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The subarachnoid angleAn area of transition in peripheral nerve.

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The Subarachnoid Angle: An Area of
Transition in Peripheral Nerve '
JOHN S. McCABEa AND FRANK N. LOW
Department of Anatomy, University of North Dakota,
Grand Forks, North Dakota
ABSTRACT
The lateral limit of the subarachnoid space, where nerve roots enter
and leave, forms the subarachnoid angle. This is an important site of transition for
nerve sheaths. Here the perineurium of peripheral nerve leaves the surface of the
nerve and extends between the dura mater and the arachnoid. The perineurium is
therefore open-ended with respect to the subarachnoid space. The central perineurial
extension is histologically the same as perineurium in some areas but in others forms
a layer of hydrated cells without basement membranes. These lie in close apposition
with the outermost cells of the arachnoid membrane. At the subarachnoid angle the
arachnoid membrane may either reflect onto the root sheath or be attached to it by
punctate junctions. The root sheath covers the nerve roots as they pass through the
subarachnoid space. It is composed of loosely arranged cells bound by punctate junctions. Its intercellular spaces may contain connective tissue fibrils. A single basement
membrane separates it from the endoneurium. The histological structure in the region
of the subarachnoid angle is consistent with clinical evidence implicating the endoneurium of nerve trunks as a pathway for the transmission of infection from the
periphery to the central nervous system.
Peripheral nerves and the meninges of
the central nervous system are intimately
related in the region of the subarachnoid
space. The central termination of the perineurium, the middle sheath of peripheral
nerve, remains unclear despite a considerable body of investigative work devoted to
this area. Histological relationships are of
more than theoretical interest here because of clinical phenomena related to
nerve-borne infections. Initial peripheral
infection leads to asymptomatic latency
followed by central recrudescence. The peripheral nerve sheath most strongly implicated in this course of events is the
perineurium, which consists of a cylinder
of flattened cells surrounding the endoneurium and the nerve fibers. The perineurium
can be traced centrally along peripheral
nerve to the subarachnoid space. In this
general area the peripheral nerve sheaths
are known to undergo change. The epineurium becomes continuous with the dura
mater while the endoneurium continues
centrally with the nerve fibers. The fate of
the perineurium is uncertain. A study of
the electron microscopic histology of this
area should provide decisive evidence regarding the nature of the central termination of the perineurium.
ANAT.REC., 164: 15-34.
A brief historical account may serve to
clarify the more detailed aspects of the
problem. Key and Retzius (1876)first described the three sheaths of peripheral
nerve, designating them epineurium, perineurium and endoneurium. Both epineurium and endoneurium were believed to be
connective tissues, an interpretation that
prevails to the present day. Perineurium,
long considered to be composed of flattened
fibroblasts, has since been shown by electron microscopy to be a sheath of organized
flattened cells possessing basement membranes (Rohlich and Knoop, '61;Shanthaveerappa, Hope and Bourne, '63).Further
studies by Thomas ('63) and Burkel ('67)
revealed tight junctions joining perineurial
cells and confirmed the presence of basement membranes. These essentials of fine
structure in the perineurium were also observed by Gamble and Eames ('64) in human material. Burkel ('67), working on
small nerves of rats, reported that the perineurium terminated peripherally as an
open-ended sleeve. This open-endedness
Received Sept. 5, '68. Accepted Dec. 18, '68.
1 Supported by HE 09041, United States Public
Health Service.
National Defense Graduate Fellow. September
1966 to August, 1968. This work was done in partial
ful6llment of the requirements for the degree of
Master of Science.
15
16
JOHN S. McCABE AND FRANK N. LOW
also occurred at the entry of blood vessels
and at the points where reticular fibers
pierced the perineurium. He suggested that
the communications thus effected between
the epineurial and endoneurial portions of
the tissue space might be significant in the
dissemination of toxins from the periphery
to the subarachnoid space. These observations correlated well with the fact that
nerve trunks are known to act as a conduit
for the transmission of infection (Wright,
'53) and with Kmjevic's ('54) physiological studies of sheathed and desheathed
nerves that recognized the perineurium as
the diffusion barrier of peripheral nerve.
The central portion of the perineurium
has been studied by electron microscopy.
Benke and Rohlich ('63), using young rats,
reported that perineurium and arachnoid
membrane fused and became continuous
near the subarachnoid angle, the lateralmost extent of the subarachnoid space (Elman, '23). Differences were noted between
the dorsal and ventral surfaces of the dorsal root. The continuities of the various
histological layers and their relationship to
known structures in the area were unclear.
Gamble ('64) studied peripheral nerve
(sural) and dorsal nerve roots (sacral) in
the rat. He reported that the pial sheath
(root sheath) of the latter possessed as
many as four lamellae of cells, each with
basement membranes, as it passed through
the subarachnoid space. He considered
it indistinguishable from perineurium.
