Effects of Inhibitory Timing on Contrast Enhancement in Auditory Circuits in Crickets (Teleogryllus oceanicus)

Abstract

In crickets ( Teleogryllus oceanicus), the paired auditory interneuron Omega Neuron 1 (ON1) responds to sounds with frequencies in the range from 3 to 40 kHz. The neuron is tuned to frequencies similar to that of conspecific songs (4.5 kHz), but its latency is longest for these same frequencies by a margin of 5–10 ms. Each ON1 is strongly excited by input from the ipsilateral ear and inhibits contralateral auditory neurons that are excited by the contralateral ear, including the interneurons ascending neurons 1 and 2 (AN1 and AN2). We investigated the functional consequences of ON1's long latency to cricket-like sound and the resulting delay in inhibition of AN1 and AN2. Using dichotic stimuli, we controlled the timing of contralateral inhibition of the ANs relative to their excitation by ipsilateral stimuli. Advancing the stimulus to the ear driving ON1 relative to that driving the ANs “subtracted” ON1's additional latency to 4.5 kHz. This had little effect on the spike counts of AN1 and AN2. The response latencies of these neurons, however, increased markedly. This is because in the absence of a delay in ON1's response, inhibition arrived at AN1 and AN2 early enough to abolish the first spikes in their responses. This also increased the variability of AN1 latency. This suggests that one possible function of the delay in ON1's response may be to protect the precise timing of the onset of response in the contralateral AN1, thus preserving interaural difference in response latency as a reliable potential cue for sound localization. Hyperpolarizing ON1 removed all detectable contralateral inhibition of AN1 and AN2, suggesting that ON1 is the main, if not the only, source of contralateral inhibition.