the spinal cord || the spinal cord blood vessels

Figure 5.1 Coronal section of spinal cord at C5 level from ananimal injected with diluted India ink to fill all vessels

The hemicord on the right shows the contrast between capillary abundance of grey and white matter. Numbers identify Rexed’s laminae; gr = gracilefasciculus; cu = cuneate fasciculus; dcs = dorsal corticospinal tract; lc = lateral column; vc = ventral column.

gr1

23

4

567

8

cu

dcs

9

vc

lc

The Spinal Cord Watson, Paxinos & Kayalioglu 57

surrounding them (Zagzag, 1995). In fact, vascular endothelial

growth factor (VEGF), the main molecule inducing

proliferation of endothelial cells has been recently shown to

also influence growth and differentiation of nerve cells. The

same applies to fibroblast growth factor (FGF). On the other

hand, neural growth factors such as nerve growth factor (NGF)

and brain-derived neurotrophic factor (BDNF) can also induce

angiogenesis (Raab and Plate 2007). Once development is

completed, proliferation and differentiation of nerve cells as

well as angiogenesis essentially cease and can only occur in

restricted regions of vertebrates under physiological conditions

(Risau, 1997; Bordey, 2006). In these regions, dividing nerve

cells are found associated with dividing endothelial cells

(Palmer et al., 2000).

Capillary networksEarly work on vascular microanatomy revealed that the clear

anatomical segregation of anterior, lateral and posterior

columns, composed mostly of axons and glia and central gray

matter, with neuronal bodies and synapses in addition to axons

and glia, is paralleled by a spatial variation in blood vessel

density (Figure 5.1). A large body of work was devoted in the

1930s and 1940s to detailed descriptions of the microvascular

network of the spinal cord in relation to cyto and

myeloarchitecture (Fazio, 1938; Zeman and Innes, 1963).

Several important features were discovered. The large increase

in capillary abundance characteristic of the central gray matter

5 The Spinal Cord Blood Vessels

Oscar U Scremin

Blood flow and spinal cord functionBlood flow is intricately related to function in the spinal cord,

as in the rest of the nervous system. Exchange of gases and

nutrients is commonly cited as a cardinal function of blood

circulation. However, other effects of circulatory convection,

are important for the optimal operation of nervous tissue.

Metabolic heat in active brain areas need to be cleared by

circulatory convection requiring enhancement of blood flow to

avoid a local elevation in temperature. Cooling the spinal cord

within a narrow range is associated with enhanced excitation,

inhibition and post-tetanic potentiation (Koizumi et al., 1954).

Thus, local cooling by circulatory convection could result in

enhanced synaptic efficacy. In addition, perfused blood vessels

provide a ‘sink’ for the effective dissipation by diffusion of

neurotransmitter gradients, thus accelerating the termination

of neurotransmitter action. Partial pressure of gases in the

neuronal microenvironment is also controlled by the

circulation. Given a stable metabolic CO2 production and

arterial PCO2, local PCO2 will decrease when local blood flow

increases. Decreased PCO2 is associated with an increase in

synaptic efficacy within the spinal cord (Esplin et al., 1973). All

of these functions require adaptations of the circulatory system

to match the rate of blood flow with the levels of synaptic and

metabolic activity. The first of these adaptations occurs during

development. The rate of local blood flow is dependent upon,

among other factors, hydraulic conductance which in turn

correlates directly with the number of blood vessels connected

in parallel. It is then not surprising that angiogenesis

accompanies neurogenesis. Capillaries are first detected within

the neuroepithelium of mice at day 9 (Herken et al., 1989). In

rat embryos, vascular development of the spinal cord is well

advanced by days 12-13 of development (Simon-Marin et al.,

1983).

A capillary network can be found on the surface of the human

spinal cord at the 8 mm stage and by the end of the fourth

month of pregnancy, capillaries are evenly distributed between

gray and white matter. Greater abundance of capillaries in gray

matter is later achieved and it appears to reflect the adult

pattern at term (Woollam and Millen, 1955).

