Journal of Neuroscience, Vol 7, 2081-2096, Copyright © 1987 by Society for Neuroscience
Postsynaptic inhibition mediates high-frequency selectivity in the cricket Teleogryllus oceanicus: implications for flight phonotaxis behavior
TG Nolen and RR Hoy
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.
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