patterns of the cranial venous system from the comparative ... · patterns of the cranial venous...

www.centauro.it Interventional Neuroradiology 14: 21-31, 2008

21

venous system. This system involves drainageof the paleopallium (or pyriform area), archi-pallium, archicerebellum and brain stem. Allthe venous systems which we classified canconnect to each other through many anasto-moses (Diagram 1).

The lateral-ventral venous system is the sys-tem which continues longitudinally from thespinal cord. This study focuses only on the ve-nous drainage of the five brain vesicles becauseit has a special arrangement. We named the ve-nous system based on the location on the brain.

The recent evolution of this cranial venoussystem in man includes the cavernous sinuscaptured from the tentorial sinus, the definitiveposition of the superior petrosal sinus and itsmedial drainage into the cavernous sinus.

Materials and Methods

Literature on the cranial venous anatomy invertebrates was reviewed. Using the area of ve-nous drainage, the veins involved and theirfunctions, we classify the cranial venous systemin vertebrates into four systems compared tothe venous drainage of the five brain vesicles inman. The vertebrates reviewed are fish (Myx-ine glutinosa, Eptatretus stouti, and Danio re-rio), amphibians (Amblystoma tigerinum), rep-tiles (Testudo geometrica), birds (Larus argen-tatus and hen), rodents (inbred Sprague-Daw-

Summary

Comparing the adult submammalian brainwith the human embryonic brain, some patternsof venous drainage are quite similar. The veinslying on the lateral surface of the brain in sub-mammals resemble those of the human embryo.In addition, the new longitudinal venous anasto-mosis ventral to the brain vesicles occurring latein human embryonic development seems to besimilar to the late appearance of the basal veinand the ventral brain stem venous plexus foundin adult mammals including man. The evolutionof the new structures of the brain vesiclesthroughout the vertebrate series may have an in-duction role on the appearance of the cranial ve-nous system.

This part of the article series focuses on theevolution of the lateral-ventral venous system ofthe five brain vesicles. Nevertheless, the limita-tion of this article is due in part to the paucity ofcircumstantial papers and different names usedfor the veins.

General Introduction

We have already described the dorsal venoussystem which is mainly involved in draining theneopallium and neocerebellum in vertebrates.This study compares another proposed divisionof the cranial venous system, the lateral-ventral

Patterns of the Cranial Venous Systemfrom the Comparative Anatomyin VertebratesPart II. The Lateral-Ventral Venous System

T. AURBOONYAWAT 1,2, V. PEREIRA 1, T. KRING 1, F. TOULGOAT 1,A. CHUROJANA 3, P. LASJAUNIAS 1

1 Diagnostic and Therapeutic Neuroradiology Service, Hôpital de Bicêtre, Le Kremlin-Bicêtre, Paris, France2 Division of Neurosurgery, Department of Surgery, Siriraj Hospital, Mahidol University, Thailand3 Department of Radiology, Siriraj Hospital, Mahidol University, Thailand

Key words: classification of the cranial venous system, comparative anatomy, deep venous system

Patterns of the Cranial Venous System from the Comparative Anatomy in Vertebrates T. Aurboonyawat

22

ley strain of rats, guinea pigs), tree shrews (Tu-paia glis), opossums (Didelphis virginiana), do-mestic animals (dogs, cats, rabbits, pigs, horses,oxen, sheep and goats) and primates (Macacamulatta, Cebus paella, Papio ursinus, Cercop-ithecus pygerithrus, Galago senegalensis).

Results

For the viewpoint of comparative anatomy,we present the lateral-ventral venous system ofthe brain vesicles separately in two differentgroups: the lateral and ventral venous groups.When comparing these groups, the lateral ve-nous group seems to be more ancient in evolu-tion. We found this venous group early in sub-mammals when the other group is not well-de-veloped.

Lateral Venous Group

The lateral venous group was labeled basedon its position on the lateral surface of thebrain vesicles in vertebrates, especially in sub-mammals. From human embryo we include thelateral positioned telencephalic, diencephalic,mesencephalic, metencephalic and myelen-cephalic veins in this category.

