Paper - The development and structure of the otic (endolymphatic) sac
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Watzke D. and Bast TH. The development and structure of the otic (endolymphatic) sac. (1950) Anat. Rec. : 361-379.
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- 1 The Development and Structure of the Otic (Endolymphatic) Sac
- 1.1 Introduction
- 1.2 Historical
- 1.3 Problem
- 1.4 Material
- 1.5 Observations
- 1.5.1 A. Gross changes
- 1.5.2 B. Histological Considerations
- 1.5.3 C. Functional Considerations
- 1.6 Summary
- 1.7 Literature Cited
- 1.8 Plates
The Development and Structure of the Otic (Endolymphatic) Sac
Donald Watzke and T. H. Bast
Department of Anatoariy, University of Wiscons-in, Madison, Wisconsin
(1950) Seventeen Figures
A review of the literature on the ear reveals the general concept that the structure and extent of the otic sac in the adult is like that of the half term fetus. The purpose of this report is to show that while most of the internal ear attains adult proportions at midterm, the otic sac undergoes great change in late fetal and postnatal life. This difference will seem less odd if one recalls that most of the internal ear becomes encased i11 the bony otic capsule shortly after midterm whereas the otic sac which is a. terminal saccular enlargement of the otic duct, lies between the inner and outer layers of the dura on the posterior surface of the petrous portion of the temporal bone Where it can expand with the growing dura. The proximal part of the sac comes gradually to lie in the slit-like distal expansion of the aquaeductus vestibuli formed by a shelf-like spur of bone which grows over the original opening of the aqueduct. This slit-like opening of the aquaeductus vestibuli is readily seen in dry skulls. Just caudal to this slit a more or less prominent depression can be observed on the bone which is apparently produced by the ﬂuid pressure in the otic sac which overlies this area (fig. 14) . The shape and extent of this depression varies in different skulls as does also the size of the shelf of bone which overlies the slit-like opening of the aqueduct. Results of the study of the size and position of these structures in a large number of skulls will be presented in a later paper. It was in part the large size of the depression that led us to investigate the suspicion that the otic sac in the adult was much larger than was generally believed.
It should be recalled brieﬂy that the otic duct and sac, which are parts of the otic labyrinth and are of ectodermal origin, are very early differentiated from the otic vesicle in the 7 mm embryo as a medial diverticular projection (Bast, Anson and Gardner, ’47). This projection is produced because of an anteroposterior crease in the otic vesicle known as fold I. In subsequent development, fold II grows in to delimit the future otic duct from the sacculus, while later fold III, by deepening into the vesicle, comes to divide the proximal part of the otic duct into two ducts which connect the latter to the sacculus and utriculus, respectively. The otic duct, terminating in the otic sac, is a relatively smooth-contoured projection from the otic vesicle. At this early stage, the duct lies within the otic capsule paralleling the crus commune of the posterior and superior semicircular canals. The sac lies in a straight line with the duct, also parallel to the crus commune (fig. 1), but outside the otic capsule and between the layers of the dura.
This embryological forerunner of the adult duct and sac does not always remain as a smooth-walled tube (Anson, ’34). After the 25 mm stage low rugae appear in the proximal portion of the tube, as described by Anson and Wilson (’36). Guild described these rugae as seen in the adult guinea pig where they possess a specialized epithelium and subjacent vascular stroma. These rugosities were described earliest by Boettcher (1869) in the cat and in the human newborn, and later by Sterzi (’10) in man. That these rugae are actually elongate plaits has been shown by means of wax reconstructions (Anson and VVilson, ’36; Anson and Nesselrod, ’36; Bast, Anson and Gardner, ’47).
Another feature of the early sac is its relation to the lateral sinus. Bast, Anson and Gardner (’47) pointed out that the sac overlies the sinus in the 50 mm embryo.
After midterm (about the 180 mm stage) the sac undergoes certain changes, a few of which have brieﬂy been referred to in the literature. Thus, Bast and Anson (’49) in a 3-year-old child showed that the earlier straight course of the otic duct and sac undergoes alteration and assumes a rather marked downward bending, so that the long axis of the sac is directed more caudally instead of dorsally.
