Paper - The formation of the cranial subarachnoid spaces

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Weed LH. The formation of the cranial subarachnoid spaces. (1916) Anat. Rec. 10(7): 475 - 481.

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This historic 1916 paper by Weed described human subarachnoid space development.

See Meninges Development


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The Formation of the Cranial Subarachnoid Spaces

Lewis H. Weed

From the Anatomical Laboratory of Johns Hopkins University

Introduction

One of the interesting changes in viewpoint in anatomy in the last half century has Abeentthe development of a truer conception of the fluid-containing cavities of the body. From the belief that these spaces were largely alike (i.e., serous), realization has come that there exist at least two types of these peculiar fluid-sacs, excluding from the consideration synovial cavities and bursae. For the first of the two great classes, the term ‘serous cavities’ has been retained and is now more or less generally limited to such spaces as are derived from the coelom. None of these are to be regarded as being intimate portions of the lymphatic system; rather is their connection with this closed vascular network probably more of a functional than anatomical type.


Distinguished from this first group is the second type, comprising two fluid-systems, possessing characteristic organs of elaboration and specialized mechanisms for the absorption of their individual fluids. These cavities, the cerebro-spinal spaces and the aqueous chamber of the eye, are to be considered on these bases of a specialized mode of fluid-production and drainage, as apart from the serous cavities as they are now known. The two systems, that of the central nervous system with its cerebro-spinal fluid, and that of the eye with its aqueous humor, possess an extraordinary number of analogous processes, as pointed out by Henderson (’12) and amplified by Wegefarth and Weed (’14).


Following an investigation of the physiological anatomy of the cerebro-spinal (particularly the meningeal) spaces in the ordinary laboratory mammals (Weed, ’14), attention was directed to the problems of these perimedullary cavities in the embryo.


The results of a portion of this work were reported before the Christmas meeting of the American Association of Anatomists (Weed, ’16). At that time a method of replacing the existent embryonic cerebro-spinal fluid with a foreign substance was presented, permitting the substitution to be made without increasing the normal intramedullary pressure. The procedure was employed on living pig embryos, which were subsequently kept alive for varying lengths of time in a 38° incubator. Using this method and introducing an isotonic solution of potassium ferrocyanide and iron-ammonium citrate (later precipitated as Prussian blue), evidence was presented which indicated that in pig embryos the first extraventricul.ar spread of the fluid occurred at a stage of about 14 mm. and that a total filling of the perimedullary space took place when the embryos attained a length of 26 mm.


The passage of fluid from the cerebral ventricles into the perimedullary spaces occurred only from two localized areas of epen— dymal differentiation in the two halves of the roof of the fourth ventricle. The superior of these areas was found to function actively during only a short period of growth; it was finally occluded by the changing relations of the developing rhombic structures. The more inferior area remains as a functional membrane during early fetal life and possibly throughout the adult existence. The question naturally arose as to the character of the tissues into which the replaced foreign solution was carried by the production of more of the normal cerebro-spinal fluid. For the course of this foreign solution, under the experimental conditions, must be assumed to ind:icate exactly the course and perimedullary distribution of the true cerebro-spinal fluid. Not only is the question answered by the results of these replacements, but also the histological changes are such as to give insight into the processes concerned in the formation of the subarachnoid spaces.


Surrounding the central nervous system in the stages before the outpouring of -cerebro—spinal fluid from the cerebral ventricles, is the undifferentiated perimedullary mesenchyme. This tissue is of a loose character, forming a syncytial network of rather small mesh, but fragile. The nuclei of these cells are oval; the cytoplasm is largely devoted to the long processes which connect with adjacent cells. Adhering to these cytoplasmic strands are tiny albuminous coagula, of such amount as to be hardly noticeable; also in the meshes of the mesenchyme very small quantities of this protein-material may be identified. These albuminous coagula represent undoubtedly the albumen of the tissue-fluids in these undifferentiated stages.