Angiogenesis is central to the development and differentiation

of the nervous system, and a concerted action of a number of

angiogenic factors leads to the parallel growth and

differentiation of nerve cells and the blood vessel networks

Spinal Cord Atlas Text+Index.qxp 21/08/08 4:40 PM Page 57

7Sp

5Sp

3Sp

7Sp

5Sp

3Sp

3Sp

5SpL

7Sp

C4

T5

L3

Figure 5.2 Local arterial supply in the spinal cordAutoradiographs from an animal infused with Iodo-14C-antipyrine to measureblood flow (left side images) paired with anatomical outlines of thecorresponding spinal cord level (right side images). Darkness on theautoradiographs correlates with 14C activity. Simultaneous measurement of thetime course of arterial 14C activity allows calculation of local blood flow, to befound for different spinal cord regions in Figure 5.3. (Sp 3 = lamina 3 etc.)

58 The Spinal Cord Watson, Paxinos & Kayalioglu

greater capillary supply of the pyramidal (cortico-spinal) tract

that Craigie (Zeman and Innes, 1963) reported with twice the

number of capillaries as the fasciculus cuneatus.

Spinal cord blood flow imagingThe assessment of capillary abundance, a rather constant

parameter for any given CNS compartment, cannot offer

information about moment to moment variations in local

blood flow that may reflect neural function. The changing

requirements of energy substrates, local thermoregulation and

gaseous exchange associated with variations in functional level

of the nervous system are met by control of the hydraulic

resistance of the blood vessels system mediated by the

contractile state of vascular smooth muscle.

The advent the autoradiographic methodology (Kety et al.,

1955) allowed visualization of local blood flow with the use of

diffusible tracers such as Iodo-antipyrine (Sakurada et al.,

1978). This technique provides blood flow ‘images’, as

illustrated in Figure 5.2. These images indicate a variation of

blood flow not only between, but also within, the gray and

white matter compartments. The lowest levels of blood flow

within the white matter are found in the space corresponding

to the dorsal columns, with the exception of their deepest

portion occupied in the rat by the direct cortico-spinal fibers

that show the highest blood flow of all white matter regions

(Blisard et al., 1995). Within gray matter, the highest blood

flow is found in the ventral horn (Figures 5.2 and 5.3).

Arterial anatomyThe arterial supply to the spinal cord originates from ventral,

posterolateral and dorsal systems that extend throughout the

entire cord. One ventral spinal artery (vsp) is virtually a

continuous channel that extends from the cervical segments to

the filum terminale, analogous to the human anterior spinal

artery (Figure 5.4). This vessel can be found at the entrance of

the ventral median fissure. Two dorsal spinal arteries (dsp)

located just ventral to the entrance of the dorsal roots, also tend

to form continuous channels along the cervical, thoracic and

lumbar cords, but in this case the continuity of these channels is

often interrupted and the single vessels are in places replaced by

two or more parallel elements. Less consistently, two additional

longitudinal arterial channels formed by anastomoses between

the lateral spinal arteries (lsp) are found on the lateral surface of

the cord. The lateral spinal arteries are found about midway

between the attachment of the dorsal and that of the ventral

roots. A median dorsal spinal artery (mdosa), situated at or

close to the dorsal septum, is frequently found along all

segments of the cord (Figure 5.4). The longitudinal channels

was found associated with the presence of synapses rich in

mitochondria more than with nerve cell bodies. This was

supported by Scharrer’s observations of various central

nervous system (CNS) regions in many animal species

comparing nerve cell and mitochondria-rich synapses densities

(Scharrer, 1945). Thus, the rate of brain tissue energy exchange

was early on related to the level of vascularization. Some of the

differences in capillary densities within the gray and white

matter related to specific functional regions described by

earlier workers (Woollam et al., 1958) have been confirmed by

functional blood flow imaging as discussed below, such as the


CERVICAL THORACIC LUMBAR

Blo

od F

low

(ml/

g/m

in)

Lam 7-10 Lam 5 L am 1-4 dcs lc vc dc1.8

1.6

1.4

1.2

1.0

0.8

0.6

0.4

0.2

0

Figure 5.3 Blood flow in different laminae of the spinal cordMeans (bars) and standard errors (brackets) of local spinal cord blood flow (ml/g/min) calculated in eight normal Sprague-Dawley rats with the autoradiographictechnique. Tracer activity was acquired from regions of interest in autoradiographs including Rexed’s laminae 1-4, 5, 7-10, dorsal column (dc), dorsal corticospinaltract (dcs), lateral column (lc), and ventral column (vc).


