Humans can hear from 20 Hz to about 20 kHz, yet previous reports of middle-ear motion have consistently showed that the transmission of sound through the middle ear seems to not reach such high frequencies1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11. Measurements of stapes motion, the cochlear input in human cadaveric specimens, suggest that the middle ear is not capable of transmitting appreciable sounds above 4 kHz, but these sounds are certainly heard by human subjects. This apparent discrepancy between sound transmission and sound perception has been a mystery in the field of hearing research for decades.
Knowledge about middle-ear function in human has relied on experiments in fresh human cadaveric specimens. The use of such specimens has also revolutionized our understanding of middle-ear pathology, reconstruction, and design of prostheses3, 12, 13. Because middle-ear motion in fresh cadaveric specimens is similar to the live ear up to about 3 kHz, stapes motion, the input to the cochlea, is often used as a proxy for hearing13, 14, 15, 16. However, the relationship between stapes velocity measurements and hearing has not been established for frequencies above about 4 kHz – frequencies important for speech perception and sound localization17.
The link between stapes velocity and hearing in human is generally accepted, especially below 3 kHz where robust stapes velocity measurements have been reported. A standard for stapes velocity was established based on several published studies (Fig. 1a), becoming the American Society for Testing and Material (ASTM) international consensus standard7. This standard shows a decrease in stapes velocity above 1 kHz (Fig. 1a) of about 20 dB per decade. When inverted to show sound threshold for a specific stapes velocity, this threshold of stapes velocity can be compared with the threshold of hearing. Sound thresholds for stapes velocity versus frequency has a similar shape as the human threshold of hearing below ~ 2.5 kHz (Fig. 1b).
At higher frequencies this similarity of threshold shape between stapes velocity and hearing does not hold; human hearing is better above ~ 2.5 kHz than would be predicted by stapes velocity. The hearing threshold (green curve) in Fig. 1b is lower than the stapes velocity threshold (black curve). Somehow human hearing is more sensitive at high frequencies than what measurements of stapes motion seem to indicate.
Although past studies have attempted to explain this discrepancy between human stapes motion and hearing ability at high frequencies, there has been no satisfactory explanation. It is a difficult problem with several parts:
(1) Do stapes velocity measurements represent cochlear input? Piston motion of the stapes at the oval window is considered the effective input to the cochlea. However, one-dimensional (1D) stapes velocity is usually measured with laser Doppler velocimeter (LDV) at one point on the stapes posterior crus or footplate with 45–60 degree angle relative to the piston direction (Fig. 2a). Here we refer to the 1D measurement as Stapes Typical.
(2) Stapes motion is known to be complex, with varying modes of motion above a few kHz. Can non-piston stapes motion at high frequencies, such as rocking motion (Fig. 2a), contribute to cochlear input? Studies have tried to answer this question, but results were inconclusive4, 16, 18, 19.
(3) Is it possible that standard clinical surgical methods to access the middle ear (also used to prepare fresh cadaveric temporal bone for experimentation) result in loosening the ossicular chain? A study that intentionally loosened the ossicular joints showed a reduction in high-frequency middle-ear sound transmission20.
To address the questions above, we measure high-frequency stapes motion in the piston direction. Additionally, we determine sound transmission into the cochlea at high frequencies by measuring the motion of the cochlear partition. To do this, we used novel techniques in six fresh human cadaveric specimens:
(1) We determine Stapes Piston velocity for a wide range of frequencies. As shown in Fig. 2b, we use a 3D LDV to measure stapes velocity along three axes simultaneously, then use coordinate transformation to compute Stapes Piston velocity.
(2) We determine sound transmission to the cochlea. While measuring Stapes Typical with 1D LDV (Fig. 2a), we simultaneously measure Cochlear Partition motion in situ in an intact cochlea with optical coherence tomography (OCT) vibrometry. This determines the correspondence between motion of the stapes and cochlear partition and whether high-frequency sound is transmitted to the cochlea.
(3) We modify surgical preparation of our specimens to minimize contact with or displacement of the ossicular chain to prevent loosening of the ossicular chain.
Measurements of stapes motion above 4 kHz as an input reference to cochlear response measurements have both great scientific and clinical utility. Robust high-frequency stapes velocity measurements also pave a path to test new implantable prostheses targeted to improving frequencies important in speech perception, sound transmission during surgery, and many other valuable applications21, 22. Moreover, we report human cochlear partition motion in situ through an intact round-window membrane with OCT for a wide frequency range.