Ann Otol 88 :1979
OBSERVATIONS OF HUMAN FETAL OTOCONIAL MEMBRANES CHARLES G. WRIGHT, PhD DALLAS, TEXAS
DAVID G. HUBBARD, MD
GEOFFREY M. CLARK, PhD
DALLAS, TEXAS
SEATTLE, VVASHlNGTON
Intact otoconial membranes from 31 human fetuses ranging in gestational age from 14 to 36 weeks were studied. At all stages of development specimens from different individuals showed marked variations in overall shape. During the course of the second and third trimesters, both saccular and utricular otoconial membranes were found to increase three to fourfold in surface area and more than twofold in weight. Near the end of gestation the fetal specimens were about equal in area and weight to otoconial membranes from children up to 13 years of age. However, the crystal layers of the fetal membranes had less prominently developed surface contours than usually observed in children and adults, indicating that maturational changes continue after the time of birth.
Decades ago, Schilder! and Bender" published clinical findings which implicated the vestibular system in neurological development and behavior. Their observations have been corroborated by the case studies of Ornitz" and Hubbard/ who emphasized the role played by gravity in human development. Although informative work has been carried out in experimental animals.":" we still have much to learn regarding the basic morphological development of the vestibular apparatus in man. More complete data regarding normal anatomical variation and time-course of maturation is essential to any consideration of human vestibular development in relation to that of the central nervous system as a whole. Studies of the gravity-receptor organs of the saccule and utricle have been hindered by technical limitations of conventional temporal bone histology. This is particularly true in regard to the otoconia which are radically altered by the action of decalcifying agents. The alternative method of microdissection,
as applied to human material by Johnsson and Hawkins," has proved more satisfactory for investigation of these structures. This approach allows rapid preparation of specimens so that surface views of intact otoconial membranes are obtainable without lengthy storage of tissues in preservatives or acidic solutions. Its usefulness in direct anatomical study of human otoconia is amply demonstrated by the recent work of Ross et al.9 The present study of macular suprastructures in human fetuses, using the method of microdissection, is part of a broader investigation of the peripheral vestibular apparatus and its central projections in individuals of all ages. This report presents examples of anatomical variation as well as data on growth in surface area and weight of otoconial membranes from fetuses ranging in gestational age from 14 weeks to approximately term. Weight measurements of fetal specimens are compared with those obtained from a group of infants and children using the same analytical methods.
From the Callier Center for Communication Disorders. University of Texas at Dallas, the Aberrant Behavior Center, Dallas and the Department of Psychology, University of Washington Seattle, Washington. This work was carried out under the auspices of the Lauretta Bender-Paui Schilder Memorial Project and was supported by a grant from the Leland Fikes Foundation to the University of Texas at Dallas subcontracted through the Aberrant Behavior Center, Dallas, Texas.
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METHODS AND MATERIALS Inner ears from a total of 39 individuals were included in this study. Thirty-one of these cases were fetuses, of which 16 were obtained from premature deliveries during the third trimester of pregnancy; the remaining 15 were products of prostaglandin abortions induced in the second trimester. Gestational ages were estimated with the help of data on crownrump, crown-heel, and body weight recently published by Brenner et al." In addition to the fetal specimens, representative cases from a collection of temporal bones taken at autopsy with the Stryker boneplug cutter were studied. This material included inner ears from eight individuals ranging from four days postpartum to 31 years in age. With minor modifications, all material was prepared according to the method described in detail by Hawkins and Johnsson." After removal of temporal bones from the fetal skull using surgical scissors, the middle ear cavity was opened under saline and cleared of mesenchymal tissue when necessary. The ossicular chain was then disarticulated and the stapes gently lifted from the oval window to allow perilymphatic perfusion with either 2% glutaraldehyde or 1% osmium tetroxide. Both fixatives were veronal buffered at pH 7.4. When glutaraldehyde was used as the primary fixative the inner ear structures were stained with 1% osmium tetroxide after overnight glutaraldehyde fixation at refrigerator temperature. After staining, specimens were partially dehydrated in ethanol and studied promptly to avoid any artifacts due to prolonged storage. For photography," the vestibule was widely opened by enlargement of the oval window. The wall of the saccule opposite the macula sacculi was carefully removed and the saccular otoconial membrane was photographed in situ. The anterior portion of the utricle containing the macula utriculi was then dissected from the vestibule and trimmed with iris scissors so as to permit visualization of the utricular otoconial membrane.
