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Ultrastructural demonstration of cilia in the adult human ependyma.

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BRIEF COMMUNICATION
Ultrastructural Demonstration of Cilia in the
Adult Human Ependyma '
SUBIMAL ROY, ASAO HIRANO AND HARRY M. ZIMMERMAN
Division of Neuropathology, Department of Pathology, Montefiore
Hospital a n d Medical Center, a n d Albert Einstein College of
Medicine, Bronx, N e w York, N e w York 10467
Ependyma from random sites of lateral, third and fourth ventricles including the aqueduct in five adult human brains was examined by transmission electron microscopy. In all the specimens studied, cilia were present in
variable numbers in the ependymal cells. Our study thus establishes that there
is widespread presence of cilia in the ependymal cells of the ventricular system
in the adult human brain.
ABSTRACT
It has been stated in many standard
textbooks that human ependymal cells are
ciliated only in embryonic life and that in
the adult, cilia are either absent or occur
only in patchy areas (Strong and Elwyn,
'53; Ranson and Clark, '59; Bloom and
Fawcett, '62; Truex and Carpenter, '70).
These observations are apparently based
on light microscopic study which does not
appear to provide unequivocal evidence of
the presence or absence of cilia. Worthington and Cathcart ('63) showed evidence of
ciliary movement in the adult human
ependymal cells examined by water immersion lenses. Scanning electron microscopic
examination by Bruni, Montemurro, Clattenburg and Singh ('72) has also suggested
the presence of cilia in the adult human
ependyma in the third ventricle. However,
since there is a possibility that the cilia
may be confused with elongated microvilli
under the scanning electron microscope
(Bruni et al., '72), transmission electron
microscopic demonstration of cilia is considered to be definitive evidence of their
presence. Malinsky ('68) examined human
adult ependyma only from the lateral ventricle in one case and demonstrated the
presence of both cilia and microvilli in the
ependymal cells. The purpose of the present investigation was to examine the adult
human ependyma from the lateral, third
and fourth ventricles, including the aqueduct, for the presence of absence of cilia.
MATERIALS AND METHODS
Small pieces of ventricular wall with
ANAT. REC., 180: 547-550.
ependymal lining were collected from random sites of the lateral, third and fourth
ventricles and the aqueduct of five adult
human brains.a The brains were fixed in
formalin for 10 to 14 days before the
tissues for electron microscopy were obtained. The pieces were post-fixed in 4%
glutaraldehyde and then in 1% osmium
tetroxide and processed for electron microscopy. The tissue was flat-embedded to
maintain the proper orientation of the
ependymal surface. Thin sections were cut
with the ultramicrotome, stained with
uranyl acetate and lead citrate and examined under the electron microscope.
OBSERVATIONS
In all five brains, cilia were found in
many ependymal cells of all the ventricles
and the aqueduct. In some cells, only occasional cilia were present (fig. 1 ) while in
others, many cilia were observed (fig. 2).
The cilia in the human ependymal cells
were found to have structural similarity to
those present in many other cells (Fawcett,
'66). Thus, they appeared as tubular structures containing ten pairs of filaments
within them with characteristic (9 4-2)
pattern, i.e. nine pairs of peripherallyarranged filaments and a pair in the
center. Their association with the basal
body could be found in sections cut at appropriate planes.
Received April 1, '74. Accepted June 20, '74.
1 This investigation received financial support from
the World Health Organizatlon.
zThe specimens were obtained at autopsy with the
consent and signature of the next of kin.
547
548
SUBIMAL ROY, ASAO HIRANO AND HARRY M. ZIMMERMAN
Fig. 1 Ependymal cell with a small number of cilia ( C ) . Many microvilli ( M ) are also
present. Formalin-fixed postmortem material from the fourth ventricle. X 12,000.
In many cells, well preserved microvilli
were also found (fig. 3 ) . They, too, were
variable in number and were particularly
numerous in a small number of cells. They
appeared smaller and thinner than the
cilia, had a different internal structure and
occasionally showed branching. In many
cells, both microvilli and cilia could be
observed (fig. 1 ) .
