AUDITORY

PATHWAY
Structure a n d
Function

Edited by

Josef Syka
Czechoslovak Academy o f Sciences
Prague, Czechoslovakia

and

R. Bruce Masterton
Florida State University
Tallahassee, F l o r i d a

P L E N U M PRESS NEW YORK A N D LONDON

NEW ASPECTS OF COMPARATIVE PERIPHERAL AUDITORY PHYSIOLOGY

Geoffrey A. Manley, J u t t a B r i x , Otto G l e i c h , Alexander Kaiser,

C h r i s t i a n e Kttppl and *Graeme Yates
I n s t i t u t e of Zoology
Technical U n i v e r s i t y Munich
Lichtenbergstr. 4, 8046 Garching, F.R.G.
Department of Physiology
U n i v e r s i t y of Western A u s t r a l i a
Nedlands, 6009, A u s t r a l i a

Although the study o f the auditory system of nonmammals has a long

h i s t o r y , i t has only been i n the l a s t ten years that there has been
a g r e a t l y increased i n t e r e s t i n comparative s t u d i e s . There are two main
reasons f o r t h i s upsurge i n i n t e r e s t . F i r s t l y , the hearing organs o f
amphibians, r e p t i l e s and b i r d s d i s p l a y a s t r u c t u r a l v a r i e t y not found i n
the cochlea o f mammals, o f f e r i n g the chance to i n v e s t i g a t e s t r u c t u r e function r e l a t i o n s h i p s without i n t e r f e r i n g with the normal s t r u c t u r e .
Secondly, i t has been recognized that the sensory p a p i l l a e o f many nonmammals are mechanically and p h y s i o l o g i c a l l y r e l a t i v e l y robust, which
allows extensive and d e t a i l e d i n v e s t i g a t i o n of h a i r - c e l l f u n c t i o n i n
i s o l a t e d organs.
These and other advantages have l e d to a s i g n i f i c a n t increase
i n the quantity of data derived from nonmammalian preparations, data
which has made i t p o s s i b l e to d i s t i n g u i s h between those f u n c t i o n a l
features which are a l s o found i n mammals and those features which are
apparently observable only i n nonmammals. Thus, we are i n c r e a s i n g l y
m a b e t t e r p o s i t i o n t o judge which aspects of comparative auditory
Physiology are d i r e c t l y comparable t o mammalian inner ear f u n c t i o n
and provide an a l t e r n a t i v e means of i n v e s t i g a t i o n , i f not n e c e s s a r i l y
a 'simple' model of the mammalian ear.
A number of features of the organization o f the auditory receptors o f
t e r r e s t r i a l vertebrates are common to both mammals and nonmammals. Taken
together with a comparison to other h a i r - c e l l systems such as the auditory
receptors of f i s h , and v e s t i b u l a r and l a t e r a l - l i n e receptors, t h i s f a c t
suggests that many o f these features are the r e s u l t o f the conservation
throughout e v o l u t i o n of fundamental, p r i m i t i v e h a i r - c e l l p r o p e r t i e s
(Manley, 1986). Thus, the receptor c e l l s themselves and the genetic
programmes which determine t h e i r ontogeny i n t o an organized mosaic are the
primary determinants o f many b a s i c features of the f u n c t i o n of the inner
ear.
There are, on the other hand, several d i f f e r e n t mechanisms by which
i n d i v i d u a l h a i r c e l l s and h a i r - c e l l arrays achieve t h e i r frequency
s e l e c t i v i t y , and there are v a r i a t i o n s i n the expression o f d i f f e r e n t

