Talk:Paper - The lamina terminalis and its relation to the fornix system (1911)
THE LAMINA TERMINALIS AND ITS RELATION TO THE FORNIX SYSTEM! By Joun Cameron, M.D., DSc. F.RS.E., Lecturer on Anatomy, Middlesex Hospital Medical School.
(1) THE Lamina TERMINALIS IN THE EARLY STAGES.
In the early human embryo, that is to say, from the beginning of the second to about the middle of the third month, the lateral limitations of the lamina terminalis cannot be defined with any degree of accuracy. Up to the latter date it simply exists as that portion of the cerebral wall closing in the cavity of the fore-brain anteriorly, and merging with the hemisphere vesicles laterally. During the early part of the third month a slight folding of the cerebral wall takes place on each side to mark the line of the arcuate fissure (fig. 1). Hochstetter (7) pointed out some years ago that the early fissures of the hemispheres were really artefacts produced during the fixation of the tissues. The arcuate fissure does not appear, however, to be merely an adventitious infolding, but is really of great morphological importance, for it will be shown presently that the whole of the area of cerebral wall included between the right and left fissures becomes traversed in a fore and aft direction by longitudinal fibres. The latter, as will be indicated later, may all be included under the heading of “fornix system.” The remarkable fact is that this system has its lateral limits exactly at the points where the arcuate fissures merge with the mesial walls of the hemispheres (fig. 2). This is surely sufficient guarantee to magnify still further the important significance of these fissures. In 1896 Elliot Smith (9) described a well-marked arcuate fissure in the brain of a foetal ornithorhynchus, and at the same time pointed out that it had “an exact morphological significance, being strictly confined to the region which is to become hippocampus.” .
A study of the further development of the lamina between the arcuate fissures will be found to disclose several features of interest. The first remarkable change is that it folds upon itself in a downward direction about the middle of the third month. The result is that the two halves come into close apposition, thus forming the lateral boundaries of a groove
1 Part of a paper communicated at the International Congress of Anatomy, Brussels, 1910. 212
Dr John Cameron
Cerebral hemisphere. _ Lamina terminalis,
Fie. 1.—Coronal section of the cerebral hemispheres and
lamina terminalis of an embryo corresponding to the early part of the third month.
_-- Mesial wall of hemisphere.
Fornix zone. ._ Le-* Arcuate fissure.
Sand! . . . .
“*, Lamina terminalis.
Fic. 2.—Coronal section of the lamina terminalis and arcuate fissures of an embryo corresponding to the latter part of
the third month. Note the continuity of the fornix zone from side to side. .
or “gutter.” The latter commences behind, about the level of the posterior margin of the foramen of Monro, and gradually deepens when traced forwards. This increase in depth is explained by the fact that the width The Lamina Terminalis and its Relation to the Fornix System 213
between the arcuate fissures is very slight opposite the foramen of Monro, but rapidly increases in a forward direction, thus furnishing a greater area of wall for the purposes of the folding. The formation of this gutter was found to occur in all the mammalian types studied, namely, the rabbit, rat, guinea-pig, and man. Figs. 3 to 14 illustrate the result of this folding. They represent a series of transverse sections through the region of the lamina terminalis of a thirteen-day rabbit embryo, starting opposite the posterior margin of the foramen of Monro and proceeding in a forward direction. The figures have been drawn from every third section, so that, numbered from behind, they are the Ist, 4th, 7th, 10th, 13th, 16th, 19th, 22nd, 25th, 28th, 31st, and 34th of the series. In fig. 3 the foramen of Monro is shown on the left side with, above it; the involution of the lateral edge of the epithelial roof of the third ventricle, to form part of the choroid plexus. The arcuate fissures may be observed as prominent objects on the mesial aspects of the hemispheres. The broad black band represented as lining each of these fissures is part of the fornix system, the fore and aft fibres of which are cut transversely in the section. The position of the remainder of the fornix fibres is to be looked for in the mesial wall of the descending horn, and is indicated by the thick black spots in figs. 3, 4, 5, and 6. It will be recognised from these figures that in order to reach the latter situation the fibres must arch dorsally to both the foramen of Monro and the velum interpositum. Elliot Smith (18) has shown that the matrix for these fornix fibres is the “caudal prolongation of the paraterminal body.” In fig. 4 the lamina terminalis makes its appearance, and is shown folding upon itself. The resultant gutter is, however, very shallow at this level, owing to the narrowness of the lamina. The fornix fibres are now seen to form a continuous system from side to side across the mesial plane, terminating exactly at the point where the arcuate fissures merge with the mesial hemisphere walls. On examining in turn figs. 5, 6, 7, 8, and 9, the depth of the gutter will be observed to have greatly increased, whilst the sides are getting into closer apposition. In these figures the interruptions in the continuity of the black band indicate approximately the points at which the fibres of the corpus callosum break up the fornix system into its constituent elements. In figs. 10, 11, and 12 the lateral walls of the gutter are now in close contact, and.in figs. 13 and 14 are shown opening out again. It will be observed further that in the last two figures of the series the fornix band is rapidly becoming smaller. It fact it was found to disappear immediately anterior to section 34 (fig. 14). Not only so, but the arcuate fissures ceased to exist at about the same point (compare figs. 3 and 14). This intimate relationship of these to the fornix system is certainly remarkable. It will now be recognised from the series of figs. 3 to 14 that the bottom of 214 Dr John Cameron
Fie, 5. Fic. 6. The Lamina Terminalis and its Relation to the Fornix System 215
VOL. XLV. (THIRD SER. VOL. VI.)—APRIL 1911. 15 216 Dr John Cameron
Fic. 11. Fig. 12.
