Basic Issues in Hearing
Proceedings of the 8th International Symposium on Hearing
Paterswolde, Netherlands, April 5 - 9 , 1988 E d i t e d by
H. Duifhuis
Biophysics Department University of GroningenThe Netherlands
J. W. Horst and H. P. Wit
Institute of Audiology University Hospital Groningen
The Netherlands
1988
Academic Press
Harcourt Brace Jovanovich, Publishers London S a n Diego New York Berkeley Boston
Sydney Tokyo Toronto
Functional parallels between hair-cell populations of birds and mammals
G e o f f r e y M a n l e y , O t t o G l e i c h , J u t t a B r i x and A l e x a n d e r K a i s e r
Institut filr Zoologie der Technischen Universitat Mimchen, Lichtenbergstr. 4, 8046 Garching, FRG
Introduction
T h e e v o l u t i o n o f land vertebrates has p r o d u c e d an e x t r e m e l y interesting v a r i e t y o f structure and f u n c t i o n o f the hearing organ. We f i n d not o n l y large d i f f e r e n c e s i n the o v e r a l l dimensions o f the basilar p a p i l l a , but also i n the structure, arrangement and i n n e r v a t i o n o f the hair cells. L a r g e , s p e c i a l i z e d h e a r i n g organs d e v e l o p e d d u r i n g the mesozoic adaptive r a d i a t i o n o f the reptiles w i t h i n two e v o l u t i o n a r y lines: the mammals and the archosaurs ( c r o c o d i l i a n s a n d b i r d s ) . Since a n u m b e r o f r e p t i l i a n groups w h i c h also o r i g i n a t e d d u r i n g the same adaptive r a d i a t i o n still show s i m p l e , h e a r i n g organs, it is reasonable to assume f r o m the p a l e o n t o l o g i c a l evidence that the c o m m o n , early mesozoic, ancestor o f these groups had a rather s i m p l e , u n s p e c i a l i z e d h e a r i n g organ. T h e c o m p l e x i t i e s we see today i n the i n n e r ears o f mammals and c r o c o d i l i a n s are thus independent developments f r o m a c o m m o n stock. T h e s i m i l a r i t i e s we discuss b e l o w are the result o f p a r a l l e l e v o l u t i o n and show convergence i n some i m p o r t a n t features. In this report, we discuss two points. F i r s t l y , we s u m m a r i z e the e v i d e n c e c o n c e r n i n g both the s t r u c t u r a l differences but also the s i m i l a r i t i e s between the hearing organs o f b i r d s and m a m m a l s . S e c o n d l y , we p o i n t out that our recent p h y s i o l o g i c a l studies p r o v i d e the first evidence for the s u p p o s i t i o n that f u n c t i o n a l parallels exist between the hearing organs o f birds a n d mammals.
Structural differences between the anatomy of the avian and of the mammalian hearing organ
T h e structure o f the b i r d basilar p a p i l l a (see b e l o w , F i g . 1) is d i f f e r e n t to that o f m a m m a l s ( O r g a n o f C o r t i ) . A l t h o u g h the total n u m b e r o f h a i r cells can be s i m i l a r , the sensory e p i t h e l i u m is not so stretched out a n d c o i l e d . R a t h e r , a l t h o u g h also s h o w i n g the f a m i l i a r b a s e - t o - a p e x w i d t h gradient, it is g e n e r a l - ly shorter than 5 m m (some owls b e i n g a r e m a r k a b l e e x c e p t i o n ) a n d , at the most, somewhat bent and twisted along its length ( S c h w a r z k o p f f and W i n t e r ,
1960). T h e h a i r cells o f the a v i a n p a p i l l a are not so c l e a r l y d i v i d e d into two
populations as i n the m a m m a l i a n hearing organ, where there is one single r o w of inner hair cells ( I H C ) and mostly three rows o f outer hair cells ( O H C ) . A v i a n papillae do show structural variety o f the hair cells, the tall hair cells ( T H C ) l o o k i n g very d i f f e r e n t to the short hair cells ( S H C ) . H o w e v e r , the extremes grade into one another, so that a strict d i v i s i o n o f hair cells into different types s h o u l d perhaps be regarded as merely convenient for d e s c r i p - tive purposes.
