10
www.centauro.it Interventional Neuroradiology 13: 335-344, 2007 335 Classifications of the intracranial venous sys- tem are found in the literature, but most of them are based on the cerebral venous anato- my of humans 2,3 . Cerebral venous variations are also reported. Some of them can be eluci- dated using ontogenetic viewpoints. Neverthe- less, an explanation using the phylogenic evolu- tion of the cranial venous system has been poorly discussed. Like phylogenic ascent, the venous system of the brain vesicles among vertebrates has been modified and relocated according to the evolu- tion of the pallia, deep nuclei and cerebellum. This study devises a new classification of pat- terns of cranial venous system and focuses on the evolution of the dorsal venous system among vertebrates, which is associated with the development of the neopallium and neocere- bellum. Material and Methods Literature on the cranial venous anatomy in vertebrates was reviewed. Using the area of ve- nous drainage, the veins involved and their functions, we classify the cranial venous system in vertebrates into three systems compared to the venous drainage of the five brain vesicles in man. The vertebrates reviewed are fish (Myx- ine glutinosa, Eptatretus stouti, and Danio re- rio), amphibians (Amblystoma tigerinum), rep- tiles (Testudo geometrica), birds (Larus argen- Summary Many classifications of the cerebral venous system are found in the literature but they are seldom based on phylogenic study. Among ver- tebrates, venous drainage of the brain vesicles differs depending on the species. Due to the vari- ability, poorly descriptive articles, and many dif- ferent names used for the veins, the comparative study of the cranial venous system can hardly be performed in detail. The cranial venous system in vertebrates can be divided into three systems based on the evolution of the meninges and structures of the brain vesicles: the dorsal, later- al-ventral and ventricular systems. This study proposes a new classification of the venous drainage of brain vesicles using knowledge from a comparative study of verte- brates and focusing on the dorsal venous sys- tem. We found that the venous drainage of the neopallium and neocerebellum is involved with this system which may be a recent acquisition of cranial venous evolution. General Introduction The vertebrate circulatory system not only shows a difference between the anatomy and function of the arterial and venous system, but molecular differences can also be demonstrat- ed between arterial and venous endothelial cells before blood vessels are formed 1 . Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates Part I, Introduction and the Dorsal Venous System T. AURBOONYAWAT 1,2 , S. SUTHIPONGCHAI 3 , V. PEREIRA 1 , A. OZANNE 1 , P. LASJAUNIAS 1 1 Service de Neuroradiologie Diagnostique et Thérapeutique, Hôpital de Bicêtre, Le Kremlin-Bicêtre, Paris, France 2 Division of Neurosurgery, Department of Surgery, Siriraj Hospital, Mahidol University,Thailand 3 Department of Radiology, Siriraj Hospital, Mahidol University, Thailand Key words: classification, cranial venous system, comparative anatomy, vertebrates

Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

  • Upload
    others

  • View
    2

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

www.centauro.it Interventional Neuroradiology 13: 335-344, 2007

335

Classifications of the intracranial venous sys-tem are found in the literature, but most ofthem are based on the cerebral venous anato-my of humans 2,3. Cerebral venous variationsare also reported. Some of them can be eluci-dated using ontogenetic viewpoints. Neverthe-less, an explanation using the phylogenic evolu-tion of the cranial venous system has beenpoorly discussed.

Like phylogenic ascent, the venous system ofthe brain vesicles among vertebrates has beenmodified and relocated according to the evolu-tion of the pallia, deep nuclei and cerebellum.This study devises a new classification of pat-terns of cranial venous system and focuses onthe evolution of the dorsal venous systemamong vertebrates, which is associated with thedevelopment of the neopallium and neocere-bellum.

Material 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 three 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-

Summary

Many classifications of the cerebral venoussystem are found in the literature but they areseldom based on phylogenic study. Among ver-tebrates, venous drainage of the brain vesiclesdiffers depending on the species. Due to the vari-ability, poorly descriptive articles, and many dif-ferent names used for the veins, the comparativestudy of the cranial venous system can hardly beperformed in detail. The cranial venous systemin vertebrates can be divided into three systemsbased on the evolution of the meninges andstructures of the brain vesicles: the dorsal, later-al-ventral and ventricular systems.

This study proposes a new classification ofthe venous drainage of brain vesicles usingknowledge from a comparative study of verte-brates and focusing on the dorsal venous sys-tem. We found that the venous drainage of theneopallium and neocerebellum is involved withthis system which may be a recent acquisition ofcranial venous evolution.

