NEUROGLIA
The term glia was introduced by Virchow to describe a second cell type whose
function was to bind the nerve cells together in the brain. Later the glial
cells were classified into three categories: the first and second corresponded
to the two varieties of astrocytes (protoplasmic and fibrous), whilst the third
'element' referred to a group of cells which was subsequently shown by del Rio
Hortega to comprise both
oligodendrocytes and microglial cells. Del Rio Hortega introduced the silver
carbonate method, which not only
distinguished and separated
oligodendrocytes from microglia, but also indicated that they were of
different derivation. Thus oligodendrocytes have a similar neuroepithelial origin
to astrocytes, whereas microglial cells originate from mesenchyme. Thus, the
term neuroglia should not be applied to microglial cells. Neuroglia includes
only astrocytes, oligodendrocytes, ependymal
cells, and the
choroid plexus epithelium
derived from ependyma.
ASTROCYTES
Of the neuroglial cells, astrocytes are the most varied
morphologically and the most versatile functionally. It is traditional and
convenient to distinguish protoplasmic and fibrous astrocytes. The difference
between these two types is based upon the configuration and the number of
processes rather than on the filament content of the
cell body. the processes of fibrous astrocytes are fewer and
longer and branch less frequently and at a more acute angle than those of
protoplasmic astrocytes.
Protoplasmic astrocytes are found mainly in the grey matter
whilst fibrous astrocytes occur mainly in the white matter of the brain and
spinal cord. Fibrous astrocytes,
however, are also found in the outer cortical layer, around penetrating
arterioles and, together with protoplasmic astrocytes, in the deep grey matter:
the inferior olive contains a particularly large proportion of fibrous
astrocytes. A varietv of
fibrous astrocytes, the so-called marginal glia, sends short, robust processes
towards the pial surface, and contributes to the formation of the external
glial limiting membrane (glia limitans).
Subdivision of protoplasmic astrocytes in the grey matter,
according to their localisation, into neuronal satellites, interneuronal
astrocytes and vascular satellites serves little useful purpose. However,
astrocytes of the cerebellar cortex, which are principally of the protoplasmic
type, merit separate consideration on the basis of morphological variation and
functional difference. The smooth astrocyte is found throughout the cerebellar
cortex, the velate or lamellar type chiefly in the granular layer, and the
Golgi epithelial cell in the Purkinje and molecular layer. Golgi epithelial cells are in fact the
Bergmann glia, whose processes cover large areas of the cell body and dendrites
of Purkinje cells. A further type in the cerebellar cortex is the feathered
glia of Fafianas: these cells are more superficial than Bergmann cells and
their short stout processes do not reach the pial surface. One form of
astrocyte which has features of both the protoplasmic and fibrous astrocytes,
but is identical with neither, occurs in the corpus callosum, basis pontis and
spinal cord. This intermediate or mixed astrocyte has long fibril-containing
processes identical to those of the fibrous type, whilst their shorter
processes are more protoplasmic in structure. Astrocytic density varies greatly in various parts of the brain.
The ratio of glial cells to neurons, for example, is 4:1 in the striatum and
100:1 in the globus pallidus. These variations in astrocytic morphology in
different parts of the central nervous system are well established, but
information has only recently emerged from immunocytochemical and tissue
culture work regarding the possible differences in astrocyte physiology and
development in various topographical sites in the brain.
Although astrocytes can be identified in haematoxylin and cosin
stained sections, the intricate pattern of cytoplasmic processes which render
these cells star-shaped can be better demonstrated by the use of special stains.
The oval or round vesicular nucleus usually lacks a prominent nucleolus and
this feature proves particularly convenient in identifying cells in the cortex:
neurons are distinguished by their conspicuous nucleoli. Astrocytic processes
cover the external surfaces of the central nervous system, surround blood
vessels and abut upon nerve cells. The external glia limitans is formed by
stout astrocytic processes which, in turn, are covered by a basal lamina
beneath the pia.
Similarly, end-feet, the expansions of astrocytic processes,
envelop blood vessels and form a limiting membrane around the adventitia of
larger vessels. These astrocytic end-feet or foot processes also invest the
capillaries, and this intimate relationship has provided the structural basis
for the astroglial involvement in the blood-brain barrier. Astrocyte cell
bodies can be in close apposition to neurons, and astrocytic processes are
frequently seen covering the extensive surfaces of neuronal perikarva and dendrites.
Electron microscopy has revealed that the vesicular
astrocyte nucleus contains evenly dispersed, fine chromatin which is
occasionally clumped at the nuclear membrane. The nuclear profiles can be
somewhat irregular with
indentations, and the nucleolus, when present, is small.