Considering the telencephalic region, we ob-serve a special arrangement of the venous dra-inage of the paleopallium. With the phylogenicascent of the brain in vertebrates, the paleopal-lium is shifted from the dorsal part of the te-lencephalon in fish to ventromedial position of

the telencephalon in man. Using the homolo-gous anatomical position of the venous dra-inage in different species, it is interesting thatthe vein moves together with the paleopallium.

Phylogenic Evolutionof the Lateral Venous SystemSubmammalsFish

The brain vesicles of hagfishes 6 are the largeolfactory bulbs, primitive hemispheres, dien-cephalon, mesencephalon and large medullaoblongata. The areas of the primodial piriformcortex and prepyriform area are drained corre-spondingly by the “anterior cerebral vein” orig-inating from the ventral telencephalic and di-encephalic regions at about the level of the hy-pophysis and curving around the brain to emp-ty into the “sagittal sinus”(vein).

The “anterior cerebral”, “middle cerebral”and “rhombencephalic” veins drain the ventraland lateral surfaces of the diencephalon, mes-encephalon, rhombencephalon and mylelen-cephalon, respectively.

Amphibians

In tiger salamander, Roofe 3 reported thatthe “vena prosencephali lateralis” receivesblood from most of the pyriform area, striatum,diencephalon and a part of the optic tectum. Itlocates at the dorsolateral surface of the telen-cephalon and empties into the “rete of the en-dolymphatic sac” on the dorsal and lateral sur-faces of the brain stem.

The veins of the brain stem drain blood fromthe ventral and ventrolateral surface of thebrain stem, and empty into the “endolymphaticrete”: the “vena mesencphali”, “vena basilarisanterior” and “vena basilaris posterior”

Reptiles

In turtle 2, the corresponding pyriform area isdrained by the “anterior and posterior lateralcerebral veins”. They locate on the dorsolateralsurface of the hemispheres and empty into the“dorsal longitudinal vein”. The “diencephalic”,“anterior and posterior mesencephalic”, and“posterior medullary” veins drain the lateralsurface of the diencephalon, mesencephalon,metencephalon and myelencephalon, respec-tively. They course dorsally and terminate into

Diagram 1 The venous systems and their connections in man.


23

Figure 1 Lateral venous group (light blue) indifferent adult vertebrates. A) Hagfish. B) Am-blytoma tigerinum. C) Testudo geometrica. D)Guinea pig. E) Dog. F) Man (arrow points tothe variation of middle cerebral vein draininginto the transverse sinus). (After 1-6 with modifi-cation).

A B

C

D

E

F


24

the “dorsal longitudinal vein” which furtherconnects to the internal jugular vein.

Birds

A homologue of the superior petrosal sinus,the “middle cerebral vein”, drains the lateralcerebellum, flocculus and posterior aspect ofthe tectum, entering the occipital sinus 7.

Mammals

Rodents

On the study of brain vessels in guinea pig 5,the venous blood from the palepallium is likelyto be drained into the “superior lateral cerebralvein” which locates on the lateral surface of thetelencephalon. It further empties into the trans-verse sinus as “the vein of flocculus” does.

In rats 8,9, the corresponding pyriform area isdrained by the “superficial cerebral vein”. It lo-cates on the ventrolateral surface of the hemi-sphere and empties into the transverse sinus.

Domestic Animals

The “ventral cerebral veins” of domestic ani-mals could be compared to the middle cerebralveins in man. They drain the rhinencephalonand the insular region, course in the rhinal sul-cus, and open into the “dorsal petrosal sinus”,which seems to be compatible with the tentori-al sinus in man.

In horses, the “dorsal petrosal sinus” arisesby convergence of small veins in the region ofthe fossa for the pyriform lobe and the olfacto-ry bulbs. It locates on the ventral surface of thecerebral hemisphere and joins the transversesinus 4.

