Constancy of olfactory cilia in rodents

In terrestrial mammals, odorant receptors and associated sensory transduction machinery in olfactory sensory neurons (OSNs) are compartmentalized in the cilia, a critically important organelle for odor detection. The large number and length of olfactory cilia provide an extensive receptive surface for odor detection. The stability of these organelles is critical for olfactory function, as damage to olfactory cilia due to environmental factors, age, or disease impairs odor detection. However, it is unclear if there are innate structural or functional features of olfactory cilia that vary between OSN subtypes and affect the fidelity of the odorant receptive field. Using ciliary-targeted fluorescent probes, we analyzed cilia morphology in live, intact OSNs in situ from mice and rats. This unbiased approach revealed a previously unappreciated constancy of average cilia length and number in OSNs across the olfactory epithelium, measures that were also independent of animal age, sex, genetic background, and even rodent species. However, average OSN cilia length did vary with the cyclic nucleotide they use to transduce olfactory stimuli: OSNs expressing the non-canonical olfactory receptor guanylate cyclase-D, which use cGMP as the second messenger, had dramatically shorter cilia than the canonical odorant receptors M71 or I7 or the trace amine-associated receptor TAAR3, each of which instead employs the second messenger cAMP. These findings suggest that differences in cyclic nucleotide signaling are associated with cilia length in OSNs. Together, the data provide a basis for understanding structure-function relationship between cilia morphology and odorant transduction as a foundation for building a high-fidelity chemosensory organ.