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Structure of the Barn Owl's (Tyto alba) inner ear
231
Hearing Research, 11 (1985) 231-241 Elsevier
HRR
00585
Structure Catherine
of the Barn Owl’s
A. Smith’,
Masakazu
( 7”~
Konishi
alba) inner ear ’ and Nancy Schuff
’
’ Kresge Hearing Research Laboratocy, Medical School, Oregon Health Soences Center, Portland, Ore., and .’ CahJorma Instrtute of Technology, Pasadena, Cabi, (Received
The that the present unusual
25 October
1984; accepted
U.S.A. 13 February
1985)
basilar papilla of the Barn Owl’s (Tyto alba) cochlea was found to be 9.5-11.5 mm long. Histological examination revealed sensory hair cells had a characteristic distribution: The proximal half contained mostly typical short cells: tall hair cells were only on the distal half along with many short cells. Lenticular short cells occupied the proximal tip of the papilla. Another feature of the proximal part was a dense fibrous mass in the basilar membrane. This was absent from the distal one-fourth.
Barn Owl, cochlea,
cochlear
hair cell, basilar
membrane
Introduction Hearing in birds has been the subject of a number of investigations in recent years and it has been found that most birds have a peaked audiogram with good sensitivity over a narrow range [5]. The Barn Owl (Tyto afba) is one exception, for this bird’s hearing is very good at 2-9 kHz [9]. Schwartzkopf and Winter [15] and Schwartzkopf [14] demonstrated that the cochleas of owls are longer than those of many other birds but details of microscopic structure of the basilar papilla have not been previously available. The question arose as to whether there might not be some other specializations within the owl’s cochlea besides its length which could account for this unusual avian sound reception. The present studies have revealed that the basilar papilla of Tyto alba has two unique features: a proliferation of lenticular short cells and a thickening of the basilar membrane, both on the basal end. Materials and methods The ears from three Barn Owls were studied. These were fixed at the laboratories of one of us (M.K.) by the intravascular perfusion of 1% for0378-5955/85/$03.30
0 1985 Elsetier
Science Publishers
maldehyde (made from paraformaldehyde) plus 1.25% glutaraldehyde in a 0.1 M phosphate buffer, pH 7.3. The two temporal bones were then removed from the skull (still attached at the midline), immersed in the fixative and shipped by Express Mail to C.A.S. where the processing was completed. The length of time in the aldehyde varied from 5 (No. 768) or 6 days (No. 767) to 27 days (No. 769). They were post-fixed in 1% 0~0, in 0.1 M phosphate buffer (without previous wash) by intra-labyrinthine perfusion with the pipette inserted through the round window membrane permitting outflow through the open oval window. The ears were post-fixed for lf h and then dehydrated in ethanol. The bone over the tegmentum vasculosum was thinned and small spicules removed in order to facilitate penetration of the embedding media. The cochlear duct from round window to macula of the lagena was thus exposed. Dehydration was completed and the entire bone embedded in Araldite. Measurements were made on the dissected basilar papillas with, as well as without, the macula of the lagena, both in the fixative and after embedding in Araldite. The measurements were made roughly by means of cut suture thread lengths as well as by caliper. The hardened Araldite blocks
B.V. (Biomedical
Division)
238
Microscopic
have been found in other birds. The basilar papilla is formed by supporting and sensory cells arranged in a compact mass on a fibrous basilar membrane. The free apical surfaces of hair cells and supporting cells are covered by a thick tectorial membrane which has a wide attachment zone at the epithelial cells on the ‘superior’ side *. The basilar membrane is suspended between the two fibro-cartilaginous plates and separates the perilymph of Scala tympani from the endolymph of scala media. A heavy tegmentum vasculosum closes off the scala media (Fig. 1). The basilar papilla changes in width from proximal to distal ends being the same width as the basilar membrane proximally but somewhat wider in the distal part where it encroaches upon the superior fibro-cartilaginous plate (Fig. 2). The supporting cells of the basilar papilla as well as the tectorial membrane are very similar to those previously described in the pigeon [20] and in the chicken [21,22] and will not be considered here. However, sensory cell distribution and basilar membrane structure at the proximal end of the Barn Owl’s cochlea are unique and these features are described in detail below. (b) Sensory cell structure and distribution. The sensory cells may be divided into three major types, tall, intermediate and short (Fig. 2) on the basis of previous descriptions [20]. The tall hair cells have a height that is greater than surface diameter. This type of cell is present only on the distal half of the Barn Owl’s papilla (Figs. 2 and 3). There are no tall cells at all on the proximal one-half, although a few intermediate cells are present. The tall hair cells make their first appearance at about 5 mm from the proximal end and increase steadily in number toward the distal end, where they are the predominant, and at the tip the only, type of hair cell. The intermediate cells are more widely distributed over the papilla but are not numerous at any place (Fig. 3). The short hair cells have enlarged apical ends, the diameters of which are greater than their heights. These sensory cells include the type common ih other birds, i.e., a type with broad apical
(1) Basilar papilla (a) General features. The Barn Owl’s cochlear duct has the same general structural features that
* ‘Superior’ and ‘inferior’ are used in the same context as in the description of the pigeon’s papilla [20].
were then divided into two pieces and l-pm serial sections cut and stained with toluidine blue. The ears from owls Nos. 767 and 768 had dissection artifacts in some locations and were not sectioned in entirety. Both ears from owl No. 769 had section samples cut from proximal to distal ends: 50 to 100 l-pm sections were cut at approximately 0.5-l mm intervals. This resulted in lo-14 samplings (of 0.1 mm each) along the papilla. Measurements of the basilar membrane and its related structures were made microscopically at 400 x magnification by means of a calibrated eyepiece micrometer. Camera lucida drawings of the papilla and basilar membrane structures were made at 600 x in order to clarify their relationships along the length of the basilar membrane. Thin sections were cut for electron microscopy with a diamond knife from the right ear of owl No. 768 at a position approximately 2.0 mm from the proximal end. They were stained with uranyl acetate and lead citrate and photographed in a Philips EM 300. Results Macroscopic The membranous cochlear duct contains the basilar papilla and related, nerve fibers, the tectorial membrane, the tegmentum vasculosum and the macula of the lagena. The duct is slightly curved (approximately 110’ for owl 767 left). The length varied in the birds examined. Total length of the duct of 767 L including the lagenar macula was 12 mm. The distal rip of this bird’s duct was curved back on the papilla. The basilar papilla alone was 10.5 to 11 mm in length. The length of 768 left was similar: the cochlear duct, 12.5 mm and basilar papilla, 11.5 mm in length. The third owl (769) had a slightly shorter auditory receptor organ: the basilar papilla of the right ear was 9.5 mm long. There was little difference in measurements made before and after embedment.
