Understanding tympanal mechanics in insect ears

Insects have marvelous ears. Some insects, like mosquitoes, use antennae in front of their heads to detect sounds, mainly those of approaching females. Notably, our research has shown the ear of a mosquito is as sensitive to vibrations as the human ear and contains just as many vibration sensitive cells -16,000. Other insect, like crickets, locust and some rare flies use ears equipped with an eardrum, or tympanal membrane. The human ear also has an eardrum that serves to convert sound into motion. This motion is in turn transduced into the electrical signal that vibration sensitive cells then convey to the brain. Because sound-induced vibrations are very small, this process is extremely delicate. In insects, a similar process takes place, but with an ear that is sometimes 100 times smaller. Our research and that of others has shown that the eardrums of insects are sophisticated instruments that evolved for hundreds of millions of years to extract the faint sound energy and deliver it to the vibration sensitive cells. In particular we showed that in locusts the tympanum has at least one additional function: sorting the tone frequencies relevant to the life and survival of the animal. This is a form of mechanical information processing that takes place even before neuronal processing. Normal membrane vibrations are in the range of nanometers and take the shape of a traveling wave across the membrane surface area. We discovered that this wave is exquisitely timed, lasting 100 millionth of a second, strongly resembling a tsunami coming up to a shore. Interestingly, the propagation of this biological nanotsunami depends on the frequency of the sound that creates it, not its direction. The build up of the wave in effect provides the animal with the perception of tones. The work proposed aims at discovering the exact material properties and membrane architecture that allow for that wave to build up and generate directional frequency decomposition. We will use laser beams to monitor the vibrations, using the Doppler effect applied to light, to detect membrane motion with a resolution of the diameter of an atom of hydrogen. For the first time we will use focused ion beam milling to modify the geometry, tension and mass characteristics of the membranes and then explore the resulting vibrational behaviour. Ion beam milling uses an atomically thin jet of metal ions projected onto the object and can be used to either cut through objects, hard or soft, or add matter to that object. This technique has never been used to study micro and nanomechanics. Importantly, mathematical modeling will guide the search for mechanisms, by predicting the best way to alter the membrane to generate desired effects and thereby also delineating the key physical parameters, materials and architecture, that are sufficient and necessary for membrane function. Because we use three species of tympanate insects, we will be able to compare and contrast the results and adequacy of the approach. Why the membrane of the locust is vibrating one way, and that of the cricket another way, with different information coding properties, is still elusive. Using focused ion beams we will attempt to add or remove functions from the respective species, and understand what evolution by natural selection has achieved in the developing the tiny ears of insects. From the proposed research, we will also learn how to make better microphones, using in technology what we have observed in biology. This is especially useful when the goal is manufacture robust microphones a millimeter in size and less. Examples of application pertain to hearing aid microphones capable of on-board frequency and directional processing as well as subminiature microphone for electronic application with minimal power consumption.

The proposed work seeks a 1. Test the mechanical response and properties of the tympanal membranes of several Orthoptera insect species. 2. Produce for analytical purposes modifications of these membranes using innovative FIB technology, either by controlled accretion or deletion of material. 3. Generate predictive and structurally explicit models that will allow for the material and structural design of artificial smart sensor membranes. To achieve our objectives, the vibrational mechanics of insect tympana will be studied using a microscanning laser Doppler vibrometer (mLDV). Tympana will be examined by mLDV employing a destructive (removal of elements) and constructive (addition of elements) approach using focused ion beam (FIB) techniques. Physical models of the tympana will be constructed and tested in order to study the contribution of individual elements to the behaviour of the entire membrane. In addition, computer simulations of these membranes will be used to model and hence dissect the physics underlying membrane behaviour, leading the way to rational miniature acoustic sensor design. The interplay between modeling and experimentation will embody the systems biology approach of our research.

The research planned will have impact on scientific research beyond the field of hearing in insects. Whilst enhancing our knowledge of insect systems, the results are expected, as it has been the case for our past research, to have implications for our fundamental and mechanistic understanding of auditory function in general. The function that the structure of tympanal membranes plays in vibration conduction is still very much unknown, even for humans. Novel data indicates that information processing already takes place at that level, and that efficient acousto-mechanical transduction relies on subtle mechanical properties of tympanal membranes. Because the ears of animals surpass all technological devices known today in sensitivity, adaptability and robustness, it is important we learn more about how they work, how to make them, how to predict their behavior when they change/age, and how to repair them. Outside our own community of sensory research, two main sectors can be now identified as potential beneficiaries; sensor technology (ST) and ear nose and throat surgery (ENT). Sensor research has already benefited from our work (subminiature directional microphones; NIH, Sandia labs). The work proposed will have impact on how the membranes of microphones can be designed as to be smaller, more robust, more sensitive, and carry out some of the signal processing. A microphone 10 times smaller, less energy demanding and more sensitive is the target of such endeavour, massively improving the quality of acoustic and pressure micro-sensors with signal processing capabilities. Attractively, because the work proposed in this project includes the prototyping of plastic-based sensors, manufacturing could rely on cheap raw materials and existing production and packaging technology. Foreseeable beneficiaries in the in the high-tech manufacturing sector will be microphone and pressure sensors manufacturers, and hearing aid companies. The mechanisms planned to engage with this community are multiple, through articles in the relevant journals, and more efficiently by inviting visits and workshops to present the work done. This would only be done once advancement is sufficient. As done in the past, collaborations can be suggested, in the best form of a case-award. Medically, the replacement of the eardrum, or tympanoplasty is a usually restorative intervention that offers some durability. Our research on the importance of the fine structure of eardrums on their sound collecting capacity indicates that there is some knowledge to contribute to tympanal grafts. Although not in the plan, it our intention to explore with our colleagues in ENT (with whom we measure middle ear implants in situ, Dr. Nunez and Mr. Holland, and related biomedical engineering fims), what type of improvement a microstructured graft (natural tissue or plastic) could bring to auditory function. More such research can be anticipated to lead to the improvement of health in the UK, and pioneer novel medical technology. The PI's previous work has led to the development and patenting of directional silicon-based microphones. This development has proved useful in human health applications (in ear hearing aids, blind location devices). It also prompted developments in surveillance technology (sound triggered superdirectional cameras). However, the PI's experience of these cases shows that the development time can be very long (10 years). Another aspect of importance is the continuation of collaborations that we have been developing with the Indian Institute of Science in Bangalore, India. This collaboration was enabled by the award of UK-India Education and Research Initiative grant (British Council). The recent award of a Marie Curie Research Fellowship to Dr. Natasha Mhatre is a direct result from the UKIERI activity. The impact here will be to continue developing the links to India, with insider knowledge, and recruit students and research fellows.