Final Report Summary - INSECT EARS (The tympanal ears of insects: structural solutions to acoustic signal analysis)
The primary research goal of this project is to foster a deeper understanding of insect tympanal ears using field crickets, tree crickets and locusts as model systems. The aim is to understand signal processing in microscale auditory systems, and characterise the microarchitecture and structural properties of their eardrums. The principal approach used to garner this understanding is to use state of the art experimentation and biophysical mathematical models.
To pursue these research objectives we have used several experimental and modelling approaches. The principal technique used to examine the behaviour of these membranes is the extremely high sensitivity and spatial resolution laser Doppler vibrometry (LDV). In complement to several other imaging techniques, such as focused ion beam (FIB) milling, confocal microscopy and micro-computed (micro-CT) tomography, vibrometry allows us to understand the functional architecture of these tympanal membranes and associated structures. Finally, the insights derived from these techniques are synthesised into models with unprecedented space and time resolution and predictive power, using a modelling technique known as finite element modelling (FEM) using the software COMSOL Multiphysics. The main results are as follows:
Membrane architecture determines tympanal orthotropy in tree crickets: The vibration behaviour of tree cricket tympanal membrane is found to be distinct from that of other tympanal membranes. The membranes behave asymmetrically and their displacement is remarkably concentrated at the position of neuronal attachment. This behaviour is unlike field crickets where the membrane behaves like a conventional drum and does not appear to concentrate displacement. We have found using both FIB sectioning micro-CT that the eardrum of tree crickets possess asymmetric corrugations. Using FEM emulating the observed histoarchitecture, we are able to recreate this behaviour and establishing that it is the corrugations that create a membrane that is stiffer in one direction compared to the other and hence create the energy localising asymmetric vibration pattern. This apparently simple microscale eardrum is therefore more sophisticated than previously surmised. The same methods allow us to conclude that membrane architecture, however, is not sufficient to explain other features of this membrane, in particular its frequency response and directionality.
Architecture dependent tympanal tonotopy in locust membranes: Like in tree crickets, the vibrational behaviour of locust tympanal membrane differs from a field cricket membrane. The ears of these insects are not only able to localise membrane displacement to neuronal attachment points, but also are able to do so in a frequency dependent manner. Using FIB, we were able to ascertain unexpected and unknown membrane histoarchitecture. The locust membrane was found to exhibit a complex composite structure, with a steep concentric thickness gradient and a remarkable previously unknown membrane-liquid interface at the centre of the membrane, embedded within the membrane structure. FEM allowed us to prove that a combination of three important features, e.g. the concentric histoarchitecture, tension-dominated biophysics and the liquid-solid interface together work in concert to produce both displacement localisation and frequency discrimination. Importantly, these behaviours can be reproduced in a physical membrane analogue that incorporates these features, opening up the path to the construction of miniature frequency-selective microphones.
Active mechanics in tympanal ears: An unexpected and exciting discovery was made investigating the basis of directionality and frequency response in the tree cricket tympanum. The ears of humans incorporate a mechanism called cochlear amplification in which the sensory hair cells expend energy to enhance the mechanical oscillations of the auditory system, thus amplifying incoming sounds. We have found that this very unique and sophisticated mechanism is present even in the ears of tree crickets, amongst the oldest known ears of animal. Not only do tree crickets use active auditory mechanics, they also exhibit functionalities unknown from other active systems. For instance, the active system can be turned on and off, it copes with temperature changes by changing the frequencies it amplifies and it works to suppress low frequency noise.
In fact, this unexpected and unforeseen result, not part of initial project planning, has impact in terms of societal impact and health and wealth. Finding active mechanics in an ancient insect ear suggests that the active amplification may be extremely widespread amongst insects and arthropods. This is significant in environmental terms because active hearing is a delicate physiological mechanosensory mechanism that is extremely vulnerable to excessive sound levels (acoustic pollution), climatic change (temperature shifts) and chemical damage (ototoxocity).
Outcomes and impact of research: Our finding suggests that disruptions to vast insect communication networks by such anthropogenic insults maybe going undetected causing unknown damage to the ecosystems these insects participate in. More generally, the toxicological vulnerability of insect mechanosensory systems is largely unknown; ecologically and economically important insects such as pollinators (bees, flies, beetles, moths) are susceptible to disruptions of their sensory systems. Resulting alterations or vanishing of their orientation and feeding behaviours could lead to significant loss of ecological services and agricultural crop yields. As such, the outcomes of this research impact on fundamental neurobiological science, ecology and environmental protection.