Fie, 13. Fic. 14. The Lamina Terminalis and its Relation to the Fornix System 217
Choroid plexus. ’ ¢
. bt : Fornix zone, *” ~ * Descending horn.
Fic. 15.—The inner walls of the descending horns, showing the fornix zones. Embryo corresponding to the latter part of the third month, .
3rd vent. Fic. 16.—Coronal section of the lamina terminalis and arcuate fissures of a 18th-day rabbit embryo, showing the relation of the falx cerebri to these. : . 218 Dr John Cameron
the gutter forms the lamina terminalis, whilst its lateral walls become the paraterminal bodies.
The relation of the developing falx cerebri to the arcuate fissures and lamina terminalis is rather significant. Before folding occurs, the mesoblastic tissue between the two hemispheres is in contact with the surface of the lamina. When, however, the gutter is produced,-the depth between the hemispheres is, of course, increased ;. but, notwithstanding this, the rudiment of the falx remains in the same relative position, which now corresponds to about the lower margins of the arcuate fissures (compare figs.4 to 14).
(2) THE DEVELOPMENT OF THE FoRNIX FIBRES.
The stratum of fore and aft fornix fibres, as previously stated, terminates laterally at the points where the margins of the arcuate fissures merge with
Mesial hemisphere wall. °**+ _,
- s. Choroid plexus
of lat. vent.
Fornix zone, .--="
Fic. 17.—The arcuate fissure and neighbouring parts of the mesial hemisphere wall and paraterminal body. Embryo corresponding to the early part of the third month. The fornix system is represented by the clear zone at the bottom of the arcuate fissure.
the mesial walls of the hemispheres (compare figs. 3 to 14). Fig. 17 represents a coronal section of the arcuate fissure and neighbouring parts of the cerebral wall and paraterminal body of a 56-mm. human embryo}!
1 I wish to express my deep indebtedness to Professor E. Fawcett for kindly granting
permission to take a photomicrograph of this specimen, as also for unlimited facilities to study material from his valuable embryological series. The Lamina Terminalis and its Relation to the Fornix System 219
preserved in excellent condition. Above the ‘fissure is the mesial hemisphere wall with its well-defined zone of embryonic nerve cells. Immediately on entering the fissure it will be observed that this zone becomes gradually replaced by the commencement of the fornix system. The latter may be readily traced downwards through the arcuate fissure into the paraterminal body as the clear band situated between the rudiments of the nerve cells and the superficial surface (on the left). These fibres thus occupy that part of the wall of the cerebral vesicle designated by His the randschlever. A closer inspection of fig. 17 will, moreover, demonstrate another interesting fact ; for it may be noted that as the fornix system becomes more and more marked, the zone of embryonic nerve cells or neuroblasts gets rapidly narrower and narrower. As a matter of fact, the fornix fibres are developing at the expense of these neuroblasts, which are being transformed into what may be not inaptly termed newro-fibroblasts. A study of the latter elements in longitudinal sections of the paraterminal body revealed the
Fic. 18.—Fibrillation of the syncytium to form the fibres of the fornix 16th-day rabbit embryo. x 500.
interesting fact that their processes fused together to form what has recently been termed by Held! the newrencytium, or the syncytiwm of Cameron and Milligan (4). In this cytoplasmic material a delicate fibrillation develops, thus giving rise to the axons of the fornix system (fig. 18). That is to say, the histogenesis of each of these axons is not brought about by the outgrowth of a process from a single neuroblast, but is the result of the fibrillation of cytoplasmic material derived from several cell-elements, and is thus multicellular in character. In this way, and in this way alone, can these neuro-fibroblasts exercise their formative function. It may be mentioned that these conclusions confirm recent investigations on the development of the olfactory nerves (18), the auditory nerve (4), the optic nerve (2), and the spinal nerves (3 and 8).