The cytoplasm is of low electron-density and contains the usual assortment of
organelles. The cisternac of the rough endoplasmic reticulum are short,
ribosomes few and Go Igi complexes not well developed. Mitochondria are present
both in the perikaryon and the cell processes, and the larger, more unusual
forms are likely to correspond to the gliosomes detected by light microscopy.
Glycogen granules are numerous in well-fixed tissues and appear to be
concentrated in areas of high synaptic density and near neuronal perikarya.
Lysosomes are also seen as electron-dense bodies limited by a single unit membrane.
Astrocytic filaments, 10 mm in
diameter, belong to the class of intermediate filaments of the cytoskeleton and
are conspicuous in the perikaryon and in cell processes. The filaments are
present in protoplasmic astrocytes, usually in the form of cytoplasmic bundles,
but they are more abundant in fibrous astrocytes, in which they occur
throughout the cell body and extend into the larger processes.
Microtubules, although present, are not plentiful in mature
astrocytes. Astrocytes often form specialised cell contacts of the gap junction
type (so-called nexus) in which the outer leaflets of the apposed plasma
membranes are separated by an interval of 2-3 mm. Adjacent astrocytes are also joined by puncta
adhaerentia, where the plasma membranes run parallel, separated by a gap of
25-30 mm.
Astrocytic filaments and glial fibrillary acidic protein
(GFAP)
Astrocytic filaments are 10 mm in
diameter and indeterminate in length. They are composed of four globular
protein subunits, each measuring 2.5 mm, and linked by a cross-arm l.5 mm in
thickness. These units are stacked upon each other to produce the
characteristic configuration: in transverse section a hollow central core is surrounded
by a dense wall of 2.5 mm, whilst
in longitudinal section two parallel dense lines enclose the lumen.
The filaments are composed of glial fibrillary acidic
protein (GFAP) which was first isolated in a water-soluble form from glial scar
tissue of burntout plaques of multiple sclerosis and from hydrocephalic
brains. GFAP has a molecular
weight in the range of 50000 daltons and is well characterised chemically. Immunocytochemistry indicates that GFAP may exist in two
structural states, diffuse in the cytoplasm or localised to filaments, and
these in turn may correspond to the water-soluble and water-insoluble forms,
respectively 69 Metabolic studies of cytoskeletal proteins in cultured
astrocytes have revealed that GFAP is amongst the most actively
synthesised proteins with
a relatively fast turnover, and both the level of synthesis and
accumulation of GFAP can be experimentally manipulated. It is present in normal, reactive and
neoplastic astrocytes and has become the most reliable immunocytochemical
marker by which the identity of astrocytes can be positively established both
in diagnostic work and for research. In addition to astrocytes, GFAP can be demonstrated by
immunocytochemistry in other cells which
contain glial filaments:
in reactive ependymal cells,
tanycytes, reactive Muller cells of the retina, in the pituicytes of the neurohypophysis
and in the glial cells of the
enteric nervous system. It
is also present transiently during development in the myelin-forming
oligodendrocytes of the human fetal spinal cord, and in ependymal cells of
human fetuses between the 15th and 40th week of gestation. The
function of GFAP has yet to be determined, but experimental evidence suggests
an important role in fibrillogenesis which, in turn, is associated with
astrocytic differentiation.
Functions of astrocytes
The concept of astrocytic function has changed profoundly
during the last 20 years: cells which
once were thought to be mere physical supporting elements
have been shown to have a wide range of activity in the developing, normal and
diseased central nervous system.
Structural support.
Virchow's original view of neuroglia as cells which somehow held the neurons
together has been supported by successive observations of astrocytic
morphology. First, astrocytic processes cover the outside surfaces of the
central nervous system, forming the glia limitans, and envelop intraparenchymatous
blood vessels, constituting a sleeve of end-feet. Second, astrocytic filaments
provide mature astrocytes with a cytoskeleton which stabilises the cell
configuration and endows processes with considerable strength. These processes
may form bundles which interweave with nerve fibres, particularly in the white
matter. Finally, astrocytic processes are often joined together by specialised
cell contacts which increase their strength and cohesion. Although microtubules
play a role in process formation in differentiating astrocytes, filaments are
the organelles which maintain and influence the overall morphology of mature
cells.
Repair.
The ability of astrocytes to produce abundant filaments is
seen in various pathological conditions. Although the formation of glial scar
tissue is important in repair of the central nervous system following injury,
fibrillary gliosis may occur physiologically in certain areas including the
olivary nuclei, the floor of the fourth ventricle, and around both the cerebral
aqueduct and the central canal of the spinal cord.
The blood-brain barrier.
The structural proximity of astrocytic foot processes to
capillaries has provided a morphological basis for the view that astrocytes
contribute to the maintenance of the blood-brain barrier.
