Paper - The mammalian cerebellum - its lobes and fissures 2 (1904)
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The Mammalian Cerebellum: Its Lobes and Fissures
By O. Charnock Bradley, M.B., F.RS.E., Royal Veterinary College, Edinburgh; Goodsir Fellow, University of Edinburgh. (PLaTES XLVI.-L.).
Part II. The Cerebellum in Primates
The brains of Hapale jacchus, Nyctipithecus trivirgatus, Cebus capucinus, Lagothrix humboldti, Ateles ater, Macacus rhesus (two specimens), Cynopithecus niger, and Cercocebus fuliginosus have been examined. The description of the cerebella of the first two had better be given separately, as they differ in many respects from those of the remaining monkeys. The other specimens will be described together, since they do not differ sufficiently widely to justify individual consideration.
Hapale jacchus (Pl. XXIV. figs. 48, 49, 50 and 51).—At the very first glance, one is struck with the remarkable simplicity of this cerebellum. It is certainly not a simplicity of so severe a type as that met with in some other small mammals, but it is sufficiently pronounced to call for remark. Paramedian sulci are exceedingly faint in lobes A, B and C. In the remaining lobes they are easily recognisable, but not deep. The number of folia in the vermis is small enough to allow one to speak of the different lobes as being composed of a certain number.
Fissure I. is very easily recognised in mesial sections, Its depth is “about as great as that of any other fissure with the exception of II. Lobe A consists of five folia, three of which go to lobule A,, the remaining two to A,. Fissure ¢ is undoubted. It is difficult to say if lobe A assists in the formation of the hemisphere, owing to the doubtful character of the paramedian sulcus at this point.
Fissure II. is placed farther back than one would expect, in view of the comparative simplicity of the cerebellum as a whole. Consequently, lobe B is relatively large in the vermis, but becomes more restricted in the hemisphere, owing to the course of fissure IL. in a downward and forward direction. Only one, or possibly two, of the intralobular fissures is what Bolk would describe as ‘complete,’ 2.¢, runs completely across the cerebellum.
Lobe C calls for a detailed description. It consists of four folia in the vermis, but in the hemisphere—following the customary behaviour of this lobe—its folia are more numerous. Three of the folia pass outwards and forwards to the border of the cerebellum without undergoing much alteration. The fourth folium is connected with several short folia, which are arranged in a radiating manner, their centre of radiation being towards the middle line. This increase in the number of the folia, with a corresponding increase in the size of lobe C, is what we have been led to expect ; but the point to which: attention is asked is the comparative simplicity of their arrangement in a cerebellum in which, as will be shown immediately, certain parts are much better developed than is customary in a cerebellum with a simple lobe C. Neither fissure @ nor 0 can be determined, though serial sections through the half of the cerebellum have been made and examined microscopically, in order to settle this and some other particulars to be presently detailed.
Lobe D is divided into two lobules by a very distinct fissure d. Lobule D, consists of two folia in both vermis and hemisphere, there being no difficulty in determining the connection of the two districts, owing to the shallowness of the paramedian sulcus. Lobule D, also carries two folia, but does not reach the hemisphere.
Lobe E is likewise composed of two folia, or one compound folium, and microscopic sections show that it entirely disappears at the limits of the vermis, and that a white area takes its place. Considerable difficulty has been experienced in arriving at any conclusion as to the line of separation of flocculus and paraflocculus. There is a well-developed and clearly-defined lobulus petrosus which, attached to the rest of the cerebellum by a narrow neck, is closely surrounded by a capsule of bone. In addition, there are five folia lying anterior to the point of attachment of the lobulus petrosus ; and it becomes a question as to how many—if any—of these belong to the paraflocculus. Unfortunately Bolk (13) affords no assistance in the reading of the riddle, since he does not mention these folia in the text of his paper, nor do they appear in his text figures. In fig. 2, taf. ii, he apparently shows two of them. But here they are simply labelled “Form. verm.” (formatio vermicularis). An examination of serial microscopic sections leads one to conclude that, as in the rabbit, these folia anterior to the lobulus petrosus all belong to the flocculus. In looking over sections beginning in the middle line, it is first noticed that a trace of grey matter appears in the small area of white matter which has been left on the disappearance of lobule D, and lobe E. This gradually increases in amount until a veritable folium is formed, which is ultimately divided into two, an upper and a lower, to the former of which the lobulus petrosus is attached. There can be little doubt that this is the paraflocculus ; and, incidentally, it may be remarked that its mesial commencement lies far under lobule D,, 7.e. it commences within measurable distance of the vermis. No microscopic connection can be traced between the paraflocculus as just described and the five folia in the anterior part of the cerebellum ; they are therefore held to constitute the flocculus, which, as in the rabbit, is far removed from the vermis.
Nyctipithecus trivirgatus (Pl. XXIV. figs. 52, 53 and 54).—The cerebellum of this Douroucouli is not unlike that of Hapale, except that it is a little more complex. In this specimen, as in the preceding, microscopic sagittal sections have been made of one-half of the organ. Instead of giving a detailed description, it will suffice to compare the cerebellum of Nyctipithecus with that of Hapale.
