Abstract
It is widely thought that organisms detect sound by sensing the deflection of hair-like projections, the stereocilia, at the apex of hair cells. In the case of mammals, the standard interpretation is that hair cells in the cochlea respond to deflection of stereocilia induced by motion generated by a hydrodynamic travelling wave. But in the light of persistent anomalies, an alternative hypothesis seems to have some merit: that sensing cells (in particular the outer hair cells) may, at least at low intensities, be reacting to a different stimulus — the rapid pressure wave that sweeps through the cochlear fluids at the speed of sound in water. This would explain why fast responses are sometimes seen before the peak of the travelling wave. Yet how could cells directly sense fluid pressure? Here, a model is constructed of the outer hair cell as a pressure vessel able to sense pressure variations across its cuticular pore, and this ‘fontanelle’ model, based on the sensing action of the basal body at this compliant spot, could explain the observed anomalies. Moreover, the fontanelle model can be applied to a wide range of other organisms, suggesting that direct pressure detection is a general mode of sensing complementary to stereociliar displacement.
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References
Afzelius B A 1983 Basal bodies in the immotile-cilia syndrome; J. Submicrosc. Cytol. 15 111–114
Albrecht-Buehler G 1992 Function and formation of centrioles and basal bodies; in The centrosome (ed) V I Kalnins (San Diego: Academic Press) pp 69–102
Alkon D L 1983a The role of statocyst sensory cilia in mechanotransduction; J. Submicrosc. Cytol. 15 145–150
Alkon D L 1983b Sensory function of cilia; J. Submicrosc. Cytol. 15 173–176
Allen J B 2001 Nonlinear cochlear signal processing; in: Physiology of the ear (eds) A F Jahn and J Santos-Sacchi (San Diego, CA: Singular Thomson Learning) (2nd edition), pp 393–442
Békésy G v 1960 Experiments in hearing (New York: McGraw-Hill)
Békésy G v 1967 Some similarities in sensory perception of fish and man; in Lateral line detectors (ed.) P H Cahn (Bloomington: Indiana University Press) pp 417–435
Bell A 2003 Are outer hair cells pressure sensors? Basis of a SAW model of the cochlear amplifier; in Biophysics of the cochlea: from molecules to models (ed.) A W Gummer (Singapore: World Scientific) pp 429–431
Bell A 2004 Hearing: travelling wave or resonance? PLoS Biol. 2 e337
Bell A 2004 Resonance theories of hearing: a history and a fresh approach; Acoustics Australia 32 108–113
Bell A 2005 The underwater piano: a resonance theory of cochlear mechanics, Ph.D. thesis, Australian National University, Canberra, Australia
Bell A 2006 Sensors, motors, and tuning in the cochlea: interacting cells could form a surface acoustic wave resonator; Bioinsp. Biomim. 1 96–101
Bell A 2007 Tuning the cochlea: wave-mediated positive feedback between cells; Biol. Cybern. DOI 10.1007/s00422-006-0134-0
Bell A and Fletcher N H 2004 The cochlear amplifier as a standing wave: “squirting” waves between rows of outer hair cells? J. Acoust. Soc. Am. 116 1016–1024
Bornens M 1979 The centriole as a gyroscopic oscillator. Implications for cell organization and some other consequences; Biol. Cellulaire 35 115–132
Brinkley B R and Stubblefield E 1970 Ultrastructure and interaction of the kinetochore and centriole in mitosis and meiosis; Adv. Cell Biol. 1 119–185
Brownell W E 1986 Outer hair cell motility and cochlear frequency selectivity; in Auditory frequency selectivity (eds) B C J Moore and R D Patterson (New York: Plenum)
Brownell W E 1990 Outer hair cell electromotility and otoacoustic emissions; Ear Hear. 11 82–92
