Introduction ......................... 95 Arteries of the Brain ................... 95 Meninges, Cisterns and Cerebrospinal Fluid Circulation ........ 110 Circumventricular Organs ................ 126 Veins of the Brain ..................... 126 Vessels and Meninges of the Spinal Cord ..... 128 Introduction The vascularization and the circulation of the cerebrospinal fluid (liquor cerebrospinalis, CSF) of the brain and the spinal cord are of great clinical importance. The main vascular syn- dromes are summarized in Table 4.1. In this chapter, the anatomy of blood vessels, meninges and circumventricular organs will be discussed. The central nervous system, which is of ectoder- mal origin (Chap. 2), is surrounded by meso- dermal structures. A system of three connective tissue layers, the meninges, and a fluid compart- ment containing CSF are located between the bony skull and vertebral column and the ner- vous tissue of the brain and the spinal cord. Blood vessels, themselves of mesodermal origin, are surrounded by derivatives of the meninges over their full extent, until the interface between the capillary wall and the glial basal membrane makes exchange of substances possible. CSF is produced by the choroid plexus of the ventri- cles. It circulates from the interstitial spaces of the nervous tissue and the choroid plexus, through the ventricles and their apertures in the roof of the fourth ventricle, to the CSF com- partment of the subarachnoid space and its exit through the arachnoid villi to the venous sys- tem. The nervous tissue of the central nervous system and the CSF spaces remain segregated from the rest of the body by barrier layers in the meninges (the barrier layer of the arach- noid), the choroid plexus (the blood-CSF bar- rier) and the capillaries (the blood-brain bar- rier). The circulation of the CSF plays an impor- tant role in maintaining the environment of the nervous tissue; moreover, the subarachnoidal space forms a bed that absorbs external shocks. Arteries of the Brain The arteries of the brain originate from two of the greater vessels in the neck: the paired inter- nal carotid and vertebral arteries (Fig. 4.1). The internal carotid artery enters the skull through the petrosal bone in the carotid canal. It loops through the sinus cavernosus (carotis syphon), where it emits the ophthalmic artery . Immedi- ately beyond the origin of the posterior commu- nicating artery it splits into the middle and ante- rior cerebral arteries. The vertebral arteries en- ter the skull through the foramen magnum. After their passage through the dura, the ar- teries become located within connective tissue derived from the pia mater and the arachnoid. The middle cerebral artery supplies the con- vexity of the hemisphere (Figs. 4.3, 4.4, 4.5) and the anterior cerebral artery vascularizes approximately the anterior and upper half of the medial aspect of the hemisphere, up to the precuneus (Fig. 4.2). The vertebral arteries unite into the basilar artery at the ventral as- pect of the medulla oblongata. Its terminal 4 Blood Supply, Meninges and Cerebrospinal Fluid Circulation
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4 Blood Supply, Meninges and Cerebrospinal Fluid Circulation · cerebrospinal fluid (liquor cerebrospinalis, CSF) of the brain and the spinal cord are of great clinical importance.
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Vessels and Meninges of the Spinal Cord . . . . . 128
Introduction
The vascularization and the circulation of thecerebrospinal fluid (liquor cerebrospinalis,CSF) of the brain and the spinal cord are of greatclinical importance. The main vascular syn-dromes are summarized in Table 4.1. In thischapter, the anatomy of blood vessels, meningesand circumventricular organs will be discussed.The central nervous system, which is of ectoder-mal origin (Chap. 2), is surrounded by meso-dermal structures. A system of three connectivetissue layers, the meninges, and a fluid compart-ment containing CSF are located between thebony skull and vertebral column and the ner-vous tissue of the brain and the spinal cord.Blood vessels, themselves of mesodermal origin,are surrounded by derivatives of the meningesover their full extent, until the interface betweenthe capillary wall and the glial basal membranemakes exchange of substances possible. CSF isproduced by the choroid plexus of the ventri-cles. It circulates from the interstitial spaces ofthe nervous tissue and the choroid plexus,through the ventricles and their apertures inthe roof of the fourth ventricle, to the CSF com-partment of the subarachnoid space and its exit
through the arachnoid villi to the venous sys-tem. The nervous tissue of the central nervoussystem and the CSF spaces remain segregatedfrom the rest of the body by barrier layers inthe meninges (the barrier layer of the arach-noid), the choroid plexus (the blood-CSF bar-rier) and the capillaries (the blood-brain bar-rier). The circulation of the CSF plays an impor-tant role in maintaining the environment of thenervous tissue; moreover, the subarachnoidalspace forms a bed that absorbs external shocks.
