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Inner ear structure in the deaf and normally hearing Dalmatian dog
J.
COMP.
PATH.
INNER
1985. VOL.
EAR
95
STRUCTURE HEARING
IN THE DEAF AND DALMATIAN DOG
NORMALLY
BY
M. BRANIS
and H. BURDA
Institute of Experimental Medicine, Czechoslovak Academy of Sciences, Lidovjch milici 61, 120 00 Praha 2, C,pchoslouakia
INTRODUCTION
Hereditary deafness in Dalmatian dogs is a problem familiar not only to dogfanciers but also to specialists in otology. A number of workers who have studied this condition e.g. Hudson and Ruben (1962), Igarashi, Alford, Saito, Muraski, and Preston Cohn, and Watanabe (1972), J o h nson, Hawkins, (1973), Lurie (1948), and Mair ( 1976) have suggested that advanced degenerative changes are already present in pups one to 2 months old. The distinctive features of this degeneration include descent of Reissner’s membrane, collapse of the Scala media, atrophy of the stria vascularis, dedifferentiation of the organ of Corti and atrophy of the tectorial membrane. We had the opportunity to study the auditory organ in 2 male littermates, 6-weeks-old, one of which was normally coloured but deaf and the other one had normal hearing but was hypopigmented (yellow dotted) and so could not be used for breeding. This reverse combination between pigmentation and the state of the inner ear has not previously been described in the literature and so is worth mention. According to the literature (e.g. Deol, 1980; Mair, 1976) the hereditary inner ear dysplasia in Dalmatian dogs as well as in several other mammalian species is connected with anomalies of pigmentation (hypopigmentation). The case described here seems to be an exception to the rule since the “wrongly coloured” Dalmatian pup had normal hearing with a normal cochlear duct while the normal coloured pup was deaf, with typical inner ear pathomorphological findings. Since no comparison with quantitative data obtained for ears of normally hearing Dalmatian dogs has been available so far as we know, a brief description of our findings in this respect may be of interest. During this investigation on the structure of degenerate ears, several new observations have been made which complement the hitherto published conclusions on the course of the degenerative process. MATERIALS
AND
METHODS
The pups were deeply narcotized and then intravitally perfused via the carotid artery with 10 per cent neutral formaldehyde. The pups were decapitated and their 002 l-9975/85/020295 + 05 $03.00/O
0 1985 Academic Press Inc. (London) Limited
296
M. BRANIS
and
H.
BURDA
auditory bullae were opened and immersed in the fixative. The right ears of both animals were processed to total surface specimens of the cochlear partition and stained with toluidine blue and Ehrlich’s haematoxylin. The left cochleae were decalcified and then processed to paraffin sections 15 to 20 pm thick which were stained by Ehrlich’s haematoxylin or MacCallum’s modification of Verhoeff s haematoxylin method with picrofuchsin. Specimens were examined under a light microscope. RESULTS
AND
DISCUSSION
The cochlea of the Dalmatian dog has about 3 turns. The basilar membrane (along the tunnel of Corti) was 28.5 and 27.5 mm long in the normal hearing
and in the deaf pup, respectively. The width of the basilar membrane was about 0.24 mm at the base, 0.285 mm in the middle turn and 0.39 mm at the apex in the normal cochlea. The estimated total number of outer hair cells was 10 548 and of inner hair cells 2603 in the right cochlea of the healthy dog. The pattern of hair cell density changes along the organ of Corti is plotted in Fig. 1. Neither the examination of surface specimens nor that of paraffin sections revealed any morphological anomaly in the cochleas of the healthy pup and all the structures examined were normal.
375
345
330
Fig. I. Inner hair cell (IHC) and outer hair cell (OHC) density per mm of the length of the organ of Corti particular segments along the cochlear duct of the normal hearing Dalmatian dog.
In
the
degeneration
other
(i.e.