239
Fig. 1. Cross-section of the cochlear duct of owl No. 769 at 5.6 mm from the proximal end, showing basilar membrane (BM) which is suspended between the superior (SP) and inferior fibro-cartilaginous points between which width of basilar membrane was measured. SM: Scala media; ST: scala tympani; tegmentum vasculosum. Mag. 112 x
end covered by a cuticular plate. This common type of short cell has a wider distribution than the tall hair cells in the Barn Owl: it can be found on all parts of the papilla except for the proximal and distal tips. The distal tip is occupied exclusively by tall hair cells; the proximal tip is occupied by the lenticular cells (Figs. 2 and 3). The lenticular cells (an uncommon type of short cell) have a large luminal surface (Figs. 2a and 4) but only about one-third of this free area is covered by the cuticular plate. They can be differentiated from the other short cells even at a light-microscopic level of magnification, because the cuticular plate plus ciliary bundle is on the ‘superior side’ * of the cell. The ciliary bundles of other short cells (common or hemispherical) are on the ‘inferior’ side or more centrally placed. The lenticular cells are quite numerous on the proximal one-third of the papilla and seem to be the only type of sensory cell present on the first millimeter of basilar membrane. The number and types of hair cells visible in
* ‘Superior side’: toward tectorial membrane.
the
wide
attachment
site of the
the basilar papilla (BP) on the plates (IP). Arrows indicate TM: tectorial membrane; TV:
cross sections were counted from the left ear of owl 769 and plotted in Fig. 3. The papilla of 769 was serial-sectioned in its entirety. Dissection artifacts prevented the use of complete papillae from owls 767 and 768 and a composite was made from 767 right and left and 768 right. Hair cell populations were the same in all three birds. There are 3 to 4 hair cells across the papilla at the proximal tip. The number rapidly reaches ten within the first millimeter with minimal changes for the next three millimeters. After about the four millimeter point, numbers increase more rapidly to a maximum of about 35 in 769, and 43 in the longer cochleas. Electron micrographs of hair cells of the proximal end from 768 R gave evidence that these cells were similar to the lenticular cells described earlier in the chicken [22]. Figs. 2a and 4 show typical lenticular cells. The cuticular plate with the cilia is toward the superior side of the papilla. A large part (half to two-thirds) of the apical cell membrane exposed to the endolymph is without cuticular plate. The ellipsoidal nucleus occupies a large part of the cytoplasm below. A moderate sized nerve ending filled with small round vesicles and opposite a sub-synaptic cisterna within the hair
240
Fig. 2. Cross-sections of the basilar papilla (owl No. 769) at three different positions along the basilar membrane showing the differences in hair cell distribution and structure of the basilar membrane. ,A11at same magnification: 280 x . (a) 2.25 mm, from proximal end, with typical short (S) and lenticolar (L) hair cells. The basilar membrane was ruptured at left and the tectorial membrane (TM) pulled away from the papilla during dissection. DFM, dense fibrous mass; LFM, loose fibrous mass. Arrows indicate part of basilar membrane shown in Fig. 5. (b) 5.6 mm from proximal end, with a few tall (T) and many typical short (S) hair cells. The DFM and LFM are quite prominent. B, border cells. (c) 8.7 mm from proximal end, showing many tall (T’) and short (S) hair cells. Note that the DFM no longer exists at this point and that LFM is much thinner.
241
:
40
40
;3O
30
= 20
20 IO
.z IO P 0
I
2
3 Length
4 of Basilar
5
6 Membrane
7
0
9
10
(mm)
Fig. 3. Graph showing the distribution of the three types of hair cells (owl No. 769) along typical short as well as the lenticular short hair cells.
cell is visible at right. Other lenticular cells also had small neural boutons which were apparently efferent nerve endings. Except for the location and type of nerve endings, these cells look much like flattened tall hair cells with one side at the surface of the papilla instead of being buried among the supporting cells. (2) Basilar membrane The basilar membrane is a fibrous, extracellular structure (Figs. 1 and 2) similar to basilar membranes of all vertebrates. In birds it is attached to the two fibro-cartilaginous plates. For descriptive purposes, it will be separated into a
the basilar
membrane.
‘Short’
includes
vestibular part which is composed of a packed fibrous matrix and a tympanic portion, composed of loosely arranged fibers, which appears as an appendage projecting into Scala tympani. Actually, the two parts are continuous and the terms used here only reflect different organizations of the fibers. (a) The vestibular part. The vestibular surface of the basilar membrane is completely covered by a large number of supporting cells plus a few border cells at the inferior edge (Fig. 2). Inside the supporting cell basal plasma membrane is a series of structures resembling hemidesmosomes (Fig. 5). A well-defined basal lamina separates the cells
Fig. 4. Electron micrograph of lenticular hair cell from the proximal end of owl No. 768. The cuticular plate (C) occupies the left half of cell surface. The right half of the apical cell membrane has no cuticular plate. E, efferent nerve ending; EN, endolymph; N. nucleus; SC, supporting cell; ST, stereocilia. Mag. 9400 X
Fig. 5. Electron micrograph of part of basilar membrane (location between arrows in Fig. 2a) showing the edge of the DFM as it merges with the remainder of the basilar membrane. The fine webby material of the LFM is visible below. BL, basal lamina; SC. supporting cells. Mag. 6000 x
from the basilar membrane fibers (Figs. 5 and 6). Toward the distal end of the papilla, the entire basilar membrane is relatively thin (Fig. 2~). The basilar membrane in the proximal half is considerably different in appearance due to the presence of a thick fibrous mass, spindle-shaped in cross-section. The basilar membrane and papilla do not co-exist at the proximal tip because the basilar papilla including the hair cells extends slightly further toward the vestibule than does the basilar membrane. In 767 R the structure of the basilar membrane was clearly defined at about 0.2 mm from the papillar tip. It was 91 nm in width and contained within it (toward the inferior edge) a spindle-shaped mass of closely packed fibers, the dense fibrous mass (DFM). The DFM was 37 pm wide, 8.5 pm in thickness and occupied an area 40% of the basilar membrane’s width. The basilar papilla above it had seven hair cells in cross-section, all lenticular in type. The DFM rapidly acquires a thickness of approximately 10 nrn and this increases only slightly in the next 5-6 mm (Figs. 2 and 7). Fig. 2a shows a section taken at 2.25 mm from the proximal end (769 R) where the DFM
Fig. 6. Higher magnification basal lamina; SC, supporting
of the fibers in the DFM. cell. Mag. 43000 X
BL.
243
was 57 pm in width and 11 pm in thickness. The width does increase and continues to do so until at 6-7 mm it reaches a maximum of 105-110 pm (Fig. 7). The DFM in Fig. 2b occupies 62% of the width of the basilar membrane. After 7 mm it gradually diminishes in thickness and within another millimeter it is hardly noticeable and has lost its distinctive character (Figs. 2c and 7). The vestibular part of the basilar membrane then continues to its distal terminus as a fairly (but not entirely) homogenous layer of compacted fibers. The superior one-third (Fig. 2c) is thinner, a difference which is accompanied by an array of adjacent supporting cell nuclei. Electron micrographs (Figs. 5 and 6) demonstrated that the DFM was composed of closely packed fibers with their longitudinal dimension for the most part positioned in a radial direction. Either the fibers are branched or there are also shorter fibers running at a direction other than that of the radial preponderance. At the tympanic edge of the density (Fig. 5), cords of longer radial fibers are visible which seem to have short perpendicular arms.
DENSE
LENGTH
I1
0
FIBROUS
OF
-
I
LENGTH
BASILAR
0.0
MASS
(769)
MEMBRANE
1
I
I
(mm)
a4
2345676910 OF
BASILAR
MEMBRANE
(mm)
Fig. 7. Graphs showing, above, the width changes of the DFM along the basilar membrane and, below, the changes in thickness. ‘Thickness’ was measured at the point of greatest thickness in cross-section.
