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

Abstract

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 2 kHz 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 Ϫ21 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.

Auditory DUM neurons in a bush‐cricket: A filter bank for carrier frequency

“…Studies in Ensifera (crickets and bush‐crickets) focus on ear function and afferent sensory neurons (reviewed in Mason & Faure, 2004; Yack, 2004; Stumpner & Nowotny, 2014), central auditory processing including information coding and its relevance for intraspecific behavior and predator detection (reviewed in Gerhardt & Huber, 2002; Hedwig, 2014) and the evolution of the auditory systems (Desutter‐Grandcolas, 2003; Shaw & Lesnick, 2009; Strauß & Lakes‐Harlan, 2009; Stumpner & von Helversen, 2001). The structure and response properties of prothoracic auditory interneurons are well studied (Atkins & Pollack, ; Kostarakos & Römer, ; Rheinlaender, ; Stumpner & Molina, ; Triblehorn & Schul, ), but little is known about the prothoracic auditory network and its functional design (Molina & Stumpner, ; Pollack & Imaizumi, ; Römer et al, ; Triblehorn & Schul, ). Experimental evidence indicates that local prothoracic neurons contribute to the processing of sound direction, carrier frequency, and temporal patterns in crickets (Faulkes & Pollack, ; Hardt & Watson, ; Selverston et al, ) and bush‐crickets (Prešern et al, ; Rheinlaender, ; Römer, ; Römer et al, ; Schul, ; Stumpner, ; Stumpner & Molina, ).…”

Plasticity of signaling and mate choice in a trilling species of the Mecopoda complex (Orthoptera: Tettigoniidae)

“…The spectrum in the song covers a wide frequency range, which includes both audio and ultrasonic frequencies up to 80 kHz. A frequency analysis has shown that both song motifs exhibit similar spectral compositions (Kostarakos and Römer 2015 ).…”

Matched Filters in Insect Audition: Tuning Curves and Beyond

“…Apparently, this species uses its potential for frequency analysis in the ear to detect the small spectral difference between the conspecific and a heterospecific signal to avoid strong masking. Intracellular recordings of identified interneurons revealed two mechanisms providing response selectivity to the chirp (Kostarakos and R€ omer 2015). Several identified interneurons exhibit remarkably selective responses to the chirps, even at signalto-noise ratios of -21 dB, since they are sharply tuned to 2 kHz.…”