The differences in the anterior region are too slight to require mention, and lobe C need not be dilated upon. It is with lobes D and E that it was found especial attention was necessary. In this part of the cerebellum paramedian sulci are very pronounced, and their presence removes the obvious connection of the parts of lobule D, which is so clear in Hapale. When a series of sections are examined, it is found that lobule D, (which is larger than in Hapale) ends somewhat abruptly about the paramedian sulcus. At the same time lobule D, adds to the number of its folia, so that there are three of these visible in the hemisphere when the intact cerebellum is examined. Sections show avery definite continuity of them with the paraflocculus, which, though not very large, is of good size, and carries a bulky lobulus petrosus.
The mesial part of lobe E retains its grey matter slightly more laterally than lobule D, extends. Then all that remains is the edge of the medullary velum, above which lies fissure IV., which can be followed without difficulty until it separates the paraflocculus and flocculus.
Cebus, Lagothrix, Ateles, Macacus, Cynopithecus, and Cercocebus (Pl. XXV. figs. 55 to 62; Pl. XXVI. figs. 63 and 64).—These cerebella will be described together, as their resemblance is very great. In the anterior part of the organ there is little to note. Until lobe C is reached, the lobes, lobules and fissures are not unlike those met with in animals with a cerebellum of about the same degree of complexity. And it may be further stated that in all six monkeys the -corresponding parts are of about the same relative size and disposition. It is in the district which lies behind fissure IT. that the main features of interest are encountered.
Lobe C is marked by a pronounced antero-posterior increase in the hemisphere. With the exception of Cebus, there is little difficulty experienced in finding fissure 6, which cuts the vermis fairly deeply, and curves downwards and forwards to the margin of the hemisphere. Lobule C,, thus bounded posteriorly, is of about equal antero-posterior diameter throughout, and its intralobular fissures run approximately parallel. It is a perfectly good exhibition of Bolk’s lobulus simples. In Cebus, however, it is difficult to decide upon a sulcus posterior such as is figured and described by Bolk (13), fig. 13. In the other monkeys the deepest fissure in the vermis in lobe C can be traced as a continuous and deep sulcus to the margin of the hemisphere. But in the specimen of Cebus, examined for the purpose of this paper, the deepest fissure in the vermis is neither deep nor continuous in the hemisphere. Judging from the condition as described by Bolk, I can only conclude that my specimen was one illustrating the subsidiary morphological position of the fissure.
Lobule C, is not quite the same in all the specimens. In Cebus, as noted above, fissure 6 cannot be determined ; therefore the exact limits of lobule C, cannot be defined. In Macacus, C, has apparently no existence in the vermis, because fissure a runs into fissure 6 in the paramedian sulcus. That part of it which does exist, however, has the same form as the hemisphere portion of the lobule in the other monkeys, 7.e. it consists of a number of folia arranged in the form of a half-opened fan, the handle of which is directed towards the vermis. The fissures between the folia all disappear before reaching either fissure a or fissure b, with the exception of one which arrives at the apex of the triangle, and therefore opens into the conjoint fissure a+b (Pl. XXV. fig. 61). In Cercocebus and Cynopithecus fissure a is deep in the hemisphere, but in the vermis is traceable into a shallow interfoliar cleft in the depths of fissure ITI. Lobule C, is therefore present and of some size in the vermis. In the hemisphere it need only be noted that it is relatively larger than in Macacus. It has the same radial arrangement as in the latter animal, and there is the same fissure running inwards towards the point of convergence of fissures a and b. It should be noted that there is a very narrow link connecting the three parts of lobule C, on each side, this being invisible on the surface. In Lagothrix and Ateles fissure a cannot be followed into the vermis, therefore the limit between lobules C, and C, is problematic.
Lobule C, in Cebus and Macacus consists of a narrow part in the vermis, continued into a much larger portion in each hemisphere, there being a slight stricture in the paramedian sulcus. In Cercocebus and Cynopithecus, owing to the peculiarity of fissure a, lobule C, can hardly be said to have any existence in the vermis. The most that can be said of it is that it is represented by three or four folia on the anterior wall of fissure III. In the hemisphere, however, it is large, and resembles the homologous part in the other cerebella.
Lobules D, and D, are very similar in all the specimens. D, is largely developed in the hemisphere, and there is little difficulty in finding its connections with the vermis. This is very easily done in Cebus, owing to the comparative lack of depth of the paramedian sulci (Pl. XXV. fig. 57). Lobule D, belongs entirely to the vermis. In order to ascertain if there was any continuation whatever beyond the vermis, microscopic sections of this region were made in Cercocebus. It was found that lobule D, ends somewhat abruptly, and gives place to a considerable stretch of white matter which underlies lobule D, in the mesial part of the hemisphere.
In all but Cebus, lobe E also ends at the level of the paramedian sulcus. In Cebus, however, the lowest folium is continued outwards, undiminished in size, underneath lobule D, (Pl. XXV. fig. 58), It proceeds laterally for some distance and then fades away, giving place, as it appears, to the posterior medullary velum to which it has been previously adherent.
The same general arrangement of the flocculus and paraflocculus obtains in all the monkeys examined. The paraflocculus consists of a single row of transverse folia, which turns downwards a little in front and appears to be continuous with the flocculus (Pl. XXV. figs. 55 and 60). This appearance would lead to the description of the paraflocculus as composed of dorsal and ventral parts, and to the statement that the flocculus is wanting, were it not for two circumstances which cannot be put on one side unconsidered. The one is that there is a deep sulcus separating the anterior end of the flocculus from the paraflocculus. Again, the flocculus is closely related to, and partly adherent to, the lateral prolongation of the posterior medullary velum. This is best seen in Cebus, where, owing to the lateral extension of lobe E (as described above), there is very little interval between flocculus and lobe E (Pl. XXV. fig. 58).
