Department of Physiology, Development and Neuroscience

Matthew J. Mason PhD

University Physiologist Tel: +44 (0)1223 333829, Fax: +44 (0)1223 333840, E-mail: mjm68@cam.ac.uk

 
 
 

My research: structure and function of the middle ear

Consider the first and last major steps in anatomical construction of the mammalian middle ear - for we know no better or more intriguing story in the evolution of vertebrates. Stephen Jay Gould (1993)

The middle ear apparatus (Fig. 1) improves the efficiency of sound energy transfer from the air through to the fluid-filled inner ear, which contains the hair cells that will turn vibrations into electrical signals interpretable by the brain. It consists of a tympanic membrane (eardrum) which receives the sound, an air-filled middle ear cavity behind it and, within the cavity, a series of conducting elements to convey vibrations from the tympanic membrane to the oval window, the entrance to the inner ear. In mammals, these conducting elements take the form of three tiny bones, or auditory ossicles. Other terrestrial vertebrates have a different ossicular system, described below. It is believed that a tympanic middle ear evolved several times in parallel, in different vertebrate groups.

My research involves examining a wide range of different ears (museum specimens or natural casualties), using techniques such as light microscopy, electron microscopy and micro-CT scanning. I then use models of middle ear function to investigate the likely hearing range of the animal in question, in order to answer questions about how hearing is matched to particular acoustical properties of the environment that the animal lives in, and how the ear might have evolved.

 

The middle ear of mammals

In mammals, vibrations of the tympanic membrane are transferred to the inner ear by means of three auditory ossicles, the malleus, incus, and stapes (meaning "hammer", "anvil" and "stirrup": see Fig. 1). Although people tend to refer to 'the' mammalian middle ear, in fact the morphology of the ossicles and other auditory structures differs considerably between different groups. These differences are of important physiological and ecological significance since they will help to determine what an animal hears.

One might expect that animals living in unusual environments would have unusual ear adaptations. This is indeed the case in subterranean mammals such as moles, mole-rats and golden moles, which have formed a key focus of my studies. For example, some have middle ear cavities which connect with each other through the middle of the skull, while others have missing muscles or massive mallei. Although many people are interested in whether airborne hearing in these curious animals is tuned to the low frequencies which propagate best through tunnels underground, subterranean mammals can in principle also use seismic vibrations, which travel well through soil or sand, to gain information about prey species, microhabitat or approaching predators (Mason & Narins, 2010). Those species which generate their own seismic signals by thumping might use substrate vibrations to subserve intraspecific communication or even, perhaps, seismic echolocation. In the golden moles (Chrysochloridae) of sub-Saharan Africa, the malleus can be enormously enlarged and composed of unusually dense bone (Mason, 2003a, Mason et al., 2006; Fig. 2). These bizarre bones seem to be adapted towards the transmission of low-frequency seismic vibrations, via a mechanism referred to as inertial bone conduction (Mason, 2003b). Field-work that I participated in, based in Namibia, suggests that the desert golden mole Eremitalpa granti uses its enlarged ossicles to detect vibrations generated as wind blows through tussocks of dune grass, where its prey species live (Lewis et al., 2006).

By looking at the diversity of ear types found among mammals, we can address the important question of to what extent model species are actually representative of mammals in general and humans in particular. For example, unlike humans, mice and rats have microtype ear ossicles which feature a large orbicular apophysis, a lump of bone which increases their mass and moment of inertia. This structure has previously been misidentifed as the "processus brevis" in developmental studies, which have drawn attention to its derivation from the second branchial arch (see Mason, 2013). Perhaps this mistake was made because researchers are more used to looking at human ear bones, which lack the apophysis! Bats and shrews also have microtype middle ears, and I have collaborated with Prof. Brock Fenton's group in Canada regarding bat ears (Veselka et al., 2010) and Prof. Ilya Volodin's group in Moscow which works on shrews.

Guinea pigs and chinchillas, commonly used as study animals in hearing research, have particularly unusual middle ears featuring fused ossicles, reduced or missing muscles and synovial stapedio-vestibular articulations (Mason, 2013). I have called this the "Ctenohystrica type" ear, referring to the wider group to which these mammals belong. The unique features of the Ctenohystrica type ear may collectively improve low-frequency hearing. In fact, there is a surprising diversity of ear types among rodents, which I have summarized in a forthcoming book chapter (Mason, 2015).