Arteries of the Brain
The arteries of the brain originate from two ofthe greater vessels in the neck: the paired inter-nal carotid and vertebral arteries (Fig. 4.1). Theinternal carotid artery enters the skull throughthe petrosal bone in the carotid canal. It loopsthrough the sinus cavernosus (carotis syphon),where it emits the ophthalmic artery. Immedi-ately beyond the origin of the posterior commu-nicating artery it splits into the middle and ante-rior cerebral arteries. The vertebral arteries en-ter the skull through the foramen magnum.After their passage through the dura, the ar-teries become located within connective tissuederived from the pia mater and the arachnoid.
The middle cerebral artery supplies the con-vexity of the hemisphere (Figs. 4.3, 4.4, 4.5)and the anterior cerebral artery vascularizesapproximately the anterior and upper half ofthe medial aspect of the hemisphere, up to theprecuneus (Fig. 4.2). The vertebral arteriesunite into the basilar artery at the ventral as-pect of the medulla oblongata. Its terminal
96 Section I Orientation, Development, Gross Anatomy, Blood Supply and Meninges
Fig. 4.1. Collateral circulation in the arterial system of the head; semidiagrammatic lateral view (2/3x). Black:external carotid artery with extracranial branches; black hatched: system of the vertebral artery (maintrunk); solid red: meningeal arteries; red hatched: internal carotid artery with orbital and lateral corticalbranches; open red: medial cortical branches of internal carotid artery
4 Blood Supply, Meninges and Cerebrospinal Fluid Circulation 97
Fig. 4.2. The arteries of the medial hemisphere; the anterior and posterior cerebral arteries (1/1 �). Somecentral branches of the posterior cerebral artery are also shown. End branches of the anterior cerebral arterythat reach the lateral side of the superior frontal gyrus are illustrated in Fig. 4.3. Figures 4.2–4.6 are allderived from the same specimen
1 Central sulcus2 Marginal branch of the cingulate sulcus3 Precuneus4 Artery of the precuneus5 Pericallosal artery, posterior branch
98 Section I Orientation, Development, Gross Anatomy, Blood Supply and Meninges
Fig. 4.3. The arteries of the lateral cerebral cortex: the middle cerebral artery (1/1 �). In this figure the lateraland medullary cisterns are left intact. On the lateral surface of the cerebellum one inferior and two superiorcerebellar branches are illustrated (see Fig. 4.11). On the superior frontal gyrus some end branches of theanterior cerebral artery can be seen
1 Central sulcus2 Posteromedial frontal branch3 Intermediomedial frontal branch4 Anteromedial frontal branch5 Medial frontobasal artery6 Lateral frontobasal artery7 Prefrontal artery8 Inferior frontal sulcus9 Artery of the precentral sulcus
10 Artery of the central sulcus11 Artery of the postcentral sulcus
(anterior parietal artery)12 Posterior parietal artery13 Artery of the angular gyrus14 Intraparietal sulcus
4 Blood Supply, Meninges and Cerebrospinal Fluid Circulation 99
Fig. 4.4. The branches of the middle cerebral artery seen at their full extent: lateral view (1/1 �). In this spec-imen, as in most cases, a trifurcation can be seen of the artery. The branches of the anterior (frontal) trunkare shown in black and red; the branches of the middle (parietal) trunk are in black only; the branches ofthe posterior (temporal) trunk are in red. The candelabrum-like branching, especially of the anterior trunk,is a common phenomenon
1 Central sulcus2 Artery of the central sulcus (branches)3 Postcentral gyrus4 Precentral gyrus5 Artery of the precentral sulcus6 Inferior frontal sulcus7 Inferior frontal gyrus, triangular part8 Prefrontal artery (candelabrum artery)9 Lateral frontobasal artery (branched)
10 Anterior trunk of the middle cerebral artery(ascending frontal artery)
11 Anterior temporal artery (branches)12 Temporopolar artery13 Middle trunk of the middle cerebral artery14 Posterior trunk of the middle cerebral artery15 Middle temporal artery16 Posterior temporal artery17 Superior temporal sulcus
18 Temporo-occipital artery19 Lateral sulcus, posterior branch20 Artery of the postcentral sulcus
Fig. 4.6. The cerebral arteries viewed from the basal side (1/1 �). Part of the left temporal lobe has been re-moved to show the sphenoid part of the middle cerebral artery and the arterial supply of the choroid plexusof the lateral ventricle. The lateral occipital artery has been interrupted to gain a clear view of the diencepha-lic, mesencephalic and retrosplenial branches of the posterior cerebral artery
26 Posterior cerebral artery,postcommunicating part
27 Medial posterior choroidal branch28 Anterior choroidal artery29 Choroidal branches of the anterior
choroidal artery30 Lateral posterior choroidal branch31 Lateral geniculate body32 Thalamic branch (inferior)33 Thalamic branch (posterior)34 Thalamic branch (superior)35 Dorsal branch of the corpus callosum
19 + 20 + 21 + 24 Arterial circle(left half)
101
branches are the left and right posterior cere-bral arteries, which supply the posterior, medi-al and basal aspects of the cerebral hemi-sphere. The vertebro-basilar arteries also sup-ply the brain stem and the cerebellum. It givesrise to the inferior, middle and superior cere-bellar arteries (Fig. 4.11). Frontal and lateralprojections of the arterial system are shown inFigs. 4.9 and 4.10.
