Cues for Directional Hearing in the Fly Ormia ochracea

Andrew C Mason

doi:10.3389/fevo.2021.679064

Abstract

Insects are often small relative to the wavelengths of sounds they need to localize, which presents a fundamental biophysical problem. Understanding novel solutions to this limitation can provide insights for biomimetic technologies. Such an approach has been successful using the fly Ormia ochracea (Diptera: Tachinidae) as a model. O. ochracea is a parasitoid species whose larvae develop as internal parasites within crickets (Gryllidae). In nature, female flies find singing male crickets by phonotaxis, despite severe constraints on directional hearing due to their small size. A physical coupling between the two tympanal membranes allows the flies to obtain information about sound source direction with high accuracy because it generates interaural time-differences (ITD) and interaural level differences (ILD) in tympanal vibrations that are exaggerated relative to the small arrival-time difference at the two ears, that is the only cue available in the sound stimulus. In this study, I demonstrate that pure time-differences in the neural responses to sound stimuli are sufficient for auditory directionality in O. ochracea.

Highlights

The fly Ormia ochracea (Diptera:Tachinidae) possesses an auditory system that performs analagous functions to those of vertebrate hearing, albeit for a restricted range of stimuli (Gray et al, 2007)
I conducted a set of experiments (1–3) aimed a manipulating neural interaural time differences (nITD) and neural interaural level differences (nILD) separately, to address the question of how much each of these response parameters contributes to the coding of auditory directionality
Previous studies (Oshinsky and Hoy, 2002) have suggested that these nILDs could contribute to the coding of sound source direction, with some data suggesting that nILDs provide more accurate directional information than nITDs (Pollack and Mason, 2014)

Summary

INTRODUCTION

The fly Ormia ochracea (Diptera:Tachinidae) possesses an auditory system that performs analagous functions to those of vertebrate hearing (detection, recognition, segregation, and localization or sources), albeit for a restricted range of stimuli (Gray et al, 2007). Mechanical coupling of the two eardrums amplifies the small direction-dependent ITDs in the sound field, and generates ILDs in the tympanal vibration responses, so that both cues are present in the tympanal (Robert et al, 1996b) and neural responses (Mason et al, 2001; Oshinsky and Hoy, 2002). The majority of auditory receptors associated with each ear respond with tonic bursts at the onset of sound pulses (Oshinsky and Hoy, 2002) with response latencies that are dependent on tympanal vibration level, such that tILDs result in directiondependent interaural latency differences in receptor responses These neural interaural time differences (nITD) scale with the azimuth of the sound source location (Mason et al, 2001; Figure 2). As in vertebrate hearing, ITDs and ILDs may both contribute to directional hearing in Ormia ochracea, the way these cues are combined in fly directional hearing is not fully resolved

MATERIALS AND METHODS

RESULTS

DISCUSSION