cranial vessel embryology and imaging anatomycranial vessel embryology and imaging anatomy pedro...

Cranial vessel embryologyand imaging anatomy

Pedro Vilela

ContentsConcepts in Vessel Development: Vasculogenesis, Angiogenesis, Arteriogenesis,

and Intracranial Arterial and Venous Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3Vasculogenesis, Angiogenesis, Arteriogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3Intracranial Arterial Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5Intracranial Venous Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11Metameric (Segmental) Vascular Syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

Intracranial Arterial Anatomy: Anterior and Posterior Arterial Circulation . . . . . 13Anterior Circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Internal Carotid Artery Segment (ICA) – Intradural Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Anterior Choroidal Artery (AChA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16Anterior Cerebral Artery (ACA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16Middle Cerebral Artery (MCA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18Posterior Circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22Vertebral and Basilar Arteries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23Posterior Communicating Artery (PCommA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24Posterior Cerebral Artery (PCA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24Cerebellar Arteries: SCA, AICA, PICA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25Superior Cerebellar Artery (SCA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26Anterior-Inferior Cerebellar Artery (AICA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26Posterior-Inferior Cerebellar Artery (PICA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27Variant Anatomy of Willis Circle and Other Intracranial Vessels . . . . . . . . . . . . . . . . . . . . . . . 28Intracranial Venous Anatomy and Variability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

This publication is endorsed by: European Society ofNeuroradiology (www.esnr.org).

P. Vilela (*)Hospital Beatriz Ângelo, Loures – Lisbon, Portugal

Hospital da Luz, Lisbon, Portugal

Hospital Garcia de Orta, Almada, Portugale-mail: [email protected]

© Springer Nature Switzerland AG 2019F. Barkhof et al. (eds.), Clinical Neuroradiology,https://doi.org/10.1007/978-3-319-61423-6_20-1

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Intracranial Venous Variability and Anomalies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36

Collateral Circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42

AbstractThe brain vascularization is extremely complexwith a large range of possible vascular variants,providing for each individual an exclusive arte-rial and venous system configuration.

The overview of the arterial and venous brainvascular development presented is essential forthe understanding of some vascular dispositions,such as the persistence of embryonic vessels/vascular patterns and complex vascularmalformations, like the metameric syndromes.

The review of the fundamental aspects ofthe arterial circulation, including the descrip-tion of the anterior and posterior circulation,arterial variants, and territories, provides thebasis for the understanding of the diseaseslater discussed in other chapters.

The intracranial venous system is also over-viewed, encompassing the dural sinus anatomy,the supratentorial and infratentorial superficialand deep venous anatomy, and the venous anas-tomosis. The development venous anomaliesand sinus pericrannii are also discussed.

Radiology has contributed tremendously forthe recent advances in brain vascular anatomyknowledge using the acquisition of high-resolution 3D DSA images and supraselectivecatheterization during endovascular procedures.Clinical neuroradiology plays a major role forthe evaluation of brain vascular anatomy that isessential for the diagnosis and treatment (surgi-cal or endovascular) of vascular diseases.

KeywordsVasculogenesis · Angiogenesis ·Arteriogenesis · Arterial development · Venousdevelopment · Vascular · Anatomy · Internalcarotid artery(ies) · Vertebral artery(ies) ·Basilar artery · Anterior cerebral artery(ies) ·Posterior cerebral artery(ies) · Middle cerebralartery(ies) · Anterior-inferior cerebellar artery

(ies) · Posterior-inferior cerebellar artery(ies) ·Superior cerebellar artery(ies) · Cerebellarveins · Cortical veins · Vein of Galen · Venoussinus(es)

List of AbbreviationsAA Aortic archACA Anterior cerebral artery(ies)AChA Anterior choroidal artery(ies)ACommA Anterior communicating arteryAICA Anterior-inferior Cerebellar artery

(ies)Ang-1 Angiopoietin-1AV Arterio-venousAVM Arterio-venous malformationBA Basilar arterybFGF Basic fibroblast growth factorCAMS Cerebrofacial arteriovenous

metameric syndromesCMS Cerebrofacial metameric

syndromesCoW Circle of WillisCT Computed tomographyCTV computed tomography venogramCVMS Cerebrofacial venous metameric

syndromesDSA Digital subtraction angiogramDVA Development venous anomaliesECA External carotid artery(ies)ICA Internal carotid Artery(ies)LPChA Lateral posterior choroidal artery

(ies)MCA Middle cerebral artery(ies)MIP Maximum intensity projectionMPChA Medial posterior choroidal artery

(ies)MRV Magnetic resonance venogramPCA Posterior cerebral artery(ies)PChA Posterior choroidal artery(ies)PCommA Posterior communicating artery

(ies)

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PDGF Platelet derived growth factorPHACES Posterior cranial fossa

malformations, hemangiomas,arterial anomalies, coarctation ofthe aorta and cardiac defects, andabnormalities of the Eye

PICA Posterior-inferior cerebellar artery(ies)

SAMS Spinal arteriovenous metamericsyndromes

SCA Superior cerebellar artery(ies)SMCs Smooth muscle cellsSP Sinus pericraniiSWI Susceptibility weighted imageTA Trigeminal artery(ies)TOF Time of flightVEGF Vascular endothelial growth

factor

Concepts in Vessel Development:Vasculogenesis, Angiogenesis,Arteriogenesis, and IntracranialArterial and Venous Development

Vasculogenesis, Angiogenesis,Arteriogenesis

Vascular development is a complex and dynamicprocess starting at a very early phase of theembryo development, shortly after gastrulation(early embryonic development to a double-wallstage). Several biological processes intervene,such as precursor cell migration to the targetorgans, de novo formation of primitive vesselchannels (vasculogenesis), shaping of these prim-itive new vessels channels (angiogenesis). Anintricate signaling pathway, mainly guided byvascular growth factors, such as vascular endothe-lial growth factor (VEGF) for vasculogenesis,basic fibroblast growth factor (bFGF) and VEGFfor angiogenesis, and platelet derived growth fac-tor (PDGF) plus angiopoietin-1 (Ang-1) for vesselstabilization. These factors are produced inresponse to genetic, systemic, and local (targetorgan) factors and are responsible for regulationof the vessel development. Local hypoxia is animportant stimulus for the release of these

angiogenic factors during these phases (Milner2014; Ribatti 2015).

Blood vessels walls are composed of two maincell types, the endothelial cells and mural cells.Endothelial cells are the chief cell type for devel-opment and remodeling of the vascular system.Multiple layers of smooth muscle cells and anouter layer of pericytes compose the vessel wallof arteries and veins. Pericytes have two majorfunctions: structural, supporting the blood ves-sels, and functional, forming with the endothelialcells the blood –brain barrier (Milner 2014;Ribatti 2015).

These cells have different embryologicalorigins. The blood vessel endothelial cells origi-nate from the mesoderm and the vessel mediacomponents from the neural crest. The mesenchy-mal stem cells (mesoderm) differentiate intoangioblasts and hemangioblasts, which are pre-cursors of endothelial cells and hematopoieticcells, respectively. The neural crest also givesrise to the skin, connective tissue, skeleton of thecraniofacial region, and meninges (Milner 2014;Ribatti 2015).

Endothelial cells can initiate the vasculardevelopment process but are not sufficient to com-plete this process alone. The mural cells, espe-cially the pericytes, the extracellular vessel wallmatrix, and elastic membranes, are important forthe vessel stabilization. Pericytes contribute forvessel stabilization by inhibiting endothelial pro-liferation and migration, and by stimulating pro-duction of extracellular matrix (Milner 2014;Ribatti 2015).

Blood vessel development includes the forma-tion of new vessels from cellular precursors(vasculogenesis), and the growth and remodelingof the primitive vessel network into a complexvascular network (angiogenesis). The angioblastsmigrate into the developing target organs, prolifer-ate, and differentiate into endothelial cells, formingthe initial blood vessels (vasculogenesis). Subse-quently, the other vascular cells (the mural cells),such as pericytes, fibroblasts, mesenchymal cells,and smooth muscle cells, are recruited in responseto growth factors released by the endothelial cells(Milner 2014; Ribatti 2015).

Cranial vessel embryology and imaging anatomy 3

Vasculogenesis occurs at an initial stageof vascular development and is responsible forthe emergence of the blood vascular system.This biological process is responsible for theblood vessels de novo formation from migratingangioblasts. The angioblasts will proliferate anddifferentiate into endothelial cells, forming cordsof cells and a primitive network of vascular chan-nels (Milner 2014; Ribatti 2015).

Vasculogenesis will produce an immature andpoorly functional vasculature. After vasculogenesis,several vascularmaturationmechanisms occur, suchas vascular branching, pruning, remodeling occurcontinuously, in response to local organ develop-ment, producing mature and stable vessels (Milner2014; Ribatti 2015).

Angiogenesis always follows vasculogenesis,being the biological process of growth andreshaping of the primitive network of vascularchannels formed during vasculogenesis. Inarteriogenesis, there is collateral artery growththrough the outgrowth of pre-existent collateralarterioles, requiring proliferation of endothelialcells and smooth muscle cells (SMCs), in theirdiameter to compensate for changes/disturbancesin blood flow. It may occur postnatal in physio-logical processes like wound healing and femalereproductive cycle, or in a variety of pathologicalprocesses, such as diabetic retinopathy or tumor(neo) angiogenesis (Milner 2014; Ribatti 2015).

Two different angiogenesis processes are gen-erally described: sprouting (new vessels formedby the ramification and growth of pre-existing)and intussusception or non-sprouting (splittingof one pre-existing vessel into other vessels)angiogenesis. Sprouting angiogenesis is essentialfor brain vascular network, like in other ectoder-mal organs (Milner 2014; Ribatti 2015).

In sprouting angiogenesis, group of migratorycells, located at the tip of the primitive vessel,extends with the formation (“sprouting”) of newvessels. This vessel expansion may also accom-modate the incorporation of newer migratingangioblasts. Non-sprouting angiogenesis mecha-nisms, such as intussuscepted microvasculargrowth, in which there is the insertion of intersti-tial cell columns into pre-existing vessels, createvascular partitions (Milner 2014; Ribatti 2015).

It seems that shear stress is the main force toinitiate arteriogenesis, in opposition to angiogen-esis in which hypoxia is a leading stimulus.Hemodynamic forces drive arteriogenesis,namely, increased luminal shear stress inducescapillary expansion without branching and exter-nal stimulus induces vessel sprouting (Milner2014; Ribatti 2015).

After recruitment of mural cells, especiallysmooth muscle cells, mural cells will sprout andmigrate alongside the pre-existing vessels,accordingly to local hemodynamic forces. Arter-ies will be earlier and more extensively coveredwith smooth muscle cells (SMCs) than veins.Simultaneously, the smooth muscle cells differen-tiation is happening and these cells acquire specialproprieties, such as contractility (Milner 2014;Ribatti 2015).