Fig. 1. Saccular (A) and utricular (B) otoconial membranes from a 31-year-old man showing typical adult form and surface contours. Arrows indicate "snowdrift" line. DL - Dorsal lobe.
For ease of comparison, all photomicrographs are shown at the same scale with the bar at lower right representing one-half millimeter in each case. With the exception of Figure 3, which shows right and left sides, all specimens are illustrated in the same orientation.
were weighed. The dissected membranes were placed on preweighed aluminum foil tabs (0.3 mg or less) and dried at 60 C for 48 to 72 hours. Individual membranes were then weighed on a microbalance.... with maximum sensitivity of 0.1 fig.
After photographs were obtained, an attempt was made to remove the whole otoconial membrane, including both the gelatinous and crystalline layers, from the surface of the sensory efithelium. When this procedure was suecessfu a dry-weight determination was then carried out. Great care was taken in these dissections; only those specimens known to represent at least 95% of the entire membrane mass
RESULTS
The general surface morphology of the saccular and utricular otoconial membranes is illustrated in Figure 1 by specimens from a young adult. The otoconial membranes cover the entire macular surface and have approximate-
"Model 78 stereomlcroscope. Wild-Heerbrugg Instruments, Inc., Farmingdale, NY. "'Model 440, Calm Division, Ventron Instruments Corp., Paramount, CA.
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Fig. 2. Variations in shape of saccular otoconial membranes from fetuses of 20 weeks (A), 22 weeks (B), 30 weeks (C), and 34 weeks (D) gestational age.
ly the same shape as the underlying sensory epithelia. Occasionally, accumulations of crystals extending beyond the borders of the maculae are present. This is true of the utricular specimen in Figure IB where a sizeable mass of extramacular otoconia can be seen surrounding the posterior end of the membrane.
present which contribute to the complex texture of the surface. The characteristic hook shape of the saccular otoconial membrane is due to an extension of its anterior portion which projects dorsally. We have found this dorsal lobe (or, dorsal extension) to be quite variable in size from one individual to another.
In man, a distinct, curved ridge is typically found on the surface of the crystalline layer of both the saccular and utricular otoconial membranes. This contour marks the position of a specialized region in the gelatinous layer of the membrane which overlies the striola of the neuroepithelium.P-" In accordance with the terminology first applied by Ades and Engstrom> and later used by Johnsson and Hawkins" in the description of human material, this surface feature of the otoconial layer will be referred to as the "snowdrift" line. Especially on the utricular membrane, many smaller ridges and grooves are
Striking differences in the form and size of the dorsal lobe are apparent in the four fetal specimens shown in Figure 2. These membranes are, in fact, quite varied in overall shape. At this stage in development (20-34 weeks), the otoconial layer appears almost as thick as that in the adult, but the "snowdrift" line is usually less prominent. Left and right saccular membranes from a 16-week fetus are seen in Figure 3. Compared to the specimens shown in Figure 2, these membranes are smaller in surface area and the crystal layers are noticeably thinner. Particularly near
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Fig. 3. Left (A) and right (B) saccular otoconial membranes from a fetus of 16 weeks gestational age. Note the thin crystal layers on both specimens and accumulations of otoconia in the region between the dorsal lobe and main body.
the margins, the crystals are sparsely distributed, giving the membranes a sieve-like appearance. Three fetuses of approximately 16-weeks gestational age were included in our material; the otoconial membranes showed very similar characteristics in each of these cases. The rather ahnond-shaped specimen shown in Figure 3A illustrates a form which has occasionally been seen in saccular membranes from infants and children as well as fetuses. In this case, a thin layer of crystals is present in the area between the dorsal lobe and the main body of the crystal layer. On the opposite side, this region is nearly devoid of crystals so that the dorsal lobe is more clearly outlined. As was generally observed, however, the overall shape of these membranes from the right and left sides is quite similar rela-
Fig. 4. Saccular otoconial membranes from fetuses of 14 weeks (A) and 32 weeks (B) gestational age. The more mature membrane is approximately four times larger in surface area.
tive to the large variations seen between different individuals. The youngest gestational age in the present series is represented by the 14week specimen shown in Figure 4, where it is compared to a saccular otoconial membrane from a 32-week fetus. Planimeter measurements showed an approximately fourfold difference in surface area between the two membranes. In spite of its small size, the 14-week specimen displays a clear "snowdrift" line and has a well-differentiated dorsal lobe. Photomicrographs of utricular otoconial membranes from four fetuses in the 17 to 30-week gestational age group are presented in Figure 5. Like the saccular membranes, the specimens from the utricle show marked variations in shape - from nearly round to distinctly
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Fig. 5. Variation in shape and surface morphology of utricular otoconia! membranes from fetuses of 17 weeks (A), 22 weeks (B), 26 weeks (C), and 30 weeks (D) gestational age.
elongated. In the 17 and 20-week specimens the otoconial layer has a thin, porous appearance much like that seen in the membranes from the saccule at approximately 16 weeks.
