REVIEW PAPER
REPTILE EARS AND MAMMALIAN EARS: HEARING WITHOUT A TRAVELLING WAVE
Andrew Bell 1  
 
More details
Hide details
1
Eccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, ACT 0200, Australia
CORRESPONDING AUTHOR
Andrew Bell   

Andrew Bell, e-mail: andrew.bell@anu.edu.au
Publication date: 2012-09-30
 
J Hear Sci 2012;2(3):14–22
 
ABSTRACT
This paper takes a closer look at the functional similarities between reptile ears and mammalian ears. The ears of the first class of animal are generally acknowledged to lack travelling waves – because the sensing cells sit upon a stiff support – whereas the ears of the second group are commonly thought to act differently, having hair cells arranged upon a compliant basilar membrane that moves under the action of a travelling wave (created by a pressure difference across the membrane) so that the wave bends the cells’ stereocilia. However, recent work suggests that the mammalian case can be explained without reliance upon a travelling wave as a causal stimulus and that the responses observed can be interpreted as local resonances driven by a fast pressure wave. In this light, reptiles and mammals may have more in common than currently appreciated – they might both be forced resonant systems – and this paper explores such a possibility.
 
REFERENCES (58)
1.
Bergevin C, Shera CA: Coherent reflection without traveling waves: on the origin of long-latency otoacoustic emissions in lizards. J Acoust Soc Am, 2010; 127: 2398–409.
 
2.
Ruggero MA, Temchin AN: Similarity of traveling-wave delays in the hearing organs of humans and other tetrapods. J Assoc Res Otolaryngol, 2007; 8: 153–66.
 
3.
Meenderink SWF, Narins PM: Stimulus frequency otoacoustic emissions in the Northern leopard frog, Rana pipiens pipiens: implications for inner ear mechanics. Hear Res, 2006; 220: 67–75.
 
4.
Manley GA, Yates GK, Koeppl C: Auditory peripheral tuning: evidence for a simple resonance phenomenon in the lizard Tiliqua. Hear Res, 1988; 33: 181–90.
 
5.
Peake WT, Ling A: Basilar-membrane motion in the alligator lizard: its relation to tonotopic organization and frequency selectivity. J Acoust Soc Am, 1980; 67: 1736–45.
 
6.
Wever EG: The Reptile Ear. Princeton: Princeton University Press, 1978.
 
7.
Manley GA: Peripheral Hearing Mechanisms in Reptiles and Birds. New York, Springer-Verlag, 1990.
 
8.
Bell A: A resonance approach to cochlear mechanics. PLOS One. 2012; (in press).
 
9.
Miller MR: Scanning electron microscopy of the lizard papilla basilaris. Brain, Behaviour and Evolution, 1974; 10: 95–112.
 
10.
Bell A: Sensors, motors, and tuning in the cochlea: interacting cells could form a surface acoustic wave resonator. Bioinsp Biomim, 2006; 1: 96–101.
 
11.
Bell A, Fletcher NH: The cochlear amplifier as a standing wave: “squirting” waves between rows of outer hair cells? J Acoust Soc Am, 2004; 116: 1016–24.
 
12.
Bergevin C, Velenovsky DS, Bonine KE: Tectorial membrane morphological variation: effects upon stimulus frequency otoacoustic emissions. Biophys J, 2010; 99: 1064–72.
 
13.
Bergevin C: Comparison of otoacoustic emissions within Gecko subfamilies: morphological implications for auditory function in lizards. J Assoc Res Otolaryngol, 2011; 12: 203–17.
 
14.
He W, Fridberger A, Porsov E et al: Reverse wave propagation in the cochlea. Proc Nat Acad Sci, 2008; 105: 2729–33.
 
15.
Wilson JP: Model for cochlear echoes and tinnitus based on an observed electrical correlate. Hear Res, 1980; 2: 527–32.
 
16.
de Boer E, Nuttall AL: Inverse-solution method for a class of non-classical cochlear models. J Acoust Soc Am, 2009; 125: 2146–54.
 