General Introduction

The vertebrate circulatory system not onlyshows a difference between the anatomy andfunction of the arterial and venous system, butmolecular differences can also be demonstrat-ed between arterial and venous endothelialcells before blood vessels are formed 1.

Patterns of Cranial Venous System fromthe Comparative Anatomy in VertebratesPart I, Introduction and the Dorsal Venous System

T. AURBOONYAWAT1,2, S. SUTHIPONGCHAI3, V. PEREIRA1,A. OZANNE1 , P. LASJAUNIAS1

1 Service de Neuroradiologie Diagnostique et Thérapeutique, 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, cranial venous system, comparative anatomy, vertebrates

Page 2: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

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

336

tatus and Light Sussex birds), rodents (inbredSprague-Dawley strain of rats), opossums (Di-delphis virginiana), domestic animals (dogs,cats, rabbits, pigs, horses, oxen, sheep andgoats), primates (Macaca mulatta, Cebus pael-la, Papio ursinus, Cercopithecus pygerithrus,Galago senegalensis) and hominids.

Short messages from comparing five brainvesicles and spinal cord anatomy 4-6

The brain of the early embryo and of lowervertebrates is all in one plane and almost in astraight line, but that of adult higher verte-brates becomes progressively folded. In theevolution from quadrupedal mammals to bi-pedal humans, the brain stem has graduallyshifted from horizontal with the cerebrum to anearly vertical position through the foramenmagnum. The cerebral cortex is a relatively re-cent acquisition.

The telencephalon. The archipallium is oftenconsidered continguous with the olfactory cor-tex, but the extent of the archipallium variesamong species. The olfactory lobes are verylarge in lower vertebrates, but their relativesize decreases steadily as other parts of thebrain become progressively larger. The telen-cephalic vesicles (cerebral hemispheres) beginto develop in fish which have the cerebrummade of the archipallium. Amphibians developthe archipallium and paleopallium. In reptiles,the median dorsal portion broadens out toform the primitive neopallium between thearchi- and paleopallium. With marked develop-ment of the neopallium, the two more primitiveones are finally pushed medially. In man, thearchipallium makes up the hippocampus, whe-

reas the paleopallium consists of the parahip-pocampal gyrus and the primary and secondaryolfactory cortices. The growth of the neopalli-um is also responsible for a change in shape ofthe other areas, since when the occipital lobe isdeveloped, the archi- and paleopallium arepushed posteriorly, and eventually with the de-velopment of a temporal lobe, anteriorly againand ventrally as seen in most mammals, espe-cially in man.

The cerebral hemispheres of mammals areconnected by three commissures: anterior andhippocampal commisures connect the olfactoryportion of the two hemispheres, and the largecorpus callosum connects the neopallium (no-nolfactory parts). The corpus callosum appearsin mammals owing to the development of theabundant interhemispheral association fibers.

A primodial pallidum is found in primitivevertebrates. The development of the caudatenucleus and putamen (neostriatum) parallelsthe development of the thalamus and neopalli-um. This structure first appeared in reptiles, andis well-developed from birds onward.

The diencephalon. The diencephalon of ver-tebrates from fish to mammals consists of thesame three major components: epithalamus,thalamus and hypothalamus.

The mesencephalon. The tectum displays apair of prominent “optic lobes” or superior col-liculi and, caudally, “auditory lobes” or inferiorcolliculi in all vertebrates. The superior colliculiare especially large in birds. The inferior colli-culi are prominent in reptiles.

The metencephalon. The pons has two por-tions which reflect its phylogenic development,an older tegmentum lying in the floor of the4th ventricle, and a more recent acquisition, theventral portion. The cerebellum increases con-siderably in size in the phylogenic ascent ofvertebrates. Petromyzonts have only a primodi-al cerebellum (auricles) which is homologouswith the flocculi and nodules of higher verte-brates. In bony fish, the auricles are also pre-sent. The corpus of cerebellum, which is a ho-molog of the vermis, becomes developed inthese animals as in frogs. In reptiles, the corpusof the cerebellum has medial and lateral por-tions which correspond to the vermis, and theprimodium of the paravermal part of the cere-bellar hemisphere, respectively. The cerebellum

Pallium Area involved

archipallium the hippocampal formation,the dentate gyrus, the fasciolargyrus, the indusium griseum(supracallosal gyrus)

paleopallium the olfactory bulb, tract,(rhinencephalon) tubercle and striae, the anterior

olfactory nucleus,parts of the prepyriform cortex

neopallium others of the cerebral cortices

Table 1 The terms of the cortical derivatives and their areasinvolved 7.