mechanisms i n the various vertebrate groups (Manley, 1986) and perhaps even
i n h a i r c e l l s of d i f f e r e n t frequency ranges w i t h i n one p a p i l l a . I t i s
u s e f u l to begin by summarizing some of the published data on important
s i m i l a r i t i e s and d i f f e r e n c e s between n e r v e - f i b r e a c t i v i t y i n the various
groups of t e r r e s t r i a l v e r t e b r a t e s .
S i m i l a r i t i e s i n Auditory-Nerve F i b r e A c t i v i t y between Mammals and Nonmammals
1) In the equivalent frequency range (amphibians up to about 3 kHz,
r e p t i l e s and most b i r d s up to 5-6 kHz), the frequency s e l e c t i v i t y of
nonmammalian auditory-nerve tuning curves i s g e n e r a l l y as high as or even
higher than that of mammalian primary f i b r e s (Manley, 1981; Manley et a l . ,
1985; Sachs et a l . , 1974; Turner, 1987).
2) A l l vertebrate auditory p a p i l l a e are strongly t o n o t o p i c a l l y organized,
although i n c e r t a i n cases i n l i z a r d s , the d i s t r i b u t i o n o f CFs i s not
monotonic as i n mammals (Manley, 1981).
3) The general p a t t e r n s i n the d i s t r i b u t i o n of i n t e r v a l s i n the spontaneous
a c t i v i t y of nerve f i b r e s are s i m i l a r ; that i s , a modified Poisson d i s t r i b u t i o n u n d e r l i e s the a c t i v i t y i n both mammals and nonmammals.
4) Otoacoustic emissions (OAE) have been demonstrated i n frogs (Palmer and
Wilson, 1981), i n the caiman (Klinke and Smolders, 1984) and i n the
s t a r l i n g (Manley et a l . , 1987b), which i n most respects resemble those
reported from mammals.
Aspects i n which Auditory-Nerve F i b r e A c t i v i t y D i f f e r s between Mammals
and Nonmammals
1) Tuning curve symmetry seldom shows the t y p i c a l form of the asymmetry
seen i n mammalian f i b r e s of CF >1 kHz. There are o f t e n d i f f e r e n c e s between
d i f f e r e n t frequency ranges, however, as i n mammals (Manley, 1981; Manley
et a l . , 1985; Turner, 1987). An explanation o f these f i n d i n g s assumes an
understanding of the mechanisms of frequency s e l e c t i v i t y i n each case.
2) Spontaneous a c t i v i t y i n a number o f nonmammals shows systematic deviat i o n s from a Poisson d i s t r i b u t i o n (red-eared t u r t l e , Crawford and F e t t i place, 1980; a l i z a r d , Eatock and Manley, 1981; Manley, 1979; the s t a r l i n g ,
Manley and G l e i c h , 1984;Manley e t a l . , 1985; the pigeon, Temchin, 1985).
Low-CF ( c h a r a c t e r i s t i c frequency) c e l l s (seldom above CF 1.5 kHz) show
p r e f e r r e d i n t e r v a l s i n t h e i r spontaneous a c t i v i t y , i n t e r v a l s which are
roughly the same as or m u l t i p l e s of the CF p e r i o d . In the t u r t l e , i t has
been shown that these i n t e r v a l s r e f l e c t the presence o f o s c i l l a t i o n s o f
the h a i r - c e l l membrane p o t e n t i a l , o s c i l l a t i o n s whose main energy l i e s
near the c e l l ' s CF (Crawford and F e t t i p l a c e , 1981). These o s c i l l a t i o n s
seem to be i n t i m a t e l y r e l a t e d to an e l e c t r i c a l f i l t e r mechanism i n the
p r o p e r t i e s of the i o n i c channels o f the c e l l membrane. Such p r e f e r r e d
i n t e r v a l s have not been reported i n mammalian auditory-nerve f i b r e s .
3) With the exception of b a s i l a r - p a p i l l a u n i t s i n the amphibia (Moffat
and Capranica, 1976), a l l nonmammalian primary auditory-nerve f i b r e s
i n v e s t i g a t e d show a systematic temperature s e n s i t i v i t y (Gekko, Eatock
and Manley, 1976, 1981; Caiman, Smolders and Klinke, 1984; pigeon,
Schermuly and K l i n k e , 1985). Although the most obvious e f f e c t i s a
r e v e r s i b l e r i s e of CF with a r i s e i n temperature (at about 0.06 octaves/
C), the spontaneous a c t i v i t y may also be a f f e c t e d . In mammals, there i s
no temperature s e n s i t i v i t y over a non-lethal range of temperatures (Gummer
and Klinke, 1983). The temperature s e n s i t i v i t y of nonmammalian f i b r e s
can be explained i n terms of an e f f e c t on c e l l membrane channels involved
i n an e l e c t r i c a l tuning mechanism (Eatock and Manley, 1981).

