Lehrstuhl für Zoologie, Technische Universität München, 85747 Garching, Germany
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ABSTRACT |
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Manley, Geoffrey A.. Evidence for an Active Process and a Cochlear Amplifier in Nonmammals. J. Neurophysiol. 86: 541-549, 2001. The last two decades have produced a great deal of evidence that in the mammalian organ of Corti outer hair cells undergo active shape changes that are part of a "cochlear amplifier" mechanism that increases sensitivity and frequency selectivity of the hearing epithelium. However, many signs of active processes have also been found in nonmammals, raising the question as to the ancestry and commonality of these mechanisms. Active movements would be advantageous in all kinds of sensory hair cells because they help signal detection at levels near those of thermal noise and also help to overcome fluid viscosity. Such active mechanisms therefore presumably arose in the earliest kinds of hair cells that were part of the lateral line system of fish. These cells were embedded in a firm epithelium and responded to relative motion between the hair bundle and the hair cell, making it highly likely that the first active motor mechanism was localized in the hair-cell bundle. In terrestrial nonmammals, there are many auditory phenomena that are best explained by the presence of a cochlear amplifier, indicating that in this respect the mammalian ear is not unique. The latest evidence supports siting the active process in nonmammals in the hair-cell bundle and in intimate association with the transduction process.
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INTRODUCTION |
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The great sensitivity
of sensory systems has often been a source of amazement to
neuroscientists. Over the years, evidence has accumulated indicating
that in many cases, sensitivity has essentially reached its
"theoretical" maximum (e.g., Hudspeth 1997). In the
case of the vertebrate auditory inner ear, sensitivity has been
increased by a number of mechanisms, including using the external
ear
or its equivalent, e.g., in the facial disk of owls
to funnel
sounds to the eardrum. By this and other means, behavioral
sensitivities down to
20 dB SPL (2 µPa) have been achieved
(Fay 1988
). Further increases in sensitivity would not seem to be useful for three reasons
because of much higher levels of
external noises that mask signals, because of thermal noise that
becomes very significant at these levels, and because of the drag
exerted by the viscosity of the fluids surrounding the hearing organ
(Hudspeth 1997
).
Exactly how the mammalian earincluding the healthy human
ear
achieved its high sensitivity was a mystery for a long time. The
earliest measurements of the motion of inner-ear components were made
at unphysiologically high sound pressure levels (von Bekesy
1960
). Extrapolating from these measurements, von Bekesy concluded that at threshold, inner-ear sensory cells responded to
motions equivalent to the diameter of hydrogen atoms. These early
results added fuel to discussions of mechanisms of achieving such
sensitivity in the face of molecular noise sources and the viscosity of
inner-ear fluids. In 1948, Gold (1948, cited in
Kemp 1978
) had already concluded that using only passive
responses to sound, the inner ear simply could not be as sensitive as
it is. His conclusion was that in some way, the inner ear must contain an amplifying mechanism that released coherent mechanical energy into
the cellular system and thus boosted sensitivity at low sound levels.
Gold's speculations were untestable at the time of their publication since contemporary measurement equipment was too insensitive and too slow. In 1978, Kemp discovered what he termed "echos" being emitted with a short delay by the ear when stimulated with brief sound stimuli. Kemp was soon able to show that these signals were in fact not echos since they sometimes contained more energy than was present in the stimulus itself. These were sounds actively emitted from the inner ear in a way that could have been expected from Gold's predictions if the energy produced by the inner-ear amplifier was not being perfectly absorbed by the organ of Corti.
This discovery of what over the years came to be known as
otoacoustic emissions was mildly revolutionary for research
in peripheral hearing mechanisms. At one and the same time, it provided
evidence that there was, in fact, an active process in the inner ear,
and it also made it possible to investigate exactly those properties of
the hearing organ noninvasively. For the first time, a technique became
available to carry out the same objective and nondestructive tests on
human and animal cochleae, in this case by measuring the
characteristics of sounds emitted by the ear. The assumption of
cochlear amplification also had powerful explanatory value for earlier
findings on, for example, the deleterious effects of hypoxia on the
sensitivity and frequency selectivity of hearing, and on the
physiological consequences of damage to hair cells on cochlear
frequency selectivity. Davis (1983) suggested that such
an active process underlies all sensitive hearing and coined the term
"cochlear amplifier" as a global designation for as then undescribed mechanisms that feed mechanical energy into hair-cell motions with a phase appropriate, at some frequencies at least, to
strongly increase the cells' sensitivity.
