Sound localization by the internally coupled ears of lizards: From biophysics to biorobotics.

As they are generally small and only hear low frequencies, lizards have few cues for localizing sound. However, their ears show extreme directionality (up to 30 dB direction-dependent difference in eardrum vibrations) created by strong acoustical coupling of the eardrums, with almost perfect internal transmission from the contralateral ear over a broad frequency range. The activity of auditory nerve fibers reflects the eardrum directionality, so all auditory neurons are directional by default. This suggests that the ensuing neural processing of sound direction is simple in lizards. Even the simplest configuration of electrical analog models-two tympanic impedances connected via a central capacitor-produces directional patterns that are qualitatively similar to the experimental data on lizard ears. Several models, both analytical and (very recently) finite-element models, have been published. Robotic implementations using simplified models of the ear and of binaural comparison show that robust phonotaxic behavior can be generated with little additional processing and be performed by simple (and thus small and cheap) units. The authors review lizard directional processing and attempts at modeling and robotics with a twofold aim: to clarify the authors' understanding of central processing of sound localization in lizards, and to lead to technological developments of bioinspired robotics.

Travelling waves and tonotopicity in the inner ear: a historical and comparative perspective.

In the 1940s, Georg von Békésy discovered that in the inner ear of cadavers of various vertebrates, structures responded to sound with a displacement wave that travels in a basal-to-apical direction. This historical review examines this concept and sketches its rôle and significance in the development of the research field of cochlear mechanics. It also illustrates that this concept and that of tonotopicity necessarily correlate, in that travelling waves are consequences of the existence of an ordered, longitudinal array of receptor cells tuned to systematically changing frequencies along the auditory organ.

Salient features of otoacoustic emissions are common across tetrapod groups and suggest shared properties of generation mechanisms.

Otoacoustic emissions (OAEs) are faint sounds generated by healthy inner ears that provide a window into the study of auditory mechanics. All vertebrate classes exhibit OAEs to varying degrees, yet the biophysical origins are still not well understood. Here, we analyzed both spontaneous (SOAE) and stimulus-frequency (SFOAE) otoacoustic emissions from a bird (barn owl, Tyto alba) and a lizard (green anole, Anolis carolinensis). These species possess highly disparate macromorphologies of the inner ear relative to each other and to mammals, thereby allowing for novel insights into the biomechanical mechanisms underlying OAE generation. All ears exhibited robust OAE activity, and our chief observation was that SFOAE phase accumulation between adjacent SOAE peak frequencies clustered about an integral number of cycles. Being highly similar to published results from human ears, we argue that these data indicate a common underlying generator mechanism of OAEs across all vertebrates, despite the absence of morphological features thought essential to mammalian cochlear mechanics. We suggest that otoacoustic emissions originate from phase coherence in a system of coupled oscillators, which is consistent with the notion of "coherent reflection" but does not explicitly require a mammalian-type traveling wave. Furthermore, comparison between SFOAE delays and auditory nerve fiber responses for the barn owl strengthens the notion that most OAE delay can be attributed to tuning.

Releases of surgically deafened homing pigeons indicate that aural cues play a significant role in their navigational system.

Experienced homing pigeons with extirpated cochleae and lagenae were released from six sites in upstate New York and western Pennsylvania on 17 days between 1973 and 1975 by William T. Keeton and his co-workers at Cornell University. The previously unpublished data indicate that departure directions of the operated birds were significantly different from those of sham-operated control birds (314 total), indicating that aural cues play an important part in the pigeon's navigational system. Moreover, propagation modeling of infrasonic waves using meteorological data for the release days supports the possibility that control birds used infrasonic signals to determine their homeward direction. Local acoustic 'shadow' zones, therefore, could have caused initial disorientation of control birds at release sites where they were normally well oriented. Experimental birds plausibly employed an alternate 'route-reversal' strategy to return home perhaps using their ocular-based magnetic compass. We suggest, based on Keeton's results from another site of long-term disorientation, that experienced pigeons depend predominantly on infrasonic cues for initial orientation, and that surgical removal of their aural sense compelled them to switch to a secondary navigational strategy.

