Tympanal Membrane Research Articles

Listening to the environment: hearing differences from an epigenetic effect in solitarious and gregarious locusts.

Locusts display a striking form of phenotypic plasticity, developing into either a lone-living solitarious phase or a swarming gregarious phase depending on population density. The two phases differ extensively in appearance, behaviour and physiology. We found that solitarious and gregarious locusts have clear differences in their hearing, both in their tympanal and neuronal responses. We identified significant differences in the shape of the tympana that may be responsible for the variations in hearing between locust phases. We measured the nanometre mechanical responses of the ear's tympanal membrane to sound, finding that solitarious animals exhibit greater displacement. Finally, neural experiments signified that solitarious locusts have a relatively stronger response to high frequencies. The enhanced response to high-frequency sounds in the nocturnally flying solitarious locusts suggests greater investment in detecting the ultrasonic echolocation calls of bats, to which they are more vulnerable than diurnally active gregarious locusts. This study highlights the importance of epigenetic effects set forth during development and begins to identify how animals are equipped to match their immediate environmental needs.

Hearing in the crepuscular owl butterfly (Caligo eurilochus, Nymphalidae).

Tympanal organs are widespread in Nymphalidae butterflies, with a great deal of variability in the morphology of these ears. How this variation reflects differences in hearing physiology is not currently understood. This study provides the first examination of hearing organs in the crepuscular owl butterfly, Caligo eurilochus. We examined the tuning and sensitivity of the C. eurilochus hearing organ, called Vogel's organ, using laser Doppler vibrometry and extracellular neurophysiology. We show that the C. eurilochus ear responds to sound and is most sensitive to frequencies between 1 and 4 kHz, as confirmed by both the vibration of the tympanal membrane and the physiological response of the associated nerve branches. In comparison to the hearing of its diurnally active relative, Morpho peleides, C. eurilochus has a narrower frequency range with higher auditory thresholds. Hypotheses explaining the function of hearing in this crepuscular butterfly are discussed.

Temperature effects on the tympanal membrane and auditory receptor neurons in the locust.

Poikilothermic animals are affected by variations in environmental temperature, as the basic properties of nerve cells and muscles are altered. Nevertheless, insect sensory systems, such as the auditory system, need to function effectively over a wide range of temperatures, as sudden changes of up to 10 °C or more are common. We investigated the performance of auditory receptor neurons and properties of the tympanal membrane of Locusta migratoria in response to temperature changes. Intracellular recordings of receptors at two temperatures (21 and 28 °C) revealed a moderate increase in spike rate with a mean Q10 of 1.4. With rising temperature, the spike rate–intensity–functions exhibited small decreases in thresholds and expansions of the dynamic range, while spike durations decreased. Tympanal membrane displacement, investigated using microscanning laser vibrometry, exhibited a small temperature effect, with a Q10 of 1.2. These findings suggest that locusts are affected by shifts in temperature at the periphery of the auditory pathway, but the effects on spike rate, sensitivity, and tympanal membrane displacement are small. Robust encoding of acoustic signals by only slightly temperature-dependent receptor neurons and almost temperature-independent tympanal membrane properties might enable locusts and grasshoppers to reliably identify sounds in spite of changes of their body temperature.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-014-0926-y) contains supplementary material, which is available to authorized users.

Mechanical tuning of the moth ear: distortion-product otoacoustic emissions and tympanal vibrations

The mechanical tuning of the ear in the moth Empyreuma pugione was investigated by distortion-product otoacoustic emissions (DPOAE) and laser Doppler vibrometry (LDV). DPOAE audiograms were assessed using a novel protocol that may be advantageous for non-invasive auditory studies in insects. To evoke DPOAE, two-tone stimuli within frequency and level ranges that generated a large matrix of values (960 frequency-level combinations) were used to examine the acoustic space in which the moth tympanum shows its best mechanical and acoustical responses. The DPOAE tuning curve derived from the response matrix resembles that obtained previously by electrophysiology, and is V-shaped and tuned to frequencies between 25 and 45 kHz with low Q10dB values of 1.21±0.26. In addition, while using a comparable stimulation regime, mechanical distortion in the displacement of the moth's tympanal membrane at the stigma was recorded with a laser Doppler vibrometer. The corresponding mechanical vibration audiograms were compared with DPOAE audiograms. Both types of audiograms have comparable shape, but most of the mechanical response fields are shifted towards lower frequencies. We showed for the first time in moths that DPOAE have a pronounced analogy in the vibration of the tympanic membrane where they may originate. Our work supports previous studies that point to the stigma (and the internally associated transduction machinery) as an important place of sound amplification in the moth ear, but also suggests a complex mechanical role for the rest of the transparent zone.