His observations therefore implied uninterrupted continuation of the perineurium
along the peripheral nerve to the central
nervous system. Andres ('67), working on
cats and dogs, described a layer of cells
between the arachnoid membrane and the
dura mater. He named this layer the 'neurothelium." It was interpreted to be a direct
central extension of the perineurium which
turned away from the nerve fibers and their
endoneurium at the subarachnoid angle.
He recognized both the presence of basement membranes on perineurium and their
absence on neurothelium. His figure 13, an
excellent reconstruction of the area investigated, is so drawn as to suggest that the
change took place at the subarachnoid angle. Micrographs supporting the structural
situation depicted at this point were
not included. More recently Lieberman
('68) studied the peripheral nerve sheaths
around the mammalian nodose ganglion
and reported morphological findings that
were in essential agreement with previous
studies in h e structure.
The cytological identity of the perineurium itself has been the subject of some
speculation. Identification of perineurial
cells as fibroblasts is argued against by the
presence of basement membranes (sometimes called boundary membranes because
of their relationship to the tissue space)
which are uniformly associated with nonconnective tissue cells (Low, '61, '64).
The uncertain and conflicting evidence
cited above suggests that the central termination of the perineurium might be
examined more closely with profit, with
emphasis on the subarachnoid angle and
closely associated areas. This paper reports
an investigation of this area in the rat.
MATERIALS AND METHODS
Seventeen adult Sprague-Dawley rats of
both sexes and varying ages were anesthetized with chloral hydrate, 0.35 gm per kilogram of body weight, and perfused by the
method of Rosen, Basom and Gunderson
('67). A paraformaldehyde-glutaraldehyde
mixture buffered at pH 7.4 with sodium
cacodylate was the perfusate (Karnovsky,
'65). In the last seven animals 0.1% aqueous procaine hydrochloride was added to
the washout solution to prevent peripheral
vasoconstriction (Forssmann et al., '67).
The lower cervical and upper thoracic spinal column, containing undisturbed nervous tissue in situ, was dissected free and
immersed in a 3.2% aqueous solution of
sodium cacodylate. All subsequent dissections were performed in this fluid. The dorsal surface of the spinal cord was exposed
by laminectomy. Ventrally the cord was
exposed by longitudinal section of the bodies of the vertebrae with fine pointed scissors. The dura was then cut longitudinally
in the midline on both dorsal and ventral
surfaces. It was retracted laterally and the
dorsal and ventral roots were cut close to
their attachment with the spinal cord.
After removal of the cord the entire preparation separated readily into two longitudinal halves with roots and associated
meninges intact. To obtain intact preparations of the roots leading to each spinal
nerve, the dura was cut vertically from its
dorsal to its ventral extent. This was done
SUBARACHNOID ANGLE
some distance cephalic and caudal to the
separate exits of the dorsal and ventral
roots from the subarachnoid space. The
dura was then freed from its attachments
to bone by careful probing. At this stage it
was possible to insert iridectomy scissors
into the medial aspect of the intervertebral
foramen far enough to cut the trunk lateral
to the spinal ganglion. The resultant dissection contained roots, associated meninges
and the spinal ganglion in a single piece
of tissue.
Light microscopy. It was discovered
that the myelin of tissue perfused with
buffered aldehydes could be preserved for
light microscopy by weak post-osmication
without interfering with the response of
the tissue to chromatic stains. Therefore,
tissues intended for light microscopy were
post-fhed in 0.2% OsOr buffered with
0.05N sodium cacodylate for three hours
immediately following dissection. Subsequent procedures followed the technique of
Rosen, Basom and Gunderson (’67). Unusual features included high melting point
paraffin (60” to 62”C), specially sharpened
steel knives and minor modifications of
chromatic staining approaches. Best results
were obtained with Masson’s trichrome
method in which aniline blue, Heidenhain’s hematoxylin and Ponceau-orange
were used. In general it was found expedient to reduce exposure time to the darker
stains because of the light brown color of
the osmicated tissue.
Electron microscopy. Electron microscopic preparations were post-fixed in 2%
OsOl buffered with 0.05 N sodium cacodylate for one hour. Dehydration and embedding were conventional. Epon 812 in 6:4
proportion was used (Luft, ’61). Each
specimen was sketched and then carefully
oriented in the Epon. Thick (one micron)
sections were stained with toluidine blue
for orientation. Nearby thin sections were
stained with both uranyl acetate (Greenlee,
Ross and Hartman, ’66) and lead citrate
(Reynolds, ’63). They were viewed in a
Philips EM-200 electron microscope.
OBSERVATIONS
The nomenclature used to describe peripheral nerve sheaths is taken from the
descriptions of Key and Retzius (1876)
with refinements suited to fine structure as
used by Burke1 (’67). Epineurium is the
17
outermost sheath; the connective tissue
that surrounds the entire nerve. Internal
to this is the multilayered cellular sheath,
the perineurium. Endoneurium is the connective tissue enclosed by the perineurium.