T h e c o m b i n a t i o n o f a r e l a t i v e l y large n u m b e r o f hair cells and a short papilla lead to the fact that i n a transverse section o f the a v i a n p a p i l l a at the apical e n d , there can be up to about 50 hair cells; at the basal end there are about 10 hair cells. T h e cells on the neural side are c o l u m n a r i n shape ( T a l l hair cells, T H C ) , those on the abneural edge are b o w l - s h a p e d (short hair cells, S H C ; T a k a s a k a and S m i t h , 1971). U n l i k e i n the c r o c o d i l i a n s , h o w e v e r , these cell types i n birds are not c l e a r l y - d e f i n a b l e separate classes, but f o r m a m o r p h o l o g i c a l c o n t i n u u m . H a i r cells w i t h intermediate shape have been termed intermediate hair cells. In some papillae, a fourth type s i m i l a r to S H C has been r e c o g n i z e d (lenticular hair cells; S m i t h , 1985). U n l i k e i n the m a m m a l i a n hearing organ, not a l l h a i r - c e l l types are necessarily f o u n d throughout the a v i a n p a p i l l a . In a d d i t i o n , u n l i k e in m a m m a l s , a l l a v i a n hair cells are f i r m l y connected to the tectorial membrane.
A further d i f f e r e n c e , w h i c h has o n l y come to light through recent i n v e s - tigations, concerns the h a i r - c e l l o r i e n t a t i o n . In mammals, both I H C and O H C have their axis o f s t i m u l a t i o n ( p e r p e n d i c u l a r to the stereovillar bundle) oriented at or close to a right angle to the edge o f C o r t i ' s organ. A l t h o u g h early reports suggested that the situation in birds is the same (e.g. T a k a s a k a and S m i t h , 1971), this was an error. In the c h i c k ( T i l n e y et al., 1987), pigeon and starling ( G l e i c h and M a n l e y , 1988) and the barn o w l ( F i s c h e r et al., 1988) papillae, h a i r - c e l l o r i e n t a t i o n i n the center o f the a p i c a l part is rotated up to 90° towards the apex. T h e hair cell orientation changes back to 0° (i.e., abneural) towards both edges o f the p a p i l l a .
Structural similarities between the two types of papillae
In spite o f these considerable differences in m o r p h o l o g y , there are s t r i k i n g parallels, both i n the arrangement and structure o f hair cells and in the patterns o f afferent and efferent i n n e r v a t i o n . These convergences suggest that the p h y l o g e n e t i c development and o r g a n i z a t i o n o f a v i a n and m a m m a l i a n hearing organs were strongly i n f l u e n c e d by certain c o m m o n features. We suggest that these features are some o f the fundamental mechanisms o f stimulus processing i n vertebrate hair cells and i n h a i r - c e l l mosaics.
T h e structural s i m i l a r i t i e s between I H C and O H C on the one hand and T H C and S H C on the other can be s u m m a r i z e d as follows:
1) T h e relative placement o f the d i f f e r e n t cell types i n the respective papillae is almost the same. B o t h I H C a n d , i n general, T H C are not f o u n d over the free basilar m e m b r a n e . E x c e p t for a p i c a l T H C , they are situated w i t h i n the neural side o f the p a p i l l a , w h i c h overlies the superior cartilaginous plate i n birds and
Hair-cell populations in birds and mammals
the s p i r a l l a m i n a i n mammals ( S m i t h , 1985).
2) T h e hair cells l y i n g on the neural side o f the p a p i l l a are regarded as being the less s p e c i a l i z e d i n both vertebrate classes ( C h a n d l e r , 1984, T a k a s a k a a n d S m i t h , 1971).
3) L i k e I H C , T H C are usually e x c l u s i v e l y i n n e r v a t e d , that is, their afferents synapse o n l y w i t h one single hair c e l l ( L i b e r m a n , 1982; also see data b e l o w ) . A l t h o u g h Whitehead a n d M o r e s t (1985) f o u n d m a n y afferents w h i c h penetrated between t w o T H C and innervated both, this pattern is v e r y seldom in o u r data. In a d d i t i o n , both I H C a n d T H C are i n n e r v a t e d b y the b u l k o f the afferent fibers. In contrast, S H C , l i k e O H C , are i n n e r v a t e d n o n - e x c l u s i v e l y by a r e l a t i v e l y small percentage o f the afferent fibers ( m a m m a l 5 to 10%, starling 14%), w h i c h have small synaptic endings ( v o n D u r i n g et al., 1985;
S p o e n d l i n , 1979).