A utricular otoconial membrane of 14-weeks gestational age is shown together with one from a 36-week fetus in Figure 6. The more mature membrane is approximately 3.4 times larger
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WRIGHT ET AL UTRICLE
•
110 100 -;;; 90
•
~
80 ~ 70 ;: 60 ~ 50 ~ 40
•
••
•
•
• •
•
'"
z ~ 80
SACCULE
~ 70 ~ 60 50 « Z 40 8 30 ...J
••
•
•
•
0
b
•
••
20 10 12
16
20
24
28
32
36
GESTATIONAL AGE (Weeks)
Fig. 7. Weights (in pg) of utricular and saccular otoconial membranes from fetuses 14 to 36 weeks in gestational age. The points on the graphs represent weights of single membranes from different individuals.
Fig. 6. Utricular otoconial membranes from fetuses of 14 weeks (A) and 36 weeks (B) gestational age. The 36-week specimen is 3.4 times larger in surface area.
in surface area. Numerous tiny perforations can be seen in the thin posterior half of the smaller specimen and an easily discernible "snowdrift" line is present. Compared to the adult specimen shown in Figure lB, the 36-week utricular membrane is about equal in surface area but has less well-developed surface contours. These features were typical of both saccular and utricular otoconial membranes near term. The differing surface areas illustrated in Figures 3, 4, and 6 suggest that otoconial membranes undergo a sizable increase in mass during the period of
fetal development we have studied. In order to obtain a quantitative estimate of the change in mass occurring during the second and third trimesters, dryweight measurements of saccular and utricular membranes were made in cases in which it proved possible to remove the membranes intact from the macular surfaces. Only specimens comprising at least 95% of the total membrane mass (including both the gelatinous and crystalline layers) were weighed. The data obtained are presented in Figure 7. Eight saccular membranes from individuals of 18 to 36-weeks gestational age were included in this portion of the study. These specimens varied in weight from about 24 flg at 18 weeks to 65 flg at 36 weeks with a consistent increase in mass indicated between weeks 18 and 26. Weights for ten utricular membranes from 14 to 34-weeks gestational age are also plotted in Figure 7. The youngest of these specimens weighed 46 fLg and the oldest 98 fLg. A steady increase in mass between weeks 14 and 26 is indicated by these data. For comparison with the measure-
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FETAL OTOCONIAL MEMBRANES
TABLE 1. WEIGHTS OF SACCULAR AND UTRICULAR OTOCONIAL MEMBRANES (OM) FROM 7 INDIVIDUALS 4 DAYS TO 13 YEARS OF AGE
Age 4 days
5 days 2 rno 2 yr 6yr 12 yr 13 yr
Weight (pg) Saccular OM Utricular OM 66.6 58.0 65.2 63.4 66.1 52.2 61.8
100.9 104.0 106.6 120.0 108.6 96.6 120.9
ments in fetuses, weights were obtained for otoconial membranes from seven individuals from four days to 13 years in age. Table 1 shows the values found in each of these cases. Weights for this group of specimens ranged from 96.6 to 120.9 fLg for utricular membranes and from 52.2 to 66.2 fLg for saccular otoconial membranes. The average weight of utricular specimens was 108.2 fLg and of saccular membranes was 61.9 og. The distribution of weights according to age does not suggest that either the saccular or utricular otoconial membrane tends to increase appreciably in weight during the period from infancy to the beginning of the teens. DISCUSSION
In the course of this study, it became clear that the otoconial membranes of the human saccule and utricle vary in shape between individuals to a greater degree than previously recognized. As Figures 2 and 5 illustrate, this variability in form is obvious in specimens from fetuses of similar gestational age. On the other hand, the overall shape and surface topography of membranes from the two sides of the same individual are, in most cases, quite similar. It is probable that the morphological variations we have observed are correlated with differences in head size and/or body weight in different individuals of the same age. We must, however, obtain more specimens in each
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age-group before this correlation can be clarified. The specimens we studied showed a consistent increase in both surface area and weight during the second and third trimesters of development. Although our sample is still too small for detailed quantitative assessment, the present measurements indicate an increase in surface area of three to fourfold and a more than twofold increase in weight for both the saccular and utricular membranes between weeks 14 and 36 of gestation. Data gathered thus far show that the otoconial membranes approach their final weight by the 26th week of gestation. Though the membranes reach approximately adult size and weight during the third trimester, they tend to have less strongly developed surface contours at term than in adulthood. A recently completed study of otoconial membranes in human infants" revealed postpartum changes in the physical character of the gelatinous layer of both saccular and utricular membranes. On the basis of scanning electron microscopic observations, Boss et al" described changes in the configuration of individual otoconial crystals during childhood. These findings, at both the light and electron microscopic levels, indicate that physical properties of the macular suprastructures continue to change well after the time of birth. It is to be expected that such maturational changes at the morphological level are accompanied by alterations in physiological response of the peripheral sense organs. Past medical opinion frequently has failed to include the vestibular receptors among the variables which may influence neurological development in the human infant. Evidence now accumulating for developmental change after birth, as well as for sizable morphological variations between individuals, points toward the desirability of reassessment of this concept.