Page 3: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

www.centauro.it Interventional Neuroradiology 13: 335-344, 2007

337

Figure 1 The evolution of the pallia of the brain. A; Hagfish, B; Urodele, C; Turtle, D; Bird, E; Opossum, F; Human (AfterElizabeth C.Crosby 8 with modification) yellow; Archipallium, blue; Paleopallium, dark brown; Neopallium, light brown;Striatum.

Figure 2 Illustration shows similar development of the primary head vein in fish, reptile, bird, rat, calf and man, respective-ly. A) A 28 hour-old zebrafish embryo. B) A late embryo of Tropidonotus natrix. C) A herring gull embryo after 5-6 days ofincubation. D) A rat embryo on day E12-17. E) A 5 week-old calf. F) A 5 mm long human embryo. (Modified from 9-14).

A

A

FED

BC

B C

FED

Page 4: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

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

338

of birds is similar to that of reptiles but it islarger and has more folia.

The myelencephalon. There are no obviousdifferences in terms of gross morphology of themedulla among vertebrates.

In fish, ten pairs of cranial nerves are identi-fied. In mammals, these ten cranial nerves have

similar relations both centrally and peripheral-ly. But the mammalian brain has incorporated apart of the neural tube which in primitive fishwas an unmodified spinal cord. The first tencranial nerves are homologous with those offish and the last two represent a modificationof nerves which in fish were the anterior spinalnerves.

The spinal cord. In cyclostomes, the gray mat-ter of the cord is a solid mass with no dorsal orventral horns. In fish, the gray matter has dorsaland ventral columns but the dorsal column is asolid mass. The cord of the urodeles resemblesthat of fish but that of salientiens shows cervicaland lumbar enlargement for the first time. Forreptiles, the cord resembles that of mammals.Reptiles with well-developed appendages havecervical and lumbar enlargement but none isfound in snakes. In birds, the gray matter is dif-ferentiated like that of mammals.

Results

The development of the cranial venous sys-tem among vertebrates is quite similar in hav-ing a primary head vein in the embryonic peri-od. But after maturation, it differs dependingon each species. Most of the neural tube is cov-ered by a primitive capillary plexus, which isdrained by three well defined veins or stems in-to the more superficially placed primary headvein (figure 2).

Proposed classifications of cranial venoussystem in vertebrates

Using the comparative anatomy of the cra-nial venous patterns in difference species ofvertebrates and areas of the venous drainage,we can organize a new system of the venousdrainage patterns of the five brain vesicles intothree different systems (Tables 2 and 3).

SubmammalsFish

Cecon et Al 18 studied the brain of Myxineglutinosa and Eptatretus stouti by scanningelectron microscopy of microvascular casts. Thestudy showed that all cerebral veins lie superfi-cially and ascend from ventral and lateral brainterritories.

The veins drain exclusively into the dorsallylocated large “sagittal sinus”. However, the

Table 2 Proposed classifications of prosencephalic venousdrainage patterns (supratentorial) in vertebrates, their relat-ed palliums and venous structures.

Venous Related Venous structuresSystem area compare to man

Dorsal venous Neopallium SSS, ISS, Str-S,system FS, TS

Lateral- Paleopallium Tentorial sinusVentral venous (middle

system cerebral vein)

Archipallium Basal veinof Rosenthal

“Ventricular lateral and Tributariessystem” 3rd ventricles of the forerunner

of the medianprosencephalic vein

of Markowski

SSS, superior sagittal sinus; ISS, inferior sagittal sinus;Str-S, straight sinus; FS, falcine sinus; TS, transverse sinus;

ICV, internal cerebral veins

Venous Related cerebellum Venous structuresSystem and brain stem compare to man

Dorsal venous Neocerebellum TS, OS, MS,system

Lateral- Archicerebellum, mesencephalicVentral venous Cerebellar pontine

system peduncles, medullary veins,Choroid plexus veins ofof 4th ventricle, cerebellopontine

Brain stem fissure

“Ventricular Paleocerebellum, paracentral andsystem” tectum superior vermian

of the midbrain veins, tectal vein

TS, transverse sinuses; OS, occipital sinuses;MS, marginal sinuses

Table 3 Proposed classification of mesencephalic and rhom-bencephalic venous drainage patterns (infratentorial) in ver-tebrates, their related parts of drainage and venous structures.