4) T h e efferent i n n e r v a t i o n o f both O H C and S H C is m a r k e d l y stronger than that to T H C or that to the afferent fibers o f I H C , and the synaptic endings are m u c h larger ( F i r b a s and M u l l e r , 1983; H i r o k a w a , 1978; S p o e n d l i n , 1979;
T a k a s a k a and S m i t h , 1971). A l s o , i n both cases, the i n n e r v a t i o n density o f efferents is higher i n the basal than i n the a p i c a l half o f the p a p i l l a .
5) T h e ontogenetic development o f the afferent a n d efferent i n n e r v a t i o n f o l l o w s very s i m i l a r patterns i n birds and mammals (Whitehead a n d M o r e s t ,
1985; P u j o l s al., 1978).
6) W i t h regard to their s e n s i t i v i t y to noise damage, both S H C a n d O H C tend to be the first to show m o r p h o l o g i c a l changes (Cotanche et al., 1987; L i b e r m a n and K i a n g , 1978; R o b e r t s o n , 1982).
A functional parallel in the two types of cochleae
T h e m o r p h o l o g i c a l parallels o u t l i n e d above have, to date, not been matched by equivalent f i n d i n g s o f s i m i l a r i t i e s i n the p h y s i o l o g i c a l responses of, f o r e x a m p l e , p r i m a r y nerve fibers. A l t h o u g h the response a c t i v i t y o f b i r d p r i m a r y afferents c e r t a i n l y does resemble that o f m a m m a l i a n afferents i n many respects, these s i m i l a r i t i e s are, i n general, features o f a l l vertebrate a u d i t o r y organs ( t o n o t o p i c i t y , frequency s e l e c t i v i t y , etc.). T h e r e are both q u a n t i t a t i v e a n d q u a l i t a t i v e differences i n the a c t i v i t y patterns o f p r i m a r y a u d i t o r y neurons o f birds a n d mammals ( M a n l e y et al., 1985; S c h e r m u l y et al., 1983; S c h e r m u l y and K l i n k e , 1985). E v e n though otoacoustic emissions w i t h features s i m i l a r to those o f mammals have been reported f r o m a b i r d species ( M a n l e y et al., 1987b) and the related C a i m a n ( K l i n k e a n d S m o l d e r s ,
1984), they have also been f o u n d i n a frog (Palmer a n d W i l s o n , 1981). T h u s , such p h e n o m e n a s h o u l d perhaps be attributed more to general properties o f hair cells than to unique properties o f hearing organs w i t h s p e c i a l i z e d h a i r - cell p o p u l a t i o n s . We report here an investigation o f the i n n e r v a t i o n patterns o f active afferent fibers i n t w o a v i a n species, where the results i n d i c a t e an u n e x p e c t e d a n d r e m a r k a b l e parallel to the situation i n m a m m a l s .
We have recently m a p p e d the tonotopic arrangement o f the basilar p a p i l l a o f t w o b i r d species, using H R P i n the c h i c k e n ( M a n l e y et al., 1987a) a n d the
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Figure 1 a , b : Light micrograph (a) and corresponding schematic drawing (b) of a 15 pm transverse section through the starling basilar papilla (bar-50 fim).
A single, cobalt-stained afferent auditory nerve fiber (CF=0.4 kHz:
threshold=45 dB SPL) runs to the seventh THC from the neural edge (left).
The fiber can be followed from the synapse through the habenula perforata and a short distance towards the cochlear ganglion The receptor epithelium ruptured from the basilar membrane during the histological procedure. For the same reason, the abneural part of the basilar papilla is missing.
QA: Higher-magnification micrograph (c) and schematic drawing (d) of a HRP-stained afferent auditory fiber in the same frequency range from a chick's basilar papilla synapsing with the second THC (bar=10 \im).