The paraflocculus carries a lobulus petrosus, springing from its lateral face close to the anterior end. The extent to which the paraflocculus proceeds backwards and inwards varies in some degree.
In Cebus, lobule D, passes on to the inferior surface of the hemisphere, and consequently sets a limit to the parafloeculus. In the other monkeys, however, the paraflocculus is continued unarrested in a mesial direction until it almost reaches the vermis. But it is not fused with any part of the vermis, as microscopic sections show ; and for this reason the term paraflocculus is applied to the whole of it, however nearly it may approach the middle line.
In no specimen could one feel convinced that there was a dorsal and a ventral limb to the paraflocculus, such as Elliot Smith indicates (10). I am inclined to think that the paraflocculus of the monkey corresponds to the ventral limb of that structure in the majority of mammals, and that the dorsal paraflocculus has been replaced, so to speak, by the enlarged hemisphere segment of lobule D,.
The Human Cerebellum
Thanks to the kindness of Professor D. J. Cunningham, I have been enabled to examine a number of human foetal cerebella. Although several of them are of approximately the same age, and none is illustrative of the earlier stages of development of the fissures and lubes, there are at least four of them which throw light upon some of the problems of the growth of the fissures in man. The remainder have been of the greatest use in enabling me to check my results, and in showing in what manner some of the fissures are liable to variation. Seeing that the several cerebella had been separated (along with the pons and medulla) from the rest of the brain, no definite idea could be formed as to the age of the embryos from which any one had been taken, This is: perhaps not of the greatest importance, since the literature contains figures illustrating several different stages in the growth of the human cerebellum, with the age or size of the embryo appended. Anyone who is curious on the matter may compare the figures given herewith with those of previous writers (Stroud, Kuithan, Elliot Smith), The cerebella mentioned here will be known by numbers.
In Cerebellum No. I. (Pl. XXVI. figs. 65, 66, 67, 68 and 69), the anterior part of the organ is already provided with a fairly numerous set of folia. In the posterior part the fissures are less numerous, and it is on this district that especial attention will be bestowed, for the reason that here are located the lobes and lobules concerning which there is most difficulty in arriving at conclusions regarding homologies. In all parts of the organ a distinction can readily be made into a vermis and two hemispheres, this being the more easily done in the posterior district. When the cerebellum is viewed from the front (fig. 65), fissures c, I, II. and & can be at once recognised, their disposition being very similar to that in the adult brain. Special attention is asked to the appearance presented by a mesial sagittal section (fig. 69). A noteworthy feature here is the large size of what is no doubt to become the ‘lingula.’ Further, the depth of fissure I. is to be noticed, since this, as previously tentatively stated, is not recognised by the human anatomist as a fissure of any importance in the division of the vermis into its several lobes. Between fissures c and I. there is only one folium visible when the surface is examined, this folium being even narrower in the hemisphere than in the vermis. That part of the organ which lies posterior to fissure II. is of great interest, chiefly because, as already said, its development is not so far advanced. Appearances seem to point to the development of fissure b as having been from two lateral halves, which have gradually grown towards the middle line. These two halves, in this particular specimen, seem to have missed arriving at exactly the same point in the middle line, with the result that they overlap to some extent (fig. 66). In a mesial section the fissure is double, appearing as two shallow depressions (fig. 69), Fissure a is still in the form of two halves, which are approaching each other in the vermis. It will be observed that fissures a and 6 develop in man in the same manner as has been found in the pig, rabbit and sheep. Fissure III. has obviously commenced its development in the middle line (cf. Kuithan). It is deep in the vermis, but gradually becomes shallower as it curves outwards and downwards into the hemisphere, to disappear finally before reaching the margin of the cerebellum (fig. 67). Fissure d is as deep as III. in the vermis, and in each hemisphere is continuous with a curved groove which reaches the border of the organ. It is well to remark that d is very shallow in the paramedian sulcus.
Lobe E is small, and confined to the vermis. A simple unfoliated flocculus is visible when the cerebellum is looked at from behind or from the side (figs. 67 and 68), There are no paraflocculi in this specimen.
A few intralobular fissures have appeared in the vermis in lobules D, and D,; and that part of the hemisphere which lies between fissures a and d is marked by a groove, which begins at the border of the cerebellum and, passing for some distance towards the middle -line, becomes gradually less deep, until it finally ends before reaching the vermis (fig. 67). There seems little reason to doubt that this groove ultimately becomes continuous with III., and so separates lobe C from lobe D (ef. Stroud’s figure 62 (1), and Elliot Smith’s emendation of it in his figure 9 (12)). If this supposition is correet— and there seems little reason to question it—then the similarity of development of fissure JII. in its entirety in man, and in the rabbit, pig, sheep and calf, is very striking.
