Postnatal Odorant Exposure Induces Peripheral Olfactory Plasticity at the Cellular Level

Abstract

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.

Adaptation of olfactory receptor abundances for efficient coding

“…The model predicts that in a noisy odor environment: (a) the distribution of receptor types will be highly non-uniform, but reproducible given fixed receptor affinities and odor statistics; and (b) an adapting receptor neuron repertoire should reproducibly reflect changes in the olfactory environment; in a sense it should become what it smells. Precisely such findings are reported in experiments [24,25,26,27,28,22].…”

“…In addition, in mammals, the olfactory epithelium experiences neural degeneration and neurogenesis, resulting in replacement of the OSNs every few weeks [23]. The distribution of receptors resulting from this replacement has been found to have a mysterious dependence on olfactory experience [24,25,26,27,28,22]: increased exposure to specific ligands leads reproducibly to more receptors of some types, and no change or fewer receptors of other types.…”

Poor human olfaction is a 19th-century myth

“…Critically, new evidence shows that 60% of human olfactory receptor “pseudogenes” are actually transcribed into mRNA in the human olfactory epithelium (22) and work in model organisms suggests that some olfactory receptor pseudogenes may actually result in functional receptors (23). Should these non-coding RNAs or unexpectedly-coding RNAs turn out to be a powerful regulatory network unique to primates (say, for matching olfactory receptor gene expression to the environment; 24, 25), would we then conclude that it is the basis for superior olfactory function in primates? If not, then we must be wary of confirmation bias whenever we find data “consistent with” a weak olfactory sense in humans.…”

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

“…However, even without outright changes in sensory abilities, sensory plasticity could be useful for directing attention, optimizing memory encoding and retrieval, metabolic savings, or other functions. Some of these functions could also be served by non-associative plasticity evoked by mere exposure to a particular sensory environment Eggermont 2009, 2010;Jakkamsetti et al 2012;Kass et al 2013b,c;Cadiou et al 2014), and could potentially use overlapping mechanisms.…”