deaf)
of the tectorial
pup,
there
membrane,
several further changes corresponding 1976). According to his own findings and
was
collapse
atrophy to those
the findings
of
the
Scala
of the vascular previously of previous
in
media,
stria, and
described authors,
(Mair, Mair
(1976) described 2 types of abnormalities of the tectorial membrane occurring simultaneously in affected ears of deaf Dalmatians. Either the tectorial membrane was shrunken and lying in the internal sulcus as in human Scheibe dysplasia (Schuknecht, 1980) or (even within the same cochlea) it
EAR
STRUCTURE
IN A DEAF
DALMATIAN
297
projected as a flat shelf into the Scala media, or both anomalies were present. The former situation was not recorded in the ear under our study, while the latter was more prominent than described and documented by Mair (1976). It could even be denoted as a third type of situation since a more detailed examination of our material revealed, in the atrophied region of the cochlear duct, an apparent contact-even coalescence-of all the 3 membranes which form the space of the Scala media-i.e. basilar, tectorial and Reissner’s membranes (Fig. 2). As can be seen in the specimens, the middle layer of that “sandwich-like” structure is formed by the tectorial membrane which projects up to the spiral ligament. At many points, the tectorial membrane was found to be fused with the spiral ligament, pulling it towards the modiolus. Resting spaces of the Scala media were entirely filled with ligamentous fibres and atrophied Claudius(?) cells. Such a state was recorded within the course of all the cochlear turns, but was most evident in the apical regions, which showed evidence of an advanced stage of degeneration. A similar feature-fusion of membranes-was described by Deol (1980) as a genetic malformation in hypopigmented mice. As far as the organ of Corti is concerned, we cannot confirm that it was already totally dedifferentiated at the time of collapse of the Scala media and atrophy of the stria vascularis. In surface specimens of the cochlear partition, we observed inner hair cells in a continuous row (Fig. 3) along the course of almost one entire cochlear coil (the middle one). These hair cells have wellpreserved cuticular plates and-at least in the basal portion of the middle coil-distinct hairs. Very often, even the nuclei of inner hair cells were apparent. Sporadically, even impressions of the hair formations of the outer hair cells may be seen on the degenerated tectorial membrane in the second cochlear turn. The density of the remainder of the inner hair cell population corresponded to densities in the ear of the hearing dog. This finding is at variance with the suggestion (Anderson, Henricson, Lundquist, Wedenberg and Wersall, 1968; Igarashi et al., 1972) that the degenerative process in the deaf Dalmatian starts in a certain central part of the cochlear duct and proceeds toward the base and apex. It was, in fact, in the central portion of the cochlea i.e. in the second coil, that part of the neuro-epithelium was preserved for longest. SUMMARY
Both cochleae of two 6-week-old Dalmatian dogs of the same litter were examined by means of surface specimens and histological section techniques. Basic quantitative data on the morphometry of the cochlear duct in the hearing (though hypopigmented) pup are presented. The cochlear ducts of the deaf (though normally coloured) pup exhibited in general the same alterations (collapse of the Scala media) as described in the literature. In addition, we describe also the coalescence of membranous structures, projection of the tectorial membrane up to the spiral ligament and preservation of inner hair cells in the second (i.e. middle) cochlear coil. These new findings complement the previous data and indicate an alternative possible course of hereditary inner ear degeneration in the Dalmatian dog.
298
M.BRANI~
and
H.BURDA
Fig. 2. Cochlrar partition of the second turn with fused membranes in the deaf Dalmatian do!g. BM: basilar membrane with remains of the organ of Corti, RM: Rrissner’s membrane, TM: tectonal membrane. HE x 500. Fig. 3. Surface specimen HE x 420.
of the cochlear
partition
of the deaf
Dalmatian
dog.
IHC:
inner
hair
crlls.
ACKNOWLEDGMENT
The authors material.
would
like to thank Ing. J an Findejs for supplying
us with the valuable
EAR
STRUCTURE
IN A DEAF
DALMATIAN
299
REFERENCES
Anderson, H., Henricson, B., Lundquist, R. G., Wedenberg, E., and Wersall, J. (1968). Genetic hearing impairment in the Dalmatian dog. Acta Ololnryngolo~+ca (Stockh.) [Suppl.], 232, l-32. Deol, M. S. (1980). Genetic malformations of the inner ear in the mouse and in man. Birth Defects, Original Article Series, 16 (4)) 243-26 1. Hudson, W. R., and Ruben, R. J. (1962). Hereditary deafness in the Dalmatian dog. Archiues of Oto-Rhino-Laryngology,
75, 2 13-2 19.
Igarashi, M., Alford, B. R., Saito, R., Cohn, A. M., and Watanabe, T. (1972). Inner ear abnormalities in dogs. Annals of Otology (St Louis), 81, 2499255. Johnson, L. G., Hawkins, J. E. Jr, Muraski, A. A., and Preston, R. E. (1973). Vascular anatomy and pathology of the cochlea in Dalmatian dogs. In Vascular disorders and hearing defects, de Lorenzo, A. D. J., Ed., Baltimore, University Park Press, pp. 249-293. Lurie, M. H. (1948). The membranous labyrinth in the congenitally deaf Collie and Dalmatian dog. Laryngoscope (St Louis), 58. 279-287. Mair, I. W. S. (1976). Hereditary deafness in the Dalmatian dog. Archives of Oto-RhinoLaryngology, 212, 1-14. Schuknecht, H. F. (1980). Dysmorphogenesis of the inner ear. Birth Defects, Orz’ginal Article Series, 16 (4), 47-71. [Received for publication,
February
2nd, 19841
COMP.