Conditions Underlying the Appearance of Spontaneous Otoacoustic Emissions in Mammals.

Across the wide range of land vertebrate species, spontaneous otoacoustic emissions (SOAE) are common, but not always found. The reasons for the differences between species of the various groups in their emission patterns are often not well understood, particularly within mammals. This review examines the question as to what determines in mammals whether SOAE are emitted or not, and suggests that the coupling between hair-cell regions diminishes when the space constant of frequency distribution becomes larger. The reduced coupling is assumed to result in a greater likelihood of SOAE being emitted.

Otoacoustic emissions in African mole-rats.

African mole-rats display highly derived hearing that is characterized by low sensitivity and a narrow auditory range restricted to low frequencies < 10 kHz. Recently, it has been suggested that two species of these rodents do not exhibit distortion product otoacoustic emissions (DPOAE), which was interpreted as evidence for a lack of cochlear amplification. If true, this would make them unique among mammals. However, both theoretical considerations on the generation of DPOAE as well as previously published experimental evidence challenge this assumption. We measured DPOAE and stimulus-frequency otoacoustic emissions (SFOAE) in three species of African mole-rats (Ansell's mole-rat - Fukomys anselli; Mashona mole-rat - Fukomys darlingi; naked mole-rat - Heterocephalus glaber) and found unexceptional otoacoustic emission values. Measurements were complicated by the remarkably long, narrow and curved external ear canals of these animals, for which we provide a morphological description. Both DPOAE and SFOAE displayed the highest amplitudes near 1 kHz, which corresponds to the region of best hearing in all tested species, as well as to the frequency region of the low-frequency acoustic fovea previously described in Ansell's mole-rat. Thus, the cochlea in African mole-rats shares the ability to generate evoked otoacoustic emission with other mammals.

Mosaic evolution of the mammalian auditory periphery.

The classical mammalian auditory periphery, i.e., the type of middle ear and coiled cochlea seen in modern therian mammals, did not arise as one unit and did not arise in all mammals. It is also not the only kind of auditory periphery seen in modern mammals. This short review discusses the fact that the constituents of modern mammalian auditory peripheries arose at different times over an extremely long period of evolution (230 million years; Ma). It also attempts to answer questions as to the selective pressures that led to three-ossicle middle ears and the coiled cochlea. Mammalian middle ears arose de novo, without an intermediate, single-ossicle stage. This event was the result of changes in eating habits of ancestral animals, habits that were unrelated to hearing. The coiled cochlea arose only after 60 Ma of mammalian evolution, driven at least partly by a change in cochlear bone structure that improved impedance matching with the middle ear of that time. This change only occurred in the ancestors of therian mammals and not in other mammalian lineages. There is no single constellation of structural features of the auditory periphery that characterizes all mammals and not even all modern mammals.

A model for the relation between stimulus frequency and spontaneous otoacoustic emissions in lizard papillae.

Spontaneous otoacoustic emissions (SOAEs) and stimulus frequency otoacoustic emissions (SFOAEs) have been described from lizard ears. Although there are several models for these systems, none has modeled the characteristics of both of these types of otoacoustic emissions based upon their being derived from hair cells as active oscillators. Data from the ears of two lizard species, one lacking a tectorial membrane and one with a chain of tectorial sallets, as described by Bergevin et al. ["Coupled, active oscillators and lizard otoacoustic emissions," AIP Conf. Proc. 1403, 453 (2008)], are modeled as an array of coupled self-sustained oscillators. The model, originally developed by Vilfan and Duke ["Frequency clustering in spontaneous otoacoustic emissions from a lizard's ear," Biophys. J. 95, 4622-4630 (2008)], well describes both the amplitude and phase characteristics of SFOAEs and the relation between SFOAEs and SOAEs.