Abbreviations: BM basilar membrane, BP basilar papilla, HP habenula perforata, HC hair cells, LF labeled fiber, NF nerve fibers, NL neural limbus, TM tectorial membrane.
cobalt technique i n the starling ( G l e i c h , i n preparation; K o p p l a n d G l e i c h , 1988). In each case, we stained single a u d i t o r y - n e r v e cells or fibers i n the cochlear g a n g l i o n . F o l l o w i n g the investigation o f the frequency response characteristics o f i n d i v i d u a l fibers, either H R P or cobalt h e x a m m i n e c h l o r i d e
n r . of h a i r cell in c r o s s - s e c t i o n d i s t a n c e f r o m a p i c a l e n d (%)
Figure 2. Distribution of labeled and physiologically-characterized fibers in the basilar papilla of the starling with respect to their relative distance from the neural edge of the papilla. The CF is plotted against the location of the innervated hair cell as counted from neural to abneural in a transverse section.
The solid line indicates the abneural border of the sensory epithelium; the dotted line shows the location of hair cells with a 1:1 ratio of length to width. It is evident that, with two exceptions, all labeled fibers terminate on THC (O).
The two apical cells in the abneural region (x) innervated one and six hair cells, respectively (see text).
Figure 3. Second-order polynomial regressions of the distribution of CF of labeled auditory nerve fibers in the basilar papillae of the starling and in chicks of two different age groups (2nd postnatal day P2 and 21st day P21).
Starling: n=34; r2=0.79; chick, P2: n=13; r*=0.98; P21: n=8; r2=0.93.
was i n j e c t e d i o n t o p h o r e t i c a l l y t h r o u g h the electrode. A f t e r a s u r v i v a l time o f at least t w o hours, the animals were perfused t h r o u g h the heart a n d the c o c h l e a r ducts processed to d e v e l o p the stain. T h e cochleae were e m b e d d e d i n S p u r r , e x a m i n e d a n d measured both as w h o l e - m o u n t preparations a n d as serial sections. T h e p o s i t i o n o f the f i b r e terminations were measured f r o m the a p i c a l e n d , as the strong t w i s t i n g o f the basal e n d makes an accurate c o r r e c t i o n f o r the c u r v a t u r e more d i f f i c u l t . A s d i f f e r e n t cochleae d i f f e r i n length ( p a r t l y as a result o f d i f f e r e n t ages i n the c h i c k s ) , the locations o f the stained terminals ( F i g . 1) are g i v e n i n the f i g u r e as a percentage o f the distance f r o m the a p i c a l e n d . F u r t h e r details o n techniques are g i v e n i n the papers c i t e d .
T h e t o n o t o p i c arrangement i n both the s t a r l i n g a n d the c h i c k is u n r e m a r k - able; the f r e q u e n c y d i s t r i b u t i o n i n the s t a r l i n g c a n be represented as 0.33 m m / o c t , i n the c h i c k e n as about 0.6 m m / o c t . B o t h o f these values are o b t a i n e d f r o m linear regressions over the available range o f data. A s we have noted elsewhere, h o w e v e r , the d i s t r i b u t i o n o f octaves is not u n i f o r m i n vertebrate h e a r i n g organs ( M a n l e y et at., 1988). In b o t h the c h i c k a n d the
starling, less space is devoted to the l o w e s t - f r e q u e n c y octaves. I n the s t a r l i n g , where more data are a v a i l a b l e , a s e c o n d - o r d e r p o l y n o m i a l regression reveals that l o w frequencies are represented w i t h about 0.1 m m / octave, whereas m i d d l e - t o - h i g h frequencies o c c u p y 0.5 m m / o c t a v e ( F i g . 2). What is r e m a r k - able is the locations o f the s i n g l e - f i b r e stains w i t h respect to the w i d t h o f the papilla. A l l cases o f u n a m b i g u o u s single f i b r e s t a i n i n g were o f fibers w h i c h innervated T H C ( F i g . 3; M a n l e y et al., 1987a). O n l y i n cases o f o v e r s t a i n i n g , where m a n y fibers were i n a d v e r t e n t l y stained (this o n l y o c c u r r e d using H R P , these cases were not used i n the above analysis), d i d we f i n d stained fibers i n n e r v a t i n g S H C . W i t h t w o exceptions ( o f a total o f 54), we d i d not f i n d a n y cases i n w h i c h o n l y fibers to short hair cells were stained. These t w o exceptions were o f cells i n the s t a r l i n g , w h i c h had unusual response p r o p e r - ties; they were insensitive a n d e x t r e m e l y p o o r l y tuned to frequencies near 100 H z . T h e y i n n e r v a t e d one or several cells o n the abneural side o f the p a p i l l a . In our m a t e r i a l it was not possible to classify the i n n e r v a t e d h a i r cells as intermediate or short a c c o r d i n g to the c r i t e r i a o f T a k a s a k a a n d S m i t h (1971).