This pattern, although generally accepted
for peripheral nerve, is difficult to apply to
all areas encountered in this study. The
covering of spinal roots during their course
through the subarachnoid space has been
designated by many terms (pia-arachnoid,
pial sheath, rootlet arachnoid, root sheath,
etc.). During this investigation it became
clear that this covering had unique characteristics, especially on the surface bordering the endoneurium. In this paper this
structure is called the “root sheath.”
Figure one represents the region encompassed by this study. The standard pattern
for peripheral nerve sheaths prevails in the
area of the spinal ganglion. Between the
spinal ganglion and the nerve root in the
subarachnoid space radical differences in
the morphology of these sheaths exist, the
principal change occurring at the subarachnoid angle. Figures 2 to 17 are micrographs
flustrating these morphologic characteristics. The specific location of each field is
indicated on figure one.
Area of spinal gangZion. The nerve
sheaths of this area are typical of peripheral nerve. Spinal ganglion cells are enclosed by capsule (Schwann) cells and
endoneurium in the same manner as peripheral nerve fibers elsewhere. Perineurium and endoneurium occupy their CUStomary relative position. The epineurium
is composed of a dense arrangement of
unit collagen fibrils and fibroblasts (fig. 2).
It is somewhat heavier than the epineurium of most peripheral nerves because
here it represents an area of transition
approaching the thicker dura mater. The
perineurium is a highly organized, multilayered sheath of flattened cells (figs. 2,3,
4). The number of layers is variable and
there are abrupt terminations of the inner
layers (fig. 3). Abundant connective tissues run between each layer. Basement
membranes separate the perineurial sheath
from the epineurial and endoneurial portions of the tissue space and from most of
the intervening connective tissues (figs. 2,
3,4). However, between two closely approximated perineurial layers, basement
membranes may be incomplete (fig. 4).
18
JOHN S. McCABE AND FRANK N. LOW
Fig. 1 Spinal cord and nerue roots. The numbers indicate the location of the fields illustrated
in figures two to 19. T h e plane of section of figures two, three, 5 to 12, 18 and 19 is the same as
in the drawing above. Figures 4 and 13 to 17 are cut in a plane at cross-section to the nerve fibers.
The detailed orientation of each micrograph is given with its individual caption. The spinal ganglion area is represented by figures two to 4, the subarachnoid angle by figures 5 to 8, the duraarachnoid complex by figures 9 to 12 and the root sheath by figures 13 to 17. Figures 18 and 19 are
reconstruction drawings summarizing the structural features illustrated in the micrographs of figures two to 17.
Outer layers of the perineurium may possess thickened basement membranes (fig.
3). The endoneurium around the ganglion
cells is very thin (fig. 2). Otherwise it has
no special features. The arrangements of
the nerve sheaths around the ventral root
at the level of the spinal ganglion cannot
be distinguished from those of peripheral
nerve elsewhere (fig. 4).
Subarachnoid angle. The subarachnoid
angle marks the lateral limit of the subarachnoid space (Elman, '23). The arachnoid membrane forms a relationship with
each emerging root in either of two ways.
The cell bordering on the subarachnoid
space may reflect back onto the surface of
the root (figs. 5,6,7)or, it may attach to
the root sheath by means of punctate junc-
tions marking the subarachnoid angle (fig.
8). At the subarachnoid angle the outermost nerve sheath, the epineurium, is continuous with the dura mater. The perineurium of the dorsal root usually maintains
its position deep to the epineurium-dura
continuum, passing along the outer wall of
the subarachnoid space between the dura
and the arachnoid membrane (fig. 7). It is
clear that most of the perineurial layers
follow this course. The fate of the innermost layers is uncertain because of the extreme irregularity of these tissues at the
subarachnoid angle. The situation at the
subarachnoid angle of the ventral root
tends to differ. The cells adjacent to the
arachnoid membrane are of low density
suggesting that they are strongly hydrated
19
SUBARACHNOID ANGLE
(figs. 8 , 9 ) . They are apparently continuous with the perineurium near the subarachnoid angle. These hydrated cells can
be traced for some distance along the outer
wall of the subarachnoid space (fig. 9).
They are in close apposition to each other
and to the outermost cell layer of the arachnoid membrane. Along these cells, the
greater part of their surfaces are devoid of
basement membranes. In contrast, perineurial cells near the subarachnoid angle
of the dorsal root possess typical investment by basement membranes.
Outer wall of subarachnoid space. The
outer wall of the subarachnoid space is
composed chiefly of dura mater and arachnoid membrane. There may be a variable
number of perineurial layers between them
(fig. lo), depending on location. The dura
consists of dense, regularly arranged connective tissue without notable features.