In another study of brain venous system ofdogs 10, the “ventral cerebral vein” follows thepseudosylvian fissure ventrally, passes caudallyin the caudal lateral rhinal sulcus on the ven-trolateral surface of the cerebral hemisphere toenter the “dorsal petrosal sinus”. It is interest-ing to note that the role of the lateral venoussystem in dogs could be shifted from drainingthe pyriform area to draining the neopalliumbecause the paleopallium is less dominant. Forthe venous drainage of the cerebellum, the“rostral ventral cerebellar veins” run laterallyacross the rostral base of the cerebellum andsuperior cerebellar peduncle. They anastomosewith veins of the pons and midbrain, drain

parts of brain stem, the paramedian and ansi-form lobules of the cerebellum, and empty intothe sigmoid or transverse sinuses.

Monkeys

In rhesus monkeys and tufted capuchin, themiddle cerebral vein does not drain into thecavernous sinus. The empty site varies amongspecies. That of rhesus monkeys drains into thesuperior petrosal sinus whereas it drains intothe distal transverse sinus in tufted capuchin.The superior petrosal sinus of rhesus monkeysdoes not communicate with the cavernous si-nus. It is relatively short and touches only thelateral part of the petrosal crest 11. In baboons,vervet monkeys and bushbaby, the superiorpetrosal sinus becomes apparent half-wayalong the superior petrous ridge, drains bloodinto the transverse-sigmoid junction and has al-so no connection with the cavernous sinus.

Man

Morphological changes in the lateral venousgroup in neonates after birth are the cavernoussinus capture of the tentorial sinus, and theconnection between the superior petrosal sinusand cavernous sinus 11. The middle cerebral veinin man functions like the neopallium venousdrainage. It can empty along the way of the lat-eral venous system evolution e.g. the cavernoussinus, tentorial sinus, superior petrosal sinus,and even transverse sinus (figure 2).

In the 11-week-old human fetus, the petrosalveins are seen running from the floccular re-gion to the superior petrosal sinus. At this time,its course is totally intradural. Later on the veinunites with the anterior cerebellar veins andthe brain stem veins 12.

Hypothesis of the comparative lateral venousgroup anatomy

Comparing the primitive brain of submam-mals and the late embryonic human brain, thelateral located veins are similar. We purposethe middle cerebral vein, the tentorial sinus, in-ferior ventricular vein, lateral mesencephalic-pontine-medullary veins, the petrosal (superiorpetrosal) vein, and the condyloid (the bridgingvein draining the vicinity of medulla) vein asthe lateral venous system of the brain vesiclesin man.


25

Their definitive disposition is a new forma-tion phylogenetically.

On evolutionary progression, the paleopalli-um or pyriform area is moved from the dorsalto ventromedial position. It is interesting to

note that the lateral venous system in verte-brates always follows the rhinal fissure. It has amajor role in draining the paleopallium. Wefound that it moves along with the paleopalli-um from the dorsal position of the hemisphere

Figure 2 In man, the lateral venous group can empty into several veins or sinuses depending on the way it evolutes phylo-genically. The middle cerebral veins can drain into the cavernous sinus (A) and tentorial sinus (white arrow in B), and fur-ther into the superior petrosal sinus (G in white) or distal end of transverse sinus (B and C in different views). Subependy-mal veins can drain into either a fully persistent lateral venous group in the infratentorium (G in blue) or medially into thecavernous sinus via the superior petrosal sinus (H and I in blue). It seems that the petrosal vein draining medially into thecavernous sinus by the way of the superior petrosal sinus (black arrow in E and F) is a new venous evolutional pathwayfound only in man (D and E).

G

D

A B

E

H

C

F

I


26

in fish and amphibians to the lateral position inreptiles 13. Finally, its function of draining bloodfrom the paleopallium is taken over by the ven-tral venous group (basal vein of Rosenthal)when the neopallium is dominant in higher ver-tebrates. This pattern of the “shift in function”is apparent from domestic animals onward. Itsrole has changed into draining the lateral sur-face of the neopallium in primates and man.The tentorial sinus in rat, horse, cow and doglies in the tentorium like that in man.