It is not my purpose in this paper to review the evidence that
indicates that the mechanical energy really derives from the sensory
hair cells themselves or to describe the many pieces of work that have
attempted to localize and dissect the motor mechanism at the level of
single cells. For this, the reader is referred to previous reviews
(e.g., Ashmore 1992; Ashmore and Kolston
1994
; Dallos et al. 1993
; Hudspeth 1989
,
1997
; Pickles 1993
). Suffice it to say that in
mammals, there is evidence that the specialized outer hair cells (OHC)
have an amplification motor consisting of densely packed protein
complexes located in the lateral cell membrane. Activation of
conformational changes in these proteins causes cell contraction and
elongation that in turn increase the amplitude of the vibrational
patterns of the organ of Corti.
The focus of this paper is on the question as to whether this
phenomenon, which has played such an important role in research on the
mammalian cochlea for the past 18 yr, is unique to mammals. Certainly
most of the literature on the subject of active processes in the inner
ear has derived from work on mammals, and it has become an unspoken
expectationin the long and harmful tradition of anthropocentric views
on science
that in this regard the mammalian
and thus human
hearing
organ is very special. In the words of cladistic phylogeny, the active
process is often regarded as an apomorphy of mammals
a feature newly
derived during the early evolution of the mammals. Is this so or are
active mechanisms much older (Manley and Köppl
1998
)?
To avoid terminological confusion, it is useful here to clarify the
meaning I attach to some terms that will appear repeatedly in this
paper. The term "active mechanism" will be used for any cellular-biochemical or -biophysical process that is capable of generating a force that produces motions of hair-cell parts at frequencies in the audio range. The term "cochlear amplifier" is
used for the summed effects of the active process as seen in phenomena measurable in the organ itself, in the responses of the
auditory nerve afferent fibers, or as otoacoustic emissions. Thus
cochlear amplification is the result of an active process at the
hair-cell level. Since the term "cochlear amplifier" was coined by
Davis (1983) before the underlying cellular mechanisms were known, it cannot be claimed that this term should be restricted to
describing what happens in mammals.
In recent years, it has become customary to refer to a "cochlea" in
lizards, birds, and even amphibia, animals in which the hearing organ
is enclosed in bony recesses that are differently shaped and not coiled
as in mammals. Thus the term cochlear amplifier canif
active processes are found
also be extended to cover the phenomena
seen in all terrestrial vertebrates. Finally, I shall use the term
stereovillar bundle rather than stereocilial bundle of the hair cells
since the structure concerned is essentially not made up of cilia but
of large microvilli.
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HISTORICAL PERSPECTIVE |
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Since the early 1980s, many cochlear models had already been based on the assumption of the existence of some kind of cochlear amplifier, but the authors had used other terms to describe the phenomenon, such as feedback motor, negative damping, active feedback, reverse transduction, etc. The basic idea in all cases was that hair cells can react in a frequency-selective fashion to faint sounds with a response that in some way favorably affects the local motion of the hearing organ. Initially, the molecular basis of active processes was not considered to be important for creating models, it was simply assumed that they were fast enough to enhance cycle-by-cycle motion at auditory frequencies. Nonetheless, the elucidation of the molecular basis of the active process quickly became a focus of physiological studies, and nonmammalian data have played an important role in this undertaking.
From an evolutionary perspective, dissipative losses in hair-cell
motion due to the drag caused by fluid viscosity is a problem that
confronts hair cells of all systems (lateral line, vestibular, auditory). It would thus not be surprising if an active process that
reduces these losses originated early in the evolution of hair-cell
systems and thus early in vertebrate evolution. Ancestral systems had
no hair-cell specializations such as seen in the different kinds of
hair cells of the cochleae of mammals and birds, and they also had no
freely moving basilar membrane supporting the hair cells and that could
have been driven as part of a micromechanical resonance system. The
hair cells of the lateral line and vestibular organs were and are
firmly embedded in the tissue complex of the sensory organ. The
ancestral amplifier motor mechanism must thus have been sited in the
hair-cell bundle (Manley and Köppl 1998) as it was
the only freely moving component of the system. Could such hair-cell
bundles perform useful work? The amount of work done by hair cells to
produce the energy in otoacoustic emissions is very small, and is well
within the capabilities of several different potential motor mechanisms
driving the bundle (Hudpeth 1997
; Manley and
Gallo 1997
).
