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J. Neurol. Neurosurg. Psychiat., 1955, 18, 97.

THE ARTERIAL SUPPLY OF THE SPINAL CORDAND ITS SIGNIFICANCE

BY

D. H. M. WOOLLAM and J. W. MILLENFrom the Department ofAnatonmy, Cambridge

It has long been recognized that an adequate the capillaries, to be visualized in the same organ.blood supply is an essential prerequisite to the In a previous paper (Millen and Woollam, 1953) anormal functioning of the neuron. The major method was described which allows such a differ-contributions to the study of the vascular architec- entiation to be made. Briefly the technique was asture of the central nervous system have naturally follows. Blue and red dispersion media were usedbeen based on the examination of the brain. for the injection. (These media were supplied byInvestigations of the arterial supply of the spinal the B.B. Chemical Co., Ltd., Ulverscroft Road,cord have been few, and have been limited to the Leicester, England, who state that the dispersionsexamination of human material obtained at necropsy ' were prepared by ball-milling pigments with a small(Adamkiewicz, 1882; Kadyi, 1889; Tureen, 1938-quantity of a highly active surface wetting agent.Suh and Alexander, 1939). It appeared therefore The blue pigment used was copper phthalocyanine,that a study of the arterial patterns of the spinal and the red was a red lake pigment.) When thecord based primarily on the use of an experimental red pigment was introduced into the heart oranimal might serve to elucidate the principles on ascending aorta it filled the arteries and arterioles,which the blood vessels are distributed to the spinal passed on into the capillaries, and filled both thecord, at the same time providing additional informa- capillaries and veins. The introduction of thetion concerning the manner of vascularization of blue pigment immediately afterwards at the samethe central nervous system in general. site pushed the red pigment on into the capillariesA major obstacle to the study of the vascular and veins, but the blue pigment did not itself enter

arrangements of the central nervous system has the capillaries. By this method a picture of thebeen the problem of differentiating the arteries whole vascular system of the animal could befrom the veins. Indeed, as recently as 1938, Campbell obtained, in which the arteries were outlined bywas obliged to point out that the extensive mono- blue pigment and the veins and capillaries by red.graph of Pfeifer (1930) on the angio-architecture of This method was used for the study of the arterialthe cerebral cortex suffered from the serious defect patterns in the rat's spinal cord which is the subjectthat the structures described as veins were in reality of the present communication.arteries and vice versa. The first experimental Materials and Methodsmethod which allowed of the certain differentiationof the cerebral arteries and veins was that introduced The spinal cords of 16 adult rats were examined. Inby Scharrer (1940). In this method the arterial each case the rat was killed with ether, and 2 ml. ofsystewasi.w.i...thageainssolut the red dispersion was injected into the ascending aorta

ssmainjectedwith a geltin solutonincor through the heart at a pressure of about 80 mm. Hg.porating rice starch, the particle size of which As soon as this injection was completed, 3 ml. of theprevented the injection mass from entering the blue dispersion was introduced in a similar fashion.capillaries. Thick sections of the brain treated in After fixation in 10%' formalin for a week, the spinalthis way were immersed in iodine solution, the cord of the animal was dissected free from the surround-starch-iodine reaction took place, and the arteries ing structures and the surface distribution of the bloodappeared deep black. Using the same technique, vessels studied and photographed in colour. Sectionsthe venous system of a similar animal was filled were then cut with the freezing microtome at 100 to 200 1,and the results compared. in the transverse, sagittal, and coronal planes at eachandtheIresultscompared. level of the spinal cord. These sections were rapidly

Scharrer's method, although allowing a clear dehydrated in ascending grades of alcohol, cleared indistinction to be made between arteries and veins, xylol, and mounted in balsam.does not enable the whole vascular system, including In addition, a number of dissecting-room specimens

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D. H. M. WOOLLAM AND J. W. MILLEN

of human spinal cords were examined. In all of thesethe arteries were outlined by the injection of red lead.

