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The subdural neurothelium of the cranial meninges in man.

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The Subdural Neurothelium of the Cranial
Meninges in Man
Service de Neurologie d u C. H . U. de Purpan, Toulouse 31052, France
and Laboratoire d'Histologie de 1'U. E. R. de Mddecine, C. H . U.
CBte Nacre, C m n 14033, France
The neurothelium obtained from human biopsy specimens is a
very thin cellular layer located between the dura mater and the arachnoidea. It
is a pluri-stratified squamous layer which has some epithelial features (desmosomes and tonofilaments), and lacks connective tissue fibers in the extracellular
spaces. Usually there is increased nuclear and cytoplasmic density and enlarged
extracellular spaces from the deepest to the most superficial layer.
Since neurothelium is fragile and easily torn apart, it probably occupies the
position considered to be the subdural space.
Within the framework of a general study
of normal and pathological human meninges, we have already examined the corticopial junction (Rascol and Izard, '72),
arachnoid granulations (Rascol and Izard,
'69), and meningiomas (Rascol et al., '65).
The ultrastructural analysis of one layer
which is still poorly understood is to be presented here. This is the subdural neurothelium of the cranial meninges. Other
than work specific to the arachnoid granulations, very little electron microscopic investigation has been devoted to the human
menix (Thomas, '66; Klika, '67; Anderson,
'69; Lopes and Mair, '74). In man, as in
lower species, the subdural neurothelium,
described for the first time by Andres ('66,
'67) has not always been clearly differentiated from the dura mater and the arachnoidea. On those occasions when it has
been, the terms employed to describe it
have been both different and numerous. In
addition to ambiguities inherent in the
terminology, research into the human subdural neurothelium encounters difficulties
in obtaining the specimens from living subjects.
Specimens were taken during the course
of neurosurgical operations. Due to the
position of the neurothelium between the
dura mater and the arachnoidea, we examined pieces from the leptomeninx and
pieces from the dura mater, in as much as
ANAT. REC., 186. 4 2 9 4 3 6
it is not possible to obtain in one specimen
all of the meningeal layers together.
I n this manner, we obtained 35 specimens of the leptomeninx. Only eight of
them could be used for the ultrastructural
examination of the neurothelium. The preliminary examination of thick sections
showed that the other specimens were difficult to orientate or were invaded by erythrocytes. The eight specimens employed
came from six men and two women, from
17 to 60 years of age, who for the most
part underwent surgery for a deep cerebral
tumor or for a malformation of the atloidooccipital articulation. I n one particularly
propitious case, the patient, age 17, underwent a prefrontal lobotomy (and, therefore, was not suffering from any prior
organic lesion). In none of the cases was
there any clinical or biological meningeal
reaction. Frontal, temporal, and parietal
specimens, a5 well as specimens from the
posterior fossa were taken, and as far as
possible from the site of the lesion within
the surgical field.
In some of the patients we also removed
pieces of the dura mater. Most of these,
however, could not be used as the neurothelium was no longer adherent.
Specimens were first fixed in phosphate
buffered 2% glutaraldehyde or in Karnovsky's fixative ('65), and post-fixed in osmium tetroxide. They were embedded in
epon (Luft, '61). The ultra-thin sections
Received Dec. 10, '75. Accepted M a y 19, '76.
Fig. 1 Thick section. Arachnoidea ( a ) which is clear, loose and contains fasciculi of connective tissue fibers ( c ) . Boundary betwccn arachnoidea and neurothelium (+). Neurothelium ( n ) . There are a few clear nuclei and cytoplasmic lamellae in the deep layer. The superficial zone contains very basophilic cell prolongations and wide extracellular spaces. Zone
of surgical cleavage from the dura mater ( c l j . x 1,200.
were contrasted with uranyl acetate and
lead according to Reynolds ('63). In the
case of thick sections, staining with methylene blue-borax was employed (Richardson
et al., '60).
( A ) Thick sections
(fig. 1)
Thc subdural neurothelium is a pluristratified cellular layer. In the deep layeT,
most of the nuclei are vesicular and poorly
stained. The cytoplasm is generally clear.