4) The primary f i b r e discharge patterns i n nonmammals are not always

"primary-like" (Manley, 1981, Manley et a l . , 1985). For example, evidence
i s accumulating that many r e p t i l e and b i r d primary f i b r e s d i s p l a y primary
suppression, that i s , the spontaneous a c t i v i t y i s depressed by c e r t a i n
s i n g l e tones (Gross and Anderson, 1976; Manley et a l . , 1985; Temchin,
1985). This e f f e c t i s probably r e l a t e d to a f i r m connection between most
h a i r c e l l s i n nonmammals and the t e c t o r i a l membrane and the apparent
absence of such a connection i n mammalian inner h a i r c e l l s .
D i f f e r e n c e s i n a c t i v i t y patterns between mammalian and nonmammalian
auditory-nerve f i b r e s are traceable to features at two d i f f e r e n t l e v e l s .
The f i r s t l e v e l c o n s i s t s of c e l l u l a r and biochemical features (such as
membrane ion channels) which are not amenable to normal anatomical
a n a l y s i s . At the second l e v e l are features which can be described i n
normal anatomical terms.
Morphological
Patterns

Substrate as a P o t e n t i a l O r i g i n of Differences i n A c t i v i t y

Between mammals and nonmammals there are d i f f e r e n c e s i n the s i z e of

the p a p i l l a , which ranges from l i t t l e over 100 Am up to a few cm,
associated, of course with enormous d i f f e r e n c e s i n the t o t a l number of
h a i r c e l l s from about 100 to many thousands. Some p a p i l l a e are even d i v i d e d
into two s u b p a p i l l a e . The h a i r c e l l s may or may not be o v e r l a i d by a
t e c t o r i a l membrane, whose s i z e and form can vary widely between species
and even w i t h i n one p a p i l l a . The h a i r c e l l s i n p r i m i t i v e r e p t i l i a n p a p i l l a e
(e.g., t u r t l e s , Tuatara) a l l resemble each other, but i n other groups of
r e p t i l e s they are d i v i d e d i n t o two or more types recognizable by t h e i r
l o c a t i o n and t h e i r c y t o l o g i c a l features (Manley, 1981; M i l l e r and Beck,
1988). L i z a r d s show a d i v i s i o n of the two h a i r - c e l l types between the two
d i f f e r e n t frequency areas. The low-CF area i s covered by u n i d i r e c t i o n a l type h a i r c e l l s , the high-CF area by b i d i r e c t i o n a l - t y p e h a i r c e l l s ( M i l l e r
and Beck, 1988). In the Archosaurs ( C r o c o d i l i a and birds) and mammals,
two or more h a i r - c e l l types are g e n e r a l l y found i n a l l frequency areas.
A d d i t i o n a l l y , the i n n e r v a t i o n a l p a t t e r n of the h a i r c e l l s plays an
important r o l e . Recent data i n d i c a t e s that there are systematic innervat i o n a l d i f f e r e n c e s between d i f f e r e n t h a i r - c e l l types, and between species
i n r e p t i l e s , b i r d s and mammals. I t i s apparent i n mammals that only the
inner h a i r - c e l l population plays a s i g n i f i c a n t r o l e i n stimulus transformat i o n and transmission of information to the b r a i n (Liberman, 1982).
In view of these d i f f e r e n c e s , one might w e l l be surprised that
s u p e r f i c i a l l y , the response patterns i n auditory-nerve f i b r e s of d i f f e r e n t
vertebrates are so s i m i l a r . As o u t l i n e d above, however, i t should be
remembered that many s i m i l a r i t i e s are based on common h a i r - c e l l p r o p e r t i e s .
In a d d i t i o n , the p o s s i b i l i t y of convergent or p a r a l l e l evolution, t h i s i s ,
the independent evolution of a s i m i l a r s o l u t i o n to the same problem i n
d i f f e r e n t groups, should be kept i n mind. Some of our recent data from
r e p t i l e s and b i r d s i n d i c a t e that there are greater resemblances between
a c t i v i t y patterns which can be observed i n mammals and nonmammals than
some of us had a n t i c i p a t e d . The presence of otoacoustic emissions i n
nonmammals has already been mentioned above. Here, we w i l l b r i e f l y discuss
three f u r t h e r recent f i n d i n g s from our research groups, which i n d i c a t e
unexpected s i m i l a r i t i e s i n (1) the response patterns of d i f f e r e n t h a i r - c e l l
Populations, i n (2) the mechanical resonance p r o p e r t i e s which contribute
to tuning and i n (3) the tonotopic d i s t r i b u t i o n on the p a p i l l a e of mammals
n d nonmammals.
a