To pursue these research objectives we have used several experimental and modelling approaches. The principal technique used to examine the behaviour of these membranes is the extremely high sensitivity and spatial resolution laser Doppler vibrometry (LDV). In complement to several other imaging techniques, such as focused ion beam (FIB) milling, confocal microscopy and micro-computed (micro-CT) tomography, vibrometry allows us to understand the functional architecture of these tympanal membranes and associated structures. Finally, the insights derived from these techniques are synthesised into models with unprecedented space and time resolution and predictive power, using a modelling technique known as finite element modelling (FEM) using the software COMSOL Multiphysics. The main results are as follows:
Membrane architecture determines tympanal orthotropy in tree crickets: The vibration behaviour of tree cricket tympanal membrane is found to be distinct from that of other tympanal membranes. The membranes behave asymmetrically and their displacement is remarkably concentrated at the position of neuronal attachment. This behaviour is unlike field crickets where the membrane behaves like a conventional drum and does not appear to concentrate displacement. We have found using both FIB sectioning micro-CT that the eardrum of tree crickets possess asymmetric corrugations. Using FEM emulating the observed histoarchitecture, we are able to recreate this behaviour and establishing that it is the corrugations that create a membrane that is stiffer in one direction compared to the other and hence create the energy localising asymmetric vibration pattern. This apparently simple microscale eardrum is therefore more sophisticated than previously surmised. The same methods allow us to conclude that membrane architecture, however, is not sufficient to explain other features of this membrane, in particular its frequency response and directionality.
Architecture dependent tympanal tonotopy in locust membranes: Like in tree crickets, the vibrational behaviour of locust tympanal membrane differs from a field cricket membrane. The ears of these insects are not only able to localise membrane displacement to neuronal attachment points, but also are able to do so in a frequency dependent manner. Using FIB, we were able to ascertain unexpected and unknown membrane histoarchitecture. The locust membrane was found to exhibit a complex composite structure, with a steep concentric thickness gradient and a remarkable previously unknown membrane-liquid interface at the centre of the membrane, embedded within the membrane structure. FEM allowed us to prove that a combination of three important features, e.g. the concentric histoarchitecture, tension-dominated biophysics and the liquid-solid interface together work in concert to produce both displacement localisation and frequency discrimination. Importantly, these behaviours can be reproduced in a physical membrane analogue that incorporates these features, opening up the path to the construction of miniature frequency-selective microphones.
Active mechanics in tympanal ears: An unexpected and exciting discovery was made investigating the basis of directionality and frequency response in the tree cricket tympanum. The ears of humans incorporate a mechanism called cochlear amplification in which the sensory hair cells expend energy to enhance the mechanical oscillations of the auditory system, thus amplifying incoming sounds. We have found that this very unique and sophisticated mechanism is present even in the ears of tree crickets, amongst the oldest known ears of animal. Not only do tree crickets use active auditory mechanics, they also exhibit functionalities unknown from other active systems. For instance, the active system can be turned on and off, it copes with temperature changes by changing the frequencies it amplifies and it works to suppress low frequency noise.
In fact, this unexpected and unforeseen result, not part of initial project planning, has impact in terms of societal impact and health and wealth. Finding active mechanics in an ancient insect ear suggests that the active amplification may be extremely widespread amongst insects and arthropods. This is significant in environmental terms because active hearing is a delicate physiological mechanosensory mechanism that is extremely vulnerable to excessive sound levels (acoustic pollution), climatic change (temperature shifts) and chemical damage (ototoxocity).
Outcomes and impact of research: Our finding suggests that disruptions to vast insect communication networks by such anthropogenic insults maybe going undetected causing unknown damage to the ecosystems these insects participate in. More generally, the toxicological vulnerability of insect mechanosensory systems is largely unknown; ecologically and economically important insects such as pollinators (bees, flies, beetles, moths) are susceptible to disruptions of their sensory systems. Resulting alterations or vanishing of their orientation and feeding behaviours could lead to significant loss of ecological services and agricultural crop yields. As such, the outcomes of this research impact on fundamental neurobiological science, ecology and environmental protection.