The first cochlear models to assume an active process (e.g., Kim
et al. 1980) incorporated negative damping into their equations and were quite successful at modeling the then-known behavior of the
cochlear partition. As those authors stated: "It is unknown what kind
of mechanism may underlie the hypothesized internal energy source in
the cochlear partition. Our conjecture is that energy available through
cellular metabolism in the cochlear partition may be somehow transduced
into mechanical energy." In a later, more complex model, the source
was later assumed to be in the outer hair cells (Neely and Kim
1983
).
An active process in the hair-cell stereovillar bundle
The first model that proposed a specific cellular location for the
active process implicated the stereovillar bundles of the hair cells.
Weiss (1982) assumed that hair-cell bundles would move
under the influence of electrical potential changes of the cell
membrane. Since such changes in electrical potential could be the
consequence of the transduction of sound stimuli, the resulting motion
of the hair-cell bundle
that is also responsible for stimulus transduction
would set up a feedback mechanism. This
feedback, if occurring with appropriate phase relationships to the
original signal, could amplify the stimulus. Following the discovery of whole cell motion of outer hair cells (see following text), Kim (1986)
incorporated into his model two active processes: the
hair-cell bundle mechanism as the basis of a fast cellular motor and a
cell-membrane mechanism driving whole cell motion and underlying a slow motor.
Between 1985 and 1990 several research groups, using in vitro
preparations, showed that in some hair-cell systems at least, the
bundles are indeed capable of active motions. Following Crawford and Fettiplace's (1985) description of such bundle properties in the turtle auditory organ, Howard and Hudspeth (1987)
demonstrated the presence of an adaptational motor system in the
stereovillar bundle of saccular hair cells from the frog. Also using
vestibular hair cells of the frog sacculus, Denk and Webb
(1989)
found a correlation between intracellular
voltage noise and the bundle position that suggested a
reverse-transduction process just as Weiss (1982)
had
proposed. Recent measurements on lateral-line organs revealed similar
nonlinearities to those associated with low-level amplification and
thus support the idea that an active process evolved very early in the
evolution of vertebrate hair cells (van Netten 1997
).
Similarly Rüsch and Thurm (1990) described
movements of both the kinocilium and the stereovilli of ampullary hair
cells of the vestibular system, movements that were both spontaneous
and could be electrically induced. In the same year and using saccular hair cells, Jaramillo et al. (1990)
demonstrated that
hair bundles could execute more rapid movements than those previously
observed during adaptation (e.g., Assad et al. 1989
) and
that these movements were strongly influenced by the concentration of
calcium ions. In a similar vein, Benser et al. (1996)
demonstrated rapid bundle movements whose frequency components lay in
the same range as those necessary for normal saccular responses. More
recently, Hudpeth's group has demonstrated that hair-cell bundles are
really capable of doing work by providing clear confirmation that the bundle actually amplifies the response to mechanical stimuli
(Martin and Hudspeth 1999
). Ricci et al.
(2000)
provided further evidence for a calcium-sensitive force
generator linked to the gating of the transducer channels in turtle
auditory hair cells. Finally, Manley et al. (2001)
described evidence from in vivo experiments using ac electrical current
injection into the cochlea of the bobtail lizard that can only be
explained on the assumption that an active process is present in the
hair-cell bundle.
To close this historical section, two points should be made. At
present, the motor mechanism driving the hair-cell bundle is not
finally understood and there is no evidence for or against such a
mechanism in mammals, although an active process in the bundle in
mammals is held by some authors to be at least as appropriate as the
oft-discussed active process that is sited in the cell membrane
(Yates and Kirk 1998).
An active process in the hair-cell membrane
In 1985, the same year as Crawford and Fettiplace were providing
evidence to support the then-current models of feedback systems in the
hair-cell bundle, Brownell et al. (1985) reported that isolated outer hair cells of mammals move in response to electrical fields by shortening or lengthening the entire cell. This finding unleashed efforts in many labs to describe the phenomenon in detail and
quantify its capabilities (e.g., Zenner et al. 1985
)
and, of course, to incorporate the idea into cochlear models (e.g., Neely and Kim 1986a
,b
). These data have been the subject
of a number of reviews (e.g., Ashmore 1992
;
Dallos and Evans 1995
; Hudspeth 1989
) and
will not be repeated here. Today, the majority of papers describe the
active process in mammalian auditory outer hair cells as resulting from
very fast configurational changes in densely packed protein complexes
of the basolateral hair-cell membrane. Studies of possible movements of
hair-cell bundles in mammals are few.