(b) The tympanic part. The loose fibrous mass (LFM) projects into the perilymph of Scala tympani (Figs. 1 and 2). It underlies that part of the basilar membrane which is covered by the sensory cells but it does not extend to the border cell area (Fig. 2a, b, c). There is often a cluster of cells beneath the basilar membrane covered by the border cells but the basilar membrane itself is thin in this region (Fig. 2b). Electron micrographs (Fig. 5) show that the webby material which is the largest component of the dispersed LFM is continuous with the same type of material in the vestibular part of the basilar membrane. This fine webby background material may actually be compacted with the parallel fibers in the DFM. Only thin, discontinuous cords of fibers separate vestibular and tympanic parts. Cords of packed fibers are visible at the pendulous tympanic edge of the LFM in the proximal part of the papilla (Fig. 2a) but are more scattered throughout the mass more distally (Fig. 2b, c). A few spindle-shaped cells can be found within the LFM. Other cells (similar to the mesothelial layer in mammals) cover the tympanic surface and continue over the cartilaginous plates. The loose fibrous mass arises at the proximal tip along with the dense fibrous mass but the LFM covers a considerably greater width of basilar membrane than does the DFM (Fig. 2a, b). In 769 L, its greatest thickness of approximately 25 pm was achieved at about 1 mm from the proximal end. This thickness was fairly consistent up to 7 mm (except at the 2.7 mm position where it dipped to 16 pm). The thickness decreased rapidly over the next 2 mm and the LFM was absent from the distal tip. (c) Dimensions. The width of the basilar membrane was measured between its two attachment points at the superior and inferior cartilaginous plate crests (Fig. 1). The basilar membrane was almost 0.1 mm wide at its proximal end and reached a maximum of approximately 0.35 mm at the distal end in 769 R (Fig. 8). The proximal tip of the membrane (the first 50-75 pm) is narrower than 0.1 mm, but the membrane is very thick and poorly formed at this point and probably nonfunctional, At the point where it appears to have achieved its normal structure (at 0.15 mm) it was already 88 pm wide in 769 R. The basilar mem-
2
0.5-
s y 0.4-
!t 5
0
769 768 +--f 767 O---O
PROXIMAL L t ‘1 I 2 3 4
‘ 5
1 6
L 7
a 8
@ L 9 IO
DISTAL I ., It 12 13
LENGTH OF BASILAR MEMBRANE (mm) Fig. 8. Graph showing width changes of basilar membrane from proximal to distal end. The curves for owls Nos. 767 and 768 are incomplete (immeasurable in part due to dissection artifacts) but at the points where they overlap (8.5-9.5 mm) correspondence is very good. Both 767 and 768 had longer cochleas.
brane of 768 R, which was approximately 11.75 mm in length, achieved a width of 0.470 mm before rounding off sharply. The shape of the <
0.5
E
BARN OWL
( 769)
curves from all of the birds (767, 768 and 769) were very similar when width was plotted against length (Fig. 8). The slope was gradual and gentle
o-----o o---e
3
0.4
5 g
0.3
% g
0.2
a g
0.1 DISTAL
PERCENTAGE OF LfiNGTH OF 6A6lLAR
MEM6RANE
Fig. 9. Changes in the width of the basilar membrane of owl No. 769 plotted against percent of basilar membrane length and compared with curve from the guinea pig, taken from Fernandez 161.
245
from one to seven millimeters and then took a sharp upward turn. At that point, the curves of the longer ears (767 and 768) were shifted slightly to the right. There is an overall increase in width of 3.5-4.5 fold from proximal to distal ends, but this increase is quite irregular. Fig. 8 illustrates that the change in width is negligible for the first 2 mm. There is then a gradual 50% increase up to about 5-6 mm and a region of one-half to 1 mm where the width is more static. After that width changes are more rapid. When the data are presented with width relative to percentage of length of the basilar membrane (Fig. 9), it becomes more apparent that the width curve rises steeply over the distalmost 25% of the papilla. There is also a correspondingly larger number of hair cells in this region. Discussion
Evidence has accumulated that the auditory receptor organs of most birds have certain common structural features. The basilar papilla is formed by an organized cluster of sensory cells and supporting cells which is covered by a thick tectorial membrane. The basilar membrane is narrow and elongated but not as long as in mammals of comparable size. Schwartzkopf and Winter in Schwartzkopf [14] examined the inner ears of a number of bird species and found the longest cochlear ducts in Tyto alba (Barn Owl), Strix &co (Tawny Owl) and Bubo bubo (Eagle Owl). The present studies have confirmed this feature for Tyto alba and have further revealed that this bird has other structural features that are unique: a distinctive arrangement of sensory cell types and a localized thickening of the basilar membrane. The basilar membrane has two thickenings, the vestibular dense fibrous mass (DFM) and the tympanic loose fibrous mass (LFM). The latter is present in other birds. It can be readily detected in published micrographs of the pigeon [20] and the chicken [22], although this particular feature was not discussed in those publications. Reexamination of the basilar membranes from the parakeet (Melopsittucas unduhtus) and the House Sparrow (Passer domesticus) revealed that tympanic masses were also present in these species [18]. According
to data available at present, then, the dispersed tympanic mass seems to be a common feature in birds. The dense vestibular fibrous mass, however, has not been found in pigeon, chicken, parakeet or sparrow, and in birds, it may be unique to the Barn Owl. Basilar membrane specializations have been reported in a few mammals. Pye found thickenings in the kangaroo rat [II] and in some Chiroptera [12]. Henson [7] has reported basilar membrane thickenings in the Moustache Bat (Pteronotus p. parnellii). In most cases, the thickenings seem to be similar to the tympanic mass (LFM) in birds although it is difficult to make comparisons because of differences in preparation techniques. Thickenings in the mammalian basilar membrane which seem to be most similar to those of Tyto ulbu were described by Bruns [3] for the Horseshoe Bat (Rhinolophus ferrumequinum). He found a vestibular, as well as a tympanic, component. Both of those were thickest in the basalmost 4.7 mm. Only the vestibular thickening persisted toward the apex. More recently, Wilson and Bruns [23] have measured basilar membrane movements in the Horseshoe Bat’s ear by use of a capacitive vibration probe. They found there were phase shifts between measurements made on thickenings in the Pars Tecta and Pars Pectinata on the same segment of basilar membrane but that the shifts were variable and not always present. It is probable that the effect of the thickenings is to facilitate high frequency hearing in both classes although the high frequency sensitivity of bat and owl actually is quite different (respectively 80 and 7 kHz). In addition, the thickenings may be an important factor in the excellent high-frequency discrimination which has been demonstrated in the Barn Owl [13]. It may not be possible to compare the damping qualities of basilar membrane thickenings in bird and mammal because of other structural variables between the two classes. The cellular mass of the bird’s basilar papilla is quite different from that of the organ of Corti. Furthermore, hair cell stimulation may not be equivalent because avian sensory cell cilia have a stronger attachment to the tectorial membrane [21]. Possibly the thickenings are important in temporal qualities of sound reception. Indeed, behavioral as well as neurophysio-
