Christian Bech Christensen

Hearing with an atympanic ear: good vibration and poor sound-pressure detection in the royal python, Python regius

SUMMARY Snakes lack both an outer ear and a tympanic middle ear, which in most tetrapods provide impedance matching between the air and inner ear fluids and hence improve pressure hearing in air. Snakes would therefore be expected to have very poor pressure hearing and generally be insensitive to airborne sound, whereas the connection of the middle ear bone to the jaw bones in snakes should confer acute sensitivity to substrate vibrations. Some studies have nevertheless claimed that snakes are quite sensitive to both vibration and sound pressure. Here we test the two hypotheses that: (1) snakes are sensitive to sound pressure and (2) snakes are sensitive to vibrations, but cannot hear the sound pressure per se. Vibration and sound-pressure sensitivities were quantified by measuring brainstem evoked potentials in 11 royal pythons, Python regius. Vibrograms and audiograms showed greatest sensitivity at low frequencies of 80–160 Hz, with sensitivities of –54 dB re. 1 m s–2 and 78 dB re. 20 μPa, respectively. To investigate whether pythons detect sound pressure or sound-induced head vibrations, we measured the sound-induced head vibrations in three dimensions when snakes were exposed to sound pressure at threshold levels. In general, head vibrations induced by threshold-level sound pressure were equal to or greater than those induced by threshold-level vibrations, and therefore sound-pressure sensitivity can be explained by sound-induced head vibration. From this we conclude that pythons, and possibly all snakes, lost effective pressure hearing with the complete reduction of a functional outer and middle ear, but have an acute vibration sensitivity that may be used for communication and detection of predators and prey.

Specialization for underwater hearing by the tympanic middle ear of the turtle, Trachemys scripta elegans

Turtles, like other amphibious animals, face a trade-off between terrestrial and aquatic hearing. We used laser vibrometry and auditory brainstem responses to measure their sensitivity to vibration stimuli and to airborne versus underwater sound. Turtles are most sensitive to sound underwater, and their sensitivity depends on the large middle ear, which has a compliant tympanic disc attached to the columella. Behind the disc, the middle ear is a large air-filled cavity with a volume of approximately 0.5 ml and a resonance frequency of approximately 500 Hz underwater. Laser vibrometry measurements underwater showed peak vibrations at 500–600 Hz with a maximum of 300 µm s−1 Pa−1, approximately 100 times more than the surrounding water. In air, the auditory brainstem response audiogram showed a best sensitivity to sound of 300–500 Hz. Audiograms before and after removing the skin covering reveal that the cartilaginous tympanic disc shows unchanged sensitivity, indicating that the tympanic disc, and not the overlying skin, is the key sound receiver. If air and water thresholds are compared in terms of sound intensity, thresholds in water are approximately 20–30 dB lower than in air. Therefore, this tympanic ear is specialized for underwater hearing, most probably because sound-induced pulsations of the air in the middle ear cavity drive the tympanic disc.

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

In the transition from an aquatic to a terrestrial lifestyle, vertebrate auditory systems have undergone major changes while adapting to aerial hearing. Lungfish are the closest living relatives of tetrapods and their auditory system may therefore be a suitable model of the auditory systems of early tetrapods such as Acanthostega. Therefore, experimental studies on the hearing capabilities of lungfish may shed light on the possible hearing capabilities of early tetrapods and broaden our understanding of hearing across the water-to-land transition. Here, we tested the hypotheses that (i) lungfish are sensitive to underwater pressure using their lungs as pressure-to-particle motion transducers and (ii) lungfish can detect airborne sound. To do so, we used neurophysiological recordings to estimate the vibration and pressure sensitivity of African lungfish (Protopterus annectens) in both water and air. We show that lungfish detect underwater sound pressure via pressure-to-particle motion transduction by air volumes in their lungs. The morphology of lungfish shows no specialized connection between these air volumes and the inner ears, and so our results imply that air breathing may have enabled rudimentary pressure detection as early as the Devonian era. Additionally, we demonstrate that lungfish in spite of their atympanic middle ear can detect airborne sound through detection of sound-induced head vibrations. This strongly suggests that even vertebrates with no middle ear adaptations for aerial hearing, such as the first tetrapods, had rudimentary aerial hearing that may have led to the evolution of tympanic middle ears in recent tetrapods.

