Jakob Christensen-Dalsgaard

Sound detection by the longfin squid (Loligo pealeii) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure

SUMMARY Although hearing has been described for many underwater species, there is much debate regarding if and how cephalopods detect sound. Here we quantify the acoustic sensitivity of the longfin squid (Loligo pealeii) using near-field acoustic and shaker-generated acceleration stimuli. Sound field pressure and particle motion components were measured from 30 to 10,000 Hz and acceleration stimuli were measured from 20 to 1000 Hz. Responses were determined using auditory evoked potentials (AEPs) with electrodes placed near the statocysts. Evoked potentials were generated by both stimuli and consisted of two wave types: (1) rapid stimulus-following waves, and (2) slower, high-amplitude waves, similar to some fish AEPs. Responses were obtained between 30 and 500 Hz with lowest thresholds between 100 and 200 Hz. At the best frequencies, AEP amplitudes were often >20 μV. Evoked potentials were extinguished at all frequencies if (1) water temperatures were less than 8°C, (2) statocysts were ablated, or (3) recording electrodes were placed in locations other than near the statocysts. Both the AEP response characteristics and the range of responses suggest that squid detect sound similarly to most fish, with the statocyst acting as an accelerometer through which squid detect the particle motion component of a sound field. The modality and frequency range indicate that squid probably detect acoustic particle motion stimuli from both predators and prey as well as low-frequency environmental sound signatures that may aid navigation.

Evolution of a sensory novelty: Tympanic ears and the associated neural processing

Tympanic hearing is a true evolutionary novelty that appears to have developed independently in at least five major tetrapod groups-the anurans, turtles, lepidosaurs, archosaurs and mammals. The emergence of a tympanic ear would have increased the frequency range and sensitivity of hearing. Furthermore, tympana were acoustically coupled through the mouth cavity and therefore inherently directional in a certain frequency range, acting as pressure difference receivers. In some lizard species, this acoustical coupling generates a 50-fold directional difference, usually at relatively high frequencies (2-4kHz). In ancestral atympanate tetrapods, we hypothesize that low-frequency sound may have been processed by non-tympanic mechanisms like those in extant amphibians. The subsequent emergence of tympanic hearing would have led to changes in the central auditory processing of both high-frequency sound and directional hearing. These changes should reflect the independent origin of the tympanic ears in the major tetrapod groups. The processing of low-frequency sound, however, may have been more conserved, since the acoustical coupling of the ancestral tympanate ear probably produced little sensitivity and directionality at low frequencies. Therefore, tetrapod auditory processing may originally have been organized into low- and high-frequency streams, where only the high-frequency processing was mediated by tympanic input. The closure of the middle ear cavity in mammals and some birds is a derived condition, and may have profoundly changed the operation of the ear by decoupling the tympana, improving the low-frequency response of the tympanum, and leading to a requirement for additional neural computation of directionality in the central nervous system. We propose that these specializations transformed the low- and high-frequency streams into time and intensity pathways, respectively.

Vertebrate pressure-gradient receivers

The eardrums of all terrestrial vertebrates (tetrapods) are connected through Eustachian tubes or interaural canals. In some of the animals, these connections create pressure-gradient directionality, an enhanced directionality by interaction of sound arriving at both sides of the eardrum and strongly dependent on interaural transmission attenuation. Even though the tympanic middle ear has originated independently in the major tetrapod groups, in each group the ancestral condition probably was that the two middle ears were exposed in the mouth cavity with relatively high interaural transmission. Recent vertebrates form a continuum from perfect interaural transmission (0 dB in a certain frequency band) and pronounced eardrum directionality (30-40 dB) in the lizards, over somewhat attenuated transmission and limited directionality in birds and frogs, to the strongly attenuated interaural transmission and functionally isolated pressure receiver ears in the mammals. Since some of the binaural interaction already takes place at the eardrum in animals with strongly coupled ears, producing enhanced interaural time and level differences, the subsequent neural processing may be simpler. In robotic simulations of lizards, simple binaural subtraction (EI cells, found in brainstem nuclei of both frogs and lizards) produces strongly lateralized responses that are sufficient for steering the animal robustly to sound sources.

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.