Additionally, significant remodeling of thevessels occur adapting to the blood flow changesof the target organ. Vessel remodeling processesoccurs throughout all development and includesthe growth of new vessels, the regression ofothers and establishing of new vessel networkpatterns. This process appears to be triggeredand mediated by local environmental factorsrather than genetically determined. Hemody-namic forces are also critical for reshaping thevascular networks, such as the type and angles ofvessel branching (Milner 2014; Ribatti 2015).

In the early embryonic phases, there is nodistinction between arteries and veins, which aremorphologically similar. The differentiation is deter-mined at a molecular level; different signalling path-ways stimulate the differentiation into arteries orveins, such as ephrins, i.e., transmembrane ligands.This molecular explanation replaces the previoustheory that hemodynamic forces were ruling theartery/vein differentiation (Milner 2014; Ribatti2015).

Specifically regarding brain vasculature devel-opment, different steps have been identified, themost important being:

• First 2 weeks: The neural tissue receives theiroxygen and nutrients through direct diffusionfrom the amniotic fluid.

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• Between the second and forth week: Develop-ing of the meninx primitive (mesodermal ori-gin structure that is the forerunner of themeninges).

• The meninx primitive comprises a primitiveperineural vascular plexus.

• The vasculogenesis starts with angioblastsmigration into the head creating superficialextracerebral perineural vascular plexus, cov-ering the brain. Several vascular maturationprocesses, such as extramural cell recruitment,vessel remodeling and regression, allow thedevelopment of meninx primitive meningealvessels/plexus.

• These meningeal plexus receive the bloodcoming from the dorsal aortas and drain intothe anterior cardinal veins. The anterior cardi-nal veins are the forerunners of the internaljugular veins. These are two short embryonicveins that, after confluence with the posteriorcardinal veins forming the common cardinalveins, empty into the sinus venosus (forerunnerof the atrium).

• Later, progressive intracerebral vessel sproutingangiogenesis occurs into the deeper neuro-ectodermal tissue towards the subventricularzone. These new vessels are initially locatedaround the ventricles. The primitive choroidplexus result from the invagination of the neu-ral tube, associated with the formation of thechoroidal vessels.

• Subsequently, capillary development occurswith an inside-out order, extending from theventricular surface into the developing whitematter and cortical plate. The brain is suppliedperipherally by the capillary network develop-ing from the meninx primitiva vessels anddeeply through the choroid plexuses.

During all these maturation steps, the brainvascularization (arterial and venous) developmentfollows the metabolic needs of the emerging brainareas (Milner 2014; Ribatti 2015).

Intracranial Arterial Development

The carotid arterial system originates from thematuration of the aortic arches, also known asbrachial/pharyngeal arches. From the aortic sacarise a pair of ventral aortas that communicatewith the ipsilateral dorsal aorta through sixpaired aortic arches. The aortic are present simul-taneously and they have complex developmentchanges, including complete regression.

The first aortic arch (AA) is present at the1.3 mm stage and successively; from cranial tocaudal, the other aortic arches will develop (sec-ond AA at 3–4 mm; third and fourth AA at 4 mm;sixth AA at 5–7 mm stages). The fifth AA is notdiscussed in this chapter, since its existence, as aseparate structure, and development is subject toon going controversy. Therefore, the aortic archsystem is present from a very early stage (1.3 mm)until the 28 mm stage with regression of the sixthAA. A post-aortic arch phase with continuousremodeling of these arteries originates the defini-tive aortic arch, pulmonary, carotid, and subcla-vian arteries (Lasjaunias et al. 2001; Raybaud2010).

The sequential arterial developments include(Fig. 1a–c):

• Dorsal aorta:– The pair of two arteries – dorsal aortas –

present at the 4 mm stage will fuse into asingle channel – aorta – at the 10 mm stage.

– The dorsal aorta between the III and IVAA(ductus caroticus) regresses.

• 6th AA: Originates the pulmonary arteries.• 5th AA: Regresses completely.• 4th AA: The left 4th AA originates the aortic

arch in association with the ventral aorta, andthe right 4th AA forms the proximal subclavianartery.

• 3th AA: Proximal 3rd AA originates the com-mon carotid artery, and the distal third AAsegment together with the near dorsal aortaoriginate the internal carotid artery.

• 2nd AA: The regression of the 2st AA origi-nates the hyoid artery (dorsal remnant), thecarotid tympanic artery (ventral remnant), anda segment of the ventral remnant and the


Fig. 1 (continued)

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Fig. 1 (a–d) Schematic representation of the evolution ofthe aortic arches, dorsal and ventral aortas at the head and

neck region, and the correspondent arteries that originatefrom these embryonic vessels. (a) At the cranial end of the


ventral aorta originate the ventral-pharyngealartery.

• 1st AA: The regression of the 1st AA origi-nates the supraorbital artery (dorsal remnant)and the mandibular artery (ventral remnant).

The external carotid artery embryonic devel-opment will not be addressed in this section, butthe main external carotid artery branches progressfrom the following primitive arterial systems(Fig. 1e):

• The hyoid artery derived from the 2nd AAwillgenerate the internal maxillary artery system.

• The ventral pharyngeal artery, originatingmainly from the regressed ventral aorta willcreate the thyroid-facial-lingual artery system.

• The carotid-vertebro-basilar anastomosis (hypo-glossal, proatlantal I and II) will originate theascending pharyngeal-occipital artery system.

The internal carotid arteries (ICA) emerge atthe 3 mm embryo stage resulting from the fusionof the 3rd AA and distal dorsal aorta. The distalembryonic ICA bifurcation occurs at the level ofthe posterior communicating artery and becomesevident at the 4 mm stage with the development of

the anterior and posterior division (Lasjauniaset al. 2001; Raybaud 2010).

• The anterior (rostral) division: Includes theanterior cerebral artery and the anterior choroi-dal artery (and later the middle cerebral artery)

• The posterior (caudal) division: Includes theposterior communicating, posterior cerebralartery, superior cerebellar, and the posteriorchoroidal arteries

Initially, the anterior division is mainly respon-sible for the arterial supply of the optic and olfac-tory areas. Two major branches are identified: themedial olfactory artery, the forerunner of the ante-rior cerebral artery, and the lateral olfactory artery,which provides the striate (which originateHeubner artery and MCA) and posterior telence-phalic (which will originate the anterior choroidalartery) arteries (Lasjaunias et al. 2001; Raybaud2010).

The anterior cerebral artery originates frommedial olfactory artery is the oldest cerebral cor-tical artery. The middle cerebral artery (MCA) is arecent phylogenetic acquisition resulting from theneed to supply a large cortical territory of progres-sive enlarging brain. At the 11–12 mm embryo-logical stage, it is possible to identify the MCA

��

Fig. 1 (continued) dorsal aorta is represented the embry-onic internal carotid artery division: caudal division –PComA (posterior communicating artery); and anteriordivision – ACA (anterior cerebral artery). Dorsal ophthal-mic artery; primitive maxillary artery; I-IV AA – aorticarches representation. The adult ophthalmic artery is theresult of the maturation of three embryonic arteries: theventral ophthalmic (originating from the ACA), the dorsalophthalmic originating from the cavernous ICA segment(corresponding to the ILT), and the most common config-uration in which the ophthalmic artery originates from the6th ICA segment. (b) The dorsal ophthalmic artery willoriginate the inferolateral trunk (ILT). The primitive max-illary artery will originate the inferior and posterior hypo-physeal artery. I aortic arch originate the mandibular arteryand the supraorbital artery. II aortic arch originates carotidtympanic artery and the hyoid/stapedial arteries. The IIIaortic arch corresponds to the level of the carotid bulb. TheIVaortic arch originates the adult aortic arch. (c, d) Internalcarotid artery (1–7) embryonic segments (yellow) divided

by the landmarks of the origin of embryonic arteries. CCA– common carotid artery (blue) and ECA – external carotidartery origins (green). The hyoid/stapedial system givesrise to the middle meningeal (MMA), accessory meningeal(AMA), and internal maxillary (IMAX) arteries. The thy-roid-facial-lingual artery system (superior thyroid, lingual,and facial arteries) derives from the ventral pharyngealartery (VPA) originating from the ventral aorta. Note:Although it is classically described that ITL is the forerun-ner of the primitive dorsal ophthalmic artery, and that anophthalmic artery arising from ICA cavernous segment isnamed “dorsal ophthalmic artery” (variant), it is probablymore precise to accept that the branch giving rise to the ILTis the primitive maxillary artery. The ophthalmic arterywould be the result of the contribution of several embry-onic arteries, namely: primitive maxillary artery from ICAcavernous segment, primitive dorsal and ventral ophthal-mic arteries arising from the supraclinoid ICA segment,and stapedial artery and primitive olfactory artery fromACA

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origin from the proximal anterior division of theICA (i.e., MCA corresponds to an dominant –primitive – ACA perforator that annexes corticalterritory). Initially, the “MCA” has a plexiformstructure that will progressively fuse into a singlechannel at the 18 mm stage (Lasjaunias et al.2001; Raybaud 2010).

The posterior division of the ICA will beresponsible for the arterial supply of the occipitallobe and cerebellum through the posterior cerebraland superior cerebellar arteries and will fuse withthe primitive vertebro-basilar system (originatingfrom the parallel longitudinal neural channels).

The circle of Wills is formed at the 6–7 weeksembryological stage with the development of theanterior communicating artery and “basilar tip”maturation (Lasjaunias et al. 2001; Raybaud2010).

• The anterior communicating artery resultsfrom the medial extension of the anterior cere-bral arteries, with a plexiform arterial structurethat fuses at the midline at the 21–24mm stage.

• The maturation of the posterior division of theICA includes the cranio-caudal fusion with thebasilar artery segment (originating from thelongitudinal neural arteries), and midlinefusion forming the distal end of the basilarartery (“basilar tip”).

At an early stage (4–5 mm embryo), there aretwo parallel longitudinal neural channels corre-sponding to the cranial extension of the metamericarterial supply of the spine and spinal cord. Fromthese parallel neural arterial channels arise several(transversal) segmental arteries (such as C1 orproatlantal 1 and C2 or proatlantal 2 arteries) thathave a metameric distribution and follow theperipheral/cranial nerves (Lasjaunias et al. 2001;Raybaud 2010).

The hindbrain arterial supply is, initially andtransiently, dependent of the carotid system,which comes from the transient carotid-vertebro-basilar (ventral-dorsal) anastomoses. Theseembryonic arterial anastomoses develop at a5 mm or earlier embryo stage starting their invo-lution at the 7–12 mm embryo stage. With theprogressive enlargement of the posterior fossa

structures, the carotid system becomes insuffi-cient to provide adequate blood supply, and theposterior circulation system development is trig-gered. The carotid-vertebro-basilar (ventral-dorsal)anastomoses regression is inversely parallel to thedevelopment of the posterior circulation. If theypersist, the proximal posterior circulation will beproportionally underdeveloped (hypoplastic). Thelife span of these anastomoses is extremely short,around 1 week, and complete regression occurswhen the posterior communicating artery con-nects with the basilar artery segment arisingfrom the ventral longitudinal neural arteries(Lasjaunias et al. 2001; Raybaud 2010).