Page 5: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

www.centauro.it Interventional Neuroradiology 13: 335-344, 2007

339

meninges in fish do not develop as well asthose in mammals. Therefore, we will use sagit-tal “vein” instead of “sinus” because they didnot describe the layer of the meninges wherethe veins are located.

The sagittal vein forms rostrally from the“middle olfactory vein” and the “lateral olfac-tory vein” which drain blood from olfactorybulbs and anterior part of the telencephalon,and receives the “anterior and middle cerebralveins” and then, the “rhombencephalic vein”. Itlies on the mid-sagittal plane along the dorsalaspect of the brain vesicles and splits into theright and left “posterior cerebral veins” at thecaudal end of the medulla, which leave thebrain capsule and become the cardinal veins.The venous drainage pattern of all of the brainvesicles is dorsally oriented.

Amphibians

Roofe 16 studied the endocranial blood ves-sels of Amblytoma tigerinum. The study sho-wed very thin “vena medialis durae” and “venalateralis medialis durae” which are located inthe dura mater on the dorsal, mid-sagittal planeof the telencephalon. They empty into the“nodus vasculosus” which is a dense rete of ve-nous sinusoid structures located next to the pa-raphysis. The blood is then discharged furtherinto the “oblique sinuses’’.

They are the pair dural sinuses for flow ofblood from the “nodus vasculosus” to the reteof the “saccus endolymphaticus” and to the in-ternal jugular vein respectively. The pattern ofvenous drainage is dorsally oriented as in hag-fish.

Figure 3 Dorsal located veins or sinuses in different adult vertebrates. Even though the mid-dorsal located vein or sinusseems to be similar among vertebrates, the evolution and function are different depending on the species. A) Hagfish. B) Am-blytoma tigerinum. C) Testudo geometrica. D) Light Sussex bird. E) Guinea pig. F) Dog. (Modified from 15-20).

A B C

ED F

Page 6: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

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

340

The dural veins described do not play a ma-jor role in draining the blood from the telen-cephalon. The “dorsal pallium” (primitiveneopallium) is, in fact, drained by the “venahemisphaerii posterior” which may dischargeeither into the “oblique sinus” or the rete of the“saccus endolymphaticus. It is located on thedorsolateral surface of the hemisphere.

ReptilesSchepers et Al 15 described the venous system

of the Testudo geometrica. The veins are not si-nusoidal in character as in Amblytoma tiger-inum. The large “dorsal longitudinal vein” lyingin the arachnoidal spaces was confirmed on his-tological examination. All endocranial veinsare comparable with the intermeningeal veinsof fish. Peridural vessels can be identified butthey are diminutive. The “anastomotic vein’’unites the “dorsal longitudinal vein” with theextracranial vein. It courses between thetrigeminal and facial nerves, and then leavesthe cranial cavity. No evidence of dural venoussinuses is shown in the Tortoise brain.

BirdsThe dural venous sinuses become prominent

in birds and mammals. We found that the de-velopment of the neopallium in birds occursalong with the cranial venous sinuses, well-de-veloped meninges and arachnoid villi.

Richards 20 showed that the comparable su-perior sagittal sinus, “mid-dorsal sinus”, re-ceives venous blood from the olfactory area,communicates with the anterior part of theophthalmic system and drains the area of theforebrain and choroid plexus. It continues withthe comparable transverse sinus, “anteriorcerebral vein”, and the occipital sinus. The “an-terior cerebral vein” runs between the fore-brain and cerebellum, enters the “temporalrete” which is the extracranial venous plexuson the temporal area. The major blood drainsthrough the occipital sinus and exits the crani-um by way of the vertebral veins. The homo-logue of internal jugular vein, “the posteriorcephalic vein”, is quite small compared to thevertebral veins.

Mammals Rats

In rats 21,22, the pattern of the dorsal venoussystem is quite similar to that of man. The supe-

rior sagittal sinus, the straight sinus and thetransverse sinuses join together at the torcularherophilli. The difference is that the transversesinus runs laterally between the attached edgesof the tentorium cerebelli and branches near thepetrosquamosal fissure into the dorsally direct-ed sigmoid sinus and the laterally directed“petroquamosal sinus”. The petrosquamosal si-nus emerges through the wide petrosquamosalfissure to run extracranially between it and thetemporomandibular joint and finally empties in-to the external jugular vein. The minor venousblood is drained by the sigmoid sinus whichopens into the tiny internal jugular vein andanastomoses with the vertebral venous plexus.