H o w e v e r , they were c e r t a i n l y not tall hair cells. A f f e r e n t fibres w i t h s i m i l a r response properties a n d i n n e r v a t i o n patterns have been reported i n the pigeon, where they appear to belong to a p o p u l a t i o n s p e c i a l i z e d f o r the reception o f i n f r a s o u n d ( K l i n k e a n d S c h e r m u l y , 1986).
We thus c o n c l u d e that, i n both species, a l l the neural recordings were f r o m single afferent fibers w h i c h innervate single T H C . T h i s is an u n e x p e c t e d parallel to the s i t u a t i o n i n m a m m a l s , where s i n g l e - f i b r e stains o f p r i m a r y afferents i n the cat a n d guinea p i g were e x c l u s i v e l y o f fibers i n n e r v a t i n g I H C ( L i b e r m a n a n d O l i v e r , 1984; R o b e r t s o n , 1984). T h e o n l y d o c u m e n t e d cases o f recordings f r o m afferent fibers to O H C i n d i c a t e d that, under e x p e r i m e n t a l conditions at least, these fibers do not respond to sound ( R o b e r t s o n , 1984).
T a k e n together, the a n a t o m i c a l a n d p h y s i o l o g i c a l data indicate that it is reasonable to expect that some o f the mechanisms u n d e r l y i n g the f u n c t i o n o f the h a i r - c e l l mosaics o f birds a n d mammals w i l l be v e r y s i m i l a r , i f not i d e n t i c a l . T h i s e x p e c t a t i o n increases the usefulness o f investigations i n a v i a n species w i t h respect to the understanding o f the f u n c t i o n o f c o m p l e x h e a r i n g organs a n d , more s p e c i f i c a l l y , to the e l u c i d a t i o n o f f u n c t i o n i n the m a m m a l i a n c o c h l e a .
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" A c t i v i t y patterns o f cochlear g a n g l i o n neurones i n the s t a r l i n g . " J . C o m p . P h y s i o l . 157, 1 6 1 - 1 8 1 .
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Comments
Evans:
H o w far can y o u push this i n t r i g u i n g analogy between m a m m a l i a n and b i r d cochleas? F u c h s has recently s h o w n e l e c t r i c a l t u n i n g o f tall hair cells i n the avian c o c h l e a . Does this mean we s h o u l d expect to f i n d , e v e n t u a l l y , e l e c t r i c a l t u n i n g i n m a m m a l i a n i n n e r h a i r cells (for w h i c h at present there is c o n t r a r y evidence) or are there real differences between m a m m a l i a n and a v i a n m e c h a - nisms o f f r e q u e n c y s e l e c t i v i t y ?
Fuchs, P.A., & Mann, A . C . (1986). "Voltage oscillations and ionic currents in hair cells isolated from the apex of the chick's cochlea." J. Physiol. 371, 31P.