numerous and evenly distributed, but of a smaller size, than the

ventral radicular arteries. The total number of ventral radicular

arteries merging into the anterior spinal artery in Tveten’s

study ranged from 3 to 14, with an average of 7. They were

more frequent at C5 and C6, and from T11 to L1. The lowest

frequencies of occurrence of these vessels were at C1-C3, T1-T3

and caudal to L2. Dorsal radicular arteries merging into the

dorsal spinal arteries ranged from 16 to 35, with an average of

25, and were more abundant at the level of the cervical and

lumbar enlargements. Although some authors have reported

the consistent presence of a single large ventral radicular artery

supplying most of the lumbar enlargement of the rat spinal

cord (Tveten 1976), an arrangement similar to that of the

human spinal cord (Adamkiewicz, 1881, 1882; Lazorthes et al.,

1971). This was contradicted by a later study (Schievink et al.,

1988) that identified between three and five such vessels

between the T11 and L4 segments in a series of 26 Wistar rats.

Our own material from Sprague-Dawley rats confirms the

existence of several ventral and dorsal radicular arteries

supplying the lumbar cord.

The ventral spinal artery gives off, at regular intervals, the

ventromedian or sulcal arteries (Figure 5.4). These vessels

described above are joined on the surface of the cord by

transverse anastomoses that may take the form of a well-

developed artery (arterial transverse anastomotic circle)

(Figure 5.4) or an irregular anastomotic network.

The ventral spinal artery originates rostrally from two caudally

directed branches stemming off the two vertebral arteries

before they join to form the basilar artery. Radicular arteries,

branching off deep cervical, intercostal, lumbar and sacral

arteries, enter the spinal canal through the intervertebral

foraminae along with the spinal nerves and are variable in

diameter. They divide, outside the dura mater, into branches

that follow the course of ventral and dorsal roots (ventral and

dorsal radicular arteries respectively). Some of the central

radicular arteries supply blood only to the ventral roots but a

number of them are larger and merge into the ventral spinal

artery, either directly or after dividing into a rostral and a

caudal branch. A similar arrangement is found for the dorsal

spinal arteries. The number of the larger ventral and dorsal root

arteries that contribute to the ventral and dorsal spinal arteries

is quite variable. They are more abundant in the cervical and

lumbar enlargements and almost absent in the thoracic cord

(Tveten, 1976) found that dorsal radicular arteries were more


Figure 5.4 Spinal cord arterial system demonstrated with an injected contrast medium

This figure shows a coronal section, 1 mm thick, of the spinal cord (C5) injectedintraarterially with neoprene latex-black ink mixture, which does not penetratecapillaries. Ventral (vsp), dorsal (dsp), median dorsal (mdosa), and lateral (lsp)spinal arteries are labelled. Contrast is provided by the presence of injectionmaterial in small arteries and precapillary vessels. The remarkable difference inmicrovascular density of gray and white matter is apparent in this unstainedsection. Variations in capillary density are shown in Figure 5.1.


the thoracic and lumbar cords, a large ventral radicular vein

divides into a cranial small vessel continuous with the thoracic

vsv and a much larger caudal vessel continuous with the

similar sized lumbar vsv. This vein ends as a continuous

channel that follows a tortuous path along the sacral segments

and cauda equina. On the dorsal cord surface, a dorsal spinal

vein (dsv) is found ventral or adjacent to the dorso-median

spinal artery. The ventral and dorsal spinal veins are connected

by a large number of smaller veins that surround the cord,

although occasionally, and particularly at the cervical and

lumbar enlargements, prominent venous transverse

anastomotic circles can be found. Internal spinal veins drain

into the ventral or dorsomedian veins and into other vessels of

the cord surface plexus.

