title: 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.
authors.affiliation: Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD 21201, USA. smung001@umaryland.edu
authors.forename: Steven D
authors.initials: SD
authors.lastname: Munger
authors.forename: Trese
authors.initials: T
authors.lastname: Leinders-Zufall
authors.forename: Lisa M
authors.initials: LM
authors.lastname: McDougall
authors.forename: Renee E
authors.initials: RE
authors.lastname: Cockerham
authors.forename: Andreas
authors.initials: A
authors.lastname: Schmid
authors.forename: Petra
authors.initials: P
authors.lastname: Wandernoth
authors.forename: Gunther
authors.initials: G
authors.lastname: Wennemuth
authors.forename: Martin
authors.initials: M
authors.lastname: Biel
authors.forename: Frank
authors.initials: F
authors.lastname: Zufall
authors.forename: Kevin R
authors.initials: KR
authors.lastname: Kelliher
mesh_terms: D000819:Animal Communication; D000818:Animals; D001522:Behavior, Animal; D002246:Carbon Disulfide / Q000737:chemistry* / Q000494:pharmacology; D024402:Carbonic Anhydrase II / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D054815:Cyclic Nucleotide-Gated Cation Channels / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D005518:Food Preferences; D006162:Guanylate Cyclase / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D051379:Mice; D018034:Olfactory Receptor Neurons / Q000378:metabolism*; D018408:Patch-Clamp Techniques; D011956:Receptors, Cell Surface / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D012919:Social Behavior
chemical_list: C518237:Cnga3 protein, mouse; D054815:Cyclic Nucleotide-Gated Cation Channels; D011956:Receptors, Cell Surface; D024402:Carbonic Anhydrase II; D006162:Guanylate Cyclase; C484774:Gucy2d protein, mouse; D002246:Carbon Disulfide