Dr. Matthew Mason
University Physiologist
Tel: +44 (0)1223 333829, Fax: +44 (0)1223 333840, E-mail: mjm68@cam.ac.uk
- My Departmental teaching page
- My St. Catharine's College teaching page
- A short article about my research (.pdf)
- My publications list
Structure and function of the middle ear
In vertebrates, sound vibrations are detected by hair cells, which send electrical signals via the auditory nerve to the brain. The middle ear apparatus represents a means of increasing the efficiency of sound energy transfer from the air through to the fluid-filled inner ear, where the hair cells are located. It consists of a tympanic membrane (eardrum) which receives the sound, an air-filled middle ear cavity behind it and a series of conducting elements to convey vibrations from the tympanic membrane across the cavity to the oval window, the entrance to the inner ear. In mammals, these conducting elements take the form of three tiny bones (ossicles), the malleus, incus and stapes. Other vertebrates have just one bone, the stapes, connected to the tympanic membrane via a cartilaginous extrastapes. It is believed that a tympanic middle ear evolved several times in parallel, in different vertebrate groups.
My research on the structure and function of the middle ear involves examining a wide range of different species with techniques including 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.
Studies of the middle ear in 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 (Fig. 1). Some of my research focusses on the middle ear of subterranean species, including moles, mole-rats and golden moles. 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. Those species which generate their own seismic signals by thumping might use substrate vibrations to subserve intraspecific communication or even, perhaps, seismic echolocation. The bizarre golden moles (Chrysochloridae) of sub-Saharan Africa have been of particular interest to me, since the malleus in some species is enormously enlarged and composed of unusually dense bone (Fig. 2). The ear ossicles of golden moles seem to be adapted towards the transmission of low-frequency seismic vibrations, via a mechanism referred to as "inertial bone conduction". Field-work that I have been involved with, 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.
Another species known to use seismic vibrations is the blind mole-rat Spalax ehrenbergi, from Israel. This fiercely solitary animal generates vibrations by thumping its flattened snout on the walls of its tunnels, using these signals to inform neighbours of its presence. Despite a wealth of studies, the way that Spalax detects ground vibrations is still controversial, with different researchers arguing for predominantly auditory or somatosensory (touch-based) mechanisms. Using information from micro-CT scans of the skulls of Spalax, the zokor Eospalax (a Chinese mole-rat, Fig. 3) and an African species (Tachyoryctes), my colleagues and I were able to demonstrate that the proposed route for auditory transmission which has been widely accepted in the literature is actually rather unlikely. We have suggested alternative and more likely pathways, including a potential route involving transmission via the mandible, a venous sinus and the cerebrospinal fluid.
As well as my work on subterranean species, I investigate the evolution and function of the middle ear apparatus in many other groups of mammals. For example, I have been collaborating with Prof. Brock Fenton's group in Canada regarding a connection between the hyoid apparatus and the middle ear of bats (Nature 463: 939-942, 2010). I am also interested in issues relating to human middle ear function and dysfunction.
A short and accessible article about my mammal work was recently published in the alumnus magazine of my former College: click here to read an adapted version.
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!
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. 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.
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 disk, 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 disks than females. A rocking movement of the stapes is found in the Xenopus ear, as in the bullfrog, but in Xenopus the extrastapes (tympanic disk) is more rigidly coupled to the stapes and the resulting lever ratio is much smaller. This probably represents an adaptation to improve hearing underwater.
Please see my publications list for the original articles describing these findings in more detail.
Some of my recent collaborators
Arnoldus Blix (University of Tromsø, Norway)
Matthew Farr (University of Warwick Medical School, UK)
Brock Fenton (University of Western Ontario, Canada)
Peter Narins (University of California at Los Angeles, USA)
Eviatar Nevo (University of Haifa, Israel)
Pim van Dijk (University Medical Center Groningen, The Netherlands)
My work has been sponsored by the BBSRC and the National Institutes of Health.
Fig. 1: Photomicrograph of the left middle ear apparatus of a tuco-tuco (Ctenomys sociabilis), a subterreanean rodent from South America (see Mason, 2004).
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).
Fig. 3: Micro-CT scan of the skull of the Gansu zokor Eospalax fontanierii (see Mason et al., 2010).
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).
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.