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Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing.

ABSTRACT: The auditory ossicles-malleus, incus and stapes-are the smallest bones in mammalian bodies and enable stable sound transmission to the inner ear. Sperm whales are one of the deepest diving aquatic mammals that produce and perceive sounds with extreme loudness greater than 180 dB and frequencies higher than 30 kHz. Therefore, it is of major interest to decipher the microstructural basis for these unparalleled hearing abilities. Using a suite of high-resolution imaging techniques, we reveal that auditory ossicles of sperm whales are highly functional, featuring an ultra-high matrix mineralization that is higher than their teeth. On a micro-morphological and cellular level, this was associated with osteonal structures and osteocyte lacunar occlusions through calcified nanospherites (i.e. micropetrosis), while the bones were characterized by a higher hardness compared to a vertebral bone of the same animals as well as to human auditory ossicles. We propose that the ultra-high mineralization facilitates the unique hearing ability of sperm whales. High matrix mineralization represents an evolutionary conserved or convergent adaptation to middle ear sound transmission.

SUBMITTER: Schmidt FN

PROVIDER: S-EPMC6304038 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing.

Schmidt Felix N FN Delsmann Maximilian M MM Mletzko Kathrin K Yorgan Timur A TA Hahn Michael M Siebert Ursula U Busse Björn B Oheim Ralf R Amling Michael M Rolvien Tim T

Proceedings. Biological sciences 20181201 1893

The auditory ossicles-malleus, incus and stapes-are the smallest bones in mammalian bodies and enable stable sound transmission to the inner ear. Sperm whales are one of the deepest diving aquatic mammals that produce and perceive sounds with extreme loudness greater than 180 dB and frequencies higher than 30 kHz. Therefore, it is of major interest to decipher the microstructural basis for these unparalleled hearing abilities. Using a suite of high-resolution imaging techniques, we reveal that a ...[more]

PMID: 30963901

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Project description:SignificanceMeasurements of auditory ossicles displacement are commonly carried out by means of laser-Doppler vibrometry (LDV), which is considered to be a gold standard. The limitation of the LDV method, especially for in vivo measurements, is the necessity to expose an object in a straight line to a laser beam operating from a distance. An alternative to this approach is the use of a handheld laser-fiber vibrometry probe (HLFVP) with a curved tip.AimWe evaluate the feasibility of an HLFVP with a curved tip for measuring sound-induced displacement of the auditory ossicles.ApproachA handheld vibrometer probe guiding the laser beam with a fiber-optic cable was used for displacement measurements of the incus body and the posterior crus of the stapes. Tonal stimuli at frequencies of 0.5, 1, 2, and 4 kHz were presented by means of an insert earphone positioned in the outer ear canal. The probe was fixed at the measurement site using a tripod or hand-held by one of the two surgeons.ResultsThe measurements were carried out on six fresh temporal bones. Multivariate analysis of variance showed statistically significant differences for stimulus frequency (F3,143 = 29.37, p < 0.001, and η2 = 0.35), bone (F5,143 = 4.61, p = 0.001, and η2 = 0.01), and measurement site (F1,143 = 4.74, p = 0.03, and η2 = 0.02) in the absence of statistically significant differences for the probe fixation method (F2,143 = 0.15, p = 0.862, and η2 = 0.001). Standard deviations of the means were 6.9, 2.6, 1.9, and 0.6 nm / Pa for frequency, bone, site, and fixation, respectively. Ear transfer functions were found to be consistent with literature data.ConclusionsThe feasibility of applying HLFVP to measure the displacement of auditory ossicles has been confirmed. HLFVP offers the possibility of carrying out measurements at various angles; however, this needs to be standardized taking into account anatomical limitations and surgical convenience.

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Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing.

Publications

Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing.

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