Manley pre-1980

My earlier work,
before I became Head of Zoology at the T.U. München (1980)

Early in my career I was advised not to waste time trying to record electro-physiologically from the auditory nerve of lizards, as the fibres were too small. I later proved this to be erroneous, but it did mean that my first recordings during my thesis work were from the cochlear nucleus of different lizards, of a turtle, and of a crocodilian species. These recordings established that the cochlear nucleus of Caiman crocodilus was remarkably like that of birds. Since crocodilians and birds are closely related, this finding intensified my interest in the comparative study of hearing organs, not only to understand their function, but also how they evolved. My thesis work showed that lizard hearing varied in a number of respects from that of other groups of amniotes and paved the way for the many later studies of lizard audition, both in my first laboratory at McGill University in Montreal and later in Germany at the Technische Universität München. These early studies provided some new insights into the evolution of hearing organs and mechanisms in vertebrates, leading to my first tentative attempts to describe their evolution in the journals Evolution (Manley, 1973) and Nature (Manley, 1971).

During my Postdoc in Perth, Western Australia (9 months in the laboratories of Brian Johnstone), I was excited about being able to use the techniques Johnstone had developed for measuring extremely small movements of ear components. They used the Mössbauer method, with relies on small velocities changing the frequencies (by the Doppler effect) of emitted radiation from very tiny radiation sources (radioactive Cobalt diffused into steel). Here a big thank you to the late Graeme Yates, who tirelessly and selflessly kept the (essential!) multi-channel-analyser functioning during this time. In later years, we collaborated a lot with Graeme while studying lizards and emus in Australia. Using the Mössbauer technique, I studied the sound-induced vibrations of different parts of gecko middle ears (Manley, 1972), showing, as Wever had estimated using cochlear microphonics, that the extracolumella-columella complex of this single-ossicle middle ear acts like a lever (also found in a different form in the three-ossicle middle ear of mammals). The leverage varies with frequency and, when the inner ear no longer responds well to higher-frequency sounds (>4 kHz), the extracolumella bends and little energy gets transmitted to the inner ear papilla. Johnstone and I also measured the middle ear of guinea pigs (Manley and Johnstone, 1974) to much higher frequencies than had previously been possible and showed, among other things, that here also at high frequencies (in this case nearer 40 kHz) where the inner ear no longer responds well, middle-ear transmission breaks down and the middle-ear lever fails.

I was especially excited about measuring the middle ears of bats, since the Mössbauer technique, being velocity-sensitive, works well even at really high frequencies. Following some difficult preparations and with permission from the nature authorities, Dexter Irvine (who was also a Postdoc in Perth at the time) and I took an adventurous drive into the Australian "Outback" to a remote cave, where we caught half a dozen bats of the species Eptesicus fuscus and brought them back to the lab. Brian Johnstone, who had taken all of these preparations with a relaxed attitude and suspected we would never come back with bats, went immediately into high gear. He stayed up the whole night building an amplifier that would drive the electret loudspeaker, which I had constructed, at really high frequencies (over 100 kHz). The amplifier looked dangerous (and was, since it was not enclosed and it generated 400V high-frequency AC signals riding on 200V DC) but it worked reliably. Using this apparatus, we managed to measure eardrum velocities in this bat species up to 115 kHz. Remarkably, and similar to the guinea pig and gecko middle ear, the bat middle ear also failed at high frequencies. In this case, the collapse began, however, at frequencies above 70 kHz. Thus all of these middle ears, whether with a single ossicle or three, only work well when the inner-ear impedance is relatively low - relatively high impedances being attained at a quite different frequency in the three species studied. The bat middle ear work was sufficiently important back then to appear in Nature (which at that time still published whole-organism Biology; Manley et al., 1972).

This early work on middle ears raised my consciousness for them and their evolution, and this led to some later work on middle ears and which is briefly described elsewhere in this web site.

One of Brian Johnstone's students, Don Robertson, later followed me back to McGill University in Montréal to do his doctoral work, beginning in 1972. This "loss" for Brian was later more than compensated when Don - after a short Postdoc in Belgium - returned to Brian's department and stayed there until he became Full Professor of Physiology. He is now retired. Don wanted to work with mammals, and at that time one of the hottest questions in auditory science was how the sharp frequency tuning of auditory-nerve fibres was achieved. Thus one aspect of Don's doctoral work was to look for ways of manipulating frequency tuning. He developed a way of recording from the auditory nerve of the guinea pig by opening the scala tympani of the lowest coil of the cochlea and picking off a sliver of bone that covered the spiral ganglion. He was able to show that his recordings came from nodes of Ranvier of the myelinated primary fibres, since sometimes double-peaked action potentials were recorded (the Ranvier nodes on the two sides of the myelinated ganglion-cell bodies are only about 40µm apart). Not all recordings were under optimal physiological conditions - as is often the case - and Don was able to show that in a large population of recordings, there was a correlation between sensitivity loss and selectivity loss. Insensitive fibres had less sharp frequency-tuning curves. Following up the possibility that the sensitivity losses could be related to the fluid level in scala tympani (which, being exposed, could lose fluid to evaporation), Don discovered that if the fluid in the scala tympani of the cochlear base was removed, nerve fibres lost a great deal of their sensitivity. Don's surgical approach enabled controlled extraction of fluids, which involved entering the sound-insulated chamber, using a tiny strip of paper (baby nappies' cover layer, which consists of parallel strips of cellulose) to draw out fluid and then getting back to the apparatus quickly enough to record fibres before the fluid returned. The data were repeatable and showed that without fluid beneath the basilar membrane, fibre sensitivity was very much poorer (Robertson and Manley, 1974). I suggested to Don, however, that the really convincing thing would be to repeat this procedure while maintaining contact with single fibres. Don considered this almost impossible, but it gave him no rest and, in credit to his tenacity and consummate operative skills, he managed to achieve the "impossible" and was rewarded with a paper in Science (ROBERTSON, D. 1974, Cochlear neurones: frequency selectivity altered by perilymph removal. Science 186, 153-155.). He showed that single-fibre selectivity could be manipulated in a repeatable way This was one of the papers that clearly showed that frequency selectivity in the inner ear was labile and depended exquisitely on normal physiological conditions.

At McGill, work on lizards continued with a large study of the auditory nerve of the Tokay gecko in collaboration with my then master's student Ruth Anne Eatock and my technical assistant Lorraine Pawson. We published the first broad study of the characteristics of auditory-nerve activity in a lizard (Eatock et al., 1981) and the sensitivity of the frequency tuning of single fibres to temperature changes (Eatock and Manley, 1981). Within their relatively narrow frequency-response range (up to about 5 kHz), these lizards showed a remarkably sharp frequency sensitivity easily rivalling and indeed bettering that of birds and mammals. I also reported the response characteristics of auditory nerve fibres and cochlear nuclei neurons in the Bengal monitor lizard Varanus bengalensis (Manley 1976, 1977a). This was followed by a long series of anatomical and physiological studies in my Munich laboratory and in Western Australia that aimed to understand the structure, function and evolution of lizard hearing organs (see below). Ruth Anne continued her successful career with a move to Jim Hudspeth's lab at Rockefeller University to do doctoral work recording from lizard hair cells.

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