Brownell W E 1998 How the ear works: Nature’s solutions for listening; Volta Rev. 99 9–28
Brownell W E 2002 On the origins of the outer hair cell electromotility; in Hair cell micromechanics and otoacoustic emission (eds) C I Berlin, L J Hood and A Ricci (Clifton Park, NY: Delmar Learning / Singular Publishing) pp 25–47
Brownell W E and Popel A S 1998 Electrical and mechanical anatomy of the outer hair cell; in Psychophysical and physiological advances in hearing (eds) A R Palmer, A Rees, A Q Summerfield and R Meddis (London: Whurr) pp 89–96
Brownell W E and Shehata W E 1990 The effect of cytoplasmic turgor pressure on the static and dynamic mechanical properties of outer hair cells; in Mechanics and biophysics of hearing (eds) P Dallos, C D Geisler, J W Matthews, M A Ruggero and C R Steele (Berlin: Springer) pp 52–59
Corwin J T 1977 Morphology of the macula neglecta in sharks of the genus Carcharinus; J. Morphol. 152 341–362
Corwin J T 1981a Audition in elasmobranchs; in Hearing and sound communication in fishes (eds) W N Tavolga, A N Popper and R R Fay (New York: Springer) pp 81–105
Corwin J T 1981b Peripheral auditory physiology in the lemon shark: evidence of parallel otolithic and non-otolithic sound detection; J. Comp. Physiol. 142 379–390
Dallos P 1996 Overview: cochlear neurobiology; in The cochlea (eds) P Dallos, A N Popper and R R Fay (New York: Springer), 1–43
Davis H, Derbyshire A J, Lurie M H and Saul L J 1934 The electric response of the cochlea; Am. J. Physiol. 107 311–332
de Boer E and Nuttall A L 2003 Properties of amplifying elements in the cochlea; in Biophysics of the cochlea: from molecules to models (ed.) A W Gummer (Singapore: World Scientific) pp 331–342
Dieler R, Shehata-Dieler W E and Brownell W E 1991 Concomitant salicylate-induced alterations of outer hair cell subsurface cisternae and electromotility; J. Neurocytol. 20 637–653
Dorn E 1961 Über den Feinbau der Swimmblase von Anguilla vulgaris L; Z. Zellforsch. 55 849–912
Engström H 1955 Morphological studies on the possible origin of cochlear microphonics; Rev. Laryngol. Otol. Rhinol. (Bord). 76 808–816
Engström H and Ades H W 1973 The ultrastructure of the organ of Corti; in The ultrastructure of sensory organs (ed.) I Friedman (Amsterdam: North-Holland) pp 83–151
Engström H, Ades H W and Hawkins J E 1962 Structure and functions of the sensory hairs of the inner ear; J. Acoust. Soc. Am. 34 1356–1363
Engström H and Wersäll J 1958 The ultrastructural organization of the organ of Corti and of the vestibular sensory epithelia; Exp. Cell Res. Suppl. 5 460–492
Ewing A W 1989 Arthropod bioacoustics: neurobiology and behaviour (Edinburgh: Edinburgh University Press)
Fänge R 1953 The mechanisms of gas transport in the euphysoclist swimbladder; Acta Physiol. Scand. Suppl. 110 1–133
Fänge R 1966 Physiology of the swimbladder; Physiol. Rev. 46 299–322
Fex J 1974 Neural excitatory processes of the inner ear; in Handbook of sensory physiology (eds) W D Keidel and W D Neff (Berlin: Springer) vol 5.1 pp 585–646
Fletcher N H 1992 Acoustic systems in biology (New York: Oxford University Press)
Flock Å 1971 Sensory transduction in hair cells; in Handbook of sensory physiology (ed) W R Loewenstein (Berlin: Springer) vol. 5.1, pp 396–441
Flock Å, Kimura R S, Lundquist P-G and Wersäll J 1962 Morphological basis of directional sensitivity of the outer hair cells in the organ of Corti; J. Acoust. Soc. Am. 34 1351–1355
Forge A, Zajic G, Li L, Nevill G and Schacht J 1993 Structural variability of the sub-surface cisternae in intact, isolated outer hair cells shown by fluorescent labelling of intracellular membranes and freeze-fracture; Hear. Res. 64 175–183
Gray E G and Pumphrey R J 1958 Ultra-structure of the insect ear; Nature (London) 181 618