The b a s i l a r p a p i l l a of b i r d s contains a continuum of h a i r - c e l l forms,

from the columnar t a l l h a i r c e l l s on the neural edge to the bowl-shaped
short h a i r c e l l s on the abneural edge. The a c t u a l d i s t r i b u t i o n of the
h a i r c e l l s (Smith, 1985) and of various aspects of h a i r - c e l l morphology
(Gleich and Manley, 1988) are s p e c i e s - s p e c i f i c . For d e s c r i p t i v e purposes,
d i f f e r e n t h a i r - c e l l types ( t a l l , intermediate, short and l e n t i c u l a r ) have
been defined (Smith, 1985; Takasaka and Smith, 1971). In the r e l a t e d
C r o c o d i l i a , the t a l l and short h a i r - c e l l s are much more sharply d i f f e r e n t i a t e d and e a s i l y d i s t i n g u i s h a b l e from one another (Leake, 1977).
The t a l l h a i r c e l l s are the l e s s s p e c i a l i z e d of the two. This f a c t ,
the pattern of innervation and the f a c t that the t a l l h a i r c e l l s are found
on the neural (inner) side of the p a p i l l a has led to the supposition that
the t a l l and short h a i r c e l l s are d i r e c t l y comparable to the inner and
outer h a i r c e l l s of mammals, r e s p e c t i v e l y . I t should, however, be kept
i n mind that mammals and b i r d s are derived from d i f f e r e n t groups of
a n c e s t r a l r e p t i l e s and have a very long h i s t o r y of separate e v o l u t i o n .
The ancestors of the d i f f e r e n t groups of modern r e p t i l e s , of b i r d s
and of mammals diverged from each other during p e r m i a n t r i a s s i c times
(about 200 m i l l i o n years ago). R e p t i l e s regarded as having p r i m i t i v e ears
(e.g., Tuatara, t u r t l e s ) do not show a d i v i s i o n i n t o more than one h a i r c e l l population. Assuming t h i s represents the p r i m i t i v e ( t r i a s s i c ) condit i o n , i t i s u n l i k e l y that the r e p t i l e s a n c e s t r a l to b i r d s and mammals
already possessed two equivalent h a i r - c e l l populations. We are thus forced
to conclude that the mammals and b i r d s have evolved neural and abneural
h a i r - c e l l groups independently. We w i l l describe evidence that there are
not only anatomical p a r a l l e l s , but a l s o at l e a s t one p h y s i o l o g i c a l funct i o n common to t a l l h a i r c e l l s of b i r d s and inner h a i r c e l l s of mammals.
This i s a remarkable case of p a r a l l e l e v o l u t i o n .
In studies of the tonotopic o r g a n i z a t i o n of the b a s i l a r p a p i l l a and
i t s ontogeny i n b i r d s , we have used both HRP and cobalt s t a i n i n g techniques
to l a b e l p h y s i o l o g i c a l l y characterized primary nerve f i b r e s i n the
s t a r l i n g and the chick (Gleich, i n prep.;Manley et a l . , 1987a). With only
two exceptions, a l l characterized, unambiguously-labelled f i b r e s made
contact with t a l l h a i r c e l l s (usually only one c e l l , F i g . l a , b ) . Two
broadly-tuned, i n s e n s i t i v e c e l l s i n the s t a r l i n g with CF near 100 Hz
innervated a b n e u r a l l y - l y i n g c e l l s (Gleich, i n prep.) i n an area described
i n the pigeon by Klinke and Schermuly (1986) as responding to infrasound.
Thus, as i n the cat (Liberman, 1982), only the n e u r a l l y - l y i n g ( t a l l ) h a i r
c e l l s of b i r d s seem to transmit information to the b r a i n . These are the
f i r s t p h y s i o l o g i c a l data which support the working hypothesis that a
f u n c t i o n a l equivalence e x i s t s between h a i r - c e l l populations of b i r d s and
mammals.
A Simple Mechanical Resonance Phenomenon as the Basis of Sharp Tuning
in the Auditory Nerve of the B o b t a i l L i z a r d
An i n t e r a c t i v e (hair c e l l - t e c t o r i a l membrane) mechanical resonance
phenomenon has been suggested to underly the sharp tuning of mammalian
nerve f i b r e s (e.g., Neely and Kim, 1983; S t r e l i o f f and Flock, 1984;
Zwislocki, 1979, 1985). Our study of the tuning p r o p e r t i e s of the b a s i l a r
membrane and of nerve f i b r e s i n the b o b t a i l l i z a r d suggested that a s i m i l a r
resonance could be involved (Manley et a l . , 1987c).
The b a s i l a r p a p i l l a of t h i s skink i s about 2mm long and contains
almost 2000 h a i r c e l l s . I t i s d i v i d e d i n t o a shorter a p i c a l area, where
the h a i r c e l l s are covered by a huge, helmet-like t e c t o r i a l s t r u c t u r e