Otoacoustic Emissions in Non-Mammals.

Otoacoustic emissions (OAE) that were sound-induced, current-induced, or spontaneous have been measured in non-mammalian land vertebrates, including in amphibians, reptiles, and birds. There are no forms of emissions known from mammals that have not also been observed in non-mammals. In each group and species, the emission frequencies clearly lie in the range known to be processed by the hair cells of the respective hearing organs. With some notable exceptions, the patterns underlying the measured spectra, input-output functions, suppression threshold curves, etc., show strong similarities to OAE measured in mammals. These profound similarities are presumably traceable to the fact that emissions are produced by active hair-cell mechanisms that are themselves dependent upon comparable nonlinear cellular processes. The differences observed-for example, in the width of spontaneous emission peaks and delay times in interactions between peaks-should provide insights into how hair-cell activity is coupled within the organ and thus partially routed out into the middle ear.

An evolutionary approach to middle-ear prostheses.

The erroneous idea that mammalian three-ossicle middle ears are superior to single-ossicle ones has influenced thinking about prostheses. Evolutionary facts and measurements indicate that single-ossicle ears are equivalent and more flexible, supporting - in spite of new technological reconstruction techniques - their continued use as prostheses.

Exceptional high-frequency hearing and matched vocalizations in Australian pygopod geckos.

We describe exceptional high-frequency hearing and vocalizations in a genus of pygopod lizards (Delma) that is endemic to Australia. Pygopods are a legless subfamily of geckos and share their highly specialized hearing organ. Hearing and vocalizations of amniote vertebrates were previously thought to differ clearly in their frequency ranges according to their systematic grouping. The upper frequency limit would thus be lowest in chelonians and increasingly higher in crocodilians, lizards, birds and mammals. We report data from four Delma species (D. desmosa, D. fraseri, D. haroldi, D. pax) from the Pilbara region of Western Australia that were studied using recordings of auditory-nerve compound action potentials (CAP) under remote field conditions. Hearing limits and vocalization energy of Delma species extended to frequencies far above those reported for any other lizard group, 14 kHz and >20 kHz, respectively. Their remarkable high-frequency hearing derives from the basilar papilla, and forward masking of CAP responses suggests a unique division of labor between groups of sensory cells within the hearing organ. These data also indicate that rather than having only strictly group-specific frequency ranges, amniote vertebrate hearing is strongly influenced by species-specific physical and ecological constraints.

Modeling the characteristics of spontaneous otoacoustic emissions in lizards.

Lizard auditory papillae have proven to be an attractive object for modelling the production of spontaneous otoacoustic emissions (SOAE). Here we use an established model (Vilfan and Duke, 2008) and extend it by exploring the effect of varying the number of oscillating elements, the strength of the parameters that describe the coupling between oscillators, the strength of the oscillators, and additive noise. The most remarkable result is that the actual number of oscillating elements hardly influences the spectral pattern, explaining why spectra from very different papillar dimensions are similar. Furthermore, the spacing between spectral peaks primarily depends on the reactive coupling between the oscillator elements. This is consistent with observed differences between lizard species with respect to tectorial covering of hair cells and SOAE peak spacings. Thus, the model provides a basic understanding of the variation in SOAE properties across lizard species.

Suppression tuning of spontaneous otoacoustic emissions in the barn owl (Tyto alba).