It seemed to the writer desirable to obtain a sagittal section of the paraterminal body in order to demonstrate this fore and aft system. This, however, proved a more difficult task than was at first imagined. Fig. 19 represents the result of fairly successful sectioning, and is probably from a stage corresponding to a sixteenth-day rabbit embryo. The triangular
1 Die Entwickelung des Nervengewebes bei den Wirbelthieren, 1910. 220 Dr John Cameron
opening in the middle is the foramen of Monro, immediately above which is the paraterminal body cut sagittally, thus showing the fore and aft disposition of the fornix fibres. It was manifestly impossible to demonstrate the whole course of these in one section. Below and in front (to the left) of the foramen of Monro, however, the fibres again become very prominent, and appear to terminate immediately below the foramen in a well-defined collection of nerve cells. The latter was found to constitute the rudiment of the corpus mammillare, from which the system is continued upwards and
Fornix fibres in paraterminal body.
Arcuate fiss. _-* 3rd vent.
-¢ Optic. thal.
- Bundle of Vicq
Fic. 19.—Sagittal section to show the arrangement of the fore and aft fornix fibres in the brain of a 16th-day rabbit embryo. The triangular opening in the centre of the figure is the foramen of Monro.
backwards behind (to the right of) the foramen into the optic thalamus, represented by the dense mass of cell-elements bounding the cavity of the third ventricle. The manner in which the constituent fibres of the bundle of Vieq d’Azyr spread out amongst the cell-elements of the optic thalamus is thus demonstrated. The identity of the corpus mammillare and the bundle of Vicq d’Azyr in fig. 19 was confirmed by making reconstructions from sagittal sections of that region.
The anterior commissure cannot be identified in fig. 19 owing to its being a very low-power photomicrograph. The position of its main bundles can, however, be recognised (immediately to the left of the letters a. c.) by higher The Lamina Terminalis and its Relation to the Fornix System 221
powers of magnification. As a result, it will be observed that in fig. 19 the fornix fibres are passing partly precommissurally and partly postcommissurally. The cleft in the centre of the upper margin of fig. 19 immediately above the paraterminal body is the arcuate fissure cut sagittally.
(3) Tue. EFFECT OF THE CoRPUS CALLOSUM UPON THE DISPOSITION OF THE FoRNIX SYSTEM.
The development of the corpus callosum produces a remarkable effect upon the disposition of the fornix fibres, for it divides these into what may
On, tr. Oi he
ee Te Hipp. Con, Gya. Dent.
Fic. 20.—Arrangement of the fibres of the fornix system in a brain minus a corpus callosum.
be termed supracallosal, intracallosal, and infracallosal groups. If these be studied in the series of figs. 8, 9, 10, 11, and 12, it will be recognised that even at that early stage the supracallosal group consists of the fibres of the strie longitudinales. These, therefore, line the arcuate fissures. The intracallosal group and those infracallosal fibres which lie in the paraterminal bodies represent the precommissural fibres of the fornix. The meeting of the fibres at the bottom of the “ gutter” immediately in front of (ultimately both in front of and above) the foramen of Monro forms the anterior pillars. The psalterial fibres of the fornix appear to develop later than the fore and aft system. There was certainly no evidence of these long after the longitudinal system was well established. It is likewise 222 Dr John Cameron
interesting to mention that they were absent from a brain without a corpus callosum (1) in which the remainder of the fornix was prominently displayed.
These observations on the development of the fornix certainly indicate that the strie longitudinales are integral parts of that system. Elliot Smith (12) several years ago suggested that they were an outlying group of fornix fibres, so that the present investigation confirms this impression. Zuckerkandl (19) has pointed out that the striz, together with a scanty amount of grey matter in relation thereto, represent an aborted convolytion, to which he gave the name of “gyrus supracallosus,” whilst Elliot Smith (10) has been enabled to trace clearly “the gradual transformation of the
cally’ he . Hie. etag sul (a.p) \ foal she. S
Fic. 21.—Relation of the fornix system to the callosal sulcus in a brain minus a corpus callosum.
supracommissural hippocampus of the marsupial into the thin supracallosal film of grey matter which is found in the cerebrum of the Primates and Cetacea.”
