The Malleable Middle Ear: An Underappreciated Player in the Evolution of Hearing in Vertebrates

Christensen‐Dalsgaard, Jakob; Manley, Geoffrey A.

doi:10.1007/2506_2013_33

Cited by 20 publications

(26 citation statements)

References 111 publications

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“…Christensen-Dalsgaard and Manley [2013] outlined a scenario with four stages of ear morphology leading to increased sensitivity of the nonmammalian ear prior to development of the tympanum, beginning with an early inner ear similar to the lungfish ear and sensitive to very low-frequency sound and substrate vibrations. Subsequently, high-frequency sensitivity of the inner ear could have been increased by reducing the mass of the otolith(s).…”

Section: The Transition Onto Land: Early Tetrapodsmentioning

confidence: 99%

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Walton

Christensen‐Dalsgaard

Carr

2017

Brain Behav Evol

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The earliest vertebrate ears likely subserved a gravistatic function for orientation in the aquatic environment. However, in addition to detecting acceleration created by the animal's own movements, the otolithic end organs that detect linear acceleration would have responded to particle movement created by external sources. The potential to identify and localize these external sources may have been a major selection force in the evolution of the early vertebrate ear and in the processing of sound in the central nervous system. The intrinsic physiological polarization of sensory hair cells on the otolith organs confers sensitivity to the direction of stimulation, including the direction of particle motion at auditory frequencies. In extant fishes, afferents from otolithic end organs encode the axis of particle motion, which is conveyed to the dorsal regions of first-order octaval nuclei. This directional information is further enhanced by bilateral computations in the medulla and the auditory midbrain. We propose that similar direction-sensitive neurons were present in the early aquatic tetrapods and that selection for sound localization in air acted upon preexisting brain stem circuits like those in fishes. With movement onto land, the early tetrapods may have retained some sensitivity to particle motion, transduced by bone conduction, and later acquired new auditory papillae and tympanic hearing. Tympanic hearing arose in parallel within each of the major tetrapod lineages and would have led to increased sensitivity to a broader frequency range and to modification of the preexisting circuitry for sound source localization.

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Section: The Transition Onto Land: Early Tetrapodsmentioning

confidence: 99%

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Walton

Christensen‐Dalsgaard

Carr

2017

Brain Behav Evol

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“…Mammals have three middle ear bones that could favor higher frequency sound conduction. These differences, plus a scenario where early mammals were small and possibly nocturnal, might therefore provide different selective strategies for the evolution of sound localization circuits in modern mammals and archosaurs [Christensen-Dalsgaard and Manley, 2013; Manley, 2012]. However, three middle ear ossicles are not essential for high frequency hearing, which has also appeared among the reptiles, notably the pygopod geckos [Manley and Kraus, 2010].…”

Section: Maps and Meters And The Evolution Of Sound Localizationmentioning

confidence: 99%

“…Tympanic hearing in mammals is yet another ‘experiment in hearing’, a novel origin of a tympanic ear [Christensen-Dalsgaard and Manley, 2013; Manley, 2010; Manley, 2012; Grothe and Pecka, 2014]. The mammalian middle ear originated through coupling of the middle ear bone to two other bones, first contacting the jaw through Meckel’s cartilage and later freed and evolving into a tympanic ear.…”

Section: Sound Localization Meters – Directional Hearing In Mammals Amentioning

confidence: 99%

“…Birds and crocodilians are sister groups among the extant archosaurs, while geckos are lepidosaurs. It is not clear whether or not these reptiles and birds share a common ancestor with a tympanic middle ear [Christensen-Dalsgaard and Manley, 2013; Clack, 2011]. Nevertheless, their central auditory pathways are very similar, suggesting their common ancestors may have been rudimentarily sensitive to airborne sound through bone conduction [Christensen et al, 2015; Lombard and Sumida, 1992].…”

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Sound Localization Strategies in Three Predators

Carr

Christensen‐Dalsgaard²

2015

Brain Behav Evol

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In this paper, we compare some of the neural strategies for sound localization and encoding interaural time differences (ITDs) in three predatory species of Reptilia, alligators, barn owls and geckos. Birds and crocodilians are sister groups among the extant archosaurs, while geckos are lepidosaurs. Despite the similar organization of their auditory systems, archosaurs and lizards use different strategies for encoding the ITDs that underlie localization of sound in azimuth. Barn owls encode ITD information using a place map, which is composed of neurons serving as labeled lines tuned for preferred spatial locations, while geckos may use a meter strategy or population code composed of broadly sensitive neurons that represent ITD via changes in the firing rate.

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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 Malleable Middle Ear: An Underappreciated Player in the Evolution of Hearing in Vertebrates

Cited by 20 publications

References 111 publications

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Sound Localization Strategies in Three Predators

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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