Paper - On the nature and mode of origin of the foramen of magendie (1937)
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Wilson JT. On the nature and mode of origin of the foramen of magendie. (1937) J Anat. 71(4): 423-428 PMID 17104654
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On the Nature and Mode of Origin of the Foramen of Magendie
By J. T. Wilson
In 1906 I published a paper in which, incidentally, the question of the nature of the foramen of Magendie was discussed. I drew attention to the complete confirmation by Retzius, in his great work on the human brain in 1896, of the genuineness of the foramen originally described by Magendie. In this he fully corroborated the detailed description of the foramen provided by Key & Retzius in 1875. I further directed attention to the important work of Blake, published in 1900. This author had been drawn onwards from a study of the morphology of the foramen of Magendie to that of the entire roof of the fourth ventricle. His account of previous studies of the foramen and of the caudal region of the roof of the ventricular cavity, is still, in my opinion, the most enlightening, illustrated, as it is, by the results of his study of the comparative anatomy of the ventricular roof. His own methods of investigation appear to have been adequate, judged by present standards of technique. His conclusions concerning the nature and mode of origin of the foramen of Magendie included the following, quoted by me in 1906:
(4) That in Mammalia and Aves a caudal protrusion of the roof of the fourth ventricle is formed at some stage in their embryonic life.
(5) That in Mammalia there is a tendency to the absorption of the ventricular epithelium unless it is supported by nervous matter or by the pia of neigbbouring structures. ,
(6) That in man the caudal protrusion becomes lost, giving rise to a metapore.
(9) That in the lower Mammalia the caudal protrusion as a rule remains closed.
Although Blake was the first to recognize and elucidate fully the real nature of the foramen of Magendie as the aperture of an actual saccular evagination of the ventricular cavity, he himself points out that several observers had recognized the resemblance of the foramen to, a tubular aperture, e.g. Hoffmann, Rauber and Minot.
In my own paper of 1906 I embodied a number of stereoscopic illustrations, which, in my view, entirely bore out Blake’s interpretation of the real character of the foramen. In this same connexion I devoted some attention to the configuration of the roof of the ventricle in its extreme caudal region and its relation to the obex, of which I recognized two types, distinguished as “true” and “‘false”’, respectively; the latter being actually 4 pia-ependymal reflexion of the tela chorioidea inferior, at, and in such cases constituting, the caudal lip of the foramen of Magendie itself.
My own observations had been mainly concerned with the human adult. Blake, however, had examined the human foetal condition at the early part of the fifth month of foetal life. He figured a sagittal section through the fourth ventricle at that period which shows the dorso-caudal evagination, although its lining of ependymal epithelium had already in large part disappeared except at the neck of the sac. Comparison of this figure with his figures from other mammals left, in my opinion, little room for doubt of the validity of his interpretation of the nature of the developmental process involved, and consequently of the essential nature of the foramen of Magendie.
The question of the foramen was again raised when Prof. Weed, in 1917, published his monograph on the development of the cerebrospinal spaces in the pig and man. In this important study he recognized, in quite early embryos of both of these types, a specialized differentiation of two circumscribed areas of the expanded roof-plate of the rhombencephalon. These areas were characterized by a special thinning of the ependymal epithelium. One of them was in the more rostral region of the roof of the ventricle. The other occupied a position in the triangular caudal area of the roof. Hé named them respectively, area membranacea superior and area membranacea inferior. He showed experimentally that both of these areas exhibit a special permeability to transudation of fluid. The superior area undergoes retrogression and becomes indistinguishable at about the 20 mm. stage, in both pig and human embryos. The inferior area, on the other hand, continues to increase both in size and in functional importance and finally occupies the greater portion of what he calls the “‘ velum chorioidea inferior” (by which he obviously means the tela chorioidea inferior as indeed he names it elsewhere in his work—not the velum medullare inferior). He remarks that “‘these observations cannot solve the interesting question of a perforation of the ‘inferior velum’ to form the foramen of Magendie”’.
In another part of the paper he explicitly discusses the problem of this foramen, recognizing that this is bound up with the question of the ultimate fate of his area membranacea inferior. He recapitulates the views of previous investigators on the subject and concludes that “‘the majority of investigators to-day incline to the belief that the roof of the fourth ventricle in man is perforated to form the median foramen of Magendie”’. In the course of his discussion he makes reference to Blake’s view of an “‘outpouching becoming more and more extensive in the older embryos”’, and reports Blake as maintaining that ‘‘in man this pouch became sheared off at its neck, leaving the foramen of Magendie”’. I must point out that this is a slight misrepresentation of Blake’s statement. ‘Shearing off” at the neck is not a correct description of what Blake believed to occur, which was really an atrophy or absorption of most of the ependymal epithelium originally lining the whole of the saccular evagination of the roof of the ventricle. This is evident from Blake’s Fig. 26, already referred to.
