Neural Mechanisms for Acoustic Signal Detection under Strong Masking in an Insect

Communication is fundamental for our understanding of behavior. In the acoustic modality, natural scenes for communication in humans and animals are often very noisy, decreasing the chances for signal detection and discrimination. We investigated the mechanisms enabling selective hearing under natural noisy conditions for auditory receptors and interneurons of an insect. In the studied katydid Mecopoda elongata species-specific calling songs (chirps) are strongly masked by signals of another species, both communicating in sympatry. The spectral properties of the two signals are similar and differ only in a small frequency band at 2 kHz present in the chirping species. Receptors sharply tuned to 2kHz are completely unaffected by the masking signal of the other species, whereas receptors tuned to higher audio and ultrasonic frequencies show complete masking. Intracellular recordings of identified interneurons revealed two mechanisms providing response selectivity to the chirp. (1) Response selectivity is when several identified interneurons exhibit remarkably selective responses to the chirps, even at signal-to-noise ratios of -21 dB, since they are sharply tuned to 2 kHz. Their dendritic arborizations indicate selective connectivity with low-frequency receptors tuned to 2 kHz. (2) Novelty detection is when a second group of interneurons is broadly tuned but, because of strong stimulus-specific adaptation to the masker spectrum and novelty detection to the 2 kHz band present only in the conspecific signal, these interneurons start to respond selectively to the chirp shortly after the onset of the continuous masker. Both mechanisms provide the sensory basis for hearing at unfavorable signal-to-noise ratios.