FindingsThe method employed in this investigation enabled

a clear distinction to be made between the arteriesand veins, for the arteries were filled with the bluedispersion and the veins with the red. The differencein the morphology of the vessels was exactly similarto that which Scharrer (1944) described in theintracerebral vessels, for the arteries ran in smooth,graceful curves and gave off their branches atacute angles, whereas the veins received theirtributaries at more obtuse angles.The spinal cord of the rat receives its major

arterial supply from a number of radicular arterieswhich run along the ventral nerve roots to reachthe anterior surface of the cord. Each of theseradicular vessels divides near the midline into an

ascending and a descending branch (Fig. 1). Theascending and descending branches form a midlinechain of anastomoses which run the whole lengthof the cord from the medulla to the beginning ofthe filum terminale. The uppermost ascendingbranch is joined by a descending vessel formed by theunion of branches from the vertebral arteries (Fig. 2).The radicular vessels are derived from arteries in

the neighbourhood of the vertebral column and arecomparatively constant in their arrangement. Threeor four large radicular arteries supply the cervicalregion of the spinal cord, but, in the thoracicregion, the radicular arteries are small in size,inconstant in arrangement, and only two or threein number. In the lumbar region, an extremelylarge vessel invariably runs along the second orthird lumbar nerve root. This vessel is unilateraland most often enters from the right side. It appearsto be the sole arterial supply to the whole of thelower lumbar and sacral parts of the spinal cord.This large lumbar radicular artery shows clearlythe usual divisions into ascending and descendingbranches. In the case of this vessel the divisionoccurs quite some distance from the midline andthe descending branch is much larger than theascending branch (Fig. 3).

In the cervical region the anastomoses betweenthe adjacent branches of the radicular vessels arewell marked, and the anastomotic chain has atfirst glance the appearance of a median arterycontinuing downwards from the anterior spinalvessel formed by the branches from the vertebralarteries. On more careful examination, however,its composition from the ascending and descendingbranches of the radicular arteries is apparent.The ascending and descending branches of the

thoracic radicular arteries are slender vessels whichrun considerable distances before anastomosingwith each other or with the descending branch ofthe lowest cervical artery or the small ascendingbranch of the great lumbar radicular artery (Fig. 1).In consequence the anastomoses between thesevessels are of an exiguous nature, and the anterioranastomotic chain is poorly defined and in someinstances almost discontinuous over the thoracicpart of the spinal cord.The arrangement of the arterial supply to the

anterior surface of the spinal cord of the rat (Fig. 4)may be summarized as follows:The anterior surface of the cord is supplied by

radicular arteries reaching the cord along theventral nerve roots. Each of these arteries dividesinto an ascending and a descending branch, and isprimarily responsible for the blood supply to aparticular region of the cord. The ascending anddescending branches anastomose freely inthe cervicalregion but only to a very slight extent in thethoracic region. The lumbar and sacral parts of thecord are supplied by the branches of the single greatlumbar radicular vessel. The smaller ascendingbranch of this vessel anastomoses poorly with thelowest thoracic descending branch.Only a small number of human spinal cords

have so far been examined. These showed thatthe arrangement of the radicular vessels is essentiallysimilar to that described for the rat. The vesseldescribed as the anterior spinal artery is in fact alongitudinal anastomotic chain formed by theascending and descending branches of the radiculararteries in a manner similar to that observed inthe rat, rather than a continuous vessel coursingdown the anterior midline from the medulla to thefilum terminale. The anastomoses in the thoracicregion are also, as in the rat, extremely slender.

In each segment of the rat's cord, central branchespass, from the ascending and descending branchesof the radicular arteries, into the anterior medianfissure to enter the substance of the spinal cord.Because of the distance of the bifurcation of thegreat lumbar vessel from the midline, some of thecentral branches of this vessel can be seen coursingover the anterior surface of the cord to gain theanterior fissure (Fig. 3). In general, however, thecentral branches pass directly downwards into theanterior fissure and have no course outside thenervous tissue. The central branches, as seen in theseries of coronal sections, enter the bases of theanterior horns of the grey matter and usually passalternately to the right and left sides (Fig. 5). Onentering the grey matter each vessel breaks up intoarterioles which are distributed to the anterior

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ARTERIAL SUPPLY OF THE SPINAL CORD

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THORACICFIG. 4.

FIG. 3.