Isolation of neuronal
surfaces.
Astrocytes establish intimate spatial relationships with
nerve cells. They are occasionally satellites to neurons, but more importantly
their processes regularly cover receptive surfaces of the nerve cells,
including the perikarya and dendrites. Moreover, astrocytic processes often
abound in areas of intense synaptic activity; the most striking example of this
phenomenon is to be found in the thalamus, where the synaptic glomeruli are
wrapped in astrocytic sheets which form capsules several layers thick.
Astrocytic processes are thus not disposed at random, but they conform to a
pattern which ensures that receptive neuronal surfaces are protected from
non-specific afferent influences. Astrocytes also play a role in
synaptic remodelling in the mature, normal brain by removing degenerating
synapses.
Neuronal development.
Evidence for astrocyte involvement in neuronal development
originates from both in vivo and in vitro observations. Radial astroglial
fibres appear to guide immature, migrating neurons and to form a template for
the growth of nerve cells. Neurons of the central nervous system are
difficult to grow in primary cultures, unless an astrocyte mono layer is provided or the medium is conditioned by
growing astrocyte cultures. In
vitro studies have also shown that glial cells can influence the prolection and
branching patterns of nerve cells and may be instrumental in determining the
neuronal polarity observed in vivo.
Electrophysiology
and ion transport.
Recent investigations have revealed that astrocytes are not
inactive cells: they respond to K accumulation or release, with changes in
intracellular K + concentration. Astrocytes can act both as spatial buffers,
merely redistributing extracellularly accumulated K+, and as active
accumulators of K+. These mechanisms complement each other and may enable
astrocytes to monitor the extracellular ionic milieu and consequently to
control neuronal function.
Furthermore, release of potassium ions (K +) from astrocyte
end-feet may play an important role in regulating regional cerebral blood flow
in response to changes in neuronal activity. It has been demonstrated in
primary astrocyte cultures, which are presently the best experimental system
for ion transport studies, that not only K+, but also Na+ and Cl-
can enter and leave these cells, suggesting that astrocytes contain significant
ion transport pathways. Under
controlled conditions in culture, astrocytes show both spontaneous action
potentials and action potentials induced by current. These responses indicate
the presence of voltage-dependent Ga2 -channels which may be
important in the regulation of excitability within the central nervous system.
Furthermore, both glutamic and
aspartic acid directly depolarise brain astrocytes in primary cultures,
suggesting that the electrophysiological effects of excitatory amino acids in
situ may not be exclusively a neuronal property.
Creatine kinase (isoenzyme BB) has been shown by
immunocytochemistry to be present in human astrocytes. The function of this
enzyme in the brain may be related to the increase in respiration and the fall
in both ATP and creatine phosphate levels which result from exposure to high
potassium concentrations or from electrical stimulation.
Neurotransmitter
metabolism.
Astrocytes in culture possess receptors for
neurotransmitters, and exposure to noradrenaline results in increased levels of
intracellular cyclic adenosine mono-phosphate (cAMP). Adrenergic x- and
fl-receptors have also been identified on astrocytes, and dopamine, for
example, enhances cAMP by activation
of fl-receptors. Astrocytic
processes surrounding synapses could control the levels of transmitters by
taking up these compounds, but it remains to be determined whether this uptake
is involved in the further metabolism or inactivation of the neurotransmitter.
Primary cultures of astrocytes indeed take up dopamine, noradrenaline,
serotonin, GABA (g-aminobutyric
acid) and glutamate and have some of the enzyme systems required for their
metabolism. Astrocytes in
culture also respond to histamine and its agonists, but the functional role of
histamine receptors remains to be elucidated. However, the wide
range of receptors on astrocytes allows these cells to play an important and
varied role in the central nervous system.
The role of astrocytes in the metabolism of glutamate, a
putative excitatory neurotransmitter, is well documented. Glutamate is released
by neurons at synapses and is taken up by astrocytes in which glutamine
synthetase catalyses the reversible formation of glutamine from glutamate and
ammonia. Glutamine is freely diffusible and reaches nerve cells in which
glutaminase will produce glutamate and thus complete this metabolic pathway.
The small glutamate pool in the brain is, therefore, compartmentalised in astrocytes
. Immunohistochemical studies have demonstrated that glutamine synthetase
is confined to astrocytes, and the amount present in various brain areas
correlates well with sites of presumed glutaminergic activity.
Detoxification of ammonia.
From the above description it follows that as astrocytes
possess glutamine synthetase activity, they are also important in the
detoxification of ammonia.
Phagocytosis.