Earlier descriptions of the sac of fetuses also include reference to a prominent pointed projection at its distal end (Macklin, ’21; Bast, ’30; Anson, ’33). It appears that, with age, this slender distal projection becomes absorbed into the sac proper.
It became apparent to us in studying adult petrous bone sections that oftentimes the entire otic sac was not included in the sections made. We have also noticed that accounts of the sac in textbooks and recent literature represent the general form and relationship of the adult sac as that of a fetus. It is very probable that one reason this structure has not previously been studied in the adult in any detail is that in the preparation of petrous—temporal bones for histological sectioning, the dura mater on the posterior surface is torn off, thus destroying the sac which is lodged in it, or the block of tissue was out too small thus removing much of the sac. Realizing this we took special precautions to cut our blocks of the petrous bone so that the dura with the otic sac together with part of the sigmoid sinus remained intact. Thus, the entire structure could be modeled from the serial sections into which the block was cut.
Our findings are based upon study of histological sections of petrous bones and recostructions of internal ears, both fetal and adult. The internal ears were reconstructed from serial sections of petrous bones at an-enlargement of 20 diameters. Two fetal ears were chosen for reconstruction; the one 18% week-old (150 mm C.R. length), and the other 34-week—o1d (310 mm C.R. length). In our adult series, ears from individuals aged 38, 62 and 65 were chosen for reconstruction. In all, about 18 adult petrous bones, with complete serial sections, were studied.
A. Gross changes
A study of our reconstructions (figs. 1-4) reveals three significant gross changes in the otic duct and sac during late fetal and postnatal life, namely: bending of the duct, enlargement of the sac, and altered relationship of the sac to the sigmoid sinus.
1. Bending of duct
In a fetus of 1837-weeks (150 mm) (fig. 1), the otic duct and sac lie in a straight line parallel to the long axis of the crus commune. The pointed distal projection of the sac points dorsalward. In the fetus of 34 weeks (310 mm) (fig. 2) a slight bend occurs at the junction between the isthmus of the duct and sac. The sac thus shifts from a position overlying the upper limb of the posterior canal to one overlying the middle of the posterior canal and its long axis is somewhat caudally directed. In the adult (figs. 3 and 4) the bending is most prominent and occurs more in the proximal part of the sac than in the isthmus of the duct. The long axis of the sac now definitely points in a caudal direction. This change in the relationship of the sac to the rest of the internal ear is definitely a result of the growth of the posterior cranial fossa, whose lining dura and periosteum carry the contained otic sac along as they expand. This bending of the otic duct and sac is not a new finding, but a Verification of the observation of Bast and Anson (’49) in a. three-year-old child.
2. Enlargement of the sac
The second change noted is the marked increase in size of the sac from the fetus to the adult. In a fetus of 30 mm the sac measures about 1.3 mm in length, in the 150 mm and 310 mm fetus (figs. 1 and 2) it is 5 mm in length, and in two of the adult specimens reconstructed the sac is 13 mm and 15 mm long, respectively (figs. 3 and 4). These figures represent the longest dimension of the sac proper. There is also a corresponding increase in the width of the sac. THE OTIC sno 365
It can be seen that there is as much as a three-fold increase in the size of the sac from midterm to adult life. This fact becomes more significant when it is recalled that the remainder of the otic labyrinth has reached its maximum size by midterm. The internal ear of the 310 mm fetus resembles the adult ear in all respects except that the otic sac is much smaller (compare figs. 1 and 4). There is not much gross change in the thickness of the sac when fetal and adult ears are compared, however, as will be pointed out, adult specimens show some variations. At all ages the structure is grossly leaf-like in appearance, the proximal portion connecting to the otic duct like a leaf attached to its stem. The fetal specimens usually show thinner sacs, however, commensurate with the smaller total size of the sac.