LUMBAR

FIG. 1.-Anterior surface of injected spinal cord of a rat. Th(region. Two radicular arteries are shown dividing into asceland descending branches. x 4.

FIG. 2.-Anterior surface of medulla and cervical region of injspinal cord of a rat, showing the contributions from the verarteries to the midline anastomotic chain. x 4.

FIG. 3.-Anterior surface of injected spinal cord of a rat. Luregion. The large radicular artery, corresponding to the 5of Adamkiewicz in man, is shown dividing into its two brarCentral branches run on the surface of the cord towardanterior median fissure. x 4.

FIG. 4.-Diagram illustrating the arrangement of the anterior radarteries, the midline anastomotic chain, and the distribof the central arteries in the spinal cord of the rat.

FIG. 5.-Coronal section through the cervical region of the injspinal cord of a rat, showing the alternate distribution ccentral branches. x 16.

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CERVICAL

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FIG. 7.

and lateral horns and the basal part of theposterior horn (Fig. 6).The density of distribution of these central

branches varies from region to region of the cord.Thus in 1 cm. of the cervical cord 12 central branchesare distributed to each side; in 1 cm. of the lumbarcord 17 branches go to each side, whereas in thesame length of the thoracic cord only seven centralbranches are given off on each side. Because of thelong distance separating the central branches in thethoracic region, their manner of distribution differsfrom that of the other regions. In the lumbar andcervical regions the branches are distributed in a

compact, bushy manner, whereas in the thoracicregion they trail away horizontally and are lessclosely packed (Fig. 4).

In addition to the anterior anastomotic chain,there are two smaller anastomotic chains situated onthe posterior aspect of the rat's spinal cord in

FIG. 6.

P77

FIG. 8.FIn. 6 ,Transverse sections through the injted spinal cord of a

rat. x 16. (a) central artery running in the anterior medianfissure to the base of the anterior horn; (b) the distribution ofthe central branch in the substance of the grey matter.

FIG. 7.-Posterior surface of the injected spinal cord of a rat. Theanastomoses between the posterior radicular arteries are in theform of irregular loops. x 7.

FIG. 8.-Transverse section through the injected spinal cord of arat, showing a branch from a posterior radicular artery enteeingthe posterior horn of the grey mattrr. x 16

relation to the dorsal nerve roots. These are muchless constant in their situation than the anterioranastomotic chain, and they form irregular loops

between each other and in their individual courses

(Fig. 7). They are formed by radicular vessels whicharise from the arteries in the neighbourhood of thevertebral column and reach the postero-lateralsulcus by passing along the dorsal nerve roots.Central branches arise from these posterior arteriesand pierce the tip of the posterior horn of greymatter (Fig. 8) to supply that part of the posteriorhonwhich is not supplied by the central branchesof the anterior vessels. The central branches of theposterior arteries are very restricted in their distri-bution and travel upwards and downwards only toa limited extent. The density of distribution ofthese branches in the various parts of the cordclosely parallels that of the anterior central branches.

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ARTERIAL SUPPLY OF THE SPINAL CORD

DiscussionThere are no descriptions in the literature of the

arterial supply of the spinal cord in mammals otherthan man, but in current textbooks of humananatomy an anterior spinal artery is described whichstarts above by the union of branches from thevertebral arteries and traverses the cord to itslower extremity, being reinforced by a successionof small contributions from vessels in the neigh-bourhood of the spinal cord. In such descriptionsthe main emphasis is placed on the median arteryon the anterior surface of the spinal cord, and theradicular arteries are relegated to a secondaryposition. In the rat, as the illustrations show,there can be little doubt that there is anarterial anastomotic chain formed entirely by theanterior radicular arteries with the exception of theupper cervical part of the chain which is formed bythe anterior spinal branches of the vertebral arteries.Each of these anterior radicular arteries divides intoascending and descending branches which anas-tomose with a branch from the next significantradicular artery above and below. The examinationof the human spinal cord made during the courseof this investigation suggested that a similar arrange-ment is present in man, and in this respect amplifiedthe views of Suh and Alexander (1939). The clearestillustration of the manner in which the anterioranastomotic chain is formed is seen in the illustra-tion of the large lumbar radicular artery of the rat(Fig. 3), which corresponds to the arteria radicalisanterior magna described by Adamkiewicz (1882)in man. The fact that central branches supplyingthe grey matter of the spinal cord are given offfrom this artery from the point of its division wellaway from the midline leaves little doubt that itrepresents the equivalent in the rat of the arterydescribed as the " anterior spinal artery " in mosttextbooks of human anatomy. The examination ofhuman material made during the course of thisinvestigation confirmed that the arrangements areessentially similar, and indicated that the lowerthoracic, lumbar, and sacral regions of the cordreceive their blood supply from the ascending anddescending limbs of the arteria radicalis anteriormagna of Adamkiewicz which is the "anteriorspinal artery " of anatomical textbooks or" truncusarteriosus anterior" of Suh and Alexander (1939)in this situation. Furthermore this particular arteryserves to show to a marked extent a point, which isalso borne out by examination of the thoracic andcervical regions of the cord, that the arterial supplyof the spinal cord is from a series of individualarteries which anastomose with each other ratherthan from a " truncus arteriosus anterior " re-

