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Brain 2006 129(5):1078-1080; doi:10.1093/brain/awl086
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© The Author (2006). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

From the Archives

Some observations on the cerebral veins. By J. E. A. O'Connell. Department of Anatomy, St Bartholomew's Hospital Medical School, London. Brain 1934: 57; 484–503.

John O'Connell (1906–2001) writes from the Department of Anatomy at St Bartholomew's Hospital, London, 3 years after qualifying in medicine in 1931, on the developmental anatomy of the cortical veins and sinuses. The work was carried out at the suggestion of Professor (Herbert Henry) Woollard (1889–1939: Professor of anatomy at St Bartholomew's Hospital, 1929–36). O'Connell's anatomical observations are illustrated by Miss Z. M. Stead. Later, O'Connell was to use this knowledge of embryology to explain abnormal anatomy, in suggesting that craniopagus twins can be classified as partial—where the union is of limited extent—or total—a situationin which two brains lie within a single cranium (J. E. A. O'Connell. Craniopagus twins: surgical anatomy and embryology and their implications. Journal of Neurology Neurosurgery and Psychiatry 1976; 39: 1–22). The partial cases represent localized fusion of the cranium and brain coverings but not of deeper structures. The prospect for separation is good. The total cases are more problematic. Essentially, two heads lie within one deformed skull and several structures, notably the circulation, are shared. Whilst the arterial supplies do not anastomose, a single circular venous sinus commonly lies at the point of fusion with drainage from one twin to the transverse sinus of the other, and vice versa. It is in the attempt to reconcile this situation that, as often as not, vascular catastrophes intervene and usually prove fatal for one of the twins. Indeed, by 1976, O'Connell had reached the conclusion that one twin is bound not to survive separation of total craniopagus owing to the venous infarction imposed on one partner in securing an autonomous vascular circulation for the other.

John O'Connell's 1934 study is motivated by the notion that, whereas the microanatomy of draining veins in most parts of the body ‘has little interest’, rather more orderly and predictable arrangements exist for the course of the superior cortical veins and their relationships to the gyri and sulci of the cerebral cortex. First, this is a study of the normal anatomy in five foetuses. Out of the lateral fissure emerge tributaries of the middle cerebral vein: 1–2 reach the frontal pole; 1–2 drop down over the temporal lobe; and 5–6 pass obliquely over the remaining surface of the hemisphere (Fig. 1). Most converge on the superior sagittal and transverse sinuses, respectively, increasing in size as they near those structures and the eventual calibre of each being inversely proportional to the number of draining veins. In brains with larger numbers of such vessels, superficial cortical veins tend to reach the sinus in clusters. The angle of insertion is at right angles for the frontal veins; and increasingly angled for the posterior vessels so that the direction of arrival points towards the frontal pole for the more posterior placed cortical veins—the angle changing from 90° (at the front) to 20° (at the back).


Figure 1
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Fig. 1 Drawing of a specimen, showing cortical veins in a foetus at term (a large infant). The radiation of the vessels from the stem of the lateral fissure is seen—the majority passing to the superior sagittal sinus, but two to the transverse sinus. This specimen also shows that as regards their direction, the superior cortical veins are in two portions: (i) that radiating from the lateral fissure and (ii) the terminal portion that changes its direction as it enters the sinus. A, vein from the medial surface of hemisphere passing anteriorly to unite with vein B immediately before it terminates in sinus.

 
Next, O'Connell considers whether, in the foetus, the larger cortical veins provide landmarks for the underlying cerebral structures. Generally, two vessels straddle the frontal lobe, and three the parietal. Whereas no vessel is consistently found overlying the occipital lobe itself, one invariably traverses the parieto-occipital fissure. Perhaps, there are veins that—at least in their inferior sections—correspond to the pre-central, central and post-central sulci. But as these approach the sinus, a supply from medial veins may join those draining the lateral surface of the hemispheres and the latter tend to merge. As a result, no relationship of the cerebral veins to gyral brain structure persists. Vessels tend to lie within a sulcus rather than riding the surface of a nearby gyrus. Perhaps this assists the circulation, for mechanical reasons. Each of the three main sulci that separate the opening of the opercula of the insula accommodate a large branch of the middle cerebral vein as these emerge from the lateral fissure to distribute over the surface of the hemisphere.

Unsurprisingly, the general arrangements of origin, number and distribution of draining veins is similar in the adult cerebrum. Thus, the tributaries of the middle cerebral vein, emerging from the lateral fissure, also eventually reach the superior sagittal sinus. Some anatomical ‘distortions’, or differences from the foetal arrangement, may arise as the result of post-natal growth of the frontal lobes, tending also to produce a more acute angle of entry in this front part of the sinus. That said, the portal of entry does show some special features. Strands of epithelium create the impression of valves—but none such exist. Rather, the lumen of the sinus is parcellated into ventral and dorsal portions, both at the front and at the back. The most prominent of these divisions corresponds to the intrusion of arachnoid villi into the lumen of the sinus. The feeding veins tend to enter not through the lacunae laterales but directly into the sinus and through the inferior sections of these folds. The feeding veins attach for several centimetres to the outer surface of the sinus before penetrating the outer wall, and then entering the lumen (Figs 2 and 3).


