The Frog Inner Ear: Picture Perfect?

Mason, Matthew J.; Segenhout, J. M.; Cobo-Cuan, Ariadna; Quinones, Patricia Martinez; Dijk, Pim van

doi:10.1007/s10162-015-0506-z

Cited by 19 publications

(22 citation statements)

References 30 publications

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“…Thus, hearing in anurans is thought to be a key trait for survival and reproduction. In most anurans, perception of airborne sounds is enabled by a tympanic middle ear (TME) composed minimally of a tympanic membrane, middle ear cavity, and middle ear bone (=columella, columella auris, stapes, plectrum) that conducts sound waves from the environment to the inner ear where they are transduced into electrical signals via hair cells 1 2 3 4 .…”

mentioning

confidence: 99%

The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura)

Pereyra

Womack

Barrionuevo

et al. 2016

Sci Rep

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Most anurans possess a tympanic middle ear (TME) that transmits sound waves to the inner ear; however, numerous species lack some or all TME components. To understand the evolution of these structures, we undertook a comprehensive assessment of their occurrence across anurans and performed ancestral character state reconstructions. Our analysis indicates that the TME was completely lost at least 38 independent times in Anura. The inferred evolutionary history of the TME is exceptionally complex in true toads (Bufonidae), where it was lost in the most recent common ancestor, preceding a radiation of >150 earless species. Following that initial loss, independent regains of some or all TME structures were inferred within two minor clades and in a radiation of >400 species. The reappearance of the TME in the latter clade was followed by at least 10 losses of the entire TME. The many losses and gains of the TME in anurans is unparalleled among tetrapods. Our results show that anurans, and especially bufonid toads, are an excellent model to study the behavioural correlates of earlessness, extratympanic sound pathways, and the genetic and developmental mechanisms that underlie the morphogenesis of TME structures.

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mentioning

confidence: 99%

The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura)

Pereyra

Womack

Barrionuevo

et al. 2016

Sci Rep

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“…In the cyclostomes and all the fish species investigated, as well as in urodeles, he only observed a single-layered, simple epithelium [Retzius, 1881]. Additional studies in other amphibians reported its lack in primitive species such as Ascaphus or Leiopelma [Wagner, 1934] and in pipids including Xenopus [Paterson, 1960;Mason et al, 2015]. In general, the tegmentum vasculosum is found in all neobatrachian ears investigated so far [Mason et al, 2015], whereas it is absent or very poorly developed in archaeoand mesobatrachians.…”

Section: Amphibian Auditory Inner Earmentioning

confidence: 99%

“…However, these auditory compartments are small and in close connection to the other endolymph spaces of the inner ear [Mason et al, 2015]; therefore, the distinction between vestibular and auditory endolymph is probably not useful and we may assume uniform conditions throughout. There is one specific measurement of EP in the basilar-papilla compartment of the leopard frog inner ear [Schmidt and Fernandez, 1962] (Table 1) which, at +3 mV, further supports this assumption.…”

Section: Amphibian Auditory Inner Earmentioning

confidence: 99%

“…The underlying reason for this variability is unknown. Ascaphus or Leiopelma are characterized by the absence of the middle ear [Wagner, 1934[Wagner, , 1934[Wagner, , 1935, but this is not the case for X. laevis [Mason et al, 2015]. Retzius [1981], as well as Kuhn [1880] and Hasse [1868], described the cells in the anuran tegmentum vasculosum as yellowish pigmented, heavily granulated cells.…”

Section: Amphibian Auditory Inner Earmentioning

confidence: 99%

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Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear

et al. 2018

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The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Examples include the middle ear or the unique specializations of the mammalian cochlea. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. This differs both between the vestibular and auditory part of the inner ear as well as between the auditory periphery in different vertebrates. Here we provide a comparison of the cellular and molecular mechanisms in different endorgans across vertebrates. We begin with the lateral line and vestibular systems, as they likely represent plesiomorphic conditions, then review the situation in different vertebrate auditory endorgans. All three systems harbor hair cells bathed in a high (K⁺) environment. Superficial lateral line neuromasts are bathed in an electrogenically maintained high (K⁺) microenvironment provided by the complex gelatinous cupula. This is associated with a positive endocupular potential. Whether this is a special or a universal feature of lateral line and possibly vestibular cupulae remains to be discovered. The vestibular system represents a closed system with an endolymph that is characterized by an enhanced (K⁺) relative to the perilymph. Yet only in land vertebrates does (K⁺) exceed (Na⁺). The endolymphatic potential ranges from +1 to +11 mV, albeit we note intriguing reports of substantially higher potentials of up to +70 mV in the cupula of ampullae of the semicircular canals. Similarly, in the auditory system, a high (K⁺) is observed. However, in contrast to the vestibular system, the positive endolymphatic potential varies more substantially between vertebrates, ranging from near zero mV to approximately +100 mV. The tissues generating endolymph in the inner ear show considerable differences in cell types and location. So-called dark cells and the possibly homologous ionocytes in fish appear to be the common elements, but there is always at least one additional cell type present. To inspire research in this field, we propose a classification for these cell types and discuss potential evolutionary relationships. Their molecular repertoire is largely unknown and provides further fertile ground for future investigation. Finally, we propose that the ultimate selective pressure for an increased endolymphatic potential, as observed in mammals and to a lesser extent in birds, is specifically to maintain the AC component of the hair-cell receptor potential at high frequencies. In summary, we identify intriguing questions for future directions of research into the molecular and cellular basis of the endolymph in the different compartments of the inner ear. The answers will provide important insights into evolutionary and developmental processes in a sensory organ essential to many species, including humans.

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“…After all ear structures have formed, sound is transmitted through the tympanic hearing system in anurans similarly to the transmission of sound through comparable tympanic hearing systems across other eared tetrapods (reviewed in Christensen-Dalsgaard and Manley, 2013;Mason et al, 2015). The tympanum vibrates in response to airborne sound and transmits these vibrations to the columella.…”

Section: Introductionmentioning

confidence: 99%

Better late than never: effective air-borne hearing of toads delayed due to late maturation of the tympanic middle ear structures

Womack

Christensen‐Dalsgaard

Hoke

2016

Journal of Experimental Biology

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Most vertebrates have evolved a tympanic middle ear that enables effective hearing of airborne sound on land. Although inner ears develop during the tadpole stages of toads, tympanic middle ear structures are not complete until months after metamorphosis, potentially limiting the sensitivity of post-metamorphic juveniles to sounds in their environment. We tested the hearing of five species of toads to determine how delayed ear development impairs airborne auditory sensitivity. We performed auditory brainstem recordings to test the hearing of the toads and used micro-computed tomography and histology to relate the development of ear structures to hearing ability. We found a large (14-27 dB) increase in hearing sensitivity from 900 to 2500 Hz over the course of ear development. Thickening of the tympanic annulus cartilage and full ossification of the middle ear bone are associated with increased hearing ability in the final stages of ear maturation. Thus, juvenile toads are at a hearing disadvantage, at least in the high-frequency range, throughout much of their development, because late-forming ear elements are critical to middle ear function at these frequencies. We discuss the potential fitness consequences of late hearing development, although research directly addressing selective pressures on hearing sensitivity across ontogeny is lacking. Given that most vertebrate sensory systems function very early in life, toad tympanic hearing may be a sensory development anomaly.

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The Frog Inner Ear: Picture Perfect?

Cited by 19 publications

References 30 publications

The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura)

The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura)

Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear

Better late than never: effective air-borne hearing of toads delayed due to late maturation of the tympanic middle ear structures

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