i<? 1.

a) H R P - s t a i n e d p r i m a r y n e r v e f i b r e i n a c r o s s - s e c t i o n o f t h e
p a p i l l a o f a young c h i c k . T h i s f i b r e a p p e a r s t o make a cup-shaped
s y n a p s e on a s i n g l e t a l l h a i r c e l l , b) A p r i m a r y f i b r e i n t h e
s t a r l i n g p a p i l l a seen i n s u r f a c e v i e w . T h i s f i b r e was s t a i n e d
w i t h c o b a l t and makes a b u t t o n - s h a p e d synapse on a h a i r c e l l on
the n e u r a l s i d e o f t h e p a p i l l a , c) An a u d i t o r y - n e r v e f i b r e o f
the b o b t a i l l i z a r d , s t a i n e d w i t h c o b a l t d u r i n g t h e r e c o r d i n g
and seen i n a wholemount o f t h e p a p i l l a . The arrow i n d i c a t e s
the f i b r e ' s p o i n t o f e n t r y i n t o t h e p a p i l l a . I n s e c t i o n e d
m a t e r i a l , t h i s f i b r e was seen t o synapse w i t h a t l e a s t f i v e
d i f f e r e n t h a i r c e l l s . The c a l i b r a t i o n b a r i s 10 Aim i n a l l
cases.

and a long b a s a l area, where the h a i r c e l l s are covered by a d e l i c a t e

chain of i n d i v i d u a l " s a l l e t s " .
These s a l l e t s each cover a s t r i p of h a i r c e l l s running across
the p a p i l l a and are connected to each other by a t h i n s t r i p of t e c t o r i a l
m a t e r i a l running along the midline o f the p a p i l l a (Koppl, i n preparation) .

Fig.

2.

Scanning-electron-microscope
photograph of a small p o r t i o n of
the upper surface of the b a s a l area of the p a p i l l a o f the
b o b t a i l skink. I t can be seen that the t e c t o r i a l membrane
c o n s i s t s of a chain of s a l l e t s , each of which j o i n s a s e r i e s
of h a i r c e l l s across the p a p i l l a . The bundles o f marginal h a i r
c e l l s are d i s t o r t e d due t o shrinkage of the t e c t o r i a l structures
caused by the h i s t o l o g i c a l procedure. The s a l l e t s are themselves
l i n k e d together by a r o p e - l i k e t e c t o r i a l s t r u c t u r e . The c a l i b r a t i o n bar i s 10 Aim.

