Neurite-specific Ca2+ dynamics underlying sound processing in an auditory interneurone

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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 Ca2+ 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 Ca2+ rise followed the onset spike rate of ON1, while the final Ca2+ level depended on the mean spike rate. Ca2+ rapidly increased in both dendritic and axonal arborizations and only gradually in the axon and the cell body. Ca2+ levels were particularly high at the spike-generating zone. Through the activation of a Ca2+-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 Ca2+ level in the chirp rhythm, but not the faster syllable rhythm. The Ca2+-mediated hyperpolarization of ON1 suppressed background spike activity between chirps, acting as a noise filter. During directional auditory processing, the functional interaction of Ca2+-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

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