Weed does not venture to identify himself with any one opinion although he remarks that “‘in the larger part the views presented have been in favour of the consideration of the true occurrence of the foramen of Magendie”. He says that “‘even in the largest foetuses examined there was no evidence which indicated a breaking down or a shearing off of the inferior roof of the fourth ventricle”. But inasmuch as the largest foetus at his disposal, in which the histological condition was good enough, was one of only 52 mm. the negative evidence from it cannot outweigh the positive observations of Blake from foetuses of 125 and 130 mm. stages.
To these observations of Blake I am now able to add the evidence of photographs of the condition in the human foetus which, in my opinion, afford a convincing demonstration of the validity of Blake’s explanation of the nature and the manner of origin of the foramen of Magendie. The photographs illustrate transverse sections across the medulla oblongata and fourth ventricle of a foetus of 129 mm. C.R. length—i.e. of the fifth month period—of a stage identical with that of Blake’s Fig. 26.
This foetus was obtained by operation and immediately after opening the amniotic sac it was injected with 10 per cent isotonic formalin solution.
The head was then embedded in celloidin and after decalcification was cut in continuous series of alternate thick and thin sections in accordance with the technique devised by me to afford the most advantageous exploitation of series of sections of large embryos, for low-power examination of the thick. sections, supplemented by high-power study of the alternate thin ones.
Of this series I now figure three consecutive sections, two thin and the intermediate thick section. All three are reproduced at a magnification of approximately two diameters.
Fig. 1 represents No. 36 in the group of sections in this region. It passes in front of the rostral margin of the foramen of Magendie. It affords an excellent view, in cross-section, of the tela chorioidea inferior with its paired chorioid plexuses. Dorsal to it is seen the roomy saccular cavity correctly described by Blake as a caudal or caudo-dorsal protrusion from the fourth ventricle as figured by him in his Fig. 26 in longitudinal median section. It is to be noted that at this stage this saccular cavity is clearly and entirely distinct from the numerous subarachnoid spaces surrounding the brain-stem, with which it will subsequently be incorporated by partial atrophy of its wall, thus becoming merged in the cisterna magna.
Fig. 2 shows the next succeeding section, No.‘37 of the group: it is one of the alternating thick sections. It just grazes the rostral margin of the foramen of Magendie close to the neck of the saccular ventricular diverticulum. (Note that since this section is one of the thick ones, a small strip of the ventricular floor is visible in the thickness of the section. Note also the bilateral widening of the ventricular cavity towards the basal portions of the lateral recesses. The hypophysis is seen ventrally to the median basilar cartilage.)
Fig. 3 illustrates the next succeeding section, No. 38 of the group series. Like No. 36 it is a thin section. The plane of this section passes through the foramen of Magendie itself. One can see the reflexed margins of the aperture continued dorsally to form the pia-ependymal wall of the saccular evagination of the ventricular cavity. The paramedian chorioid plexuses are seen turning dorsally, along with their ependymal covering, into the wall of the sac as a “trimming” which can be followed for a short distance, and which eventually, at later stages, will be found stranded upon the adjacent parts of the cerebellum. (On each side of the main ventricular cavity the dilated commencement of the lateral recess of the fourth ventricle is seen to be occupied by a portion of the lateral chorioid plexus.)
Under high-power examination the ependymal lining of the ventricular roof can be traced as a layer of flattened cells into the lining of the very thin wall of the saccular diverticulum. But this is already undergoing atrophy and as this atrophic degeneration progresses, and considerable areas of the wall of the saccular cavity disappear, its cavity will become incorporated with the large subarachnoid cavities which are already apparent around it, so as to constitute the large subarachnoid cistern in this situation. But the neck of the saccular evagination will be preserved more or less completely as the adult foramen of Magendie, with the reflexed margins which I formerly demonstrated in the adult specimen (Figs. 12 and 18, 1906).
The normal presence of such a foramen in the human adult has been generally, though not invariably, accepted for many decades and would seem in small need of further confirmation at so late a date as this. Nevertheless, that there still lingers some discrepancy of opinion on this question is indicated by the appearance in 1931 of a paper by Mr Lambert Rogers and Prof. West, under the title of ‘‘The foramen of Magendie”’.
It was rather surprising to find that, in the face of the statistical contributions of Gustav Retzius and others, these authors should recognize, and designate as ‘“‘a school of thought” on this problem, those who still consider the normal adult ventricular roof as “completely closed”. The evidence to the contrary is overwhelming.