Guild S R 1937 Comments on the physiology of hearing and the anatomy of the inner ear; Laryngoscope 47 365–372
Guinan J J, Lin T and Cheng H 2005 Medial-olivocochlear-efferent inhibition of the first peak of auditory-nerve responses: evidence for a new motion within the cochlea; J. Acoust. Soc. Am. 118 2421–2433
Harada Y, Tagashira N, Takunida M, Suzuki M, Nagasawa A and Sakai T 1990 Three-dimensional ultrastructure of cochlea: a review; in Inner ear pathobiology (Adv. Otorhinolaryngol. v. 45) (eds) M Ciges and A Campos (Basel: Karger) pp 49–68
Hawkins J E 1965 Cytoarchitectural basis of the cochlear transducer; Symp. Quant. Biol. 30 147–157
Hawkins J E 1976 Drug ototoxicity; in Handbook of sensory physiology (eds) W D Keidel and W D Neff (Berlin: Springer) vol. 5.3 pp 707–748
Helmholtz H L F v 1874 The mechanism of the ossicles and the membrana tympani (translated by J Hinton) (London: New Sydenham Society)
Helmholtz H L F v 1875 On the sensations of tone as a physiological basis for the theory of music (London: Longmans, Green)
Higgs D M 2004 Neuroethology and sensory ecology of teleost ultrasound detection; in The senses of fish (eds) G von der Emde, J Mogdans and B G Kapoor (Boston, MA: Kluwer) pp 173–188
Hillman D E 1969 New ultrastructural findings regarding a vestibular ciliary apparatus and its possible functional significance; Brain Res. 13 407–412
Hillman D E and Lewis E R 1971 Morphological basis for a mechanical linkage in otolithic receptor transduction in the frog; Science 174 416–419
Hudspeth A J 1997 How hearing happens; Neuron 19 947–950
Hudspeth A J 2000 Hearing; in Principles of neural science (eds) E R Kandel, J H Schwartz and T M Jessell (New York: McGraw-Hill) 4th edition, pp 590–613
Hudspeth A J and Corey D P 1977 Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli; Proc. Natl. Acad. Sci. USA 74 2407–2411
Ikeda K and Takasaka T 1993 Confocal laser microscopical images of calcium distribution and intracellular organelles in the outer hair cell isolated from the guinea pig cochlea; Hear. Res. 66 169–176
Iwasa K H and Chadwick R S 1992 Elasticity and active force generation of cochlear outer hair cells; J. Acoust. Soc. Am. 92 3169–3173
Kalmijn A J 1988a Hydrodynamic and acoustic field detection; in Sensory biology of aquatic animals (eds) J Atema, R R Fay, A N Popper and W N Tavolga (New York: Springer) pp 83–130
Kalmijn A J 1988b Detection of weak electric fields; in Sensory biology of aquatic animals (eds) J Atema, R R Fay, A N Popper and W N Tavolga (New York: Springer) pp 151–186
Kalmijn A J 2000 Detection and processing of electromagnetic and near-field acoustic stimuli in elasmobranch fishes; Philos. Trans. R. Soc. London B355 1135–1141
Kharakoz D P 2000 Protein compressibility, dynamics, and pressure; Biophys. J. 79 511–525
Lavigne-Rebillard M and Pujol R 1986 Development of the auditory hair cell surface in human fetuses; Anat. Embryol. 174 369–377
Leighton T G 2004 From seas to surgeries, from babbling brooks to baby scans: the acoustics of gas bubbles in liquids; Int. J. Modern Phys. B18 3267–3314
Leonova E V and Y Raphael 1998 Alteration of membranous structures in ototoxically damaged outer hair cells of the organ of Corti (Midwinter Meeting, Florida, Association for Research in Otolaryngology)
Lewis E R, Leverenz E L and Bialek W S 1985 The vertebrate inner ear (Boca Raton, FL: CRC Press)
Lim D J 1986 Functional structure of the organ of Corti: a review; Hear. Res. 22 117–146
Lowenstein O and Wersäll J 1959 A functional interpretation of the electron-microscopic structure of the sensory hairs in the cristæ of the elasmobranch Raja clavata in terms of directional sensitivity; Nature (London) 184 1807–1808
