Postsynaptic inhibition mediates high-frequency selectivity in the cricket Teleogryllus oceanicus: implications for flight phonotaxis behavior

Abstract

The frequency selectivity of the identified auditory interneuron, Int-1, in the cricket Teleogryllus oceanicus was examined using intracellular recording and staining techniques. Previous behavioral assays showed that crickets discriminate the low frequencies of the species calling song (4-5 kHz) from the high frequencies contained in the vocalizations of insectivorous bats (Nolen and Hoy, 1986a). Int-1 was excited by frequencies between 3 and 40 kHz, being similar, therefore, to the tympal organ (ear) in its broad range sensitivity; however, it responded differentially to high and low frequencies in terms of the number of action potentials evoked per stimulus tone pulse, the average discharge rate, and the latency of response. It was especially responsive to ultrasound (greater than 20 kHz), discharging at rates up to 400 spikes/sec (average rate), with 10 msec latencies; its response to pulses of the calling song was less than 150 spikes/sec, with 30 msec latencies. Int-1's dynamic range for ultrasound was also quite large, about 50 dB, compared to 20 dB for the calling song frequency. In addition, it responded well to trains of short, batlike pulses of ultrasound. These results are consistent with previous behavioral experiments showing that during flight, Int-1 was both necessary and sufficient for the ultrasound avoidance steering behavior (Nolen and Hoy, 1984), as long as it discharged above a rate of 180 spikes/sec. Ultrasound readily produced such high rates, whereas calling song rarely did; ultrasound reliably evoked avoidance steering over a wide dynamic range, while tone pulses of the calling song rarely did so (Nolen and Hoy, 1986a). A unique source of ipsilaterally mediated inhibition, tuned to the calling song frequency, accounted for the poor response to calling song and hence the neuron's high-frequency selectivity, and the behavioral and physiological effects of 2-tone suppression of high frequencies by the calling song (Nolen and Hoy, 1986b). These results further strengthen Int-1's proposed role as a "bat-detector" during flight and suggest only a limited role in other contexts such as social behavior.