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The Insect cochlea: a non-invasive path towards enhanced sound detectors

Periodic Reporting for period 3 - The insect cochlea (The Insect cochlea: a non-invasive path towards enhanced sound detectors)

Reporting period: 2021-05-01 to 2022-10-31

There is ongoing interest in developing biomimetic acoustic sensors inspired by the hearing mechanisms evolved by animals. Potential applications of such devices include frequency spectrum analysers inspired by the human cochlea and acoustic triangulation mimicking the hyper-accurate ears of parasitic flies. However, dissecting an animal ear is challenging, requiring invasive protocols that compromise the natural function of the system. A non-invasive experimental protocol for characterising these processes will break the challenge of producing cochlea-inspired sensors. Remarkably, cochlear processes are not unique to mammals, as a similar mechanism for frequency analysis has been found in the ears of bush-crickets. Bush-cricket ears share the three basic steps of hearing observed in mammals: 1) sound capture, 2) impedance conversion, and 3) frequency analysis. In other words, bush-crickets have outer, middle, and inner ear components. Female bush-crickets must listen for both singing males and predatory bats. Bush-crickets and crickets are too small to have ears in the head (as in vertebrates) at a sufficient distance apart. Instead, they have evolved an ear in each foreleg, allowing for optimal separation for binaural computation. Interestingly, each ear is equipped with two tympanic membranes (only one in humans) and the two tympana receive sound both externally and internally via an ear canal derived from the respiratory tracheal system [Fig. 1B]. Bush-crickets therefore have two acoustic inputs to each ear (one per ear in humans). In other words, the two ears triangulate a sound signal using four separate acoustic inputs [Figs. 2, 3]. These sounds converge onto a complex organ of tonotopically organised sensory cells, with broadband frequency sensitivity like the mammalian cochlea, though the insect “cochlea” is uncoiled [Figs. 2, 3B]. This linear arrangement allows non-invasive measurement in some species that exhibit transparent body cuticle. This permits inner ear visualisation through the cuticle without the need to dissect it; something impossible to achieve in the mammalian cochlea. Using a highly interdisciplinary approach, this project aims to create a new platform of knowledge that will form the basis for a new generation of acoustic sensors.
So far, we measured real-time ear responses to sound using Laser Doppler vibrometry (LDV), and the material properties of the ear canal using atomic force microscopy (AFM) and micro- and nano-CT [Figs. 3, 4]. This information fed into mathematical models using true 3D geometries of the bush-cricket ear. Eight species of bush-cricket, one grig and one field cricket have been analysed so far, with some being chosen because they have transparent cuticles allowing non-invasive access to the inner ear. During selection we discovered Speculophlugis hishquten; a new genus of highly transparent predatory bush-cricket named after the alien from the Predator films [Fig. 1A]. Focusing on the outer ear, we showed that the narrowing ear canal [Fig. 3C] works as an acoustic horn that passively amplifies sound by several decibels (15-18 dB). However, the most important role of this acoustic path is in reducing sound velocity by nearly 20% relative to sound acting through the air on the external surfaces of the tympana, which enables bush-crickets to have two versions of the same signal separated by fractions of milliseconds. The ear canal is also bifurcated in each leg, with asymmetrical anterior and posterior branches of different diameters feeding on to the two tympanal membranes. Sound therefore travels faster inside one ear canal division than in the other [Fig. 4D], allowing bush-crickets to triangulate a sound source in the dark. Our non-invasive experiments of the inner ear using LDV through transparent cuticles show that the ‘insect cochlea’ functions in a similar way to mammals. During dual stimulation of the ear with two acoustic tones, the ear produces phantom tones – believed to be a side product of over-amplification of the system. As hypothesized for the mammalian cochlea, we have been able to directly prove that these tones are generated at the site of frequency discrimination, and that their amplitude is dependent on location, and the physiological state of the system. This may hold clues about the high sensitivity of these ears, as it would mean less energy is lost by the process of reverse transduction once it enters the ear.
Engineering: We seek to measure the material properties of tympanic membranes and the fine structures of the inner ear (tectorial membrane, mechanosensory cells). We are building a database for nanoscale mechanical data from these biological materials. We have developed a novel method to quantify the properties of ear canal using AFM. Our progress will allow cross-disciplinary developments in fields of biomaterials, synthetic biology and tissue engineering, with strong impact in the field of biomedical engineering.

Structural biology: Ear structure is being measured using micro- and nano-CT, and surface scanning microscopy to produce high-resolution 3D geometries. We have already discovered fine structures of the inner ear. We have expertise in cloning and histology, enabling us to tease apart the molecular nature of the hearing organ, including the function and location of mechanosensory proteins using confocal microscopy and Raman spectroscopy.

Neurosciences: We will fill the auditory nerve with harmless dyes that spread to the sensilla of the inner ear, and glow when the ear hears sound. The auditory sensilla are tonotopically arranged on the inner ear surface, and we will visualize the real-time activity of these neurons in response to sound by imaging through the transparent cuticles of our in-house bush-cricket species.

Biophysics: We use LDV to non-destructively measure auditory processes of the tympanic membrane and inner ear. The ERC grant paid for a unique set of three laser vibrometers that can measure the simultaneous vibrations in the outer and inner ear components of a single ear, or between left and right ears. With a novel experimental arena, we are measuring various processes of the inner ear including frequency analysis, active amplification, the formation of travelling waves, and in combination with state-of-the-art imaging techniques mentioned above, we hope to image the motility of the cilia.

Mathematics: Finally, using our 3D geometries alongside our other data, we will produce numerical models of each hearing step to facilitate our understanding of how such a small hearing system operates in a similar way to that of mammals. These models will aid the prediction of processes that we are not able to see, including origin of travelling waves, broadband sensitivity, and acoustic triangulation; the information needed to develop miniaturized acoustic sensors.
Fig. 3. 3D reconstruction of the ear canal in Copiphora gorgonensis, simulation of sound propagation