3. Relationship of sac to the sigmoid sinus
A third fact to be noted is that in the fetus the sac overlies the sigmoid sinus (fig. 1). In the 310 mm fetus the sinus has begun to move away from the internal ear as the posterior cranial fossa expands. The sac still extends to the sinus, but no longer overlies it. The rich venous plexus described by Bast (’32) opens widely into the sigmoid sinus (fig. 2). As the posterior fossa grows during postnatal life, the sinus is “pulled away’ ’ from the sac, the are formed by the junction of the sinus with the jugular bulb becomes larger, and the adult sac now lies in less intimate relation with the sinus. The rich venous plexus surrounding the sac still drains into the somewhat removed sinus. Even though the sac is increasing in size after birth, it does not quite keep up with the increase in size of the cranial cavity, but the tip and medial margin of the otic sac always end near the sigmoid sinus (fig. 4).
B. Histological Considerations
Three regions of the otic sac are commonly recognized, the proximal or rugose portion, the sac proper and the distal projection. In the adult the latter is essentially absent as it has been absorbed by the sac proper. For the consideration of structure and function in the adult it will be advantageous to subdivide the sac proper further into a lateral and a medial portion. The latter is nearest to the sigmoid sinus and juglar bulb.
1. Folds and rugosities
As already indicated the otic sac is not a smooth walled structure in all of its parts. The proximal part of the sac which lies in the distal expanded part of the aquaeductus Vestibuli, under the shelf of bone, is as a rule thrown into prominent folds or rugae previously described. These rugosities are not confined to the proximal part of the sac but extend caudally along the medial part of the sac proper (fig. 5). Such rugosities on the sac proper were noted in a three-year-old child by Bast and Anson ( H19) and pictured in their figure 23B. In our present series of adult ears they were a constant feature (figs. 5, 8, 9, and 13). In some cases Where the otic sac was widely distended they were reduced to a minimum (fig. 12) but they were always present.
2. Epithelium of the otic sac
The otic sac is lined by a simple epithelium whose cells have for the most part a cuboidal to columnar form (figs. 15, 16 and 17). In those places Where rugosities occur the cells as a rule are taller than in the smoother portions of the otic sac. Consequently the taller columnar cells are more constant in the medial part which lies near the sigmoid sinus, than in the lateral part of the sac. The significance of this will be discussed in a subsequent paragraph in relation to Venous drainage.
Special attention should be directed to the position of the nuclei in the lining epithelial cells since their location may indicate functional polarity. In most of the cells of the epithelium lining the otic sac the nuclei lie nearer their free than their basal end (figs. 15 and 16). Already in a fetus of 34 Weeks (310 mm) the nuclei lie closer to the free than basal end of the cell. The same polarity is seen in the lining epithelial cells of the adult otic sacs. This peripheral location of the nucleus gains significance if one recalls that in simple columnar epithelia, which function as external secreting glands and eliminate their product from the free end of the cell, the nucleus is, as a rule, placed near the basal end of the cell. On the other hand in internal secreting glands and resorptive epithelia where the cells pour their secretion through the basal end, as in the beta cells of the pancreas, or the cells of the thyroid, or the ameloblasts of the enamel organ, there is a marked tendency for the nuclei to lie at the opposite pole or free margin of the cells. If such polarity is of any significance then the epithelium of the otic sac should have a resorptive function.
3. Content of otic sac
Guild ( ’27 ) in his histological studies of the otic sac in the guinea pig, noted the presence of cellular debris in its lumen. Such cellular debris has also been noted in the adult human. In sacs that are distended as in figure 12, little or none is found, but in the more collapsed sacs, as seen in figures 9 and 10, and figure 13, the deposits are abundant. The contents of such sacs consist of cellular debris and often a homogeneous stainable ﬂuid which appears viscid in histological preparations.
4. Subepithelial connective tissue and blood vessels
The rugose portion of the otic sac lies in the fan-shaped slit-like portion of the aquaeductus vestibuli. Here the sac is surrounded by the periosteum of the aquaeduct. This periosteum, as it emerges from the duct, becomes the periosteum on the posterior surface of the petrous bone where it is frequently spoken of as the outer dura. Overlying it is the dura proper. The otic sac proper lies between these two layers of dense fibrous connective tissue. The epithelium of the sac does not, however, rest directly on this dense connective tissue, but is separated from it by varying amounts of very fine, loose, vascular connective tissue containing a rich venous capillary plexus which drains into larger veins which in turn drain into the sigmoid sinus. All of these vessels lie between the two layers of the dura. Along the medial part of the otic sac the loose vascular tissue is very abundant, but around the lateral part of the sac this loose tissue is almost absent. This difference between the subepithelial tissue is best seen by comparing figure 9 which is the medial and figure 10 which is the lateral part of the otic sac of a 65-year-old man. It is significant to note that the loose vascular subepithelial tissue surrounds that part of the sac where most rugae occur and where the rich venous plexus lies which drains into the sigmoid sinus.