Domestic animals 19,23,24

It is interesting to note that the internal jugu-lar veins in domestic animals are quite smalland non-dominant compared to the externaljugular veins and vertebral venous plexus. Thedorsal venous system of rats and this animalgroup is quite similar. The transverse sinus re-ceives major venous blood from the brain andleaves the cranium through the same foramen.Another significant pathway of venous blooddraining is the vertebral venous plexus. The sig-moid sinus in domestic animals is differentfrom that in man. It passes through the bonycanal and opens in the internal vertebral ve-nous plexus.

The veins lying on the dorsal surface of thecerebellum in the groove between the vermisand the hemispheres, “the dorsal cerebellarveins”, in sheep, dogs and oxen drain the dorsalsurface of the cerebellum and empty into eitherthe confluence of sinuses, the occipital sinuses,or the transverse sinuses. The pattern of thedorsal venous sinuses in camels is quite similarto those of domestic animals 25.

Monkeys 26,27

Primates have the pattern of intracranial ve-nous drainage in between domestic animalsand man. They have both internal and externaljugular veins dominant.

The dorsal venous system in tufted ca-puchins, rhesus monkeys, vervet monkeys, bus-hbabies, and baboons is similar to man exceptfor the presence of a prominent pretrosqua-mosal sinus which empties into the externaljugular vein.

The occipital-marginal system varies amongspecies. The occipital sinus is absent in rhesus

Page 7: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

www.centauro.it Interventional Neuroradiology 13: 335-344, 2007

341

monkeys whereas it is present in pairs in ba-boons, vervet monkeys and bushbabies.

HominidsFalk 28 studied fossil hominid skulls and found

that the early bipeds (Australopithecus afaren-sis) and robust australopithecines are charac-terized by a very high frequency of an enlargedoccipital-marginal sinus system. She stated thatselection for bipedalism was related to the epi-genetic adaptations of the circulatory systemfor emptying blood into the vertebral venousplexus, since the occipital-marginal sinus sys-tem has numerous connections with it. In ro-bust australopithecines, the transverse sinusesmay be reduced or even missing. The initial se-lection for bipedalism related to a dominantoccipital-marginal system in some hominids de-scribed above was relaxed in the other subse-quent hominids. The decrease in the frequency

of the system coincided with an increase in thefrequency of other routes for discharging ve-nous blood into the vertebral venous plexus,the foramina which conduct emissary veins.

ManMorphological changes in the dorsal venous

system in neonates after birth are the progres-sive jugular bulb maturation, gradually disap-pearance of the occipital-marginal system, thedecreasing diameter of the transverse sinuses 29

and the disappearance of the petrosquamosalsinus30,31. The persistence of the disposition canbe seen (figure 4).

Hypothesis of the comparative dorsal venoussystem anatomy

We use the term dorsal venous system be-cause it has a special kind of evolution. We in-clude all venous sinuses which relate to the

Figure 4 Some of the dorsal venous dispositions in adult man are shown.The occipital sinus can be separated (A) or single (B).The occipital-marginal system can persist as an alternative venous pathway as in hominids (C, right side). The transverse sinusis usually dominant on the right side, which receives venous blood from the superior sagittal sinus whereas the left one is usu-ally small and collects blood from the straight sinus as described ontogenetically by Padget[10] (D), or even missing (E). TheSSS can be off-midline but respecting the falx cerebri (E and F are from the same patient).When the epidural veins do not con-nect with the pial veins, the SSS can be missing leaving a long pial vein runing parallel before emptying into it (D, arrows).

A B C

D E F

Page 8: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

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

342

membranous neurocranium in this category. Itconsists of the superior sagittal sinus (SSS), in-ferior sagittal sinus (ISS), straight sinus (Str-S),falcine sinus (FS), transverse sinus (TS), andoccipital-marginal system (OM). The majorarea of venous drainage in the supratentorialcompartment involves with neopallium, little ifany deep nuclei, whereas in the infratentorialcompartment it involves the neocerebellum.

In fish, the archipallium makes up most ofthe cerebrum. Amphibians develop the archi-pallium and paleopallium, whereas reptiles de-velop the archipallium, paleopallium and a pri-mitive neopallium.

In mammals, a new processing area, theneopallium, develops between the archi- andpaleopallia. Among more advanced mammals,the neopallium expands greatly. It pushes thepaleopallium to the underside of the hemi-spheres, and the archipallium towards the mid-line. As these pallia expand, they move fromthe primitive position near to the ventricle, to amore superficial position, overgrowing the ven-tral basal ganglia.