17.
Ruggero MA, Temchin AN: Unexceptional sharpness of frequency tuning in the human cochlea. Proc Nat Acad Sci USA, 2005; 102: 18614–19.
 
18.
Dong W, Olson ES: Supporting evidence for reverse cochlear travelling waves. J Acoust Soc Am, 2008; 123: 222–40.
 
19.
de Boer E, Zheng J, Porsov E, Nuttall AL: Inverted direction of wave propagation (IDWP) in the cochlea. J Acoust Soc Am, 2008; 123: 1513–21.
 
20.
Bell JA: The Underwater Piano: A Resonance Theory of Cochlear Mechanics. PhD thesis, Australian National University, Canberra, 2005. Available at http://hdl.handle.net/1885/493....
 
21.
Bell A: Hearing: travelling wave or resonance? PLoS Biology, 2004; 2: e337.
 
22.
Patuzzi RB: Cochlear micromechanics and macromechanics. In: Dallos P, Popper AN, Fay RR (eds.), The Cochlea. New York, Springer, 1996; 186–257.
 
23.
Bell A: Detection without deflection? A hypothesis for direct sensing of sound pressure by hair cells. J Biosci, 2007; 32: 385–404.
 
24.
Bell A: The pipe and the pinwheel: is pressure an effective stimulus for the 9+0 primary cilium? Cell Biol Int, 2008; 32: 462–68.
 
25.
Bell A: Are outer hair cells pressure sensors? Basis of a SAW model of the cochlear amplifier. In: Gummer AW (ed.), Biophysics of the Cochlea: From Molecules to Models. Singapore: World Scientific, 2003; 429–31.
 
26.
Bell A: Tuning the cochlea: wave-mediated positive feedback between cells. Biol Cybern, 2007; 96: 421–38.
 
27.
Narayan SS, Temchin AN, Recio A, Ruggero MA: Frequency tuning of basilar membrane and auditory nerve fibers in the same cochlea. Science, 1998; 282: 1882–84.
 
28.
Shera CA, Guinan JJ: Stimulus-frequency-emission group delay: a test of coherent reflection filtering and a window on cochlear tuning. J Acoust Soc Am, 2003; 113: 2762–72.
 
29.
Shera CA, Guinan JJ, Oxenham AJ: Revised estimates of human cochlear tuning from otoacoustic and behavioral measurements. Proc Nat Acad Sci, 2002; 99: 3318–23.
 
30.
Greenwood DD: Critical bandwidth and the frequency coordinates of the basilar membrane. J Acoust Soc Am, 1961; 33: 1344–56.
 
31.
Sisto R, Moleti A, Botti T, Bertaccini D, Shera CA: Distortion products and backward-traveling waves in nonlinear active models of the cochlea. J Acoust Soc Am, 2011; 129: 3141–52.
 
32.
Neely ST, Norton SJ, Gorga MP, Jesteadt W: Latency of auditory brain-stem responses and otoacoustic emissions using tone-burst stimuli. J Acoust Soc Am, 1988; 83: 652–56.
 
33.
Moleti A, Sisto R: Comparison between otoacoustic and auditory brainstem response latencies supports backward propagation of otoacoustic emissions. J Acoust Soc Am, 2008; 123: 1495–503.
 
34.
Shera CA: Mammalian spontaneous otoacoustic emissions are amplitude-stabilized cochlear standing waves. J Acoust Soc Am, 2003; 114: 244–62.
 
35.
Ren T: Reverse propagation of sound in the gerbil cochlea. Nat Neurosci, 2004; 7: 333–34.
 
36.
Meenderink S, Van der Heijden M: Reverse propagation in the intact cochlea of the gerbil: evidence for slow traveling waves. J Neurophysiol, 2010; 103: 1448–55.
 