There is now little doubt that astrocytes have
pinocytotic and phagocytic functions and by removing various
substances, including plasma, particulate material and cell debris from
the extracellular space,
they contribute to the maintenance of a controlled internal environment.
Immune response.
Recent experimental evidence suggests that astrocytes may
have a physiological function essential for the generation of immune responses
within the brain: they respond to lymphocyte-derived growth factors and secrete
immunoregulatory molecules in culture. They can be activated to release
prostaglandin E and interleukins. Rat astrocytes appear to be able to present
antigen to T lymphocytes in a specific manner which is restricted by the major
histocompatibility complex. Astrocytes
are stimulated in the presence of intefferon, produced by T lymphocytes, to
express Ia antigens. Astrocytes and their precursors also respond, in culture,
to glial maturation factor and produce interleukin 1; this, in turn, stimulates
the proliferation of astrocytes.
OLIGODENDROCYTES
Oligodendrocytes can be subdivided according to their
location: satellite cells are adjacent to neurons in the grey matter and
interfascicular oligodendrocytes occur between nerve fibres in the white
matter. In the grey matter, oligodendrocytes are also associated with nerve
fibres or are adjacent to blood vessels. Perineuronal oligodendrocytes are
functionally similar to those in the white matter. Immunocytochemistry for
myelin basic protein and myelin-associated glycoprotein reveals a similar
staining pattern for all oligodendrocytes in the normal brain, during remyelination
and following trauma. Based
on ultrastructural features, particularly
on cytoplasmic density,
three subtypes can be distinguished: light, intermediate and dark. This
separation is arbitrary and these forms represent developmental stages through
which oligodendrocytes evolve during postnatal life. Light oligodendrocytes appear
to be mitotically the most
active and they become smaller and darker as they mature.
In sections stained with haematoxylin and eosin,
oligodendrocytes can be recognised by their round or oval nuclei which are
surrounded by a rim of cytoplasm. Silver impregnation reveals only a few
processes, which are usually long and delicate and radiate from the polygonal
or spherical perikaryon. By electron microscopy, oligodendrocytes are, in
general, darker cells than astrocytes, with an intrinsic density of the cytoplasmic
matrix created by tiny granules which occupy all the space between organelles.
The chromatin in the round oval or, occasionally, irregular nucleus often
forms clumps, which is another difference from the evenly dispersed
chromatin of astrocytes. Oligodendrocyte cytoplasm
contains abundant rough
endoplasmic reticulum, many
free ribosomes and a well-developed Golgi apparatus. Mitochondria, lysosomes
and heterogeneous inclusion
bodies are present. Unlike in astrocytes, however, glycogen granules are not
seen in oligodendrocytes. There is a striking difference between the
cytoskeletons of oligodendrocytes and astrocvtes in that the ratio of filaments
to micro-tubules is reversed: oligodendrocytes have many microtubules and only
an occasional filament. The microtubules are dispersed at random in the cell
body, whilst in processes they are arranged in parallel bundles. The following
features distinguish the oligodendrocyte from the astrocyte: greater nuclear
and cytoplasmic density, the lack of filaments and glycogen granules, and the
abundance of microtubules.
Functions of oligodendrocytes
Two major functions are usually attributed to
oligodendrocytes: the formation and maintenance of myelin, and the nutrition of
neurons. There is now little doubt that the myelinforming cell in the central
nervous system is the oligodendrocyte, which first appears immediately before
myelination begins. in the developing brain direct connection can be seen between
oligodendrocytes and the myelin sheath as it forms. Biochemical studies have
shown that oligodendrocytes, particularly neuronal satellites, can contribute
to the nutrition of nerve cells. The metabolic activities of neurons and oligodendrocytes can complement each
other in a symbiotic fashion, and these two cell types form a functional unit.
Furthermore, mature oligodendrocytes, in vitro, proliferate only in the
presence of neurons, indicating that axons are mitogenic for these cells. Tissue
culture studies have also shed new light on the functions of oligodendrocytes. Isolated
cells synthesise both galactocerebrosides and sulphatides
and contain various enzymes
including 2' :3'-cyclic-nucleotide 3'-phosphodiesterase, carbonic anhydrase,
glycerol phosphate dehydrogenase and glucose-6-phosphate dehydrogenase,
indicating a high rate of metabolic activity. Oligodendrocytes respond to a variety of lymphokines and
other growth factors and thus may be involved in immunological reactions.
EPENDYMAL CELLS
The ependyma lines the ventricular system, the cerebral
aqueduct and the central canal of the spinal cord. These epithelium-like cells
are cuboidal or colurnnar and show characteristic polarity of cellular
organisation. A round or oval nucleus is located in the basal part of the cell,
whilst most organdIes occupy the apical portion. The cell membrane is
specialised according to surface. Thus the lateral membranes of adjacent cells
run parallel and are joined together by
specialised junctions; the
cell membrane at the base of the cell has an irregular contour and rests
upon glial fibres; the apical surface is studded with cilia. Ependyma lining
the ventricular system varies in its morphology. In general, cells covering the
white matter are more flattened and have fewer cilia than those covering grey
matter.