There is some interesting evidence from thecomparative anatomy of the meninges. In fish,the membranes surrounding the neuraxis con-sist of a thin, poorly differentiated vascularmeninx primitiva closely investing the centralnervous system, and continuous with a similarinvestment of the nerve roots. In amphibians,the meninx primitiva provides an outer, dense

(periosteodural) layer, which becomes the duramater, and an inner, less dense one, the meninxsecundaria which later differentiates into arach-noid and pia mater in mammals. In reptiles, thedura mater is fairly well separated from the un-derlying arachnoid and pia mater. In birds, themeninges are rather similar to those in reptilesbut they show a higher degree of differentia-tion. It is generally assumed that in all fish theleptomeningeal space does not contain CSF asthose filled in mammals. In Hagfish, variousSelachians, Osteichthyes, and Dipnoans, theylack of either direct ventricular communicationwith, or of significant fluid diffusion flow into,leptomeningeal spaces 32. On the basis of scat-tered reports, the arachnoid villi can be as-sumed to occur in birds 33 and mammals. Theycan be found along large intracranial veins andvenous sinuses, especially on the dorsal andsome parts of the lateral venous system.

Having looked at the evolution of themeninges and arachnoid villi, along with theevolution of the neopallium and the role ofCSF absorption, it can be assumed that the dor-sal venous system and some parts of the lateralvenous group are found only in higher verte-brates.

The evolution of the dorsal venous systemshows that in fish, amphibians and reptilesmost of the venous blood from the telen-cephalon is drained dorsally into the dorsalsagittal vein which is located in the inter-

Table 4 The dorsal venous system in difference species of vertebrates and its outlets.

SSS TS PSS Str-S SS OM IJV EJV VP

Fishes – – – – – – + – +

Amphibians – – – – – – + – +

Reptiles +a – – – – – + – +

Birds + + + – – + + – +

Domestic animals + + + +/–b – – –a + +

Monkeys + + + + + +b + + +

Hominids N/A N/A N/A N/A + +b + N/A N/A

Man + + –c + + –d + – +

SSS, superior sagittal sinus; TS, transverse sinus; PSS, petrosquamosal sinus; Str-S, straight sinus; SS, sigmoid sinus;OM, occipital-marginal system; IJV, internal jugular vein; EJV, external jugular vein; VP, vertebral venous plexus

A) It does not have a major role of venous drainage of brain vesicles. B) Depending on species. C) Rare case reports30,31.D) Except for neonates, infants, and some adults.

Page 9: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

www.centauro.it Interventional Neuroradiology 13: 335-344, 2007

343

meningeal space. The dural veins of these ani-mals do not have a role in draining blood fromthe brain. With the evolution of the periduralor epidural veins and dura matter in the high-er vertebrates, it seems that the penetratingveins from the telencephalon are merged withthe epidural veins to become the dural venoussinuses found from birds onward. The majorrole of dural venous sinuses is not only dra-inage of venous blood from the developingneopallium but also drainage of the CSF fromthe cranial cavity.

However, it seems that the large dorsal lon-gitudinal vein in fish and reptiles would be theforerunner of the median prosencephalic veinof Markowski. The vein runs dorsally above thediencephalon, mesencephalon and metence-phalon. It exits the cranial cavity along with thelower cranial nerves into the internal jugularvein.

In the Tortoise, the “anastomotic vein” con-stitutes an anastomosis between the dorsal lon-gitudinal vein and the internal jugular vein out-side the cranial cavity. It passes between thetrigeminal and facial nerves and exits the cra-nial cavity. Padget 10 mentioned that, in reptiles,it is the dwindling of the head sinus so that thevenous blood of the brain can drain throughthis connection into the internal jugular vein.

Butler 34 reported that in all mammals, exceptMonotremes, without a caudally expanded cere-bral cortex the transverse sinus retains the morevertical position relative to the skull base andconsequently the petrosquamosal sinus remainsas a large channel which empties into the exter-nal jugular vein through the postglenoid fora-men. The foramen is located between the tym-panic ring and the temporo-mandibular joint. Inmonotremes, the petrosquamosal sinus coursesalong the anterior surface of the temporal bone,runs into the facial canal and then exits the cra-nium through the stylomastoid foramen. Someadult animals including man have no postgle-noid vein e.g. rabbits, pigs34 and cats 24.