246
logical studies point toward a remarkable temporal resolution in the Barn Owl’s audition [10,19]. Two distinct patterns of sensory ceil distribution were found on the proximal and distal halves of the Barn Owl’s cochlea. The proximal half was occupied by large numbers of short hair cells and an occasional intermediate cell. On the distal half there were many tall and short hair cells with a few intermediates in between. The large number of the lenticular type of short hair cells on the proximal portion was remarkable. Lenticufar cells are an unusual type of inner ear sensory cell. They were first described by Baird in the Caiman ear [l]. Tanaka and Smith [22] found a few on the basal tip of the chicken’s papilla but they do not seem to be present in parakeet, pigeon or sparrow. Their abundance on the proximal-most two millimeters of the Barn Owl’s papilla and presence in a very limited degree in the same location in the chicken might indicate that they play some role in high frequency reception. Variables in the distribution of sensory cell types seem to be a common feature in the papillae of birds. These variations have been previously observed in the cochleas of the pigeon, chicken, House Sparrow and parakeet [U-18]. The Barn Owl can now be added to the list and its sensory cell pattern is dissimilar from all the others thus far examined. Neurophysiological studies [8] in a number of species showed that different species had similar low-frequency sensitivity but different high-frequency cut-off points. Perhaps one way in which birds achieve this selective sensitivity is by special arrangements of cell types. Basilar membrane dimensions (as well as thickenings, etc.) are likewise important. The basilar membranes of the cochleas of mammals vary in length from 7 mm in the mouse to 50 mm in the elephant [Z] but, with the exception of some bats, the width invariably shows a fairly regular increase from basal (high frequency) to apical end (low frequency). Such an increase is also present in the chicken [18]. Although basilar membrane measurements were not made on the pigeon 1201a systematic increase in the cell numbers might indicate a comparable increase in basilar membrane width. On the other hand, the basilar membranes of some small birds have quite variable dimensions [16,17]. The 2.3 mm long
membrane of the parakeet shows little change in width in the distal 1.5 mm. The width of the long basilar membrane of Qro albu changes only negligibly in its proxima1 quarter, has a 50% increase for several millimeters up to midpoint, and then a more rapid increase to the distal tip where it is somewhat more than three times that of the proximal end. Width changes in the first 5-7 mm of the Barn Owl’s basilar membrane are not too different from those of the guinea pig as measured by Fernandez f63, although the bird’s slope is more gentle. At the 7 mm (9 mm in the longer cochleas) point the slope takes a sudden upturn. If the Barn Owl and guinea pig width changes are plotted relative to percentage of basilar membrane length (Fig. 9), a sharp upcurve at approximately 75% of the basilar membrane length is seen to be present in Barn Owl but not the guinea pig. However, a very similar type of sharp terminal curve was described by Cabezudo [4] for the cat. Whatever the significance of the irregularities in basilar membrane width may be, there seems little doubt that the unusual length of the Barn Owl’s basilar membrane is related to its wide frequency sensitivity band. It seems probable that the basilar membrane thickening and peculiar hair cell arrangement likewise play a significant role in its special hearing properties. Aeknawkdgements
The authors thank Donna Himes and Jill Lilly for their expert assistance with the graphs and typing. This work was supported in part by NIH grants Nos. 08813 and 14617. References Baird, I.L. (1974): Anatomical features of the inner ear in submammalian vertebrates. In: Handbook of Sensory Physiology, pp. 197-198. Editors: H. Autrum, R. Jung, W. Lowenstein, D. McCay and H. Teuber. Springer-Verlag, New York. MkCsy, G. von (1960): Experiments in Hearing, pp. 504-510. McGraw-Hill, New York. Bruns, V. (1976): Peripherat auditory tuning for fine frequency analysis by the CF-FM bat, Rhidophus firrumequinum. .l. Comp. Physiology 106, 77-86. Cabezudo, L.M. (1978): The ultrastructure of the basilar membrane in the cat. Acta Otolaryngof. 86, 160-175.
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5 Dooling. R.J. (1980): Behavior and psychophysics of hearing in birds. In: Comparative Studies of Hearing in Vertebrates, pp. 261-288. Editors: A.N. Popper and R.R. Fay. Springer-Verlag, New, York. 6 Fernandez. C. (1952): Dimensions of the cochlea (guinea pig). J. Acoust. Sot. Am. 24. 519-523. 7 Henson. M. (1978): The bastlar membrane of the bat, !‘teronoru.s p. purnellii. Am. J. Anat. 153, 143-158. 8 Konishi. M. (1970): Comparative neurophysiological studtes of hearing and vocalizations in songbirds. Z. Vergl. Phystol. 66. 257-212. 9 Komshi. M. (1973): How the owl tracks its prey. Am. Sci. 61. 414-424. 10 Moiseff. A. and Konishi. M. (1981): Neuronal and behavioral sensitivity to binaural time differences in the owl. J. Neurosci. 1. 40-48. 11 Pye. A. (1965): The auditory apparatus of the HereromCfue (Rodentia. Scruromorpho). J. Anat. 99, 161-174. 12 Pye. A. (1966): The structure of the cochlea in Chiroptera, I Mmwhmppreru: Emhullonurordeu and Rhonolophoiderr. J. Morphol. 118, 495-510. 13 Quine. D.B. and Konishi, M. (1974): Absolute frequency discrmination in the Barn Owl. J. Comp. Physiol. 93. 3477360. 14 Schwartzkopf. J. (1968): Structure and function of the ear and of the auditory brain areas in birds. In: Hearing Mechanisms in Vertebrates, pp. 41-58. Editors: A.V.S. de Reuck and J. Knight. Little, Brown and Co., Boston.
15 Schwartzkopf, J. and Winter, P. (1960): Zur Anatomie der Vogel-Cochlea unter natiirlichen Bedingungen. Biol. Zbl. 79. 607-625. 16 Smtth, C.A. (1981): Recent advances in structural correlates of auditory receptors. In: Progress in Sensory Physiology 2. pp. 135187. Editor: D. Ottoson. Springer-Verlag. New York. 17 Smith. C.A. and Tanaka. K. (1981): Further observations on the avian basilar papilla. In: Abstr. ARQ 4th Meeting. pp. 79980. Association for Research in Otolaryngology. 18 Smith, C.A. and Tanaka. K. Unpublished data. 19 Sullivan, W.E. and Konishi. M. (1984): Segregation of sttmulus phase and intensity coding in the cochlear nucleus of the Barn Owl. J. Neurosct. 4. 178771799. 20 Takasaka. T. and Smith, C.A. (1971): The structure and innervation of the pigeon’s basilar papilla. J. Ultrastruct. Res. 35. 20-65. 21 Tanaka, K. and Smith, C.A. (1975): Structure of the avian tectorial membrane. Ann. Otol. Rhinol. Laryngol. 84, 287-291. 22 Tanaka. K. and Smith, C.A. (1978): Structure of the chicken’s inner ear. Am. J. Anat. 153. 251-271. 23 Wilson, J.P. and Bruns. V. (1983): Basilar membrane tuning properties in the specialized cochlea of the CF-bat. Rhrnolophus Jerrumequinum. Hearing Rea. 10. 15-36.
