State-dependent sculpting of olfactory sensory neurons is attributed to sensory enrichment, odor deprivation, and aging

doi:10.1016/j.neulet.2010.07.059

Neuroscience Letters

Volume 483, Issue 2, 11 October 2010, Pages 90-95

https://doi.org/10.1016/j.neulet.2010.07.059 Get rights and content

Abstract

Gene-targeted deletion of the predominant Shaker potassium channel, Kv1.3, in the mitral cells of the olfactory bulb, decreases the number of presynaptic, odorant receptor (OR)-identified olfactory sensory neurons (OSNs) in the main olfactory epithelium (MOE) and alters the nature of their postsynaptic connections to mitral cell targets. The current study examined whether OSN density was state-dependent by examining the impact of (1) odor enrichment, (2) sensory deprivation, and (3) aging upon the number of P2- or M72-expressing neurons. Histological approaches were used to quantify the number of OSNs across entire epithelia for wildtype (WT) vs. Kv1.3-null (KO) mice bred onto an ORtauLacZ reporter background. Following either odor enrichment or early unilateral naris-occlusion, the number of M72-expressing OSNs was significantly decreased in WT mice, but was unchanged in KO animals. Following naris-occlusion, the number of P2-expressing OSNs was decreased regardless of genotype. Animals that were reared to 2 years of age demonstrated loss of both P2- and M72-expressing OSNs in WT mice and a concomitant loss of only M72-expressing neurons in KO mice. These findings suggest that voltage-gated activity of the mitral cells is important for OSN plasticity, and can prevent neuronal loss via sensory- and OR-dependent mechanisms.

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Acknowledgements

We would like to thank our FSU undergraduate scholars for their assistance with changing of the mice cages, odor stimulation, neuron counting, or routine technical assistance. We also thank Drs. Peter Mombaerts and Leonard Kazcmarek for the donation of the odor receptor-tagged and Kv1.3−/− mice, respectively, and Dr. Stanley Watson for his generous gift of the Ki67 antiserum. This work was supported by grants DC03387 and DC00044 from the National Institute of Deafness and Communication Disorders

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Mammals typically have hundreds of distinct olfactory sensory neuron subtypes, each defined by expression of a specific odorant receptor gene, which undergo neurogenesis throughout life at rates that can depend on olfactory experience. Here, we present a protocol to quantify the birthrates of specific neuron subtypes via the simultaneous detection of corresponding receptor mRNAs and 5-ethynyl-2′-deoxyuridine. For preparation prior to beginning the protocol, we detail procedures for generating odorant receptor-specific riboprobes and experimental mouse olfactory epithelial tissue sections.
For complete details on the use and execution of this protocol, please refer to van der Linden et al. (2020).¹
Olfactory Stimulation Regulates the Birth of Neurons That Express Specific Odorant Receptors
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Citation Excerpt :
To do so, we used UNO, a procedure that provides a simple method for reproducibly reducing olfactory stimulation (broadly defined here as both odor- and mechanically derived; Grosmaitre et al., 2007) on the closed side of the OE, as well as a within-animal control (the open side of the OE). Previous studies have found that UNO causes both selective changes in the transcript levels of specific ORs (Cavallin et al., 2010; Coppola and Waggener, 2012; Fischl et al., 2014; Santoro and Dulac, 2012; Zhao et al., 2013) and the abundance of OSNs of corresponding subtypes (Cavallin et al., 2010; Santoro and Dulac, 2012; Zhao et al., 2013) on the closed side of the OE relative to the open side. After defining a set of OSN subtypes with altered representation following UNO, we investigated whether selective changes in neurogenesis contribute to the observed changes in OSN abundance.
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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Chronic perinatal odour exposure with heptaldehyde affects odour sensitivity and olfactory system homeostasis in preweaning mice
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Exposure to specific odorants in the womb during pregnancy or in the milk during early nursing is known to impact morpho-functional development of the olfactory circuitry of pups. This can be associated with a modification in olfactory sensitivity and behavioural olfactory-based preferences to the perinatally encountered odorants measured at birth, weaning or adult stage. Effects depend on a multitude of factors, such as odorant type, concentration, administration mode and frequency, as well as timing and mice strain. Here, we examined the effect of perinatal exposure to heptaldehyde on the neuro-anatomical development of the olfactory receptor Olfr2 circuitry, olfactory sensitivity and odour preferences of preweaning pups using mI7-IRES-tau-green fluorescent protein mice. We found that perinatal odour exposure through the feed of the dam reduces the response to heptaldehyde and modulates transcript levels of neuronal transduction proteins in the olfactory epithelium of the pups. Furthermore, the number of I7 glomeruli related to Olfr2-expressing OSN is altered in a way similar to that seen with restricted post-natal exposure, in an age-dependent way. These variations are associated with a modification of olfactory behaviours associated with early post-natal odour preferences at weaning.
Anatomical and molecular consequences of Unilateral Naris Closure on two populations of olfactory sensory neurons expressing defined odorant receptors
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Citation Excerpt :
In the closed side, a general reduction of the number of OSNs is observed [9]. However, at the level of the individual populations expressing defined ORs, the results are more balanced with increase in the number of neurons of some populations and decrease of others [7,13,38]. Here, by counting the GFP labeled cells in two gene-targeted strains, we confirm that changes induced by UNO are different depending on the population observed: while the M71 population appears unaffected (Fig. 2), the density of MOR23 neurons is reduced in the closed side (Fig. 1).
Mammalian olfactory sensory neurons (OSNs), the primary elements of the olfactory system, are located in the olfactory epithelium lining the nasal cavity. Exposed to the environment, their lifespan is short. Consequently, OSNs are regularly regenerated and several reports show that activity strongly modulates their development and regeneration: the peripheral olfactory system can adjust to the amount of stimulus through compensatory mechanisms. Unilateral naris occlusion (UNO) was frequently used to investigate this mechanism at the entire epithelium level. However, there is little data regarding the effects of UNO at the cellular level, especially on individual neuronal populations expressing a defined odorant receptor. Here, using UNO during the first three postnatal weeks, we analyzed the anatomical and molecular consequences of sensory deprivation in OSNs populations expressing the MOR23 and M71 receptors. The density of MOR23-expressing neurons is decreased in the closed side while UNO does not affect the density of M71-expressing neurons. Using Real Time qPCR on isolated neurons, we observed that UNO modulates the transcript levels for transduction pathway proteins (odorant receptors, CNGA2, PDE1c). The transcripts modulated by UNO will differ between populations depending on the receptor expressed. These results suggest that sensory deprivation will have different effects on different OSNs’ populations. As a consequence, early experience will shape the functional properties of OSNs differently depending on the type of odorant receptor they express.

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¹: Current address: Department of Medicine, University of Texas Health Sciences Center, San Antonio, TX, United States.

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State-dependent sculpting of olfactory sensory neurons is attributed to sensory enrichment, odor deprivation, and aging

Abstract

Graphical abstract

Section snippets

Acknowledgements

Neurosci. Lett.

Neuron

Cell

J. Biol. Chem.

Int. J. Dev. Neurosci.

Neurobiol. Learn. Mem.

Physiol. Behav.

Curr. Opin. Neurobiol.

Neuron

Neuron

Deletion of voltage-gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

J. Comp. Neurol.

Effects of ageing on smell and taste

Postgrad. Med. J.

Short-lasting exposure to one odour decreases general reactivity in the olfactory bulb of adult rats

Eur. J. Neurosci.

Axonal dynactin p150Glued transports caspase-8 to drive retrograde olfactory receptor neuron apoptosis

J. Neurosci.