The basilar artery is formed at an early stage(5–6 mm) by a complex process characterized bydouble fusion: midline fusion between the twoparallel neural arterial channels; and a cranial-caudal fusion between the caudal ICA divisionand the midline fused parallel neural channels. Itis classically accepted that the cranial-caudalfusion area corresponds to the level of the trigem-inal artery (Lasjaunias et al. 2001; Raybaud2010).

The vertebral arteries are originated from theintersegment arterial anastomosis between thecervical segmental arteries that occurs during the7–12 mm stages, extending in a cranial-caudalfashion from the proatlantal system to the 6thcervical segmental artery (Lasjaunias et al. 2001;Raybaud 2010).

The cerebellar arteries originate from the pos-terior/caudal ICA division (Superior CerebellarArtery – SCA) and from the development of thetwo parallel neural arterial channels (Anterior-inferior Cerebellar arteries – AICA andPosterior-inferior Cerebellar arteries – PICA). Inanalogy to the spinal cord arterial anatomy, AICAmay be regarded as a dominant perforator(ventral/radiculo-medullar) that has annexedother territories such cortical cerebellar territoryand PICA may be an analogue to a radiculo-pial(lateral/dorsal) spinal cord artery that has annexedother territories, such as cerebellum and choroidplexus (Lasjaunias et al. 2001; Raybaud 2010).

The carotid-vertebrobasilar anastomoses are:trigeminal artery, hypoglossal artery, proatlantalI and proatlantal II. The optic artery probably doesnot exist and the reported cases may represent a


Fig. 2 (a, b) Carotid-vertebrobasilar anastomoses. (a)DSA lateral view after the right ICA contrast injectionillustrates the presence of a trigeminal artery (TA) arisingfrom the cavernous segment of the internal carotid artery(ICA) (caudal to the origin of the posterior communicating

(PCommA)) and anterior choroidal artery (AChA) alsoseen in the angiogram. (b) 3D TOF VR and MIP imagesand fused high-resolution axial T2 and 3D TOF MRAshowing hypoglossal artery persistence and the course ofthis artery at the hypoglossal canal

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low (caudal) origin of the trigeminal artery(Fig. 2) (Lasjaunias et al. 2001; Raybaud 2010).

The trigeminal artery follows the V cranialnerve route, being responsible for its arterialblood supply. The persistent trigeminal artery isthe most common carotid-vertebro-basilar anasto-moses persistence with a prevalence of 0.1–0.6%approximately (Lasjaunias et al. 2001; Raybaud2010).

The trigeminal arteries (TA) are generally sub-divided into (Saltzman Classification):

• Type 1 – TA joins the BA between the superiorcerebellar artery (SCA) and the anterior infe-rior cerebellar artery (AICA), the caudal seg-ment of the BA can be hypoplastic.

• Type 2 – TA joins the BA above the origin ofthe SCA, and it supplies most of the flow to theSCA. Usually accompanied by normalPCOMM supplying most of the PCA flow.

• Type 3 – TA supply one of the cerebellar arter-ies (“persistent TAvariant”) bypassing the BA,was firstly described for SCA.

The Saltzman classification revision, sub-divided the type 3 into:

• Type 3a – ICA gives rise to SCA• Type 3b (the most common) – ICA gives rise to

AICA• Type 3c – ICA gives rise to PICA

The hypoglossal artery is the forerunner ofascending pharyngeal artery. It is a metamericartery that follows the course of the hypoglossalnerve, being responsible for its arterial blood sup-ply. The persistent primitive hypoglossal arteryoriginates at the cervical ICA, ascends parallel tothe cervical ICA and enters the cranial cavitythrough the hypoglossal canal anastomosingwith the caudal basilar artery segment (Lasjauniaset al. 2001; Raybaud 2010).

The proatlantal arteries correspond to the firstcervical (C1) and second (C2) segmental andmetameric cervical arteries. They follow theroute of the C1 and C2 cervical nerves, respec-tively. The regression originates the C1 and C2occipital and vertebral arteries branches. The per-sistence of proatlantal arteries is better classified

accordingly to the route at the craniovertebraljunction rather than from the ECA/ICA origin(Lasjaunias et al. 2001; Raybaud 2010).

• The type 1 proatlantal artery is the commonestproatlantal artery type, corresponding toapproximately 60% of cases. It originatesfrom the proximal ICA or ECA, ascends post-erolaterally to the ICA and passes through theforamen magnum to join the ipsilateral intra-cranial vertebral artery.

• The type 2 proatlantal artery originates fromthe ECA, ascends posterolaterally to the ICA,passes through the transverse foramen of C1vertebra to join the ipsilateral extracranial ver-tebral artery below the C1.

In the spine vascular metameric organization,each segmental artery receives the name of thenerve that it is following and supplies the peripheralnervous system (peripheral nerve), which is derivedfrom the neural crest; the central nervous system(myelomere), which is derived from the neuraltube; and the somite that has a mesodermic originand is composed by dermis (dermatome), muscle(myotome), and bone (sclerotome). At the head,face, and cranio-vertebral junction areas, a similarmetameric organization is present, which explainsthe phenotype appearance of the segmental vascu-lar syndromes, which will be discussed later(Lasjaunias et al. 2001; Raybaud 2010).

Intracranial Venous Development

The venous drainage is composed of deep medul-lary and dorsal nuclear veins draining into thesubependymal venous system and cortical medul-lary veins and ventral nuclear veins draining intothe leptomeningeal venous system. There are alsotranscerebral/transmedullary veins anastomosisbetween the two systems (Lasjaunias et al. 2001;Raybaud 2010).

At the 4 mm embryo stage, it is possible toidentify the earliest precursor of the intracranialvenous system, a unique middle line located vein,Vena Capitis Medialis (or primary head vein).Afterwards, this vein will split into two major


veins, which migrate laterally forming the primi-tive cranial sinuses (Lasjaunias et al. 2001;Raybaud 2010).

In the initial phases, during the weeks 6 to8 (10–26 mm stage), the choroidal plexuses, theforerunner of the subependymal venous system,are formed. These plexuses are supplied by theACA, AChA, and PChA and drain into dorsalchoroidal veins that drain into a major venouscollector, the Markowski’s vein (also deno-minated “primary internal cerebral vein” and“median prosencephalic vein”). This is a singlevein, median and dorsal prosencephalic vein, thatdrains exclusively the blood from the choroidplexuses. The Markowski’s vein appears at week6 and regresses after the week 11, when the sub-ependymal venous system, internal cerebral veinsand the Galen vein have developed. The persis-tence of Markowski’s vein is seen in associationwith Vein of Galen Aneurysmal Malformation.

At the 14 mm embryo stage, there are threemajor meningeal plexus (anterior, middle, andposterior) covering the developing brain andcollecting their blood into the primitive cranialsinuses. These venous plexuses are in close rela-tionship with the developing forebrain – prosen-cephalon (anterior venous plexus), midbrain –mesencephalon (middle venous plexus), andhindbrain – rhomboencephalon (posterior venousplexus). The primitive cranial sinuses drain theirblood into the anterior cardinal vein, which is theforerunner of the internal jugular vein.

Between the 14 mm and 40 mm embryo stage,several venous developments occur: some primi-tive cranial sinuses regress to become the tentorialsinuses; the venous anastomosis (venous stalk)between the anterior and middle venous plexuswill become the transverse sinuses, and thevenous anastomosis (venous stalk) between mid-dle and posterior venous plexuses will originatethe sigmoid sinus. Additionally, between 24 and40 mm embryo stage, there will be a middle linefusion of the venous plexus originating the supe-rior sagittal sinus.

From the 3 months of fetal age (60–80 mm)until the postnatal development, the dural sinusessuffer significant remodeling processes. Trans-verse sinuses increase in diameter until of the

6 months of fetal age, acquiring a balloon shape.Then, after 7 months (fetal) until 2 years after birth(postnatal), they will decrease in diameter. Addi-tionally, sigmoid sinuses will increase in diameteruntil the age of 2 years (postnatal).

The superior petrosal sinuses are late venousdevelopment acquisitions, occurring at the 80 mmembryo stage, deriving from the metencephalicveins connection with the cavernous sinuses.

The cavernous “sinuses” maturation is animportant biological process since it has implica-tion in intracranial venous drainage. Immediatelyafter birth, all intracranial venous drainagedepends fully on the sigmoid sinuses drainage.The use of the cavernous sinuses for brain venousdrainage (“cavernous sinuses capture”) occursafter birth until the age of 2 years through theconnection of the cavernous “sinuses” with thesuperficial sylvian veins through the spheno-parietal sinuses.

The venous system not fully developed afterdelivery is an important feature of intracranialvenous physiology. The post birth vessel matura-tion in one of the typical particularities of venousdevelopment and includes the cavernous sinusesmaturation (“capture of the cavernous sinus”), theregression in size/disappearance of the occipital–marginal sinuses and the decrease in size of trans-verse sinuses.

Metameric (Segmental) VascularSyndromes

The concepts of tissue embryological origin andprecursor cell (cephalic neural crest and meso-derm cell) migration and differentiation explainsome of the phenotypic appearance of complexvascular syndromes, metameric syndromes. Ifthere is mutation of the neural crest or adjacentcephalic mesoderm before the cellular migration,it is expected to produce metameric malformations,with segmental distribution and different type oftissues involved.

These metameric diseases are defined as Spineand Craniofacial Metameric Syndromes. In thespine, this distribution is transverse, but at headand neck this distribution in less obvious. These

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syndromes may affect one or more metameres andmay be bilateral. The type of vascular phenotypicexpression may target mainly the capillary-venoustree in Cerebrofacial Arteriovenous MetamericSyndromes (CAMS) and Spinal ArteriovenousMetameric Syndromes (SAMS), the veno-lymphatic tree in Cerebrofacial Venous MetamericSyndromes (CVMS) and the arterial-capillary treein PHACES (Posterior cranial fossamalformations,Hemangiomas, Arterial anomalies, Coarctation ofthe aorta and cardiac defects, and abnormalities ofthe Eye) (Lasjaunias et al. 2001, 2006; Raybaud2010).

The spine metameres are divided from 1 to31 corresponding to the myelomeres. Lasjauniaset al. suggested that craniofacial metameres divi-sion into: CMS type 1 with a midline topographicdistribution, medial prosencephalic (olfactory)group, involving the hypothalamus, corpuscallosum, hypophysis, and nose; CMS type2 with lateral topographic distribution, prosence-phalic (optic) group, involving the optic nerve,retina, thalamus, parietal, temporal, and occipitallobes and maxilla; CMS type 3 with caudal distri-bution, rhombencephalic (otic) group, involving ofthe cerebellum, pons, petrous bone, and mandible(Lasjaunias et al. 2001, 2006; Raybaud 2010).