Hearing Research, 11 (1985) 231-241 Elsevier
HRR
00585
Structure Catherine
of the Barn Owl’s
A. Smith’,
Masakazu
( 7”~
Konishi
alba) inner ear ’ and Nancy Schuff
’
’ Kresge Hearing Research Laboratocy, Medical School, Oregon Health Soences Center, Portland, Ore., and .’ CahJorma Instrtute of Technology, Pasadena, Cabi, (Received
The that the present unusual
25 October
1984; accepted
U.S.A. 13 February
1985)
basilar papilla of the Barn Owl’s (Tyto alba) cochlea was found to be 9.5-11.5 mm long. Histological examination revealed sensory hair cells had a characteristic distribution: The proximal half contained mostly typical short cells: tall hair cells were only on the distal half along with many short cells. Lenticular short cells occupied the proximal tip of the papilla. Another feature of the proximal part was a dense fibrous mass in the basilar membrane. This was absent from the distal one-fourth.
Barn Owl, cochlea,
cochlear
hair cell, basilar
membrane
Introduction Hearing in birds has been the subject of a number of investigations in recent years and it has been found that most birds have a peaked audiogram with good sensitivity over a narrow range [5]. The Barn Owl (Tyto afba) is one exception, for this bird’s hearing is very good at 2-9 kHz [9]. Schwartzkopf and Winter [15] and Schwartzkopf [14] demonstrated that the cochleas of owls are longer than those of many other birds but details of microscopic structure of the basilar papilla have not been previously available. The question arose as to whether there might not be some other specializations within the owl’s cochlea besides its length which could account for this unusual avian sound reception. The present studies have revealed that the basilar papilla of Tyto alba has two unique features: a proliferation of lenticular short cells and a thickening of the basilar membrane, both on the basal end. Materials and methods The ears from three Barn Owls were studied. These were fixed at the laboratories of one of us (M.K.) by the intravascular perfusion of 1% for0378-5955/85/$03.30
0 1985 Elsetier
Science Publishers
maldehyde (made from paraformaldehyde) plus 1.25% glutaraldehyde in a 0.1 M phosphate buffer, pH 7.3. The two temporal bones were then removed from the skull (still attached at the midline), immersed in the fixative and shipped by Express Mail to C.A.S. where the processing was completed. The length of time in the aldehyde varied from 5 (No. 768) or 6 days (No. 767) to 27 days (No. 769). They were post-fixed in 1% 0~0, in 0.1 M phosphate buffer (without previous wash) by intra-labyrinthine perfusion with the pipette inserted through the round window membrane permitting outflow through the open oval window. The ears were post-fixed for lf h and then dehydrated in ethanol. The bone over the tegmentum vasculosum was thinned and small spicules removed in order to facilitate penetration of the embedding media. The cochlear duct from round window to macula of the lagena was thus exposed. Dehydration was completed and the entire bone embedded in Araldite. Measurements were made on the dissected basilar papillas with, as well as without, the macula of the lagena, both in the fixative and after embedding in Araldite. The measurements were made roughly by means of cut suture thread lengths as well as by caliper. The hardened Araldite blocks
B.V. (Biomedical
Division)
238
Microscopic
have been found in other birds. The basilar papilla is formed by supporting and sensory cells arranged in a compact mass on a fibrous basilar membrane. The free apical surfaces of hair cells and supporting cells are covered by a thick tectorial membrane which has a wide attachment zone at the epithelial cells on the ‘superior’ side *. The basilar membrane is suspended between the two fibro-cartilaginous plates and separates the perilymph of Scala tympani from the endolymph of scala media. A heavy tegmentum vasculosum closes off the scala media (Fig. 1). The basilar papilla changes in width from proximal to distal ends being the same width as the basilar membrane proximally but somewhat wider in the distal part where it encroaches upon the superior fibro-cartilaginous plate (Fig. 2). The supporting cells of the basilar papilla as well as the tectorial membrane are very similar to those previously described in the pigeon [20] and in the chicken [21,22] and will not be considered here. However, sensory cell distribution and basilar membrane structure at the proximal end of the Barn Owl’s cochlea are unique and these features are described in detail below. (b) Sensory cell structure and distribution. The sensory cells may be divided into three major types, tall, intermediate and short (Fig. 2) on the basis of previous descriptions [20]. The tall hair cells have a height that is greater than surface diameter. This type of cell is present only on the distal half of the Barn Owl’s papilla (Figs. 2 and 3). There are no tall cells at all on the proximal one-half, although a few intermediate cells are present. The tall hair cells make their first appearance at about 5 mm from the proximal end and increase steadily in number toward the distal end, where they are the predominant, and at the tip the only, type of hair cell. The intermediate cells are more widely distributed over the papilla but are not numerous at any place (Fig. 3). The short hair cells have enlarged apical ends, the diameters of which are greater than their heights. These sensory cells include the type common ih other birds, i.e., a type with broad apical
(1) Basilar papilla (a) General features. The Barn Owl’s cochlear duct has the same general structural features that
* ‘Superior’ and ‘inferior’ are used in the same context as in the description of the pigeon’s papilla [20].
were then divided into two pieces and l-pm serial sections cut and stained with toluidine blue. The ears from owls Nos. 767 and 768 had dissection artifacts in some locations and were not sectioned in entirety. Both ears from owl No. 769 had section samples cut from proximal to distal ends: 50 to 100 l-pm sections were cut at approximately 0.5-l mm intervals. This resulted in lo-14 samplings (of 0.1 mm each) along the papilla. Measurements of the basilar membrane and its related structures were made microscopically at 400 x magnification by means of a calibrated eyepiece micrometer. Camera lucida drawings of the papilla and basilar membrane structures were made at 600 x in order to clarify their relationships along the length of the basilar membrane. Thin sections were cut for electron microscopy with a diamond knife from the right ear of owl No. 768 at a position approximately 2.0 mm from the proximal end. They were stained with uranyl acetate and lead citrate and photographed in a Philips EM 300. Results Macroscopic The membranous cochlear duct contains the basilar papilla and related, nerve fibers, the tectorial membrane, the tegmentum vasculosum and the macula of the lagena. The duct is slightly curved (approximately 110’ for owl 767 left). The length varied in the birds examined. Total length of the duct of 767 L including the lagenar macula was 12 mm. The distal rip of this bird’s duct was curved back on the papilla. The basilar papilla alone was 10.5 to 11 mm in length. The length of 768 left was similar: the cochlear duct, 12.5 mm and basilar papilla, 11.5 mm in length. The third owl (769) had a slightly shorter auditory receptor organ: the basilar papilla of the right ear was 9.5 mm long. There was little difference in measurements made before and after embedment.
