Variation in olfactory neuron repertoires is genetically controlled and environmentally modulated

Ibarra-Soria, Ximena; Nakahara, Thiago Seike; Lilue, Jingtao; Jiang, Yue; Trimmer, Casey; Souza, Mateus A.A.; Netto, Paulo H.M.; Ikegami, Kentaro; Murphy, Nicolle R.; Kusma, Mairi; Kirton, Andrea; Saraiva, Luís R.; Keane, Thomas; Matsunami, Hiroaki; Mainland, Joel D.; Papes, Fábio; Logan, Darren W.

doi:10.7554/elife.21476

Cited by 82 publications

(94 citation statements)

References 73 publications

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“…Past work demonstrating a correlation between OR transcript abundance and the number of OSNs expressing those ORs, led us to quantify the number of OSNs expressing these ORs by in situ hybridization 13, 14 . We probed specifically for the expression of Olfr910 , Olfr912 , and Olfr1295 on the MOE of sex-separated male and female mice using anti-sense probes against the open reading frames (ORF) of each of these ORs.…”

Section: Resultsmentioning

confidence: 99%

“…Emerging literature has evidenced a role for experience in influencing sensory-cell representations within the olfactory epithelium 14, 23, 24 . Thus, our identification of a subset of over-represented ORs in sex-separated female mice led to us to hypothesize a role for experience in generating this dimorphism.…”

Section: Resultsmentioning

confidence: 99%

“…Given the capacity of the MOE to regenerate throughout the life of an animal 28 , it has been suggested activity-mediated mechanisms may “individualize” the olfactory system by influencing OSN population dynamics 14 . While we acknowledge cohabitation of the opposite sexes induces a number of changes in the nervous system of mice (compared to sex-separation) 2, 3 , we propose that changes in OSN population dynamics, following cohabitation, for OSNs expressing Olfr910/912 and Olfr1295 , are in part mediated by olfactory experience with SBT and MTMT.…”

Section: Discussionmentioning

confidence: 99%

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Semiochemical responsive olfactory sensory neurons are sexually dimorphic and plastic

Vihani

Gundala

et al. 2019

Preprint

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24Understanding how genes and experiences work in concert to generate phenotypic variability will 25 provide a better understanding of individuality. Here, we considered this in the context of the main 26 olfactory epithelium, a chemosensory structure with over a thousand distinct cell-types, in mice. We 27 identified a subpopulation of at least three types of olfactory sensory neurons, defined by receptor 28 expression, whose abundances were sexually dimorphic. This subpopulation of olfactory sensory 29 neurons was over-represented in sex-separated female mice and responded robustly to the male-30 specific semiochemicals 2-sec-butyl-4,5-dihydrothaizole and (methylthio)methanethiol. housing led to a robust attenuation of the female over-representation. Testing of Bax null mice 32 revealed a Bax-dependence in generating the sexual dimorphism in sex-separated mice. Altogether, 33 our results suggest a profound role of experience in influencing homeostatic neural lifespan 34 mechanisms to generate a robust sexually dimorphic phenotype in the main olfactory epithelium. a subset of ORs that exhibit sexually dimorphic expression under sex-separated conditions. In situ 61 mRNA hybridization probing for the expression of these ORs demonstrated the proportions of OSNs 62 expressing these ORs to be over-represented in female mice. Activity-dependent labeling experiments 63 further identified this subpopulation of OSNs as selective responders to odor cues generated by 64 mature male mice. Targeted screening of previously identified sex-specific and sex-enriched volatiles 65 demonstrated that this subpopulation of OSNs responded robustly to the reproductive-behavior and 66 physiology modifying semiochemicals 2-sec-butyl-4,5-dihydrothaizole (SBT) and 67 (methylthio)methanethiol (MTMT) in vivo. Finally, to test the role of experience in generating this 68 sexual dimorphism, we switched male and female mice from sex-separated conditions to sex-69 combined conditions and learned the sexual dimorphism had severely attenuated. Examination of sex-70 separated mutant mice null for the BCL2-associated X protein (Bax -/-) revealed a failure to generate 71 robust sexual dimorphisms within the whole olfactory mucosa. During the course of our investigations, 72 a report, van der Linden et al. 2018, was also published with some overlapping findings. Altogether, 73 these results suggest a link between specific olfactory experiences and OSN lifespan as a means to 74 influence sensory cell-level odor representations in the olfactory system. 75 76Results 77 Identification of sexually dimorphic ORs in the MOE 78We first performed RNA-Seq on the whole olfactory mucosa of male and female mice at various ages 79 housed under sex-separated conditions ( Figure 1A). Differential expression analysis of ORs revealed no 80 obvious sexually dimorphic OR expression at 3 weeks (weaning) age. In contrast, progressive 81 differential expression analysis of ORs at 9, 26, and 43 weeks age revealed at least three OR genes: 82Olfr910, Olfr912, and Olfr1295, to...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Semiochemical responsive olfactory sensory neurons are sexually dimorphic and plastic