This rather fine—meshed mesenchyme is the tissue into which the replaced foreign solution and the embryonic cerebro-spinal fluid passes when the elaboration of the fluid exceeds the intraventricular capacity. Shortly after the initial transit of the fluid into the extraventricular spaces (at 14 mm. in the pig), the process of differentiation of the tissue to form the final subarachnoid spaces occurs. Already the cranial blastemal condensation has become evident in the basilar regions, delimiting the loose meshes of the perimedullary mesenchyme. This undifferentiated mesenchyme, then, with the outpouring of the ventricular fluid, undergoes a metamorphosis into a far looser tissue; the process is apparently one of disruption of certain of the mesenchymal strands to form the heavier and stronger trabeculae of the subarachnoid spaces.


The first evidences of this enlargementof the mesh in the periaxial mesenchyme is met with in the region around the medulla oblongata. It becomes first noticeable in stages of from 15 to 18 mm. thus following shortly the extraventricular spread of the cerebro-spinal fluid. The first change does not concern a real disruption of the syncytial strands but resembles more the spreading apart of the cell—bodies by the introduction of more fluid into the so-called tissue-spaces. Thus in a given area of this mesenchyme under consideration, the number of nuclei will diminish as the process of differentiation proceeds.


After the length of 18 mm. is passed, at which stage a great augmentation in the extraventricular spread of the cerebrospinal fluid occurs, the phenomenon of the disruption of the mesenchymal strands in the peribulbar tissues may be made out.


Many of these strands may be observed broken off, sacrificed to a few larger persisting trabeculae. The cells which give rise to these disrupted strands appear to recede until one of the larger surviving elements is reached, when they adhere and apparently aid in the future production of a permanent arachnoidal trabecula. But associated with this breaking down of the mesenchymal mesh and this formation of a smaller number of persisting strands, is another phenomenon of great importance. The larger meshes formed by the process appear filled with a fluid much richer in protein than were the original much smaller interstices. This is shown by the great quantity of the albuminous coagulum found, on histological examination, in all of the enlarged spaces in the tissue. The occurrence of this large amount of albuminous coagulum is apparently related directly to the distribution throughout this tissue of the embryonic cerebro-spinal fluid, for this embryonic fluid is very rich in proteinmaterial as can be seen by the partial filling of the embryonic cerebral ventricles with the clotted albumen. In this respect, the embryonic fluid differs markedly from the adult, where the protein—content is surprisingly low.


This general plan of the formation of the subarachnoid channels attains its maximum in the transformation of the primitive mesenchymal meshes into the larger cisternae of the adult cerebro-spinal fluid. The process is best illustrated in the posterior cerebello-bulbar angle where the cisterna cerebello-medullaris is formed. The initial process of dilatation of the mesenchymal interstices is observed in embryo pigs of 18 to -20 mm.; at a stage of 23 mm., the mesenchymal strands are already broken down in part and the exposed surfaces of these are covered by an extensive albuminous coagulum. Likewise, at this length, the larger spaces are replete with similar coagula, indicating the presence of a protein-rich fluid. During the next 10 millimeters’ growth, extensive changes in the future cisternae occur; the whole region is now an almost unbroken space, filled with a dense coagulum and interrupted by a few remaining mesenchymal strands. The outer portion of the cisterna is formed by a continuous membrane, which, after somewhat further differentiation, will become the outer continuous layer of the arachnoidea.


In addition to this formation of the subarachnoid spaces in the adult through the enlargement of the embryonic mesenchymal spaces, the perimedullary mesenchyme undergoes in these same localities condensations which result ultimately in the formation of the arachnoid membrane and the trabeculae dividing up the cavum subarachnoideale. Mention has already been made of the adhesion of the cell-bodies of the disrupted mesenchymal elements to the persisting strands——the initial step apparently in the ultimate differentiation of the mesothelial cells which line these spaces. Gradually with the increasing growth of the embryo these cells seemingly become arranged in definite columns covering the persisting arachnoidal trabeculae. At the same time a differentiation of these primitive mesenchymal elements occurs, the cells ultimately being transformed into the typical cuboidal mesothelium of the subarachnoid spaces. This difi"erentiation begins first in the basilar portions of the cranium and spreads upward, in a way similar to the course of development of the cranium and of the enlargement of the pericerebral spaces.