The Cobb’s syndrome (SAMS) is character-ized by multiple vascular malformations (AVM)affecting different tissues of a myelomere,namely, the spinal cord, nerve root, bone, para-spinal space, subcutaneous, and skin.

The Bonnet-Dechaume-Blanc or Wyburn-Mason syndrome (CAMS) presents with multiple,high-flow AVMs having a metameric distributionaffecting the brain, orbit (retinal or retrobulbarlesions), and maxillofacial region (Lasjaunias etal. 2001, 2006; Raybaud 2010).

The Sturge-Weber syndrome is the typical exam-ple of CVMS. It generally affects the first two meta-meres (CVMS 1–2) and is characterized by cortical/pial venous obstructions with collateral venous cir-culation through capillary venous proliferation andenlargement of the transmedullary collateral venousdrainage, with or without choroid plexus hypertro-phy. Other common features include facial “portwine stains,” lymphangiomatous malformation,and facial/skull base bone hypertrophy. Secondary

brain abnormalities, such as gyral calcifications andatrophy, are commonly seen as the result of chronicpial venous occlusion (Lasjaunias et al. 2001, 2006;Raybaud 2010).

The typical finding in PHACES is the pres-ence of a large facial hemangioma. Intracranialhemangiomas are also seen. Intracranial arterialstenoses have been also added to the syndromespectrum. The phenotypic expression of this dis-ease is more complex affecting the arterial-capillary vascular tree and multiple metameres.This causes different types of phenotypic lesionexpression and distinct target lesions, such ashemangiomas and arterial abnormalities andintracranial and thoracic localization. It may beexplained by a larger and longitudinal cephalicneural crest dysfunction (Lasjaunias et al. 2001,2006; Raybaud 2010).

Intracranial Arterial Anatomy: Anteriorand Posterior Arterial Circulation

The intracranial arterial circulation is generallydivided into two major territories: the anterior cir-culation, encompassing the internal carotid arterycirculation (internal carotid (ICA), anterior choroi-dal (AChA), anterior cerebral (ACA), and middlecerebral arteries (MCA), and the posterior circula-tion comprehending the vertebro-basilar system(vertebral arteries, basilar artery, postero-inferiorcerebellar arteries (PICA), antero-superior cerebel-lar arteries (AICA), superior cerebellar arteries(SCA), and posterior cerebral arteries (PCA).

Reminding the embryonic development, theprimitive ICA anterior (cranial) embryonic divi-sion corresponds to the anterior circulation; andthe primitive ICA posterior (caudal) embryonicdivision and the vertebro-basilar system corre-spond to the posterior circulation.

The brain arteries have superficial/corticalbranches that are responsible for the arterial sup-ply of the brain surface and deep/perforatorbranches that supply the brain stem, grey nuclei,and deep white matter.

The superficial/cortical arteries are responsiblefor the supply of the brain surface, including cor-tex and adjacent subcortical white matter. They


have prominent leptomeningeal anastomosis atthe brain surface. Additionally, the supratentorialcortical arteries are connected at the base of thebrain through the circle of Willis.

The ACA, MCA, and PCA are responsible forarterial supply of the cerebrum.

• ACA supplies the medial surface of the frontaland parietal lobes, the inferior surface of thefrontal lobe, the cingulate gyrus, and corpuscallosum.

• MCA supplies the lateral surface of the frontal,parietal, and temporal lobes.

• PCA is responsible for the supply of the tem-poral, occipital, and parietal lobes.

The SCA, AICA, and PICA (cerebellar arter-ies) are responsible for arterial supply of thecerebellum.

• SCA supplies the superior (tentorial) cerebellarsurface.

• AICA supplies the anterior (petrosal) cerebel-lar surface.

• PICA supplies the inferior (occipital) cerebel-lar surface.

The perforators (deep arteries) are responsiblefor the arterial supply of the inner brain structures,namely, the thalamus, basal ganglia, and deepwhite matter, cerebellar nuclei, and the brain stem.

The perforators arising from the anterior circu-lation (ICA, AChA, ACA, ACM) and posteriorcerebral artery (PCA) may be grouped into the:

• Anterior choroidal group, encompassing theICA and AChA perforators

• Striatal group, including the medial and laterallenticulostriate arteries originating from theACA and MCA

• Thalamic group, comprising posterior choroidalarteries, the thalamoperforators, thalamo-geniculate, thalamotuberal arteries arising fromthe posterior communicating artery, PCA, andbasilar tip

The posterior circulation perforators arisingfrom the basilar artery, vertebral arteries, and

cerebellar arteries (SCA, AICA, PICA) areresponsible for the arterial supply of the brainstem (medulla and pons).

Anterior Circulation

The anterior circulation is composed by the inter-nal carotid artery (ICA) system, including theanterior and middle cerebral arteries and the ante-rior choroidal arteries. The posterior communicat-ing artery branches will be discussed togetherwith the posterior cerebral artery anatomy. Theproximal ICA branches, namely, the petrous andcavernous segment branches and the ophthalmicartery are beyond the scope of this chapter.

Internal Carotid Artery Segment (ICA) –Intradural Segment

Different classifications have divided the internalcarotid artery (ICA) into several embryologicaland/or topography segments.

Accordingly, to the embryological develop-ment, Lasjaunias et al. proposed the segmentationof the ICA into seven segments (Lasjaunias et al.2001):

• 1st segment – cervical segment: From thecarotid artery bifurcation into the ICA entranceat the skull base

• 2nd segment – ascending petrous segment:Starts at the carotid foramen and extends tothe origin of the carotico-tympanic artery atthe petrous bone

• 3rd segment – horizontal petrous segment:In-between the origins of the carotico-tympanic artery and vidian/mandibular artery,crossing the carotid canal until the foramenlacerum

• 4th segment – ascending cavernous segment:Extends within the cavernous sinus from theorigins of the vidian/mandibular artery and themeningo-hypophyseal trunk

• 5th segment – horizontal cavernous segment:Extends inside the cavernous sinus from theorigin of the meningo-hypophyseal trunk intothe infero-lateral trunk origin

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• 6th segment – clinoidal segment: Extendsin-between the origins of infero-lateral trunkand ophthalmic artery

• 7th segment – terminal/supraclinoid segment:Extends from ophthalmic artery and anteriorcerebral artery having an intradural course.

A surgical anatomical classification considersfour ICA segments:

• C1 segment (cervical portion): Extending fromthe carotid bifurcation to the skull base

• C2 segment (petrous): Running within thecarotid canal and terminating at the cavernoussinus entrance

• C3 segment (cavernous): Coursing inside thecavernous sinus

• C4 segment (supraclinoid): Corresponding tothe intradural artery segment ending at thebifurcation into the anterior and middle cere-bral arteries

The intradural ICA gives rise to the ophthal-mic, posterior communicating and anterior

Fig. 3 (a, b) Internalcarotid artery (ICA). (a)DSA lateral view after theright ICA contrast injectionillustrates the majorbranches of the supraclinoidICA segment: posteriorcommunicating, anteriorChoroidal (AChA), middlecerebral (MCA), andanterior cerebral arteries(ACA). (b) DSA ap/frontalview after the bilateral ICAcontrast injection illustratesthe proximal branches ofthe supraclinoid ICAsegment and the proximalsegments of ACA andMCA in a patient with ananterior communicatinganeurism (*)


choroidal arteries and has several perforatorbranches (Fig. 3).

The proximal group of perforators, arising nearthe ophthalmic artery, include the superior hypo-physeal arteries (supplying the pituitary stalk andgland) and small branches to the optic chiasm andnerves and the floor of the III ventricle. There is asmall group of perforators originating from thesegment near the posterior communicating arteryorigin supplying the optic chiasm/tract, the floorof the III ventricle and the infundibulum. The ICAsegment near the origin of the anterior choroidalartery has the largest number of perforators andsupply the optic track; the infundibulum and theanterior and posterior perforate substances.

Anterior Choroidal Artery (AChA)

The anterior choroidal artery is one of the oldest(phylogenetic) arteries being of primordial impor-tance for the brain supply during the embryonicchoroidal stage. During embryonic development,AChA supplies a significant cortical (telencephalic)territory that will be later annexed by the posteriorcerebral artery. Therefore, there is an inverse rela-tionship between the sizes of AChA and PCA. Insome rare congenital variants, a large cortical terri-tory may remain under the supply fromAChA, witha concordant posterior cerebral artery hypoplasia(Lasjaunias et al. 2001; Raybaud 2010).

In adults, AChAoriginates from the supraclinoid(intradural) ICA segment distally to the posteriorcommunicating artery origin, at the carotid cistern,runs through the perimesencephalic cistern (cis-ternal segment), enters the choroidal fissure andbranches at the level of the temporal horn choroidplexus (plexal segment) (Lasjaunias et al. 2001;Rhoton 2002c).

The cisternal segment of the AchA suppliesthe optic tracts, cerebral peduncles, posteriorlimb of the internal capsule, globus pallidus, lat-eral geniculate body, and mesial temporal lobe(hippocampus, dentate gyrus, and fornix). Forthese territories, there is a balance between thedeep territory of the AChA and the branchesfrom ICA, PCA, PComA, and MCA. The plexalsegment gives branches to the choroid plexus of

the temporal horn, atrium, and body of the lateralventricles (Lasjaunias et al. 2001; Rhoton 2002c).

Anterior Cerebral Artery (ACA)

The anterior cerebral artery arises from the distalsupraclinoid ICA segment, coursing medially,generally above the optic chiasm and nerves,entering the interhemispheric fissure (Figs. 4aand b).

The anterior cerebral artery is divided into fiveanatomical segments, namely (Rhoton 2002c):

• A1 (precommunicating segment): Correspon-ding to the segment between ICA and AnteriorCommunicating Artery

• A2 (infracallosal segment): Corresponding tothe segment between the rostrum and the genuof the corpus callosum

• A3 (precallosal segment): Corresponding tocurve around the genu of the corpus calosum

• A4 (supracallosal segment): Corresponding tothe segment that follows the superior part ofthe corpus callosum and the “coronal suture”point

• A5 (posterocallosal segment): Correspondingto the segment located distal to the “coronalsuture point”

ACA can exhibit several anatomical variants,specially comprising the A2 segment and the peri-callosal and calloso-marginal arteries, but the dis-tribution of the deep and cortical branches isgenerally constant. Most commonly, the A2 seg-ment gives rise to the orbito-frontal and polarfrontal arteries and at the distal end of the A2segment the ACA divides into: pericallosal arteryand calloso-marginal artery. The sizes of peri-callosal and calloso-marginal arteries are in bal-ance and vary inversely (Lasjaunias et al. 2001;Rhoton 2002c).