But the attitude to the problem which Rogers and West take up is a peculiar one. So far are they from adherence to the “school of thought” to which they refer, that they only deny the existence of the foramen of Magendie in favour of their own thesis that the roof of the fourth ventricle in the normal adult is altogether absent over the lower or caudal portion of that cavity. The first of their numbered conclusions is that “there is no roof-plate to the lower part of the fourth ventricle, but this cavity is freely open to the cisterna magna and is here only covered in by the cerebellar tonsils”; their third conclusion is that ‘there is no relatively small and roughly circular, median aperture, as frequently depicted and regarded as the foramen of Magendie”’. I would here remark that such terms as “relatively small”, “roughly circular”, “frequently depicted”’, are not very precise or useful expressions. I would recall the fact that long ago Key & Retzius commented on the variability of the aperture they were describing, both in shape and in size. They found it rounded or rounded-oval, or rhomboidal with rounded angles; in size, as 5 mm. broad and somewhat longer ; not seldom 6 mm. and, under tension, 8 mm. or even more. These characters are clearly shown in the two well-known figures from Gustav Retzius (Das Menschenhirn, 1896, Taf. XX XVIII, fig. 5 and Taf. XL, fig. 7) both of which are reproduced by Rogers & West, who expressly state that these figures ‘showed an opening such as we describe”. But it is clear that these illustrations are in fact quite typical examples of the foramen of Magendie, and they were so regarded by their author. So far as they are concerned it seems immaterial whether we describe such a hiatus in the roof as a foramen or a “roof defect”.
The second of the conclusions formulated by Rogers & West is that “‘the upper part of the lower half of the ventricle is closed above by the inferior medullary velum which varies somewhat in extent, but. is usually narrow and makes a relatively small covering”. Again, in their conclusion 5, it is stated that “the opening extends roughly from the inferior medullary velum above to the obex below, etc.” It is clear from these statements that the authors have failed to distinguish between the inferior medullary velum and the tela chorioidea inferior. The former term is, of course, applicable only to that portion of the roof of the lower half of the fossa rhomboidalis which flanks the nodulus on either side (see Retzius’s Taf. XL, fig. 7, above referred to). It thus consists of a pair of delicate crescentic medullary laminae which extend caudally for only a few millimetres and are then continued onwards, not as a medullary velum, but as the pia-ependymal ventricular roof, the tela chorioidea inferior. The foramen of Magendie is an aperture of varying size in the lower, or caudal, triangular portion of this telar roof. It is true that when the foramen is tolerably large, its lateral margins may be not very far from the lateral taenial (ligular) attachments of the roof, which might thus be said to be “defective” in this region. Even then, however, the narrow lateral portions of the telar roof-plate may often be seen to be everted at the marginal rim of the foramen and to be continued dorsally for some distance, as was shown in the stereoscopic Figs. 12 and 13 illustrating my 1906 paper. These figures show a typical foramen of Magendie, bounded caudally by a “‘false” or membranous obex; the everted, dorsally reflected, margins of the foramen are best seen in Fig. 18, where they have been put on the stretch by pinning outwards.
It is to be noted that the tela chorioidea inferior normally extends for quite a considerable distance in front of the cranial margin of the foramen, roofing over the greater part of the lower half of the fossa rhomboidalis, before it becomes continuous with the inferior medullary velum on either side of the nodulus. The integrity of the tela chorioidea inferior, cranially to the foramen, is convincingly demonstrated in Fig. 6 of my 1906 paper, which shows a crosssection through the fourth ventricle with its intact telar roof. No one, I suggest, could look at this photograph of a cross-section of the adult human brain-stem and concur in the view of Rogers & West as to the absence of a ventricular roof to the caudal portion of the fossa rhomboidalis. 428 J.T. Wilson
Buaxg, J. A. (1900). J. comp. Neurol. vol x, p. 79
Key, A. & Rerzius ,G. (1875-6). Studien in der Anat. d. Nervensystems, &c. Erste Halfte. Stockholm. ,
Retztvs, G. (1896). Das Menschenhirn. Stockholm.
Rogers, L. & Wust, C. M. (1931). J. Anat., Lond., vol. Lxv, p. 457.
WEED, L. (1917). Contr. Embryol. Carneg. Instn, vol. v, No. 14.
Wuson, J. T. (1906). J. Anat., Lond., vol. xt, pp. 210 and 357.
EXPLANATION OF PLATE I
Figs. 1-3. Photographs of transverse sections of hindbrain region of human foetus of fifth month: 129 mm. C.R. length, magnification. x 2 approx. Fig. 1. Serial number of section 36: plane of section passes just in front of foramen of Magendie.
Fig. 2. Serial number of section 37: this is one of the alternate thick sections; its ngminal thickness is 0-25 mm., its plane of section just grazes the rostral lip of the foramen of Magendie.
Fig. 3. Serial number of section 38; this section passes through the anterior part of the opening of the foramen of Magendie.
For further details, see text. Journal of Anatomy, Vol. LX XI, Part 4 Plate I
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