 

The ear structures of other vertebrates

The middle ear structures of birds, reptiles and frogs differ from those of mammals in that the tympanic membrane is coupled to the stapes, the only ear ossicle in these animals, by means of a cartilaginous structure called the extrastapes (the stapes and extrastapes of these animals are sometimes referred to as the "columella" and "extracolumella" respectively). Fishes lack a tympanic middle ear, but some species have Weberian ossicles to couple swimbladder vibrations to the sensory structures of the inner ear. Find out more by following the links below:

Using a laser interferometer to make precise measurements of nanometer-scale movements, Prof. Peter Narins (of UCLA) and I were able to establish exactly how the middle ear apparatus vibrates in the bullfrog. We found that there is some flexibility between stapes and extrastapes (Fig. 4), and that a cartilaginous band called the ascending process of the extrastapes provides pivotal support. Although text-book illustrations tend to represent the stapes and extrastapes of frogs as simple pistons, the extrastapes of frogs actually works, in effect, as a second ossicle (Mason & Narins, 2002a)!

Within the caudal half of the oval window in many frogs and salamanders is a second otic element called the operculum. Although long believed to be part of a separate pathway involved in seismic sensitivity, our laser interferometric work suggests that in bullfrogs the operculum is actually coupled to the stapes footplate: it moves in response to airborne sound (Mason & Narins, 2002b). The operculum may confer protection against quasi-static pressure changes associated with breathing and perhaps vocalization. Flexibility within the ossicular apparatus may turn out to be universal among terrestrial vertebrates, perhaps because of the advantages conferred with respect to pressure buffering. This is an intriguing avenue of research which I am continuing to explore (see Mason & Farr, 2013).

I have also investigated ear function in the aquatic frog Xenopus laevis, best-known as an animal model in developmental biology studies. This strange frog lacks a tympanic membrane but instead has a cartilaginous tympanic disc, formed as an expansion of the extrastapes. The ear of this animal, like that of the bullfrog, is sexually dimorphic, with male Xenopus having much larger tympanic discs than females. A rocking movement of the stapes is found in the Xenopus ear, as in the bullfrog, but in Xenopus the extrastapes (tympanic disc) is more rigidly coupled to the stapes and the resulting lever ratio is much smaller (Mason et al., 2009). This probably represents an adaptation to improve hearing underwater.

Please see my publications list for the articles cited here, and more.

 

Some of my recent collaborators

Peter Narins (University of California at Los Angeles, USA)
Sunil Puria (Stanford University, USA)
Galen Rathbun (California Academy of Sciences, USA)
Pim van Dijk (University Medical Center Groningen, The Netherlands)
Ilya Volodin (Lomonosov Moscow State University, Russia)

My work has been sponsored by the BBSRC and the National Institutes of Health.

Photomicrograph of the left 
middle ear apparatus of a tuco-tuco, a subterranean rodent from South 
America.

Fig. 1: Internal view of the left middle ear apparatus of a vole. The stapes footplate, projecting towards the viewer, would normally be contained within the oval window, the entrance to the inner ear.

Rotating radiograph of the skull 
of a golden mole

Fig. 2: Rotating radiograph of the skull of a golden mole, Eremitalpa granti granti. Note the enormously enlarged mallei, which appear as rounded, white masses in each ear (see Mason, 2003).

Zokor

Fig. 3: Micro-CT scan of the skull of the Gansu zokor Eospalax fontanierii (see Mason et al., 2010).

Frog ear animation

Fig. 4: Animation of the middle ear structures of a bullfrog. The tympanic membrane (green), vibrates in response to airborne sound; these vibrations, much exaggerated here, are communicated to the inner ear via extrastapes (light blue) and stapes (dark blue). Note the hinge-point between extrastapes and stapes (see Mason & Narins, 2002).

Weberian ossicles

Fig. 5: Micro-CT scan of the anterior vertebral region of the zebrafish Danio rerio, with three of the Weberian ossicles coloured. Click here for more information.