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

Curr Biol. 2010 Aug 24;20(16):1438-44. doi: 10.1016/j.cub.2010.06.021. Epub 2010 Jul 15.

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animal Communication
  • Animals
  • Behavior, Animal
  • Carbon Disulfide / chemistry*
  • Carbon Disulfide / pharmacology
  • Carbonic Anhydrase II / genetics
  • Carbonic Anhydrase II / metabolism
  • Carbonic Anhydrase II / physiology
  • Cyclic Nucleotide-Gated Cation Channels / genetics
  • Cyclic Nucleotide-Gated Cation Channels / metabolism
  • Cyclic Nucleotide-Gated Cation Channels / physiology
  • Food Preferences*
  • Guanylate Cyclase / genetics
  • Guanylate Cyclase / metabolism
  • Guanylate Cyclase / physiology
  • Mice
  • Olfactory Receptor Neurons / metabolism*
  • Patch-Clamp Techniques
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism
  • Receptors, Cell Surface / physiology
  • Social Behavior

Substances

  • Cnga3 protein, mouse
  • Cyclic Nucleotide-Gated Cation Channels
  • Receptors, Cell Surface
  • Carbonic Anhydrase II
  • Guanylate Cyclase
  • Gucy2d protein, mouse
  • Carbon Disulfide