Since there is no evidence from nonmammals for hair-cell motion based
on such cell-membrane components, it has been tacitly assumed that
cochlear amplification is a process unique to mammals. In fact, the
available evidence clearly shows that the physiological phenomena in
mammals that are usually attributed to a cochlear amplifier are
universally present in tetrapods, suggesting that active processes in
hair cells are an ancientsynplesiomorphic
feature of tetrapod
vertebrates. An active mechanism may even have been inherited from the fishes.
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HOW DO WE RECOGNIZE THE EXISTENCE OF AN ACTIVE PROCESS? |
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This question cansince almost all work to date has been carried
out on mammals
initially be reduced to the questions: What is accepted
as evidence for the existence of a cochlear amplifier in mammals? How
does the underlying active process
OHC producing motion that
influences the micromechanical environment and thus the movement of the
whole organ
manifest itself?
In mammals, a cochlear amplifier is taken to underlie many phenomena, such as the high sensitivity to sound, the narrow frequency selectivity (tuning) of hair cells or their afferent nerve fibers, the typical patterns in rate-level functions of primary auditory neurons, the sensitivity of both threshold and frequency selectivity of auditory afferent nerve fibers to hypoxia and other insults, and the presence and characteristics of otoacoustic emissions. Is similar evidence available from nonmammals? We can consider the preceding points in turn.
Trivial comparisons show that some nonmammals have hearing systems that
are as sensitive as those of the most sensitive mammals. If we take,
for example, the two most sensitive representatives of the endothermic
vertebrates, the cat for the mammals and the barn owl for the birds, it
is clear that there is no difference between their best sensitivities
(Fig. 1). It is true that the catlike
many other mammals
has an upper frequency limit much higher than that
of any bird, but there is as yet no evidence that this is related to
peculiarities of cochlear amplifiers. It is more likely related to the
evolutionary accident that the three-ossicle middle ear of mammals
transfers higher frequencies better than do the columellar middle-ear
systems of nonmammals (Manley 1990
). Thus if a high
absolute sensitivity in mammals is a manifestation of a cochlear
amplifier, then at least some birds must also have one.
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The frequency selectivity of single primary auditory nerve fibers can
be very high. Once it became possible to measure the motion of the
organ of Corti in uncompromised preparations (e.g., Sellick et
al. 1982), it became clear that in mammals, a high-frequency selectivity is intrinsic to the entire organ and is produced by coupled
interactions between the hair cells and the micromechanics of
structures of the entire local organ. Thus the frequency selectivity, or tuning, of afferent nerve fibers strongly reflects the workings of
an active process. Interestingly, frequency selectivity in mammals is
usually less selective that that seen in nonmammals at the
same frequencies (Fig. 2). In the cases
shown, frequency selectivity measured as the Q10dB coefficient (the
center frequency divided by the frequency bandwidth at 10 dB above the
best sensitivity) is highest in primary afferents from a bird, the emu.
In a lizard, the Tokay gecko, tuning is not as high as in the emu but
still substantially higher than in the guinea pig, an animal that has been extensively studied with regard to tuning of the entire organ of
Corti. Of course, examples could be chosen where the differences are
not as great as illustrated here, but this does not detract from the
fact that in general, the frequency selectivity in mammals over the
frequency range where nonmammals can also hear is not especially great.
If an active process is necessary for establishing frequency tuning in
mammals, then it is can equally well be considered necessary for the
more selective tuning in nonmammals. The possibility exists, of course,
that some of the selectivity in nonmammals is due to electrical tuning
of the hair cells, which would not be dependent on a cochlear amplifier
process. However, the evidence for electrical tuning at higher
frequencies is weak (e.g., in birds, Gleich and Manley
2000
). In lizards, there is no evidence for electrical tuning
in cells with best frequencies higher than 1kHz (refs in Manley
1990
, 2000
).
