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The Circumventricular Organsof the Brain

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The Circumventricular Organsof the Brain Annals of the Royal College of Surgeons of England (1982) vol. 64 The circumventricular organs of the brain: their role as possible sites for future neurosurgery D H M Woollam MA MD ScD FRCP MRCS Fellow, Tutor, and Director ofStudies in Medicine, Emmanuel College, Cambridge; University Lecturer in Anatomy, University of Cambridge Key words: BRAIN; CIRCUMVENTRICUIAR ORGANS; CEREBROSPINAL FLUID; HYDROCEPHALUS Summary cumventricular organs' (Fig. 1), notwithstanding In this paper an attempt is made to give an account ofthe the fact that in most cases very little is known possible significance ofthe circumventrzcular organs to the about their independent function. They have cer- neurosurgeon. Two major members ofthe group, the neuro- tain things in common, however. They are all hypophysis and thepineal organ, are not considered, largely located around the median ventricular system because ofthe vast literature which has already accrued on and thus in close contact with the cerebrospinal these two structures. Particular attention is paid to the fluid. Although they are highly vascularised relationship between the circulation of the cerebrospinal structures, they differ from the ordinary fluid and theproblem ofhydrocephalus, the choroidplexus, parenchyma of the brain in the ultrastructure not and the possible roles of Reissner's fibre and the only of their blood vessels but also of their subcommissural organ. ependymal, glial, and neuronal components (3). Although there is a remarkable similarity in com- Introduction parative anatomy between various mammals, this There is a group of structures which present a is by no means the case when one descends the peculiar problem, not least perhaps to the neuro- animal kingdom; in cold-blooded animals such as surgeon and to the neuroanatomist. In 1958 fish a number oforgans which are probably, ifnot Hofer (1) thought it appropriate to group these certainly, absent in mammals have been structures together under the name of the 'cir- described. FIG. 1 Diagrammatic representation of a median section of a mammalian brain with the CV'Os illustrated. Structures: OC, optic chiasma; AC, antenror commissure; CC, corpus callosum; PC, posterior commissure; MI, massa intermedia; FAM, foramen of Mlonro. CVOs: ME, median eminence; OVLT, organum vasculosum of the lamina terminalis; SFO, subfornical organ; HE, habenular ependyma; HC, habenular commissure; SCO, subcommissural organ; ARO, aqueductal recess organ; CRO, collicular recess organ; AP, area postrema. From Collins and Woollam (2). Arris and Gale Lecture delivered at the Norfolk and Norwich Hospital, Norwich, on May 8th 1981 310 D HMIl$4oollam Of the circumventricular organs (CVOs) it is area of those in the lateral ventricles is so very impracticable to say anything about the two most much greater than that of the rest combined that important, the neurohypophysis and the pineal when we are looking for an explanation as to the gland. This is not only because such vast function of the choroid plexuses it is obviously to quantities have been written about these organs the lateral ventricles that we look. Until compara- that it would take many years to give even a tively recently it was almost universally agreed precis of the information available about them. It that the purpose of the plexuses was to produce is also for two other reasons: firstly, because the the cerebrospinal fluid, although there has always other CVOs, the functions ofwhich may well bear been a small group ofworkers who regarded their on a variety of medical problems ranging from function as the absorption of the fluid. The avant obesity to mental disease, need highlighting; and garde from 1957 to the present time has always secondly, because in this fascinating group of seen something of a two-way flow, however over- structures we come face to face with one of the whelmingly in the productive direction, and there worst problems anatomy is leaving clinical prac- has been a tendency to get into very deep waters titioners to face. over the question whether a fluid can or cannot be This is the main aspect of the problem. When produced in the body's interior by a simple pro- we see something on histological or cytological cess of outpouring like the production of urine examination which resembles something else we from the urethra. This has led those ofa biophysi- assume that they are to all intents and purposes cal mind to regard the choroid plexus as an organ the same both in function and in every other way. in which work is done by the surface cells to This is not very rational, since it is quite possible excrete ions into the ventricles. Water is then that glands, for example, which produce quite attracted into the ventricles, on this theory, to re- different substances appear identical to our