Near the subarachnoid angle of the dorsal
root, the perineurium is essentially the
same as that covering the spinal ganglion
(fig. 10). However, the number of layers
is reduced. As the midline of the body is
approached from this location, the number
of layers of perineurium diminishes gradually. Figure 11 illustrates the arachnoiddura complex at a point 170 p from the
dorsal subarachnoid angle. No perineurium
is present. Near the ventral subarachnoid
angle, a variable number of hydrated cells
are interposed between the dura and the
arachnoid membrane (fig. 12). Although
they are continuous with the perineurium,
their morphologic features are distinctly
different.
The arachnoid membrane is composed
of loosely arranged cells with dense cytoplasm (figs. 10, 11, 12). Cytoplasmic lacunae contain bundles of unit collagen fibrils
that constitute reticular fibers (figs. 1 0 , l l ) .
Some lacunae are empty and elsewhere
fibrous material is distributed throughout
the intercellular spaces (fig. 12). Arachnoid trabeculae with similar structural patterns occur nearby in the subarachnoid
space (fig. 10).
Spinal neme roots. The root sheaths are
composed of loosely arranged cells closely
resembling the arachnoid membrane (figs.
9,14,15). The arrangement of these cells
varies with the region of the root. In the
distal half the root sheath is indistinguishable from the arachnoid membrane (figs.
14, 15). The proximal half of the root
sheath is characterized by cells that are
more flattened with a reduction in the number of lacunae filled with unit collagen
fibrils (figs. 16,17). The flattened cells are
loosely arranged but are often joined by
punctate junctions (fig. 16). A constant
feature of the root sheath is the presence
of a basement membrane on the basal surface of the deepest cell of the sheath (figs.
9, 13, 14, 15, 16, 17). Although this basement membrane maintains the relationship
with the basal cell of the root sheath, it
occasionally penetrates the endoneurial
portion of the tissue space to enclose unit
collagen fibrils (fig. 17). The basal cell
cytoplasm of the root sheath is sometimes
highly vesicular (fig. 13). The endoneurial
portion of the tissue space contains connective tissues and is indistinguishable from
the endoneurial tissue space of peripheral
nerve.
DISCUSSION
The observations reported in this study
emphasize the transition of peripheral
nerve sheaths that occurs at the subarachnoid angle. Three distinct histological patterns are found in adjoining regions and
are significant with regard to the central
termination of the perineurium. The structural situations observed during this study
are schematically summarized in figures 18
and 19. In the area of the spinal ganglion
typical perineurium is found. In the duraarachnoid complex a layer of hydrated
cells, or layers of perineurium, or a combination of the two exists between the dura
mater and the arachnoid membrane. The
hydrated cells, although very different in
appearance, represent a continuation of
the perineurium. The root sheath covers
the endoneurium and the nerve fibers in
their pathway through the subarachnoid
space but is histologically distinct from
perineurium. It is loosely constructed, with
generous, often empty intercellular spaces
and punctate intercellular junctions. The
only coherent structural barrier between
endoneurium and subarachnoid space is a
basement membrane. The peculiar histology of this area has important implications
regarding the role of the perineurial sheath
in the transmission of infections from the
periphery to the subarachnoid space, as explained below.
20
JOHN S. McCABE A N D FRANK N. LOW
The perineurium has been established
as the diffusion barrier around peripheral
nerve (Krnjevic, ’54; Waggener, Bunn and
Beggs, ’65; Olsson, ’66; Luft, ’66). Burke1
(’67) has demonstrated that the perineurial sleeves are open-ended peripherally.
Our observations are in agreement with
those of Andres (’67),who pointed out that
the perineurium extended centrally only as
far as the subarachnoid space. At the subarachnoid angle it left the neural tissue,
coming to lie between the dura mater and
the arachnoid membrane. We have further
demonstrated the loose structure of the
root sheath, an arrangement not suggesting a diffusion barrier. The central extent
of the perineurium may therefore be considered to be “open-ended with respect
both to the subarachnoid space and to the
central nervous system in general.
The observations made during this study
indicate some differences between the central relationships of the nerve sheaths of
the dorsal and ventral roots although considerable variation seems to exist. In the
dorsal root the perineurium can be identified at the subarachnoid angle between the
dura-epineurium and the arachnoid membrane (fig. 18). It possesses basement
membranes and has a typical laminar appearance. The perineurial cell layers terminate proximally within 170 LI from the
subarachnoid angle. In the ventral root the
hydrated cells are continuous with the perineurium and occupy a position similar to
that of the perineurial extension in the
dorsal root (fig. 19). These cells are devoid
of basement membranes, do not have the
laminar appearance of perineurium and
are very closely applied to the outermost
cell layer of the arachnoid membrane. Although the hydrated cells may constitute
a diffusion barrier comparable to that of
perineurium, the layer in this specific situation is effective between the dura and the
subarachnoid space rather than between
endoneurium and epineurium. It follows
that the differences between dorsal and
ventral roots are not significant with reference to the function of the perineurium
as a diffusion barrier. It is effectively “opene n d e d in either case since the endoneurium of both dorsal and ventral roots is,
in the course of their passage through the
subarachnoid space, separated from the
cerebrospinal fluid only by the root sheath.