plenished by a succession of small radicular contri-butions.The question arises as to the normal direction of

blood flow in the midline anastomotic chain.Inferiorly there can be little doubt that the bloodmust flow upwards and downwards respectively inthe ascending and descending branches of theartery of Adamkiewicz, so that from the point ofdivision of this artery blood flows downwards tothe lumbo-sacral enlargement of the cord andupwards to the thoracic region. Superiorly thevertebral artery corresponds very closely to theartery of Adamkiewicz, differing largely in the factthat it is bilateral. Its large ascending branchmeets that of the opposite side to form the basilarartery and its descending division joins its fellow ofthe other side to form the anterior spinal artery,in which the blood must flow downwards to thecervical region of the cord to meet blood enteringthe anastomotic chain in the ascending branch ofthe first significant cervical radicular artery. It isevident therefore that the blood flow in the midlineanastomotic chain is by no means all in one direc-tion, from above downwards, but that it flows inopposite directions at different levels. It followsfrom this that several water-sheds are produced atpoints more or less equidistant from the point ofdivision of the large radicular arteries into ascendingand descending branches. Such water-sheds aremost evident in the mid-thoracic portion and at thejunction of the thoracic cord with the cervical andlumbar regions.

Experimental injections into the vessels of thehuman spinal cord have produced curious andinconsistent findings. Thus, when making injectionsinto the human spinal cord at various levels, Tanon(1908) found that, whereas he could fill the vascularsystem of the entire cord from injections made intothe lumbar vessels, injections into the thoracicportion above the ninth segment filled only smallstretches, and in the cervical region the territoryinjected from each artery was only slightly larger.On the other hand Suh and Alexander (1939) foundthat injections from above could only be made intothe cervical region and from below only into thelumbar and thoracic regions. They considered thatthis was because the anastomoses between thearteries of the cervical and upper thoracic regionswere so thin as to be inadequate. Apart frompossible criticisms of the technique and injectionmedia employed, the discrepancies between theseobservations may well be explained by the effectsof post-mortem clotting in the vessels and the traumainevitably associated with the removal of the spinalcord from the cadaver. It is not unreasonable

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therefore to conclude that it is undesirable forinferences to be drawn as to the normal directionof blood flow in the midline anastomotic chainfrom the behaviour of injection media introducedafter death at a single point into the vascular systemof the isolated human spinal cord.