REFERENCES 1. Schilder P: The vestibular apparatus in neurosis and psychosis. J Nerv Ment Dis 78: 1-23, 137-164, 1933
2. Bender L: Childhood schizophrenia, clinical study of one hundred schizophrenic children. Am J Orthopsychiatry 17:40-56,1947
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3. Ornitz EM: Vestibular dysfunction in schizophrenia and childhood autism. Compr Psychiatry 11: 159-173, 1970 4. Hubbard DG: The Sky;acker. His Flights of Fantasy. New York, Collier, 1973 5. Lyon MF: The development of the otoliths of the mouse. J Embryol Exp Morph 3: 213-229, 1955 6. Veenhof VB: The Development of Stateconia in Mice. Akademie van Wetenschappen Amsterdam. Verhandelinger, 2° reeks 58, 1969 7. Ross MD, Peacor D: The nature and crystal growth of otoconia in the rat. Ann Otol Rhinol Laryngol 84:22-36, 1975 8. Johnsson L-G, Hawkins JE [r: Otolithic membranes of the saccule and utricle in man. Science 157: 1454-1456, 1967 9. Ross MD, Johnsson L-G, Peacor D, et al: Observations on normal and degenerating human otoconia. Ann Otol Rhino! Laryngol 85:310-326, 1976 10. Brenner \VE, Edelman DA, Hendricks CH: A standard of fetal growth for the United
States of America. Am J Obstet Gynecol 126: 555-564, 1976 11. Hawkins JE [r, Johnsson L-G: Microdissection and surface preparations of the inner ear, in Smith CA, Vernon JA (eds l : Handbook of Auditory and Vestibular Research Methods. Springfield, lll, Charles C. Thomas, 1975, pp 5-52 12. Lindeman H: Studies on the morphology of the sensory regions of the vestibular apparatus. Ergeb Anat Entwicklungsgesch 42: 1-113, 1969 13. Lim DJ: Formation and fate of the otoconia. Ann Otol Rhinal Laryngol 82:23-3.5, 1973 14. Ades HW, Engstrom H: Form and innervation of the vestibular epithelia, in Graybier A (ed): The Role of the Vestibular Organs in the Exploration of Space. Washington, D. C., NASA, 1965, pp 23-41 15. Wright CG, Hubbard DG: Observations of otoconial membranes from human infants. Acta Otolaryngol, in press
ACKNOWLEDGMENTS - The authors are indebted to Norman Gant, MD, Associate Professor of Obstetrics and Gynecology, University of Texas Health Science Center at Dallas, for his help in obtaining the material used in this study. We wish also to thank Jacqueline Pate and LeNece Lomonte for their assistance in preparation of the manuscript. REPRINTS - Charles G. Wright, PhD, Callier Centcr for Communication Disorders, 1966 Inwood Road, Dallas, TX 75235.
INTERNATIONAL CONGRESS ON EDUCATION OF THE DEAF The International Congress on Education of the Deaf will be held in Hamburg, West Germany, August 4-8, 1980. For further information write: German Convention Service, Hamburg Office, Hohe Bleichen 13, D-2000 Hamburg 36.