The unique histology of the root sheath,
recognized many years ago by Nageotte
(’02), now takes on added significance in
fine structure. Its basal layer of cells in the
rat is consistently separated from the endoneurial portion of the tissue space by a
continuous basement membrane and the
remaining cellular layers are loosely arranged. Cellular attachments seem to be
limited to punctate junctions and the voluminous intercellular spaces are occupied in
many places by fibrous connective tissues.
Although it is unlikely that the root sheath
could function as a diffusion barrier, the
presence of the basement membrane suggests continuity with the perineurium.
Gamble’s (’64) suggestion that the root
sheath is a central extension of the perineurium tends to support this but Andres’
(’67) sketch of the root sheath shows no
basement membrane at all. In the present
study continuity between perineurium and
root sheath was extremely difficult to determine and then involved only the deepest
layers of the perineurium (fig. 19). More
often, continuity of the cellular layers of
the root sheath was interrupted at the subarachnoid angle as represened in figure 18.
Whichever may be the case the root sheath
interposes only one coherent structure between the endoneurium and the subarachnoid space, its own basement membrane.
Since basement membranes are known to
be macromolecular filters (Majno, ‘65, and
others) permeability of the root sheath is
clearly indicated by its structural makeup.
The observations made during this study
stress the existence of a potential pathway
between the endoneurium of peripheral
nerve and the subarachnoid space. As well
as suggesting a morphological pathway for
the transmission of neural infections, the
fine structure of the root sheath and the
subarachnoid angle may also provide information about the passage of cerebrospinal fluid along peripheral nerves. For
nearly a century, investigators attempted
to resolve this latter question by using subarachnoid or intraneural dye injections to
determine continuity (or discontinuity) between the endoneurial and subarachnoid
spaces. This body of work has been concisely reviewed by Benke and Rohlich (‘63).
Two essentially conflicting opinions arose;
one group contending that there was no
communication and the other favoring a
SUBARACHNOID ANGLE
limited communication between the endoneurial and subarachnoid spaces. Although
the question is stdl unresolved, most of
these investigators agreed that the critical
site was the subarachnoid angle. The observations made in the course of the present work reveal a variable situation answerable to either opinion. In some areas a
barrier exists (fig. 18) but elsewhere structural features provide for slow seepage
from one area to another (fig. 19). As suggested by Benke and Rohlich ('63) hydrostatic pressure may be a significant determinant of the outcome. It appears that fine
structure in the subarachnoid angle and
surrounding areas stands in good agreement with a large body of evidence drawn
from experimental and clinical sources.
ACKNOWLEDGMENTS
Thanks are extended to Dr. Christopher
J. Hamre and Dr. Theodore Snook for help
and advice during the preparation of the
paper. We are also indebted to Carol Soutor
for thin sectioning and to Elvina Rolette,
who typed the manuscript.
LITERATURE CITED
Andres, K. H. 1967 Uber die Feinstruktur der
Arachnoidea und Dura mater von Mammalia.
Z. Zellforsch., 79: 272-295.
Benke, B., and P. Rohlich 1963 Elektronenmikroskopische Untersuchungen a n den Hiillen
der Riickenmarkswurzeln, I. Hintere Wurzel.
J. Hirnforsch., 7: 87-93.
Burkel, W. 1967 The histological fine structure
of perineurium. Anat. Rec., 158: 177-189.
Elman, R. 1923 Spinal arachnoid granulations
with especial reference to the cerebrospinal
fluid. Johns Hopkins Hosp. Bull., 34: 99-104.
Forssmann, W. G., G. Siegrist, L. Orci, L. Gerardier, R. Pictet and C. Rouiller 1967 Fixation
par perfusion pour la rnicroscopie Blectronique.
Essai de g6nhralisation. J. Microscopie, 6: 279304.
Gamble, H. J. 1964 Comparative electronmicroscopic observations on the connective tissues of
a peripheral nerve and a spinal nerve root i n
the rat. J. Anat. (Lond.), 98: 17-25.
Gamble, H.J., and R. A. Eames 1964 A n electron microscope study of the connective tissues
of human peripheral nerve. J. Anat. (Lond.),
98: 655-663.
Greenlee, T. K., R. Ross and J. L. Hartman 1966
The fine structure of elastic fibers. J. Cell Biol.,
30: 59-71.
21
Karnovsky, M. J. 1965 A formaldehyde-glutaraldehyde fixative of high osmolality for use in
electron microscopy. J. Cell Biol., 27: 137A138A.
Key, A., and G. Retzius 1876 Studien in der
Anatomie des Nervensystems und des Bindegewebes. Samson and Wallin, Stockholm.
Kmjevic, K. 1954 The connective tissue of the
frog sciatic nerve. Quart. J. exp. Physiol., 39:
55-72.