In the thoracic part of the spinal cord of the rat,

the midline arterial anastomosis is not only narrow

with few slender radicular contributions, it alsosends relatively few central branches into thesubstance of the cord. This arrangement is similarto that described in the human spinal cord by Suhand Alexander (1939) and Herren and Alexander(1939). Because of this arterial pattern Suh andAlexander (1939) have suggested that the vulnera-bility of the thoracic region of the spinal cord incertain diseases is due to the fact that the thoracicregion has a relatively poor blood supply. Scharrer(1944) sought to explain the early vulnerability ofthe hippocampus in carbon monoxide poisoning bythe rake-like arrangement in which the arteriessupplying the hippocampus come off the main stem.He believed that in the rake-like system theretended to be a fall in pressure towards the end of themain artery, whereas in the dichotomous systemthe pressure was even throughout the system ofultimate branches. The diagram (Fig. 4) showshow the situation of the thoracic cord resemblesthat of the hippocampus, and it may well be arguedthat the blood pressure is lower in the thoracic partof the cord than in the other parts. Suh andAlexander (1939) believed that the early suscepti-bility of the thoracic cord in subacute combineddegeneration could be explained by the anoxiceffect of pernicious anaemia on the nervous system,and the consequent early involvement of those partswhere the blood pressure was lowest. The lesions,however, which appear in the thoracic cord in thisdisease are lesions of the fibre tracts, and thecapillary bed appears to receive no arterioles in thewhite matter, the white matter being supplied fromthe capillary bed of the grey matter. If anaemia was

the cause of the damage to the white matter, onewould expect the grey matter adjoining it to beequally affected. It would therefore seem unlikelythat the pathology of subacute combined degenera-tion of the cord can readily be explained on avascular basis.

Gerard and Serota (1936) have concluded that theamount of blood reaching a neuron varies with thedegree of activity of the part of the body it supplies.The arterial supply of the spinal cord of the ratseems admirably designed to fit this principle. Thecervical and lumbar regions of the cord whichsubserve the regions capable of the greatest activity,

the limbs, are supplied with major arteries cateringfor their specific requirements, while the thoracicregion may perhaps be regarded as taking the bloodthat is left over from both. Although it is obviouslyjustifiable to comment on the manner in whicha concentration of blood in the cervical and lumbarregions of the cord is achieved, there is no reasonto assume as a natural corollary that the bloodsupply of the thoracic region is inadequate.The examination of the arterial patterns of the

spinal cord of the rat reveals two significant features.First there is the fact that the motor neurons of thespinal cord are all supplied from the same anterioranastomotic chain. Secondly there is the mannerin which the arterial supply of the spinal cord ofthe rat exactly parallels that of man. This secondobservation suggests that the spinal cord of the rataffords an excellent site for study and experimentupon the general significance of the vascular supplyto the central nervous system.

SummaryThe arterial patterns of the spinal cord of the rat

were studied by means of a technique in which,from an injection into the aorta, the arteries werefilled with a blue dispersion and the veins andcapillaries with a red. The arterial supply of therat's spinal cord was found to bear a close resem-blance to that of the human cord. From a midlineanterior anastomotic chain formed by anteriorradicular arteries central branches supply theanterior and lateral horns and the basal parts ofthe posterior horns of grey matter. This supply isless rich in the thoracic region than it is in thecervical and lumbar regions of the cord, a findingwhich may be related to, the differing metabolicrequirements of the various regions.

We wish to express our gratitude to Professor J. D.Boyd for his advice in the preparation of this paper.Our thanks are also due to Mr. T. R. L. Brooks for thephotographic work.

REFERENCESAdamkiewicz, A. (1882). S.B. Akad. Wiss. Wien. Math-nat. KI.

Abt 3, 85, 101.Campbell, A. C. P. (1938). Res. Publ. Ass. nerv. ment. Dis., 18, 69.Gerard, R. W., and Serota, H. (1936). Amer. J. Phvsiol., 116, 59.Herren, R. Y., and Alexander, L. (1939). Arch. Neurol. Psychiat.,

Chicago, 41, 678.Kadyi, H. (1889). Ober die Blutgefasse des menschlichen Rucken-

markes. Gubrynowicz and Schmidt. Lemberg.Millen, J. W., and Woollam, D. H. M. (1953). J. Anat., Lond.,

87, 114.Pfeifer, R. A. (1930). Grundlegende untersuchungen far die

Angioarchitektonik des menschlichen Gehirns. Springer,Berlin.

Scharrer, E. (1940). Anat. Rec., 78, 173.---1944). Quart. Rev. Biol., 19, 308.Suh, T. H., and Alexander, L. (1939). Arch. Neurol. Psychiat.,

Chicago, 41, 659.Tanon, L. (1908). These de Paris, No. 98. Vigot Freres, Paris.Tureen, L. L. (1938). Res. Pub!. Ass. nerv. ment. Dis., 18, 394.

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