Having looked at the site of emptying, thecomparable lateral venous group in hagfishes,salamanders, and turtles joins with the veinwhich is the forerunner of the median prosen-cephalic vein of human embryo, on the mid-dorsal surface of the hemisphere. In treeshrew 14, rats, guinea pigs and domestic animals,

it empties into the transverse sinus. In mon-keys, it can enter either the superior petrosal si-nus or the transverse sinus depending on thespecies, without connection with the cavernoussinus resembling the tentorial sinus during fetalstages in man.

A homologue of the ventral diencephalicvein in human embryo is the inferior ventricularvein in the adult. For the mesencephalic vein, itis the posterior part of the basal vein of Rosen-thal 11. Looking at the diencephalic and mesen-cephalic veins in lower vertebrates, they locateon the lateral surface of the diencephalon andoptic lobes and drain venous blood into themid-dorsal located vein which is a homologueof the primitive internal cerebral veins.

The comparable vessel in fish, amphibiansand reptiles, of the superior petrosal vein in

Figure 3 Ventral venous group (light blue) in different adult vertebrate brains. Ventral venous group of the Tiger salaman-der’s brain (A sagittal view: B ventral view) is an example in submammals. This venous group at the telencephalic region islocated in the midline whereas this group of the other regions is not well developed. The ventral venous group becomes ev-ident in mammals (C guinea pig; D dog). (After 3-5 with modification).

A

DCB


27

man is the vein that drains the metencephalon(pons and archicerebellum). Because of almostdorsally oriented venous drainage in lower ver-tebrates, the comparable “metencephalicveins” of those animals collect venous bloodfrom the ventral part of the metencephalic areaand run dorsally near the trigeminal nerveemptying into the “rete of the endolymphaticsac”, and the “dorsal longitudinal vein” in Am-blystoma, and Testudo, respectively. These veinslie in the comparable subarachnoid space inmammals. The homologue vein of the hen re-ceives venous blood from the lateral cerebel-lum and dorsal of tectum, and empties into theoccipital sinus. It seems that like phylogenic as-cent, the metencephalic veins move togetherwith the archicerebellum from the dorsal posi-tion in submammals to the lateral position inmammals due to the newly developed neocere-bellum. In bat, the sinus is found only by thedural end of the major metencephalic veins. Inhorses and dogs, the sinus is not in contact withthe petrous bone 11. Armstrong 10 described thehomologue of the superior petrosal sinus indogs, the “rostral ventral cerebellar vein” thatanastomoses with the brain stem veins, anddorsal cerebellar veins. It runs laterally acrossthe rostral base of the cerebellum and superiorcerebellar peduncle. It is epidural in positionwhen it passes over the ventral paraflocculusand terminates into either the sigmoid sinus ortransverse sinus. In monkeys, it touches thebone only in the lateral part and does not com-municate with the cavernous sinus.

The condyloid vein can be compared withthe vein that drains the medulla oblongata andaccompanies the hypoglossal nerve in animals.This vein has changed its direction of drainagefrom dorsal direction in amphibians and rep-tiles to ventral direction in higher animals.

Ventral Venous Group

We describe the ventral venous group due toits ventral location on the brain vesicles in ver-tebrates. This group seems to be well apparentonly in mammals due to the induction of therecent acquisition structures on the ventral sur-face of the brain vesicles such as the neostria-tum, the red nuclei, the crus cerebri and theventral pontine tegmentum. The ventral venousgroup occurs as the longitudinal venous anasto-mosis of the lateral venous group. The mostcephalic end of this group is interesting. It func-

tions mainly as drainage of the archipallium inlower vertebrates. Like phylogenic ascent, itsfunction and location are gradually changed.

Phylogenic Evolution of Ventral Venous Group

The venous drainage of the olfactory systemhas changed from a dorsal position into a ven-tral one. In hagfishes, tiger salamander, tortoise,hen and rats venous blood from olfactory tractsand lobes is drained by the “olfactory veins”and discharged into the dorsal sagittal vein orsinus depending on the species. The pattern ofdrainage has changed in other mammals by theventral venous group.