Spontaneous otoacoustic emissions (SOAEs) have been observed in a variety of different vertebrates, including humans and barn owls (Tyto alba). The underlying mechanisms producing the SOAEs and the meaning of their characteristics regarding the frequency selectivity of an individual and species are, however, still under debate. In the present study, we measured SOAE spectra in lightly anesthetized barn owls and suppressed their amplitudes by presenting pure tones at different frequencies and sound levels. Suppression effects were quantified by deriving suppression tuning curves (STCs) with a criterion of 2 dB suppression. SOAEs were found in 100% of ears (n = 14), with an average of 12.7 SOAEs per ear. Across the whole SOAE frequency range of 3.4-10.2 kHz, the distances between neighboring SOAEs were relatively uniform, with a median distance of 430 Hz. The majority (87.6%) of SOAEs were recorded at frequencies that fall within the barn owl's auditory fovea (5-10 kHz). The STCs were V-shaped and sharply tuned, similar to STCs from humans and other species. Between 5 and 10 kHz, the median Q10dB value of STC was 4.87 and was thus lower than that of owl single-unit neural data. There was no evidence for secondary STC side lobes, as seen in humans. The best thresholds of the STCs varied from 7.0 to 57.5 dB SPL and correlated with SOAE level, such that smaller SOAEs tended to require a higher sound level to be suppressed. While similar, the frequency-threshold curves of auditory-nerve fibers and STCs of SOAEs differ in some respects in their tuning characteristics indicating that SOAE suppression tuning in the barn owl may not directly reflect neural tuning in primary auditory nerve fibers.

A Functional Perspective on the Evolution of the Cochlea.

This review summarizes paleontological data as well as studies on the morphology, function, and molecular evolution of the cochlea of living mammals (monotremes, marsupials, and placentals). The most parsimonious scenario is an early evolution of the characteristic organ of Corti, with inner and outer hair cells and nascent electromotility. Most remaining unique features, such as loss of the lagenar macula, coiling of the cochlea, and bony laminae supporting the basilar membrane, arose later, after the separation of the monotreme lineage, but before marsupial and placental mammals diverged. The question of when hearing sensitivity first extended into the ultrasonic range (defined here as >20 kHz) remains speculative, not least because of the late appearance of the definitive mammalian middle ear. The last significant change was optimizing the operating voltage range of prestin, and thus the efficiency of the outer hair cells' amplifying action, in the placental lineage only.

Acoustical coupling of lizard eardrums.

Lizard ears are clear examples of two-input pressure-difference receivers, with up to 40-dB differences in eardrum vibration amplitude in response to ipsi- and contralateral stimulus directions. The directionality is created by acoustical coupling of the eardrums and interaction of the direct and indirect sound components on the eardrum. The ensuing pressure-difference characteristics generate the highest directionality of any similar-sized terrestrial vertebrate ear. The aim of the present study was to measure the gain of the direct and indirect sound components in three lizard species: Anolis sagrei and Basiliscus vittatus (iguanids) and Hemidactylus frenatus (gekkonid) by laser vibrometry, using either free-field sound or a headphone and coupler for stimulation. The directivity of the ear of these lizards is pronounced in the frequency range from 2 to 5 kHz. The directivity is ovoidal, asymmetrical across the midline, but largely symmetrical across the interaural axis (i.e., front-back). Occlusion of the contralateral ear abolishes the directionality. We stimulated the two eardrums with a coupler close to the eardrum to measure the gain of the sound pathways. Within the frequency range of maximal directionality, the interaural transmission gain (compared to sound arriving directly) is close to or even exceeds unity, indicating a pronounced acoustical transparency of the lizard head and resonances in the interaural cavities. Our results show that the directionality of the lizard ear is caused by the acoustic interaction of the two eardrums. The results can be largely explained by a simple acoustical model based on an electrical analog circuit.

What have lizard ears taught us about auditory physiology?

The structure of the basilar papilla of the inner ear of lizards is the most diverse among all vertebrates. Research on a variety of lizard ears, animals that are remarkably robust under laboratory conditions, has provided the field of auditory research with valuable information, particularly on the minimum structural requirements for sensitive, selective hearing and on the importance of the tectorial membrane and active processes in this regard. Despite the absence of a tuned basilar membrane, lizard ears produce highly frequency selective hearing through micromechanical tuning of small, resonant hair-cell-tectorial units or of free-standing hair bundles. These units are driven by an active process that also underlies spontaneous and other otoacoustic emissions. Lizard ears provided the first in vivo evidence that the active process is calcium-sensitive and lies within the stereovillar bundles of the hair cells.

