Ca ²⁺ -Activated Ion Channels Exert Opposite Effects in Different Signaling Compartments of Vomeronasal Sensory Neurons

Abstract

In most mammals, conspecific chemical cues that drive innate social and sexual behavior are detected by the vomeronasal organ (VNO) and processed in the accessory olfactory bulb (AOB). Chemosensory stimulation of vomeronasal sensory neurons (VSNs) at their microvillous dendritic knobs triggers, first, a local signal transduction and amplification cascade and, second, transformation of that signal into action potential (AP) discharge at the soma. Both processes—signal transduction and AP generation—involve local Ca 2+ elevations in the knob and soma, respectively. Here, we revisit the somewhat still controversial functions of Ca 2+ -activated ion channels in both VSN compartments. In acute mouse VNO slices (of either sex), focal photorelease of Ca 2+ reveals that VSN knob and soma both act as independent Ca 2+ signaling compartments, in which Ca 2+ elevations exert opposite effects. While Ca 2+ signals in the knob drive an excitatory inward current, Ca 2+ elevations in the soma primarily activate hyperpolarizing outward currents that silence VSNs. A substantial fraction of the latter current is mediated by SK and/or BK channels. Notably, SK channel activity strongly affects VSN firing. Together, our study reveals a diverse composition of Ca 2+ -activated currents in VSN somata and uncovers an unexpected role of SK channels in dampening excitability and, thus, in controlling VSN-to-AOB information transfer.