the isocortex of tarsius

THE ISOCORTEX O F TARSIUS

GERHARDT VON BOXIN De2iartwient of Anatomy, University of Illinois s c l ~ o o l of Meclirine,

Chicago, Illinois

TWELVE FIGURES

The “ tarsier-hypothesis ” has stirred the scientific world for so long that it appears unnecessary to motivate by many words the reexamination of the brain of Tarsius which is here offered. Nor does it seem necessary to explain the “tarsier- hypothesis” in detail, since that has been done only a short while ago by Stranss (’49) in an easily accessible article.

TThatever the exact line of man’s ancestry, the study of a primitive primate which, so it has been said (Matthem, ’as), has not much changed during the last 12-20 million years, might throw light on the evolution of the human brain.

I n primates, the recognition of the environment shifted from olfaction to vision, and this shift might be reflected in the structure of the cortex. It is therefore not without interest to know the living habits of the animals whose brains one is about to study. Relevant data have been communicated by Clark (’24), Cook (’39), Catchpole and Fulton (’39). That Tarsius is a nocturnal animal, is well known. Tarsius can leap with astonishing accuracy from branch to branch. His leaps may be as long as 6 feet, far beyond the length of his own body, even including his tail. He will jump on his prey (grasshoppers, lizards, etc.) much as a cat does. But when a tidbit is offered on the point of a forceps, he may grasp clumsily the forceps instead of his food. Should the food drop to the ground, tarsius will close his eyes, nose around for the morsel and find it only when his nose is almost in contact

387

388 GERHARDT VON BONIN

with the piece for which he searches. Dr. Stephen Polyak who observed specimens in captivity, informs me, however, that in his opinion Tarsius has quite good eyesight, and can grasp objects well with his hands. His difficulties in grasping ohejects may simply be due to his being blinded by the light which humans need to observe his private life. None of those who liave observed the tarsier noticed his using the nose for the recognition of objects, as the galago appears to do. One might assume that the shift to vision as the chief sensory modality f o r the recognition of the outside world has bccn acconiplished by the tarsier.

Members of the infraorder " Tarsiifornies " (see Sinipsoii, '45) were widespread from Paleocene to oligocene when the family Anaptoniorphidac flourished. Three subfamilies, the Paromomyinae, the Omompinae and the Anaptomorphinae left their records in North America, while the fossil bones of the Nccrolemurinae have been found in western Europe.

At present, Tarsius spectrum is the only survivinq meinher of n once numerous family, leading a nocturnal life in the jungles of Borneo and the Philippine Islands (see Fulton,

Tlie first scientific descriptions of tlie brain of Tarsius appear to he that of v. d. Howen (1544), which Zielieii ('033) cites, and of Burmeister (1846). A detailed description of the macroscopic features of the brain were given hp Smith ('00-'03) and by Ziehen ('031). Smith's account has good line drawings, and contains numerous comparisons with other primate forms. Both authors stress the remarkably short and broad shape of the brain. Smith's brain had an enceplialic index of 116 (if the breadth of the hemisphere is taken to be half tlie breadth of the endbrain). The hemisphere has a large parietal and occipital lobe but a small, rather rudimentary frontal lobe. The olfactory lobe and the rhinencephalon is small. The parolfactory tubercle, on the other hand, of which Reccari ('10) gives a good illustration (his fig. 14) is fairly large when compared with that of other primates. Beccari

'39).

CORTEX O F TARSIUS 389

measured 2 by 4.5 mm in Tarsius, and 3.5 by 7 mm in nian. Ziehen recognized a short “Sylvian” fissure on the basal aspect of the hemisphere. Due to the rudimentary nature of the rhinencephalon, the fissura Sylvii arises in Tarsius not from the rhinal fissure (which is absent) but “quite freely.” I t also does not resemble the fissure of that name in the higher primates, where it “curves around the insula as tlie fissu1.a circularis externa, ” but shows “the primitive condition of a relatively microsmatic mammal in a very interesting and instructive manner. ”

Smith left open whether the sulcus in question was the “ Sylvian, ” “ or, perhaps the pseudosylvian element. ” On the dorsolateral aspect, Ziehen described a shallow indenta- tion, a parietal furrow which he considered as a constant feature. On the medial side there is the relatively deep calcarine fissure, sending off a short dorsal spur of hardly 2 rnm length, the parieto-occipital fissure, well shown in Smith’s figure 47. A hippocampal fissure completes the list.