Electron microscopy shows that the nucleus contains evenly
distributed, fine chromatin and a small eccentric nucleolus. The well developed
Golgi apparatus is supranuclear, and mitochondria tend to crowd the apical
portion of
the cell. The rough endoplasmic reticulum consists of only a
few, short cisternae , but free
ribosomes are numerous. Multivesicular bodies, lysosomes and vesicles of
various sizes are also present. The cyto skeleton is composed of 10 mm
intermediate filaments, 4.6 mm microfilaments
and occasional 24 mm
microtubules. Intermediate filaments are similar to those found in astrocytes,
but they do not appear to contain GFAP in normal, mature ependyma. However,
ependymal cells in human fetuses contain GFAP transiently between the 15th and
40th week of gestation. The nature of filaments in mature ependymal
cells remains an enigma: they may be antigenically different from astrocytic
filaments or the binding of GFAP within the filament may have resulted in loss
of affinity for the specific antiserum.
Cilia spring from the basal bodies in the apical cytoplasm
which can occasionally be seen as blepharoplasts with the light microscope in
good PTAII preparations. Each cilium is composed of 9 pairs of microtubu]es
surrounding a central pair. Between the cilia, microvilli and simple cytoplasmic
protrusions increase the apical surface area of the cell. The lateral plasma
membranes of adjacent ependymal cells often interdigitate, forming gap
junctions (nexus), extensive zonulac adhaerentes and occasional tight
junctions (zonulae occiudentes) toward the apices.
Tanycytes
Tanycytes are modified
ependymal cells distinguished by
their long, radially orientated and unbranching basal processes which usually
reach subependymal capillaries These cells, which owe their name to their
elongated shape, have a somatic portion, which lies in the ependyma and
contains the nucleus, a neck portion, which is located in the periventricular
neuropil, and a tapering tail. The apical surfaces of tanycytes have more thin
cytoplasmic projections and fewer cilia than other ependymal cells and, by
electron microscopy, their cytoplasm is somewhat darker and contains fewer filaments
and more microtubules.
Functions of ependymal cells
The cilia of ependymal cells beat rapidly during life and
this movement may contribute to the circulation of the cerebrospinal fluid
(CSF). The structural organisation of ependyma, with its interdigitations and
specialised junctions at the lateral cell surfaces, is suggestive of a
supportive function, similar to that performed by astrocytes. As ependyma forms
a barrier between the ventricular CSF and the parenchyma of the central nervous
system, it is ideally situated to influence the transport of substances. When
electron-dense markers, such as horseradish peroxidase and ferritin, are
injected into the ventricles they penetrate into the brain between ependymal
cells. In addition, these materials are taken up by the ependyma and
transported in vesicles and multivesicular bQdies, suggesting that other
substances in the CSF may follow a similar pathway. As tanycytes connect the
ventricular surface and capillaries, it is thought that they transport material
from the CSF to the brain and into the vascular circulation, but their major
function is structural.112 Ependymal cells may perform sensory and
secretory functions in various animal species, but evidence for
these activities in man is still not available.
MICROGLIAL CELLS
The profusion of names which exist for microglial cells is a
good indicator of the controversy surrounding the Origin and morphological
heterogeneity of microglia. Hortega or Robertson-Hortega cell, cerebral
histiocyte, phagocyte, rod cell and mesoglia are synonyms for the microglial
cell. It has been established that microglial cells are present in the normal
brain.
Microglial cells are ubiquitous in the central nervous
system, although they are somewhat more numerous in the cortex than in the
white matter. Most appear to be distributed at random, but some are
preferentially located near neurons and blood vessels. The nucleus is
triangular or elongated and the chromatin pattern is less vesicular than in
astrocytes, although not as dense as in oligodendrocytes. Very little
cytoplasm is visible in haematoxylin and eosin stained sections, but
immunocytochemical techniques and silver impregnation demonstrate the cell processes, which are occasionally very long,
but less numerous than astrocytic processes. Electron microscopy reveals the
usual complement of organelles in microglial cytoplasm. Thus, a few, long
cisternae of the rough endoplasmic reticulum, some ribosomes, an active Golgi
apparatus, mitochondria, microtubules and a few filaments are seen. The most
prominent feature of the cytoplasm is the presence of dense inclusion bodies,
mainly lysosomes. The nucleus contains coarsely clumped chromatin, and is often
located at one end of the cell, surrounded by a thin rim of cytoplasm, whilst
the organdIes occupy the opposite pole.