Spontaneous otoacoustic emissions in teiid lizards.

SOAE from the last major lizard family not yet systematically investigated, the teiids, were collected from the genera Callopistes, Tupinambis and Cnemidophorus. Although their papillae show characteristics of the family Teiidae, the papillae differ both in their size and in the arrangement of uni- and bi-directional hair-cell areas. Among these three genera, Callopistes showed few (2 or 3) SOAE peaks, whereas the other two genera showed more (up to 6 per ear). In the absence of knowledge of the tonotopic maps, however, it was not possible to clearly relate the spectral patterns to the differences in papillar anatomy, suggesting that the determinants of these patterns may be more subtle than anticipated.

Comparative Auditory Neuroscience: Understanding the Evolution and Function of Ears.

Comparative auditory studies make it possible both to understand the origins of modern ears and the factors underlying the similarities and differences in their performance. After all lineages of land vertebrates had independently evolved tympanic middle ears in the early Mesozoic era, the subsequent tens of millions of years led to the hearing organ of lizards, birds, and mammals becoming larger and their upper frequency limits higher. In extant species, lizard papillae remained relatively small (<2 mm), but avian papillae attained a maximum length of 11 mm, with the highest frequencies in both groups near 12 kHz. Hearing-organ sizes in modern mammals vary more than tenfold, up to >70 mm (made possible by coiling), as do their upper frequency limits (from 12 to >200 kHz). The auditory organs of the three amniote groups differ characteristically in their cellular structure, but their hearing sensitivity and frequency selectivity within their respective hearing ranges hardly differ. In the immediate primate ancestors of humans, the cochlea became larger and lowered its upper frequency limit. Modern humans show an unusual trend in frequency selectivity as a function of frequency. It is conceivable that the frequency selectivity patterns in humans were influenced in their evolution by the development of speech.

The mammalian Cretaceous cochlear revolution.

The hearing organs of amniote vertebrates show large differences in their size and structure between the species' groups. In spite of this, their performance in terms of hearing sensitivity and the frequency selectivity of auditory-nerve units shows unexpectedly small differences. The only substantial difference is that therian, defined as live-bearing, mammalian groups are able to hear ultrasonic frequencies (above 15-20 kHz), whereas in contrast monotreme (egg laying) mammals and all non-mammalian amniotes cannot. This review compares the structure and physiology of the cochleae of the main groups and asks the question as to why the many structural differences seen in therian mammals arose, yet did not result in greater differences in physiology. The likely answers to this question are found in the history of the mammals during the Cretaceous period that ended 65 million years ago. During that period, the therian cochlea lost its lagenar macula, leading to a fall in endolymph calcium levels. This likely resulted in a small revolution and an auditory crisis that was compensated for by a subsequent series of structural and physiological adaptations. The end result was a system of equivalent performance to that independently evolved in other amniotes but with the additional - and of course "unforeseen" - advantage that ultrasonic-frequency responses became an available option. That option was not always availed of, but in most groups of therian mammals it did evolve and is used for communication and orientation based on improved sound localization, with micro-bats and toothed whales relying on it for prey capture.

Spontaneous otoacoustic emissions from free-standing stereovillar bundles of ten species of lizard with small papillae.

Spontaneous otoacoustic emissions (SOAE) were measured in 10 lizard species from the families Iguanidae, Agamidae and Anguidae. The typical feature of these papillae is that the hair cells in the higher-frequency papillar regions that produce SOAE are not covered by a tectorial structure. The number of hair cells in the species used here was between 58 and 292 per ear. SOAE could be measured from all species, but some of their characteristics varied with papillar anatomy. Thus very small papillae produced fewer and smaller SOAE than larger papillae.