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 (dorso-ventral). To determine if birthdate and/or dorso-ventral organization could align the entire circuit, we measured the spatial and temporal development of the sensory circuit node: the vestibular ganglion neurons. We discovered progressive dorsal-to-ventral development in the vestibular ganglion that diverges from its functional (rostrocaudal) organization. With an acute optical lesion and calcium imaging paradigm, we found that this common spatiotemporal axis anticipated functional sensory-to-central partner matching. We propose a "first-come, first-served" model in which birthdate organizes the sensory, central, and motor populations that comprise the gaze stabilization circuit. Our work suggests a general means for poly-synaptic circuit assembly across embryonically-diverse neural populations.