SubmammalsIn hagfishes 6, the venous drainage of the

archipallium is found in the medial surface be-tween the hemispheres. The “middle olfactoryvein” originates from the ventromedial surfaceof the telencephalon and ascends dorsally be-tween the olfactory bulbs receiving blood fromthe bulbs and the primordium hippocampi. Itempties into the “sagittal sinus”(vein).

The primordium hippocampi of the tigersalamander are drained by the “vena hemis-phaerii ventromedialis”. They locate in be-tween the hemispheres and empty into the“rete of the paraphysis” 3.

The area corresponding to the archipalliumin turtle is drained by the “anterior and inter-mediate medial cerebral veins”. They lie on themedial surface of the hemisphere above thelevel of the interventricular foramen and jointhe “dorso-medial veins” 2.

Mammals

Domestic Animals

The course and tributaries of drainage of thebasal vein of dogs is similar to that of man. Butit can anastomose either medially with thegreat cerebral vein or laterally, a larger one,with the “dorsal petrosal sinus” which could becompared to the tentorial sinus in man. Arm-strong et Al 10, found that the “basal vein” ofdogs originates as far rostrally as the olfactorybulb, proceeds around the rostral perforatedsubstance and drains the optic tract, inferiorventricular vein of the lateral ventricle, thecerebral peduncle, the tuber cinereum, mamil-lary bodies, caudal perforated substance andmedial geniculate body. Both sides of the basal


28

veins can anastomose through the anastomoticveins as in man. Some rostral territories extenddorsally to the rostral lateral rhinal sulcus andinto the pseudosylvian fissure, and drain therostral pyriform area. One can see that thebasal vein of dogs takes over the drainage areaof the lateral venous group, the piriform area.

Having looked at the ventral venous groupof the infratentorium, the “ventral cerebralvein” in horses, which is homologous to the lat-eral venous group in man, drains the rhinen-cephalon and also the ventral brain stem. Thesmall veins from the medulla oblongata and thepons run to either the “basilar sinus” or the ho-mologue of the tentorial sinus in man. Thecomparable petrosal veins in dogs can drain thebrain stem and flow into the sigmoid or occipi-tal sinuses 4.

Man

We consider the ventral longitudinal venousconnection from the telencephalon all the wayfrom the ventral brain stem surface to the ven-tral myelencephalon in human embryo as theventral venous group. This venous connectioncan be found in the late embryonic period ofhuman 11.

The formation of the basal vein of Rosenthalin human consists of the anastomosis betweenthe telencephalic, diencephalic and mesen-cephalic veins 11. Its existence is sometimes infragmentary form and possibly found only inmammals. In the usual disposition, it emptiesinto the ventricular system medially. Neverthe-less, it can empty laterally into the distal trans-verse sinus which represents the primary me-tencephalic vein in the embryo (figure 4).

Hypothesis of the comparative ventral venousgroup anatomy

As we observed the pattern of the venousdrainage of primitive brains of submammals,we found that the first two venous systemswhich appeared in these animals are the oneresulting from the induction of dorsal migra-tion of the gray matter due to cephalization(the ventricular system which will be detailedin the next part of these article series), and theother that lies on the lateral surface of thebrain vesicles (the lateral venous group). Theventral venous group develops late in evolu-tion, possibly due to the appearance of the newbasal nuclei or white matter tracts such as the

neostriatum at the telencephalon, the red nu-clei and crus cerebri at the mesencephalon, andthe pontine tegmentum at the metencephalon,which need a new venous system to be drained.

Among vertebrates’ telencephalons, the evo-lution and the position of the archipallium aredifferent.