Discovery of a lipid synthesising organ in the auditory system of an insect.

Weta possess typical Ensifera ears. Each ear comprises three functional parts: two equally sized tympanal membranes, an underlying system of modified tracheal chambers, and the auditory sensory organ, the crista acustica. This organ sits within an enclosed fluid-filled channel–previously presumed to be hemolymph. The role this channel plays in insect hearing is unknown. We discovered that the fluid within the channel is not actually hemolymph, but a medium composed principally of lipid from a new class. Three-dimensional imaging of this lipid channel revealed a previously undescribed tissue structure within the channel, which we refer to as the olivarius organ. Investigations into the function of the olivarius reveal de novo lipid synthesis indicating that it is producing these lipids in situ from acetate. The auditory role of this lipid channel was investigated using Laser Doppler vibrometry of the tympanal membrane, which shows that the displacement of the membrane is significantly increased when the lipid is removed from the auditory system. Neural sensitivity of the system, however, decreased upon removal of the lipid–a surprising result considering that in a typical auditory system both the mechanical and auditory sensitivity are positively correlated. These two results coupled with 3D modelling of the auditory system lead us to hypothesize a model for weta audition, relying strongly on the presence of the lipid channel. This is the first instance of lipids being associated with an auditory system outside of the Odentocete cetaceans, demonstrating convergence for the use of lipids in hearing.

파리의 청각 구조를 이용한 음원 방향 검지용 센서 설계

The technique for estimation of sound source direction is one of the important methods necessary for various engineering fields such as monitoring system, military services and so on. As a new approach for estimation of sound source direction, this paper propose the bio-mimetic localization sensor based on mechanically coupling structure motivated by hearing structure of fly, Ormia Ochracea. This creature is known for its outstanding recognition ability to the sound which has large wavelength compared to its own size. ITTF (Inter-Tympanal Transfer Function) which is the transfer function between displacements of the tympanal membranes on each side has the all inter-tympanal information dependent on sound direction. The peak and notch features of desired ITTF can be generated by using the appropriate mechanical properties. A example of estimation of sound source direction using generated ITTF with monotonically changing notch and peak patterns is shown.