Reply by Manley et al.:
O u r paper describes data w h i c h do not d i r e c t l y address the question o f the mechanisms o f f r e q u e n c y s e l e c t i v i t y i n birds and m a m m a l s , unless we imagine that the outer h a i r cells i n mammals and the short hair cells i n birds are necessary f o r c r e a t i n g appropriate m e c h a n i c a l c o n d i t i o n s for the t u n i n g o f inner a n d tall h a i r cells, respectively. A t present, we k n o w too little to seriously discuss this p o s s i b i l i t y . We ( M a n l e y et al., 1985) e m p h a s i z e d that, although m a n y characteristics o f the a c t i v i t y o f p r i m a r y a u d i t o r y nerve fibres of b i r d s s t r o n g l y resemble equivalent measures i n m a m m a l s , there are also consistent differences i n both the t u n i n g - c u r v e s y m m e t r y and the presence o f preferred intervals i n spontaneous a c t i v i t y . In the r e d - e a r e d turtle, such preferred intervals are correlated w i t h m e m b r a n e - p o t e n t i a l oscillations i n the hair cells a n d can be regarded as a neural i n d i c a t o r o f the presence o f electrical t u n i n g i n the h a i r c e l l . In the s t a r l i n g , such p r e f e r r e d intervals are characteristic o f l o w - f r e q u e n c y (< 1,5 k H z ) fibres. P r e f e r r e d intervals have also been reported i n some reptile preparations at l o w frequencies. A l t h o u g h
comments
there are f e w data o n l o w - C F fibres i n mammals i n the l i t e r a t u r e , G e i s l e r (pers. c o m m . ) c a r e f u l l y investigated m a n y l o w - C F fibres o f a m a m m a l a n d f o u n d no e v i d e n c e f o r p r e f e r r e d intervals i n the spontaneous a c t i v i t y . O n the other h a n d , o u r data f r o m reptiles suggests that the presence o f p r e f e r r e d intervals is correlated w i t h fibres o n l y i n n e r v a t i n g one single h a i r c e l l . T h e a v i a n t a l l - h a i r - c e l l fibres o n l y innervate one hair c e l l . In m a m m a l s , there is e v i d e n c e ( P u j o l , pers. c o m m . ) that the i n n e r v a t i o n pattern o f the m i d d l e - a n d b a s a l - t u r n h a i r - c e l l regions is not necessarily c o n t i n u e d i n the l o w - f r e q u e n c y a p i c a l - t u r n regions. I f a p i c a l - t u r n r a d i a l fibres i n m a m m a l s do not s i m p l y innervate one hair c e l l , then the absence o f p r e f e r r e d intervals i n p r i m a r y fibres does not necessarily mean that the hair cells are not e l e c t r i c a l l y t u n e d . T h u s , w h i l e we s h o u l d not necessarily expect to f i n d e l e c t r i c a l t u n i n g i n m a m m a l i a n h a i r cells, the present data do not c o m p l e t e l y rule it out.
N e v e r t h e l e s s , there are c o m m o n patterns across m a n y groups o f terrestrial vertebrates, w h i c h w o u l d suggest that certain f u n d a m e n t a l features o f f r e q u e n c y s e l e c t i v i t y r e m a i n e d unchanged i n the e v o l u t i o n along the various lines. O n e s u c h c o m m o n pattern is the consistent tendency f o r the a m o u n t o f space i n the h e a r i n g organ devoted to l o w - f r e q u e n c y octaves to be s u b s t a n t i a l l y less than the space devoted to h i g h - f r e q u e n c y octaves (see M a n l e y et al., 1988). In l i z a r d s , the l o w - C F area (below a p p r o x . 0.8 to 1.0 k H z ) is a n a t o m i c a l l y separated f r o m the one or t w o h i g h - C F areas. In at least some o f these cases, the presence o r absence o f strong a n a t o m i c a l gradients suggest a m i c r o m e c h a n i c a l l y - b a s e d frequency analysis o n l y i n the h i g h - C F area.
Wilson:
D o y o u t h i n k that the graded s e n s i t i v i t y o f hair cells across the basilar p a p i l l a c o u l d be due to d i f f e r i n g m e c h a n i c a l i n p u t levels to the stereocilia?
Reply by Manley:
T h e graded s e n s i t i v i t y may w e l l be due to a change i n the m e c h a n i c a l i n p u t to the h a i r c e l l s , a l t h o u g h this is somewhat c o u n t e r - i n t u i t i v e . A l m o s t a l l o f the tall h a i r cells are not f o u n d o n the free basilar m e m b r a n e , so that one m i g h t expect their m e c h a n i c a l i n p u t to be reduced c o m p a r e d to the short hair cells. H o w e v e r , o u r recent a n a t o m i c a l data indicate strong changes i n o r i e n t a t i o n o f hair cells across the a p i c a l h a l f o f the p a p i l l a o f the s t a r l i n g ( G l e i c h a n d M a n l e y , i n press). C l e a r l y , we s i m p l y k n o w too little about h a i r - c e l l s t i m u l a t i o n at present.