The tentorium cerebelli emerged relativelylate in evolution. It is absent in fish, reptiles andamphibians. Initially when it appears in somemammals, e.g. bats, rodents and opossums, itconsisted of delicate bilateral symmetrical duralfolds not united in the midline. When the poste-rior portion of the falx cerebri became united

with the tentorium cerebelli in higher verte-brates e.g. cats, dogs, goats, deer, rabbits, mink,sheep, porpoises, wallabies, dolphins, primatesand man, the straight sinus was apparent.The si-nus is absent in fish, amphibians, reptiles, birds,bat, rodents and opossums 35.

Without the tentorium cerebelli, the trans-verse sinus could not exist as seen in cases ofparietal cephalocele with venous sinus anom-aly 36. Absence of the falx cerebri is also associ-ated with no superior sagittal sinus 37. These ob-servations strongly suggest the significant ef-fect of the falx cerebri on the development ofthe superior sagittal sinus, and that of the falxcerebelli on the development of the straight si-nus.

We doubt that the sigmoid sinus was only theemissary vein receiving blood from the trans-verse sinus in the bony canal found in domesticanimals 19 and camels 25. Therefore, we do not in-clude the sigmoid sinus with the dorsal venoussystem. The sigmoid sinus is apparent in allmammals except monotremes 34. It becomesdominant with phylogenic ascent. It can emptyinto both the vertebral venous plexus and in-ternal jugular vein depending on each species.The vertebral venous plexus has a dominantrole in draining blood from the sigmoid sinusover the internal jugular vein in rats, hedge-hogs, bats and dogs.

The occipital-marginal system becomes evi-dent from birds onward. Its dominance variesbetween species. In the adult Light Sussexbirds 20, it is the major venous outlet of all brainvesicles to the internal vertebral veins while itis non-dominant in domestic animals. It be-comes prominent in certain primates and ho-minids probably due to the epigenetic adapta-tion of the circulatory system for the uprightposition as mentioned.

Conclusions

This article describes the comparative cranialvenous system among vertebrates with specialemphasis on the dorsal venous system which isa recent acquisition in the evolution. The draw-backs of this article may stem from insufficientanatomical data due to the venous variations,different venous names, and poorly descriptiveliterature.

Page 10: Patterns of Cranial Venous System from the Comparative Anatomy in Vertebrates · 2019. 11. 17. · Literature on the cranial venous anatomy in vertebrates was reviewed. Using the

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

344

References

1 Jesús Torres-Vázquez MK, Weinstein BM: Moleculardistinction between arteries and veins. Cell Tissue Re-search 314: 43-59, 2003.

2 Rhoton ALJ: The cerebral veins. Neurosurgery 51(4Sup): S159-205, 2002.

3 Lasjaunias P, terBrugge KG, Berenstein A: eds. SurgicalNeuroangiography. 2nd ed Clinical Vascular anatomyand Variations. Vol 1, Springer, 2001.

4 Kent CG: ed Brain. Comparative Anatomy of the Ver-tebrates. Times Mirror/Mosby College Publishing. 530-543, 1987.

5 Montagna W: ed. Comparative anatomy of the centralnervous system. Comparative anatomy. John Wiley &Sons, Inc: New York 322-339, 1959.

6 Harvey B, Sarnat MGN: eds. Evolution of the NervousSystem. Oxford University Press: New York, 1974.

7 Raymond C, Truex MBC: Human Neuroanatomy. Bal-timore: The Williams& Wilkins Company, 1971.

8 Crosby EC: eds. Comparative Correlative Neuroanato-my of the Vertebrate Telencephalon. Macmillan Pub-lishing Co., Inc: New York, 1982.

9 Szabó K: The Cranial Venous System in the Rat:Anatomical Pattern and Ontogenetic Development II.Dorsal Drainage. Annals of Anatomy 177: 313-322, 1995.

10 Padget DH: The development of the cranial venoussystem in man from the viewpoint of comparativeanatomy. Contribute Embryology 36: p. 81-151, 1957.

11 MidtGard U: The Blood Vascular System in the Headof the Herring Gull (Larus argentatus). Journal ofMorphology 179: 135-152, 1984.

12 Isogai S, Horiguchi M, Weinstein BM: The VascularAnatomy of the Developing Zebrafish: An Atlas ofEmbryonic and Early Larval Development. Develop-mental Biology 230: 278-301, 2001.

13 Bruner LH: On The Cephalic Veins and Sinuses ofReptiles, with Description of a Mechanism for Raisingthe Venous Blood-Pressure in the Head. AmericanJournal of Anatomy 7(1): 1-117, 1907.

