Tight temporal coupling between synaptic rewiring of olfactory glomeruli and the emergence of odor‐guided behavior in Xenopus tadpoles

Olfactory sensory neurons (OSNs) are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb. OSNs undergo continuous turnover throughout life, causing the constant replacement of their synaptic contacts. Using Xenopus tadpoles as an experimental system to investigate rewiring of glomerular connectivity, we show that novel OSN synapses can transfer information immediately after formation, mediating olfactory‐guided behavior. Tadpoles recover the ability to detect amino acids 4 days after bilateral olfactory nerve transection. Restoration of olfactory‐guided behavior depends on the efficient reinsertion of OSNs to the olfactory bulb. Presynaptic terminals of incipient synaptic contacts generate calcium transients in response to odors, triggering long lasting depolarization of olfactory glomeruli. The functionality of reconnected terminals relies on well‐defined readily releasable and cytoplasmic vesicle pools. The continuous growth of non‐compartmentalized axonal processes provides a vesicle reservoir to nascent release sites, which contrasts to the gradual development of cytoplasmic vesicle pools in conventional excitatory synapses. The immediate availability of fully functional synapses upon formation supports an age‐independent contribution of OSNs to the generation of odor maps. Olfactory sensory neurons are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb and undergo continuous turnover throughout life. In Xenopus tadpoles novel olfactory sensory neuron synapses contain well‐structured synaptic vesicle pools that allow the transfer information immediately after formation, mediating an olfactory‐guided behavior.