5. The lumen of the otic sac
The lumen of the otic sac is as a general rule a slit-like space because the sac lies compressed between the two layers of the dura. The width of this space is not the same in all cases and varying degrees of distension can be noted (figs. 7-13). Whether such distension as shown in figure 12 is due to pressure of the contained otic ﬂuid or to the technical procedures in the preparation of histological sections is one that cannot be definitely determined. A careful study of histological sections of a number of such distended sacs leaves the impression that most of them are not technical artifacts. In all such cases of distension the subepithelial connective tissue is much denser and less vascular than in the more collapsed sacs. This may have a functional significance.
On the other hand there are sacs in which the lumen is slitlike and where the epithelia from the opposing walls meet. In such cases, especially where the tips of rugae meet, the opposing epithelia seem to fuse thus interrupting the continuity of the lumen (fig. 17). This was first described in a three-yearold child by Anson and Nesselrod (’36) and then by Bast and Anson ( ’49). Later, at these points of fusion, the epithelium seems to disintegrate and be replaced by connective tissue. Thus the continuous epithelial lining of the sac in the fetus becomes changed, in some adult cases, to one in which the fused epithelium is replaced at numerous points by a vascular connective tissue (figs. 9 and 13). At these points the connective tissue has completely grown through the sac so that in histological sections the sac appears as a series of isolated pockets surrounded by vascular connective tissue. In models of portions of such an otic sac (figs. 5 and 6) the holes represent the places where the epithelial sac is interrupted and is replaced by connective tissue. Obliteration of areas in the sac by connective tissue was not noted in fetuses, but is present in a little less than half of the adults. The extreme stretching of the sac due to the growth of the posterior cranial fossa may contribute to this condition.
C. Functional Considerations
In 1927 Guild concluded from his studies on the otic sac in guinea pigs, that the sac was a place where resorption of the otic ﬂuid took place. The presence in the sac of cellular debris and materials injected into the cochlear duct led to this conclusion.
Bast (’32) and Bast and Anson (’49) describe and show pictures of the rich Venous plexus around the medio-caudal part of the otic sac in the human fetus, and drainage of this plexus into the sigmoid sinus. This indicates that the sac should be an ideal place for filtration of otic ﬂuid. Hallpike and Cairns (’38) reported the absence of the normal vascularity around the sac in two cases of Meniere’s disease which showed a generalized distension of the otic system. Portmann (’27) surgically drained the otic sac as a treatment for vertigo, resulting in a cure for several of his patients. In order to determine whether the lack of resorption of otic ﬂuid is to blame for increased fluid pressure in the otic labyrinth, known as hydrops, Lindsay (’47) reported that obliteration of the otic sac in monkeys did 11ot seem to alter the normal volume of otic ﬂuid. His animals were sacrificed about three months after operation which may be too short a period for appreciable changes to take place.
If one may use anatomical structure and organization to suggest function then our present findings indicate that the sac in adult man is the logical structure for the resorption of otic ﬂuid. The anatomical evidences which indicate this are: (1) The otic sac lies in close relationship to the sigmoid sinus into which the rich Venous plexus of the sac drains. (2) The Viscid ﬂuid and cellular debris noted in many of the partially collapsed sacs indicates concentration of the content (figs. 9, 10, and 13). (3) The epithelium of most sacs shows a reversed polarity with the nuclei lying nearer the free than the basal margin of the cells (figs. 15 and 16). (4) finally, the subepithelial connective tissue is loose and very vascular around those sacs which are collapsed and contain debris (figs. 9 and 13), Whereas in distended sacs (fig. 12) there is no debris and the surrounding tissue is dense and less vascular. This latter agrees with the finding of Hallpike and Cairns.