The pericallosal artery runs at the corpuscallosum sulcus giving branches to the corpuscallosum and distally originating the precunealartery and small branches at the level of thesplenium of the corpus callosum. The later,

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Fig. 4 (a, b) Anterior cerebral artery. (a) Schematic representation of the ACA branching pattern. (b) Anterior cerebralartery. DSA lateral view after the right ICA contrast injection illustrates the ACA cortical branches


anastomose with the corresponding branches of theposterior cerebral artery (posterior pericallosalartery) (Lasjaunias et al. 2001; Rhoton 2002c).

The calloso-marginal artery courses at the cin-gulate sulcus and giving rise to the medial (ante-rior, middle, and posterior) frontal arteries andparacentral artery (Lasjaunias et al. 2001; Rhoton2002c).

The internal/medial frontal arteries can arisefrom the calloso-marginal artery or from the A2segment (anterior medial frontal artery) and peri-callosal artery (middle medial frontal artery). Theparacentral artery originates from the calloso-marginal artery (Lasjaunias et al. 2001; Rhoton2002c).

Some anatomical variants may occur at thedistal end of the ACA system, being in balancewith the PCA vascularization. ACA at the A4/A5segment of the calloso-marginal may give rise tosuperior (precuneus) and inferior parietal arteriesand inferior callosal artery (Lasjaunias et al. 2001;Rhoton 2002c).

The major ACA cortical branches include:

• Orbito-frontal/medial fronto-basal artery• Polar frontal artery• Medial anterior frontal artery• Medial intermediate frontal artery• Medial posterior frontal artery• Paracentral artery• Parietal arteries: Superior (precuneal) artery;

inferior parietal artery

The deep (perforators) branches from the ACAsystem arise most commonly from the anteriorcommunicating artery and the A1 ACA segment.

Anterior communicating artery: It gives rise tohypothalamic branches, optic nerve/chiasmbranches and the subcallosal artery that supplythe septum pellucidum, paraterminal gyrus, sub-callosal area; anterior commissure; fornix, laminaterminalis (Lasjaunias et al. 2001; Rhoton 2002c).

A1 ACA segment: It gives rise to the mediallenticulostriate arteries. The lateral (initial) half ofthe A1 segment has more perforators than themedial (distal) half. The recurrent artery ofHeubner is the largest ACA perforator, originating

at the A1, Acomm-A1 junction, being responsiblefor the supply of the head of the caudate nucleusand anteroinferior portion of the anterior limb ofthe internal capsule (other supply includes ante-rior third of the putamen, anterior part of theouter segment of the globus pallidus, uncinatefasciculus) (Lasjaunias et al. 2001; Rhoton2002c).

Middle Cerebral Artery (MCA)

MCA is a late embryonic acquisition and thelargest cortical cerebral artery. It is responsiblefor the arterial supply of large cerebral corticaland deep brain territories (Fig. 5a, b, and c).

The middle cerebral artery is divided into fouranatomical segments, namely (Lasjaunias et al.2001; Rhoton 2002c):

• M1 (Sphenoidal segment): Starts at the distalICA segment, extending laterally within theSylvian fissure until the MCA division; smallcortical branches (such as anterior temporalartery) may arise from this segment;

• M2 (Insular segment): This segment includesthe MCA division trunks that lie in front of theinsula and give rise to short cortical branches tothe insula;

• M3 (Opercular segment): Begins at the insulacircular sulcus and ends at the surface of thesylvian fissure and is responsive for the corticalbranches to the operculum;

• M4 (Cortical segment): Corresponds to thecortical branches of the MCA.

There is a wide variation of MCA division anddominance of the MCA trunks, but the corticalarteries distribution is fairly constant. The MCAmay divide into two major trunks (“bifurcation”),the superior and the inferior trunks, of a similarsize (co-dominance). There may be an inferior orsuperior dominance with a larger territory sup-plied by one of the trunks. Other possibilities arethe presence of three major MCA division trunks(“trifurcation”) or multiple (more than three)trunks (Lasjaunias et al. 2001; Rhoton 2002c).

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Fig. 5 (continued)


The major M4 (cortical) branches include(Lasjaunias et al. 2001; Rhoton 2002c):

• Lateral frontobasal/orbitofrontal artery• Prefrontal artery• Precentral (pre-rolandic) artery• Central (rolandic) sulcus artery• Anterior parietal (postcentral sulcus) artery• Posterior parietal artery• Angular artery• Temporooccipital artery• Posterior temporal artery• Intermediate temporal artery• Anterior temporal and temporopolar arteries

The group of lateral frontobasal/orbitofrontalartery, prefrontal artery, precentral (pre-rolandic)artery, and central (rolandic) sulcus artery arisesgenerally from the superior MCA trunk.

The group of temporo-occipital artery, poste-rior temporal artery, intermediate temporal artery,commonly originates from the inferior MCAtrunk (Lasjaunias et al. 2001; Rhoton 2002c).

The anterior temporal and temporo-polar arter-ies can arise from the M1 segment or from theinferior trunk (Lasjaunias et al. 2001; Rhoton2002c).

The origin of the anterior parietal (postcentralsulcus) artery, posterior parietal artery, and angu-lar artery is more variable: Balanced origin from

Fig. 5 (a–c) Middle cerebral artery. (a) Schematic repre-sentation of the MCA branching pattern. (b) DSA lateralview after the right ICA contrast injection (2D image –upper image; 3D MIP image – lower image). (c) Ante-roposterior view after the right ICA contrast injection (2D

image – right image; 3D MIP image – middle and leftimages – show the different MCA segments, the origin ofthe perforators (lenticulostriate arteries) from the M1 seg-ment and the cortical branching pattern

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Fig. 6 (continued)


superior and inferior trunks (co-dominance); ori-gin from one of the trunks (inferior/superior trunkdominance); origin from an individual trunk (“tri-furcation”) (Lasjaunias et al. 2001; Rhoton2002c).

The deep (perforators) branches from theMCAsystem arise mostly (up to 80% of the totalbranches) from the M1/prebifurcation segment.

The perforator branches of the MCA are thelenticulo-striate arteries, which may be sub-divided into (Lasjaunias et al. 2001; Rhoton2002c):

• Medial lenticulo-striate arteries which are aninconstant group of 1 to 5 arteries that may notbe present and originate from the initial M1(prebifurcation) segment.

• Intermediate lenticulostriate arteries originat-ing from the M1 (prebifurcation) segment.

• Lateral lenticulo-striate arteries that are themost constant group, which can arise from theM1 or M2 segments.

Posterior Circulation

The vertebro-basilar system constitutes the poste-rior circulation. The posterior circulation has twoembryonic origins: from the internal carotid artery(ICA) system, comprising the posterior cerebralartery and superior cerebellar artery (originatingfrom the caudal division of the “embryonic”ICA); and from the metameric organized arterialsystem, encompassing the vertebral arteries,PICA, and AICA (Fig. 6a, b, and c) (Lasjauniaset al. 2001).

Fig. 6 (a–c) Vertebral and basilar arteries. (a) DSA ante-roposterior view after right VA (right image) and left VA(left image) contrast injection illustrates the course andbranches of the VAs and BA and the presence of right VAhypoplasia mostly at the V4 segment. (b) DSA lateral viewafter VA contrast injection (3D MIP image – right image;

2D image – left image) illustrates the course and branchesof the VAs and BA and the filling of the posterior commu-nicating artery (PComA) on the left image. (c) DSA ante-roposterior view after left VA contrast injection shows theorigins and courses of the cerebellar arteries and posteriorcerebral arteries

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Vertebral and Basilar Arteries

The vertebral arteries originate at the level of thesubclavian arteries, having an ascending routewithin the neural foramen and entering the cranialcavity through the foramen magnum. They aregenerally divided into four segments (Lasjauniaset al. 2001):

• V1 (extradural/extracranial segment extendingfrom the subclavian artery to the entrance at the6th transverse foramina)

• V2 (extradural/extracranial segment extendingfrom 6th to 2nd transverse foramina

• V3 (extradural segment extending from thesecond transverse foramina to the foramenmag-num crossing the atlas transverse foramina, theupper surface of the posterior atlas arch andascending to the foramen magum)

• V4 (extradural/intracranial segment ascendingat the anterolateral medullary surface to jointhe contralateral and continue as the basilarartery)

At the cervical segments, the vertebral arteriesgive rise to several small muscular and radicular/spinal branches. The intracranial vertebral arteriesbranches are meningeal branches, spinal branches,such as the posterior spinal and/or anterior spinalarteries, several perforating branches for the brainstem, and the posterior inferior cerebellar artery(PICA).

The basilar artery starts with the vertebral arter-ies confluence at the level of the ponto-medullaryjunction, running grossly at the mid-line of thebasilar sulcus (central pontine sulcus), within theprepontine cistern ventral to the pons, until theinterpeduncular cistern at the level of ponto-mesencephalic junction. At the interpeduncularcistern, the basilar tip divides into two pairs ofarteries, the superior cerebellar and posterior cere-bral arteries. The basilar artery provides supplyfor both the infratentorial and supratentorial terri-tories. Along its course, the basilar artery givesrise to several perforators for the brain stem andthe antero-inferior cerebellar artery (AICA)(Lasjaunias et al. 2001).

Fig. 7 Posterior cerebral artery. DSA anteroposterior view after VA injection (right image) and 3D MIP axial imageobtained from 3D DSA, illustrates the PCA course and distal cortical branches


Posterior Communicating Artery(PCommA)

The posterior /caudal ICA division is the forerun-ner of the posterior communicating artery(PcommA). The PCommA arises from the póst-ero-lateral surface of the ICA supraclinoid seg-ment, running backwards (oblique trajectory:posterior/ascending and medial) within carotidand interpeduncular cisterns, joining the posteriorcerebral artery. PCommA has several perforatorbranches, namely, the premammilar artery (whichis an anterior thalamo-perforating artery), thethalamo-tuberal and thalamo-perforating arteries,supplying hypothalamus, anterior thalamus, pos-terior limb of the internal capsule, tuber cinereum,mammilary bodies, subthalamic nucleus, and pos-terior perforated substance (Duvernoy 2010;Lasjaunias et al. 2001; Rhoton 2002c).

Posterior Cerebral Artery (PCA)

Posterior cerebral artery begins at the basilar tipand is in communication with the carotid systemthrough the posterior communicating artery(Fig. 7).

Anatomically, the posterior cerebral artery isgenerally divided into four segments, namely(Lasjaunias et al. 2001; Rhoton 2002c):

• P1 (precommunicating) segment: Correspondsto the initial segment between the basilar tipand the posterior communicating artery.

• P2 (crural and ambient) segment: Running inthe crural and ambiens cisterns and ending atthe postero-lateral margin of the midbrain. Itcan be subdivided into P2 a segment (anterior:Crural) and P2 P segment (posterior:Ambient).

• P3 (quadrigeminal) segment: Coursing at thequadrigeminal cistern and ending at thecalcarine fissure anterior limit. At the distalend of the P3 segment, PCA bifurcates intoparietooccipital and calcarine arteries.

• P4 (cortical) segment: Corresponds to the dis-tal cortical branches segment that begins at theend of calcarine sulcus.

