudal) axis. With an acute optical lesion and calcium imaging paradigm, we found that this common temporal axis anticipated functional sensory-to-central partner matching. We propose a 'first-come, first-served' model, in which birthdate organizes and assembles the sensory, central and motor populations that comprise the gaze stabilization circuit, a general strategy for polysynaptic circuit assembly across embryonically diverse neural populations.