A system of communicating arteries, knownas the circle of Willis [18, 36], interconnectsthe anterior and middle cerebral arteries ofboth sides with the vertebro-basilar system(Figs. 4.6 and 4.14). It is located at the base ofthe brain and surrounds the infundibulum andthe optic chiasm. It includes the anterior com-municating artery, which interconnects theanterior cerebral arteries, immediately in frontof the optic chiasm, and the two posterior com-municating arteries, which form an anastomo-sis between the most distal part of the internalcarotic and the posterior cerebral artery neartheir origin from the basilar artery.
The initial segments of the middle and ante-rior cerebral arteries give rise to central arteries(Figs. 4.6, 4.8, 4.12), which enter the brain in theanterior perforated substance (Fig. 3.4). Togetherwith branches from the posterior communicatingartery, they supply the basal ganglia, the internalcapsule and the thalamus. The middle cerebral ar-tery enters the sulcus lateralis. Just before thispoint it emits the anterior choroidal artery, whichalso supplies a branch to the globus pallidus(Fig. 4.8). At the surface of the insula the middlecerebral artery branches into anterior, middleand posterior trunks. The branches of the middlecerebral artery loop over the opercula and ramifyover the surface of the cerebral hemisphere tosupply the cerebral cortex and the adjacent whitematter (Figs. 4.3, 4.4). The anterior cerebral arteryenters the longitudinal fissure to branch on themedial aspect of the hemisphere. The anteriorcommunicating artery, which connects the twoanterior cerebral arteries, is located immediatelyrostral to the optic chiasm (Fig. 4.2).
The vertebral arteries enter the skull throughthe foramen magnum. They give rise to the ante-rior spinal artery, which descends in the anteriormedian fissure of the cord, and emit the posteri-
or inferior cerebellar arteries. The vertebral ar-teries unite into the basilar artery at the ventralaspect of the brain stem. The basilar artery givesorigin to the anterior inferior and superior cere-bellar arteries and splits into the posterior cere-bral arteries. The oculomotor nerve emerges be-tween the superior cerebellar and the posteriorcerebral arteries and thus marks the bifurcationof the basilar artery (Fig. 4.11). The posteriorcerebellar artery makes a characteristic, cau-dally directed curve before it reaches the cere-bellum. Both the posterior inferior and superiorcerebellar arteries contribute branches to thedorsolateral brain stem.
The posterior cerebral artery supplies themedial aspect of the temporal and occipitallobes. The border region of the vascularizationterritories of the posterior and middle cerebralarteries include the temporal and occipitalpoles. The latter contains the posterior portionof the primary visual (striate) cortex with therepresentation of the fovea. Occlusion of theposterior cerebral artery thus leads to loss ofperipheral vision, with maintained central vi-sion (“tunnel vision”) (Table 4.1). The bordersof the arterial territories of the cerebral hemi-sphere do not correspond to the borders of thethe four major lobes distinguished in the grossanatomy of the cerebral hemipheres (Fig. 4.7).Asymmetries of the brain’s arterial system arefrequently observed, most often in the calibreof the vertebral, the posterior cerebral and theposterior communicating arteries.