Lieberman, A. R. 1968 The connective tissue
elements of the mammalian nodose ganglion.
Z. Zellforsch., 89: 95-111.
Low, F. N. 1961 The extracellular portion of
the human blood-air barrier and its relation to
tissue space. Anat. Rec., 139: 105124.
1964 A boundary membrane concept of
ultrastructure applicable to the total organism.
Proc. Third European Regional Conf. on Electron Microscopy. Czech. Acad. Sci., Prague.
rr: 115-116.
Luft, J. H: 1961 Improvements in epoxy resin
embedding methods. J. Biophys. Biochem. Cytol., 9: 409-414.
1966 Fine structure of nerve and muscle cell membrane permeability to Ruthenium
red. Anat. Rec., 154: 37S-380.
Majno, G. 1965 Ultrastructure of the vascular
membrane. Hardbook of Physiology, Section 2,
Circulation, vol. 111,
Nageotte, J. 1902 Note sur les formations cavitaires par p e r i n k i t e dans les nerfs radiculaires. C. R. SOC.Biol. Paris, 54: 1443-1445.
Olsson, Y. 1966 Studies on vascular permeability in peripheral nerves. 1. Distribution of circulating fluorescent serum albumin in normal,
crushed and sectioned rat sciatic nerve. Acta
neuropath., 7: 1-15.
Reynolds, E. A. 1963 The use of lead citrate at
high pH as a n electron-opaque stain in electron
microscopy. J. Cell Biol., 17: 208-211.
Rijhlich, P., and A. Knoop 1961 Elektronenmikroskopische Untersuchungen a n den Hiillen
des N. ischiadicus der Ratte. Z. Zellforsch., 53;
299-312.
Rosen, W. C., C. R. Basom and L. L. Gunderson
1967 A technique for the light microscopy of
tissues fixed for fine structure, Anat. Rec., 158:
223-238.
Shanthaveerappa, T. R., J. Hope and G. H. Bourne
1963 Electron microscopic demonstration of
the perineurial epithelium in rat peripheral
nerve. Acta anat., 52: 193-201.
Thomas, P. K. 1963 The connective tissues of
peripheral nerve: an electron microscopic study.
J. Anat. (Lond.), 97: 35-44.
Waggener, J. D., S. M. Bunn and J. Beggs 1965
The diffusion of ferritin within the peripheral
nerve sheath: An electron-microscopic study.
J. Neuropath. exp. Neurol., 24: 430-443.
Wright, G. P. 1953 Nerve trunks as pathways
in infection. Proc. Roy. SOC.Med., 46: 319-330.
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Abbreviations
A, arachnoid membrane
AT, arachnoid trabecula
BM, basement membrane
C, capsule
D, duramater
E, endoneurium
EP, epineurium
F, fibroblast
G, ganglion cell
H, hydrated cell
L, lacuna
P, perineurium
R, rootsheath
S, subarachnoid angle
SG, spinal ganglion
SS, subarachnoid space
PLATE 1
EXPLANATION OF FIGURES
All sections on this plate were stained with uranyl acetate and lead
citrate.
Edge of spinal ganglion. This section passes through the tissue at a
plane perpendicular to the perineurial cells. The ganglion cell (G)is
at lower left. A capsule cell (C) lies between the ganglion cell and
the endoneurium. The endoneurial portion of the tissue space ( E )
is scanty. Five layers of perineurium ( P ) have connective tissues between them. Epineurium (EP) is composed principally of unit collagen fibrils and fibroblasts (F). The outer edge of the epineurium,
at upper right, represents the line along which the specimen was dissected free. x 4300.
Perineul.ium adjacent to spinal ganglion. The plane of this section
passes perpendicular to the perineurial cells. Six layers of perineurium
are present. Sometimes adjacent layers are traceable to a single cell.
One of the innermost layers terminates in the plane of section (arrow).
The basement membranes (BM) of the outermost perineurial layers
are thickened, some reaching one-third micron. Connective tissues lie
between each layer. x 22,000.
Nerve sheath of ventral root tn spinal ganglion area. In this section
the ventral root and its coverings are cut in cross-section. The epineurium (EP) is composed of connective tissues. The perineurium
( P ) has six cell layers. Basement membranes are lacking between the
two closely approximated inner layers of the perineurium. Elsewhere
the investment is nearly complete. The fibroblast (F) in the endoneurial portion of the tissue space (E) lacks basement membranes.
A small portion of a myelin sheath is present in each lower corner.
X 15,000.
22
SUBARACHNOID ANGLE
John S. McCabe and Frank N. Low
PLATE 1
23
PLATE 2
EXPLANATION OF FIGURES
5 Spinal ganglion (SG) and subarachnoid angle ( S ) . This section passes longitudinally
through the dorsal root at the medial extent of the spinal ganglion. The subarachnoid
angle ( S ) represents the lateral limit of the subarachnoid space. The epineurium (EP)
below is continuous with the dura mater ( D ) above. The nerve fibers a t right belong to
the dorsal root. Epoxy embedment stained with toluidine blue. x 240.