The major PCA cortical branches include(Lasjaunias et al. 2001; Rhoton 2002c):

• Anterior temporal artery• Posterior temporal artery• Posterior (peri)callosal artery• Lateral occipital artery• Anterior/inferior temporal artery• Middle/inferior temporal artery• Posterior/inferior temporal artery• Medial occipital artery• Parietooccipital artery• Calcarine artery

The deep/perforator branches of the PCA arisefrom the P1 and P2 segments and supply mainlythe midbrain and diencephalon. From the P1 seg-ment originate direct (short) and circumferential(short and long) perforating arteries and thethalamo-perforating arteries. From the P2 seg-ment originate direct (short) and circumferential(short and long) perforating arteries, the thalamo-geniculate arteries, the medial posterior choroidalarteries (MPChA) – from the P2 A segment, andthe lateral posterior choroidal arteries (LPChA) –from the P2 P segment; the latter can also origi-nate from P3 segment (Duvernoy 2010;Lasjaunias et al. 2001; Rhoton 2002c).

• Direct (short) perforating arteries supply thecerebral peduncles and geniculate bodies. Cir-cumferential (short and long) perforating arter-ies supply the quadrigeminal plate, pulvinal,and also cerebral peduncles.

• Thalamo-perforating arteries supply thediencephalic-mesencephalic junction, cerebralpeduncles and mesencephalic tegmentum,medial-ventral thalamus, hypothalamus, andposterior limb internal capsule.

• Thalamo-geniculate arteries supply posteriorlateral thalamus, posterior limb of the internalcapsule, optic tract.

• The MPChA and LPChA supply the choroidplexus of the lateral ventricles but also give riseto the superior and posterior (pulvinar) tha-lamic arteries, respectively.

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– The MPChA also supplies the cerebralpeduncles, tegmentum, geniculate bodies(medial and lateral, but primarily the for-mer), the colliculi, pineal gland, pulvinar,and medial thalamus.

– The LPChA also supplies cerebral pedun-cle, posterior commissure, part of the cruraand body of the fornix, the lateral geniculatebody, pulvinar, dorsomedial thalamicnucleus, and the body of the caudatenucleus.

Cerebellar Arteries: SCA, AICA, PICA

The cerebellar arteries – Superior CerebellarArtery (SCA), Anterior-Inferior Cerebellar Artery(AICA), Posterior-Inferior Cerebellar Artery(PICA) – supply the cerebellum and thebrain stem.

These three arteries may be divided into fouranatomical segments (Rhoton 2000a):

• Antero-medial (cisternal) segment: This seg-ment is in close relationship with the anteriorbrainstem surface:Anterior ponto-mesencephalicsegment (SCA); anterior pontine segment(AICA); anterior medullary segment (PICA).

• Antero-lateral (cisternal) segment: This seg-ment is in close relationship with the lateralbrainstem surface: Lateral ponto-mesencephalicsegment (SCA); lateral pontine segment (AICA);lateral medullary segment (PICA).

• Lateral (fissure) segment: This segment is inclose topographic relation with the cerebello-brain stem fissures: Cerebello-mesencephalicfissure (SCA), cerebello-pontine fissure (AICA)and cerebello-medullary fissure (PICA).

• Posterior (cortical) segment: This segmentcovers the superior/tentorial (SCA), anterior/petrosal (AICA), inferior/occipital (PICA) cer-ebellar cortex.

Fig. 8 Superior cerebellarartery. DSA anteroposteriorview after right VA contrastinjection illustrates the SCAcourse and cortical branchesand specifies the segment atthe cerebellomesencephalicfissure in which thebranches that supply thedentate nucleus arise


Superior Cerebellar Artery (SCA)

SCA is the most constant cerebellar artery origi-nating at the basilar tip. Its origin can have single(~86% of cases), double (~14% of cases), or triple(<1% of cases) trunks (Lasjaunias et al. 2001;Rhoton 2000a).

The SCA brainstem perforators arise from theantero-medial and antero-lateral segments. Fromthe lateral segment originates the pre-cerebellararteries that are responsible for the arterial supplyof the dentate nuclei, superior cerebellar peduncle,and inferior colliculi (Rhoton 2000a).

The SCA generally divides into a rostralmedial (vermian) and caudal lateral (hemispheric)branch at the cisternal segments. The marginalartery arises from the rostral branch at the ante-rolateral segment and anastomosis with AICA.

At posterior (cortical) segment, the rostralbranch subdivides distally the into medialand paramedical branches supplying the vermis.The caudal branch subdivides into lateral, inter-mediate, and medial hemispheric branches sup-plying the upper cerebellar hemisphere (Fig. 8)(Rhoton 2000a).

Anterior-Inferior Cerebellar Artery(AICA)

The AICA originates from the basilar artery (morefrequently from the caudal half of the basilar artery)as (~72% of cases), double (~26% of cases) oreven a triple (~2% of cases) trunks. Consideringan AICA duplication/triplication these branchesshould supply cerebellar cortex, otherwise theyshould be considered as large perforators(Lasjaunias et al. 2001; Rhoton 2000a).

The perforators to the brain stem originatefrom the cisternal segments. The labyrintine arteryto the inner ear and the subarcuate artery beingresponsible for the petrous bone dural supply andthe anastomosis with the ascending pharyngealand stylomastoid arteries originate from theAICA main trunk or the rostral trunk at the cister-nal segment (Duvernoy 2010; Lasjaunias et al.2001; Rhoton 2000a).

AICA main trunk subdivides into corticalbranches that run over the petrous cerebellar sur-face, namely the rostral branch supplying the infe-rior cerebellar petrosal surface and the caudalbranch supplying the inferior cerebellar petrosalsurface, flocculus and IV ventricle choroid plexus(Fig. 9) (Duvernoy 2010; Lasjaunias et al. 2001;Rhoton 2000a).

Fig. 9 Anteroinferior cerebellar artery. DSA ante-roposterior view after right VA contrast injection (rightimage) and 3D TOF MRA MIP image (left image)

exemplify the AICA course and branches, and identifythe course at the internal auditory meatus (M-shape con-figuration) and illustrate a variant with AICA duplication

26 P. Vilela

Posterior-Inferior Cerebellar Artery(PICA)

The PICA is the most variable cerebellar artery,regarding its origin, territory and size. Most com-monly, occurs as a single artery originating fromthe intradural (V4) vertebral artery (in up to 83%of cases). Rarely there is a PICA origin duplica-tion (~3% of cases) or extradural origin (below theforamen magnum) (Lasjaunias et al. 2001;Rhoton 2000a).

The perforators to the brain stem arise from thecisternal segments. The cerebello-medullar seg-ment exhibits a double curve: caudal loop(tonsillo-medullary segment) and cranial loop

(telovelo-medullary segment). From cisternaland lateral segments choroidal arteries originatethat supply the IV ventricle choroidal plexus andtela choroidea (Duvernoy 2010; Lasjaunias et al.2001; Rhoton 2000a).

Generally, at the lateral segment, PICA sub-divides into two cortical branches: a larger lateralhemispheric branch supplying the tonsills and thelateral inferior cerebellar hemispheric surface anda medial smaller vermian branch supplying thevermis (Fig. 10) ( Lasjaunias et al. 2001; Rhoton2000a).

Fig. 10 Posteroinferiorcerebellar artery. DSAlateral (upper image) andanteroposterior (lowerimage) views after right VAcontrast injection illustratesthe PICA course andcortical branches. ThisPICA has an extraduralorigin at the level of C1


Variant Anatomy of Willis Circleand Other Intracranial Vessels

The circle of Willis (CoW) is formed at a veryearly phase (20–40 mm stage). The CoW iscomposed of the A1 (ACA) segments, anteriorcommunicating artery (ACommA), supra-clinoid ICA segments, P1 (PCA) segments, pos-terior communicating arteries (PCommA) andbasilar tip.

During the embryonic development of theCoW there are two major maturation steps(Lasjaunias et al. 2001; Raybaud 2010):• Middle line plexiform fusion of the ACA

medial extensions, which originates the ante-rior communicating artery

• Middle line fusion of the posterior/caudal divi-sion of the ICA originating the basilar tip

The congenital anatomical variants of the CoWare very common, with different type of sizeasymmetries and hypoplasia. Some of the mostcommon examples is the segmental (A1, P1,PcomA) hypoplasia. P1 hypoplasia may be associ-ated with an enlarged ipsilateral PComA in a pat-tern classically termed as “fetal” circulation type.The presence of ACommA fenestration representsthe persistence embryonic appearance of these ves-sels that have a primitive plexiform structure.

CoW variations, such as hypoplasia or arterialsegment absence, may explain different outcomesin acute ischemic stroke and/or unusual arterialstroke territorial distribution. Arterial morphologi-cal abnormalities, such as fenestrations,may also beassociated with an increased risk for developmentof vascular disorders, like intracranial aneurysms(Lasjaunias et al. 2001).

Other common arterial variants include(Lasjaunias et al. 2001):• Persistence of carotid-vertebro-basilar ana-

stomosis (Lasjaunias et al. 2001)– Trigeminal artery– Hypoglossal artery– Proatlantal type 1– Proatlantal type 2

• Anterior cerebral artery (ACA)

– Azigos artery: Fusion of the initial ACAsegments into a single trunk that providesbranches for both hemispheres

– Bihemispheric ACA: One ACA suppliesboth hemispheres (associated with unilat-eral A1 hypoplasia)

– Multiple (triplicated) ACA: Several sepa-rated branches arise from proximal ACAsegments

– Ventral ophthalmic artery: Ophthalmicartery origin from the ACA

– Infraoptic course of ACA: A1 segmentcourses below the optic nerve and chiasm

• Middle cerebral artery (MCA)– MCA fenestration: Persistence of the plex-

iform primitive structure– Duplicated MCA: MCA is formed by two

arterial trunks originating from the supra-clinoid ICA, with the perforator branchesarising from the distal trunk

– AccessoryMCA:MCA origin fromA1 seg-ment or ACommA (the perforator branchesarise from the cranial trunk)

• Anteroinferior cerebellar artery (AICA)– AICA-PICA: Dominant AICA artery that

annexes ipsilateral PICA territory• Posteroinferior cerebellar artery (PICA)

– PICA-AICA: Dominant PICA artery thatannexes ipsilateral AICA territory

– Bihemispheric PICA: PICA supplying bothcerebellar hemispheres with a fusion of thevermian branches

Intracranial Venous Anatomyand Variability

Intracranial Venous AnatomyThe intracranial venous anatomy is organized intothe superficial and deep venous system. The deepvenous system drains into the vein of Galen and thesuperficial venous system drains through corticalveins into the dural sinuses and cavernous plexuses.Both systems are connected through the trans-medullary veins in a hemodynamic equilibrium.

The dural sinuses are intradural venous struc-tures, covered by the two dural layers, are in close

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relationship with dural attachments, such as thoseat the tentorium and falx cerebri. They have amembranous origin, similar to the dura of thecranial vault convexity. The dural sinuses are the

superior sagittal, inferior sagittal, straight, trans-verse and sigmoid sinuses (Fig. 11a) (Rhoton2000b, 2002a, b).

