Converging Axons Collectively Initiate and Maintain Synaptic Selectivity in a Constantly Remodeling Sensory Organ

Sensory receptors are the functional link between the environment and the brain [1–3]. The repair of sensory organs enables animals to continuously detect environmental stimuli [4]. However, receptor cell turnover can affect sensory acuity by changing neural connectivity patterns [5, 6]. In zebrafish, two to four postsynaptic lateralis afferent axons converge into individual peripheral mechanosensory organs called neuromasts, which contain hair cell receptors of opposing planar polarity [7]. Yet, each axon exclusively synapses with hair cells of identical polarity during development and regeneration to transmit unidirectional mechanical signals to the brain [8, 9]. The mechanism that governs this exceptionally accurate and resilient synaptic selectivity remains unknown. We show here that converging axons are mutually dependent for polarity-selective connectivity. If rendered solitary, these axons establish simultaneous functional synapses with hair cells of opposing polarities to transmit bidirectional mechanical signals. Remarkably, nonselectivity by solitary axons can be corrected upon the reintroduction of additional axons. Collectively, our results suggest that lateralis synaptogenesis is intrinsically nonselective and that interaxonal interactions continuously rectify mismatched synapses. This dynamic organization of neural connectivity may represent a general solution to maintain coherent synaptic transmission from sensory organs undergoing frequent variations in the number and spatial distribution of receptor cells. •We analyzed in vivo the dynamics of synaptogenesis in a remodeling sensory system•Sensory synaptic selectivity is an emergent property of the axonal population•Interaxonal interactions are balanced•Axonal interactions in equilibrium preserve coherent connectivity patterns Pujol-Martí et al. use the planar polarization of the mechanosensory hair cells in the lateral line to study the maintenance of synaptic selectivity in a perpetually regenerating sensory organ. Sensory-neural connectivity patterns are maintained through a self-correcting mechanism involving a continuous interaction among converging sensory axons.