The above conclusions on the relation of the striz to the fornix receive remarkable confirmation from the study of the human brain minus a corpus callosum, which the writer (1) described in 1907. What appeared to have happened in this specimen was that the lamina terminalis had not folded upon itself, but persisted as a flat plate connecting together the two hemispheres at the bottom of the callosal sulcus. Interestingly enough, however, one could readily recognise in each lateral half of this structure three longitudinal bundles of fibres lying alongside one another. These were identified from their connections as one-half of the fornix, the strie longitudinales, and the cingulum, named in that order from the mesial plane to the bottom of the callosal sulcus (fig. 21). Now if one can imagine this flat lamina terminalis folded upon itself in a manner similar The Lamina Terminalis and its Relation to the Fornix System 223
to that which occurs during normal development, then these three longitudinal systems of fibres would regain their correct relative positions. Fig. 20 is a sketch of the plate-like lamina, with the three bundles of fibres on each side of the middle line. The two halves of the fornix were completely separated from one another mesially by an epithelial transformation of the lamina. The latter bulged, owing apparently to an abnormally high intraventricular pressure, which doubtless was the cause of the condition, seeing that it had prevented the normal folding of the lamina terminalis upon itself. The cingulum in this specimen was separated from the strise and fornix anteriorly by a decided interval, a relation which appeared to confirm the impression generally held that it is not a part of the fornix system. Posteriorly, however, it blended with the striz for a short distance (tig. 20).
This brief paper is a preliminary communication, and therefore contains only a limited number of references to literature.
(1) Cameron, J., ‘‘A Brain with Complete Absence of the Corpus Callosum,” Jour. of Anat., vol. xli., 1907. (2) Camzron, J., “The Development of the Optic Nerve in Amphibians,” Studies from the Anat. Department of the Univ. of Manchester, vol. iii:, 1906. 190 (3) Cameron, J., ‘‘The Histogenesis of Nerve Fibres,” Jour. of Anat., vol. xli., 6.
(4) Cameron, J.. and Wm. Miuuiean, “The Development of the Auditory Nerve in Vertebrates,” Jour. of Anat., vol. xliv., 1910.
(5) His, Wm., “Die Formentwickelung des menschlichen Vorderhirns vom Ende des ersten bis zum Beginne des dritten Monates,” Abhandl. der Konigl. stichs. Akad. der Wissensch., Bd. xv., 1889.
(6) His, Wm., ‘Zur allgemeinen Morphologie des Gehirns,” Archiv fiir Anat. und Entwick., 1892.
(7) Hocusrerrer, F., ‘“‘ Beitrige zur Entwickelungsgeschichte des Gehirns,” Bibliotheca medica, Abth. 2, 1898.
(8) Kurr, J. Granam, “On some Points in the early Development of Nerve Trunks and Myotomes in Lepidusiren paradoxa,” Trans. Roy. Soc. Edin., vol. xli., part j., 1904.
(9) Smite, G. Exuiot, “The Brain of a Fetal Ornithorhynchus,” Quart. Jour. Micr. Sci., vol. xxxix., 1896.
(10) Smira, G. Exxiot, “The Morphology of the Indusium and the Strize Lancisii,” Anat. Anz., Bd. xiii., 1897.
(11) Smita, G. Etutot, ‘The Relation of the Fornix to the Margin of the Cerebral Cortex,” Jour. of Anat., vol. xxxii., 1898.
(12) Smira, G. Enurot, “The Fornix Superior,” Jour. of Anat., vol. xxxi., 1897. 224 'The Lamina Terminalis and its Relation to the Fornix System
(13) Sutra, G. Exxior, ‘Further Observations upon the Fornix,” Jour. of Anat., vol. xxxii., 1898.
(14) Sirs, G. Extiot, “The Origin of the Corpus Callosum, a Comparative Study of the Hippocampal Region of the Cerebrum of Marsupialia and certain Cheiroptera,” Trans. Linn. Soc. London, vol. vii., part ili., 1897.
(15) Suir, G. Exot, “ Further Observations on the Anatomy of the Brain in the Monotremata,” Jour. of Anat., vol. xxxii., 1899.
(16) Smirx, G. Extiot, ‘On the Morphology of the Cerebral Commissures in the Vertebrata, with Special Reference to an Aberrant Commissure in the Brain of certain Reptiles,” Trans. Linn. Soc. London, vol. viii., part xii.
(17) Smira, G. Extiot, “On a Peculiarity of the Cerebral Commissures in certain Marsupialia, not hitherto recognised as a Distinctive Feature of the Diprotodontia,” Proc. Roy. Soc., London, vol. Ixx., 1902.
(18) Smirn, G. Exior, “‘The Cerebral Cortex in Lepidosiren, with comparative Notes on the Interpretation of certain Features of the Fore-brain in other Vertebrates,” Anat. Anz., Bd. xxxiii., 1908.
(19) ZuckerKANDL, E., Ueber das Riechcentrum, Stuttgart, 1887.
In concluding this paper the writer desires to express his deep indebtedness to Professor G. Elliot Smith for much valuable help and criticism.