Unlike the tuning of the b a s i l a r membrane, the tuning of primary

nerve f i b r e s was s t r i c t l y p l a c e - s p e c i f i c , r e v e a l i n g a c l e a r tonotopic
o r g a n i z a t i o n . Our measurements a l s o showed that a t one and the same
l o c a t i o n i n the same p a p i l l a , the n e u r a l tuning was s u b s t a n t i a l l y
sharper than that of the b a s i l a r membrane, each neural curve having a
s e n s i t i v e t i p up to about 40 dB deep. Subtracting the basilar-membrane
tuning from the neural tuning i n each case revealed a tuning component
subsequent t o the basilar-membrane motion which resembled a sharplytuned high-pass f i l t e r .
Our model o f t h i s tuning assumed coupling between neighbouring,
sharply-tuned elements each represented as a simple, sharply-tuned
high-pass f i l t e r . Adding the modelled resonance curves t o a t y p i c a l
basilar-membrane f u n c t i o n produced a family of tuning curves f o r various
CFs which bears a close resemblance t o those of the measured n e u r a l
elements. I t was suggested that the sharp tuning i n the b a s a l area o f
the b o b t a i l skink p a p i l l a i s the r e s u l t of the resonance of l o c a l groups
of h a i r c e l l s ( s t e r e o v i l l a r bundles) and t h e i r associated t e c t o r i a l
s a l l e t . The shapes of the tuning curves suggest some form o f i n t e r a c t i o n
between adjacent s a l l e t groups, since they are simultaneously r e l a t i v e l y
broad and deep. This i n t e r a c t i o n could be a mechanical one between
adjacent s a l l e t s , or i t could be due to the p a r a l l e l connection o f
s e v e r a l nearby h a i r c e l l s t o one nerve f i b r e , or be due to both f a c t o r s

Displacement .
(dB Arbitrary)

0.01
Frequency

F i g . 3.

(kHz)

A comparison of basilar-membrane (dotted l i n e ) and s i n g l e nervef i b r e (dashed l i n e ) tuning measured f o r the same l o c a t i o n i n one
p a p i l l a of the b o b t a i l l i z a r d . The neural tuning curve has been
i n v e r t e d and i t s placement on the y axis was made using the best
match f o r the low-frequency flanks of the basilar-membrane and
n e u r a l curves. The continuous l i n e represents the c a l c u l a t e d
d i f f e r e n c e curve, which strongly resembles a high-pass f i l t e r
characteristic.

(Manley e t a l . , 1987c). L a b e l l e d s i n g l e auditory f i b r e s i n t h i s species

innervated more than f i v e or s i x neighbouring h a i r c e l l s . I t could be
that the s a l l e t s are present as semi-independent t e c t o r i a l u n i t s i n
order to increase the i s o l a t i o n of the mechanical resonances of neighbouring elements. In t h i s way, sharp tuning can be achieved over a wider
frequency range i n a short p a p i l l a .
S i m i l a r i t i e s i n the Tonotopic Pattern i n the Auditory P a p i l l a e i n a
R e p t i l e , a B i r d and a Mammal
In discussions of tonotopic organization i n u n s p e c i a l i z e d mammals,
i t i s often assumed that octaves are d i s t r i b u t e d l i n e a r l y on the receptor
mosaic. As the amount of space devoted to each octave i s roughly
equivalent to the number of receptors responsible f o r that octave,
v a r i a t i o n s i n the amount of space per octave i n s p e c i a l i z e d mammals has
been taken as an i n d i c a t o r of the r e l a t i v e "importance" of that octave
to the animal. Thus i t seems obvious that the "acoustic fovea" of some
bats i n d i c a t e s that a p a r t i c u l a r frequency region i s of s p e c i a l importance
(Vater e t a l . , 1985). Since we can no longer assume that the frequency
analysis mechanisms are the same i n a l l frequency ranges and i n a l l
animal groups, however, the assumption that the amount of space i s a
r e f l e c t i o n of "importance" may not always be true. I f the analysis
mechanisms i n d i f f e r e n t cases are not known, then n e i t h e r are the
constraints which determine the amount of space devoted to each p a r t
of the frequency range.
A comparison of the frequency d i s t r i b u t i o n on the hearing organs
of the b o b t a i l l i z a r d (Manley and K6ppl, i n prep.), chick (Manley e t a l . ,
1987a) and cat (Libermann, 1982) revealed that i n a l l three animals,
nmch less space i s devoted t o octaves below about 1 kHz than to octaves
above t h i s . The question a r i s e s as to whether t h i s means that the lower
frequencies are less "important" to a l l these animals.
The frequency map i n the b o b t a i l was studied both by d i r e c t recording of f i b r e s as they emanated from the p a p i l l a and by t r a c i n g s i n g l e
f i b r e s l a b e l l e d with cobalt (Fig. l c ; Koppl and G l e i c h , 1987). In l i z a r d s ,
^ e r e i s a d i s c o n t i n u i t y between a low-CF h a i r - c e l l area (where the h a i r

