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Hearing Research Xxx (2012) 1E8 Hearing Research xxx (2012) 1e8 Contents lists available at SciVerse ScienceDirect Hearing Research journal homepage: www.elsevier.com/locate/heares Review Sound transmission along the ossicular chain in common wild-type laboratory mice Wei Dong*, Polina Varavva, Elizabeth S. Olson Department of Otolaryngology, Head and Neck Surgery, Columbia University, P&S 11-452, 630 West 168th Street, New York, NY 10032, USA article info abstract Article history: The use of genetically modified mice can accelerate progress in auditory research. However, the Received 25 July 2012 fundamental profile of mouse hearing has not been thoroughly documented. In the current study, we Received in revised form explored mouse middle ear transmission by measuring sound-evoked vibrations at several key points 12 October 2012 along the ossicular chain using a laser-Doppler vibrometer. Observations were made through an opening Accepted 12 November 2012 in pars flaccida. Simultaneously, the pressure at the tympanic membrane close to the umbo was Available online xxx monitored using a micro-pressure-sensor. Measurements were performed in C57BL mice, which are widely used in hearing research. Our results show that the ossicular local transfer function, defined as the ratio of velocity to the pressure at the tympanic membrane, was like a high-pass filter, almost flat at frequencies above w15 kHz, decreasing rapidly at lower frequencies. There was little phase accumulation along the ossicles. Our results suggested that the mouse ossicles moved almost as a rigid body. Based on these 1-dimensional measurements, the malleuseincus-complex primarily rotated around the anatomical axis passing through the gonial termination of the anterior malleus and the short process of the incus, but secondary motions were also present. Published by Elsevier B.V. 1. Introduction defined by the line passing though the anterior process of the malleus and the short process of the incus (dashed line in Fig. 1A). The function of the middle ear is to transfer environmental In contrast, the gerbil middle ear is more like the ‘freely mobile’ sound collected by the outer ear to the cochlea via vibration of the type (Fleischer, 1978)found in chinchilla, guinea pig, cat and human tympanic membrane (TM) and the ossicles. It is known that the although the attachment of the malleus to the tympanic ring is middle ear, including the TM, middle ear air space and ossicles, the more rigid in gerbil than in human. For the ‘freely mobile’ type of malleus, incus and stapes, varies greatly in form and size among ossicles, the anterior process of the malleus is relatively short and mammals (Rosowski, 2003). The middle ear morphology relates to the attachment to the tympanic bone is not as solid as in ‘micro- its function. For example, the low frequency hearing in gerbil type’ (arrow in Fig. 1B). The incus is relatively large and the benefits from the relatively large bulla (Plassmann and Kadel, 1991) manubrium is roughly perpendicular to the anatomical axis. and the specialized malleuseincus-complex in the cetaceans is Middle ear transmission has been described as an impedance adapted for hearing under water (Fleischer, 1978). matching process, coupling the relative low acoustic impedance in The mouse middle ear falls into the category of ‘microtype’, air to the much higher input impedance of the cochlea. In the following the terminology of Fleischer (1978) (Fig. 1). The specific classic view, the impedance matching is achieved by the area ratio features of the mouse ossicular chain are (1) an elongated anterior of a large tympanic membrane to a smaller stapes e footplate, processes of the malleus (the gonial) that is fused to the tympanic together with the lever ratio between the malleus and incus ring (arrow in Fig.1B); (2) an orbicular apophysis, a prominent mass rotating about the anatomical axis. Middle ear transmission leads of bone near the base of the manubrium of the malleus (Fig. 1A) and to a pressure gain, the pressure at the stapes is much higher than (3) a wide transversal lamina (Fig. 1A and B). The manubrium is the pressure at the ear canal. This has been shown in cat (Decory almost parallel to the classical anatomical rotation axis, which is et al., 1990; Nedzelnitsky, 1980), chinchilla (Decory et al., 1990; Slama et al., 2010), gerbil (Dong and Olson, 2006; Olson, 1998, 2001), guinea pig (Dancer and Franke, 1980; Decory et al., 1990; Magnan et al., 1997) and human temporal bone (Aibara et al., 2001; * Corresponding author. Tel.: þ1 212 305 3993; fax: þ1 212 305 2249. E-mail addresses: [email protected] (W. Dong), [email protected] Nakajima et al., 2008; Puria, 2003; Puria et al., 1997). Detailed study (P. Varavva), [email protected] (E.S. Olson). of middle ear transmission suggests