Tilney ( ’28) concerned himself mainly with the brainstem. He gave, however, in his figures 45-47 views of the entire brain, and labelled the fissures. The sylvian fissure shown on the dorsal surface (Tilney’s fig. 45) is much smaller, and perhaps nearer the truth, than the one shown on the riglit lateral surface (Tilney’s fig. 47). Tilney stated that the sylrian fissure “unquestionably corresponds to that supra- rhinal fold which forms the mammalian pseudo-Splvian fissure.” This, it will be noted, is quite different from Ziehen’s interpretation, apparently not known to Tilney. Tilney closed the paragraph on the cerebral fissures with the remark that the hemisphere of Tarsius “would seem to represent the re- tention of definitely primitive characters in a brain in many other respects affected by marked progressive tendencies. ”

Ziehen described in another paper (’03b) the mes- and diencephalon of Tarsius. Of interest in the present connection is his statement that the crossed part of the optic tract is quite strong (ziemlich stark), that the thalamus allows to

390 GERHARDT vox B O R N

iwogiiize, “without forcing the issue ” (ungezwungen) only the reticular, anterior, medial and lateral nucleus as well as the habenular ganglia, and that the lentiform nucleus can be divided into two parts, a medial “portio reticulata” and a lateral “portio compactn.” The former is probably, still according to Ziehen, not homologous to the globus pallidus but may be Ganser ’s nucleus interpeduncularis, better called nucleus subpeduncularis.

A map of the cortical areas by Elliot Smith was published by Duckworth, and reproduced by Jones ( ’16). The map, constructed, so it seems, bv the same “macroscopic” method as the other maps published by Elliot Smith, shows a visual, an acoustic, a somosthetic and a motor area. A fairly large frontal and a large parietal area are left white, evidently to indicate that they form association areas. (See text under Jones ’ fig. 66.)

The cortical cytoarchitecturc was described by Woollard ( ’25a). His motor cortex is more extensive than that indicated by Smith, but there is still a fairly large frontal ter- ritory which Woollard subdivided into two areas 6 and 10. The somesthetic cortex looms large, and the temporal lobe (sit vcnia verbo) shows an elaborate subdivision.

The areas indicated on his map are not always described in his text. Thus the posterior limbic area 23 is neither de- wribed nor photographed. The inferior temporal lobe is labelled ‘ ‘ 21 ’ ’ in his figure, but described in the text as “ 20. ” The temporopolar area 28 is not mentioned in the text, while an area 25 is described but not shown on the map, although indicated in his figure 5.

The brainstem of Tarsius, too, was studied by Voollard (’28) in order to appraise the development of the epicritic and “dyscritic” (i.e. protopathic) systems. R e paid attention to the size of the posterior columns which he found fairly large (about 20% of the whole cross section) and to the trigeminal nuclei. The spinal tract is relatively very large, the main sensory nucleus appears comparatively small, but still larger than the motor nucleus. Woollard states that


his sections were not well suited to the study of the thalamus. He mentions, however, the large size of the stria terminalis and the good development of the habenular ganglia and the retroflex bundle of Meynert. I n a “preliminary note,” Wool- lard (’26) described the lateral geniculate body of Tarsius, confirming on the whole the description given many years before by Ziehen (’03b). The laminar pattern is simpler than in higher primates.

The thalamus of Tarsius was analyzed by Clark ( ’30). He described the nuclei in detail, and recognized several smaller ones which do not appear in the list which Ziehen had given earlier. We shall have occasion to allude to his description on the following pages.

The oculomotor nucleus has been investigated by Hunter (’23) and Clark (’26). The latter author found the large cells of this nucleus “compressed laterally and the cells more tightly packed together than is the case in the nucleus of the treeshrew.” One gathers that the nucleus of Perlia is poorly developed in Tarsius. LeGros Clark. cognizant of Hunter’s interpretation, specifically states that the large median cells are scarce and that the nucleus of Perlia is “feebly developed.” The Edinger-Westphal nucleus, on the other hand, is much more conspicuous and more extensive than it is in non-primates. Since Tarsius is reported not to be able to move the eyes in their sockets, the structure of the third nucleus is of special interest.

The weights of three brains have been communicated hp Ziehen (’02). After a short period in formalin he found 3.8, 4.0 and 4.1, i.e. an average of 3.97.

Kato (’38) found that brainweight increased by about 10% after an immersion in formalin for about two months, a statement that is well in accord with the earlier results of Hrdlicka (’06) who found, just as Kato, an initial rise, and then a gradual decline of the weight of conserved brains which in the course of a year or more led to an actual loss of weight as compared with that of the fresh organ of 5-10F. Ober-

steincr ('24, loc. cit., p. 452-453), in discussing the problem, points to the great difierences in the behavior of the brains of diffwent species.