The vertebral, basilar and posterior cerebralarteries also give rise to smaller branches,which enter the brain stem in the median sul-cus and more laterally (Fig. 4.11). Branchesfrom the basilar and posterior cerebral arteries(Fig. 4.18) enter the mesencephalon in the pos-terior perforated substance, located in the floorof the interpeduncular fossa (Fig. 3.12). Thevascularization territories of these arteries havebeen thoroughly studied by Duvernoy [12].These territories are illustrated in a number oftransverse sections in which both arterial sup-ply and venous drainage are visualized (Figs.4.18–4.20). These figures also document theimportant contributions of the cerebellar arte-ries to the vascularization of the brain stem.
102 Section I Orientation, Development, Gross Anatomy, Blood Supply and Meninges
Fig. 4.7. Cortical territories of the three cerebral arteries; semidiagrammatic lateral and medial views of theleft cerebral hemisphere (2/3 �). The territories correspond to the vascularization pattern illustrated in Figs.4.2–4.4. Stippled areas: sites of possible cerebrocerebral arterial anastomoses, mostly according to Gillilan[13]
4 Blood Supply, Meninges and Cerebrospinal Fluid Circulation 103
Fig. 4.8. The central arteries from the carotid and vertebral system in a frontal view (1/1 �). Substrate basedon a reconstruction. The frontal section is perpendicular to the horizontal plane of Frankfurt, passingthrough the centre of the insula. The central arteries have been derived from different sources
1 Caudate nucleus2 Putamen3 Globus pallidus, external segment4 Globus pallidus, internal segment5 Thalamus6 Anterior perforated substance7 Anterolateral central arteries, lateral branches8 Anterolateral central arteries, medial branches9 Long central artery (Heubner [16])
10 Anteromedial central arteries11 Anterior cerebral artery12 Posterior perforated substance13 Middle cerebral artery, sphenoid part14 Superior hypophyseal artery15 Inferior hypophyseal artery16 Internal carotid artery, cerebral part
17 Internal carotid artery, cavernous part18 Internal carotid artery, petrous part19 Internal carotid artery, cervical part20 Medial nucleus of the thalamus21 Midline nuclei of the thalamus22 Anterior nucleus of the thalamus23 Globus pallidus, internal segment24 Tail of the caudate nucleus25 Anterior choroidal artery26 Subthalamus with posteromedial central arteries27 Hypothalamus with hypothalamic branch28 Amygdaloid nucleus29 Posterior cerebral artery30 Posterior communicating artery31 Basilar artery32 Vertebral artery
104 Section I Orientation, Development, Gross Anatomy, Blood Supply and Meninges
Fig. 4.9. Orthogonal frontal projection of the cerebral and cerebellar arteries in situ, together with some bonylandmarks and the lateral ventricles (2/3 �). The projection was made parallel to the horizontal plane ofFrankfurt by using a graphical reconstruction from the frontal slices of one specimen, and by cross-referencewith Fig. 4.10. In this figure and the next, ample use has been made of indications by Thijssen [29]. Mostvessels are illustrated only in one half of the skull; the vertebral artery is shown bilaterally. OH, Upper hori-zontal plane (Krönlein): tangential to supraorbital margin; FH, Horizontal plane of Frankfurt (Reid): tangen-tial to infraorbital margin; double arrow, sulcus lateralis; single arrow: foramen magnum
occipital branch3 Trunk of the corpus callosum4 Lateral ventricle5 Insula6 Medial occipital artery7 Superior cerebellar artery, medial branch8 Lateral occipital artery9 Free margin of the lesser wing of the sphenoid
bone10 Middle meningeal artery, intraosseous part (in-
constant)11 Middle meningeal artery, frontal branch12 Middle meningeal artery, parietal branch13 Superior margin of petrous part of the temporal
Fig. 4.10. Orthogonal lateral projection of the cerebral and cerebellar arteries, together with external and bonylandmarks, in a schematized composition of data from different specimens and publications (2/3 �). Some neu-ral structures are also illustrated in their outlines: the left hemisphere, cerebellum, left insula, corpus callosumand ventricular system. Within the outlines of the orbita the bulbus oculi and the optic nerve are indicated. Onthe outer side of the figure a number of reference lines are added. In the centre, two lines tangential to the ante-rior (AC) and posterior (PC) commissures can be seen: the one passing above the AC and beneath the PC is partof the bicommissural line of Talairach [27] (BC); the other tangent is part of the upper horizontal line of Krön-lein (OH); CM, canthus-meatus line; FH, horizontal line or plane of Frankfurt (Reid); GI, glabella–inion line;VCA, vertical tangential to anterior commissure; VCP, vertical tangential to posterior commissure
1 Central sulcus2 Pericallosal artery3 Callosomarginal artery4 Corpus callosum5 Outline of ventricles6 Outline of insula7 Anterior cerebral artery8 Middle cerebral artery, frontal
part24 Ektocanthion (Canthus externus)25 Glabella26 Orbital (on infraorbital margin)27 Internal carotid artery, petrous part28 Basilar artery29 Superior margin of petrous part of
the temporal bone30 Anterior inferior cerebellar artery
4 Blood Supply, Meninges and Cerebrospinal Fluid Circulation 107
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108 Section I Orientation, Development, Gross Anatomy, Blood Supply and Meninges
Fig.