10

D i s t a n c e from a p i c a l end
Fig.

4.

12

(mm)

20

40

60

80

100

D i s t a n c e f r o m a p i c a l e n d {%)

A comparison of the tonotopic organization of the hearing organs

of the cat (after Liberman, 1982), chick and b o b t a i l l i z a r d .
The l e f t h a l f of the figure shows the d i s t r i b u t i o n of charact e r i s t i c frequencies i n terms of the absolute distance of the
innervated c e l l s from the a p i c a l end of the organs. On the r i g h t ,
the values are given as a percentage of each p a p i l l a r length,
in order to make the comparison e a s i e r . Less space i s devoted
to octaves below about 1 kHz i n a l l three cases.

c e l l s are o r i e n t e d i n the same d i r e c t i o n ) and one or more b i d i r e c t i o n a l l y oriented areas with CFs above about 1 kHz. More space i s devoted to each
octave i n the higher-CF area than i n the low-CF area. The f a c t that i n
mammals and i n the chick t h i s general pattern i s preserved suggests that
the d i v i s i o n i n r e p t i l e s i s not c o i n c i d e n t a l , but perhaps c o r r e l a t e s
with a change i n frequency s e l e c t i v i t y mechanisms towards higher
frequencies.
In nonmammals there are two mechanisms of frequency tuning i n which
an i n d i v i d u a l c e l l i s the f u n c t i o n a l u n i t and does not g r e a t l y i n f l u e n c e
i t s neighbours. At lower frequencies, there i s evidence f o r an e l e c t r i c a l
tuning mechanism. Depending on the required r e s o l u t i o n , such a mechanism
does not require a large number of receptor c e l l s spread over a large
area. At higher CFs, some l i z a r d s have a mechanical s e l e c t i v i t y mechanism
in which i n d i v i d u a l c e l l s can function independently of t h e i r neighbours
because they are not attached to them v i a a t e c t o r i a l membrane ( i . e . , the
s o - c a l l e d "free-standing" h a i r c e l l s of iguanid-agamid-anguid l i z a r d s ,
e.g., Weiss et a l . , 1976).
Where a t e c t o r i a l membrane i s present i n an area with CF above 1 kHz,
the l a t e r a l l i n k i n g of the h a i r c e l l s may lead to a reduced s e l e c t i v i t y
of tuning, unless more space i s devoted to each octave. In the l a t t e r
case, neighbouring c e l l s would have a very s i m i l a r CF. During the evolut i o n of the some r e p t i l e groups, b i r d s and mammals, there was a strong
tendency to devote more space to these octaves (Manley, 1986).
What about the low-CF area i n mammals? In s p i t e of the apparent
absence of e l e c t r i c a l tuning i n mammals and the f a c t that a t e c t o r i a l
membrane covers a l l frequency areas, the cat s t i l l devotes less space
to lower CF regions than to higher. Perhaps the large b r a i n of mammals
(and birds?) i s able to use other information i n the stimulus at low
frequencies (e.g. time information from phase-locked responses). This
could function with fewer l a b e l l e d l i n e s and reduce the n e c e s s i t y f o r a

large p h y s i c a l separation of frequencies i n the low-CF periphery. The

resemblance between the tonotopic d i s t r i b u t i o n s i n these three groups
may thus not n e c e s s a r i l y p o i n t t o common mechanisms.
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