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 criti...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2018-12, Vol.100 (5), p.1066-1082.e6
Main Authors: Wu, Yunming, Ma, Limei, Duyck, Kyle, Long, Carter C., Moran, Andrea, Scheerer, Hayley, Blanck, Jillian, Peak, Allison, Box, Andrew, Perera, Anoja, Yu, C. Ron
Format: Article
Language:English
Subjects:
Adenoviruses
Animals
Axons
Axons - physiology
Convergence
Critical period
Female
Gene expression
HEK293 Cells
Humans
Labeling
Life span
Male
Medical research
Mice, Transgenic
Morphology
Nervous system
Neural networks
Neurogenesis
Neurons
Olfactory bulb
Olfactory Bulb - growth & development
Olfactory Bulb - metabolism
Olfactory pathways
Olfactory Pathways - growth & development
Olfactory Pathways - metabolism
Olfactory receptor neurons
Olfactory Receptor Neurons - metabolism
Olfactory Receptor Neurons - physiology
Plasticity (neural)
Sensory neurons
Smell
Transcriptome
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Summary: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.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2018.09.051