Binaural processing by the gecko auditory periphery

Lizards have highly directional ears, owing to strong acoustical coupling of the eardrums and almost perfect sound transmission from the contralateral ear. To investigate the neural processing of this remarkable tympanic directionality, we combined biophysical measurements of eardrum motion in the Tokay gecko with neurophysiological recordings from the auditory nerve. Laser vibrometry shows that their ear is a two-input system with approximately unity interaural transmission gain at the peak frequency (∼ 1.6 kHz). Median interaural delays are 260 μs, almost three times larger than predicted from gecko head size, suggesting interaural transmission may be boosted by resonances in the large, open mouth cavity (Vossen et al. 2010). Auditory nerve recordings are sensitive to both interaural time differences (ITD) and interaural level differences (ILD), reflecting the acoustical interactions of direct and indirect sound components at the eardrum. Best ITD and click delays match interaural transmission delays, with a range of 200-500 μs. Inserting a mold in the mouth cavity blocks ITD and ILD sensitivity. Thus the neural response accurately reflects tympanic directionality, and most neurons in the auditory pathway should be directional.

The auditory brainstem response in two lizard species

Although lizards have highly sensitive ears, it is difficult to condition them to sound, making standard psychophysical assays of hearing sensitivity impractical. This paper describes non-invasive measurements of the auditory brainstem response (ABR) in both Tokay geckos (Gekko gecko; nocturnal animals, known for their loud vocalizations) and the green anole (Anolis carolinensis, diurnal, non-vocal animals). Hearing sensitivity was measured in 5 geckos and 7 anoles. The lizards were sedated with isoflurane, and ABRs were measured at levels of 1 and 3% isoflurane. The typical ABR waveform in response to click stimulation showed one prominent and several smaller peaks occurring within 10 ms of the stimulus onset. ABRs to brief tone bursts revealed that geckos and anoles were most sensitive between 1.6-2 kHz and had similar hearing sensitivity up to about 5 kHz (thresholds typically 20-50 dB SPL). Above 5 kHz, however, anoles were more than 20 dB more sensitive than geckos and showed a wider range of sensitivity (1-7 kHz). Generally, thresholds from ABR audiograms were comparable to those of small birds. Best hearing sensitivity, however, extended over a larger frequency range in lizards than in most bird species.

Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods?

Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.

Sound Exposure of Symphony Orchestra Musicians

BACKGROUND Assessment of sound exposure by noise dosimetry can be challenging especially when measuring the exposure of classical orchestra musicians where sound originate from many different instruments. A new measurement method of bilateral sound exposure of classical musicians was developed and used to characterize sound exposure of the left and right ear simultaneously in two different symphony orchestras. OBJECTIVES To measure binaural sound exposure of professional classical musicians and to identify possible exposure risk factors of specific musicians. METHODS Sound exposure was measured with microphones mounted on the musicians ears and recorded digitally. The recorded sound was analysed and the specific sound exposure of the left and the right ear was determined for the musicians. A total of 114 measurements covering 106 h were recorded in two symphony orchestras. RESULTS Sound exposure depends significantly on the specific instrument and the repertoire played by the exposed musician. Concerts, group rehearsals and individual practice were all significant contributors to the sound exposure. The highest L(Aeq) of 86 -98 dB was found among the brass players. High string players were exposed from 82 to 98 dBA and their left ear was exposed 4.6 dB more than the right ear. Percussionists were exposed to high sound peaks >115 dBC but less continuous sound exposure was observed in this group. Musicians were exposed up to L(Aeq8h) of 92 dB and a majority of musicians were exposed to sound levels exceeding L(Aeq8h) of 85 dB. CONCLUSIONS Binaural recording of the individual sound exposure showed that orchestra musicians could be exposed differently to the left and right ear and that they were primarily exposed from their own instruments. Specific repertoires as well as the specific instrument determine the level of exposure.

Analytical model of internally coupled ears

Lizards and many birds possess a specialized hearing mechanism: internally coupled ears where the tympanic membranes connect through a large mouth cavity so that the vibrations of the tympanic membranes influence each other. This coupling enhances the phase differences and creates amplitude differences in the tympanic membrane vibrations. Both cues show strong directionality. The work presented herein sets out the derivation of a three dimensional analytical model of internally coupled ears that allows for calculation of a complete vibration profile of the membranes. The analytical model additionally provides the opportunity to incorporate the effect of the asymmetrically attached columella, which leads to the activation of higher membrane vibration modes. Incorporating this effect, the analytical model can explain measurements taken from the tympanic membrane of a living lizard, for example, data demonstrating an asymmetrical spatial pattern of membrane vibration. As the analytical calculations show, the internally coupled ears increase the directional response, appearing in large directional internal amplitude differences (iAD) and in large internal time differences (iTD). Numerical simulations of the eigenfunctions in an exemplary, realistically reconstructed mouth cavity further estimate the effects of its complex geometry.