How temperature affects locust hearing

Event Abstract Back to Event How temperature affects locust hearing Monika J. Eberhard1*, Shira D. Gordon2, James Windmill2 and Bernhard Ronacher1 1 Humboldt-Universität zu Berlin, Department of Biology, Germany 2 University of Strathclyde, Department of Electronic and Electrical Engineering, United Kingdom Poikilothermic (ectothermic) animals are affected by variations in environmental temperature, as their body temperature fluctuates with ambient conditions. Their sensory systems need to function effectively over a wide range of temperatures as sudden environmental changes of up to 10°C or more are not uncommon. For species and mate recognition, many acoustically communicating insects rely on decoding the temporal characteristics of conspecific calls. Temperature will affect both sender and receiver of acoustic signals by influencing basic properties such as spike rate, conduction velocity, and spike amplitude of neurons and muscle cells. Thus, the ability to cope with changes in temperature is crucial for mate finding in those species. In the present study we investigate the performance of auditory receptor neurons and the tympanal membrane of Locusta migratoria in relation to temperature changes. In locusts, the tympanal membrane is located laterally on the first abdominal segment. Receptor neurons are attached to the tympanal membrane and, via their axons, deliver afferent signals to the metathoracic ganglion. There the first processing steps take place before further transmission to the brain. We recorded intracellularly from receptor neurons within the metathoracic ganglion; each receptor was recorded at 20°C and 30°C. From the recordings, spike rate vs. intensity curves were obtained and temperature coefficients (Q10) were determined. Additionally, the movement of the tympanal membrane was monitored at 6 representative locations, also at 20°C and 30°C, using a Laser-Doppler-vibrometer. Remarkably, a 10°C change in temperature had little effect on the receptor’s spike rate. The spike frequency changes corresponded to a Q10 of only 1.24, which is much lower than the expected value of ~2, as typical for various metabolic and physiological rates. We then tested whether the movement of the tympanal membrane could account for the increase in spike rate with rising temperature. We found a significantly enhanced movement in the hotter condition. Amplitude of the tympanal membrane exhibited a similar variation with changing temperatures as receptor spike rate, with a mean Q10 of 1.22. We conclude that temperature changes have only little effect on the spike rates of locust receptor neurons. As spike rate depends on the movement of the tympanum, its rise is at least to some extent caused by the increased movement of the tympanal membrane at higher temperature. The Q10 values of spike rate and tympanal membrane movement are similar, suggesting that locusts are affected by temperature changes already at the very periphery of the auditory pathway. Robust encoding of acoustic signals by almost temperature independent receptor neurons might enable the locusts to reliably identify sounds (e.g. approaching predators) in spite of changes of their body temperature. Acknowledgements Supported by DFG (SFB 618) Keywords: Locust, receptor neurons, temperature, tympanal membrane Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012. Presentation Type: Poster (but consider for student poster award) Topic: Sensory: Audition Citation: Eberhard MJ, Gordon SD, Windmill J and Ronacher B (2012). How temperature affects locust hearing. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00111 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 25 Apr 2012; Published Online: 07 Jul 2012. * Correspondence: Dr. Monika J Eberhard, Humboldt-Universität zu Berlin, Department of Biology, Berlin, 10115, Germany, monika.eberhard@biologie.hu-berlin.de Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Monika J Eberhard Shira D Gordon James Windmill Bernhard Ronacher Google Monika J Eberhard Shira D Gordon James Windmill Bernhard Ronacher Google Scholar Monika J Eberhard Shira D Gordon James Windmill Bernhard Ronacher PubMed Monika J Eberhard Shira D Gordon James Windmill Bernhard Ronacher Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Low pass filters and differential tympanal tuning in a paleotropical bushcricket with an unusually low frequency call

Low-frequency sounds are advantageous for long-range acoustic signal transmission, but for small animals they constitute a challenge for signal detection and localization. The efficient detection of sound in insects is enhanced by mechanical resonance either in the tracheal or tympanal system before subsequent neuronal amplification. Making small structures resonant at low sound frequencies poses challenges for insects and has not been adequately studied. Similarly, detecting the direction of long-wavelength sound using interaural signal amplitude and/or phase differences is difficult for small animals. Pseudophylline bushcrickets predominantly call at high, often ultrasonic frequencies, but a few paleotropical species use lower frequencies. We investigated the mechanical frequency tuning of the tympana of one such species, Onomarchus uninotatus, a large bushcricket that produces a narrow bandwidth call at an unusually low carrier frequency of 3.2 kHz. Onomarchus uninotatus, like most bushcrickets, has two large tympanal membranes on each fore-tibia. We found that both these membranes vibrate like hinged flaps anchored at the dorsal wall and do not show higher modes of vibration in the frequency range investigated (1.5-20 kHz). The anterior tympanal membrane acts as a low-pass filter, attenuating sounds at frequencies above 3.5 kHz, in contrast to the high-pass filter characteristic of other bushcricket tympana. Responses to higher frequencies are partitioned to the posterior tympanal membrane, which shows maximal sensitivity at several broad frequency ranges, peaking at 3.1, 7.4 and 14.4 kHz. This partitioning between the two tympanal membranes constitutes an unusual feature of peripheral auditory processing in insects. The complex tracheal shape of O. uninotatus also deviates from the known tube or horn shapes associated with simple band-pass or high-pass amplification of tracheal input to the tympana. Interestingly, while the anterior tympanal membrane shows directional sensitivity at conspecific call frequencies, the posterior tympanal membrane is not directional at conspecific frequencies and instead shows directionality at higher frequencies.