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OBSERVATIONS OF HUMAN FETAL OTOCONIAL MEMBRANES CHARLES G. WRIGHT, PhD DALLAS, TEXAS
DAVID G. HUBBARD, MD
GEOFFREY M. CLARK, PhD
DALLAS, TEXAS
SEATTLE, VVASHlNGTON
Intact otoconial membranes from 31 human fetuses ranging in gestational age from 14 to 36 weeks were studied. At all stages of development specimens from different individuals showed marked variations in overall shape. During the course of the second and third trimesters, both saccular and utricular otoconial membranes were found to increase three to fourfold in surface area and more than twofold in weight. Near the end of gestation the fetal specimens were about equal in area and weight to otoconial membranes from children up to 13 years of age. However, the crystal layers of the fetal membranes had less prominently developed surface contours than usually observed in children and adults, indicating that maturational changes continue after the time of birth.
Decades ago, Schilder! and Bender" published clinical findings which implicated the vestibular system in neurological development and behavior. Their observations have been corroborated by the case studies of Ornitz" and Hubbard/ who emphasized the role played by gravity in human development. Although informative work has been carried out in experimental animals.":" we still have much to learn regarding the basic morphological development of the vestibular apparatus in man. More complete data regarding normal anatomical variation and time-course of maturation is essential to any consideration of human vestibular development in relation to that of the central nervous system as a whole. Studies of the gravity-receptor organs of the saccule and utricle have been hindered by technical limitations of conventional temporal bone histology. This is particularly true in regard to the otoconia which are radically altered by the action of decalcifying agents. The alternative method of microdissection,
as applied to human material by Johnsson and Hawkins," has proved more satisfactory for investigation of these structures. This approach allows rapid preparation of specimens so that surface views of intact otoconial membranes are obtainable without lengthy storage of tissues in preservatives or acidic solutions. Its usefulness in direct anatomical study of human otoconia is amply demonstrated by the recent work of Ross et al.9 The present study of macular suprastructures in human fetuses, using the method of microdissection, is part of a broader investigation of the peripheral vestibular apparatus and its central projections in individuals of all ages. This report presents examples of anatomical variation as well as data on growth in surface area and weight of otoconial membranes from fetuses ranging in gestational age from 14 weeks to approximately term. Weight measurements of fetal specimens are compared with those obtained from a group of infants and children using the same analytical methods.
From the Callier Center for Communication Disorders. University of Texas at Dallas, the Aberrant Behavior Center, Dallas and the Department of Psychology, University of Washington Seattle, Washington. This work was carried out under the auspices of the Lauretta Bender-Paui Schilder Memorial Project and was supported by a grant from the Leland Fikes Foundation to the University of Texas at Dallas subcontracted through the Aberrant Behavior Center, Dallas, Texas.
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METHODS AND MATERIALS Inner ears from a total of 39 individuals were included in this study. Thirty-one of these cases were fetuses, of which 16 were obtained from premature deliveries during the third trimester of pregnancy; the remaining 15 were products of prostaglandin abortions induced in the second trimester. Gestational ages were estimated with the help of data on crownrump, crown-heel, and body weight recently published by Brenner et al." In addition to the fetal specimens, representative cases from a collection of temporal bones taken at autopsy with the Stryker boneplug cutter were studied. This material included inner ears from eight individuals ranging from four days postpartum to 31 years in age. With minor modifications, all material was prepared according to the method described in detail by Hawkins and Johnsson." After removal of temporal bones from the fetal skull using surgical scissors, the middle ear cavity was opened under saline and cleared of mesenchymal tissue when necessary. The ossicular chain was then disarticulated and the stapes gently lifted from the oval window to allow perilymphatic perfusion with either 2% glutaraldehyde or 1% osmium tetroxide. Both fixatives were veronal buffered at pH 7.4. When glutaraldehyde was used as the primary fixative the inner ear structures were stained with 1% osmium tetroxide after overnight glutaraldehyde fixation at refrigerator temperature. After staining, specimens were partially dehydrated in ethanol and studied promptly to avoid any artifacts due to prolonged storage. For photography," the vestibule was widely opened by enlargement of the oval window. The wall of the saccule opposite the macula sacculi was carefully removed and the saccular otoconial membrane was photographed in situ. The anterior portion of the utricle containing the macula utriculi was then dissected from the vestibule and trimmed with iris scissors so as to permit visualization of the utricular otoconial membrane.