DISCUSSION
Cilia have been demonstrated by electron microscopy in ventricular ependymal
cells of many adult animals like cat
(Klinkerfuss, '64) ; rat (Brightman and
Palay, '63; Rinne, '66; Hirano, Zimmerman and Levine, '66; Hirano and Zimmerman, '67; Westergaard, '70); rabbit (Tennyson and Pappas, '62); and monkey
(Knowles and Anand Kumar, '69 ) . In man
only, embryonic ependymal cells are generally believed to be ciliated. The presence
of cilia in the adult human ependymal
cells has not been adequately demonstrated. Although the scanning electron
microscopic study of Bruni et al. ('72) suggested the presence of cilia in the adult
human ependymal cells of the third ventricle, they pointed out that similar structures (cilia) may be interpreted by others
as microvilli. Transmission electron microscopic study of Malinsky ('68) based on
the examination of ependyma only from
the lateral ventricle in one human adult
brain did show the presence of cilia in the
ependymal cells. The present ultrastructural study also showed unequivocal presence of cilia in the adult human ependyma1 cells. Further, it appears from our
observations that the presence of cilia in
adult ependyma is quite widespread, being
present in all the ventricles of the brain
and the aqueduct. The ultrastructure of
cilia in the adult human ependyma
appears to be similar to those present in
ependyma of various adult animals
ADULT HUMAN EPENDYMA
549
Fig. 2 Ependymal cell with many cilia cut in longitudinal, transverse and oblique planes.
Note ( 9 2 ) arrangement of filaments i n transversely cut cilia (C). Basal bodies ( B ) are
also present. Formalin-fixed postmortem material from the third ventricle. x 23,500.
+
(Tennyson and Pappas, '62; Brightman
and Paley, '63; Klinkerfuss, '64; Fleischhauer, ' 7 2 ) , including their association
with the basal body.
ACKNOWLEDGMENT
The authors acknowledge the technical
help of Ms Ernestine Middleton.
LITERATURE CITED
Bloom, W., and D. W. Fawcett 1962 A Textbook of Histology. W. B. Saunders Co., Philadelphia, p. 239.
Brightman, M. W., and S. L. Palay 1963 The
fine structure of ependyma in the brain of the
rat. J. Cell Biol., 19: 4 1 5 4 3 9 .
Bruni, J. E., D. G. Monteniurro, R. E. Clattenburg and R. P. Singh 1972 A scanning electron microscopic study of the ependymal surface of the third ventricle of the rabbit, rat,
mouse and human brain. Anat. Rec., 174: 407420.
Fawcett, D. W. 1966 The Cell: Its Organelles
and Inclusion. W. B. Saunders Co., Philadelphia, pp. 423-430.
Fleischhauer, K. 1972 Ependyma and subependymal layer. In: The Structure and Function of Nervous Tissue. G . H. Bourne, ed. Academic Press, New York, pp. 1-46.
Hirano, A., H. M. Zimmerman and S. Levine
1966 The fine structure of cerebral fluid
accumulation: Reactions of ependyma to implantation of cryptococcal polysaccharide.
J. Path. Bact., 91: 149-155.
____
1967 Some new cytological observations of the normal rat ependymal cell. Anat.
Rec., 158: 293-302.
Klinkerfuss, G. H. 1964 An electron microscopic study of the ependyma and subependyma1 glia of the lateral ventricle of the cat.
Amer. J. Anat., 115: 71-100.
Knowles, F., and T. C. Anand Kumar
1969
Structural changes, related to reproduction, in
the hypothalamus and in the pars tuberalis.
Phil. Trans. Royal SOC.Lond. Biol. Series, B.,
256: 357-375.
550
SUBIMAL ROY, ASAO HIRANO AND HARRY M. ZIMMERMAN
Fig. 3 Ependymal cell showing many unusually long microvilli. Formalin-fixed postmortem material from the third ventricle. X 42,000.
Malinsky, J. 1968 Fine structure of ependyma in lateral ventricles of human brain. Acta
Univ. Olomuc. Fac. Med., 48: 65-72.
Ranson, S. W., and S. L. Clark 1963 The
Anatomy of the Nervous System. W. B.
Saunders Co., Philadelphia, pp. 123-124.
Rinne, U. K. 1966 Ultrastructure of the median
eminence of the rat. Z. Zellforsch, 74: 98-122.
Strong, 0. S., and A. Elwyn 1953 Human
Neuroanatomy. Williams and Wilkins, Baltimore, p. 59.
Tennyson, V. M., and G. D. Pappas 1962 An
electron microscopic study of ependymal cells
of the foetal, early post-natal and adult rabbit.
Z. Zellforsch, 56: 595-618.
Truex, R. C., and M. B. Carpenter 1970 Human
Neuroanatomy. Williams and Wilkins, Baltimore, pp. 159-160.
Westergaard, E. 1970 In: The lateral cerebral
ventricles and the ventricular walls. Odense,
Andelsbogtrykkeriet., pp. 73-91.
Worthington, W. C., and R. S. Cathcart 1963
Ependymal cilia: Distribution and activity in
the adult human brain. Science, 139: 221.
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