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An olfactory subsystem that detects carbon disulfide and mediates food-related social learning.

ABSTRACT: Olfactory signals influence social interactions in a variety of species. In mammals, pheromones and other social cues can promote mating or aggression behaviors; can communicate information about social hierarchies, genetic identity and health status; and can contribute to associative learning. However, the molecular, cellular, and neural mechanisms underlying many olfactory-mediated social interactions remain poorly understood. Here, we report that a specialized olfactory subsystem that includes olfactory sensory neurons (OSNs) expressing the receptor guanylyl cyclase GC-D, the cyclic nucleotide-gated channel subunit CNGA3, and the carbonic anhydrase isoform CAII (GC-D(+) OSNs) is required for the acquisition of socially transmitted food preferences (STFPs) in mice. Using electrophysiological recordings from gene-targeted mice, we show that GC-D(+) OSNs are highly sensitive to the volatile semiochemical carbon disulfide (CS(2)), a component of rodent breath and a known social signal mediating the acquisition of STFPs. Olfactory responses to CS(2) are drastically reduced in mice lacking GC-D, CNGA3, or CAII. Disruption of this sensory transduction cascade also results in a failure to acquire STFPs from either live or surrogate demonstrator mice or to exhibit hippocampal correlates of STFP retrieval. Our findings indicate that GC-D(+) OSNs detect chemosignals that facilitate food-related social interactions.

SUBMITTER: Munger SD

PROVIDER: S-EPMC2929674 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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An olfactory subsystem that detects carbon disulfide and mediates food-related social learning.

Munger Steven D SD Leinders-Zufall Trese T McDougall Lisa M LM Cockerham Renee E RE Schmid Andreas A Wandernoth Petra P Wennemuth Gunther G Biel Martin M Zufall Frank F Kelliher Kevin R KR

Current biology : CB 20100715 16

Olfactory signals influence social interactions in a variety of species. In mammals, pheromones and other social cues can promote mating or aggression behaviors; can communicate information about social hierarchies, genetic identity and health status; and can contribute to associative learning. However, the molecular, cellular, and neural mechanisms underlying many olfactory-mediated social interactions remain poorly understood. Here, we report that a specialized olfactory subsystem that include ...[more]

PMID: 20637621

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Project description:Behavioural responses of animals to volatiles in their environment are generally dependent on context. Most natural odours are mixtures of components that can each induce different behaviours when presented on their own. We have investigated how a complex of two olfactory stimuli is evaluated by Drosophila flies in a free-flying two-trap choice assay and how these stimuli are encoded in olfactory receptor neurons. We first observed that volatiles from apple cider vinegar attracted flies while carbon dioxide (CO2) was avoided, confirming their inherent positive and negative values. In contradiction with previous results obtained from walking flies in a four-field olfactometer, in the present assay the addition of CO2 to vinegar increased rather than decreased the attractiveness of vinegar. This effect was female-specific even though males and females responded similarly to CO2 and vinegar on their own. To test whether the female-specific behavioural response to the mixture correlated with a sexual dimorphism at the peripheral level we recorded from olfactory receptor neurons stimulated with vinegar, CO2 and their combination. Responses to vinegar were obtained from three neuron classes, two of them housed with the CO2-responsive neuron in ab1 sensilla. Sensitivity of these neurons to both CO2 and vinegar per se did not differ between males and females and responses from female neurons did not change when CO2 and vinegar were presented simultaneously. We also found that CO2-sensitive neurons are particularly well adapted to respond rapidly to small concentration changes irrespective of background CO2 levels. The ability to encode temporal properties of stimulations differs considerably between CO2- and vinegar-sensitive neurons. These properties may have important implications for in-flight navigation when rapid responses to fragmented odour plumes are crucial to locate odour sources. However, the flies' sex-specific response to the CO2-vinegar combination and the context-dependent hedonics most likely originate from central rather than peripheral processing.

Project description:BackgroundCOVID-19 threatens the global community because a large fraction of infected people are asymptomatic, yet can effectively transmit SARS-CoV-2. Finding and isolating these silent carriers is a crucial step in confining the spread of the disease. A sudden loss of the sense of smell has been self-reported by COVID-19 patients across different countries, consistent with expression of the molecular factors mediating SARS-CoV-2 uptake into human olfactory epithelial supporting cells. However, precise quantification of olfactory loss in asymptomatic COVID-19 carriers is missing to date.MethodsTo quantify olfactory functions in asymptomatic COVID-19 patients, we designed an olfactory-action meter that determines detectability indices at different odor concentrations and an olfactory matching accuracy score using monomolecular odors. The optimization of test parameters allowed us to reliably and accurately assess olfactory deficits in a patient within 20 minutes.FindingsMeasurement of detection indices at low concentrations revealed a 50% reduction in asymptomatic COVID-19 carriers. Further, patients with better detection scores showed significantly reduced olfactory matching accuracies compared to normal healthy subjects. Our quantification of olfactory loss, considering all parameters, identified 82% of the asymptomatic SARS-CoV-2 carriers with olfactory deficits. However, on subjective evaluation, only 15% of the patients noticed a compromised ability to smell.InterpretationCompromised olfactory fitness can serve as a strong basis for identifying asymptomatic COVID-19 patients. Detailed design specifications and protocols provided here should enable the development of a sensitive, fast, and economical screening strategy that can be administered to large populations to prevent the rapid spread of COVID-19.FundingThis work was supported by the DBT - Wellcome Trust India Alliance intermediate grant (IA/I/14/1/501,306 to N.A.) and UGC NET Fellowship (A.B.). All the funding sources played no roles in the study.

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An olfactory subsystem that detects carbon disulfide and mediates food-related social learning.

Publications

An olfactory subsystem that detects carbon disulfide and mediates food-related social learning.

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