Fig. 1. Saccular (A) and utricular (B) otoconial membranes from a 31-year-old man showing typical adult form and surface contours. Arrows indicate "snowdrift" line. DL - Dorsal lobe.
For ease of comparison, all photomicrographs are shown at the same scale with the bar at lower right representing one-half millimeter in each case. With the exception of Figure 3, which shows right and left sides, all specimens are illustrated in the same orientation.
were weighed. The dissected membranes were placed on preweighed aluminum foil tabs (0.3 mg or less) and dried at 60 C for 48 to 72 hours. Individual membranes were then weighed on a microbalance.... with maximum sensitivity of 0.1 fig.
After photographs were obtained, an attempt was made to remove the whole otoconial membrane, including both the gelatinous and crystalline layers, from the surface of the sensory efithelium. When this procedure was suecessfu a dry-weight determination was then carried out. Great care was taken in these dissections; only those specimens known to represent at least 95% of the entire membrane mass
RESULTS
The general surface morphology of the saccular and utricular otoconial membranes is illustrated in Figure 1 by specimens from a young adult. The otoconial membranes cover the entire macular surface and have approximate-
"Model 78 stereomlcroscope. Wild-Heerbrugg Instruments, Inc., Farmingdale, NY. "'Model 440, Calm Division, Ventron Instruments Corp., Paramount, CA.
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Fig. 2. Variations in shape of saccular otoconial membranes from fetuses of 20 weeks (A), 22 weeks (B), 30 weeks (C), and 34 weeks (D) gestational age.
ly the same shape as the underlying sensory epithelia. Occasionally, accumulations of crystals extending beyond the borders of the maculae are present. This is true of the utricular specimen in Figure IB where a sizeable mass of extramacular otoconia can be seen surrounding the posterior end of the membrane.
present which contribute to the complex texture of the surface. The characteristic hook shape of the saccular otoconial membrane is due to an extension of its anterior portion which projects dorsally. We have found this dorsal lobe (or, dorsal extension) to be quite variable in size from one individual to another.
In man, a distinct, curved ridge is typically found on the surface of the crystalline layer of both the saccular and utricular otoconial membranes. This contour marks the position of a specialized region in the gelatinous layer of the membrane which overlies the striola of the neuroepithelium.P-" In accordance with the terminology first applied by Ades and Engstrom> and later used by Johnsson and Hawkins" in the description of human material, this surface feature of the otoconial layer will be referred to as the "snowdrift" line. Especially on the utricular membrane, many smaller ridges and grooves are
Striking differences in the form and size of the dorsal lobe are apparent in the four fetal specimens shown in Figure 2. These membranes are, in fact, quite varied in overall shape. At this stage in development (20-34 weeks), the otoconial layer appears almost as thick as that in the adult, but the "snowdrift" line is usually less prominent. Left and right saccular membranes from a 16-week fetus are seen in Figure 3. Compared to the specimens shown in Figure 2, these membranes are smaller in surface area and the crystal layers are noticeably thinner. Particularly near
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Fig. 3. Left (A) and right (B) saccular otoconial membranes from a fetus of 16 weeks gestational age. Note the thin crystal layers on both specimens and accumulations of otoconia in the region between the dorsal lobe and main body.
the margins, the crystals are sparsely distributed, giving the membranes a sieve-like appearance. Three fetuses of approximately 16-weeks gestational age were included in our material; the otoconial membranes showed very similar characteristics in each of these cases. The rather ahnond-shaped specimen shown in Figure 3A illustrates a form which has occasionally been seen in saccular membranes from infants and children as well as fetuses. In this case, a thin layer of crystals is present in the area between the dorsal lobe and the main body of the crystal layer. On the opposite side, this region is nearly devoid of crystals so that the dorsal lobe is more clearly outlined. As was generally observed, however, the overall shape of these membranes from the right and left sides is quite similar rela-
Fig. 4. Saccular otoconial membranes from fetuses of 14 weeks (A) and 32 weeks (B) gestational age. The more mature membrane is approximately four times larger in surface area.
tive to the large variations seen between different individuals. The youngest gestational age in the present series is represented by the 14week specimen shown in Figure 4, where it is compared to a saccular otoconial membrane from a 32-week fetus. Planimeter measurements showed an approximately fourfold difference in surface area between the two membranes. In spite of its small size, the 14-week specimen displays a clear "snowdrift" line and has a well-differentiated dorsal lobe. Photomicrographs of utricular otoconial membranes from four fetuses in the 17 to 30-week gestational age group are presented in Figure 5. Like the saccular membranes, the specimens from the utricle show marked variations in shape - from nearly round to distinctly
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Fig. 5. Variation in shape and surface morphology of utricular otoconia! membranes from fetuses of 17 weeks (A), 22 weeks (B), 26 weeks (C), and 30 weeks (D) gestational age.
elongated. In the 17 and 20-week specimens the otoconial layer has a thin, porous appearance much like that seen in the membranes from the saccule at approximately 16 weeks.
