A Population of Navigator Neurons Is Essential for Olfactory Map Formation during the Critical Period

In the developing brain, heightened plasticity during the critical period enables the proper formation of neural circuits. Here, we identify the “navigator” neurons, a group of perinatally born olfactory sensory neurons, as playing an essential role in establishing the olfactory map during the critical period. The navigator axons project circuitously in the olfactory bulb and traverse multiple glomeruli before terminating in perspective glomeruli. These neurons undergo a phase of exuberant axon growth and exhibit a shortened lifespan. Single-cell transcriptome analyses reveal distinct molecular signatures for the navigators. Extending their lifespan prolongs the period of exuberant growth and perturbs axon convergence. Conversely, a genetic ablation experiment indicates that, despite postnatal neurogenesis, only the navigators are endowed with the ability to establish a convergent map. The presence and the proper removal of the navigator neurons are both required to establish tight axon convergence into the glomeruli. •Single-cell analyses uncover a distinct population of olfactory neurons•Chronogenetic labeling reveals distinct navigator cell axon morphology and lifespan•Transgenic expression of Bcl2 extends the lifespan of navigator cells•Alterations of navigator cell lifespan disrupt olfactory map formation Wu and colleagues identify a transient population of olfactory sensory neurons existing around the critical period. These neurons are morphologically and molecularly distinct from the adult olfactory sensory neurons and are critical for the formation of the olfactory map.