Macdonald A G and Fraser P J 1999 The transduction of very small hydrostatic pressures; Comp. Biochem. Physiol. A 122 13–36
Magariyama Y, Sugiyama S, Muramoto K, et al 1994 Very fast flagellar rotation; Nature (London) 371 752
Mammano F, Frolenkov G I, Lagostena L, et al 1999 ATP-induced Ca2+ release in cochlear outer hair cells: localization of an isositol triphosphate-gated Ca2+ store to the base of the sensory hair bundle; J. Neurosci. 19 6918–6929
Meyer J, Mack A F and Gummer A W 2001 Pronounced infracuticular endocytosis in mammalian outer hair cells; Hear. Res. 161 10–22
Moran D T and Varela F G 1971 Microtubules and sensory transduction; Proc. Natl. Acad. Sci. USA 68 757–760
Morris C E 2001 Mechanosensitive ion channels in eukaryotic cells; in Cell physiology sourcebook: a molecular approach (ed.) N Sperelakis (New York: Academic Press) 3rd edition pp 745–760
Morse P M 1991 Vibration and sound (New York: Acoustical Society of America)
Mouritsen O G 2005 Life: as a matter of fat (Berlin: Springer)
Myrberg A A 2001 The acoustical biology of elasmobranchs; Environ. Biol. Fishes 60 31–45
Namba K and Vonderviszt F 1997 Molecular architecture of bacterial flagellum; Q. Rev. Biophys. 30 1–65
Nevenzel J C, Rodegker W, Mead J F and Gordon M S 1966 Lipids of the living coelacanth, Latimeria chalumnae; Science 152 1753–1755
Nevenzel J C, Rodegker W, Robinson J S and Kayama M 1969 The lipids of some lantern fishes (family Myctophidae); Comp. Biochem. Physiol. 31 25–36
Nielsen J G and Munk O 1964 A hadal fish (Bassogigas profundissimus) with a functional swimbladder; Nature (London) 204 594–595
Pelster B 1995 Metabolism of the swimbladder tissue; in Biochemistry and molecular biology of fishes (eds) P W Hochachka and T P Mommsen (Amsterdam: Elsevier) Vol. 4 pp 101–118
Phleger C F 1991 Biochemical aspects of buoyancy in fishes; in Biochemistry and molecular biology of fishes (eds) P W Hochachka and T P Mommsen (Amsterdam: Elsevier) vol. 1 pp 209–247
Pohlman A G 1933 A reconsideration of the mechanics of the auditory apparatus; J. Laryngol. Otol. 48 156–195
Pollice P A and W E Brownell 1993 Characterization of the outer hair cell’s lateral wall membrane; Hear. Res. 70 187–196
Pujol R, Lenoir M, Ladrech S, Tribillac F and Rebillard G 1992 Correlation between the length of outer hair cells and the frequency coding of the cochlea; in Auditory physiology and perception (Advances in the biosciences volume 83) (eds) Y Cazals, L Demany and K Horner (Oxford: Pergamon) pp 45–51
Pumphrey R J 1950 Hearing; Symp. Soc. Exp. Biol. 4 3–18
Ratnanather J T, Brownell W E and Popel A S 1993 Mechanical properties of the outer hair cell; in Biophysics of hair cell sensory systems (eds) H Duifhuis, J W Horst, P van Dijk and S M van Netten (Singapore: World Scientific) pp 199–206
Ren T 2004 Reverse propagation of sound in the gerbil cochlea; Nat. Neurosci. 7 333–334
Ren T and Nuttall A L 2006 Cochlear compression wave: an implication of the Allen-Fahey experiment; J. Acoust. Soc. Am. 119 1940–1942
Rogers P H and Cox M 1988 Underwater sound as a biological stimulus; in Sensory biology of aquatic animals (eds) J Atema, R R Fay, A N Popper and W N Tavolga (New York: Springer) pp 131–149
Rossing T D and Fletcher N H 1995 Principles of vibration and sound (New York: Springer)
Saito K 1983 Fine structure of the sensory epithelium of guinea-pig organ of Corti: subsurface cisternae and lamellar bodies in the outer hair cells; Cell Tissue Res. 229 467–481
Schacht J and Zenner H P 1987 Evidence that phosphoinositides mediate motility in cochlear outer hair cells; Hear. Res. 31 155–160
Schliwa M 1992 Cell polarity and centrosomes; in The centrosome (ed.) V I Kalnins (San Diego: Academic) pp 331–351
