Acoustical Coupling of Lizard Eardrums

Christensen‐Dalsgaard, Jakob; Manley, Geoffrey A.

doi:10.1007/s10162-008-0130-2

Cited by 83 publications

(106 citation statements)

References 25 publications

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“…The differences between non-mammals are not trivial to explain and the picture recently has become confused due to the discovery of middle-ear responses in some lizards to unexpectedly high frequencies (>8kHz) (Christensen-Dalsgaard and Manley, 2005;Christensen-Dalsgaard and Manley, 2008). The results of the present study suggest that hearing limits are much less specific to systematic groups than previously thought and depend less on phylogenetic position than on species-specific physical (size) and ecological (temperature regime, lifestyle) constraints.…”

Section: Introductioncontrasting

confidence: 51%

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

Manley

Kraus

2010

Journal of Experimental Biology

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SUMMARYWe 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.

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Section: Introductioncontrasting

confidence: 51%

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

Manley

Kraus

2010

Journal of Experimental Biology

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“…Lizard ears are highly directional, with middle ears connected through the mouth cavity (Christensen-Dalsgaard and Manley, 2005Manley, , 2008. The inner ears are also highly specialized, with sensitive high-frequency hearing in a specialized region of the papilla (Manley, 2002).…”

Section: Organization Of the First-order Nucleimentioning

confidence: 99%

“…Their ears differ from those of other reptiles such as archosaurs and turtles. Lepidosaur ears are highly directional, with middle ears connected through the mouth cavity (Christensen-Dalsgaard and Manley, 2008). This patent connection enhances the directionality of the ear by allowing sound access to both sides of …”

Section: Introductionmentioning

confidence: 99%

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

Yang

Tang

Carr

2010

J of Comparative Neurology

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Geckos use vocalizations for intraspecific communication, but little is known about the organization of their central auditory system. We therefore used antibodies against the calciumbinding proteins calretinin (CR), parvalbumin (PV), and calbindin-D28k (CB) to characterize the gecko auditory system. We also examined expression of both glutamic acid decarboxlase (GAD) and synaptic vesicle protein (SV2). Western blots showed that these antibodies are specific to gecko brain. All three calcium-binding proteins were expressed in the auditory nerve, and CR immunoreactivity labeled the first-order nuclei and delineated the terminal fields associated with the ascending projections from the first-order auditory nuclei. PV expression characterized the superior olivary nuclei, whereas GAD immunoreactivity characterized many neurons in the nucleus of the lateral lemniscus and some neurons in the torus semicircularis. In the auditory midbrain, the distribution of CR, PV, and CB characterized divisions within the central nucleus of the torus semicircularis. All three calcium-binding proteins were expressed in nucleus medialis of the thalamus. These expression patterns are similar to those described for other vertebrates.Keywords cochlear nucleus; magnocellularis; laminaris; angularis; torus Over 30 years have passed since Foster and Hall (1978) reported that the ascending auditory pathways of the iguana resemble both the mammalian and the avian auditory pathways, from the level of the first-order neurons in the VIIIth nerve to the telencephalon. They recognized a basic plan for the organization of the auditory system in terrestrial vertebrates but also pointed out that the auditory capacities of the lizards were largely unknown. We now know more about the peripheral (Manley, 1990;Wever, 1978) and central (for reviews see Carr, 1992;Grothe et al., 2005;ten Donkelaar et al., 1987) auditory systems of lizards, but still know little about central auditory processing. We have therefore used Gekko gecko for further analysis of the lizard central auditory system.Geckos are auditory specialists that use vocalizations for intraspecific communication (Marcellini, 1977;Tang et al., 2001). Their ears differ from those of other reptiles such as archosaurs and turtles. Lepidosaur ears are highly directional, with middle ears connected through the mouth cavity (Christensen-Dalsgaard and Manley, 2008). This patent connection enhances the directionality of the ear by allowing sound access to both sides of NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript each tympanic membrane. The acoustically coupled ear creates directional responses from the tympanum Manley, 2005, 2008). Additionally, lizards have independently evolved micromechanical hair cell tuning, permitting emergence of sensitive high-frequency hearing in a specialized region of the papilla (Manley, 2002). Thus lizard auditory systems might reveal specializations for hearing high frequencies and sound localization.We have begun our analysis of liza...

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“…Lizards have very sensitive ears, and thin eardrums. The eardrums are connected through the mouth cavity, and since the middle ear is not enclosed in a tympanic cavity, the head is acoustically transparent [9] with unattenuated transmission of sound from the contralateral eardrum [10,11]. An example of the directionality of a lizard ear is shown in Fig.…”

Section: Structure and Function Of The Early Tympanic Earmentioning

confidence: 99%

“…The colour scale is relative interaural differences in dB. From Christensen-Dalsgaard and Manley [10,11]. Eardrum directionality in the grass frog, Rana temporaria.…”

Section: Changes In the Early Tympanic Earmentioning

confidence: 99%

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

Christensen‐Dalsgaard

Carr

2008

Brain Research Bulletin

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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 (2-4 kHz).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 lowfrequency 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.

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Acoustical Coupling of Lizard Eardrums

Cited by 83 publications

References 25 publications

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

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

Calcium‐binding protein immunoreactivity characterizes the auditory system of Gekko gecko

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

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