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For a number of years, it was difficult to explain the different shapes
of the transfer functions (spike rate vs. sound level) of primary
auditory nerve fibers of mammals. These rate-level functions describe
the increase in the rate of spike discharge to increasing sound levels,
generally at the most sensitive (characteristic) frequency
(Sachs and Abbas 1974). However, Sachs and Abbas
(1974)
and Yates (1990)
and colleagues
(Yates et al. 1990
) were able to show that these
different forms of rate-level functions were intimately related to the
nonlinear response of the organ of Corti to sound pressure. This
nonlinearity is directly due to the active process, and disappears in a
damaged organ, in parallel to the loss of sensitivity and selectivity
of the neural elements. Thus the shapes of transfer functions can also
be taken to be an indicator of the presence of an active process that
enables interactions between hair-cell populations. Interestingly, all
three shapes of transfer function (flat-saturating, sloping-saturating,
and straight) have also been described from two avian species (Fig 3) (Köppl and Yates
1999
; Yates et al. 2000
). Their relationship to
the absolute sensitivity of the neurons studied is different to that
described for the guinea pig, but Köppl and Yates suggested that
in birds the active process acts more locally rather than globally as
in the mammalian organ of Corti (Yates et al. 1990
). In
lizards, only one kind of transfer function is found for the low-frequency region and another for the high-frequency region (Eatock et al. 1991
). Since interactions between
populations do not affect lizard transfer functions, they have been
omitted from Fig. 3.
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As might be expected, the active process in mammalsat least in the
whole organ in vivo
is highly dependent on a normal physiological state. Any kind of damage, such as brief hypoxia, leads to a rapid loss
of both sensitivity and frequency selectivity of primary afferent
fibers. This loss is reversible on restoration of the normal oxygen
supply (e.g., Robertson and Manley 1974
). However, hearing sensitivity and tuning in nonmammals is similarly compromised by hypoxia. This process is rapid in birds, which are highly dependent on a constant supply of oxygen, but is in principle exactly the same in
lizards, whose oxygen requirements are lower and who thus respond more
slowly to this insult (Fig. 4).
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Finally, as in mammals, there are numerous reports of OAE in nonmammals
(see e.g., Köppl 1995; Manley and
Taschenberger 2000
). The spontaneous otoacoustic emissions
(SOAE), which can be measured in the absence of any sound stimulus and
can be traced to spontaneous movements of hair cells, are regarded as
the clearest and even the most dramatic evidence that hair cells
contain an active process. Both spontaneous and evoked emissions have
been described in amphibians, lizards, and birds (Fig.
5). More than this, there are clear and sometimes startling similarities between mammalian and nonmammalian OAE. For example, in all species, each emitting ear shows an individual pattern of SOAE frequencies (Fig. 6).
SOAE are also physiologically vulnerable, vanishing reversibly under
brief hypoxia or even (in nonmammals) when the anesthetic level is too
deep. The statistical properties of the amplitude distributions of SOAE
in frogs, lizards, and birds show that they originate, as in mammals,
from hair cells acting as sine-wave oscillators (van Dijk et al.
1996
). Also, the center frequency of each individual SOAE
spectral peak in mammals and nonmammals is sensitive to the temperature
of the inner ear (e.g., Manley 1997
; Ohyama et
al. 1992
) (Fig. 7).
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In all species, also, SOAE can be influenced by tones added via a
loudspeaker, and the reactions of the emission peaks are very similar
whether measured in a mammal or in a nonmammal. Depending on the
frequency and level of the tone and its nearness in frequency to an
emission peak, SOAE can react to tones in the ear canal with
frequency-specific suppression (i.e., a fall in amplitude of the
emission), facilitation (an increase in amplitude) and/or shifts in the
center-frequency of the SOAE peak. Using tones of different frequencies
and levels, a threshold curve can be plotted that describes the
sound-pressure level at each stimulus frequency that is necessary to
suppress the SOAE amplitude by a criterion amount. This is known as the
suppression tuning curve (STC) of the individual SOAE (e.g.,
Köppl and Manley 1994). These STC strongly
resemble primary-neural tuning curves (Fig.
8), and this is one of the strongest
pieces of evidence that the SOAE arise from groups of hair cells that
at the same time form the tuned units giving rise to auditory-nerve
fiber excitation.
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Some comparisons between mammalian and nonmammalian otoacoustic
emission properties have yielded results that are remarkably similar.
In both human and lizard OAE, for example, the frequency distances
between SOAE peaks are on average essentially identical in spite of the
fact that the mammalian cochlea has a length of more than 30 mm, the
length in the lizards so far used in measurements varies from 0.2 to 2 mm. Even the frequency distances over which interactions occur between
SOAE peaks (as manifest in correlated amplitude fluctuations) are
almost the same in both animal groups. In both cases, such influences
are only found up to a between-peaks frequency ratio of 1.6, despite
the difference in the absolute size of the hearing organs (and thus the
absolute distance between the same two frequencies in each ear)
(van Dijk et al. 1998). In humans, the hearing organ is
35 mm long, but in lizards it is only between 0.2 and 2 mm in length
(Manley 1990
).