Range-dependent flexibility in the acoustic field of view of echolocating porpoises (Phocoena phocoena)

Toothed whales use sonar to detect, locate, and track prey. They adjust emitted sound intensity, auditory sensitivity and click rate to target range, and terminate prey pursuits with high-repetition-rate, low-intensity buzzes. However, their narrow acoustic field of view (FOV) is considered stable throughout target approach, which could facilitate prey escape at close-range. Here, we show that, like some bats, harbour porpoises can broaden their biosonar beam during the terminal phase of attack but, unlike bats, maintain the ability to change beamwidth within this phase. Based on video, MRI, and acoustic-tag recordings, we propose this flexibility is modulated by the melon and implemented to accommodate dynamic spatial relationships with prey and acoustic complexity of surroundings. Despite independent evolution and different means of sound generation and transmission, whales and bats adaptively change their FOV, suggesting that beamwidth flexibility has been an important driver in the evolution of echolocation for prey tracking. DOI: http://dx.doi.org/10.7554/eLife.05651.001

Better than fish on land?: Hearing across metamorphosis in salamanders

Early tetrapods faced an auditory challenge from the impedance mismatch between air and tissue in the transition from aquatic to terrestrial lifestyles during the Early Carboniferous (350 Ma). Consequently, tetrapods may have been deaf to airborne sounds for up to 100 Myr until tympanic middle ears evolved during the Triassic. The middle ear morphology of recent urodeles is similar to that of early ‘lepospondyl’ microsaur tetrapods, and experimental studies on their hearing capabilities are therefore useful to understand the evolutionary and functional drivers behind the shift from aquatic to aerial hearing in early tetrapods. Here, we combine imaging techniques with neurophysiological measurements to resolve how the change from aquatic larvae to terrestrial adult affects the ear morphology and sensory capabilities of salamanders. We show that air-induced pressure detection enhances underwater hearing sensitivity of salamanders at frequencies above 120 Hz, and that both terrestrial adults and fully aquatic juvenile salamanders can detect airborne sound. Collectively, these findings suggest that early atympanic tetrapods may have been pre-equipped to aerial hearing and are able to hear airborne sound better than fish on land. When selected for, this rudimentary hearing could have led to the evolution of tympanic middle ears.

Ear-EEG based objective hearing threshold estimation evaluated on normal hearing subjects

Objective: Hearing threshold levels have been estimated successfully in the clinic using the objective electroencephalogram (EEG) based technique of auditory steady-state response (ASSR). The recent method of ear-EEG could enable ASSR hearing tests to be performed in everyday life, rather than in a specialized clinic, enabling cheaper and easier monitoring of audiometric thresholds over time. The objective of the current study was to evaluate the feasibility of ear-EEG in audiometric characterization of auditory sensitivity thresholds. Methods: An ear-EEG setup was used to estimate ASSR hearing threshold levels to CE-chirp stimuli (with center frequencies 0.5, 1, 2, and 4 kHz) from four different electrode configurations including conventional scalp configuration, ear electrode with scalp reference, ear electrode with reference in the opposite ear and ear electrode with reference in the same ear. To evaluate the ear-EEG setup, ASSR thresholds estimated using ear-EEG were compared to ASSR thresholds estimated using standardized audiological equipment. Results: The SNRs of in-ear ear-EEG recordings were found to be on average 2.7 to 6.5 dB lower than SNRs of conventional scalp EEG. Thresholds estimated from in-ear referenced ear-EEG were on average 15.0 ± 3.4, 9.1 ± 4.4, 12.5 ± 3.7, and 12.1 ± 2.6 dB above scalp EEG thresholds for 0.5, 1, 2, and 4 kHz, respectively. Conclusion: We demonstrate that hearing threshold levels can be estimated from ear-EEG recordings made from electrodes placed in one ear. Significance: Objective hearing threshold estimation based on ear-EEG can be integrated into hearing aids, thereby allowing hearing assessment to be performed by the hearing instrument on a regular basis.

Reference configurations for ear-EEG steady-state responses

Ear-EEG is a non-invasive EEG recording method, where EEG is recorded from electrodes placed in the ear. Ear-EEG could be implemented into hearing aids, and provide neurofeedback for e.g. objective hearing assessment through measurements of the auditory steady-state response. In cases where the objective is to measure a specific feature of an event-related potential, there will be a subject specific optimal reference configuration. This work presents a method for optimizing the reference configuration for steady-state type potentials. For given electrode positions, the method maximizes the signal-to-noise (SNR) ratio of the first harmonic of the steady-state response. This is obtained by estimating a set of weights applied to the electrode signals. The method was validated on a dataset recorded from 12 subjects. The weights were estimated from one part of the dataset, and the validation was performed on another part of the dataset. For all subjects the proposed method demonstrated a robust SNR estimate, yielding on par or better SNR compared to other well-known methods.

In defence of comparative physiology: ideal models for early tetrapods do not exist

We thank Anderson et al. [[1][1]] for engaging in our paper on hearing in salamanders [[2][2]]. We have written our paper primarily as experimental physiologists basing hypotheses on recent animals and with no research expertise in palaeontology. Therefore, discussions with palaeontologists are