14 Von Stoeter DP, Voigt K: Rontgenologishe GefaBdar-stellung bei Embryonen und Feten. Fortschr. Rontgen-str. 126(6): 581-587, 1977.

15 Schepers GWH: The Blood Vascular System of theBrain of Testudo Geometrica. 451-495.

16 Roofe PG: The Endocranial Blood Vessels of Am-blystoma Tigerinum. The Journal of Comparative Neu-rology 61(2): 257-293, 1934.

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

18 Stephan Cecon BM, 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. Journal of Morphology 253: 51-63, 2002.

19 Ghoshal NG, Popesko P: Veins of the head and neckand thoracic wall and thoracic cavity, in The VenousDrainage of the Domestic Animals. W.B.SaundersCompany. 39-93, 1981.

20 Richards SA: Anatomy of the veins of the head in thedomestic fowl. Journal of Zoology, London 154: 223-234, 1968.

21 Szabó K: The Cranial Venous System in the Rat:Anatomical Pattern and Ontogenetic DevelopmentII.Dorsal Drainage. Annals of Anatomy 177: 313-322,1995.

22 Szabó, K: The Cranial Venous System in the Rat:Anatomical Pattern and Ontogenetic Development I.Basal Drainage. Anatomy and Embryology, 1990. 182:p. 225-234.

23 Armstrong LD: The Brain Venous System of the Dog.American Journal of Anatomy 132: 479-490.

24 Barone R: Amatomie comparée des mammifères do-mestiques, in Tome cinquième. Angiologie Vigot Frè-res. 480-531, 1996.

25 Zguigal NGG: Dural Sinuses in the Camel and TheirExtracranial Venous Connections. Anatomia, Histolo-gia, Embryologia 20: 253-260, 1991.

26 Weinstein JD JR: Studies of Intracranial and OrbitalVesculature of the Rhesus Monkey (Macaca mulatta).The Anatomical Record 144: 37-41, 1962.

27 Lake AR, V.NI, Le Roux CG, Trevor-Jones TR, De WetPD: Angiology of the brain of the baboon Papio ursi-nus, the vervet monkey. Cercopithecus pygerithrus, andthe bushbaby Galago senegalensis. American Journalof anatomy 187(3): 277-86, 1990.

28 Falk D: Evolution of Cranial Blood Drainage in Ho-minids: Enlarged Occipital/Marginal Sinuses and Emis-sary Foramina. American Journal of Physiology An-thropology 70: 311-324, 1986.

29 Okudera T, Huang YP, Ohta T, Yokota A, Nakamura Y,Maehara F, Utsunomiya H, Uemura K, Fukasawa H:Development of Posterior Fossa Dural Sinuses, Emis-sary Veins, and Jugular Bulb: Morphological and Radi-ologic Study. American Journal of Neuroradiology 15:1871-1883, 1994.

30 Chell J: The squamoso-petrous sinus: a fetal remnant.Journal of Anatomy 175: 269-271, 1991.

31 Marsot-Dupuch MG-D, Elmaleh-Berge`s M, Bon-neville F, Lasjaunias P: The petrosquamosal sinus: CTand MR finding of a rare emissary vein. AmericanJournal of Neuroradiology 22: 1186-1193, 2001.

32 Kuhlenbeck H: Morphologic Pattern of the VertebrateNeuraxis, in The central nervous system of vertebrates:a general survey of its comparative anatomy with anintroduction to the pertinent fundamental biologic andlogical concepts, S.Karger, Editor: New York 668-728,1897.

33 Kelkenberg U: Chicken arachnoid granulations: a newmodel for cerebrospinal fluid absorption in man. Neu-roreport 12(3): 553-557, 2000.

34 Butler H: The development of mammalian dural ve-nous sinuses with special reference to the postglenoidvein. Journal of Anatomy 102: 33-56, 1967.

35 Klintworth G: The Comparative Anatomy and Physiol-ogy of theTentorium Cerebelli.

36 Otsubo HS, Sato N, Ito H: Cephaloceles and abnormalvenous drainage. Child’s Nervous System 15: 329-332,1999.

37 Lasjaunias P, ter Brugge KG, Berenstein A: eds. Surgi-cal Neuroangiography. 2nd ed. Clinical and Interven-tional Aspects in Children. Vol 3, Springer, 2006.

T. Aurboonyawat, M.D.Service de NeuroradiologieDiagnostique et ThérapeutiqueHôpital de Bicêtre78, rue du Général LeclercF 94275 Le Kremlin-Bicêtre CédexParis, France