Spinal cord lymphatic drainageThere is no evidence for lymph vessels inside the spinal cord or

any part of the central nervous system. However, it has been

known for over a century that large tracer molecules and

particles added to the cerebrospinal fluid can be found in the

lymphatics of the head, neck and spine at a later time (Brierley

and Field 1948). Following the work of Ivanow, apparently the

first author to detect migration of India ink from the lumbar

subarachnoid space into abdominal and thoracic lymph nodes,

Brierley and Field found that carbon particles accumulated in

the dural sacs surrounding the nerve roots of the lumbo-sacral

and cervical regions. They also observed a leash of fine black

lines, possibly corresponding to lymph vessels, passing from

the region of the nerve root dural sacs towards the

paravertebral lymph nodes. Ink particles were also found in the

cervical, posterior thoracic, posterior abdominal and pelvic

lymph nodes (Brierley and Field, 1948).

The modern evidence for a route of bulk fluid flow between

interstitial and subarachnoid spaces and the lymphatics, as

detected by the efflux of large molecules (e.g. radio-iodinated

albumin), has been extensively reviewed (Bradbury and Cserr,

1985). The relative magnitude of this efflux mechanism has

been variably estimated from one third (Bradbury and Cole,

1980) to one half (Boulton et al., 1996) of that ascribed to

transfer of these molecules through blood vessels. The flow

through these pathways is slow, with peak concentrations of

radio-iodinated albumin in lymph nodes reached several hours

after injection into the cerebrospinal fluid.

Bulk flow from cerebrospinal fluid to lymph may be

particularly important due to the existence of the blood brain

barrier that greatly limits passage of large molecules such as

proteins and polar metabolic products through brain

capillaries, except for a few areas where the blood brain barrier

does not exist. It has been suggested that the lymphatic route

ascend in the ventromedian sulcus, usually in pairs destined

one to a side, and reach the medial junction between the gray

commissure and the ventral horn. They are then distributed

widely within the gray matter, giving one or more branches to

the ventral horn with collaterals to the commissure, lateral gray

column, and base of the dorsal horn. The capillary loops that

originate in these distribution vessels travel beyond the

boundary between gray and white matter and supply the

anterior and ventral portion of the lateral white columns. The

rest of the spinal cord is supplied by perforating rami from the

pial arterial network that interconnects the dorsal, dorsolateral,

and lateral longitudinal arterial channels described above.

These perforating arteries are arranged in a radial orientation

and travel through the white matter, giving occasional small

branches, to a final distribution in the gray matter. They are

designated ventral paramedian, ventrolateral, mediolateral,

dorsolateral, dorsal paramedian, and dorsomedian arteries

(Figure 5.4).

Venous anatomyAn intricate venous plexus is found on the surface of the spinal

cord. On the ventral side, a ventral spinal vein (vsv) is found

dorsal or adjacent to the ventral spinal artery. Like its arterial

counterpart, this vessel spans the entire length of the cord, but

with notable variations in calibre. The cervical portion of the

vsv parallels in size the vsa, but it is more slender at the

thoracic segments. Approximately at the junction between



other hand, when only the thoracic aorta was occluded by

an intravascular balloon without subclavian occlusion, the

residual blood flow of the cord was enough to prolong the

time of occlusion required to provoke a permanent spastic

paraplegia to more than 40 minutes. In order to obtain a

similar critical occlusion time as with the combined aortic

and subclavian occlusion, it was necessary to reduce collateral

blood flow by lowering the arterial blood pressure proximal

to the aortic occlusion from 127 to 40 mm Hg (Taira and

Marsala, 1996). Thus, the protective effect of collateral

circulation is significant even for a complete interruption of

the thoracic aorta blood flow in the rat.

Blood flow in spinal cord traumaDirect experimental trauma to the rat spinal cord induces a

decrease in gray and white matter blood flow at the site of

injury and variable alterations in segments adjacent to the site

of trauma (Rivlin and Tator, 1978; Tei et al., 2005). The severity

of blood flow reduction correlates with the functional deficits

(Fehlings et al., 1989; Holtz et al., 1990). Time course studies

have indicated that blood flow remains at low levels in cases of

severe trauma associated with paraplegia or recovers partially

over several hours in models of milder injury with functional

restoration (Rivlin and Tator, 1978; Holtz et al., 1989). Spinal

cord ischemia may play a critical role in the causation of

functional deficits associated with trauma and may limit

reparative processes.

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the spinal cord || the spinal cord blood vessels

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