- The otic labyrinth attains adult proportions at midterm whereas the otic sac enlarges to three times the midterm size in late fetal and postnatal life.
- In the early fetus the otic duct and sac lie in a straight line parallel to the crus commune, whereas after midterm the duct and sac bend almost at a right angle. A close relationship to the sigmoid sinus is maintained throughout life.
- The proximal and medial portions of the sac are rugose and are supplied with a rich venous plexus.
- The epithelium of the sac is columnar with a tendency for the nuclei to be situated near the free border of the cells, indicating a resorptive function.
- Due perhaps to extreme stretching of the sac, the opposing epithelia, in some instances, fuse. At such points of fusion some sacs become perforated by vascular connective tissue, producing interruptions in the continuity of the epithelial sac.
Anson BJ. The distal projection of the endolymphatic sac in human embryos. (1933) Anat. Rec. 701. 57, 110. 1, pp. 55-58.
-—————— 1934 The early development of the membranous labyrinth in mammalian embryos. Anat. Rec., 59: no. 1 and Suppl. 15-25.
ANSON, B. J ., AND J. P. NESSELROD 1936 Endolymphatic and associated ducts in man. Arch. of Otolaryngology, 24: 127-140.
ANSON, B. J., AND J. G. WILSON 1936 The form and structure of the endolymphatic and associated ducts in the child. Anat. Rec., 65 : 485-498.
BAST, T. H. 1930 Ossification of the otic capsule in human fetuses. Carnegie Contrib. to Embryology (no. 121), 21: 53-82.
Bast TH. Development of the Otic Capsule I. Resorption of the cartilage in the canal portion of the otic capsule in human fetuses and its relation to the growth of the semicircular canals. (1932) Arch. Otolaryng. 16:19
--——-—'—— 1932 Development of the otic capsule. I. Resorption of the cartilage in the canal portion of the otic capsule, etc. Arch. of Otolaryngology, 16’ : 19-38.
BAST, T. H., AND B. J. ANSON 1949 The Temporal Bone and the Ear. Charles Thomas, Publ., Springfield, Illinois.
BAST, T. H., B. J. ANSON AND W. D. GARDNER 1947 The developmental course of the human auditory vesicle. Anat. Rec, 9.9: 55-74.
BOETTCHER, A. 1869 Ueber Entwicklung und Bau des Gehiirlabyrinths nach Untersuchungen an Siiugethieren. Verh. d. Kais, Leop—Carol. d. akad. d. N aturforscher, 35 : 1-203. 1869 Ueber den aquaeductus vestibuli bei Katzen und Menschen. Arch. f. Anat. u. Physiol., Jahrg. 1869. 3724380.
GUILD, S. R. 1927a Observations upon the structure and normal contents of the ductus and saccus endolymphaticus in the guinea pig. Am. J. Anat., 3.9: 1-56. 1927b The circulation of the endolymph. Am. J. Anat., 3.9 : 57-81.
HALLPIKE, O. S., AND H. CAIRNS 1938 Observations on the pathology of Meniere ’s syndrome. J. Laryng. a.nd Otol., 53: 625-654.
LINDSAY, J. R. 1947 Effect of obliteration of the endolymphatic sac and duct in the monkey. Arch. of Otolaryngology, 45 .' 1-13.
Macklin CC. the skull of a human fetus of 43 millimeters greatest length. (1921) Contrib. Embryol., Carnegie Inst. Wash. Publ., 48, 10:59-102.
MACKLIN, O. C. 1921 The skull of a fetus of 43 mm greatest length. Contrib. to Emb., no. 48, extracted from Publ. 273 Carnegie Inst., Wash., 57—103.
PORTMANN, G. 1927 Vertigo: Surgical treatment by opening the saccus endolymphaticus. Arch. of Otolaryngology, 6‘: 309-319.
STERZI, G. 1910 Il sacco endolinfatico. Richerche anatomiche ed embriologiche. Gegenbauer’s morph. Jal1rb., 3.9: 446-496.
After the printers proofs were corrected the following article came to my attention.