The weights of two more fresh brains were given by Ken- nard and Willner ( '41) as 5.3 and 4.0 gm, respectively. These authors also give the body weight of a female specimen as 225 -gm, and that of a male one as 173 mni. Taking the a ~ c i - - tlgc body weight as 200 gm, and the average brain weight as 4.2 gm, one obtains a coefficient of enceplialization of 0.iO if based on the formula for primates, and of 0.60 if based on the formula of mammals in general (see Bonin, '45). I n either case, thc development of the brain of Tarsius is below the arerage for the class of mammals with which it is compared.

MATERIAL A S D METIIODS

This study is based on the examination of two brains. Thc first one the writer owes to the generosity of Dv. John F. Fulton, of Yale University. It had been immersed in a 10% solution of formalin. The other brain came from an animal which was bought alive by the Department of Neurology and Searological Surgery of the University of Illinois. The animal was sacrificed and embalmed with formalin, and the brain was then removed from the cadaver. Doctor Oscar Sugar performed all these tasks during a hot summer when the writer was on vacation. The first brain was cut in sagittal sections, the second in transverse sections, both at 20 p . Both series were stained with thionine. The technical work was done in the Department of NeuroIogy and Xeurological Surgery of the University of Tllinois.

The writer is indebted to Dr. Percival Bailey in whose laboratoi*y the technical work was done, under the reliable supervision of Miss Beatrice Kahn, to Dr. Oscar Sugar for his help in securing an excellent series, as well as to his chief, Dr. Otto F. Kampmeier, for putting the facilities of the Department of Anatomy at his disposal.


GROSS ANATOMY

The brain of our second specimen which can be trusted to have preserved its shape, had an encephalic index of 109, and agrees reasonably well with that which had been reported on by Smith. The brain of Tarsius is very “brachencephalic.” The frontal pole is narrow and set off from the rest of the hemisphere by a groove, as has been described by all previous authors. The occipital lobe, on the other hand, covers almost completely the cerebellum although it is thin and forms not much more than a slim outgrowth of the temporo-parietal lobe. The smallness of the corpus callosum is remarkable and the anterior commissure does not compensate for its astonishing underdevelopment.

The large roof of the midbrain is perhaps the most note- worthy feature of the rest of the brain. The brainstem forins with the asis of the forebrain, as defined by the base line of the corpus callosum, an angle of 127”.

The only fissure that is at all well developed is the calcarinc (see fig. 11). It extends from the occipital pole to a point close to the splenium of the corpus callosum.

Ziehen’s sylvian fissure can be followed on the ventral side of the hemisphere from section 160 to about 240. It takes (see fig. 11) an oblique course from frontolateral to occipito- medial, and the cortex medial to it is external to the claustrnm (see fig. 9, section 200).

There is no cingulate sulcus, the small corpus callosum has not had sufficient power, as it were, to leave an imprint on the cortex. Small indentations of the second layer of the cortex, described by Woollard ( %a), can be seen here and there on the lateral aspect (see fig. 9, section 250) but their loca- tion is erratic. Nothing indicates that one is dealing with the faint beginnings of fissures. The fissurets indicated by Zie- hen (’03a) could not be found.

The inferior horn of the lateral ventricle (fig. 1) does not bend forward as it does in all higher primates. Its shape is

394 GERHARDT VON EONIN

more reminiscent of that of the dog than that of a primate, even of galago. It does not seem appropriate to speak of a temporal lobe. The posterior horn is merely a small recess. However, the actual width of the ventricle is known to vary considerably, at least in humans, with age o r with wasting diseases of the brain.

The niacroscopic appearance of the brain differs from that of most other primates. Lissenceplialy in itself is nnimpor-

Fig. 1 Outlines o f brains, with lateral rentricle (stippled lines) of T: Tar- sius; D: Dog; and G : Galago.

tant in this connection. But the lack of a temporal lobe indicates a rather profound difference between Tarsius and other primates. The astonishingly large roof of the midbrain is another unusual feature. That the anterior tubercle is larger than the posterior one is, however, in keeping with other lower primates. But there are also similarities. St. George Mivart (1873) described primates as endowed with “a brain always with an occipital lobe and a calcarine fissure.” This fully applies to Tarsius.


ALLOCORTEX

Khile a detailed report of the allocortex is not within the scope of this paper, it is impossible to judge the brain of Tarsius properly without some information on the way in which the traiisition from macrosmatic to niicrosmatic brain has been achieved. Certain structures, such a s the cornu animonis which change little among mammals, which have been analyzed to perfection by previous workers, u7ill not be reviewed, while others, such as the parolfactory and the retrosplenial areas have to be described at somewhat greater length, in order to bring the neocortex into the proper pcr- spective.