Vihani

Gundala

et al. 2019

Preprint

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“…present. Consequently, the mean concentration of a ligand in any odor reads c i = p i µ i 50 and the associated variance is var(c i ) = (p i − p 2 i )µ 2 i + p i σ 2 i . For simplicity, we consider 51 ligands with equal statistics in this paper, so the distribution P env (c) of odors is 52 characterized by the three parameters p i = p, µ i = µ, and σ i = σ.…”

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confidence: 99%

“…Various strategies could play a role in 345 keeping the activity of the receptor types similar [46]: On timescales as short as a single 346 sniff, the inhibition strength could be adjusted to regulate the relative importance of 347 receptor excitations [47]. On longer timescales of several weeks, there are changes of the 348 receptor copy number that directly affect the sensitivity of the glomeruli [48][49][50] and the 349 processing neurons in the olfactory bulb [51,52]. Receptor copy number adaptations 350 influence the signal-to-noise ratio at the receptor level, so the copy number could be 351 increased to improve the detection of frequently appearing odors [53].…”

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Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned

Zwicker

2018

Preprint

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The olfactory system faces the difficult task of identifying an enormous variety of odors independent of their intensity. Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, is one possible representation that can facilitate this task. So far, it is unclear whether primacy coding facilitates typical olfactory tasks and what constraints it implies for the olfactory system. In this paper, we develop a simple model of primacy coding, which we simulate numerically and analyze using a statistical description. We show that the encoded information depends strongly on the number of receptor types included in the primacy representation, but only weakly on the size of the receptor repertoire. The representation is independent of the odor intensity and the transmitted information is useful to perform typical olfactory tasks, like detecting a target odor or discriminating similar mixtures, with close to experimentally measured performance. Interestingly, we find situations in which a smaller receptor repertoire is advantageous for identifying a target odor. The model also suggests that overly sensitive receptor types could dominate the entire response and make the whole array useless, which allows us to predict how receptor arrays need to adapt to stay useful during environmental changes. By quantifying the information transmitted using primacy coding, we can thus connect microscopic characteristics of the olfactory system to its overall performance. Author summaryHumans can identify odors independent of their intensity. Experimental data suggest that this is accomplished by representing the odor identity by the earliest responding receptor types. Using theoretical modeling, we here show that such a primacy code allows discriminating odors with close to experimentally measured performance. This performance depends strongly on the number of receptors considered in the primacy code, but the receptor repertoire size is less important. The model also suggests a strong evolutionary pressure on the receptor sensitivities, which could explain observed receptor copy number adaptations. Taken together, the model connects detailed molecular measurements to large-scale psycho-physical measurements, which will contribute to our understanding of the olfactory system. July 9, 2018 1/22 1 The olfactory system identifies and discriminates odors for solving vital tasks like 2 navigating the environment, identifying food, and engaging in social interactions. These 3 tasks are complicated by the enormous variety of odors, which vary in composition and 4 in the concentrations of their individual molecules. In particular, the olfactory system 5 needs to separately recognize the odor identity (what is there?) and the odor intensity 6 (how much is there?). For instance, the identity is required to decide whether to 7 approach or avoid an odor source, whereas the intensity information is important for 8 localizing it. It is unclear how these two odor properties are separated. 9Odors are sensed by olfactor...

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The influence of olfactory experience on the birthrates of olfactory sensory neurons with specific odorant receptor identities

Rufenacht,

Asson,

Hossain

et al. 2024

Genesis

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SummaryOlfactory sensory neurons (OSNs) are one of a few neuron types that are generated continuously throughout life in mammals. The persistence of olfactory sensory neurogenesis beyond early development has long been thought to function simply to replace neurons that are lost or damaged through exposure to environmental insults. The possibility that olfactory sensory neurogenesis may also serve an adaptive function has received relatively little consideration, largely due to the assumption that the generation of new OSNs is stochastic with respect to OSN subtype, as defined by the single odorant receptor gene that each neural precursor stochastically chooses for expression out of hundreds of possibilities. Accordingly, the relative birthrates of different OSN subtypes are predicted to be constant and impervious to olfactory experience. This assumption has been called into question, however, by evidence that the birthrates of specific OSN subtypes can be selectively altered by manipulating olfactory experience through olfactory deprivation, enrichment, and conditioning paradigms. Moreover, studies of recovery of the OSN population following injury provide further evidence that olfactory sensory neurogenesis may not be strictly stochastic with respect to subtype. Here we review this evidence and consider mechanistic and functional implications of the prospect that specific olfactory experiences can regulate olfactory sensory neurogenesis rates in a subtype‐selective manner.

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Variation in olfactory neuron repertoires is genetically controlled and environmentally modulated

Cited by 82 publications

References 73 publications

Semiochemical responsive olfactory sensory neurons are sexually dimorphic and plastic

Semiochemical responsive olfactory sensory neurons are sexually dimorphic and plastic

Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned

The influence of olfactory experience on the birthrates of olfactory sensory neurons with specific odorant receptor identities

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