Olfactory Stimulation Regulates the Birth of Neurons That Express Specific Odorant Receptors

Abstract

SUMMARY In mammals, olfactory sensory neurons (OSNs) are born throughout life, ostensibly solely to replace damaged OSNs. During differentiation, each OSN precursor “chooses,” out of hundreds of possibilities, a single odorant receptor (OR) gene, which defines the identity of the mature OSN. The relative neurogenesis rates of the hundreds of distinct OSN “subtypes” are thought to be constant, as they are determined by a stochastic process in which each OR is chosen with a fixed probability. Here, using histological, single-cell, and targeted affinity purification approaches, we show that closing one nostril in mice selectively reduces the number of newly generated OSNs of specific subtypes. Moreover, these reductions depend on an animal’s age and/or environment. Stimulation-dependent changes in the number of new OSNs are not attributable to altered rates of cell survival but rather production. Our findings indicate that the relative birth rates of distinct OSN subtypes depend on olfactory experience.

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“…Nasal closure reduced the number of olfactory sensory neurons with specific receptor genes (input dependent) but there were olfactory sensory neurons with other specific receptor genes that did not change in number (input independent). Lack of olfactory stimulus due to nasal closure affected the production of new olfactory sensory neurons with the sensory input dependent type of receptor genes negatively but did not change the production of new olfactory sensory neurons with the sensory input independent type [149].…”

“…When one nostril was occluded to block sensory input on one side after ablation of olfactory sensory neurons of both sides, regeneration of the sensory neurons on the occluded side and the open side were not different during the first weeks, but then the occluded side showed higher apoptosis, resulting in fewer mature olfactory sensory neurons during regeneration on the occluded side [190]. However, as written above, there are differences in the regeneration of olfactory sensory neurons depending on the types of receptors [149].…”

“…When the odorants are non-pheromonal, the influence of exposure or lack of exposure becomes different. Increased exposure to odors is found to stimulate the birth of the olfactory sensory neurons [149]. When mice were exposed to a specific odor when they experienced fear, the olfactory receptors for specific odorants increased and they became more sensitive to the odor, showing avoidance at a lower concentration of the odor [150,151].…”

“…Recent studies using mice as an animal model have shown that there are specific subtypes of olfactory sensory neurons (or receptor genes) that are sensory input dependent/independent [149]. Nasal closure reduced the number of olfactory sensory neurons with specific receptor genes (input dependent) but there were olfactory sensory neurons with other specific receptor genes that did not change in number (input independent).…”

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“…An interesting review by Coppola (2012) clearly describes biases and limitations of this experimental model. Nevertheless, some studies clearly show that the dynamic of OSN population is affected differentially in terms of the expressed OR populations, indicating that sensory experience could shape the olfactory response of the OE (He et al 2012;Zhao et al 2013;van der Linden et al 2020).…”