New insect auditory organ key to super-sensory hearing

A newly identified hearing organ in a South American bush cricket, which possesses one of the smallest ears known, shows insect hearing is so sophisticated that it rivals our own. The study, published in Science, is the first to identify a hearing mechanism in an insect that is evolutionarily convergent to those of mammals.

HFSP Cross-Disciplinary Fellow Fernando Montealegre-Z and colleagues
authored on Fri, 16 November 2012

Led by HFSP Cross-Disciplinary Fellow, Dr. Fernando Montealegre-Z,  together with scientists of the University of Bristol, new research shows how the bush cricket’s auditory system has evolved over millions of years to develop auditory mechanisms strikingly similar to those of humans, but using an entirely different apparatus. The research involved the bush cricket Copiphora gorgonensis, an endemic species from the National Natural Park Gorgona Island, located in the Colombian Pacific (Fig. 1). Results were corroborated in other neotropical bush cricket species.

Fig. 1. Female Copiphora gorgonensis (Insecta: Orthoptera: Tettigoniidae), a nocturnal bush cricket from the Colombian National Natural Park Gorgona Island, standing on a bromeliad leaf.

In mammals, hearing relies on three critical processing stages: an eardrum collecting sound, a middle ear impedance converter and a cochlear frequency analyzer.  The bush cricket’s ears, which are found on its two front legs (Fig. 2A), can perform all three stages, using ears that, despite being much smaller, work like those of humans but look very different.

Dr. Montealegre-Z conducted his HFSP fellowship with Prof. Daniel Robert at the University of Bristol, a leader in insect sensory systems. He studied the biophysics of sound propagation within the narrow tubing system, derived from the insect respiratory trachea, which conducts sound inside the bush cricket ear (Fig. 2B). Using micro-scanning laser Doppler vibrometry, he was measuring the amount and quality of acoustic energy that could escape from the tubes during the hearing process. In the process, he also noticed an unusual vibrational activity in the dorsal cuticle that lies between the animal’s eardrums, or tympanal membranes (Fig. 2F). It was considered “unusual” because this cuticle is hard and not as flexible as the tympana. Members of the team were surprised and therefore decided to scan the complete area with high resolution of laser points (>1500) and observed travelling waves throughout the cuticle. During these high resolution laser recordings Dr. Montealegre-Z also observed a small thick oval area vibrating in antiphase with the rest of the tympanum. At that point the team began to suspect that something special was happening below the thick cuticle, which causes vibrations to escape through a thick insect skin in the form of travelling waves. They decided to tackle the challenge using Micro-computed tomography (Micro-CT), another non-invasive technique. Dr. Montealegre-Z teamed up with Professor Kate Robson-Brown in the Department of Archaeology at the University of Bristol, who heads the Micro-CT facility, and produced high resolution X-ray scans of the bush cricket ears.  In this way, the complex internal anatomy of the bush cricket's ears was unveiled. This is one of the major achievements of the HFSP fellowship, because in the past exploring such micrometric ear structures required tedious work and invasive methods. The Micro-CT scanning facilitates 3D reconstructions of such small structure for further multi-physics computer modeling.

Dr. Montealegre-Z and his fellow researchers called this long-neglected organ an 'auditory vesicle' (Fig. 2D). The auditory vesicle works in tandem with the tympanic membranes and with mechanoreceptors (part of a structure known as the crista acustica). The integration of these auditory structures allows the animal to distinguish between a wide range of frequencies. 

By measuring nanoscale vibration using laser Doppler technology, Dr. Montealegre-Z and collaborators went on to show that this system works just like the cochlea of mammals, yet is about sixty times smaller. Impedance conversion is critical because it dictates that air vibrations are efficiently transmitted to the fluid-immersed mechanoreceptors. In the mammalian ear this is achieved by the ossicles, which transmit tympanal vibrations to the mechanoreceptors immersed in the cochlear fluid. Bush crickets use a miniaturized solution to the problem of impedance conversion, which relies on a system of a mechanical lever that makes the link to the insect inner ear. Impedance conversion is achieved by a tympanal plate (Fig. 2E) and mechanoreceptors are immersed in the fluid of the auditory vesicle (the newly identified organ) (Fig. 2G). This arrangement is not only advantageous as it guarantees that air vibrations are efficiently transmitted to the fluid, but also provides amplification.  As a crucial stage of auditory processing in mammals, such a process was unknown in insects and, in fact, was thought to be a unique attribute of the ears of vertebrates.

Simpler than the mammal ear, the bush cricket ear veils a complex process, which opens new possibilities of research on bio-inspired sensors, and new options for cochlear research. Some of the species currently studied by Dr. Montealegre-Z and colleagues communicate at frequencies as high as 150 kHz, which constitute the most ultrasonic love songs found in nature. The ears of these insects constitute complex promising biological sensors.

Fig. 2. Ear structure in Cophiphora gorgonensis (Tettigoniidae) studied with Micro-CT scanning technology. A: Head, thorax, and forelegs indicating the position of the tympanum on the legs, and acoustic spiracle. B: Transparency of the body showing the acoustic trachea backing the tympanum and connecting to the body side with the acoustic spiracle. C: Anatomy of the ear (spiracle, acoustic trachea and tympanum) after removing cuticle and muscular layers.  D: Close up view of the ear region encircled with the dashed line in A, showing a 3D Reconstruction of acoustic trachea and tympanum (blue). A strong constriction is observed between the auditory vesicle (yellow), and  the hemolymph (blood) channel (green). E: the acoustic trachea and tympana, auditory vesicle and hemolymph channel have been removed to expose the mechanoreceptors (also known as the crista acustica). F: Auditory Vesicle vibrations escaping through the leg cuticle. Areas in colour indicate vibration activity. G: Tympanal membrane vibration at 23 kHz as recorded with a Micro-scanning laser Doppler vibrometer. Note that the tympanic membrane and tympanal plate vibrate in anti-phase.

Reference

Convergent Evolution Between Insect and Mammalian Audition. Fernando Montealegre-Z., Thorin Jonsson, Kate A. Robson-Brown, & Daniel Robert. Science, Vol. 338 no. 6109 pp. 968-971, DOI: 10.1126/science.1225271.

Press release from University of Lincoln