Lateralization of Travelling Wave Response in the Hearing Organ of Bushcrickets

Udayashankar, Arun Palghat; Kössl, Manfred; Nowotny, Manuela

doi:10.1371/journal.pone.0086090

Cited by 11 publications

(8 citation statements)

References 15 publications

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“…Like the cochlear hearing organs of mammals, the hearing organ of katydids (bushcrickets), called the crista acustica, features a smooth gradient of anatomical properties along its length (1)(2)(3)(4)(5)(6)(7)(8)(9). Upon sound stimulation, the crista acustica responds with mechanical traveling waves (10)(11)(12)(13), and as in the mammalian cochlea, the traveling waves peak at different longitudinal locations, producing a tonotopic map (2,(14)(15)(16)(17)(18)(19)(20)(21). Along the 1-mm length of sensory tissue in the crista acustica of Mecopoda elongata, frequencies ranging from 3 to 80 kHz are processed, with the lower frequencies represented in the proximal region and the higher frequencies in the distal region.…”

Section: Introductionmentioning

confidence: 99%

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

Olson

Nowotny

2019

Biophysical Journal

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The ability to detect airborne sound is essential for many animals. Examples from the inner ear of mammals and bushcrickets demonstrate that similar detection strategies evolved in taxonomically distant species. Both mammalian and bushcricket ears possess a narrow strip of sensory tissue that exhibits an anatomical gradient and traveling wave motion responses used for frequency discrimination. We measured pressure and motion in the bushcricket ear to investigate physical properties, stiffness, and mass, which govern the mechanical responses to sound. As in the mammalian cochlea, sound-induced fluid pressure and motion responses were tonotopically organized along the longitudinal axis of the crista acustica, the bushcricket's hearing organ. The fluid pressure at the crista and crista motion were used to calculate the acoustic impedance of the organ-bounded fluid mass (Z mass ). We used a theoretical wave analysis of wavelength data from a previous study to predict the crista acustica stiffness. The wave analysis also predicts Z mass , and that result agreed reasonably well with the directly measured Z mass , lending support to the theoretical wave analysis. The magnitude of the crista stiffness was similar to basilar membrane stiffness in mammals, and as in mammals, the stiffness decreased from the high-frequency to the low-frequency region. At a given location, the stiffness increased with increasing frequency, corresponding to increasing curvature of the traveling wave (decreasing wavelength), indicating that longitudinal coupling plays a substantial role in determining crista stiffness. This is in contrast to the mammalian ear, in which stiffness is independent of frequency and longitudinal coupling is relatively small.

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Section: Introductionmentioning

confidence: 99%

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

Olson

Nowotny

2019

Biophysical Journal

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“…Innovative approaches and organisms with easy-to-access inner ears could provide alternative solutions to advance our understanding of complex auditory processes. Bush-crickets provide an ideal model, having ears which lay beneath the leg cuticle allowing researchers to measure TWs and tonotopy by removing the leg cuticle and exposing the CA [ 7 , 26 ]. This method has been used with electrophysiology to measure the responses of sensory cells to sound-induced mechanical forces [ 25 ].…”

Section: Introductionmentioning

confidence: 99%

Non-invasive biophysical measurement of travelling waves in the insect inner ear

et al. 2017

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Frequency analysis in the mammalian cochlea depends on the propagation of frequency information in the form of a travelling wave (TW) across tonotopically arranged auditory sensilla. TWs have been directly observed in the basilar papilla of birds and the ears of bush-crickets (Insecta: Orthoptera) and have also been indirectly inferred in the hearing organs of some reptiles and frogs. Existing experimental approaches to measure TW function in tetrapods and bush-crickets are inherently invasive, compromising the fine-scale mechanics of each system. Located in the forelegs, the bush-cricket ear exhibits outer, middle and inner components; the inner ear containing tonotopically arranged auditory sensilla within a fluid-filled cavity, and externally protected by the leg cuticle. Here, we report bush-crickets with transparent ear cuticles as potential model species for direct, non-invasive measuring of TWs and tonotopy. Using laser Doppler vibrometry and spectroscopy, we show that increased transmittance of light through the ear cuticle allows for effective non-invasive measurements of TWs and frequency mapping. More transparent cuticles allow several properties of TWs to be precisely recovered and measured in vivo from intact specimens. Our approach provides an innovative, non-invasive alternative to measure the natural motion of the sensilla-bearing surface embedded in the intact inner ear fluid.

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“…We hypothesized that the call patterns would not prominently correlate with the CA anatomy: auditory sensilla respond usually tonically to sound stimuli (Schul, ; Pollack, ), and frequency analysis and intensity coding occur in the CA (Stumpner & Nowotny, ). The tonopic organization of the CA allows for frequency analysis (Römer, ; Stumpner, ; Stölting & Stumpner, ; Montealegre‐Z et al ., ; Palghat Udayashankar et al ., , ; Hummel et al ., ). Temporal patterns are coded but not selectively analysed in the sensory periphery, and the syllable pattern is transmitted to auditory interneurons (Rössler & Schul, ; Pollack, , ; Stumpner & von Helversen, ).…”

Section: Discussionmentioning

confidence: 99%

“…The CA sensilla are arranged linearly from proximal to distal in the tibia. They are tonotopically ordered, as individual sensilla respond with highest sensitivity to specific sound frequencies, thus giving spectral resolution (Oldfield, , ; Römer, ; Stumpner, ; Stölting & Stumpner, ; Montealegre‐Z et al ., ; Palghat Udayashankar et al ., , ; Hummel et al ., ). Detailed information on the auditory system morphology is available for species from several tettigoniid genera (reviews: Schumacher, , ; Lakes & Schikorski, ; Bailey, ; Rössler et al ., ; Stumpner & Nowotny, ; Montealegre‐Z & Robert, ).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history

Strauß

Alt

Ekschmitt

et al. 2017

J of Evolutionary Biology

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Neoconocephalus Tettigoniidae are a model for the evolution of acoustic signals as male calls have diversified in temporal structure during the radiation of the genus. The call divergence and phylogeny in Neoconocephalus are established, but in tettigoniids in general, accompanying evolutionary changes in hearing organs are not studied. We investigated anatomical changes of the tympanal hearing organs during the evolutionary radiation and divergence of intraspecific acoustic signals. We compared the neuroanatomy of auditory sensilla (crista acustica) from nine Neoconocephalus species for the number of auditory sensilla and the crista acustica length. These parameters were correlated with differences in temporal call features, body size, life histories and different phylogenetic positions. By this, adaptive responses to shifting frequencies of male calls and changes in their temporal patterns can be evaluated against phylogenetic constraints and allometry. All species showed well-developed auditory sensilla, on average 32-35 between species. Crista acustica length and sensillum numbers correlated with body size, but not with phylogenetic position or life history. Statistically significant correlations existed also with specific call patterns: a higher number of auditory sensilla occurred in species with continuous calls or slow pulse rates, and a longer crista acustica occurred in species with double pulses or slow pulse rates. The auditory sensilla show significant differences between species despite their recent radiation, and morphological and ecological similarities. This indicates the responses to natural and sexual selection, including divergence of temporal and spectral signal properties. Phylogenetic constraints are unlikely to limit these changes of the auditory systems.

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Lateralization of Travelling Wave Response in the Hearing Organ of Bushcrickets

Cited by 11 publications

References 15 publications

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

Non-invasive biophysical measurement of travelling waves in the insect inner ear

Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history

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