The extracellular spaces are either slightly
or not at all dilated. The superfirial cells
are elongated and very basophilic. Their
nuclei are difficult to distinguish from the
surrounding cytoplasm. The cytoplasm
stretches out into long, spindly and sinuous
prolongations. Most of the extracellular
spaces are wide and irregular, and of a
rounded, oval or polygonal shape. No connective tissue fibers are noted either super-
ficially or in the depth of the tissue. The
neurothelium is easily distinguishable from
the underlying arachnoidea. The general
appearance of the arachnoidea is clearer
and less compact. and the nuclei are for
the most part vesicular. Above all, the
arachnoidea contains numerous fasciculi
of connective tissue fibers. On specimens
of leptonieninx, the superficial layer of the
neurothelium borders the zone of surgical
cleavage from the dura mater. An optically
void space, or a space filled with red cells
is present at the boundary. On a few rare
specimens of dura mater, we noted, along
the deeper aspect of this layer, some long,
spindly and sinuous cellular prolongations,
Fig. 2 Neurotheliurn. Deep zone. Vesicular nuclei, clear cytoplasms containing tonofilaments
( t j , Golgi vesicles, compact mitochondria, lipid
droplets and a few ergastoplasmic cisterns; short
cellular prolongations; desmosomes ( d ) , dilated
extracellular spaces ( e s ) giving a picture of intcrcellular spines (+). The superficial zone appears
i n the upper right curiicr. :< 11,200.
43 1
which appear as the tissue shreds of neurothelium torn by surgical manipulation,
are often vacuolated. Ergastoplasmic cisterns are present. A thick feltwork of tonofilaments gives the cell and its prolonga(B) EEectron microscopy
tions a dense appearance. The cells and
Under the conditions in which specimens the prolongations are joined by desmoare obtained, it is to be noted that the somes. The extracellular spaces are most
neurothelium presents some major varia- often quite extensive, of an unequal and
tions, since it can be made up of from two varied shape. Their content is optically
to eight cellular layers. It is exceptional void or finely granular (fig. 3). In a few
cases, they are only slightly dilated (fig. 4).
to observe only a single layer.
Further these extracellular spaces of the
Basically, two zones can be described :
a deeper zone, which rests on the arach- neurothelium never contain connective
noidea, and a superficial zone which is tissue fibers. The deep zone of the neurothelium is separated from the arachnoidea
contiguous to the dura mater.
by a typical basal lamina. This measures
( 1 ) Deep zone (figs. 2, 3 )
The nuclei are generally vesicular, clear some 300 A in thickness, and is to be
and oval. The euchromatin is clearly visi- found 450 A from the deepest layer of the
ble. The perinuclear cytoplasm is abundant neurothelium (fig. 3).
On specimens of leptomeninx cleaved
and the cellular prolongations relatively
short. The cytoplasm and its prolongations from the dura mater, the examination of
are clear, although tonofilaments are nu- the superficial boundary of the neurothemerous. The filamentous feltwork is actu- lium is impossible (fig. 3 ) . By contrast, in
ally less compact than the outer surface. a few specimens of dura mater. some charSome ergastoplasmic cisterns are to be ob- acteristic neurothelial prolongations conserved, as well as Golgi vesicles, mito- tiguous with the fibroblasts and connective
chondria most often with dense matrix, fibers of the dura mater are observed. The
some lipid droplets, some pinocytotic vesi- border between the dura mater and the
cles and, rarely, a centriole. The cellular neurothelium is sinuous. No basal lamina
junctions are sinuous. The extracellular is seen at this level (fig. 4).
Finally, we made an attempt to measure
spaces are most often narrow, in the order
thickness of the neurothelium. Such
of 200 to 300 A. The cells are joined to
each other by typical desmosomes. How- an evaluation is difficult due to the surgical
ever, the extracellular spaces between the cleavage. Rather than give determinations
desmosomes are sometimes dilated. The of the mean and standard deviations,
whole is thus indicative of a picture of an which would be imprecise under these
intercellular spine as in the stratum spi- conditions, the figure most frequently encountered in measurements of thickness
nosum of the epidermis (fig. 2).
(modal class) is 9 p.
( 2 ) Superficial zone (figs. 3, 4 )
The nuclei are very elongated. HeteroDISCUSSION
chromatin is usually abundant. The cytoThe
is a meningeal celluplasm are scanty around the nuclei and extend into long prolongations which are lar lamina located between the dura
lamellar, spindly and of irregular size. The niater and the arachnoidea. The term neuprolongations are arranged in several lay- rothelium was first employed by And&
ers and they are at times parallel with ('66, '67) in a study on the meninges of
each other (fig. 4). They may also appear the dog and cat. It was retained by Bohme
sinuous when the extracellular spaces are ( ' 7 3 ) with respect to the meninges of the
of an irregular size (fig. 3). Mitochondria cock.