Origin of microglia
The Origin of microglial cells has been the subpect of long
controversy and the problem has yet to be convincingly settled. Various
hypotheses have been proposed and include origins from pial, neuroepithelial,
pericytic and monocytic cells. A mesodermal or pial origin of microglia
suggests that primitive mesodermal cells accumulate beneath the pia
and penetrate the brain parenchyma
as diverse forms of amoeboid microglia which, during differentiation, retract
their pseudopodia and
develop branching processes to become
mature microglial cells. The opposing neuroepithelial theory maintains that
microglial cells originate from the primitive cells of the subependymal plate
either directly or indirectly through amoeboid microglial cells. Microglioblasts
or amoeboid microglia are, in fact, glioblasts derived from the matrix cells
and thus, according to this theory, microglial cells would share a common
progenitor with astrocytes and oligodendrocytes.
Pericytes are cells closely apposed to the capillary
endothelium and enclosed by the basement membrane. Morphological similarities
and the phagocytic capacity of pericytes's'4 have led to the view
that they could be a source of microglia; these cells could migrate into the
brain through disruptions in the
basement membrane.517
However, pericytes have been shown to remain anchored to the vascular wall in
pathological conditions and do not become transformed into actively phagocytosing
microglial cells.
The theory that microglial cells originate from monocytes
has attracted many supporters, who maintain that monocytes from the
blood enter the brain, in which, conforming to a different environment, they
acquire the features of resting microglial cells. That blood monocytes can
permeate the brain has been shown using carbon-labelled cells;
thus, the sequential appearance of carbon particles in
monocytes, amoeboid microglia and microglia strongly suggests that monocytes
become microglial cells. However, the infiltration of blood
monocytes into the brains of experimental animals is age dependent, and the
blood-brain barrier may also play a role in preventing monocytes from entering the
brain in large numbers in mature animals. Moreover, immunological studies have produced evidence
against the monocytic origin of microglia; microglial cells do not possess monocytic
membrane antigens and mononuclear phagocytic markers. However, monocytes may lose their
rnembrane markers on entering the brain and then adapt to an entirely different
environment.
Functions of microglia
The function of resting microglia in the normal brain is far
from clear. These cells are thought to maintain a close, functional
relationship with neurons, axons and myelin sheaths, to regulate the ion and
fluid balance of the extracellular space and to transport substances.sis The
presence of Fc and complement receptors and of HLA class II complex on
microglial cells suggests that they could play a role in the immunological
defence of the nervous. Microglial cells have the ability to engulf and ingest
various substances, including particulate material, parts of other cells or
even whole cells. They are rich in lysosomal hydrolytic enzymes, which enable
them to perform phagocytic activity. This potential becomes manifest in pathological
conditions.
BLOOD VESSELS AND THE BLOOD BRAIN BARRIER
Cerebral capillaries are fundamentally similar to those of
other tissues, but there are important differences. There is a paucity of cytoplasmic
vesicles in the endothelial cells, and the tight junctions between the
endothelial cells differ from those of other tissue capillaries. In addition,
astrocytic foot processes surround each capillary. The lumen is lined by
endothelial cells which display oval or elongated nuclei located in the
thickened part of the capillary wall. The cytoplasm contains the usual set of
organelles, of which mitochondria are the most abundant. Complex membrane-bound structures, the Weibel-Palade
bodies, are difficult to find. Cytoplasmic vesicles are scarce and fewer than
in most other capillaries. The structure of the interendothelial connections is
variable, but in general the adjacent cell membranes are parallel, and, towards
the luminal end, the outer leaflets fuse to form tight junctions (zonulac
occludentes).
The endothelial cytoplasm is richly endowed with enzymes,
including adenosine triphosphatase, nicotinamide adenine
dinucleotide, monoamine oxidase, acid and alkaline phosphatases, various
dehydrogenases, DOPA
decarboxylase and g-glutamyl
transpeptidase. The wealth of these enzyme systems reflects the unique role
played by the cerebral endothelium in the blood-brain barrier. Moreover,
differences in the intensity of various hydrolytic enzymes at the luminal and
abluminal cell membrane strongly indicate the polarity of endothelial function
in the control of the blood-brain interface. Outside the endothelium lies a
continuous basal lamina or basement membrane approximately 40-50 mm thick
and composed of an admixture of substances, including type IV collagen, heparan
sulphate proteoglycan, laminin and entactin. Astrocytic foot processes abut
onto capillaries, forming a complete envelope in most cases: occasionally other
cells may have direct contact with the basal lamina. Pericytes are completely
surrounded by a duplication of the basement membrane, and are frequently seen extending their
processes around the capillary; their cytoplasm contains many lysosome-like
bodies. The origin and function of pericytes remain to be established, although
the view that they could give rise to microglial cells has gained some support.
