Neurite‐specific Ca 2+ dynamics underlying sound processing in an auditory interneurone

Abstract Concepts on neuronal signal processing and integration at a cellular and subcellular level are driven by recording techniques and model systems available. The cricket CNS with the omega‐1‐neurone (ON1) provides a model system for auditory pattern recognition and directional processing. Exploiting ON1's planar structure we simultaneously imaged free intracellular Ca 2+ at both input and output neurites and recorded the membrane potential in vivo during acoustic stimulation. In response to a single sound pulse the rate of Ca 2+ rise followed the onset spike rate of ON1, while the final Ca 2+ level depended on the mean spike rate. Ca 2+ rapidly increased in both dendritic and axonal arborizations and only gradually in the axon and the cell body. Ca 2+ levels were particularly high at the spike‐generating zone. Through the activation of a Ca 2+ ‐sensitive K + current this may exhibit a specific control over the cell's electrical response properties. In all cellular compartments presentation of species‐specific calling song caused distinct oscillations of the Ca 2+ level in the chirp rhythm, but not the faster syllable rhythm. The Ca 2+ ‐mediated hyperpolarization of ON1 suppressed background spike activity between chirps, acting as a noise filter. During directional auditory processing, the functional interaction of Ca 2+ ‐mediated inhibition and contralateral synaptic inhibition was demonstrated. Upon stimulation with different sound frequencies, the dendrites, but not the axonal arborizations, demonstrated a tonotopic response profile. This mirrored the dominance of the species‐specific carrier frequency and resulted in spatial filtering of high frequency auditory inputs. © 2006 Wiley Periodicals, Inc. J Neurobiol 67: 68–80, 2007