Differential Temporal Coding of Rhythmically Diverse Acoustic Signals by a Single Interneuron

Abstract

The omega neuron 1 (ON1) of the cricket Teleogryllus oceanicus responds to conspecific signals (4.5 kHz) and to the ultrasonic echolocation sounds used by hunting, insectivorous bats. These signals differ in temporal structure as well as in carrier frequency. We show that ON1's temporal coding properties vary with carrier frequency, allowing it to encode both of these behaviorally important signals. Information-transfer functions show that coding of 4.5 kHz is limited to the range of amplitude-modulation components that occur in cricket songs (<32 Hz), whereas coding of 30-kHz stimuli extends to the higher pulse rates that occur in bat sounds (∼100 Hz). Nonlinear coding contributes to the information content of ON1's spike train, particularly for 30-kHz stimuli with high intensities and large modulation depths. Phase locking to sinusoidal amplitude envelopes also extends to higher AM frequencies for ultrasound stimuli. ON1s frequency-specific behavior cannot be ascribed to differences in the shapes of information-transfer functions of low- and high-frequency-tuned receptor neurons, both of which are tuned more broadly to AM frequencies than ON1. Coding properties are nearly unaffected by contralateral deafferentation. ON1's role in auditory processing is to increase binaural contrast through contralateral inhibition. We hypothesize that its frequency-specific temporal coding properties optimize binaural contrast for sounds with both the spectral and temporal features of behaviorally relevant signals.