While such a general process as outlined accounts for the formation of the arachnoidal trabeculae and the subarachnoid spaces, it has but little bearing on the development of the outer intact membrane of the arachnoidea. This portion of the.arachnoidea (which might be termed the arachnoid membrane as distinguished from the arachnoid trabeculae) first appears as a distinct line of mesenchymal condensation separating the mesenchyme into the primitive arachnoid and dura mater. This rather thin zone of cellular density in reality represents not only the outer surface of the arachnoidea but also the inner surface of the dura mater. At first these develop in close fusion but as the length of 50 mm. is attained in fetal pigs, a separation of the two membranes over the cerebral hemispheres is possible. At this stage also a mesothelial polygonal cell-pattern may be made out on the inner. surface of the dura by silver nitrate reductions. With this cleavage of the two surfaces, the arachnoid membrane rapidly differentiates, forming an intact layer over the subarachnoid spaces. The cells covering the surface membrane seem to change gradually into the cuboidal type, similar to those covering the arachnoidal trabeculae.


The general process, then, of formation of subarachnoid spaces in the cranium of the pig, concerns a dilatation of the early mesenchymal spaces, a disruption and breaking down of certain of the syncytial strands, and a survival of certain selected strands to form the permanent subarachnoid channels. In addition to this rarefaction of the mesenchyme, there is a process of condensation in this tissue, giving rise ultimately to the arachnoid membrane and reinforcing the trabeculae. Associated with the breaking apart of the syncytium of the perimedullary mesenchyme, there are invariably found large coagula of albuminous material, apparently an index of the circulation through the spaces of the embryonic cerebro—spinal fluid.


Such a view of the formation of the arachnoidea from the middle germ layer is in accord with the investigations of His (’65), of Kolliker (’79), of Farrar (’06) and others. His has described the formation in the spinal meninges of dorsal and ventral spaces, derived from the perispinal mesenchyme. Likewise, Farrar differentiates, in the spinal meninges of the chick, three laminae, the middle one of Which alone becomes “the loose irregular reticulum of the pia—arachnoid.” The results of Sterzi’s (’O1 and ’02) researches on the comparative anatomy of the meninges afford an interesting comparison to the plan of development of the subarachnoid spaces outlined here. Streeter’s (’16) description of the mode of formation of the perilymphatic spaces indicates that in the internal ear a similar process holds.


This report presents one of the phases of a study of the formation of the cerebro-spinal spaces. The complete communication, with many illustrations, will be published, under the title of The Development of the Cerebro-Spinal Spaces in Pig and in Man as Volume 5, Number 14, of the Contributions to Embryology, Carnegie Institution of Washington, Publication No. 225.

Literature Cited

FARRAR, C. B. 1906 The embryonic pia. Am. Jour. Insanity, 63, 295.

HENDERSON, T. 1912 Glaucoma. London. .

His, W. 1865 Die Haute und Hohlen des Kérpers; ein academisches Programm. Basel.

KOLLIKER, A. 1879 Entwickelungsgeschichte des Menschen und der hoheren Thiere. Leipzig.

STERZI, G. 1901 Ricerche intorno all’anatomia comparata ed a1l’ontogenesi delle Ineningi, e considerazioni sulla filogenesi. Atti del R. Instituto Veneto di scienze, lettere ed Arti. 60, Parte II, 1101. 1902 Recherches sur Yanatomie comparée et sur Pontogenese des méninges. Arch. Ital. de Biol, 37, 257.


STREETER, G. L. 1916 Development of the Scala Vestibuli and Scala Tympani and their connections in the human embryo. Anat. Rec. 10, 250.

WEED, L. H. 1914 Studies on cerebro-spinal fluid, No. II. The theories of drainage of cerebro-spinal fluid with an analysis of the methods of investigation. Jour. Med. Research, 31 (N. S. 26), 21. No. III. The pathways of escape from the subarachnoid spaces with particular reference to the arachnoid villi. Ibid., 31 (N. S. 26), 51. No. IV. The dual source of cerebro-spinal fluid. Ibid. 31 (N. S. 26), 83. i 1916 The establishment of the circulation of cerebro-spinal fluid. Anat. Rec., 10, 256.

WEGEFARTH, P. AND WEED, L. H. 1914 The analogous processes of the cerebral and ocular fluids. Jour. Med. Research, 31 (N. S. 26), 167.



Cite this page: Hill, M.A. (2019, October 17) Embryology Paper - The formation of the cranial subarachnoid spaces. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_formation_of_the_cranial_subarachnoid_spaces

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