239
Fig. 1. Cross-section of the cochlear duct of owl No. 769 at 5.6 mm from the proximal end, showing basilar membrane (BM) which is suspended between the superior (SP) and inferior fibro-cartilaginous points between which width of basilar membrane was measured. SM: Scala media; ST: scala tympani; tegmentum vasculosum. Mag. 112 x
end covered by a cuticular plate. This common type of short cell has a wider distribution than the tall hair cells in the Barn Owl: it can be found on all parts of the papilla except for the proximal and distal tips. The distal tip is occupied exclusively by tall hair cells; the proximal tip is occupied by the lenticular cells (Figs. 2 and 3). The lenticular cells (an uncommon type of short cell) have a large luminal surface (Figs. 2a and 4) but only about one-third of this free area is covered by the cuticular plate. They can be differentiated from the other short cells even at a light-microscopic level of magnification, because the cuticular plate plus ciliary bundle is on the ‘superior side’ * of the cell. The ciliary bundles of other short cells (common or hemispherical) are on the ‘inferior’ side or more centrally placed. The lenticular cells are quite numerous on the proximal one-third of the papilla and seem to be the only type of sensory cell present on the first millimeter of basilar membrane. The number and types of hair cells visible in
* ‘Superior side’: toward tectorial membrane.
the
wide
attachment
site of the
the basilar papilla (BP) on the plates (IP). Arrows indicate TM: tectorial membrane; TV:
cross sections were counted from the left ear of owl 769 and plotted in Fig. 3. The papilla of 769 was serial-sectioned in its entirety. Dissection artifacts prevented the use of complete papillae from owls 767 and 768 and a composite was made from 767 right and left and 768 right. Hair cell populations were the same in all three birds. There are 3 to 4 hair cells across the papilla at the proximal tip. The number rapidly reaches ten within the first millimeter with minimal changes for the next three millimeters. After about the four millimeter point, numbers increase more rapidly to a maximum of about 35 in 769, and 43 in the longer cochleas. Electron micrographs of hair cells of the proximal end from 768 R gave evidence that these cells were similar to the lenticular cells described earlier in the chicken [22]. Figs. 2a and 4 show typical lenticular cells. The cuticular plate with the cilia is toward the superior side of the papilla. A large part (half to two-thirds) of the apical cell membrane exposed to the endolymph is without cuticular plate. The ellipsoidal nucleus occupies a large part of the cytoplasm below. A moderate sized nerve ending filled with small round vesicles and opposite a sub-synaptic cisterna within the hair
240
Fig. 2. Cross-sections of the basilar papilla (owl No. 769) at three different positions along the basilar membrane showing the differences in hair cell distribution and structure of the basilar membrane. ,A11at same magnification: 280 x . (a) 2.25 mm, from proximal end, with typical short (S) and lenticolar (L) hair cells. The basilar membrane was ruptured at left and the tectorial membrane (TM) pulled away from the papilla during dissection. DFM, dense fibrous mass; LFM, loose fibrous mass. Arrows indicate part of basilar membrane shown in Fig. 5. (b) 5.6 mm from proximal end, with a few tall (T) and many typical short (S) hair cells. The DFM and LFM are quite prominent. B, border cells. (c) 8.7 mm from proximal end, showing many tall (T’) and short (S) hair cells. Note that the DFM no longer exists at this point and that LFM is much thinner.
241
:
40
40
;3O
30
= 20
20 IO
.z IO P 0
I
2
3 Length
4 of Basilar
5
6 Membrane
7
0
9
10
(mm)
Fig. 3. Graph showing the distribution of the three types of hair cells (owl No. 769) along typical short as well as the lenticular short hair cells.
cell is visible at right. Other lenticular cells also had small neural boutons which were apparently efferent nerve endings. Except for the location and type of nerve endings, these cells look much like flattened tall hair cells with one side at the surface of the papilla instead of being buried among the supporting cells. (2) Basilar membrane The basilar membrane is a fibrous, extracellular structure (Figs. 1 and 2) similar to basilar membranes of all vertebrates. In birds it is attached to the two fibro-cartilaginous plates. For descriptive purposes, it will be separated into a
the basilar
membrane.
‘Short’
includes
vestibular part which is composed of a packed fibrous matrix and a tympanic portion, composed of loosely arranged fibers, which appears as an appendage projecting into Scala tympani. Actually, the two parts are continuous and the terms used here only reflect different organizations of the fibers. (a) The vestibular part. The vestibular surface of the basilar membrane is completely covered by a large number of supporting cells plus a few border cells at the inferior edge (Fig. 2). Inside the supporting cell basal plasma membrane is a series of structures resembling hemidesmosomes (Fig. 5). A well-defined basal lamina separates the cells
Fig. 4. Electron micrograph of lenticular hair cell from the proximal end of owl No. 768. The cuticular plate (C) occupies the left half of cell surface. The right half of the apical cell membrane has no cuticular plate. E, efferent nerve ending; EN, endolymph; N. nucleus; SC, supporting cell; ST, stereocilia. Mag. 9400 X
Fig. 5. Electron micrograph of part of basilar membrane (location between arrows in Fig. 2a) showing the edge of the DFM as it merges with the remainder of the basilar membrane. The fine webby material of the LFM is visible below. BL, basal lamina; SC. supporting cells. Mag. 6000 x
from the basilar membrane fibers (Figs. 5 and 6). Toward the distal end of the papilla, the entire basilar membrane is relatively thin (Fig. 2~). The basilar membrane in the proximal half is considerably different in appearance due to the presence of a thick fibrous mass, spindle-shaped in cross-section. The basilar membrane and papilla do not co-exist at the proximal tip because the basilar papilla including the hair cells extends slightly further toward the vestibule than does the basilar membrane. In 767 R the structure of the basilar membrane was clearly defined at about 0.2 mm from the papillar tip. It was 91 nm in width and contained within it (toward the inferior edge) a spindle-shaped mass of closely packed fibers, the dense fibrous mass (DFM). The DFM was 37 pm wide, 8.5 pm in thickness and occupied an area 40% of the basilar membrane’s width. The basilar papilla above it had seven hair cells in cross-section, all lenticular in type. The DFM rapidly acquires a thickness of approximately 10 nrn and this increases only slightly in the next 5-6 mm (Figs. 2 and 7). Fig. 2a shows a section taken at 2.25 mm from the proximal end (769 R) where the DFM
Fig. 6. Higher magnification basal lamina; SC, supporting
of the fibers in the DFM. cell. Mag. 43000 X
BL.
243
was 57 pm in width and 11 pm in thickness. The width does increase and continues to do so until at 6-7 mm it reaches a maximum of 105-110 pm (Fig. 7). The DFM in Fig. 2b occupies 62% of the width of the basilar membrane. After 7 mm it gradually diminishes in thickness and within another millimeter it is hardly noticeable and has lost its distinctive character (Figs. 2c and 7). The vestibular part of the basilar membrane then continues to its distal terminus as a fairly (but not entirely) homogenous layer of compacted fibers. The superior one-third (Fig. 2c) is thinner, a difference which is accompanied by an array of adjacent supporting cell nuclei. Electron micrographs (Figs. 5 and 6) demonstrated that the DFM was composed of closely packed fibers with their longitudinal dimension for the most part positioned in a radial direction. Either the fibers are branched or there are also shorter fibers running at a direction other than that of the radial preponderance. At the tympanic edge of the density (Fig. 5), cords of longer radial fibers are visible which seem to have short perpendicular arms.
DENSE
LENGTH
I1
0
FIBROUS
OF
-
I
LENGTH
BASILAR
0.0
MASS
(769)
MEMBRANE
1
I
I
(mm)
a4
2345676910 OF
BASILAR
MEMBRANE
(mm)
Fig. 7. Graphs showing, above, the width changes of the DFM along the basilar membrane and, below, the changes in thickness. ‘Thickness’ was measured at the point of greatest thickness in cross-section.