Shera C A 2001 Intensity-invariance of fine-structure in basilar-membrane click responses: implications for cochlear mechanics; J. Acoust. Soc. Am. 110 332–348
Sobkowicz H M, Slapnick S M and August B K 1995 The kinocilium of auditory hair cells and evidence for its morphogenetic role during the regeneration of stereocilia and cuticular plates; J. Neurocytol. 24 633–653
Sowa Y, Rowe A D, Leake M C, et al 2005 Direct observation of steps in rotation of the bacterial flagellar motor; Nature (London) 437 916–919
Spicer S S, Thomopoulos G N and Schulte B A 1998 Cytologic evidence for mechanisms of K+ transport and genesis of Hensen bodies and subsurface cisternae in outer hair cells; Anat. Rec. 251 97–113
Steele C R 1990 Elastic behaviour of the outer hair cell wall; in Mechanics and biophysics of hearing (eds) P Dallos, C D Geisler, J W Matthews, M A Ruggero and C R Steele (Berlin: Springer) pp 76–83
Stewart M J 2003 Contrast echocardiography; Heart 89 342–348
Steyger P S, Furness D N, Hackney C M and Richardson G P 1989 Tubulin and microtubules in cochlear hair cells: comparative immunocytochemistry and ultrastructure; Hear. Res. 42 1–16
Tardent P and Schmid V 1972 Ultrastructure of mechanoreceptors of the polyp Coryne pintneri (Hydrozoa, Athecata); Exp. Cell Res. 72 265–275
Tavolga W N 1981 Retrospect and prospect: listening through a wet filter; in Hearing and sound communication in fishes (eds) W N Tavolga, A N Popper and R R Fay (New York: Springer) pp 573–587
Thomas D R, Morgan D G and Derosier D J 1999 Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor; Proc. Natl. Acad. Sci. USA 96 10134–10139
Thurm U, Erler G, Godde J, Kastrup H, Keil T, Volker W and Vohwinkel B 1983 Cilia specialized for mechanoreception; J. Submicrosc. Cytol. 15 151–155
van Bergeijk W A 1964 Directional and nondirectional hearing in fish; in Marine bio-acoustics (ed) W N Tavolga (Oxford: Pergamon), vol. 1, pp 281–299
van den Berg A V and Schuijf A 1983 Discrimination of sounds based on the phase difference between particle motion and acoustic pressure in the shark Chiloscyllium griseum; Proc. Roy. Soc. London B 218 127–134
Vogel S 2003 Comparative biomechanics (Princeton: Princeton University Press)
Wartzok D and Ketten D R 1999 Marine mammal sensory systems; in Biology of marine mammals (eds) J E Reynolds and S A Rommel (Washington: Smithsonian) pp 117–175
Wersäll J, Flock Å and Lundquist P-G 1965 Structural basis for directional sensitivity in cochlear and vestibular sensory receptors; Symp. Quant. Biol. 30 115–132
Wersäll J and Lundquist P-G 1966 Morphological polarization of the mechanoreceptors of the vestibular and acoustic systems; Second symposium on the role of the vestibular organs in space exploration (Washington, DC: NASA), SP-115, pp 57–72
Wever E G 1978 The reptile ear (Princeton: Princeton University Press)
Wheatley D N 1982 The centriole: a central enigma of cell biology (Amsterdam: Elsevier)
Wheatley D N 2005 Landmarks in the first hundred years of primary (9+0) cilium research; Cell Biol. Int. 29 333–339
Wiederhold M L 1976 Mechanosensory transduction in “sensory” and “motile” cilia; Annu. Rev. Biophys. Bioeng. 5 39–62
Wittenberg J B 1958 The secretion of inert gas into the swimbladder of fish; J. Gen. Physiol. 41 783–804
Zakon H H 1988 The electroreceptors: diversity in structure and function; in Sensory biology of aquatic animals (eds) J Atema, R R Fay, A N Popper and W N Tavolga (New York: Springer) pp 813–850
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Bell, A. Detection without deflection? A hypothesis for direct sensing of sound pressure by hair cells. J Biosci 32, 385–404 (2007). https://doi.org/10.1007/s12038-007-0037-9
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DOI: https://doi.org/10.1007/s12038-007-0037-9