The archipallium is located ventral to therhinal sulcus in fish, amphibians and reptiles, onthe medial surface of telencephalic vesicle. Thevenous blood is drained into the dorsal midlinevein which is assumed to be the forerunner ofthe median prosencephalic vein of human em-bryo. When the neopallium and corpus callo-sum are developed in birds and mammals, it ispossible that the pattern of archipallium ve-nous drainage has been changed from the dor-sal into ventral pathway, taken over by the de-velopment of the veins that continue with theinferior ventricular vein (“ventral diencephlicvein” of human embryo) 11 and the continuouslateral-ventral venous plexus from the brainstem. The newly developed basal vein collectsthe venous blood from the archipallium, whichbecomes attenuated in higher vertebrates, emp-tying mostly in a lateral direction into thetransverse sinus and shifting the direction offlow medially into the galenic system with phy-logenic ascent. It is located medial and ventralto the rhinal sulcus in man. The former dorsaldraining pathway in lower vertebrates re-gressed leaving the pericallosal veins in thehigher ones, which can empty posteriorly intothe internal cerebral vein, basal vein or vein ofGalen, or anteriorly into the anterior cerebralvein which further drains into the basal veintypically in man. If this venous disposition fullyremains all the way along the dorsal surface ofthe corpus callosum with well-developed basalvein and inferior ventricular vein, one couldimagine the limbic arch of the cerebral vein(figure 4A). In chicken, rabbits, guinea pigs,cats, dogs and horses, the basal vein empties lat-erally into the homologue of the transverse si-nus then medially into the vein of Galen. Themedial drainage of the basal vein is secondaryfrom the phylogenic standpoint found in cer-tain primates and man 11.

The limbic area in man is drained by severalveins around itself (figure 4B). The veins on theparaterminal and paraolfactory gyri drain pos-teriorly toward the anterior cerebral vein,which empties into the anterior end of thebasal vein of Rosenthal. The anterior parts of


29

Figure 4 The ventral venous group dispositions in man. A) Fully persistent of the “limbic arch of the vein” is constructed byparts of the pericallosal vein, anterior cerebral vein, basal vein and inferior ventricular vein (blue). B) Illustration shows thearch. C) Dominant ventral venous group takes over from the lateral one (blue). D) The ventral venous group of both supra-and infratentorium (yellow) connects with the lateral one of the metencephalon (blue). E) The ventral venous group (a partof the basal vein of Rosenthal) goes into the lateral group (tentorial sinus, double arrows). F) This system also acts like a con-nection between the ventricular venous system through the striate veins and the lateral venous system through the deep mid-dle cerebral vein.

A B

C D

E F


30

Figure 5 The evolution of the pallia of the brain. A) Hagfish. B) Urodele. C) Turtle. D) Bird. E) Opossum. F) Human (afterElizabeth C.Crosby 13 with modification). Yellow: Archipallium. Blue: Paleopallium. Dark brown: Neopallium. Light brown:Striatum.

A B

DC

E F

T. AurboonyawatDiagnostic and TherapeuticNeuroradiology ServiceHôpital de Bicêtre78, Rue du Général LeclercF 94275 Le Kremlin-BicêtreCédex Paris, France


31

the cingulate gyrus and corpus callosum aredrained by the anterior pericallosal veins,which may join the inferior sagittal sinus or theanterior cerebral vein. The posterior part of thecingulate gyrus is drained by the posterior per-icallosal vein, which drains into the vein ofGalen or internal cerebral veins in thequadrigeminal cistern. The area adjoining theisthmus of the cingulate gyrus and the area sur-rounding the anterior part of the calcarine fis-sure is drained by anterior calcarine veins,which cross the quadrigeminal cistern to reachthe great vein or its tributaries. The medial partof the parahippocampal gyrus and uncus aredrained by the uncal, anterior hippocampal,and medial temporal veins, which pass mediallyto empty into the basal vein of Rosenthal in thecrural and ambient cisterns 15.

Ontogenetically 11, when one looks at the em-bryonic brain vesicles in man, the ventral mye-lencephalic (the forerunner of the inferior pet-rosal sinus and hypoglossal emissary vein), ven-tral metencephalic (the forerunner of superiorpetrosal sinus and petrosal vein), mesencephal-ic, ventral diencephalic (the forerunner of infe-rior ventricular vein), and basal part of telen-cephalic veins connect together by the “longi-tudinal veins” as long as through the ventralspinal cord veins. They are the ventral venousgroup described. Therefore, we can see long ve-nous connections between the basal vein ofRosenthal and the ventral brain stem veinswhen fully existent (figure 4E).

