151st ASA Meeting, Providence, RI
A Second Pair of Ears
Martin L. Lenhardt - lenhardt@vcu.edu
Popular version of paper 5aABa10
"Hey, four eyes!" I remember that expression from my elementary school days. Of course, I didn't actually have four eyes. Our ears are another story. Superficially there are two but each houses two organs, one exclusively auditory and another generally vestibular, that is, maintaining our balance, but secondarily can be stimulated with sound under the proper conditions. One of the vestibular organs, the saccule, serves as an auditory receptor in fish, amphibians and reptiles. The feature that makes otolith organs distinct is that most of its hair cells are embedded in a layer of gel on which lie little "rocks" of calcium carbonate. Otolith organs act as tiny mass/spring acceleration sensors, detecting motion or vibration. In the course of evolution, transitioning from living a watery medium to a terrestrial one, could mammals have retained this primitive hearing ability in their saccules? There have been reports that the saccule does indeed serve some auditory function, but our awareness of it is masked by the dominant role of the much more sensitive cochlea in human auditory perception. The saccule is situated very close to the stapes, the final middle ear bone which links the sound-pressure-induced vibration of the eardrum with the displacement of fluid in the inner ear. Since fluid is incompressible, the inner ear has two membranes or windows that stretch to allow fluid movement. The footplate is inserted in one, the oval window and the second, the round window, moves out of phase as a pressure-release mechanism. With moderate sound pressures at the eardrum, the saccule is not affected; however at high sound pressures the saccule is stimulated which can account for complaints of disorientation with high intensity exposure. Sound pressures in excess of 100 dB SPL are required to activate the saccule leading to the intriguing hypothesis (advanced by Todd et al.) that rock music is intense in order to stimulate these old reptilian ears of ours. When a surgical window is created in the vestibular system, specifically in the wall of one of the three semicircular canals, these organs respond vigorously to vibration. Amazingly, deaf subjects with such surgical windows are able to detect sound delivered as bone conduction vibration to the head at levels approaching the lower limits of normal hearing. Drawbacks include some imbalance but far more importantly there was a complete lack of any speech understanding since the canals are not wired to the auditory parts of the brain. The saccule is different; for it, such auditory brain connections do exist. An alternative approach to fenestration (creating a new window) is to extend the middle ear system such that the part of the stapes (a bone in the middle ear) is directly coupled to the wall of the saccule. That approach has already been tested in nature by various species of turtles for well over 200 million years. Turtles have fibroelastic strands that attach the middle ear bone to the saccular wall, thus displacement of the eardrum drives both the saccule and the cochlea. It is unclear if these strands existed in stem reptiles to help them as they slither close to or on surfaces or if the strands represent a specific adaptation to life in a shell, since vibratory stimulation of the shell activates the ear by bone conduction even when the head is retracted. Silicone struts, modeled to biomechanically mimic turtle strands, were developed. Struts are extruded through holes drilled in the stapes footplate to make contact with the saccular wall a mere 1.5 mm away. This human otosurgery has yet to be performed but success with related saccular surgery is encouraging. The human saccule is thought to respond maximally around 300 Hz with an upper range of about 1000 Hz, a range that overlaps with turtle audiograms. In the case of deafness, speech cues as the fundamental frequency, the first formant and prosodic features can be readily amplified and delivered into the ear canal through the use a stand alone saccular hearing aid or in conjunction with a cochlear implant. This procedure can also serve as a supplement to an audible ultrasonic hearing aid for the deaf. Ultrasound (~20-100 kHz) is audible by fluid or bone conduction, even in some deaf individuals with vestibular function. In 1934 Max Brodel of Johns Hopkins University depicted the so-called nerve of Oort in one of his famous drawings. This is a branch of the main saccular nerve which jointly innervates the cochlea (with the auditory nerve) but just in the region associated with ultrasonic pitch. Brain imaging indicates ultrasound activates the auditory cortex, likely via both cochlear and saccular stimulation in normal hearing listeners but probably only by the saccule in the case of complete deafness. Fitted with an ultrasonic hearing aid which modulates speech, deafened listeners can obtain intelligibility on the order of 50% with practice, presumably through saccular mediation. Integrating vibrotactile speech cues along with ultrasonic speech should further increase functionality; but that's something that needs to be tested and confirmed. The auditory aspect of the human saccule has been elusive, co-existing in the shadow of the much more powerful cochlea, but its hidden role in hearing is slowly but steadily being realized. With this novel bioinspired engineered technology, that freedom may come a little easier, thanks to turtles. References Lenhardt, M.L., Stapedial-saccular strut and method, U.S. patent #6,368,267. Lenhardt M.L., Eardrum saccule coupling; novel form of hearing. In: Vossoughi J (ed.) Biomedical Engineering: Recent Developments. Washington, DC: Medical and Engineering Publishers, 2002, pp. 51- 52. Lenhardt, M.L., Skellett, R., Wang, P. and Clarke, A.M.: Human Ultrasonic Speech Perception. Science, 253, 1991, 82-85. Todd, N.P.M. and Cody, F.W., Vestibular responses to loud dance music: A physiological basis of the "rock and roll threshold"? J. Acoust. Soc. Am. 107, 2000, 496-500.
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