Postnatal odorant exposure induces peripheral olfactory plasticity at the cellular level.
Mammalian olfactory sensory neurons (OSNs) form the primary elements of the olfactory system. Inserted in the olfactory mucosa lining of the nasal cavity, they are exposed to the environment and their lifespan is brief. Several reports say that OSNs are regularly regenerated during the entire life and that odorant environment affects the olfactory epithelium. However, little is known about the impact of the odorant environment on OSNs at the cellular level and more precisely in the context of early postnatal olfactory exposure. Here we exposed MOR23-green fluorescent protein (GFP) and M71-GFP mice to lyral or acetophenone, ligands for MOR23 or M71, respectively. Daily postnatal exposure to lyral induces plasticity in the population of OSNs expressing MOR23. Their density decreases after odorant exposure, whereas the amount of MOR23 mRNA and protein remain stable in the whole epithelium. Meanwhile, quantitative PCR indicates that each MOR23 neuron has higher levels of olfactory receptor transcripts and also expresses more CNGA2 and phosphodiesterase 1C, fundamental olfactory transduction pathway proteins. Transcript levels return to baseline after 4 weeks recovery. Patch-clamp recordings reveal that exposed MOR23 neurons respond to lyral with higher sensitivity and broader dynamic range while the responses' kinetics were faster. These effects are specific to the odorant-receptor pair lyral-MOR23: there was no effect of acetophenone on MOR23 neurons and no effect of acetophenone and lyral on the M71 population. Together, our results clearly demonstrate that OSNs undergo specific anatomical, molecular, and functional adaptation when chronically exposed to odorants in the early stage of life.
Centre National de la Recherche Scientifique, Unité Mixte de Recherche (UMR) 6265 Centre des Sciences du Goût et de l'Alimentation, F-21000 Dijon, France, Institut National de la Recherche Agronomique (INRA), UMR 1324 Centre des Sciences du Goût et de l'Alimentation, F-21000 Dijon, France, Université de Bourgogne, UMR Centre des Sciences du Goût et de l'Alimentation, F-21000 Dijon, France, INRA, UR1197 Neurobiologie de l'Olfaction et Modélisation en Imagerie, Domaine de Vilvert, F-78350 Jouy-en-Josas, France, and Institut Fédératif de Recherche des Sciences 144, NeuroSud Paris, F-91190 Gif-Sur-Yvette, France.
Hervé
H
Cadiou
Imad
I
Aoudé
Bassim
B
Tazir
Adrien
A
Molinas
Claire
C
Fenech
Nicolas
N
Meunier
Xavier
X
Grosmaitre
D000818:Animals; D000831:Animals, Newborn; D004585:Electrooculography; D005786:Gene Expression Regulation / Q000235:genetics / Q000502:physiology*; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D008564:Membrane Potentials / Q000187:drug effects / Q000235:genetics; D051379:Mice; D008822:Mice, Transgenic; D009473:Neuronal Plasticity / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D009812:Odorants; D009830:Olfactory Bulb / Q000166:cytology*; D018034:Olfactory Receptor Neurons / Q000502:physiology*; D018408:Patch-Clamp Techniques; D018035:Receptors, Odorant / Q000235:genetics / Q000378:metabolism; D012903:Smell / Q000235:genetics / Q000502:physiology*
C502656:Olfr151 protein, mouse; C118713:Olfr16 protein, mouse; D018035:Receptors, Odorant; D049452:Green Fluorescent Proteins
development; electrophysiology; mice; molecular biology; olfaction; plasticity