Considering the ventral venous group in theinfratentorial compartment, the ventral venousdrainage of the brain stem in lower vertebrates,e.g. fish, amphibians and reptiles, is dorsally ori-ented. Unfortunately, most of the reviewed ar-ticles do not pay much attention to these veins.The available evidence we had shows that theventral drainage of the brain stem becomes ev-ident in rodents 5 and domestic animals 4 on-ward. They can have connections with the samesystem as the supratentorium and the lateralvenous group.

Conclusions

It is difficult to compare the evolution of thelateral-ventral venous system among verte-brates because fully descriptive articles arescanty. Having observed the pattern of the ve-nous drainage of the spinal cord in humancompared to the brain vesicles in fish, amphib-

ians and reptiles in which the brain is still in astraight line, we found that the lateral-ventralvenous system of the brain vesicles in humanresembles that of the spinal cord. The disad-vantages of this comparative study are barelysufficient descriptive reports with differentnames for the veins used and the nature of re-viewed articles.

References

1 Richards SA: Anatomy of the veins of the head in thedomestic fowl. J Zool London, 154: 223-234, 1968.

2 Schepers GWH: The Blood Vascular System of theBrain of Testudo Geometrica. J Anat 73(pt3): 451-495,1939.

3 Roofe PG: The Endocranial Blood Vessels of Am-blystoma Tigerinum. J Comp Neurol 61(2): 257-293,1934.

4 Ghoshal NG, Koch T, Popesko P: Veins of the head andneck and thoracic wall and thoracic cavity. In: The Ve-nous Drainage of the Domestic Animals. W. B. Saun-ders Company. 39-93, 1981.

5 Majewska-Michalska E: Vascularization of the brain inguinea pig.I: Gross anatomy of the arteries and veins.Folia Morphol(Warsz) 53(4): 249-268, 1994.

6 Cecon S, Minnich B, Lametschwandtner A: Vascular-ization of the Brains of the Atlantic and Pacific Hag-fishes, Myxine glutinosa and Eptatretus stouti: A Scan-ning Electron Microscope Study of Vascular CorrosionCasts. J Morphol 253: 51-63, 2002.

7 Pearson R, ed: The Avian Brain. Academic Press Inc:London 27-33, 1972.

8 Szabó K: The Cranial Venous System in the Rat: Ana-tomical Pattern and Ontogenetic Development I. BasalDrainage. Anat Embryol (Berl) 182: 225-234, 1990.

9 Szabó K: The Cranial Venous System in the Rat:Anatomical Pattern and Ontogenetic DevelopmentII.Dorsal Drainage. Ann Anat 177: 313-322, 1995.

10 Armstrong LD, Horowitz A: The Brain Venous Systemof the Dog. Am J Anat 132: 479-490, 1971.

11 Padget DH: The development of the cranial venoussystem in man from the viewpoint of comparativeanatomy. Contrib Embryol 36: 81-151, 1957.

12 Miquel MA, Mateu JMD, Cusi V, Naidich TP: Embryo-genesis of the Veins of the Posterior Fossa: AnOverview. In: Hakuba A, Ed Surgery of the Intracra-nial Venous System. Springer: Tokyo 14-25, 1996.

13 Crosby EC, Schnitzlein HN, ed: Comparative Correla-tive Neuroanatomy of the Vertebrate Telencephalon.Macmillan Publishing Co, Inc: New York, 1982.

14 Poonkhum R, Pongmayteegul S, Meeratana W et Al:Cerebral Microvascular Architecture in the CommonTree Shrew (Tupaias Glis) Revealed by Plastic Corro-sion Casts. Microsc Res Tech 50: 411-418, 2000.

15 Rhoton AL Jr: The Cerebral Veins. Neurosurgery 51 (4Suppl): S159-205, 2002.

patterns of the cranial venous system from the comparative ... · patterns of the cranial venous...

Documents