Cerebellum No. II. (P|. X XVI. fig.70), in addition to showing further growth of the fissures and lobes, is interesting, since it illustrates an asymmetry in lobe C. It will be observed that fissure } of the left side is continuous with fissure a of the right; and a of the left and b of the right half of the cerebellum cross the middle line to terminate in the opposite hemisphere. If any instance were needed in the support of the contention that these fissures are of secondary importance merely, their tendency to irregularity of disposition might be cited. In this cerebellum the posterior portion has developed very considerably as compared with the same region in No I. Fissure III. is now complete, forming a series of graceful curves, of which that in the vermis is the most acute, and has its convexity looking upwards. Fissure d and lobule D, have not altered materially from the condition in the preceding specimen. The vermis portion of lobule D, has become foliated, but the hemisphere segments remain smooth. The flocculus is now foliated. There is a paraflocculus on one side only, and it is much smaller than the flocculus. Its connections cannot be followed with any degree of satisfaction, it being quite clear that only in much younger material can the origin of the paraflocculus and flocculus be determined beyond question.
Looking at this cerebellum as a whole, it is observed that there has been a more pronounced growth in the hemispheres than in the vermis. This growth has taken place more particularly in lobules C, and D,, lobule D,, as previously stated, being still unfoliated in the hemisphere. As a consequence of this marked local development, the hemispheres project farther posteriorly than the vermis, and overhang the medulla to a greater degree than they did in cerebellum No. I. The paramedian sulcus is deepest and best marked in lobule D,, and it will be noticed that the connection between the three parts of lobule D, has become very narrow.
In Cerebellum No, IT. (Pl. XXVII. figs. 71, 72 and 73), there is a marked resemblance to the adult organ. There is now a fairly pronounced vertical flattening. On inspecting the cerebellum from above, fissures I., II. and } are seen to run uninterruptedly across the surface, and lobes A and B and lobule C, now carry folia. Fissure a is still in the form of two lateral halves which approach each other, ze, the vermis, but have not yet fused (figs. 71 and 72). Because of this lack of continuity there is still a portion of the vermis common to lobules C, and C,. This common connection is of only small antero-posterior diameter, as indeed was the case in the younger specimens. Lobule C, is relatively small, and its intralobular fissures are few. Lobule C, in the hemisphere has again grown at a rapid rate as compared with the surrounding lobules. There is little to remark in fissures III. and d. They present much the same features as have been mentioned in connection with Cerebellum No. IL, their depth of course being greater. Lobule D, has not grown as rapidly as appeared to have been the case in the interval between No. I. and No. II. The connecting link between that part of it which lies in the vermis and its more lateral segments is narrow (as in No. II.) and consists of a single folium. Lobule D, has not grown in a manner which calls for remark, and those portions of it which are placed lateral to the paramedian sulci are still smooth. A small and simple paraflocculus is present on both sides (fig. 73). The flocculus does not appear to have made any noteworthy progress.
The external features of Cerebellum No. IV. (Pl. XX VIL fig. 74) are very similar to those of No. III. There are rather more intralobular fissures, but the lobes, in the main, present no additional points of interest. It should be noticed that the two halves of fissure a have at length joined in the middle line. This is obvious in a mesial section (fig. 74). Attention is again directed to fissure I. as seen in section. Its depth in the middle line is great, being not much less than that of c, The importance of this fissure is once again insisted upon.
The only other foetal cerebellum (No. V.) to which any reference is necessary is useful as affording evidence of the parts of the adult organ formed from the various lobes of the younger specimens, This cerebellum has arrived at such a stage that it, at one and the same time, resembles No. IV. and also the fully-developed structure. Its approaching identity with the adult organ removes any necessity for a detailed description. It will suffice to indicate what changes occur in the transition from the foetal to the adult condition. It may be said, in general terms, that the most striking alteration in the form of the whole organ is produced by a growth in the hemispheres out of proportion to that of the vermis. This we have seen to begin in the comparatively early stages illustrated by the material the description of which is given above ; it becomes still more evident in the later stages. As a consequence of this disproportionate growth, the vermis becomes a comparatively insignificant part of the human cerebellum, and the mesial connections of the corresponding parts in the two hemispheres is relatively reduced in a sagittal direction. This feature of development is not equally marked in all regions. In lobes A and B it is very trifling. In lobe C it is decidedly obvious, and particularly so in lobule C,.
The growth of the hemispheres within this lobule is so great, and the fissures which cut its surface are so deep, that human anatomists have found it expedient to divide it into three parts. This enormous growth of lobe C is very characteristic of the human brain. Indeed, Bolk has said (14) that “the distinguishing feature of the human cerebellum depends upon what may almost be called the monstrous development of the crus primum of the lobulus ansiformis” (i.e. ‘lobuli semilunares superior and inferior and gracilis), with the corresponding reduction of other parts to which attention will be directed later. The lateral portions of lobule D, also share in this developmental activity, but to a smaller extent. Lobule D, does not become nearly so conspicuous a focus of growth. Because of the backward projection of the hemispheres in the region of lobe C, the vermis appears to sink into the depths of a narrow valley, bounded by the steep heights of the hemispheres. For the same reason, the lateral portions of lobe D are constrained to form part of the sides of the valley. That part of lobule D, which contributes to the formation of the hemisphere is, indeed, so confined by the masses lying lateral to it that its growth has to take place in a sagittal direction. In the adult brain it is found to consist of two rows of folia—or rather one row doubled upon itself—radiating out from what Ziehen (15) describes as the fossa azialis.