More recently, electrically evoked emissions (EEOAE), that in mammals
are thought to derive from outer hair cell movements driven by the
injected current, have also been demonstrated in lizards (Manley
et al. 2001).
Is the motor mechanism of mammalian and nonmammalian OAE the same?
Considering all the reported data on OAE in mammals and
nonmammals, it can be said that there are only minor differences
between the phenomena in these groups. Thus these dataand indeed all the phenomena attributed to the active process
provide no a priori reason to suppose that mammals have evolved a special mechanism for
driving the cochlear amplifier. Nonetheless, the literature, especially
on single cell, in vitro studies, does contain evidence for two
possible sources of the active mechanical input
one in the hair-cell
bundle and one in the cell membrane wall of outer hair cells. The
former has only been described in nonmammal hair-cell systems and the
latter only from mammalian outer hair cells. Are we to conclude that,
although all terrestrial vertebrates show strong evidence for an active
process in their hearing organs, and the diverse phenomena described
are so remarkably similar between the groups, that the cochlear
amplifier is based on two totally different mechanisms? Is there an
evolutionarily older motor mechanism based in the hair-cell bundle that
arose in lateral-line hair cells and was "inherited" by the
vestibular and auditory systems? And is there a new, membrane-based
mechanism that arose much later and is only found in the mammalian cochlea?
At present, this question cannot be answered with certainty. In
nonmammals, all the available evidence points to a motor mechanism in
the hair-cell bundle and away from a motor in the hair-cell lateral
membrane. 1) An attempt to induce rapid hair-cell body motion in avian hair cells via current injection was unsuccessful (Brix and Manley 1994). 2) The hair-cell
membranes of nonmammals do not show the dense macromolecular complexes
thought to represent the membrane motors of outer hair cells (A. Forge, C. Köppl, and G. A. Manley, unpublished
data). 3) In birds, the hair-cell population that is
not afferently innervated (Fischer 1994
), and thus most
likely to be carrying the motor mechanism, consists of cells that are
as short as 3 µm with virtually no lateral cell membrane
(Fischer et al. 2000
; Gleich and Manley
2000
). With respect to their innervation (but not only in this
respect) (Manley et al. 1989
), these short hair cells of
birds thus resemble the outer hair cells of mammals, which have only a
sparse afferent innervation. It is hardly conceivable that these tiny
cells could produce motion using their membrane, but basal hair cells
do have remarkably robust stereovillar bundles containing up to 300 stereovilli (Fischer et al. 2000
; Gleich and
Manley 2000
; Tilney and Saunders 1983
). These
stereovillar bundles could move the tectorial membrane (Manley 1995
). 4) The patterns caused by low-frequency sound
modulation of EEOAE in lizards provide clear support for a bundle motor
(Manley et al. 2001
). In lizard auditory papillae, the
hair-cell bundle orientation patterns permit an unequivocal test as to
whether the active-process motor lies in the hair-cell membrane or in the bundle (Fig. 9). 5)
Ricci et al. (2000)
have shown that many of the fast
bundle movement phenomena already reported for saccular hair cells
(e.g., Benser et al. 1996
) can also be observed in turtle auditory hair cells. The time courses of the active movements observed were similar to the fastest time constants observed in hair-cell adaptation and were related to the activation time constants of the transduction channels.
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On the other hand, there appear to have been no serious attempts to
study whether in mammals, the hair-cell bundle is capable of motility.
Some experimental data are easier to explain if the motility is in fact
in the bundle (e.g., Yates and Kirk 1998). It is, of
course, conceivable that even if mammals have developed a new kind of
lateral-membrane motor mechanism, they have still retained the older
bundle mechanism, raising the question as to how the hair cells might
match the input phases of these two systems.
Summary
The various types of evidence accepted as indicating the presence of an active process driving a cochlear amplifier in mammalian hearing organs clearly also exist in nonmammals. Evolutionary considerations suggest that a bundle-based mechanism originated first: this mechanism certainly persists in nonmammals and is correlated with an auditory performance that is often equivalent to or better than that of mammals. In mammals, the active process appears to be at least partly driven by a membrane-based motor. Further work is necessary to examine the possible persistence of an additional, bundle-based motor.
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FOOTNOTES |
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Address for reprint requests: Lehrstuhl für Zoologie, Technische Universität München, Lichtenbergstr. 4, 85747 Garching, Germany (E-mail: geoffrey.manley{at}bio.tum.de).
Received 26 January 2001; accepted in final form 20 March 2001.
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REFERENCES |
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