J. David Pye
Professor in the Department of Zoology and Comparative Physiology
Queen Mary College, London
A Report in NATURE of a meeting on non-linear and active mechanical processes in the cochlea 17-19 September 1979 at the Institute of Laryngology and Otology of the Royal National Throat, Nose and Ear Hospital, London. It was organised by Dr. D.T. Kemp and Mr. S. D. Anderson.
The sense organ of the ear is the cochlea which, as its name implies, is shaped like a snail’s shell. Inside its hard, bony wall are three liquid-filled chambers that run together round the spiral from the base to the tip. One of the dividing partitions is a very thin, acoustically transparent membrane but the other, the basilar membrane, is an elaborate structure. It bears four rows of sensory hair cells that are connected by synapses to the ends of nerve fibres that run to the brain.
Sound-induced vibrations of the ear-drum are efficiently transmitted to the incompressible cochlear liquids by a chain of three tiny bones. A relatively slow travelling wave is then initiated in the basilar membrane and its movement excites the hair cells. For high-pitched tones the travelling wave builds up quickly to a peak near the base of the cochlea and then decays while for deeper tones it runs further toward the tip, thus exciting a different population of hair cells.
The cochlea therefore, not only transduces sound energy into nerve signals to the brain but also acts as a mechanical frequency analyser. But despite extensive study, neither of these functions is well understood in detail, for the known properties have so far not yielded a satisfactory synthesis. New findings from several sources now suggest that some parts of the mechanical action re non-linear and this realisation has greatly stimulated both theoretical speculation and new kinds of observations.
The new developments were aired at a recent meeting in London* and some of the highlights are mentioned below. Non-linearity implies that a response is not directly proportional to its cause (the response curve is not straight); it also leads to the local generation of distortion products that are not present in the original stimulus. This is of course a common feature of any system that is ‘overdriven’ by excessive stimuli and indeed the beat-notes and other combination tones produced in the ear by loud sounds are already familiar. It is surprising, however, to find that the ear is markedly non-linear, even a moderate and low sound intensities and that this property is related to active process in the living organ.
Conventional linear models of cochlear mechanics have always presented problems and non-linear models which embrace some previously unexplained phenomena have been proposed. Indirect evidence of non-linear motion has been obtained by electrophysiological and acoustic techniques. (D.O. Kim, Washington University).
Direct evidence of non-linearity has been provided by E. LePage and B. Johnstone of the University of Western Australia, Perth, who measured movements of the cochlear partition in guinea pigs by a micro-capacitive probe. The were able to confirm the results of W.S. Rhode of the University of Wisconsin, Madison who had previously demonstrated non-linearity in monkeys by a less sensitive Mossbauer technique.
Further direct evidence was provide by D.T. Kemp (The Royal National Hospital, London) who discussed in detail his newly discovered mechanical evoked response or ‘cochlear echo’. He and his collaborators have shown that brief sounds introduced into the ear canal can be detected again several milliseconds later as a vibration of the eardrum coming out from the cochlea. This is thought to occur because active non-linearity in the mechanical action of the basilar membrane would produce local changes in its impedance from which some of the energy will be reflected back towards the base of the cochlea. The involvement of active mechanical processes, using energy derived from physiological sources, was unexpected; but measurements of the echo show that under certain conditions it may contain more energy than is available from a passive reflection from that point. The theories of passive non-linearity that originally predicted the effect have there had to be revised.
The phenomenon has been independently confirmed by other workers (J.P. Wilson, University of Keele; H.P. Wit & R.J. Ritsma, University Hospital; Groningen; W.L. Rutten, Academic Hospital, Leiden; Kim). As the cochlear ‘Kemp echo’ has been shown to depend on normal physiological functioning of the living cochlea, its measurement can form a valuable new diagnostic tool. It is also realited to the fine structure of the normal hearing curve (which is not smooth by shows regular, very sharply tuned peaks of up to 10 dB) and both response can be detected by instruments at sound levels far below the audible threshold (Wilson). That the echo originates from mechanical non-linearity is further demonstrated by its relationship to the distortion products, especially the difference tone (f2-f1) and the cubic term (2f1-f2). Finally, it seems to be intimately linked with certain forms of tinnitus, where the cochlea oscillates spontaneously (for zero stimulus energy) and produces an objective tone that can be recorded from the eardrum.
In the field of psychoacoustic and electrophysiological observations, particular attention is being devoted to the physiologically vulnerable combination tones (f2-f1 and 2f1-f2) and to the elusive ‘second filter’ that makes the response of signal nerve fibres more sharply tunes than the basilar membrane that excites them. here again the properties of the cochlear echo (in response to paired stimulations) may provide a valuable new kind of evidence. But A.R. Palmer and E.F. Evans (University of Keele) found that single unit recordings from the acoustic nerve gave not evidence of mechanical non-linearity in the cochlea.
In discussions of cochlear mechanisms, of especial interest was the demonstration by A. Flock (Karolinska Institute, Stockholm) that the simple stereocilia of the hair cells are filled with actin filaments which also occur in the cuticular plate and round the apical circumference of the cell itself. The discovery of contractile proteins at these sites could be over great significance in understanding the transduction from mechanical to nervous (that is, electrical) energy and the part played by active, non-linear mechanical processes.
A.C. Crawford and R. Fettiplace (Cambridge University) showed that electrical stimulation of hair cells in the terrapin produces a finely tuned electrical response similar to that elicited by sound. The very short cochlea in the terrapin is probably an ineffective mechanical analyser and this discovery suggests that the second filter involves cellular processes. In the more traditional guinea pig, I.J. Russell and P.M. Sellick (University of Sussex) and Y. Tanaka (Dokkyo University, Tichigi) and his colleagues showed that the inner and outer rows of hair cells have very different response properties that may contribute separately to the final output of the cochlea.
It seems safe to predict that this meeting will come to be regarded as a milestone in the study of hearing. Hi-fi enthusiasts may be shocked, but non-linearity of the normal, healthy cochlea could be a key to its amazing performance.