Throughout the present paper, and also in the one which has preceded it, the various lobes and fissures have been known by means of letters and numbers. This plan has been followed with the intention of avoiding the use of terms—such as those employed in Human Anatomy, for instance—which would in any degree hamper us in our endeavour to approach the subject without preconceived ideas of any kind. It need hardly be said that these letters and numbers here employed are merely a temporary convenience, but I do not propose to substitute any other form of nomenclature for them in this communication except in the case of the human brain, and in this case merely in order that the conclusions as stated in the preceding paragraphs may be the more readily appreciated by the human anatomist.
Fissure c, then, is the sulcus postcentralis of man, and therefore forms the posterior (upper) limit of the lobus centralis (lobule Aj). Fissure I. is not recognised as being of any great importance, and is therefore unnamed in books on Human Anatomy. That it should not be relegated to a subordinate place has, it is hoped, been made clear by embryological evidence, and also by the testimony of comparative anatomy. lLobule A, is considered in the text-books as a part of the lobus culminis, though there are not lacking those who consider this lobe to be composed of two parts. Lobe B constitutes the upper part of the lobus culminis. ‘There seems to be want of agreement between Professor Elliot Smith and the present writer in connection with the subdivision of this part of the cerebellum. What has been referred to as fissure c in the foregoing descriptions is evidently equivalent to the jissura preculminata of Elliot Smith, who, nevertheless, states that the ‘culmen’ of the human brain is divided into two lobules by a fissure (a in his figures) which may be as deep as, or even deeper than, the fissura preculminata (11).
Fissure II. is the sulcus preclivalis, fissure b is the sulcus postclivalis, fissure a the sulcus horizontalis magnus, and fissure IIT. the sulcus postpyramidalis. Lobe C therefore comprises a very large proportion of the human cerebellum. Its lobule C, is the lobus elivi, consisting of a clivus monticult and its lobt lunati posteriores.
Lobule C, is the lobus cacuminis, with its diminutive foliwm cacuminis in the vermis, and its much expanded lobus postero-superior in the hemisphere. To this, and to lobule C,, as has been said, the human cerebellum owes not a little of its distinguishing characteristics, Lobule C, is the lobus tuberis with a vermis segment, the tuber valvulez, and the enormously developed appendages in the hemisphere which anatomists have found necessary to subdivide into lobus semilunaris infertor, lobulus gracilis anterior, and lobulus gracilis posterior. The sulct postgracilis and intragracilis, being confined to man and the anthropoid apes, have found no place in the foregoing descriptions. They are of no interest as forming primary subdivisions of the cerebellum; for, not only are they limited to one zoologic locality, so to speak, but in those animals in which they do occur, they are tardy in their appearance in the embryo.
It is scarcely necessary to apologise for the somewhat cavalier treatment of the sulcus horizontalis magnus, as various writers, during the past eight years, have borne witness to its utterly subsidiary position among the cerebellar fissures.
In lobe D of the human cerebellum are found points of primary importance to the morphologist. Lobe D, consists of the pyramis and its lobt biventralis, constituting the lobus pyramidis. Lobule D, is the lobus uvulx, with its wvula in the vermis and the tonsils in "the hemisphere. That part of lobe D which is so well developed in the majority of mammals, and which has come to be known as the paratflocculus, is either unrepresented in man, or, when present, is of small size. But, on the other hand, that connection between the paraflocculus and lobule D, in the vermis (pyramis), which is always comparatively small and often apparently absent in the lower mammals, is largely developed in man, forming that very considerable lobule, the lobulus biventer. And, again,-that continuation of lobule D, into the paraflocculus, which apparently has only an existence in the embryo in the lower mammals, is persistent as the tonsil in man. Lobe E is the lobus noduli (nodulus and flocculus), which, though subject to some variation in size in different animals, does not show such extreme degrees of fluctuation as are found in many of the other lobes.
No mention has been made of the lingula of the human cerebellum, and this because it is not considered to be a separate and distinct lobe of the cerebellum. It must be admitted that a very prevalent idea, as expressed in many text-books on Human Anatomy, is that the ‘lingula’ stands on the same level of importance as the ‘nodulus,’ and that these two structures should be further held of equal status, since they are similarly related to the anterior and posterior medullary vela respectively. But such assertions are not supported by comparative anatomy. The ‘nodulus’ is always present in mammals (Meta- and Eu-therian, at any rate), but the ‘lingula’ is not so constant. In the smaller mammals with a simple cerebellum, there is no trace of grey matter on the dorsal surface of the anterior medullary velum. In the larger mammals this absence also mainly obtains; and even when there is an invasion of the velum by grey matter, it is usually very small in amount. For example, in the monkeys examined, with the exception of Hapale, the velum appeared to spring from the edge of a folium of the cerebellum, instead of from the central mass of white matter as is most frequently found to be its mode of attachment. Certainly ‘lingule’ do occur of a moderate size in animals other than man but such instances are not numerous, A ‘lingula’ may be found in one specimen and not in another of the same species of animal, And even where a ‘lingula’ is accepted as being always present, as in man, for example, it is liable to great variation in size. There is certainly a degree of variability in size of the ‘nodule,’ but this is not nearly so marked as it is in connection with the ‘lingula.’ Further, the development of the anterior and posterior vela and their adjacent parts is not quite the same. The anterior velum is produced by the upward and forward growth of the cerebellar lamina, which causes a thinning, so to speak, of the roof of the neural tube. The posterior velum is originally a thin non-nervous membrane, attached to the sharp margin of the cerebellar lamina. It is readily conceivable that in the development of the anterior velum there may be an overflow into it from the cerebellar lamina of some of those cells which go to produce the grey cortex of the fully developed cerebellum. If this view be correct, then one may look upon a ‘lingula’ as an accidental circumstance. The ‘nodule,’ on the other hand, grows directly from the posterior edge of the cerebellar lamina, and makes its appearance at a very early date. Elliot Smith apparently holds a different opinion as regards the morphologic status of the ‘lingula,’ for he not only considers it in his paper on the human cerebellum, but also includes it in his latest diagram “representing the fundamental and more constant secondary fissures of the mammalian cerebellum ” (11).