Fig. 11 (a–c) (a) Dural sinus anatomy. DSAvenous phaselateral view after ICA contrast injection shows the majordural sinuses. (b) Dural sinus anatomy. DSAvenous phaselateral view after ICA contrast injection shows the four

major routes for superficial venous drainage (1-superiorsagittal, 2-sphenoid 3-tentorial, and 4-falcine groups). (c)Schematic representation of the supratentorial corticalvenous distribution and preferential drainage


The venous plexus have an epidural location,between the periosteum and the dura. They have acartilaginous origin, similar to the dura of the cra-nial base. These venous structures include the cav-ernous, retroclival venous plexuses, the venousplexus of the foramen magnum and the spine epi-dural venous plexuses (Fig. 12).

The supratentorial superficial venous system iscomposed of cortical veins that drain into fourmajor venous collectors, namely: (Fig. 11b andc) (Duvernoy 1975; Rhoton 2002b)

• Superior sagittal group, draining into the supe-rior sagittal sinus

• Sphenoid group converging into the spheno-parietal sinus or cavernous venous plexus

• Tentorial group, draining into the venoustentorial sinuses, located at the upper surfaceof the tentorium and emptying into the trans-verse sinuses

• Falcine group that drain into the inferior sagit-tal or straight sinus, or their tributaries

The superior sagittal sinus (SSS) has a variablelength, with a variable of the anterior segments.The anterior third of the sinus may be absent. Atthe anterior extremity it may communicate withthe nasal veins and with emissary veins through itsentire course. The superior sagittal sinus ends atthe torcular Herophili. The torcular Herophilireceives also the blood from the straight sinusand continues through the transverses sinuses.The SSS receives the blood from several corticalveins from the superior part of the medial andlateral surfaces of the frontal, parietal, and occip-ital lobes and the anterior part of the orbital sur-face of the frontal lobe (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2002b).

The transverse and sigmoid sinuses establishthe communication between the torcularHerophili and the internal jugular vein. The trans-verse sinuses run within the tentorium attachmentuntil the origin of the superior petrosal sinus andthe sigmoid sinus are positioned in-between theorigins of the superior and inferior petrosalsinuses (Duvernoy 1975; Lasjaunias et al. 2001;Rhoton 2002b).

Fig. 12 Cavernous sinusplexus. DSAanteroposterior view afterbilateral internal jugularvein contrast injectiondemonstrates the cavernousplexus and the venousconnections with theinferior petrosal sinus,basilar plexus, and sylvianvein

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The transverse sinus drains in both supra- andinfra-tentorial cortical veins. They receive theblood indirectly through tentorial sinuses locatedwithin the tentorium, the medial tentorial sinusdraining the cerebellum and the lateral tentorialsinus draining the temporal and occipital lobes,receiving among others the vein of Labbé.

The sigmoid sinuses communicates with theinferior petrosal sinuses, does not generallyreceive cortical veins, but has relevant venousanastomoses with the suboccipital venous plexus,condylar veins, marginal and occipital sinus andcavernous plexus (through the inferior petrosalsinus) (Duvernoy 1975; Lasjaunias et al. 2001;Rhoton 2002b).

The inferior sagittal sinus (ISS) courses at theinferior edge of the falx cerebri ending at the veinof Galen – straight sinus junction. Along itscourse there are venous channels communicatingwith the superior sagittal sinus. It receives bloodfrom the internal parietal, frontal lobe, and cingu-late gyrus through medial descending internalveins (Duvernoy 1975; Lasjaunias et al. 2001;Rhoton 2002b).

The cavernous “sinuses” are epidural venousplexus located between the perosteum and thedura matter, draining the face-orbit and the brain,and constitute the cephalic extension of the spineand basilar (clival) epidural venous plexuses. Aspreviously mentioned, the cavernous plexuses areimportant alternative intracranial venous drain-ages but they are only fully matured after birth,until around the second year of life (Rhoton2002a, b).

The cavernous plexus are a venous hub at thelevel of the skull base, they have:

• Contralateral communication through the ante-rior and posterior inter-cavernous sinuses

• Posterior continuation with the inferior andsuperior petrosal sinuses and basilar plexus

• Inferior communication with the extracranialpterygoid plexuses through emissary veins

• Anterior communication with the superior andinferior (or common venous confluent) oph-thalmic veins

• Lateral communication with the spheno-parietal sinus and sylvian veins

Fig. 13 Posterior fossa veins. A – DSA venous phaselateral view after ICA contrast injection shows the threemajor venous pathways: anterior to the petrous veins;

superior to the vein of Galen, and inferior into the tentorialsinus and transverse sinus


The superior petrosal sinuses run above thepetrous bone from the junction of the transverseand sigmoid sinuses and the cavernous plexus. Itreceives the blood from the posterior fossa ante-rior (petrosal) venous group, which is generallygathered by the petrosal veins. The inferior petro-sal sinus runs at the petroclival fissure, does notreceive cortical venous blood, and acts as avenous anastomotic pathway between the cavern-ous plexus and the internal jugular veins(Duvernoy 1975; Lasjaunias et al. 2001; Rhoton2002b).

The straight sinus runs from the union of theinferior sagittal sinus and the vein of Galen to thetorcular Herophili within a dural attachment of thefalx cerebri and tentorium (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2002b).

The infratentorial superficial venous system iscomposed of superficial cortical, deep, and brainstem veins (Fig. 13).

The infratentorial cortical veins drain into threemajor venous collectors, namely (Duvernoy1975; Lasjaunias et al. 2001; Rhoton 2002b):• Anterior (Petrosal) group: Draining into the

petrosal vein(s) and/or superior petrosalsinuses

• Superior (Galenic) group: Emptying into thebasal vein of Rosenthal and/or vein of Galen

• Inferior (Tentorial) group: Draining into thevenous tentorial sinuses, located at the lowersurface of the tentorium and empting into thetransverse sinuses

The anterior (petrosal) group, drains the anteriorcerebellar surface, includes the anterior (superior,middle and inferior) cerebellar hemispheric veins,gathered at the great horizontal fissure (Duvernoy1975; Lasjaunias et al. 2001; Rhoton 2002b).

Fig. 14 Schematic representation of the deep venous system and corresponding axial SWI MRI images illustrating theveins draining into the internal cerebral veins. (Courtesy of Dr.ª Teresa Nunes – Portugal)

32 P. Vilela

The superior vermian (anterior ascending) andsuperior hemispheric (anterior ascending) groupsdrain the superior cerebellar surface constitute thesuperior group (galenic) (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2002b).

The inferior (tentorial) group drains the inferiorcerebellar surface through the inferior vermianveins, inferior hemispheric veins, retro-tonsillarveins, medial and lateral tonsillar veins. The supe-rior vermian (posterior descending) and superiorhemispheric (posterior descending) veins alsoparticipate in this group (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2002b).

The infratentorial brain stem and deep venoussystem is formed by an extensive venous networkof veins with longitudinal and transversal arrange-ment draining into the vein of Galen, basal veinsof Rosenthal and petrosal veins. They have caudalvenous anastomoses with the spinal cord veinsand the marginal sinus (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2002b).

The supratentorial deep venous system iscomposed of the internal cerebral veins, basalvein of Rosenthal and their venous confluents,being responsible for the venous drainageof the midbrain, limbic lobe, corpuscallosum, pineal gland, choroid plexuses,basal ganglia thalami and deep cerebral whitematter (Duvernoy 1975; Lasjaunias et al.2001; Rhoton 2002b).

The internal cerebral veins are formed bythe confluence of the medial septal vein andthe thalamo-striate veins at the level of theMonro foramina. This vein runs within thevelum interpositum and at the level of thequadrigeminal cistern it joins the contralateralinternal cerebral vein forming the vein of Galen(Fig. 14) (Duvernoy 1975; Lasjaunias et al.2001).

Along its course, the internal cerebral veinsreceive several subependymal veins, which canbe divided into two groups, namely, the:• Lateral group – including the anterior and

posterior septal veins and medial atrial veins(Duvernoy 1975; Lasjaunias et al. 2001)

• Medial group – including the anterior and pos-terior caudate veins, thalamo-striate veins,superior striate, and lateral atrial veins

The septal veins receive venous blood frommedullary veins arising from the frontal lobe(anterior septal veins) and parietal/occipital lobes(posterior septal veins). The atrial veins drain theparietal/occipital lobe medullary veins (medialatrial veins) or the temporal /occipital lobe med-ullary veins (lateral atrial veins). The other medialgroup drains mainly the basal ganglia and thala-mus, the internal capsule and the deep white mat-ter (Duvernoy 1975; Lasjaunias et al. 2001).

The basal vein of Rosenthal receives bloodsupply from both superficial and deep veins. It isresponsible for the cortical venous drainage of themedial and inferior brain surface, namely themedial temporal lobe, the orbital frontal lobe sur-face, and the insula. It also drains the hypothala-mus, midbrain, striatum, internal capsule, andthalamus (Duvernoy 1975; Lasjaunias et al.2001).

The basal vein of Rosenthal is generallydivided into three segments (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2002b):• Anterior – corresponding to the segment from

the origin at to the cerebral peduncle ventralsurface. It receives the anterior cerebral anddeep middle cerebral vein at its origin. Alongits course it receives the inferior striate veinand the olfactive, insular, orbito-frontal, anduncal veins.

• Medial – corresponding to the segment locatedwithin the crural and ambiens cisterns. Itreceives the blood from the peduncular veins,hippocampal veins, and inferior ventricularand choroidal veins.

• Posterior – corresponding to the final segmentthat joins the vein of Galen or the internalcerebral vein. This is the most variable seg-ment being even absent in some cases. Insuch cases the basal vein of Rosenthal drainsinto the lateral sinus or torcula (throughtentorial sinus) or through the latero-mesencephalic vein.


Fig. 15 (continued)

34 P. Vilela

Fig. 15 (continued)


The vein of Galen is a middle line single veinthat receives the blood from the internal cerebralveins at the level of the quadrigeminal cistern. Itcan also receive the blood from the basal vein ofRosenthal directly. During its course it collects theblood from inferior pericallosal veins, medialoccipital veins and from precentral veins andsuperior vermian veins (Duvernoy 1975;Lasjaunias et al. 2001; Rhoton 2000a, 2002b).

Intracranial Venous Variabilityand Anomalies

The intracranial venous system has a wide ana-tomic variability, rich anastomosis network, bidi-rectional flow, and capacity to adapt to flowchanges. This makes the outcome of venousthrombosis unpredictable.