PATH.
INNER
1985. VOL.
EAR
95
STRUCTURE HEARING
IN THE DEAF AND DALMATIAN DOG
NORMALLY
BY
M. BRANIS
and H. BURDA
Institute of Experimental Medicine, Czechoslovak Academy of Sciences, Lidovjch milici 61, 120 00 Praha 2, C,pchoslouakia
INTRODUCTION
Hereditary deafness in Dalmatian dogs is a problem familiar not only to dogfanciers but also to specialists in otology. A number of workers who have studied this condition e.g. Hudson and Ruben (1962), Igarashi, Alford, Saito, Muraski, and Preston Cohn, and Watanabe (1972), J o h nson, Hawkins, (1973), Lurie (1948), and Mair ( 1976) have suggested that advanced degenerative changes are already present in pups one to 2 months old. The distinctive features of this degeneration include descent of Reissner’s membrane, collapse of the Scala media, atrophy of the stria vascularis, dedifferentiation of the organ of Corti and atrophy of the tectorial membrane. We had the opportunity to study the auditory organ in 2 male littermates, 6-weeks-old, one of which was normally coloured but deaf and the other one had normal hearing but was hypopigmented (yellow dotted) and so could not be used for breeding. This reverse combination between pigmentation and the state of the inner ear has not previously been described in the literature and so is worth mention. According to the literature (e.g. Deol, 1980; Mair, 1976) the hereditary inner ear dysplasia in Dalmatian dogs as well as in several other mammalian species is connected with anomalies of pigmentation (hypopigmentation). The case described here seems to be an exception to the rule since the “wrongly coloured” Dalmatian pup had normal hearing with a normal cochlear duct while the normal coloured pup was deaf, with typical inner ear pathomorphological findings. Since no comparison with quantitative data obtained for ears of normally hearing Dalmatian dogs has been available so far as we know, a brief description of our findings in this respect may be of interest. During this investigation on the structure of degenerate ears, several new observations have been made which complement the hitherto published conclusions on the course of the degenerative process. MATERIALS
AND
METHODS
The pups were deeply narcotized and then intravitally perfused via the carotid artery with 10 per cent neutral formaldehyde. The pups were decapitated and their 002 l-9975/85/020295 + 05 $03.00/O
0 1985 Academic Press Inc. (London) Limited
296
M. BRANIS
and
H.
BURDA
auditory bullae were opened and immersed in the fixative. The right ears of both animals were processed to total surface specimens of the cochlear partition and stained with toluidine blue and Ehrlich’s haematoxylin. The left cochleae were decalcified and then processed to paraffin sections 15 to 20 pm thick which were stained by Ehrlich’s haematoxylin or MacCallum’s modification of Verhoeff s haematoxylin method with picrofuchsin. Specimens were examined under a light microscope. RESULTS
AND
DISCUSSION
The cochlea of the Dalmatian dog has about 3 turns. The basilar membrane (along the tunnel of Corti) was 28.5 and 27.5 mm long in the normal hearing
and in the deaf pup, respectively. The width of the basilar membrane was about 0.24 mm at the base, 0.285 mm in the middle turn and 0.39 mm at the apex in the normal cochlea. The estimated total number of outer hair cells was 10 548 and of inner hair cells 2603 in the right cochlea of the healthy dog. The pattern of hair cell density changes along the organ of Corti is plotted in Fig. 1. Neither the examination of surface specimens nor that of paraffin sections revealed any morphological anomaly in the cochleas of the healthy pup and all the structures examined were normal.
375
345
330
Fig. I. Inner hair cell (IHC) and outer hair cell (OHC) density per mm of the length of the organ of Corti particular segments along the cochlear duct of the normal hearing Dalmatian dog.
In
the
degeneration
other
(i.e.