Having now signified my conception of the homologies of the human lobes and fissures in terms of the human atatomist, I shall again revert to the provisional use of numbers and letters.
The Cerebellum of Primates in General
Whatever opinion one may hold regarding the inclusion or exclusion of the Lemuroidea in or from the order of Primates, there can be no doubt that, so far as the cerebellum is concerned, the lemurs do not range alongside the Anthropoidea. Elliot Smith has shown that among the lemurs many types of cerebellum are to be found (12). In many respects the cerebellum of the Anthropidea stands apart from the rest of the Mammalia; and, from the Hapalide upwards, forms a graded series of forms, culminating in man. It may be permitted to summarise some of these gradations.
In the Hapalide the lobes are simple and of few folia; and the general direction of the fissures is transverse, t.c. there is none of that marked local obliquity so commonly met with in most cerebella. Lobe C can hardly be said to be subdivided at all. This circumstance, were it not relieved by an attempt at the obliquity just mentioned, would bring the lobe down to the level of the corresponding part in the rodents, insectivores, etc. Another feature of note is the small size of the paraflocculus (that is, if the statements set forth upon this point in a previous part of this paper are substantiated by further research).
In all the monkeys examined, as well as in those described by Bolk (13), there is no possibility of overlooking fissure I. In most monkeys lobule A, is, relatively speaking, small, whereas lobe B is well developed. In lobe C we find a gradual increase in size as we ascend from the Hapalide, this increase being mainly, but not entirely, in a sagittal direction. Associated with this expansion in the hemisphere is a relative reduction of the vermis posterior to fissure 0, and an arrangement in the hemisphere of the folia belonging to lobules C, and C, in a radiating manner.
The characteristic feature of lobule D, is the constancy and size of those parts of it which belong to the hemispheres. So far as the marmosets and monkeys are concerned, there is nothing very striking in the form, size and disposition of lobule D,. In all of them of which we have any account this lobule is similar to that of mammals belonging to other orders. There is therefore a remarkable difference between this lobule in the monkeys and the apes. From Stroud’s observations on the Ape Cerebellum (16), it appears that in the chimpanzee, orang and gorilla, at any rate, there is a lateral continuation of lobule D, as in man, but in these animals it “is a relatively small tetragonal mass.” It would be very interesting to find some monkey in which this condition, but on a smaller scale, is present, for then the gradations up to man would be complete in this region of the cerebellum.
The fairly uniform size of the flocculus and lobe E in general in different monkeys is noteworthy. In no order of Mammalia is there any very great variation in the dimensions of these parts ; but in monkeys and apes (Stroud) the variation is even less than might reasonably be expected in a group of animals differing widely in other particulars. In monkeys, too, the paraflocculus is fairly uniform, and is peculiar in all of them in consisting of only one well-developed row of folia. Ina previous paragraph it has been stated that there seems reason to suppose that this single limb corresponds to the ventral paraflocculus of other mammals, the dorsal limb being probably taken up in the development of the large part of lobule D, which lies within the hemisphere. It would be interesting to see. what embryology has to say on this point.
In the apes, Stroud found that the paraflocculus was variable. In a gorilla he describes it as “very large and almost entirely exposed.” In two orangs “it is small and concealed on the left side, only the tip showing on the right side.” And in a chimpanzee it “is small and concealed on the left side; the tip is visible on the right side.” The paraflocculus of the apes therefore forms a link between the well-developed lobule of the monkeys and the small, insignificant and inconstant structure in man, which is generally referred to as the “accessory flocculus.”
Arbor Vita Cerebelli
It has become a practice — not invariable, but certainly common—for those who write on the cerebellum to devote some attention to the figure presented when sagittal sections (particularly in the middle line of the vermis) are made. It is obvious that the form assumed by the white matter will vary greatly, depending upon the depth of the primary fissures, and the number, depth and disposition of the subsidiary fissures. For this reason the appearance of the arbor vitse cerebelli differs in different animals, presenting the least intricacy in those brains in which the cerebellar fissures are few. and the lobes and lobules are simple. For example, in the smaller bats the rays proceeding from the central mass of white substance are only five in number, and each ray is undivided. In the larger cerebella the rays are much more numerous and sometimes very copiously branched. Moreover, not only does the form of the arbor vite differ in different species of animal, but there is also variation to be noticed in different animals of the same species.
For these reasons it is difficult to arrive at any precise conclusion as to the absolutely typical form of arbor for any one class, or even species of animal, unless one is fortunate enough to be able to examine numerous specimens of that order or species. Bearing this in mind, it is with a certain amount of reserve that one speaks of the form and definite arrangement of the branches of the arbor vite cerebelli in any given animal. At the same time general statements may be made as to their disposition in the average mammalian cerebellum.