SECRETAN, J. P. 1944 De l’histologie normale du sac endolymphatique ehez l’homme. Acta Otolaryngologia, 32: 119-163.
His account of the loose vascular subepithelial connective tissue agrees with our findings along the rugose and medial margin of the sac. He makes no mention of the denser connective tissue along the lateral margin.
1-4 Drawings from models of human internal ears reconstructed at an enlargement of 20 diameters, and in reproduction reduced in size to X 2%. The otic sac and that portion of the otic duct not surrounded by periotic tissue is represented in heavy black shading. The rest of the model of the internal ear represents the periotic labyrinth, together with the lateral sinus and jugular bulb. With the exception of figure 3 all reconstructions are of left ears.
1 150 mm fetus (18.5 weeks).
2 310 mm fetus (34 weeks).
3 38-year-old adult.
4 65-year-old adult.
5 a11d 6 Photographs of wax plate models of portions of the otic sac shown in figure 4. figure 5 is a model from the region indicated by the arrow (-9) in figure 4, and figure 6 is a model of the distal end of the sac. These models show the interruptions in the epithelial sac as indicated in the photomicrograph shown in figures 9 and 10. The irregular folds seen at the right in figure 5 are the rugae along the medial margin of the otic sac. Magnification of 5 and 6 is X 21.
7-10 Histological sections through the otie sae. Magnification X 116.
7 The section is taken at the level shown by the X in figure 1. (Wis. series 39L, s1. 16, sec. 6, 150 mm fetus, age 18% Weeks.)
8 A section at the level represented by the )< in figure 2 a11d shows the medial, rugose edge of the sac. (Wis. series 68L, s1. 11, sec. 2, 310 mm fetus, age 34 weeks.)
9 and 10 Sections taken from the sac shown i.11 figure 4. (Cadaver specimen, left ear, s1. 89, sec. 2, age 65 years.) Both represent sections approximately through the n1iddle part of the sac at the junction with the proximal rugose portion. Connective tissue (shown at arrows) is seen to interrupt the continuity of the sac. In 9 and 10 the lumen of the sac is partially filled with debris. figure 9 is taken from the rnerlial border of the sac and shows the loose vascular subepithelial stroma which is in contrast to the more dense subepithelial comrective tissue at the lateral border of the sac shown in figure 10.
11-13 Histological sections through the otic sac. Magnification )( 116.
11 A section through the sac at the level shown by the X i11 figure 3; the lateral edge of the sac is shown. (Wis. series P.24R, sl. 470, age 38 years.)
12 A section through a11 adult sac which was large a11d dilated. (Wis. series P.10L, sl. 425, age 62 years.)
13 Another adult sac in the rugose part, demonstrating the interruptions in the continuity of the epithelium by vascular connective tissue (at arrows). (Wis. series P.25R, sl. 387, age 17 yea.rs.)
In 11 and 12 note the more uniform, dense connective tissue around the sac a.nd the relative absence of debris and secretion in the lumen.
376 emm 0.30 mwo wrwam m oozfie €>a§C._.. >26 A. m.
14 A photograph showing the posterior surface of the petrous pa.rt of the left temporal bone, i.e., the surface facing the posterior cranial fossa. In life this bony surface is covered by dura mater and the otie sae lies between the layers of the dura in the bony fossa shown at S.I. Abbreviations: C.S.C., crest of the superior semicircular canal; S.S.I., impression of the sigmoid sinus; S.I., impression lodging the otie (endolyrnphatic) sac; J .F., jugular fossa which lodges the jugular bulb; S.F., subareuate fossa; I.A.M., internal auditory meatus; A.C., opening of the aquaeduetus cochleae.
15, 16, and 17 High power photomierograplis of sections of otie sacs. Magnifi~ eation X 300. I11 15 and 1.6 the nuclei of the lining epithelium are seen to lie near the free margin. In 17 the epithelia of the opposing walls are fused, and the underlying basement membrane at these points seems to be interrupted permitting ingrowth of the underlying connective tissue.
15 Wis. series P.24B, sl. 4170, age 38 years. 16 Wis. series P.13L, sl. 405, age 62 years. 17 Wis. series P.3TL, sl. 325, age 8 3-'ea.rs.
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