A utricular otoconial membrane of 14-weeks gestational age is shown together with one from a 36-week fetus in Figure 6. The more mature membrane is approximately 3.4 times larger
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272
WRIGHT ET AL UTRICLE
•
110 100 -;;; 90
•
~
80 ~ 70 ;: 60 ~ 50 ~ 40
•
••
•
•
• •
•
'"
z ~ 80
SACCULE
~ 70 ~ 60 50 « Z 40 8 30 ...J
••
•
•
•
0
b
•
••
20 10 12
16
20
24
28
32
36
GESTATIONAL AGE (Weeks)
Fig. 7. Weights (in pg) of utricular and saccular otoconial membranes from fetuses 14 to 36 weeks in gestational age. The points on the graphs represent weights of single membranes from different individuals.
Fig. 6. Utricular otoconial membranes from fetuses of 14 weeks (A) and 36 weeks (B) gestational age. The 36-week specimen is 3.4 times larger in surface area.
in surface area. Numerous tiny perforations can be seen in the thin posterior half of the smaller specimen and an easily discernible "snowdrift" line is present. Compared to the adult specimen shown in Figure lB, the 36-week utricular membrane is about equal in surface area but has less well-developed surface contours. These features were typical of both saccular and utricular otoconial membranes near term. The differing surface areas illustrated in Figures 3, 4, and 6 suggest that otoconial membranes undergo a sizable increase in mass during the period of
fetal development we have studied. In order to obtain a quantitative estimate of the change in mass occurring during the second and third trimesters, dryweight measurements of saccular and utricular membranes were made in cases in which it proved possible to remove the membranes intact from the macular surfaces. Only specimens comprising at least 95% of the total membrane mass (including both the gelatinous and crystalline layers) were weighed. The data obtained are presented in Figure 7. Eight saccular membranes from individuals of 18 to 36-weeks gestational age were included in this portion of the study. These specimens varied in weight from about 24 flg at 18 weeks to 65 flg at 36 weeks with a consistent increase in mass indicated between weeks 18 and 26. Weights for ten utricular membranes from 14 to 34-weeks gestational age are also plotted in Figure 7. The youngest of these specimens weighed 46 fLg and the oldest 98 fLg. A steady increase in mass between weeks 14 and 26 is indicated by these data. For comparison with the measure-
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FETAL OTOCONIAL MEMBRANES
TABLE 1. WEIGHTS OF SACCULAR AND UTRICULAR OTOCONIAL MEMBRANES (OM) FROM 7 INDIVIDUALS 4 DAYS TO 13 YEARS OF AGE
Age 4 days
5 days 2 rno 2 yr 6yr 12 yr 13 yr
Weight (pg) Saccular OM Utricular OM 66.6 58.0 65.2 63.4 66.1 52.2 61.8
100.9 104.0 106.6 120.0 108.6 96.6 120.9
ments in fetuses, weights were obtained for otoconial membranes from seven individuals from four days to 13 years in age. Table 1 shows the values found in each of these cases. Weights for this group of specimens ranged from 96.6 to 120.9 fLg for utricular membranes and from 52.2 to 66.2 fLg for saccular otoconial membranes. The average weight of utricular specimens was 108.2 fLg and of saccular membranes was 61.9 og. The distribution of weights according to age does not suggest that either the saccular or utricular otoconial membrane tends to increase appreciably in weight during the period from infancy to the beginning of the teens. DISCUSSION
In the course of this study, it became clear that the otoconial membranes of the human saccule and utricle vary in shape between individuals to a greater degree than previously recognized. As Figures 2 and 5 illustrate, this variability in form is obvious in specimens from fetuses of similar gestational age. On the other hand, the overall shape and surface topography of membranes from the two sides of the same individual are, in most cases, quite similar. It is probable that the morphological variations we have observed are correlated with differences in head size and/or body weight in different individuals of the same age. We must, however, obtain more specimens in each
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age-group before this correlation can be clarified. The specimens we studied showed a consistent increase in both surface area and weight during the second and third trimesters of development. Although our sample is still too small for detailed quantitative assessment, the present measurements indicate an increase in surface area of three to fourfold and a more than twofold increase in weight for both the saccular and utricular membranes between weeks 14 and 36 of gestation. Data gathered thus far show that the otoconial membranes approach their final weight by the 26th week of gestation. Though the membranes reach approximately adult size and weight during the third trimester, they tend to have less strongly developed surface contours at term than in adulthood. A recently completed study of otoconial membranes in human infants" revealed postpartum changes in the physical character of the gelatinous layer of both saccular and utricular membranes. On the basis of scanning electron microscopic observations, Boss et al" described changes in the configuration of individual otoconial crystals during childhood. These findings, at both the light and electron microscopic levels, indicate that physical properties of the macular suprastructures continue to change well after the time of birth. It is to be expected that such maturational changes at the morphological level are accompanied by alterations in physiological response of the peripheral sense organs. Past medical opinion frequently has failed to include the vestibular receptors among the variables which may influence neurological development in the human infant. Evidence now accumulating for developmental change after birth, as well as for sizable morphological variations between individuals, points toward the desirability of reassessment of this concept.