Hearing differences of gregarious and solitary locusts (Schistocerca gregaria), an example of epigenetic effects

Hearing differences of gregarious and solitary locusts (Schistocerca gregaria), an example of epigenetic effects

Modelling locust tympanal systems: understanding the link between biomechanics and neurophysiology

Modelling locust tympanal systems: understanding the link between biomechanics and neurophysiology

Ultra high frequency hearing in a moth

Ultra high frequency hearing in a moth

Sound-induced tympanal membrane motion in bushcrickets and its relationship to sensory output

In the auditory system of bushcrickets, sound can reach the receptors via two different paths: (i) by acting on the outside of the tympana situated on both sides of each foreleg or (ii) through the acoustic trachea that opens at a spiracle on the thorax. While the spiracle is considered to be the main point of sound entry for higher audio and ultrasonic frequencies, the role of the tympana is still unclear. The tympana border the air-filled acoustic trachea as well as the fluid-filled haemolymph channel containing the receptor organs. To understand their role during sound transduction, the sound-induced neuronal response of the hearing organ was recorded in combination with measurement of tympanal membrane motion using laser-Doppler vibrometry. For far-field stimulation, the frequency of the most sensitive hearing (∼16 kHz) matched the frequency of a pronounced maximum of tympanal membrane vibration. A second maximum of tympanum motion at lower frequencies (∼7 kHz) was correlated with an increased nerve activity at higher intensities (>70 dB sound pressure level, SPL). These correlations support the hypothesis of functional coupling between tympanum motion and nerve activity. When sound stimuli were applied locally, through either the tympanum or the spiracle, significant differences between tympanum motion and nerve activity were found. These discrepancies show that tympanum motion and neuronal response are not coupled directly and that there is no linear relationship with the applied SPL. Taken together, these data verify a functional, albeit indirect, coupling of tympanum motion and sensory cell activity for one of the pronounced vibration maxima, which appears to represent a resonance frequency of the tympanum.

No evidence for DPOAEs in the mechanical motion of the locust tympanum

Distortion-product otoacoustic emissions (DPOAEs) are present in non-linear hearing organs, and for low-intensity sounds are a by-product of active processes. In vertebrate ears they are considered to be due to hair cell amplification of sound in the cochlea; however, certain animals lacking a cochlea and hair cells are also reported to be capable of DPOAEs. In the Insecta, DPOAEs have been recorded from the locust auditory organ. However, the site of generation of these DPOAEs and the physiological mechanisms causing their presence in the locust ear are not yet understood, despite there being a number of potential places in the tympanal organ that could be capable of generating DPOAEs. This study aimed to record locust tympanal membrane vibration using a laser Doppler vibrometer in order to identify a distinct place of DPOAE generation on the membrane. Two species of locust were investigated over a range of frequencies and levels of acoustic stimulus, mirroring earlier acoustic recording studies; however, the current experiments were carried out in an open acoustic system. The laser measurements did not find any evidence of mechanical motion on the tympanal membrane related to the expected DPOAE frequencies. The results of the current study therefore could not confirm the presence of DPOAEs in the locust ear through the mechanics of the tympanal membrane. Experiments were also carried out to test how membrane behaviour altered when the animals were in a state of hypoxia, as this was previously found to decrease DPOAE magnitude, suggesting a metabolic sensitivity. However, hypoxia did not have any significant effect on the membrane mechanics. The location of the mechanical generation of DPOAEs in the locust's ear, and therefore the basis for the related physiological mechanisms, thus remains unknown.