(b) The tympanic part. The loose fibrous mass (LFM) projects into the perilymph of Scala tympani (Figs. 1 and 2). It underlies that part of the basilar membrane which is covered by the sensory cells but it does not extend to the border cell area (Fig. 2a, b, c). There is often a cluster of cells beneath the basilar membrane covered by the border cells but the basilar membrane itself is thin in this region (Fig. 2b). Electron micrographs (Fig. 5) show that the webby material which is the largest component of the dispersed LFM is continuous with the same type of material in the vestibular part of the basilar membrane. This fine webby background material may actually be compacted with the parallel fibers in the DFM. Only thin, discontinuous cords of fibers separate vestibular and tympanic parts. Cords of packed fibers are visible at the pendulous tympanic edge of the LFM in the proximal part of the papilla (Fig. 2a) but are more scattered throughout the mass more distally (Fig. 2b, c). A few spindle-shaped cells can be found within the LFM. Other cells (similar to the mesothelial layer in mammals) cover the tympanic surface and continue over the cartilaginous plates. The loose fibrous mass arises at the proximal tip along with the dense fibrous mass but the LFM covers a considerably greater width of basilar membrane than does the DFM (Fig. 2a, b). In 769 L, its greatest thickness of approximately 25 pm was achieved at about 1 mm from the proximal end. This thickness was fairly consistent up to 7 mm (except at the 2.7 mm position where it dipped to 16 pm). The thickness decreased rapidly over the next 2 mm and the LFM was absent from the distal tip. (c) Dimensions. The width of the basilar membrane was measured between its two attachment points at the superior and inferior cartilaginous plate crests (Fig. 1). The basilar membrane was almost 0.1 mm wide at its proximal end and reached a maximum of approximately 0.35 mm at the distal end in 769 R (Fig. 8). The proximal tip of the membrane (the first 50-75 pm) is narrower than 0.1 mm, but the membrane is very thick and poorly formed at this point and probably nonfunctional, At the point where it appears to have achieved its normal structure (at 0.15 mm) it was already 88 pm wide in 769 R. The basilar mem-
2
0.5-
s y 0.4-
!t 5
0
769 768 +--f 767 O---O
PROXIMAL L t ‘1 I 2 3 4
‘ 5
1 6
L 7
a 8
@ L 9 IO
DISTAL I ., It 12 13
LENGTH OF BASILAR MEMBRANE (mm) Fig. 8. Graph showing width changes of basilar membrane from proximal to distal end. The curves for owls Nos. 767 and 768 are incomplete (immeasurable in part due to dissection artifacts) but at the points where they overlap (8.5-9.5 mm) correspondence is very good. Both 767 and 768 had longer cochleas.
brane of 768 R, which was approximately 11.75 mm in length, achieved a width of 0.470 mm before rounding off sharply. The shape of the <
0.5
E
BARN OWL
( 769)
curves from all of the birds (767, 768 and 769) were very similar when width was plotted against length (Fig. 8). The slope was gradual and gentle
o-----o o---e
3
0.4
5 g
0.3
% g
0.2
a g
0.1 DISTAL
PERCENTAGE OF LfiNGTH OF 6A6lLAR
MEM6RANE
Fig. 9. Changes in the width of the basilar membrane of owl No. 769 plotted against percent of basilar membrane length and compared with curve from the guinea pig, taken from Fernandez 161.
245
from one to seven millimeters and then took a sharp upward turn. At that point, the curves of the longer ears (767 and 768) were shifted slightly to the right. There is an overall increase in width of 3.5-4.5 fold from proximal to distal ends, but this increase is quite irregular. Fig. 8 illustrates that the change in width is negligible for the first 2 mm. There is then a gradual 50% increase up to about 5-6 mm and a region of one-half to 1 mm where the width is more static. After that width changes are more rapid. When the data are presented with width relative to percentage of length of the basilar membrane (Fig. 9), it becomes more apparent that the width curve rises steeply over the distalmost 25% of the papilla. There is also a correspondingly larger number of hair cells in this region. Discussion
Evidence has accumulated that the auditory receptor organs of most birds have certain common structural features. The basilar papilla is formed by an organized cluster of sensory cells and supporting cells which is covered by a thick tectorial membrane. The basilar membrane is narrow and elongated but not as long as in mammals of comparable size. Schwartzkopf and Winter in Schwartzkopf [14] examined the inner ears of a number of bird species and found the longest cochlear ducts in Tyto alba (Barn Owl), Strix &co (Tawny Owl) and Bubo bubo (Eagle Owl). The present studies have confirmed this feature for Tyto alba and have further revealed that this bird has other structural features that are unique: a distinctive arrangement of sensory cell types and a localized thickening of the basilar membrane. The basilar membrane has two thickenings, the vestibular dense fibrous mass (DFM) and the tympanic loose fibrous mass (LFM). The latter is present in other birds. It can be readily detected in published micrographs of the pigeon [20] and the chicken [22], although this particular feature was not discussed in those publications. Reexamination of the basilar membranes from the parakeet (Melopsittucas unduhtus) and the House Sparrow (Passer domesticus) revealed that tympanic masses were also present in these species [18]. According
to data available at present, then, the dispersed tympanic mass seems to be a common feature in birds. The dense vestibular fibrous mass, however, has not been found in pigeon, chicken, parakeet or sparrow, and in birds, it may be unique to the Barn Owl. Basilar membrane specializations have been reported in a few mammals. Pye found thickenings in the kangaroo rat [II] and in some Chiroptera [12]. Henson [7] has reported basilar membrane thickenings in the Moustache Bat (Pteronotus p. parnellii). In most cases, the thickenings seem to be similar to the tympanic mass (LFM) in birds although it is difficult to make comparisons because of differences in preparation techniques. Thickenings in the mammalian basilar membrane which seem to be most similar to those of Tyto ulbu were described by Bruns [3] for the Horseshoe Bat (Rhinolophus ferrumequinum). He found a vestibular, as well as a tympanic, component. Both of those were thickest in the basalmost 4.7 mm. Only the vestibular thickening persisted toward the apex. More recently, Wilson and Bruns [23] have measured basilar membrane movements in the Horseshoe Bat’s ear by use of a capacitive vibration probe. They found there were phase shifts between measurements made on thickenings in the Pars Tecta and Pars Pectinata on the same segment of basilar membrane but that the shifts were variable and not always present. It is probable that the effect of the thickenings is to facilitate high frequency hearing in both classes although the high frequency sensitivity of bat and owl actually is quite different (respectively 80 and 7 kHz). In addition, the thickenings may be an important factor in the excellent high-frequency discrimination which has been demonstrated in the Barn Owl [13]. It may not be possible to compare the damping qualities of basilar membrane thickenings in bird and mammal because of other structural variables between the two classes. The cellular mass of the bird’s basilar papilla is quite different from that of the organ of Corti. Furthermore, hair cell stimulation may not be equivalent because avian sensory cell cilia have a stronger attachment to the tectorial membrane [21]. Possibly the thickenings are important in temporal qualities of sound reception. Indeed, behavioral as well as neurophysio-