A cellular layer which can be identified
with the one which we have just described
Fig. 3 Arachnoidea ( a ) . Basal lamina between
arachnoidea and neurotheliuni (+). Neurotheis designated in humans and in different
lium. The deep layer (DL) is compact and clear. animals by the term subdural mesothelium
In the superficial layer ( S L ) the extracellular
spaces (es) are wide and the cells are very elec- (Anderson, '69; Pease and Schultz, '58;
Tripathy, '73). It has also been called a
tron dense. Desmosomes ( d ) . Tonofilaments (L).
Cleavage zone from the dura mater (cl). X 21,000. subdural cellular layer (Akashi, ' 7 2 ) , a
dura-arachnoidal interface (Waggener and
Beggs, ’67j , a n intermediate cellular layer
(Himango and Low, ’71), or the external
layer of the arachnoidea (Lopez and Mair,
’74j . We think the designation of mesothelium should be rejected. Subdural neurotheIium is made up of several layers, not a
single layer, and does not have apical microvilli such as found on pleural or peritoneal mesothelium. The term subdural
neurothelium avoids ambiguity because it
is purely descriptive.
It is necessary to differentiate clearly
neurothelium from dura mater and arachnoidea. The ultrastructure of the dura
mater is typical and completely different;
there are abundant fibroblasts and collagenous fibers. However the boundary between
dura mater and neurothelium is difficult
to study since it is the zone of surgical
cleavage. It appears that the dura mater
and neurothelium are contiguous because
there is no basal lamina between them.
The difference between neurotheliurn and
arachnoidea is readily apparent due to the
presence of collagenous fibers or reticulin
i n the extracellular spaces of the arachnoidea. It is more difficult to determine the
exact limits of the deeper aspects of the
neurothelium. And&
(’67) considered
this boundary to be an “Interzellularspalt.”
Himango and Low (’71) state that it is a
“dense line of variable thickness.” The
latter investigators do not use the term
“basal lamina,” but they find such lamina
i n their preparations of certain arachnoidal trabeculae. In studies of arachnoid
granulations (Rascol and Izard, ’69), we
were not certain whether a basal lamina
bounds the deep surface of neurothelium.
At the present time, after a great number
of ultrastructural observations on cranial
meninges as a whole, the basal lamina
does appear to be the natural boundary of
neurothelium, which i t separates from cells
and connective tissue fibers of the arachnoidea. The subdural neurothelium of the
cranial meninges in m a n appears essentially like a stratified squamous epithelium.
The explanation for this epithelial strucFig. 4 Superficial layer of the neurothelium
( n ) . The extracellular spaces are slightly dilated.
Boundary without any basal lamina between neurothelium and dura mater (+). Dura mater containing connective tissue fibers and fibroblasts
( d m ) . x 17,500.
ture should be sought in the long standing
concept of the histogenesis of meninges
from ganglionic crests (Harvey and Burr,
It remains to be determined whether a
genuine subdural space exists in vivo
above, within, or below the neurothelium.
Although Tripathy (’73j, who studied the
meninges of the monkey, reports that the
subdural space actually does exist, most of
the investigators cited previously, who
studied animals and thus were able to
maintain cohesion of pachymeninx and
leptomeninx, believe that no such space
exists. They concluded that the subdural
neurothelium, or by whatever term it might
have been described, fills that region. The
discrepancy in opinion could be explained
by the fact that neurothelium, in spite of
the presence of tonofilaments and desmosomes, is fragile and is easily torn apart
in the course of histological manipulations.
Such a cleavage could create an artifactual
subdural space. Because of this fragility,
the neurothelium could also be torn apart
during hemorrhagic processes such as subdural hematomas. In man, conditions
under which specimens are taken, e.g.
surgical cleavage between dura mater and
leptomeninx preclude our judgment as to
the existence of a true subdural space.
However there is nothing at the present
time which will make it possible to confirm the existence of a genuine subdural
space. Phylogenetically, moreover, the observations indicating that dura mater,
arachnoidea, and pia mater in vertebrates
arise from a common primitive layer (Ariens-Kappers et al., ’60; Klika, ’68) suggest
the absence of a subdural space.
The authors wish to express their appreciation to all those who have so kindly
assisted in the preparation of this paper,
and especially: Pr. C. Bimes; Pr. J. Espagno, who kindly cooperated in taking the
surgical specimens; Mr. J. C. Cayrac, Mr.
A . Prat and Mrs. G . Barruk, whose technical support has been invaluable; and Miss
A. Deshayes, who patiently typed the manuscripts.
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cranial, meningeo, subdural, neurothelium, man
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