37.
Ren T, Porsov E: Reverse propagation of sounds in the intact cochlea (letter). J Neurophysiol, 2010; 104: 3732.
 
38.
Shera CA, Tubis A, Talmadge CL: Do forward- and backwardtraveling waves occur within the cochlea? Countering the critique of Nobili et al. J Assoc Res Otolaryngol, 2004; 5: 349–59.
 
39.
Shera CA, Tubis A, Talmadge CL et al: Allen-Fahey and related experiments support the predominance of cochlear slow-wave otoacoustic emission. J Acoust Soc Am, 2007; 121: 1564–75.
 
40.
Meenderink S, Van der Heijden M: Reply to Ren and Porsov: reverse propagation of sounds in the intact cochlea. J Neurophysiol, 2010; 104: 3733.
 
41.
Li YT, Grosh K: Direction of wave propagation in the cochlea for internally excited basilar membrane. J Acoust Soc Am, 2012; 131: 4710–21.
 
42.
Reichenbach T, Hudspeth AJ: A ratchet mechanism for amplification in low-frequency hearing. Proc Nat Acad Sci, 2010; 107: 4973–78.
 
43.
Hudspeth AJ, Juelicher F, Martin P: A critique of the critical cochlea: Hopf – a bifurcation – is better than none. J Neurophysiol, 2010; 104: 1219–29.
 
44.
Reichenbach T, Stefanovic A, Nin F, Hudspeth AJ: Waves on Reissner’s membrane: a mechanism for the propagation of otoacoustic emissions from the cochlea. Cell Reports, 2012; 1: 374–84.
 
45.
Guild SR: Comments on the physiology of hearing and the anatomy of the inner ear. Laryngoscope, 1937; 47: 365–72.
 
46.
Naftalin L: The transmission of acoustic energy from air to the receptor organ in the cochlea. Life Sci, 1963; 2: 101–6.
 
47.
Pohlman AG: A reconsideration of the mechanics of the auditory apparatus. J Laryngol Otol, 1933; 48: 156–95.
 
48.
Davis H, Derbyshire AJ, Lurie MH, Saul LJ: The electric response of the cochlea. Am J Physiol, 1934; 107: 311–32.
 
49.
Dong X, Ospeck M, Iwasa KH: Piezoelectric reciprocal relationship of the membrane motor in the cochlear outer hair cell. Biophys J, 2002; 82: 1254–59.
 
50.
Békésy Gv: Some similarities in sensory perception of fish and man. In: Cahn PH (ed.), Lateral Line Detectors. Bloomington: Indiana University Press, 1967; 417–35.
 
51.
Chiappe ME, Kozlov AS, Hudspeth AJ: The structural and functional differentiation of hair cells in a lizard’s basilar papilla suggests an operational principle of amniote cochleas. J Neurosci, 2007; 27: 11978–85.
 
52.
Dorn E: Über den Feinbau der Swimmblase von Anguilla vulgaris L. Zeitschrift fur Zellforschung, 1961; 55: 849–912 [in German].
 
53.
Gold T. Hearing. II. The physical basis of the action of the cochlea. Proc Roy Soc Lond B, 1948; 135: 492–98.
 
54.
Gold T: The theory of hearing. In: Messel H (ed.), Highlights in Science. Sydney; Pergamon, 1987; 149–57.
 
55.
Guinan JJ: Physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds.), The Cochlea. New York: Springer, 1996; 435–502.
 
56.
Barral J, Dierkes K, Lindner B et al: Coupling a sensory haircell bundle to cyber clones enhances nonlinear amplification. Proc Nat Acad Sci, 2010; 107: 8079–84.
 
57.
Gelfand M, Piro O, Magnasco MO, Hudspeth AJ: Interactions between hair cells shape spontaneous otoacoustic emissions in a model of the tokay gecko’s cochlea. PLoS One, 2010; 5: e11116.
 
58.
Manley GA: Spontaneous otoacoustic emissions from freestanding stereovillar bundles of ten species of lizard with small papillae. Hear Res, 2006; 212: 33–47.