6 Subarachnoid angle (S) and subarachnoid space (SS). The plane of this section is similar to that of figure 5 but passes through the ventral root. This “turnback” area illustrates the point where the arachnoid membrane reflects from the dura mater ( D ) onto
the surface of the ventral root. Stained with Masson’s trichrome. x 770.
7 Subarachnoid angle (S) of dorsal root.
This section passes longitudinally through the
dorsal root a t the point where the perineurium leaves the nerve fibers. The arachnoid
membrane (A) reflects back on the surface of the root which is out of the field below.
The multilayered perineurium (P) lies between the epineurium (EP) above and the
arachnoid membrane below (A). It extends off the field to the left between the dura
and the arachnoid membrane. The complex arrangements of the arachnoid cells make
continuities in the “turnback” area difficult to follow i n a single section. Stained with
uranyl acetate and lead citrate. X 5600.
24
8
Subarachnoid angle (S) of ventral root. The longitudinally sectioned fibers of the ventral root are out of the field to the left. The innermost cell of the arachnoid membrane
( A ) is joined to the outermost cell of the root sheath (R) by punctate junctions (arrow).
This area marks the lateral limit of the subarachnoid space. Hydrated cells ( H ) lie between the epineurium to the right (not shown) and the arachnoid membrane (A). T h e
plasmalemmae of the innermost hydrated cell and the outermost cell of the arachnoid
membrane are very closely applied to each other (see also figs. 9, 12). The vertically
aligned cell at extreme left represents the innermost layer of the root sheath and is separated from the endoneurium by a basement membrane. The situation illustrated a t this
point, although representing the subarachnoid angle, does not constitute a “turnback”
in the sense of laminar continuities of cell layers. Stained with uranyl acetate and lead
citrate. x 17,000.
9
Subarachnoid space (SS) near subarachnoid angle of ventral root. The longitudinally
sectioned fibers of the ventral root are out of the field below. The subarachnoid space
( S S ) is bounded externally (above) by two layers of cells of the arachnoid membrane
(A) and four layers of hydrated cells (H). Covering the ventral root below, the root
sheath ( R ) is composed of four layers of cells with dense cytoplasm. The innermost
layer has a basement membrane (arrow) interposed between it and the endoneurium
( E ) . Stained with uranyl acetate and lead citrate. X 14,000.
SUBARACHNOID ANGLE
PLATE 2
John S. McCabe and Frank N. Low
25
PLATE 3
EXPLANATION OF FIGURES
All sections were stained with uranyl acetate and lead citrate.
10 Outer wall of subarachnoid space. This field, which transects the dura, perineurium and arachnoid membrane, is near the subarachnoid angle of the dorsal root.
Multilayered perineurium ( P ) lies between the dura mater ( D ) and the arachnoid
membrane (A). An arachnoid trabecula (AT) lies in the subarachnoid space (SS)
i n the lower part of the field. X 5000.
11
Outer wall of subarachnoid space. This field is about 1 7 0 p from the subarachnoid angle of the dorsal root and passes perpendicular to the thickness of the dura
and arachnoid membrane. No perineurium lies between the dura mater (D) and
the arachnoid membrane (A). The cells of the latter enclose lacunae ( L ) containing unit collagen fibrils. Similar lacunae are also found in arachnoid trabeculae (figs. 10,15). X 8900.
12 Outer wall of subarachnoid space. This field is near the subarachnoid angle of
the ventral root, the section passing perpendicular to the thickness of the dura.
Hydrated cells ( H ) lie between the dura mater ( D ) and the cells of the arachnoid
membrane (A). Intercellular spaces in the arachnoid membrane are sometimes
occupied by fibrous material. A small portion of the subarachnoid space is visible
at lower left. x 20,000.
13 Root sheath of ventral mot. This is a cross-section of the ventral root. The basal
cell of the root sheath has a basement membrane (arrows) separating it from the
endoneurial portion of the tissue space (E). The cytoplasm of the basal cell contains many vesicles that are continuous with flattened cisterns. A vertical strip of
the subarachnoid space lies at extreme right. X 19,000.
26
SUBARACHNOID ANGLE
John S. McCabe and Frank N. Low
PLATE 3
27
PLATE 4
EXPLANATION O F FIGURES
Both sections were stained with uranyl acetate and lead citrate.
14 Distal portion of dorsal root. This section of the dorsal root is cut in
cross-section. The root sheath is composed of loosely arranged cells
enclosing lacunae ( L ) . Unit collagen fibrils and fibrous material are
randomly distributed throughout them. A n extremely attenuated layer
of dark cytoplasm borders the subarachnoid space ( S S ) . X 6000.