Mechanical filtering for narrow-band hearing in the weta

This paper constitutes a major attempt to associate tympanic deflections with the mechanoreceptor organ location in an acoustic insect. The New Zealand tree weta (Hemideina thoracica) has tympanal ears located on each of the prothoracic tibiae. The tympana exhibit a sclerotized oval plate, membranous processes bulging out from the tibial cuticle and many loosely suspended ripples. We used microscanning laser Doppler vibrometry to determine how such a tympanal membrane vibrates in response to sound and whether the sclerotized region plays a role in hearing. The tympanum displays a single resonance at the calling frequency of the male, an unusual example of an insect tympana acting as a narrow bandpass filter. Both tympana resonate in phase with the stimulus and with each other. Histological sections show that the tympanal area is divided into two distinct regions, as in other ensiferans. An oval plate lies in the middle of a thickened region and is surrounded by a transparent and uniformly thin region. It is hinged dorsally to the tympanal rim and thus resembles the model of a 'hinged flap'. The thickened region appears to act as a damping mass on the oscillation of the thin region, and vibration displacement is reduced in this area. The thinner area vibrates with higher amplitude, inducing mechanical pressure on the dorsal area adjacent to the crista acustica. We present a new model showing how the thickened region might confer a mechanical gain onto the activation of the crista acustica sensory neurons during the sound-induced oscillations.

Cicada ear geometry: species and sex effects

Many insect species rely on their sense of audition to find a mate, to localize prey or to escape from a predator. Cicadas are particularly known for their loud call and the conspicuous tympanal hearing system located in their abdomen. The vibration pattern of the tympanal membrane (TM) has been investigated recently revealing mechanical properties specific to species and sex. Although TM size and shape is likely to affect these patterns, the geometry of the cicada ear has never been examined per se. Focusing on three Mediterranean cicada species, namely Cicadatra atra, Cicada orni and Lyristes plebejus, we investigated the structure of TM shape variation at two levels, within and across species. Applying an elliptic Fourier analysis to the outlines of both male and female TMs, we estimated sexual dimorphism and species effects. Cicadatra atra showed a large TM compared with its small size, probably as a result of selective constraints related to the role of the TM in sound production. Sexual dimorphism seemed to be greater than interspecific variation, indicating that constraints operating on sex might be more selective than those acting on species identification. In addition, C. orni appeared to be significantly different from the two other species. This morphological peculiarity could be related to the unique vibrational pattern of its membrane. This would establish for the first time a direct link between the shape and mechanism of a hearing organ.

Sound emission and reception tuning in three cicada species sharing the same habitat

Many animal species acoustically communicate at the same place and time generating complex acoustic environments. However, the acoustic parameter space is usually structured, with each species emitting identifiable signals. While signal partitioning has been reported, very few analyses include the mechanical spectral response of auditory organs. The loud chorus generated by three cicadas (Cicada orni, Cicadatra atra, and Lyristes plebejus) was studied. The vibration pattern of L. plebejus shows traveling waves as previously observed in Ctra. atra. The spectral properties of both calling songs and tympanal auditory systems primarily indicate that each species uses its own frequency band. Male tympanal membranes (TMs) are tuned to their own song's dominant frequency, except for C. orni, which is sensitive to the lowest frequency band of its song. In contrast, female TMs are broadly tuned to the male songs. Ctra. atra females differ by tuning to frequencies slightly higher than the male song. Hence, acoustic space partitioning occurs for both emitter and receiver, but does not seem to fully preclude interference risk as some spectral overlap exists. In addition to the local physical ecology of each species, selective attention to conspecific signals is likely to be enhanced by further mechanical and neuronal processing.

The next step in cicada audition: measuring pico-mechanics in the cicada's ear

Female cicadas use sound when they select a mate from a chorus of singing males. The cicada has a tympanal ear; and the tympanal membrane, and constituent tympanal ridge, act as both acousto-mechanical transducers and frequency filters. The tympanal ridge is physically connected to a large number of mechanoreceptor neurons via a cuticular extension known as the tympanal apodeme. Using microscanning laser Doppler vibrometry, we measured for the first time the in vivo vibrations of the apodeme of female Cicadatra atra in response to the motion of the tympanum driven by sound. These measurements reveal that the nanoscale motion of the tympanal membrane is over a magnitude greater than that of the apodeme. Furthermore, the apodeme acts as an additional mechanical frequency filter, enhancing that of the tympanal ridge, narrowing the frequency band of vibration at the mechanoreceptor neurons to that of the male calling song. This study enhances our understanding of the mechanical link between the external ear of the cicada and its sensory cells.

