The influences of chemosensory signaling on “mission-critical” mammalian behavior
Terrestrial mammals have evolved a small, direct, and behaviorally influential sensory pathway into the brain, called the accessory olfactory system (AOS). AOS chemosensation supports behaviors that are important for survival and reproduction, including predator avoidance, territorial defense, and mate choice. The AOS achieves these effects by sensing and interpreting nonvolatile (i.e., non-airborne) chemosignals found in animal excretions, including urine, saliva, and tears. Despite its behavioral importance, the understanding of AOS function lags well behind other sensory modalities.
We will present results from two projects, one aimed at discovering new AOS ligands, and the other focused on AOS plasticity. A major barrier to studying sensory processing in the AOS is limited knowledge of natural AOS ligands. We investigated whether feces, a plentiful but under-studied source of environmental chemosignals, contains AOS ligands. We discovered that bile acids, which are critical regulators of fat absorption in the gut, are enriched in feces and are natural AOS ligands. Moreover, we found that AOS neurons are selectively tuned to bile acids that vary with sex, species, and gut flora. These data reveal a new class of natural AOS ligands that are likely to influence mammalian behavior.
The AOS is often labeled as a “hard-wired” neural circuit, suggesting that the system lacks plasticity. The AOS is, in fact, a plastic pathway. Plasticity in the AOS has mainly been studied in females after mating, which causes increased GABAergic inhibition of mitral cells (MCs) in the accessory olfactory bulb (AOB). We wanted to determine whether increased MC inhibition was specific to mating, or whether it was a general phenomenon, so we studied AOB plasticity in males after territorial aggression encounters. We found that AOB interneurons expressing the plasticity-associated immediate-early gene Arc/Arg3.1 after territorial aggression were highly excitable and more responsive to sensory input stimulation than neurons that did not express Arc. Arc-expressing interneurons strongly suppressed MC activity, suggesting that increased MC inhibition by these interneurons may be a general response to social chemosensory experience.
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