15
28
Distal portion of dorsal root. The root sheath ( R ) is cut i n crosssection. It extends from the subarachnoid space ( S S ) above to the
endoneurium ( E ) below; is similar to the arachnoid membrane. A n
arachnoid trabecula (AT) lies i n the subarachnoid space. Compare
with figures 10 and 11. x 20,000.
SUBARACHNOID ANGLE
PLATE 4
John S. McCabe and Frank N. Low
29
PLATE 5
E X P L A N A T I O N OF FIGURES
Both sections were stained with uranyl acetate and lead citrate. Both
fields are cross-sections of the dorsal root.
16
Proximal portion of dorsal root. Flattened, loosely arranged cells
form the root sheath ( R ) . These cells are joined by punctate junctions (arrows). The basal cell of the root sheath is separated by a
basement membrane from the endoneurial portion of the tissue space
( E ) . X 26,000.
of dorsal root. The basal cell of the root sheath ( R )
has a basement membrane (arrows) that extends into the endoneurial
portion of the tissue space ( E ) and encloses unit collagen fibrils.
x 23,000.
17 Proximal portion
30
SUBARACHNOID ANGLE
PLATE 5
John S. McCabe and Frank N. Low
31
PLATE 6
EXPLANATION O F FIGURES
Both drawings represent cross-sections of the area surrounding the subarachnoid angle.
Their positions relative to the spinal cord and the meninges are indicated on figure one. Orientation is conventional with dorsal above and ventral below. The central nervous system
and the midline of the body are to the left. The more lateral structures including the spinal
ganglion are to the right.
Each figure was sketched from individual micrographs or montages and represents a chosen
composite of structural relationships demonstrable i n the designated area. Relative dimensions are presented i n proper scale at a magnification of about 5000 diameters. Variations i n
the composition of the perineurium, arachnoid membrane and root sheath are so common in
the area of the subarachnoid angle that the situation represented in the dorsal root might
well be encountered i n the ventral root, and vice versa. It follows that the morphologic features represented, while of common occurrence in the root in question, are not specific for it.
However, the structural situations depicted in these two figures are valid representations of
the histology observed in areas close to the subarachnoid angle.
18 Subarachnoid angle of dorsal root. The dura mater ( D ) is a n uninterrupted continuation of the epineurium (EP). The fibroblast above (F) marks the outer edge of the
dura mater where it was separated from outlying connective tissue during dissection.
A large myelinated fiber courses diagonally across the lower part of the field, running
within the endoneurium ( E ) . The subarachnoid space (SS) is bounded dorsally by the
arachnoid membrane ( A ) which becomes continuous with the root sheath ( R ) a t the
subarachnoid angle ( S ) . A single cell facing on the subarachnoid space (SS) passes
from the arachnoid ( A ) to the root sheath ( R ) by means of a “turnback” at the subarachnoid angle. The perineurium ( P ) extends centrally to occupy a position between
the arachnoid membrane (A) and the dura mater (D). It diminishes along this course
until, at 1 7 0 p from the subarachnoid angle, it is absent (fig. 11). Continuity between
the deeper layers of the perineurium ( P ) and the root sheath ( R ) cannot be established
due to the presence of “rounded-up” cells of unknown identity. It is usually very difficult
to trace the continuity of cell layers in this area. The obliquely sectioned small myelinated fiber deep to the perineurium o n the right is a common occurrence. Lacunae
formed by the cells of the perineurium, arachnoid membrane and root sheath enclose
varying amounts of extracellular connective tissues. Arachnoid trabeculae (AT), consisting of fibrous connective tissues wrapped in cells of the arachnoid membrane, are
common in this area.
19 Subarachnoid angle of ventral root. The epineurium (E)of the nerve root a t upper left
contains a large myelinated fiber. Below, the epineurium (EP) becomes continuous with
the dura mater ( D ) opposite the subarachnoid angle ( S ) . Fibroblasts ( F ) are associated
with this layer, especially near its cut edge. The multilayered perineurium (P) enters
the field a t right. Its deeper layers appear to contribute to the root sheath but, i n many
sections examined, definite continuity was not demonstrable. Most of the layers of the
perineurium clearly pass ventral to the subarachnoid angle and to the subarachnoid
space. Its middle layers contribute to a layer of hydrated cells ( H ) which are closely
applied to the arachnoid membrane ( A ) . Changes i n cytoplasmic density occur within
the extent of a single cell. The outer layers of the perineurium extend between the
hydrated cells ( H ) and the dura mater (D). More medially they either disappear or become hydrated cells. At the subarachnoid angle the surface cells of the root sheath (R)
and the arachnoid membrane ( A ) are joined by a punctate junction. There is no “turnback” of a single cell as in figure 18. The clear intercellular spaces in the vicinity may
communicate with the subarachnoid space out of the plane of the drawing. The area of
the subarachnoid angle around the ventral root displays a wider range of cytoplasmic
densities than the same area around the dorsal root.
32
SUBARACHNOID ANGLE
John S. McCabe and Frank N . Low
PLATE 6
33
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