store the tonicity of the fluid. Looming over all present methods of investigation. theories as to the function of the choroid plexus is I have worked for 30 years on the choroid the spectre of hydrocephalus. Blockage of the in- plexus and its relation to the cerebrospinal fluid. terventricular foramen on one side can result in In 1950 it would not have been unfair to suggest dilatation of the ventricle on that side, and this that the view put forward by Halliburton in 1917, fact is in itself perhaps the strongest evidence for that the cerebrospinal fluid was an ideal physio- the belief that the main purpose of the choroid logical saline and no more, suited contemporary plexus is the production of the cerebrospinal fluid. neurological views. Why was that? Possibly it was Perhaps, to be fair to the views of a number of due to the influence of Professor Dorothy eminent authorities, I should rather have said Russell's monograph in 1949 in which she really 'the greater bulk of the cerebrospinal fluid', for laid on the line the view that hydrocephalus was there is undoubtedly some evidence which points almost invariably caused by obstruction in the to the fluid being at least augmented from a cerebrospinal fluid pathways and not by over- number of minor production points on its passage production or under-absorption of the fluid. The to its seat of absorption. picture was drawn which was not to be tackled again, and then I fear not very adequately, until In recent years electron microscopists have Sweet and his collaborators in 1956 (4) suggested drawn attention to the evidence there is of other that the cerebrospinal fluid was not made activity in the plexuses beside the production of virtually exclusively by the choroid plexuses of the cerebrospinal fluid. What is thought of as the lateral ventricles but by a wide variety of absorption may in reality be the necessary structures which, in the case of blockage lower processes of ionic readjustment which keep the down, the exceedingly complex passages leading fluid at a constant state of equilibrium and to the points of absorption in the arachnoid villi, remove from it intruding and perhaps dangerous went on in a singluarly stupid manner producing contaminants. Much attention has been devoted excessive amounts of fluid which destroved the to the movements of the cilia which serve to re- parenchyma of the brain and produced hydro- move cellular debris such as red cell corpuscles cephalus without being constrained in any way by from the surface of the plexus and to mix up the nervous or humoral control. Because of its freshly produced fluid with that of an older vin- inrinsic importance in the neurosurgery of tage in the ventricles. That this mixing process hydrocephalus the choroid plexus is the first may have wider imp!ications is something I will C8VO I will be considering. be mentioning at the end of my lecture. Two years ago the scanning electron micro- The choroid plexuses scope was used to examine occluded ventricular There are choroid plexuses in the lateral, third, catheters removed at operations for shunt revision and fourth ventricles of the brain, but the surface in hydrocephalic children (5). In 10 of the speci- The circumventnicular organs of the brain: their role as possible sitesforfuture neurosurgey 311 mens examined the catheter was plugged with About 30 years ago the late Dr James Millen what was undoubtedly choroid plexus (Fig. 2) and I discovered a technique for producing and this enabled pictures to be obtained of the hydrocephalus in the rabbit without interfering freshest choroid plexus of human origin which surgically with the animal (6). The hydrocephalic had been studied up to then (Fig. 3). It is worth infant rabbit owed its hydrocephalus to one fact while viewing some of these pictures because they and one fact only - its mother was fed on a diet do illustrate the basic simplicity of form of the deficient in vitamin A during the 20-30 weeks organ we call a choroid plexus and at the same preceding pregnancy. One animal showed time show the vast number of replications of its interest because the hydrocephalic brain had basic pattern. The first picture (Fig. 3a) shows a broken out under the skin, only the tough scanning electron micrograph of material from pyramidal tract of the major cerebral structures inside a catheter, which is clearly choroid plexus. having survived the intracerebral pressure. It is At a higher magnification both filiform and extremely unfortunate that no neurosurgeon has clavate microvilli are clearly visible and a Kolmer taken up vitamin A-induced hydrocephalus (7) in cell (ventricular macrophage tracks across the a big way in an attempt to further our knowledge picture) (Fig. 3b). not only of the natural history of hydrocephalus It is possible that straight histological studies of but also of the true functions of the choroid this kind can provide information of use to the plexus.
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