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Contribution to Book
Anatomy, physiology, and function of auditory end-organs in the frog inner ear
Hearing and Sound Communication in Amphibians (2006)
  • Dwayne D Simmons, Washington University School of Medicine
  • Sebastiaan W. F. Meenderink
  • Pantelis N Vassilakis, DePaul University
Abstract
1. Overview The vertebrate ear is a highly sensitive, frequency analyzer that receives sound through a specialized accessory apparatus (the external and middle ears) prior to its transmission to discrete end organs containing sensory hair cells (the inner ear). Although there are significant differ-ences in the structures used to receive and analyze sound, amphibian and mammalian ears func-tion very similarly to one another. With few exceptions, the amphibian ear consists of a middle ear and an inner ear, but no external ear. As schematized in Figure 1, the amphibian middle ear has an exposed eardrum (tympanic membrane) overlying a funnel-shaped tympanic cavity that connects to the inner ear near the base of the skull (see Mason, chapter 6, for a review of the am-phibian middle ear). The amphibian inner ear or otic labyrinth is unique among vertebrate ani-mals in that it has two sensory organs specialized for the reception of airborne sound, the am-phibian papilla (AP) and the basilar papilla (BP). These sensory papillae reside within the poste-rior portion of the otic labyrinth and are contained in ventrally-located recesses of the large, fluid-filled saccular chamber shared with two vibration-sensitive macular organs, the sacculus and lagena (Fig. 1). Both the AP and BP chambers have a thin contact membrane that separates periotic perilymph from the endolymph fluid of the saccular chamber. Sound energy captured by the eardrum as well as other areas along the body of a frog is converted into fluid displacements and travels along pathways of the otic labyrinth that lead into the endolymphatic spaces of the inner ear (Hetherington et al. 1986; Lewis and Lombard 1988; Purgue and Narins 2000a). The sound path eventually leads into the AP and BP recesses before exiting into the caudal portion of the periotic canal and the round window (Purgue and Narins 2000a). Similar to the mammalian ear, the amphibian ear demonstrates exquisite intensity sensi-tivity and sharp frequency selectivity that are likely to arise from nonlinear, active amplification processes. How theories of mammalian auditory function apply to amphibian hearing is not known. Mechanisms of tuning and sensitivity have been extensively studied in the mammalian cochlea. It is generally agreed that the initial stage of inner ear frequency selectivity is achieved through the specialized mechanical properties of the basilar membrane, giving rise to a traveling wave (Von Békésy 1960; West 1985). Such traveling waves may be enhanced by electrically-driven somatic movements of specialized outer hair cells that provide the work required for the active process (Dallos 1992; Nobili et al. 1998; Ashmore et al. 2000). Although outer hair cell-like mo-tility has not been demonstrated in reptiles and birds, their papillae contain structures analogous to those in the mammalian cochlea such as a basilar membrane. However, one of the most strik-ing anomalies concerning the frog AP is that it lacks a basilar membrane, and yet it clearly dem-onstrates sharp frequency resolution and sensitivity as well as otoacoustic emissions (OAEs) that are comparable to those found in mammals. In amphibians, reptiles and birds, the best candidate for an active process may be the active motility of their mechanically-sensitive hair bundles (Hudspeth et al. 2000; Fettiplace et al. 2001; Bozovic and Hudspeth 2003). Although amphibian auditory organs may (Wever 1973) or may not (Will and Fritzsch 1988) have arisen independently and separately from those of other vertebrates, studies of these organs provide an opportunity to explore the details of what may be convergent design and func-tion. Do analogous physiological responses arise from similar or different anatomical features? Does the sensory end organs’ fine structure and innervation follow common principles across species? Although there have been extensive investigations into the physiology of these organs, much less is known about the detailed structure of anatomical correlates of this physiology such as the relationship between conduction velocities and response latencies. Much of the physiology of hair cell and eighth nerve responses of the AP and BP has been reviewed previously (Lewis and Narins 1999; Smotherman and Narins 2000). Sections 2 and 3 focus on the basic structural correlates of physiological responses of ranid frogs within the auditory papillae and nerve, re-spectively, while section 4 focuses on what is known about amphibian OAEs, and discusses the relationship of their properties to the underlying hearing mechanisms as well as the differences between sensory organs.
Keywords
  • hearing,
  • otoacoustic emissions,
  • amphibians,
  • inner ear
Publication Date
September 6, 2006
Editor
P.M. Narins, A.S. Feng, R.R. Fay, and A.N. Popper
Publisher
Springer
Series
Springer Handbook of Auditory Research
ISBN
0387325212
Citation Information
Simmons, D.D., Meenderink, S.W.F., and Vassilakis, P.N. (2006). "Anatomy, physiology, and function of auditory end-organs in the frog inner ear," in Hearing and Sound Communication in Amphibians, P.M. Narins, A.S. Feng, R.R. Fay, and A.N. Popper, editors, pp. 184-220. Vol. 28 in the series, “Springer Handbook of Auditory Research,” R.R. Fay, and A.N. Popper, editors. New York: Springer.