In all cerebella the central white mass is divided more or less into two parts by the fastigium cutting into it from below and fissure II. indenting it from above (Pl. XXVIII. fig. 76). The degree of division is far from being constant, nor is the result of the division always the same. In probably the majority of mammals the anterior area of white matter is the larger and more compact. The posterior area has a greater tendency to be drawn out in an antero-posterior direction. Springing from the anterior and posterior portions of the white mass are two strong main branches, which pass upwards into lobes B and C respectively. To these two branches Ziehen (15) has applied the names of truncus verticalis (to the anterior) and truncus horizontalis (to the posterior). It is unfortunate that these names do not indicate the direction of the branches in all, or even in most, mammals. Most frequently they are both more or less vertical.
In all but the simplest forms there are five prominent branches in addition to the two just mentioned, so that the average mammalian cerebellum has seven rays of white matter spreading out from the central mass. These seven rays pass into the following lobes and lobules. The lowest of the anterior branches passes into lobule A,, and is very frequently not a single ray, but rather two or three. The next ray passes into lobule A,, and arises either from the central mass directly or from the third branch. Not infrequently it is difficult to decide if these two branches come from a common point, or if the third branch gives origin to the second. The third branch, which is one of the two main and constant rays, is always thick; it forms the core of lobe B, and very frequently divides into two (sometimes more) parts. The fourth branch is usually the strongest of the seven. It curves upwards into lobe OC, and in all cases, except where this lobe is incompletely or not at all divided, splits into three sub-rays—one for each lobule. The fifth branch arises in one of four ways. It may leave the central mass independently ; it may arise in common with the fourth branch; it may spring from this branch; or it may have a common origin with the sixth branch. Whatever its mode of origin, its destination is lobule D,. The sixth branch mostly arises separately and independently ; but, as just said, it may share a common origin with the fifth. It runs into lobule D,. The last branch is always the smallest ; indeed in the simplest forms it is not more than a small projection from the white centre. It forms the axis of lobe E.
Seeing that there is so much diversity of form of the hemispheres in different animals, it would be exceedingly difficult to make any serviceable general remarks upon the arrangement of the white matter in these parts of the cerebellum.
It may be well to briefly summarise the result set forth in this paper and in the one which has preceded it, and to state the conclusions at which one has arrived. ‘he writer is fully alive to the possibility that these conclusions may require modification in the light of further research. But at the same time they are such as have emerged from a conscientious attempt to add facts as well as theories to the literature of that part of the brain concerning which, even at the present time, opinions are far from uniform.
From the examination of embryological as well as adult material, it is again made clear—if this were in any way necessary after the work done by Stroud, Kuithan, Elliot Smith, Flatau and Jacobsohn, and Ziehen—that in all mammalian cerebella, from the simplest upwards, there is one transverse fissure of pre-eminent importance. Its future status is foreshadowed at an early period of development, and is attained to and maintained in all adult forms. Were it not that it is to a degree inconvenient to do so, the cerebellum might be described as consisting of two lobes, separated by this fissure. Largely for the sake of convenience, but also and mainly from the consideration of the comparative anatomy of the mammalian cerebellum, it is better to recognise five lobes. Each of these has its own characteristics, and, in a series of cerebella, is found to undergo modifications along certain lines. The lobe in which variation is least marked is the most posterior, or E. The greatest amount of diversity of form occurs in lobes C and D. Lobes A and B change somewhat, but to a less extent. Lobe A, in all but the simplest cerebella, is divided into two parts by a transverse interlobular fissure. Lobule A,, the lower of the two, may remain simple, or, in the higher forms, be in its turn composed of more or less independent parts— generally two or three in number. Lobule A,, the upper part of lobe A, is generally the smaller, and frequently remains unsegmented. The deep fissure in lobe A has been known as ¢ throughout these communications; its importance has been recognised for long by human anatomists. Fissure I., which separates lobes A and B, has not been accorded that attention to which, it appears to me, it is entitled. Lobe B varies in different animals within certain limits, but these limits are fairly well defined. In all the small bats, for example, it is a single, undivided folium. It increases in size part passw with the increase in size of the other lobes, until it is found to be subdivided by deep sulci. Examples of the commencing division of this lobe are supplied by the squirrel and opossum. In these animals, not to multiply examples, the lobe ‘is found to be crossed transversely by a fissure which divides it into two practically equal portions. When there is dissimilarity of size the advantage nearly always rests with the more posterior division. In Phoca the division is very clear. In forms more complex than the opossum and squirrel the two portions of lobe B are themselves subdivided. This is also well exemplified in Phoca. Lobes A and B differ from the remaining lobes in the shallowness of their paramedian sulci, and in their small transverse expansion. These points have been emphasised by Bolk (14), and are excellently demonstrated in some of the Ungulates (Bos, for example). The embryology of lobes A and B is also different from that of C, D and E. In the earlier stages they lag behind in development; then comes a period of activity, in which they outdistance the posterior lobes, and so come to resemble the adult lobes while C, D and E are still comparatively rudimentary.
Lobe C occupies a developmental and anatomical position peculiarly its own. Even in the simpler forms its surpassing importance is obvious, for even here its great antero-posterior diameter in the hemispheres attracts attention. In higher forms it is clearly divided into three lobules by two fissures—a and b. These two fissures are not of equal consequence. From what has been seen in the embryos examined, a probably always (horse excepted ?) begins its existence in the hemisphere and grows into the vermis. Fissure 6 seems to begin either in the hemisphere (rabbit and pig) or in the vermis (sheep), and nearly always becomes complete, i.e. grows across the whole cerebellum. It is highly probable that fissure a frequently remains as two lateral segments which do not join in the vermis, or if they do, their union is apparently later than the conjunction of the two parts of 6. Even when fissure a is . complete, it may not cut the vermis very deeply. These variations, and the potentiality for irregularity, demonstrate the secondary importance of fissures a and 0.
