Research paperComparison of forward (ear-canal) and reverse (round-window) sound stimulation of the cochlea
Graphical abstract
Highlights
► Forward stimulation: cochlear drive depends on scalae pressure magnitude difference. ► Reverse stimulation: cochlear drive depends on scalae pressure phase difference. ► Third-window sound flow is significant for reverse stimulation. ► Stapes velocity is not a good estimate of cochlear drive during reverse stimulation.
Introduction
Acoustic energy is normally transmitted to the cochlea by “forward” stimulation, in which sound presented to the ear canal elicits vibration of the middle-ear ossicles, producing a pressure difference across the cochlear partition that results in a traveling wave (Dancer and Franke, 1980; Nedzelnitsky, 1980; Lynch et al., 1982; Voss et al., 1996). Likewise, acoustic energy can be transmitted to the cochlear partition by “reverse” stimulation, in which mechanical vibration presented to the round window (RW) results in a pressure difference across the cochlear partition (Wever and Lawrence, 1948, 1950; Shera and Zweig, 1992; Spindel et al., 1995; Voss et al., 1996; Nakajima et al., 2010a,b).
RW stimulation utilizing modified middle-ear active transducers has improved various conductive and mixed hearing losses in patients; however, great variability in the efficacy of this approach has been reported (Martin et al., 2009; Baumgartner et al., 2010; Bernardeschi et al., 2011; Colletti et al., 2011; Mandala et al., 2011; Rajan et al., 2011; Iwasaki et al., 2012; Verhaegen et al., 2012). A number of studies have tried to address this concern by determining how well the RW actuator couples its motion to the RW membrane (Arnold et al., 2010a,b; Nakajima et al., 2010a; Pennings et al., 2010; Tringali et al., 2010; Schraven et al., 2011, 2012). Schraven et al., 2011, Schraven et al., 2012 carefully studied various actuator tips and the need for pre-load to the RW and reported generally reproducible performance. Often in these studies, stapes motion is used as an estimate of cochlear drive.
Determination of the mechanism and characteristics of sound transduction for reverse RW stimulation as compared to forward ear-canal stimulation has important implications. Stapes motion is a good estimate of the input to the cochlear partition during forward sound stimulation. This relationship relies on the assumption that the cochlear shell is a rigid body filled with incompressible fluid, with the oval and round windows as the only major flexible components by which volume velocity can enter and leave the inner ear. Evidence for this two-window hypothesis in forward stimulation was shown by measuring near-equal volume velocities of the oval and round windows (Kringlebotn, 1995; Stenfelt et al., 2004; Sim et al., 2012). However, it is unknown whether the two-window hypothesis holds during reverse stimulation, and this has important implications for whether or not stapes motion can be used as a good estimate of sound transduction in reverse stimulation. Differences in how the stapes velocity relates to intracochlear pressures and sound transduction in forward and reverse stimulation are possible because the impedances that the acoustic stimuli experience in the forward and reverse directions differ, as was shown by Puria (2003). Such differences in the impedance that the sound acts against as it flows through the ear in the forward and reverse directions influence sound flow, and differences in the relative impedances between possible paths may allow sound to follow different paths during reverse stimulation. Thus, whether the motion of the stapes is a good indicator of reverse stimulation is unknown.
The aim of this study is to understand the mechanics of how sound stimulates the inner ear in forward and reverse stimulation. We measure intra-cochlear pressures in scala vestibuli (PSV) and scala tympani (PST) simultaneously, and calculate the differential pressure, which is the drive for the motion of the cochlear partition. We compare these pressure measurements with measurements of ossicular motion during forward and reverse stimulation. Additionally we use these measurements to determine whether or not there are only two significant windows (paths for volume velocity to enter or exit the inner ear) during reverse stimulation, as has been shown for forward stimulation.
Section snippets
Methods
Most of the methods used in this study are similar to that described in previous publications (Nakajima et al., 2009, 2010a,b). Therefore brief descriptions of most of the methods follow, with the exception of detailed descriptions of techniques new to this study.
Pressures in scala vestibuli and scala tympani
Intracochlear pressures in SV and ST were measured simultaneously along with the velocity of the stapes or RW actuator to obtain the transfer function of the intracochlear pressures referenced to their stimulus velocities. Fig. 3 shows comparisons of SV and ST pressures elicited by forward ear-canal stimulation and reverse RW stimulation for a representative experiment. The intracochlear pressures were referenced to stapes velocity (VStap) for forward stimulation, and RW actuator velocity (VAct
Forward stimulation
An illustration representing the cochlear system during forward stimulation is shown in Fig. 9a. During forward stimulation, the volume velocities at the oval window (UStap) and RW (URW) have been measured to be nearly equal (Stenfelt et al., 2004). Therefore, the volume velocity through the basilar membrane, meaning through the whole partition, (UBM) is also about the same as through the oval window and the RW; that is, UStap ≈ URW ≈ UBM. Alternate sound paths, such as physiological third
Acknowledgments
We dedicate this paper to Saumil N. Merchant, who was involved throughout this project contributing his insight and support. We thank Julie Merchant, Diane Jones, Mike Ravicz, Melissa McKinnon, Ishmael Stefanov-Wagner, David Chhan, Marlien Niesten, and the staff of the Otolaryngology Department and Eaton Peabody Laboratory at Massachusetts Eye and Ear Infirmary for their generous contributions. This work was carried out in part through the use of MIT's Microsystems Technology Laboratories for
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