Arterioles and small arteries differ from capillaries not
only in their larger size, but also by the presence of smooth muscle cells in
their walls. Outside the endothelium, one or two layers of smooth muscle cells
are transversely orientated and sandwiched between thick basal laminae. Venules
resemble large capillaries and the transition between the two types of vessel
is difficult to identify.
Histological demonstration of blood vessels Van Gieson's technique alone or combined
with an elastin stain gives good results in demonstrating connective tissue
components of vessel walls. The overall pattern of vascularisation is well
demonstrated by reticulin stains. Of the enzymes, the allraline phosphatase
reaction reliably identifies endothelial cells both by light and electron microscopy.
The immunocytochemical demonstration of factor VII I-related antigen is now
routinely used to define endothelial cells. Monoclonal antibodies against endothelial anglotensin-converting
enzyme are also available.
The blood-brain barrier
The concept of a blood-brain barrier was first based upon
the observation that intravenously injected vital dyes, like Evans (azovan)
blue and trypan blue, entered and stained various organs, but not the brain.
Later, ultrastructural studies with electron-dense tracers, such as
horseradish peroxidase or lanthanum, demonstrated that tracers do not penetrate
the interendothelial cell junctions in the brain, neither are they carried
across the endothelial cell by
vesicular transport. The
morphological basis for the blood-brain barrier appears to reside in two
features of endothelial cells: the presence of tight junctions and the paucity
of cytoplasmic vesicles. The oversimplified single-membrane model, however, is
no longer accepted; intercellular tight junctions, intracellular enzyme systems
and the two endothelial cell membranes all contribute to the barrier effect.
It has been demonstrated in vitro that astrocytic foot processes, unique
to cerebral capillaries, could contribute to the barrier. Astrocytes are
essential for the expression of the endothelial enzymes which play a role in
transport mechanisms and for
the induction of barrier properties in vitro.
The blood-brain barrier does not pertain in all parts of the
mammalian brain: a few, relatively small and usually periventricular structures
are freely permeable to vital dyes and electron-dense tracers. These structures
include the area postrema, median eminence, subcornmissural organ, pineal
gland, subfornical organ, supraoptic crest and neurohypophysis. The blood
vessels in these areas have ultrastructural, enzymatic and permeability
features which are different from those in other areas of the brain.
It has been realised that the blood-brain barrier is more a
regulatory interface between the blood flow and the cerebral parenchyma than a
simple rigid physical barrier. The passage of a particular substance
across the blood-brain barrier may depend upon various factors, including its
lipid solubility, electrical charge, molecular size, dissociation
constant, affinity for a carrier
molecule and the nature of the substance in relation to the capacity of the
blood-brain barrier for active transport.
The function of the blood-brain barrier is threefold. First,
it prevents or hinders the entry of most water-soluble substances into the
brain; the permeation rates are usually determined by lipid solubility.
Secondly, the blood-brain barrier promotes the transport of certain materials,
including some hexoses and several amino acids, by stereo-specific carrier
transport systems which are present in the cerebral endothelium. Thirdly, the
blood-brain barrier plays an important role in the volume regulation of the
central nervous system. This is achieved by two mechanisms which limit the bulk
flow of water across the blood-brain barrier: these are the low hydraulic
conductivity of capillaries and the high osmotic activity of the major solutes.
ThE CHOROID PLEXUS
The choroid plexus is composed of a vascular fold of the pia
mater and an epithelial layer derived from the ependymal lining. There are four
choroid plexuses, one in the medial wall of each lateral ventricle and one each
in the roofs of the third and fourth ventricles. They have clearly defined
attachments to the ventricular wall and their free edges are invaginated into
the ventricles. The surface area of the choroid plexus is greatly increased by
the many fronds, which in turn consist of tiny villous processes. The arteries
supplying the choroid plexus branch out into capillaries, one for each villus,
which then join to form a vein.
