Abstract
Controlling stimulus access to sensory organs allows animals to optimize sensory reception and prevent damage. The vomeronasal organ (VNO) detects pheromones and other semiochemicals to regulate innate social and sexual behaviors. This semiochemical detection generally requires the VNO to draw in chemical fluids, such as bodily secretions, which are complex in composition and can be contaminated. Little is known about whether and how chemical constituents are monitored to regulate the fluid access to the VNO. Using transgenic mice and immunolabeling, we found that solitary chemosensory cells (SCCs) reside densely at the entrance duct of the VNO. In this region, most of the intraepithelial trigeminal fibers innervate the SCCs, indicating that SCCs relay sensory information onto the trigeminal fibers. These SCCs express transient receptor potential channel M5 (TRPM5) and the phospholipase C (PLC) β2 signaling pathway. Additionally, the SCCs express choline acetyltransferase (ChAT) and vesicular acetylcholine transporter (VAChT) for synthesizing and packaging acetylcholine, a potential transmitter. In intracellular Ca2+ imaging, the SCCs responded to various chemical stimuli including high concentrations of odorants and bitter compounds. The responses were suppressed significantly by a PLC inhibitor, suggesting involvement of the PLC pathway. Further, we developed a quantitative dye assay to show that the amount of stimulus fluid that entered the VNOs of behaving mice is inversely correlated to the concentration of odorous and bitter substances in the fluid. Genetic knockout and pharmacological inhibition of TRPM5 resulted in larger amounts of bitter compounds entering the VNOs. Our data uncovered that chemoreception of fluid constituents regulates chemical access to the VNO and plays an important role in limiting the access of non-specific irritating and harmful substances. Our results also provide new insight into the emerging role of SCCs in chemoreception and regulation of physiological actions.
Highlights
Sensory detection of the surrounding environment requires vertebrate specialized sensory organs to have access to external stimuli
We found that the phospholipase C (PLC) expressed in the solitary chemosensory cells (SCCs) plays an important role in detecting both odorous and bitter substances, and that a functioning transient receptor potential channel M5 (TRPM5) is critical for signal transduction of bitter substances, limiting their access to the vomeronasal organ (VNO)
Since TRPM5 is only expressed in SCCs, not in the trigeminal fibers, our results strongly demonstrate the role of SCCs and TRPM5 in detecting bitter fluid constituents to limit their access to VNOs
Summary
Sensory detection of the surrounding environment requires vertebrate specialized sensory organs to have access to external stimuli. The pupillary light reflex in mammalian eyes controls the amount of light reaching the retina, allowing photoreceptors to detect a wide range of light intensity as well as protecting the retina from burning sunlight [2]. While such regulation is well documented in visual and auditory systems [2,3], little is known about whether and how the access of chemical stimuli to the VNO in the olfactory system is regulated. It is essential to monitor fluid constituents to limit the VNO access of irritating and harmful substances
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