Frequency Processing at Consecutive Levels in the Auditory System of Bush Crickets (Tettigoniidae)

Abstract

We asked how processing of male signals in the auditory pathway of the bush cricket Ancistrura nigrovittata (Phaneropterinae, Tettigoniidae) changes from the ear to the brain. From 37 sensory neurons in the crista acustica single elements (cells 8 or 9) have frequency tuning corresponding closely to the behavioral tuning of the females. Nevertheless, one-quarter of sensory neurons (approximately cells 9 to 18) excite the ascending neuron 1 (AN 1), which is best tuned to the male's song carrier frequency. AN1 receives frequency-dependent inhibition, reducing sensitivity especially in the ultrasound. When recorded in the brain, AN1 shows slightly lower overall activity than when recorded in the prothoracic ganglion close to the spike-generating zone. This difference is significant in the ultrasonic range. The first identified local brain neuron in a bush cricket (LBN1) is described. Its dendrites overlap with some of AN1-terminations in the brain. Its frequency tuning and intensity dependence strongly suggest a direct postsynaptic connection to AN1. Spiking in LBN1 is only elicited after summation of excitatory postsynaptic potentials evoked by individual AN1-action potentials. This serves a filtering mechanism that reduces the sensitivity of LBN1 and also its responsiveness to ultrasound as compared to AN1. Consequently, spike latencies of LBN1 are long (>30 ms) despite its being a second-order interneuron. Additionally, LBN1 receives frequency-specific inhibition, most likely further reducing its responses to ultrasound. This demonstrates that frequency-specific inhibition is redundant in two directly connected interneurons on subsequent levels in the auditory system. J. Comp. Neurol. 518:3101-3116, 2010. (C) 2010 Wiley-Liss, Inc.