The epithelium consists of a single layer of cuboidal cells
mounted on a basement membrane; in a few areas, however, pseudostratification
or even true stratification may occur. Choroid plexus epithelium can
be identified immunocytochemically by the presence of
carbonic anhydrase 11(c) in the cytoplasm; this enzyme probably plays a role in the production of
cerebrospinal fluid (CSF). The round or oval nucleus of the cell is usually
centrally located in the cytoplasm, which has the usual complement of
organelles. Mitochondria are particularly numerous and are mainly in the apical
portion of the cell: they provide the energy necessary for the active transport
carried out during production of the CSF. Smooth and coated vesicles of various
sizes are seen throughout the cytoplasm and these take part in the transport of
materials. The apical surface of the epithelial cell is greatly increased in
area by masses of microvilli and occasional cilia which tend to be grouped
together. The lateral plasma membranes are bound together by complex connections:
by tight junctions (zonulac occludentes) at the apical end, by zonulac
adhaerentes, and by intricate infoldings at the basal end. Occasional
phagocytes, the epiplexus or Kolmer cells, are seen on the surface of the
choroid plexus epithelium; they may play a role in keeping this surface free of
debris.
The fibrovascular core of the choroid plexus supporting the
epithelium contains arachnoid cells; whorls of collagen fibres in the fibrous
stroma become calcified with advancing age. Blood vessels of various
sizes include small arteries, arterioles,
capillaries and venous
sinuses. Capillaries in the villi are fenestrated and their endothelial
lining is very thin.
Functions of the choroid plexus
The main function of the choroid plexus is the production of
the CSF, although a proportion of the CSF, estimated to be 10-20%, is derived
from extrachoroidal sources. In man, approximately 500-700 ml is
produced every day; of this only 140 ml can be accommodated at any one time: 25-30
ml in the ventricles and the rest in the subarachnoid space. Although
it has been disputed whether the CSF is the result of passive dialysis or
active secretion, evidence now favours the latter mechanism. Factors which are
involved in the formation of CSF include pressure, serum osmolality,
temperature, age, innervation of the plexus and prostaglandins.
THE MENINGES
The meninges covering the central nervous system are
composed of three layers: the dura mater, the arachnoid mater and the pia
mater. The arachnoid and pia jointly form the leptomeninges.
The dura mater (pachymeninx) is a tough, dense membrane
which surrounds the brain. It has two extensions: the falx, between the two
cerebral hemispheres, and the
tentorium cerebelli, separating
the contents of the posterior fossa from the rest of the brain. The cranial
dura is closely attached to the skull; its two layers, the periosteal and
meningeal dura, are fused and separate only to form the venous sinuses. In the
spinal canal, however, the dura is separated from the vertebral periosteum by
the epidural space, which contains fibro-fatty tissue and an epidural venous
plexus.
The dura is formed by dense, interlacing bundles of collagen
in which flattened fibroblasts are embedded. The central part contains more
cells and occasional blood vessels. Its outer surface is covered by thin,
overlapping cell processes and its inner border also has a covering of flattened
cells. The subdural space is artefactual, since the dura and arachnoid are
closely apposed in life with no appreciable gap between them.
The arachnoid mater has a variable thickness, in places
being formed by several cell layers. Its outer, dural aspect is smoother than
the inner, pial -aspect from which trabeculae emerge to bridge the subarachnoid
space. The arachnoid cells are joined together by specialised contacts,
including tight junctions, which ensure an effective physiological barrier
impermeable to CSF.
The cells of the pia mater are similar to those of the
arachnoid, but the pia itself is thinner than the arachnoid. Pial cells form a
complete layer joined by desmosomes and gap junctions. The subpial
space separates the pia from the glia limitans of the underlying neural tissue
and the pia mater separates the subarachnoid space from the perivascular (Virchow-Robin)
spaces of the brains.
Arachnoid villi are diverticula of the arachnoid mater and
the subarachnoid space which extend into veins and venous sinuses of the dura.
Arachnoid granulations are larger than villi and are visible to the naked eye,
whereas villi are microscopical structures. Each villus or granulation is
coated on its venous aspect by endothelial cells and is bathed by venous
blood. As the villus or granulation penetrates the dura, it forms a narrow neck
which then expands to form a central core composed of channels and collagenous
trabeculac. Towards the apex of the granulations there is a cap of arachnoid
cells with wide channels running through to the coating endothelium. These
structures are a major pathway for the drainage of cerebrospinal fluid, which
percolates through the cores of the villi or granulations and is transported
across the endothelium into the blood.
THE SUBEPENDYMAL PLATE
The subependymal plate has long been recognised as a layer
of primitive cells beneath the ependymal lining of the lateral ventricles in
the adult human. It is the remnant of the embryonal matrix (the subventricular
zone). Studies of the subependymal
plate in various animal species have revealed that in the fetus it gives rise
to both neurons and glia, whilst after birth it is a source of glial cells
oflly. The cells of the subependymal
plate display ultrastructural features common to primitive cells: high
nuclear-cytoplasmic ratio, dominance of free ribosomes over membrane-bound
ribosomes and a general scarcity of organelles. Mitotic activity persists into later adult life in various
species, including primates. Unfortunately,
information on the human subependymal extrapolation from may be misleading.