Slow Dynamics of the Amphibian Tympanic Membrane

Several studies have demonstrated that delays associated with evoked otoacoustic emissions (OAEs) largely originate from filter delays of resonant elements in the inner ear. However, one vertebrate group is an exception: Anuran (frogs and toads) amphibian OAEs exhibit relatively long delays (several milliseconds), yet relatively broad tuning. These delays, also apparent in auditory nerve fiber (ANF) responses, have been partially attributed to the middle ear (ME), with a total forward delay of ∼0.7 ms (∼30 times longer than in gerbil). However, ME forward delays only partially account for the longer delays of OAEs and ANF responses. We used scanning laser Doppler vibrometery to map surface velocity over the tympanic membrane (TyM) of anesthetized bullfrogs (Rana catesbeiana). Our main finding is a circularly-symmetric wave on the TyM surface, starting at the outer edges of the TyM and propagating inward towards the center (the site of the ossicular attachment). This wave exists for frequencies ∼0.75-3 kHz, overlapping the range of bullfrog hearing (∼0.05-1.7 kHz). Group delays associated with this wave varied from 0.4 to 1.2 ms and correlated with with TyM diameter, which ranged from ∼6-16 mm. These delays correspond well to those from previous ME measurements. Presumably the TyM waves stem from biomechanical constraints of semi-aquatic species with a relatively large tympanum. We investigated some of these constraints by measuring the pressure ratio across the TyM (∼10-30 dB drop, delay of ∼0.35 ms), the effects of ossicular interruption, the changes due to physiological state of TyM (‘dry-out’), and by calculating the middle-ear input impedance. In summary, we found a slow, inward-traveling wave on the TyM surface that accounts for a substantial fraction of the relatively long otoacoustic and neurophysiological delays previously observed in the anuran inner ear. INTRODUCTION A long-standing question in auditory physiology has been the existence of substantial delays in the amphibian ear. These delays have been demonstrated to arise at both the neurophysiological [7] and otoacoustic levels [1, 11], yet appear unassociated with tuning [9, 15] as demonstrated for many other classes of land vertebrates. A recent review [4] recapitulated data from a previous study [10] and demonstrated that a significant fraction of this delay in the amphibian ear arises at the level of the middle ear, the tympanic membrane (TyM) in particular, and not at the level of the inner ear. However, the precise origin of this delay remained unclear. The present study sought to investigate the basis for this lag by examining the velocity profile across the surface of the TyM.