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Fig. 4.13. Collateral circulation in the venous system of the head; semidiagrammatic lateral view (2/3 �). Un-paired sinuses in the median plane are drawn without outlines; the extracranial veins draining into the inter-nal and external jugular veins are in black; between the intravertebral venous plexuses a fragment of thespinal medulla can be seen. The arrows indicate the continuity of the superficial temporal veins
1 Diploic veins2 Superior sagittal sinus3 Superior cerebral veins4 Parietal emissary vein5 Superficial temporal veins
(parietal branch)6 Superior anastomotic vein (Trolard [30])7 Inferior sagittal sinus8 Superior thalamostriate vein9 Superior choroidal vein
The existence of a collateral circulation is ofgreat significance for the vascularization of theCNS. There are different types and differentsites of anastomoses; moreover, the diameter ofthese anastomoses may differ considerably.Anastomoses between arteries can be found inrelation to three arterial systems, i.e. betweenthe two main arterial systems of the carotidand vertebral arteries and between the arterialsystems of the brain and the external carotidartery.
Apart from the main arterial anastomosisbetween the systems of the internal carotidand the vertebral-basilar arterial system in thearterial circle of Willis, cerebro-cerebral anas-tomoses are present between the branches ofthe middle cerebral artery (Figs. 4.2, 4.14).Anastomoses between the cerebellar arteriesare documented in Figs. 4.9 and 4.11.
Anastomoses with the external carotid ar-tery occur both with meningeal and extracra-nial branches of this artery. Four types ofanastomoses with branches of the external car-otid artery are indicated with asterisks inFig. 4.1. Orbital anastomoses with branches ofthe ophthalmic artery are enumerated as twospecial categories.
The brain is completely enclosed by three con-nective tissue layers: the meninges. These are,starting from the brain’s surface, the pia mater,the arachnoid and the dura mater. The dura isalso known as the pachymeninx, due to itsstrength and thickness, which is imparted bymultiple layers of collagen tissue. The thin andloose tissue of the pia mater and the arachnoidis collectively known as the leptomeninx.
The cranial dura is merged with the perios-teum of the inner table of the skull. As a con-sequence, the dura is firmly attached to theskull, especially at the sites of the sutures. Dur-al septa are located between the main divisionsof the brain. In the midline, the falx cerebri islocated between the cerebral hemispheres andthe tentorium cerebelli extends between the oc-cipital and temporal lobes of the hemisphereand the cerebellum. Venous sinuses occupy theinner and outer margins of the falx (superiorand inferior sagittal sinus), the junction of thefalx and the tentorium (straight sinus, or sinusrectus), and the attachment of the tentorium tothe skull transverse sinus and superior petrosalsinus (Figs. 4.14–4.16). The pia mater closelycovers the surface of the brain and intrudesinto its sulci and depressions. The arachnoidcovers the brain at a variable distance, thuscreating a subarachnoidal space between thepia and the arachnoid. This space is bridgedby many trabeculae. It contains the CSF. Wid-enings of the subarachnoid space are known asthe cisterns.
For the understanding of the production,circulation and drainage of CSF, the fine struc-ture of the interface of the CSF compartments,the nervous tissue and the mesenchymal tissueof the meninges is important. The central ner-vous system is isolated from the rest of thebody by a series of cellular barriers, whichlimit the flux of hydrophilic molecules betweenthese cells. These barriers generally consist ofextensive tight junctions between the cells,where the outer leaflets of the plasma mem-branes of two opposing cells are fused. Thesebarriers are found in the epithelium of thechoroid plexus (blood-CSF barrier), the outer(barrier) layer of the arachnoid and in the en-dothelium of capillaries located within arach-noid and the pia mater and nervous tissue(blood-brain barrier).
110 Section I Orientation, Development, Gross Anatomy, Blood Supply and Meninges