Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period

Qiu, Qiang; Wu, Yunming; Ma, Limei; Xu, Wenjing; Hills, Max; Ramalingam, Vivekanandan; Yu, Chong

doi:10.7554/elife.60546

Cited by 25 publications

(26 citation statements)

References 100 publications

(156 reference statements)

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“…Error bars denote SEM. Note that when presented with easier (less similar) odor pairs, MRT and SRT mice exhibit similar discrimination performance [ 74 ]. E. Occupancy, activation, and discrimination capacity effects in noses where each glomerulus received only 1% of its activation from each of the eight secondary receptors.…”

Section: Resultsmentioning

confidence: 99%

“…The specificity of OSN convergence onto individual glomeruli has long been hypothesized to contribute to odor discrimination capabilities [ 56 , 71 – 73 ]. We asked whether a modest disruption of this convergence specificity on the scale demonstrated by Kir2.1 (MRT) mice would yield impairments in discrimination sensitivity when presented with tests rendered difficult owing to low concentrations or highly similar odorant mixtures; notably, Kir2.1 MRT mice exhibit no significant impairments in performance when presented with easier discrimination tasks [ 74 ]. First, we performed a cross-habituation assay between 30/70 and 70/30 ratio mixtures of four odor pairs ( Table 1 ).…”

Section: Resultsmentioning

confidence: 99%

“…A. Whole tasks [74]. First, we performed a cross-habituation assay between 30/70 and 70/30 ratio mixtures of four odor pairs (Table 1).…”

Section: Fig 8 Effects Of Multi-receptor Convergence Onto Common Glomerulimentioning

confidence: 99%

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A physicochemical model of odor sampling

et al. 2021

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We present a general physicochemical sampling model for olfaction, based on established pharmacological laws, in which arbitrary combinations of odorant ligands and receptors can be generated and their individual and collective effects on odor representations and olfactory performance measured. Individual odor ligands exhibit receptor-specific affinities and efficacies; that is, they may bind strongly or weakly to a given receptor, and can act as strong agonists, weak agonists, partial agonists, or antagonists. Ligands interacting with common receptors compete with one another for dwell time; these competitive interactions appropriately simulate the degeneracy that fundamentally defines the capacities and limitations of odorant sampling. The outcome of these competing ligand-receptor interactions yields a pattern of receptor activation levels, thereafter mapped to glomerular presynaptic activation levels based on the convergence of sensory neuron axons. The metric of greatest interest is the mean discrimination sensitivity, a measure of how effectively the olfactory system at this level is able to recognize a small change in the physicochemical quality of a stimulus. This model presents several significant outcomes, both expected and surprising. First, adding additional receptors reliably improves the system’s discrimination sensitivity. Second, in contrast, adding additional ligands to an odor scene initially can improve discrimination sensitivity, but eventually will reduce it as the number of ligands increases. Third, the presence of antagonistic ligand-receptor interactions produced clear benefits for sensory system performance, generating higher absolute discrimination sensitivities and increasing the numbers of competing ligands that could be present before discrimination sensitivity began to be impaired. Finally, the model correctly reflects and explains the modest reduction in odor discrimination sensitivity exhibited by transgenic mice in which the specificity of glomerular targeting by primary olfactory neurons is partially disrupted.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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A physicochemical model of odor sampling

et al. 2021

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“…Studies from several neural systems have demonstrated that neuronal activity and Ca 2+ signaling play a vital role in the coordination and control of neuronal refinement (Golovin et al, 2019;Kanamori et al, 2013;Kano et al, 2018;Mayseless et al, 2018;Qiu et al, 2020). We therefore set out to examine the Ca 2+ dynamics during the stereotypic remodeling of γ-Kenyon cells (KCs; Figure 1 A, Lee et al, 2000), the major intrinsic cell type within the Drosophila mushroom body (MB).…”

Section: Calcium Levels In γ-Kcs Are Dynamic Upon Transition Into Metamorphosismentioning

confidence: 99%

Silencing neuronal activity is required for developmental circuit remodeling

Mayseless

Shapira

et al. 2021

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SummaryPostnatal refinement of neuronal connectivity shapes the mature nervous system. Pruning of exuberant connections involves both cell autonomous and non-cell autonomous mechanisms, such as neuronal activity. While the role of neuronal activity in the plasticity of excitatory synapses has been extensively studied, the involvement of inhibition is less clear. Furthermore, the role of activity during stereotypic developmental remodeling, where competition is not as apparent, is not well understood.Here we use the Drosophila mushroom body as a model to show that regulated silencing of neuronal activity is required for developmental axon pruning of the γ-Kenyon cells. We demonstrate that silencing neuronal activity is mechanistically achieved by cell autonomous expression of the inward rectifying potassium channel (irk1) combined with inhibition by the GABAergic APL neuron. These results support the Hebbian-like rule ‘use it or lose it’, where inhibition can destabilize connectivity and promote pruning while excitability stabilizes existing connections.

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“…TMA is a sex- and species-specific odor cue that is enriched in the urine of adult male (but not juvenile or female) Mus musculus 38,39 . While it has been reported to elicit attraction in mice 39-41 , how TMA influences social interactions is not known. Here we show that TMA, acting through TAAR5, promotes inter-male aggression, revealing a single, defined main olfactory input that drives a key social behavior in mammals.…”

Section: Introductionmentioning

confidence: 99%

Map-independent representation of an aggression-promoting social cue in the main olfactory pathway

Cichy

Dewan

Zhang

et al. 2021

Preprint

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While the olfactory system is required for proper social behaviors, the molecular basis for how social cues are detected via the main olfactory pathway of mammals is not well-characterized. Trimethylamine is a volatile, sex-specific odor found in adult male mouse urine that selectively activates main olfactory sensory neurons that express trace amine-associated receptor 5 (TAAR5). Here we show that trimethylamine, acting via TAAR5, elicits state-dependent attraction or aversion in male mice and drives inter-male aggression. Genetic knockout of TAAR5 significantly reduces aggression-related behaviors, while adding trimethylamine augments aggressive behavior towards juvenile males. We further show that transgenic expression of TAAR5 specifically in olfactory sensory neurons rescues aggressive behaviors in knockout mice, despite extensive remapping of TAAR5 projections to the olfactory bulb. Our results identify a specific main olfactory input that detects a prominent male-specific odor to induce inter-male aggression in a mammalian species and reveal that apparently innate behavioral responses are independent of patterned glomerular input to the olfactory bulb.

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Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period

Cited by 25 publications

References 100 publications

A physicochemical model of odor sampling

A physicochemical model of odor sampling

Silencing neuronal activity is required for developmental circuit remodeling

Map-independent representation of an aggression-promoting social cue in the main olfactory pathway

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