Lobule C, apparently corresponds to Bolk’s lobulus simplex, and does all that Bolk claims for it. It is unmistakably of a like constitution with lobes A and B, but it differs from them in its greater lateral extent. Lobules C, and C, are peculiar in possessing a power of growing in a sagittal direction, especially in the hemispheres. Upon this peculiarity depends the most striking differences in a series of mammalian cerebella. For this reason Elliot Smith gave the name of area crescens to the lateral part of what he then called the lobus centralis (now named by him lobus medius). Sagittal expansion is also possible in the vermis, but it is generally smaller in amount here than in the hemisphere. Phoca may be used as an example of the possible exuberant expansion of the hemisphere, and Bos as an instance of a similar growth, but to a less extent, in the vermis.
The two lobules which compose lobe D have different characters. Lobule D, is much the simpler. It is usually limited to the vermis except in the highest forms (apes and man), and does not show any sagittal expansion such as will: produce distortion of the vermis. Lobule D, may be confined 116 MR 0. CHARNOCK BRADLEY.
to the vermis, but is frequently continued into the hemisphere (as shown in man, apes and monkeys in the greatest degree). When lobule D, has a segment in the hemisphere, this is generally connected with the dorsal paraflocculus. This connection is clearly indicated in the ungulates. In monkeys it seems within the bounds of possibility that the dorsal parafiocculus is replaced by the large portion of lobule D, which lies in the hemisphere.
Lobe E is subject to some modifications in size, but the variation is not notably great. Its continuation into the hemisphere is not of common occurrence, but in Cebus and Viverra cwetta it was found to be so continued; and in Didelphis and Herpestes the continuation of its grey cortex reaches as far out as the flocculus. Like the mesial part of lobe E, the flocculus does not vary to any great extent. It appears to reach its lowest point in some of the carnivora.
The difference in the size of the paraflocculus in different mammals is very striking. In its most highly developed condition it is composed of two rows of folia, to which may, or may not, be added a lobulus petrosus. This lobulus, when present, is generally attached to the posterior end of the ventral paraflocculus, but there are exceptions to this rule. The peculiarity of the paraflocculus in the monkeys has received some detailed attention. In the apes it shows various stages of diminution, and in man it has entirely disappeared in many, if not in most cases. —
Although throughout these papers the paraflocculus and flocculus have been described by themselves in the accounts of the various cerebella, this has been done merely for the sake of convenience. It is perhaps well to repeat the assertion that the paraflocculus is an outlying part of lobe D, and the flocculus bears the same relation to lobe E (fig. 75). Both embryology and comparative anatomy demonstrate this. The separation of the paraflocculus and the flocculus, either in part or entirely, from the more mesial portions of the lobes of which they are parts, depends solely on secondary development. They are apparently crowded to one side, and their connections with the vermis weakened or broken down by the growth of the superposed parts of the hemisphere.
Explanation of the Figures
Fig. 47. Phoca vitulina. Mesial sagittal section. x 1.
Fig. 48. Hapale jacchus. Superior view. x 2.
Fig. 49. ” Posterior view. x 2.
Fig. 50. ” Left lateral view. x 2.
Fig. 51. Mesial sagittal section. x 34.
Fig. 52. Nyctipithecus trivirgatus. Superior view. x 2.
Fig. 53. ” ” Posterior view. x 2.
Fig. 54. ” ” Mesial sagittal section.
Fig. 55. Cebus capucinus. Anterior view. x !.
Fig. 56. ” Superior view. x1.
Fig. 57. ” Posterior view. x 1.
Fig. 58. ” Inferior view. Left half. x1.
Fig. 59. ” Mesial sagittal section.
Fig. 60. Macacus rhesus. Anterior view. x1.
Fig. 61. ” Superior view. x1.
Fig. 62. ” Posterior view. x1.
Fig. 63. Mesial sagittal section.
Fig. 64. Cercocebus fuliginosus, Mesial sagittal section.
Fig. 65. Human embryo. No. I. Anterior view. x 2.
Fig. 66. ” No. I. Superior view. x 2.
Fig. 67. ” No. I. Posterior view. «x 2.
Fig. 68. ” No. I. Right lateral view. x 2.
Fig. 69. ” No. I. Mesial sagittal section.
Fig. 70. ” No. II. Posterior view. x 2.
Fig. 71. » No. III. , Superior view. x 2.
Fig. 72. ” No. III. Posterior view. x 2.
Fig. 73. ” No. III. Left lateral view. x 2.
Fig. 74. No. IV. Mesial sagittal section. x 2.
Fig. 75. Schema of the lobes and lobules of the average Mammalian cerebellum arranged in one plane.
Fig. 76. Schema of the mesial sagittal section of the average mam malian cerebellum.
Cite this page: Hill, M.A. (2020, July 4) Embryology Paper - The mammalian cerebellum - its lobes and fissures 2 (1904). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_mammalian_cerebellum_-_its_lobes_and_fissures_2_(1904)
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