Figure 2
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Fig. 2 Diagram to show platform extending between the walls of the superior sagittal sinus and subdividing its lumen into dorsal and ventral parts. Several arachnoid granulations project into the ventral subdivision.

 

Figure 3
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Fig. 3 Diagram of the falx cerebri in an adult. This shows the manner in which a superior cortical vein having reached the lateral wall of the superior sagittal sinus becomes adherent to it and courses anteriorly and slightly inferior along it. B, point at which vein becomes adherent to sinus. A, point at which vein, having undergone a terminal dilation, opens into the sinus.

 
O'Connell takes as his starting point for understanding the evolution of these arrangements the already accepted vascular embryology of the foetus. ‘The primary head vein with its three—anterior, middle and posterior—plexuses is well known, the anterior and middle plexuses later fusing to form a single anterior plexus. The vessels in this anterior plexus become separated into three layers: a superficial, which forms the superficial vessels of the head; an intermediate, which forms the dural sinuses; and a deep portion which intimately covers the nervous tissue and later forms the cerebral veins’. The former communicate only through the emissary veins of the skull whereas the latter have more persistent connections. ‘The cerebral veins have ... important connections with the dural system, firstly in the region where both sets of vessels drain into the primary head vein, and secondly, on the dorsal aspect of the cerebrum close to the mid-line. In this latter region there is an anastomosis between the vessels of opposite sides which is called the sagittal plexus, and from this the superior and inferior sagittal sinuses and the straight sinus are developed’.

In the developing and mature brain, everything radiates out from the middle cerebral vein, across the surface of the hemispheres. Individual vessels are dragged along the surface and then angled into the sinus as a result of growth patterns in the underlying lobes of the cerebrum. ‘The direction of any one of the cortical veins depends upon the direction of growth of the particular part of the cerebrum to which it is related’. Put the other way, the trajectory of the vessels is an indication of the amount of growth that affects each lobe of the cerebrum. And the valves, ‘chords of Willis’ and platforms within the sinuses are the remnants of the plexiform arrangements that made up the original anastomoses. More specifically, the cortical veins do not enter the sinus through the lacunae laterales, as others had previously suggested, because these are vestigial components of the few connections between the superficial and middle embryological strata—the meningeal and diploic veins. The extent of these lateral extensions—at first frontal, parietal and occipital—increases with adult age so that they are more or less continuous along the length of the sinus in those past middle age (Fig. 4). Their floor is carpeted with arachnoid granulations projecting into the lumen of the sagittal sinus. These structures are absent in the foetus but appear with maturation in the adult. Indeed, it is the growth of arachnoid granulations that O'Connell considers to be the stimulus for maturation of the collateral track of the lacunae laterales. In the present era where venous thrombosis seems such a common event—either through better recognition or a genuine increase in frequency—it may be significant that O'Connell notes: ‘while the superior saggital sinus is itself often full of blood clot, no trace of this is ever found in the lacunae laterales ... the absence of clot ... suggests that these contain under normal circumstances little blood, and probably mainly cerebrospinal fluid and projecting granulations. As this fluid passes from the lacunae into the sinus, the pressure in the former must be higher than in the latter, and thus the flow of blood into the lacunae is prevented ... to regard the arachnoid granulations as pathological formations ... as the result of increased intracranial tension would appear to be an error’.


Figure 4
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Fig. 4 Drawing of a dissection of the superior sagittal sinus and lacunae laterales in a subject aged 55. The confluent lacunae are again seen and are everywhere carpeted with arachnoid granulations except over the cortical veins as they pass medially beneath the floor. Bristles have again been passed through the larger veins into the sinus to demonstrate this point.

 
It was his early studies on development of the venous anatomy of the cerebral hemispheres that, 42 years later, helped O'Connell to understand why, in craniopagus, the sagittal sinus cannot develop and is replaced by a circumferential structure made up of the venous plexuses of each apposed brain, draining at the front and back into the lateral sinus of each twin, respectively. Thus, much of the venous blood from each child's cerebrum, normally carried posteriorly through its own sagittal sinus and out of the head, pours into the partner's venous cerebral drainage and great vessels. Restoring the anatomy of one twin ensures the ‘Catch 22’ consequence of venous infarction in the other. Reflecting back to 1934, O'Connell remembered the anastomotic veins radiating across the cerebral hemispheres and speculated that these might be exploited to provide personal venous drainage for each twin—and hence, dual survival on separation: ‘The problem has not been solved but recognition of a problem can be a step towards its solution’. In their magisterial review, James Stone and James Goodrich bring up to date the classification and experience of this ‘highly fascinating accident of nature’.

Alastair Compston

Cambridge


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