5/21/2018 Directional Hearing & LDV

Daniel Robert

Abstract 1 - "The ears of a fly: Innovative biomechanics for directional hearing"

In most animals, the localization of sound constitutes a basic processing task of the auditory system. The directional detection of an incident sound wave relies on interaural amplitude and time differences and, in some cases, also on the spectral content of the signal. In small animals, the auditory receptors are forcibly set close together, a design constraint that imposes a very short interaural distance and that results in interaural time and amplitude cues (ITD and IID) that can become vanishingly small. Yet, some small animals are endowed with directional hearing, and are therefore very attractive study subjects because they constitute, in some sense, original biological solutions to some acute miniaturization problems.

One such small animal is a parasitoid fly that acoustically locates and attacks singing field crickets (1). This behavior is mediated by minute auditory organs that are separated from each other by only 520 µm (2). In such case, the largest ITDs and IIDs in the incident sound field (for 90° azimuth) are no larger than 2 µs and 1 dB, respectively.

The mechanical response of the tympanal membranes was measured by laser Doppler vibrometry (LDV). The mechanical response of the tympanal membranes has a pronounced directional sensitivity, in which ITD and IID in the mechanical response are significantly larger than those available in the acoustic field. At 5 kHz (6.8cm wavelength), the membrane closest to the sound source vibrates significantly more (3-6 dB), and earlier (50 µs), than the contralateral tympanal membrane. Deflection shape analysis at different frequencies reveals that the mechanical dynamics of both tympana is responsible for the observed asymmetrical response (Fig.1). Anatomically, these ears are particular in that they are physically connected by a cuticular bridge, the relative rigidity of which constitutes the key to the observed directional mechanical response (3). Hence, mechanical preprocessing increases minimal acoustic cues into more substantial mechanical cues that can be processed by the nervous system.

Ref. 3D-Video Page 1 RHW 5/21/2018 Directional Hearing & LDV

Fig.1. Mechanical response of the tympanal complex. The upper panel shows maximum outward deflection of the ipsilateral tympanal membrane (ipsi) at 5 kHz, while the lower panel depicts maximum inward deflection. Microscanning LDV was used to monitor vibration velocities at 364 tympanal locations. Coherence between acoustic input and mechanical response exceeded 0.95. The acoustic stimulus consisted in band limited random noise (1 to 30 kHz; 94 dB SPL) delivered at 90° azimuth. Supported by the Swiss National Science Foundation References: 1. Cade WH (1975) Science 190: 1312- 1313, 2. Robert D, Amoroso J, Hoy RR (1992) Science 258: 1135-1137. 3. Robert D, Miles RN, Hoy RR (1996) J. comp. Physiol. A 179: 29-44, Miles RN, Robert D, Hoy RR J (1995) Acoust Soc Am 98: 3059- 3070.

Abstract 2 - "Insect ears and principles of acoustic detection"

In technology, as in biology, the process of acoustic sensing involves, as a first step, the conversion of acoustic energy into mechanical energy. In insects, such conversion takes place in well-developed, yet small, auditory organs. In the course of evolution, insects have much diversified and such diversity is also reflected in structures and functions of their hearing organs (1). Ears can thus be found just about anywhere on the general insect body plan; on the legs, abdomen, thorax, chest, wings, mouthparts. Insects are however good at doing things small. Their ears can be thus regarded as miniaturized acoustic sensors that have, in an evolutionary sense, been proven sufficiently refined and efficient by the processes of natural and sexual selection. From this evolutionary vantage point, the resources embedded in the considerable diversity of insect auditory systems promise to be of significant inspirational value. Our investigations thus focus on questioning what are the information processing capacities of very small auditory organs, and what can be learned from it. The analysis has concentrated on peripheral auditory mechanisms in flies and mosquitoes.

One of the outcomes of this research has been to explore the possibility of transferring the some of the observed sound processing mechanisms to microphone technology. Using MEMs technology, early prototypes provide evidence that sensors inspired from the flies auditory organs are, despite their small size, directionally sensitive at about 5 kHz. Further optimization promises to provide the basis for subminiature microphones endowed with directionality in the range of human speech.

[Work supported by the Swiss National Science Foundation]. References: 1. Hoy RR, Robert D 1996 Tympanal hearing in insects. Ann Rev Entomol 41:433-450

Ref. 3D-Video Page 2 RHW 5/21/2018 Directional Hearing & LDV

Organs of sound reception in invertebrates > Types of insect auditory structures > Tympanal organs

The tympanal organ of insects consists of a group of scolophores associated with a thin, horny (chitinous) membrane at the surface of the body, one on each side. Usually the scolophores are attached at one end by a spinous process to the tympanic membrane (eardrum); the other ends rest on an immobile part of the body structure. When the membrane moves back and forth in response to the alternating pressures of sound waves, the nerve fibre from the ganglion cell of the scolophore transmits impulses to the central nervous system. Because the tympanic membrane is activated by the pressure of sound waves, this is a pressure type of ear.

Simple tympanal organs, such as those found in moths, contain only two or four elements, or scolophores. In cicadas, on the other hand, these organs are highly developed; they include a sensory body (a number of scolophores in a capsule) that may contain as many as 1,500 elements.

With 80 to 100 scolophores, the grasshopper ear, which has been studied more thoroughly than any other insect ear, is structurally between that of moths and cicadas. Ordinarily, the tympanic membrane is hidden beneath the base of the insect's wing cover. A bundle of auditory nerve fibres runs from one side of the sensory body, which lies on the inner surface of the membrane, and joins other nerve fibres of the region to form a large nerve extending to a ganglion (nerve centre) in the thorax.

Ref. 3D-Video Page 3 RHW