246
logical studies point toward a remarkable temporal resolution in the Barn Owl’s audition [10,19]. Two distinct patterns of sensory ceil distribution were found on the proximal and distal halves of the Barn Owl’s cochlea. The proximal half was occupied by large numbers of short hair cells and an occasional intermediate cell. On the distal half there were many tall and short hair cells with a few intermediates in between. The large number of the lenticular type of short hair cells on the proximal portion was remarkable. Lenticufar cells are an unusual type of inner ear sensory cell. They were first described by Baird in the Caiman ear [l]. Tanaka and Smith [22] found a few on the basal tip of the chicken’s papilla but they do not seem to be present in parakeet, pigeon or sparrow. Their abundance on the proximal-most two millimeters of the Barn Owl’s papilla and presence in a very limited degree in the same location in the chicken might indicate that they play some role in high frequency reception. Variables in the distribution of sensory cell types seem to be a common feature in the papillae of birds. These variations have been previously observed in the cochleas of the pigeon, chicken, House Sparrow and parakeet [U-18]. The Barn Owl can now be added to the list and its sensory cell pattern is dissimilar from all the others thus far examined. Neurophysiological studies [8] in a number of species showed that different species had similar low-frequency sensitivity but different high-frequency cut-off points. Perhaps one way in which birds achieve this selective sensitivity is by special arrangements of cell types. Basilar membrane dimensions (as well as thickenings, etc.) are likewise important. The basilar membranes of the cochleas of mammals vary in length from 7 mm in the mouse to 50 mm in the elephant [Z] but, with the exception of some bats, the width invariably shows a fairly regular increase from basal (high frequency) to apical end (low frequency). Such an increase is also present in the chicken [18]. Although basilar membrane measurements were not made on the pigeon 1201a systematic increase in the cell numbers might indicate a comparable increase in basilar membrane width. On the other hand, the basilar membranes of some small birds have quite variable dimensions [16,17]. The 2.3 mm long
membrane of the parakeet shows little change in width in the distal 1.5 mm. The width of the long basilar membrane of Qro albu changes only negligibly in its proxima1 quarter, has a 50% increase for several millimeters up to midpoint, and then a more rapid increase to the distal tip where it is somewhat more than three times that of the proximal end. Width changes in the first 5-7 mm of the Barn Owl’s basilar membrane are not too different from those of the guinea pig as measured by Fernandez f63, although the bird’s slope is more gentle. At the 7 mm (9 mm in the longer cochleas) point the slope takes a sudden upturn. If the Barn Owl and guinea pig width changes are plotted relative to percentage of basilar membrane length (Fig. 9), a sharp upcurve at approximately 75% of the basilar membrane length is seen to be present in Barn Owl but not the guinea pig. However, a very similar type of sharp terminal curve was described by Cabezudo [4] for the cat. Whatever the significance of the irregularities in basilar membrane width may be, there seems little doubt that the unusual length of the Barn Owl’s basilar membrane is related to its wide frequency sensitivity band. It seems probable that the basilar membrane thickening and peculiar hair cell arrangement likewise play a significant role in its special hearing properties. Aeknawkdgements
The authors thank Donna Himes and Jill Lilly for their expert assistance with the graphs and typing. This work was supported in part by NIH grants Nos. 08813 and 14617. References Baird, I.L. (1974): Anatomical features of the inner ear in submammalian vertebrates. In: Handbook of Sensory Physiology, pp. 197-198. Editors: H. Autrum, R. Jung, W. Lowenstein, D. McCay and H. Teuber. Springer-Verlag, New York. MkCsy, G. von (1960): Experiments in Hearing, pp. 504-510. McGraw-Hill, New York. Bruns, V. (1976): Peripherat auditory tuning for fine frequency analysis by the CF-FM bat, Rhidophus firrumequinum. .l. Comp. Physiology 106, 77-86. Cabezudo, L.M. (1978): The ultrastructure of the basilar membrane in the cat. Acta Otolaryngof. 86, 160-175.
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5 Dooling. R.J. (1980): Behavior and psychophysics of hearing in birds. In: Comparative Studies of Hearing in Vertebrates, pp. 261-288. Editors: A.N. Popper and R.R. Fay. Springer-Verlag, New, York. 6 Fernandez. C. (1952): Dimensions of the cochlea (guinea pig). J. Acoust. Sot. Am. 24. 519-523. 7 Henson. M. (1978): The bastlar membrane of the bat, !‘teronoru.s p. purnellii. Am. J. Anat. 153, 143-158. 8 Konishi. M. (1970): Comparative neurophysiological studtes of hearing and vocalizations in songbirds. Z. Vergl. Phystol. 66. 257-212. 9 Komshi. M. (1973): How the owl tracks its prey. Am. Sci. 61. 414-424. 10 Moiseff. A. and Konishi. M. (1981): Neuronal and behavioral sensitivity to binaural time differences in the owl. J. Neurosci. 1. 40-48. 11 Pye. A. (1965): The auditory apparatus of the HereromCfue (Rodentia. Scruromorpho). J. Anat. 99, 161-174. 12 Pye. A. (1966): The structure of the cochlea in Chiroptera, I Mmwhmppreru: Emhullonurordeu and Rhonolophoiderr. J. Morphol. 118, 495-510. 13 Quine. D.B. and Konishi, M. (1974): Absolute frequency discrmination in the Barn Owl. J. Comp. Physiol. 93. 3477360. 14 Schwartzkopf. J. (1968): Structure and function of the ear and of the auditory brain areas in birds. In: Hearing Mechanisms in Vertebrates, pp. 41-58. Editors: A.V.S. de Reuck and J. Knight. Little, Brown and Co., Boston.
15 Schwartzkopf, J. and Winter, P. (1960): Zur Anatomie der Vogel-Cochlea unter natiirlichen Bedingungen. Biol. Zbl. 79. 607-625. 16 Smtth, C.A. (1981): Recent advances in structural correlates of auditory receptors. In: Progress in Sensory Physiology 2. pp. 135187. Editor: D. Ottoson. Springer-Verlag. New York. 17 Smith. C.A. and Tanaka. K. (1981): Further observations on the avian basilar papilla. In: Abstr. ARQ 4th Meeting. pp. 79980. Association for Research in Otolaryngology. 18 Smith, C.A. and Tanaka. K. Unpublished data. 19 Sullivan, W.E. and Konishi. M. (1984): Segregation of sttmulus phase and intensity coding in the cochlear nucleus of the Barn Owl. J. Neurosct. 4. 178771799. 20 Takasaka. T. and Smith, C.A. (1971): The structure and innervation of the pigeon’s basilar papilla. J. Ultrastruct. Res. 35. 20-65. 21 Tanaka, K. and Smith, C.A. (1975): Structure of the avian tectorial membrane. Ann. Otol. Rhinol. Laryngol. 84, 287-291. 22 Tanaka. K. and Smith, C.A. (1978): Structure of the chicken’s inner ear. Am. J. Anat. 153. 251-271. 23 Wilson, J.P. and Bruns. V. (1983): Basilar membrane tuning properties in the specialized cochlea of the CF-bat. Rhrnolophus Jerrumequinum. Hearing Rea. 10. 15-36.