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.

Automated analyses of innate olfactory behaviors in rodents.

Olfaction based behavioral experiments are important for the investigation of sensory coding, perception, decision making and memory formation. The predominant experimental paradigms employ forced choice operant assays, which require associative learning and reinforced training. Animal performance in these assays not only reflects odor perception but also the confidence in decision making and memory. In this study, we describe a versatile and automated setup, "Poking-Registered Olfactory Behavior Evaluation System" (PROBES), which can be adapted to perform multiple olfactory assays. In addition to forced choice assays, we employ this system to examine animal's innate ability for odor detection, discrimination and preference without elaborate training procedures. These assays provide quantitative measurements of odor discrimination and robust readouts of odor preference. Using PROBES, we find odor detection thresholds are at lower concentrations in naïve animals than those determined by forced choice assays. PROBES-based automated assays provide an efficient way of analyzing innate odor-triggered behaviors.

A developmental switch of axon targeting in the continuously regenerating mouse olfactory system.

The mammalian olfactory system has the natural capacity to regenerate throughout the animal's life span. Despite constant neurogenesis, olfactory sensory neurons project to precise, stereotypical positions in the brain. Here, we identify a critical period of olfactory sensory axon targeting during postnatal development in mouse. Perturbing axon projection beyond postnatal day 7 permanently disrupts targeting specificity of the sensory neurons. In addition, we find that the establishment of the convergence map requires perinatal sensory neurons. Late-born neurons appear to connect with prospective glomeruli based on homotypic interactions among neurons expressing the same odorant receptor. Our results reveal a developmental switch in axon guidance and a mechanism of circuit integration of adult-born neurons.