Picometre scale mechanics in the cicada ear

Female cicadas use sound to select their mate from a chorus of singing males. Cicadas have tympanal ears, with both the ear's tympanal membrane, and constituent tympanal ridge, acting as acousto-mechanical transducers and frequency filters. Within the ear the tympanal ridge is mechanically connected to a large number of mechanosensory neurons via a cuticular extension known as the tympanal apodeme. Using microscanning laser Doppler vibrometry, the in vivo vibrations of the tympanal apodeme of female Cicadatra atra have been measured for the first time as they respond to the motion of the tympanal membrane driven by sound. These precise measurements reveal that the tympanal membrane's nanometre motion is over a magnitude greater than that of the tympanal apodeme at the point where the neurons attach. Further, the tympanal apodeme acts as an additional mechanical frequency filter, enhancing the frequency filtering of the tympanal ridge, to narrow the frequency band of vibration at the mechanoreceptor neurons solely to that of the male calling song. This study thus enhances our understanding of the mechanical links between the external ear of the cicada and its sensory cells. Poster Session held on Tuesday 30th June 2009 at the Annual Meeting of the Society for Experimental Biology, 28th June-1st July, Glasgow, UK.

Are there active hearing processes in locust ears?

Poster Session held on Monday 29th June 2009 at the Annual Main Meeting of the Society of Experimental Biology, 28th June - 1st July, Glasgow, UK. The locust tympanal organ is a sophisticated example of insect hearing. The tympanal membrane has previously been shown to analyse the frequency of incident sound, such that sound energy is funnelled into waves of motion across the membrane, travelling to frequency specific neurone groups. In vertebrates Otoacoustic emissions have been shown to indicate active hearing processes. These sound emissions are produced as a by-product in the ears of vertebrates, and can be spontaneous or evoked by acoustic stimulus. The evoked emissions, known as distortion-products, are found in active auditory systems when the organ is stimulated with two sounds of different frequencies, f1 and f2. In some insects, including locusts, previous studies have found evidence of distortion-products, but the experimental approach raises questions as to whether the results are actually driven by active hearing processes. In these previous experiments a closed-air system was used with the sound stimulus very close to the organ. The experiments have been revised, altering the experimental set-up to an open system, with appropriate sound pressure levels, such as the ear would expect in a natural setting. A laser vibrometer records the deflection of the locust tympanal membrane at specific points where the mechanoreceptor neurones attach. This allows the membrane to be measured directly for the presence of distortion-products, at the position of the neurones which are believed to be actively generating membrane sound emissions. The measurement, or lack thereof, of distortion-products in the motion of the tympanal membrane is discussed and compared with previous studies.

Mechanical response of the tympanal membranes of the tree cricket Oecanthus henryi

Crickets have two tympanal membranes on the tibiae of each foreleg. Among several field cricket species of the genus Gryllus (Gryllinae), the posterior tympanal membrane (PTM) is significantly larger than the anterior membrane (ATM). Laser Doppler vibrometric measurements have shown that the smaller ATM does not respond as much as the PTM to sound. Hence the PTM has been suggested to be the principal tympanal acoustic input to the auditory organ. In tree crickets (Oecanthinae), the ATM is slightly larger than the PTM. Both membranes are structurally complex, presenting a series of transverse folds on their surface, which are more pronounced on the ATM than on the PTM. The mechanical response of both membranes to acoustic stimulation was investigated using microscanning laser Doppler vibrometry. Only a small portion of the membrane surface deflects in response to sound. Both membranes exhibit similar frequency responses, and move out of phase with each other, producing compressions and rarefactions of the tracheal volume backing the tympanum. Therefore, unlike field crickets, tree crickets may have four instead of two functional tympanal membranes. This is interesting in the context of the outstanding question of the role of spiracular inputs in the auditory system of tree crickets.