REFERENCES 1. Schilder P: The vestibular apparatus in neurosis and psychosis. J Nerv Ment Dis 78: 1-23, 137-164, 1933
2. Bender L: Childhood schizophrenia, clinical study of one hundred schizophrenic children. Am J Orthopsychiatry 17:40-56,1947
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3. Ornitz EM: Vestibular dysfunction in schizophrenia and childhood autism. Compr Psychiatry 11: 159-173, 1970 4. Hubbard DG: The Sky;acker. His Flights of Fantasy. New York, Collier, 1973 5. Lyon MF: The development of the otoliths of the mouse. J Embryol Exp Morph 3: 213-229, 1955 6. Veenhof VB: The Development of Stateconia in Mice. Akademie van Wetenschappen Amsterdam. Verhandelinger, 2° reeks 58, 1969 7. Ross MD, Peacor D: The nature and crystal growth of otoconia in the rat. Ann Otol Rhinol Laryngol 84:22-36, 1975 8. Johnsson L-G, Hawkins JE [r: Otolithic membranes of the saccule and utricle in man. Science 157: 1454-1456, 1967 9. Ross MD, Johnsson L-G, Peacor D, et al: Observations on normal and degenerating human otoconia. Ann Otol Rhino! Laryngol 85:310-326, 1976 10. Brenner \VE, Edelman DA, Hendricks CH: A standard of fetal growth for the United
States of America. Am J Obstet Gynecol 126: 555-564, 1976 11. Hawkins JE [r, Johnsson L-G: Microdissection and surface preparations of the inner ear, in Smith CA, Vernon JA (eds l : Handbook of Auditory and Vestibular Research Methods. Springfield, lll, Charles C. Thomas, 1975, pp 5-52 12. Lindeman H: Studies on the morphology of the sensory regions of the vestibular apparatus. Ergeb Anat Entwicklungsgesch 42: 1-113, 1969 13. Lim DJ: Formation and fate of the otoconia. Ann Otol Rhinal Laryngol 82:23-3.5, 1973 14. Ades HW, Engstrom H: Form and innervation of the vestibular epithelia, in Graybier A (ed): The Role of the Vestibular Organs in the Exploration of Space. Washington, D. C., NASA, 1965, pp 23-41 15. Wright CG, Hubbard DG: Observations of otoconial membranes from human infants. Acta Otolaryngol, in press
ACKNOWLEDGMENTS - The authors are indebted to Norman Gant, MD, Associate Professor of Obstetrics and Gynecology, University of Texas Health Science Center at Dallas, for his help in obtaining the material used in this study. We wish also to thank Jacqueline Pate and LeNece Lomonte for their assistance in preparation of the manuscript. REPRINTS - Charles G. Wright, PhD, Callier Centcr for Communication Disorders, 1966 Inwood Road, Dallas, TX 75235.
INTERNATIONAL CONGRESS ON EDUCATION OF THE DEAF The International Congress on Education of the Deaf will be held in Hamburg, West Germany, August 4-8, 1980. For further information write: German Convention Service, Hamburg Office, Hohe Bleichen 13, D-2000 Hamburg 36.
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