deaf)
of the tectorial
pup,
there
membrane,
several further changes corresponding 1976). According to his own findings and
was
collapse
atrophy to those
the findings
of
the
Scala
of the vascular previously of previous
in
media,
stria, and
described authors,
(Mair, Mair
(1976) described 2 types of abnormalities of the tectorial membrane occurring simultaneously in affected ears of deaf Dalmatians. Either the tectorial membrane was shrunken and lying in the internal sulcus as in human Scheibe dysplasia (Schuknecht, 1980) or (even within the same cochlea) it
EAR
STRUCTURE
IN A DEAF
DALMATIAN
297
projected as a flat shelf into the Scala media, or both anomalies were present. The former situation was not recorded in the ear under our study, while the latter was more prominent than described and documented by Mair (1976). It could even be denoted as a third type of situation since a more detailed examination of our material revealed, in the atrophied region of the cochlear duct, an apparent contact-even coalescence-of all the 3 membranes which form the space of the Scala media-i.e. basilar, tectorial and Reissner’s membranes (Fig. 2). As can be seen in the specimens, the middle layer of that “sandwich-like” structure is formed by the tectorial membrane which projects up to the spiral ligament. At many points, the tectorial membrane was found to be fused with the spiral ligament, pulling it towards the modiolus. Resting spaces of the Scala media were entirely filled with ligamentous fibres and atrophied Claudius(?) cells. Such a state was recorded within the course of all the cochlear turns, but was most evident in the apical regions, which showed evidence of an advanced stage of degeneration. A similar feature-fusion of membranes-was described by Deol (1980) as a genetic malformation in hypopigmented mice. As far as the organ of Corti is concerned, we cannot confirm that it was already totally dedifferentiated at the time of collapse of the Scala media and atrophy of the stria vascularis. In surface specimens of the cochlear partition, we observed inner hair cells in a continuous row (Fig. 3) along the course of almost one entire cochlear coil (the middle one). These hair cells have wellpreserved cuticular plates and-at least in the basal portion of the middle coil-distinct hairs. Very often, even the nuclei of inner hair cells were apparent. Sporadically, even impressions of the hair formations of the outer hair cells may be seen on the degenerated tectorial membrane in the second cochlear turn. The density of the remainder of the inner hair cell population corresponded to densities in the ear of the hearing dog. This finding is at variance with the suggestion (Anderson, Henricson, Lundquist, Wedenberg and Wersall, 1968; Igarashi et al., 1972) that the degenerative process in the deaf Dalmatian starts in a certain central part of the cochlear duct and proceeds toward the base and apex. It was, in fact, in the central portion of the cochlea i.e. in the second coil, that part of the neuro-epithelium was preserved for longest. SUMMARY
Both cochleae of two 6-week-old Dalmatian dogs of the same litter were examined by means of surface specimens and histological section techniques. Basic quantitative data on the morphometry of the cochlear duct in the hearing (though hypopigmented) pup are presented. The cochlear ducts of the deaf (though normally coloured) pup exhibited in general the same alterations (collapse of the Scala media) as described in the literature. In addition, we describe also the coalescence of membranous structures, projection of the tectorial membrane up to the spiral ligament and preservation of inner hair cells in the second (i.e. middle) cochlear coil. These new findings complement the previous data and indicate an alternative possible course of hereditary inner ear degeneration in the Dalmatian dog.
298
M.BRANI~
and
H.BURDA
Fig. 2. Cochlrar partition of the second turn with fused membranes in the deaf Dalmatian do!g. BM: basilar membrane with remains of the organ of Corti, RM: Rrissner’s membrane, TM: tectonal membrane. HE x 500. Fig. 3. Surface specimen HE x 420.
of the cochlear
partition
of the deaf
Dalmatian
dog.
IHC:
inner
hair
crlls.
ACKNOWLEDGMENT
The authors material.
would
like to thank Ing. J an Findejs for supplying
us with the valuable
EAR
STRUCTURE
IN A DEAF
DALMATIAN
299
REFERENCES
Anderson, H., Henricson, B., Lundquist, R. G., Wedenberg, E., and Wersall, J. (1968). Genetic hearing impairment in the Dalmatian dog. Acta Ololnryngolo~+ca (Stockh.) [Suppl.], 232, l-32. Deol, M. S. (1980). Genetic malformations of the inner ear in the mouse and in man. Birth Defects, Original Article Series, 16 (4)) 243-26 1. Hudson, W. R., and Ruben, R. J. (1962). Hereditary deafness in the Dalmatian dog. Archiues of Oto-Rhino-Laryngology,
75, 2 13-2 19.
Igarashi, M., Alford, B. R., Saito, R., Cohn, A. M., and Watanabe, T. (1972). Inner ear abnormalities in dogs. Annals of Otology (St Louis), 81, 2499255. Johnson, L. G., Hawkins, J. E. Jr, Muraski, A. A., and Preston, R. E. (1973). Vascular anatomy and pathology of the cochlea in Dalmatian dogs. In Vascular disorders and hearing defects, de Lorenzo, A. D. J., Ed., Baltimore, University Park Press, pp. 249-293. Lurie, M. H. (1948). The membranous labyrinth in the congenitally deaf Collie and Dalmatian dog. Laryngoscope (St Louis), 58. 279-287. Mair, I. W. S. (1976). Hereditary deafness in the Dalmatian dog. Archives of Oto-RhinoLaryngology, 212, 1-14. Schuknecht, H. F. (1980). Dysmorphogenesis of the inner ear. Birth Defects, Orz’ginal Article Series, 16 (4), 47-71. [Received for publication,
February
2nd, 19841