that the middle ear vibration is 0378-5955/$ e see front matter Published by Elsevier B.V. http://dx.doi.org/10.1016/j.heares.2012.11.015 Please cite this article in press as: Dong, W., et al., Sound transmission along the ossicular chain in common wild-type laboratory mice, Hearing Research (2012), http://dx.doi.org/10.1016/j.heares.2012.11.015 2 W. Dong et al. / Hearing Research xxx (2012) 1e8 View from Ear Canal View from the Bulla A B Incus Anatomical Rotation Axis Transversal Lamina dorsal Malleus Gonial anterior posterior Incus Stapes Malleus ventral Manubrium Umbo Orbicular apophysis Fig. 1. Ossicular chain of mouse. (A) Diagram of mouse middle ear viewed from the ear canal showing the ossicular chain; (B) viewed from the opposite side (stapes was dis- articulated). (Drawn by Polina Varavva). not as simple as the classic model suggests, especially at high performed to maintain a patent airway. The left pinna was frequencies. For example, a complex vibration pattern on the removed. The umbo and manubrium could be accessed through the tympanic membrane (Cheng et al., 2010; Cheng et al., 2011; de La tympanic membrane. In order to access the malleus and incus, the Rochefoucauld and Olson, 2010; Khanna and Tonndorf, 1972; pars flaccida (PF) was removed (de La Rochefoucauld, et al., 2008; Rosowski et al., 2009) and bending along the manubrium in gerbil Dong et al., 2012). PF is a nearly transparent membrane with (de La Rochefoucauld and Olson, 2010) were in evidence. The a shape like a shallow bowl. When the pressure across the PF was stapes, driven by the motion of the long process of the incus, equalized, for example when the bulla was opened or vented, the PF produces the acoustic input to the cochlea and was found to be flattened out and wrinkles developed making it less transparent. rotating instead of simply moving as a piston in human temporal Measurements from the umbo and manubrium were made pre- bone (Hato et al., 2003; Heiland et al., 1999); cat (Decraemer et al., and post-removal of the PF to monitor of the effects of opening the 2003; Decraemer and Khanna, 2003; Guinan and Peake, 1967) and PF on sound transmission. For measurements done prior to opening gerbil (Decraemer et al., 2007; Huber et al., 2008; Ravicz et al., the PF, the bulla was vented with a tiny hole to avoid static pressure 2008). Understanding middle ear function is important because it buildup in the bulla cavity. shapes the sound going into the cochlea as well as the sound Fig. 2 shows the view of the mouse middle ear ossicles through traveling out from the cochlea as otoacoustic emissions (Dalhoff the opening in PF. Velocities (V) at points (filled dots in Fig. 2) along et al., 2011; Dong et al., 2012; Dong and Olson, 2006; Keefe, the ossicular chain were sequentially measured using a Laser- 2002; Keefe and Abdala, 2007; Magnan et al., 1997; Puria, 2003; Doppler vibrometer (LDV, Polytec, OFV-534, and VD-06 decoder). Voss and Shera, 2004). The vibrometer’s HeliumeNeon laser was focused on the prepara- Mice have been used in many areas in auditory research and tion with a 5 Â Mitutoyo lens with 33.5 mm focusing distance. As because of the genetic control possible, accelerate our under- reported by the manufacturer, the focused spot size (1/e2)is3mm. standing of many different levels of the auditory system. Past studies The noise level of the velocity measurement depends on the amount À on the mouse middle ear showed its specific morphology and of reflected light and was typically less than 10 4 mm/s at frequen- motion (Fleischer, 1978; Lee et al., 2009; Qin et al., 2010; Rosowski cies below 30 kHz and somewhat larger at higher frequencies. et al., 2003; Saunders and Summers, 1982). However, sound trans- Simultaneously, the pressure at the tympanic membrane (PTM) mission along the mouse ossicular chain is still not well understood. was measured at a location close to the umbo using a micro- In the current study, we describe the local transfer function (LTF) along the ossiclar chain in commonly used wide type mice. The complex LTF was calculated by dividing the complex velocity Laser (measured at several ossicular points with a Laser-Doppler vibr- Doppler ometer) by the complex pressure (measured at the tympanic V membrane close to umbo using a micro-pressure sensor.) The Incus detailed description of the velocity along the ossicular chain quantifies middle ear transmission and aids in the exploration of Malleus middle ear pathologies. The present study informs our under- PTM Micro-pressure sensor standing of the excitation to the cochlea and the hearing of mice. Stapes Umbo 2. Methods 0.5 mm Experiments were performed in C57BL mice that were 5e10 weeks old. The care and use of the animals were approved by the Institutional Animal Care and Use Committee of Columbia Univer- sity.
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