Fig. 15 (a) DSA venous phase antero-posterior viewDSA and axial CT demonstrate (congenital) left transverseand sigmoid sinuses hypoplasia. (b) Venous variants. DSAvenous phase lateral view shows a superior sagittal sinuspartial agenesis (upper image) in comparison to a complete

superior sagittal sinus (lower image). (c) Venous variants.DSAvenous phase lateral view illustrates different patternsof the cerebrum convexity venous drainage (co-dominanceand dominance)

36 P. Vilela

Fig. 16 (a) DSAvenous phase lateral and anteroposteriorview illustrating the persistence of a major occipital sinus.(b) DSA venous phase anteroposterior view showing thepersistence of the Markowski’s vein in association with

VGAM (left images) and “balloon-shaped” dural – trans-verse sinuses and torcula – sinuses in association with duralsinus malformation with AV shunts (right images)


The post birth maturation has been discussedpreviously and is extremely important for theevaluation of the pediatric vascular system.

Variability is the rule for venous anatomy.The size, number and disposition of the intra-cranial veins are extremely variable among indi-viduals and not predictable, which may explaindifferent clinical outcomes in intracranialvenous occlusion or in arteriovenous fistulae/malformations.

Hypoplasia or partial agenesis of the duralsinuses is frequent. The asymmetry of the trans-verse/sigmoid sinuses is a common example, andthe development cause of this finding can be eas-ily deducted from the size of the correspondingjugular foramen, differentiating it from acquiredconditions (Fig. 15a).

The anterior third of the superior sagittalsinus is also variable and agenesis is associatedwith hypertrophy of frontal cortical veins thatcollect the venous blood from that area(Fig. 15b).

The cortical veins distribution is another exam-ple of extreme variability. For the cerebral con-vexity there may be a pattern of equal dominanceof cortical veins, or of Trolard, Sylvian, Labbédominance with a large vein draining into thesuperior sagittal sinus, cavernous sinus, or trans-verse sinus respectively (Fig. 15c).

Other venous variants include the persistenceof prominent embryonic veins/sinuses, such as

(Fig. 16a) (Lasjaunias et al. 2001, 2006; Raybaud2010):• Occipital sinus: Beginning at the torcula and

flowing into the marginal or sigmoid sinus withcommunications to the internal jugular vein,clival plexus, and vertebral–suboccipital plexus

• Marginal “sinus”: Which is a venous plexusaround the foramen magnum, connected withthe basilar plexus, sigmoid sinus, and occipitalsinus

• Falcine “sinus”: Which is a venous plexus sitedwithin the falx cerebri and communicating thevein of Galen and the superior sagittal sinus

• Tentorial sinus: Which are transient struc-tures, located within the tentorium drainingthe temporal lobe and diencephalon towardsthe torcula/transverse sinus and that regressafter the development of the basal vein ofRosenthal

The persistence of embryonic veins/duralsinuses may occur as an isolated feature or inassociation with vascular malformations, such asthe Vein of Galen aneurysmal malformation withthe persistence of the Markowski’s vein, or thedural sinus malformation with AV shunts with the“ballooning” appearance of the dural sinusrepresenting a “frozen” anatomy at the time ofthe malformation development.

Fig. 17 (a, b) Developmental venous anomaly (DVA). (a)Axial SWI MR image showing a large cerebellar DVA. (b)DSAvenous phase lateral view demonstrating a superficial

DVA draining into the sylvian group (sylvian veins-cavernous plexus)

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Fig. 18 (a, b) Sinus pericranii (SP). (a, b) DSA of leftfrontal SP associated with a congenital middle fossa AVF.(a) The 3D bone reconstruction shows the bone defect, andthe axial images demonstrate the venous pouch crossingthe bone defect. (b) Lateral view of common carotid arteryinjection demonstrating the presence of a high flow middlefossa AVF fed by ECA branches and draining thought a

enlarge convexity vein toward the bone defect and into theextracranial scalp veins. (c) DSA Lateral view of ICAinjection showing a small SP at the cranial vault commu-nicating the superior sagittal sinus with the extracranialvenous system. There are also multiple enlarged trans-osseous veins at the posterior third of the superior sagittalsinus communicating with the extracranial venous system


Other more complex venous anomalies includethe Development Venous Anomalies (DVA) andthe sinus pericranii (see also AVM chapter).

DVAs are extreme variations of the trans-medullary venous development. They are com-mon findings with an incidence of 2.5–3% inautopsy. The etiology is not completely under-stood, being accepted that represent an in uterusfailure of normal venous development and/orvenous thrombosis (Fig. 17) (Lasjaunias et al.2001, 2006; Raybaud 2010).

They may be categorized into:• Superficial DVAs accounting for ~70% of all

DVA cases and drain the deep medullaryregions into cortical veins.

• Deep DVAs corresponding to ~20% of allDVA cases and drain the subcortical medullaryregions into deep venous collectors.

• Mixed (deep & superficial) DVAs accountingfor up to 10% of cases. They are composed of acaput medusae, corresponding to a group ofradial arranged dilated medullary veins con-verging into a single (or multiple) trans-medullary venous collector.

They are characterized by the lack of normalsurrounding venous system, they have intermingled

normal brain tissue and they participate in thenormal brain tissue venous drainage. They havebeen described in association with cavernomas,but also with Brain AVMs, cortical malformationsand in syndromatic forms such as Sturge Webersyndrome and Blue Rubber Bleb Nevus(Lasjaunias et al. 2001, 2006; Raybaud 2010).

During the neonatal period they have adynamic behaviour with flow changes, includingincrease in flow or disappearance inducing adja-cent parenchymal changes, including the appear-ance of new changes or the regression of previousbrain abnormalities. In adults, they are generallystable and asymptomatic. However, as any otherintracranial venous structure, DVA may becomesymptomatic due to mechanical compression ofneural structures causing hydrocephalus or cranialnerve palsies or due to flow changes with reducedflow associated with venous stenosis/thrombosis(which may cause any of the venous thrombosiscomplications described in the Venous Thrombo-sis chapter) or with increased flowwhenever asso-ciated with an AV shunt.

The sinus pericranii (SP) are defined as largevenous connection between the intra and

Fig. 19 Arterial collateralcirculation. DSAanteroposterior view afterthe left ICA contrastinjection shows a distal M1occlusion in the setting ofacute ischemic stroke andthe retrograde filling ofdistal MCA branchesthrough leptomeningealanastomosis with ACA

40 P. Vilela

extracranial venous drainage, formed by a net-work of thin-walled veins that form a varix onthe external table of the skull, in which the bloodmay have a bidirectional flow (Fig. 18). Sinuspericranii are generally unique, asymptomatic,located at the midline at the frontal area. Multiplesinus pericranii are very rare (Lasjaunias et al.2001, 2006; Raybaud 2010).

They may be categorized into two majorgroups:

• Accessory – SP with a small amount of venousflow crossing through

• Dominant – SP with a mainstream of intracra-nial venous blood crossing, playing a majorrole in brain venous drainage

The diagnosis of sinus pericranii is clinical.Imaging may be useful to evaluate the flow withDoppler US, the bone defect with computedtomography (CT), the complete venous patternwith computed tomography venogram (CTV) ormagnetic resonance venogram (MRV), or to lookfor other venous and brain anomalies with MRI.Digital subtraction angiography is generally notneeded unless treatment is considered and preciseevaluation of the sinus pericranii role for the brain

drainage is warranted (Lasjaunias et al. 2001,2006).

Collateral Circulation

The collateral circulation is composed of vascularredundancies from pre-existing arterial and venousvessels, with bidirectional flow (depending on thepressure gradients), allowing alternative vascularpathways maintain the blood flow, overcomingvascular stenosis/occlusions. Each individual hasa singular arterial and venous collateral status.

The arterial collateral development(collaterogenesis) occurs at a very early stage,around the 13–14 gestation weeks. This process isgenetic mediated, being chromosome 7 and theDce1 locus important regulators of collateral arter-ies. Several acquired conditions, such as aging,chronic hypertension, metabolic syndrome and dia-betes, alter the collateral status of individuals bydecreasing of collateral number and/or diameter.

Themost common arterial anastomotic pathwaysinclude external–internal carotid (or ophthalmic)arteries anastomoses, external carotid–vertebralartery anastomoses, the persistence of embryonicinternal carotid artery–vertebro-basilar anastomoses(trigeminal, hypoglossal, proatlantal type 1 and

Peduncular

Vein

Anterior communicatingvein

Midbrain

Anterior Cerebral Vein

Venous Circle fo Willis

Chiasm

Posterior communicating vein

Basal Vein

To Great Vein ofGalen or

Internal Cerebral Vein

Deep MiddleCerebral Vein

Temporal Lobe

Fig. 20 Venous collateral circulation. Schematic repre-sentation (left image) of the venous “circle of Willis” andthe corresponding finding in 3DMIP axial images obtained

with 3D DSA (right image). (Courtesy of Dr.ª TeresaNunes – Portugal)


2 arteries), the circle of Willis, and leptomeningealanastomosis through cortical/pial or deep arteries(Fig. 18).

The collateral venous status is even moreunpredictable than the arterial. The venous anat-omy is highly variable among individuals, spe-cially the superficial venous system. The venoussystem is highly prone for anastomoses allowingmultidirectional flow accordingly to local flowneeds. The major anastomotic venous pathwaysare extracranial–intracranial anastomoses, throughcavernous plexuses, meningeal, diploic, and emis-sary veins of the skull; superficial–deep venoussystem anastomoses through transmedullaryveins; infratentorial–supratentorial venous sys-tems, through large anastomotic veins such aslateral mesencephalic vein and basal vein ofRosenthal; infratentorial–spine venous system,through medullary and spinal veins. There arealso anastomoses inside each venous system,such those between veins of the deep venoussystem, through venous circle of Willis, orthrough the peripheral venous network surround-ing the brain stem, and between cortical veinsthrough pial anastomoses (Figs. 19 and 20).

References

Duvernoy HM. Human brain stem vessels. 2nd edition.Berlin: Springer 2010.

Duvernoy HM. The superficial veins of the human brain:veins of the brain stem and of the base of the brain.Berlin: Springer; 1975.

Lasjaunias P, Berenstein A, ter Brugge KG. Surgicalneuroangiography. 1. Clinical vascular anatomy andvariations. 2nd ed. Berlin: Springer; 2001.

Lasjaunias P, Berenstein A, ter Brugge KG. Surgicalneuroangiography. 3. Clinical and interventionalaspects in children. 2nd ed. Berlin: Springer; 2006.

Milner R, editor. Cerebral angiogenesis: methods and pro-tocols, methods in molecular biology, vol. 1135.New York: Springer Science+Business Media; 2014.

Raybaud C. Normal and abnormal embryology and devel-opment of the intracranial vascular system. NeurosurgClin N Am. 2010;21(3):399–426.

Rhoton AL Jr. The cerebellar arteries. Neurosurgery.2000a;47(3 Suppl):S29–68.

Rhoton AL Jr. The posterior fossa veins. Neurosurgery.2000b;47(3 Suppl):S69–92.

Rhoton AL Jr. The supratentorial arteries. Neurosurgery.2002a;51(4 Suppl):S53–120. Review

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