Parolfactory structures. I n the ventromedial angle of the hemisphere, just behind the root of the olfactory tract, lies the anterior perforated substance and adjacent to it, on the medial side of the hemisphere, the septal region. Transverse sections shorn immediately that the two are intimately connected. There is, in the septal region, the nucleus accumbeiis, the septal nuclei proper and the nucleus of the diagonal band of Broca, which is continuous in its turn with the innominate substance of Reichert. Folded into these cell masses there is the “parolfactory cortex.” (See Beccari, ’10, figs. D-H.) The intruded part consists of Beccari’s “nido del setto,” the medial island (or islands) of Calleja, described by Loo ( ’31) f o r the opossum, by Fox (’40) for the cat, by Crosby and Humphrey ( ’41) for man, by Papez and Aronson ( ’34, see figs. 1-4), and by Lauer ( ’45) for the macaque. In all mammals, the stor;V is essentially the same with but minor variations, and it will suffice, therefore, we hope, if merely a verbal description is given for Tarsius. W e shall discuss below the thcories which have been built up around this area.

The first indication of the olfactory tubercle is seen in section 220 where an island of Calleja appears at the ventromedial border of the hemisphere. The precomniissural septum is still filled by scattered small cells, in continuity with the fairly large nucleus accumbens. 111 section 230 the

396 GERHA4RDT VON B O S I N

nucleus accumbens (see fig. 9, sections 200 and 250) can be distinguished from a cell group which lies medial alld dorsal to it and which should be interpreted as the beginning of the septa1 nucleus. But this group cannot pet be divided into it medial and a lateral nucleus. I n section 240, the nucleus accumbens has become smaller, and it is now easy to distinguish a small-celled lateral and a large-celled medial septal nucleus. Also, there is a large medial island of Calleja. The prepiriform area, recognizable by the lateral islands of Cal- leja, covers the ventral aspect of the hemisphere almost up to the fissura Sylvii without, however, quite reaching it. In section 250 (fig. 9) the nucleus accumbens has become still smaller. Lateral and medial septal nuclei have become small in section 270 and have disappeared in 280. I n this section, the bed nucleus of the anterior commissure and the nucleus of the diagonal band of Broca show well. The large cells of the globus pallidus have appeared for the first time in section 270. Section 280 shows a group of large cells ventral to the anterior commissure, and in section 300 a band of these cells can be traced from the nucleus of the diagonal band of Broca, through the group of cells just mentioned, to the globus pallidus. I n section 300 (fig. 9) the dorsal hippocampus as well as the nucleus amygdalae appears. By section 330, the preoptic nucleus is reached, and the nucleus amygdalae is well developed. The amygdala reaches its highest development, however, in section 350 (fig. 9). Here, too, the stria medullaris can be traced from that nucleus along the rriedial wall of the lateral ventricle, towards the thalamus.

Area prepirifornzis (fig. 2). The cortex covering this area is characterized by a second layer which contains rather large cells, arranged in somewhat irregular clusters. Beneath this layer there is a broad layer of small cells. Then follom a thinner lamina containing mostly larger cells, and finally a layer which resembles in its appearance the 6th laper' of the isocortex and can, just as that layer, be subdivided into two parts, an upper one, containing a denser, and a lower one


containing a sparser population of medium sized cells. The boundary against the white matter is not very sharp.

The retrosplefzial region (fig. 3 ) . It is difficult t o make out clearly the regio retrosplenialis agranularis since it is just at the lip of sulcus corporis callosi. I n any event, the inner

Fig. 2 Area prepiriformis of Tarsius.

granular layer of the posterior linibic formation ends before the cortex dips into the sulcus.

The deeper part of the wall of the sulcus is covered by the granular rctrosplenial formation. The thick outer “ graniferous” layer, to speak with Beck ( ’40), is easily recognized. The picture is similar to that given by Beck (’40) of Nycti- pithccus (see his fig. 20) although it is impossible to sub-


Fig. 3 Ketrosplenial area of Tarsius (in upper par t of photograph). Tllc section goes through a plane close behind the splenimn of the corpus callosuni. Note tlic proximity of the grsniferous area to the striate area (loiz-er part of the photograph).


divide the graniferous area of Tarsius as Beck did for Nycti- pithecus. Judging by Rose’s (’27) plate 11, figure 2 or plate 14, figure 2, the retrospleiiial regions of the mouse and of Icmui. catta idespectively also resemble that of Tarsius quite closely.

Laterally, the granif erous area borders on the subiculum. The boundary between the two is very sharp, even clearer as in Nyctipitliecus, if one can judge by Beck’s photograph.

ISOCORTEX

Cytoarcliitecturally, the isocortex can be divided into “eu- laminar, ’ ‘ ‘ agranular, ’ ’ and ‘ ‘ koniose’ types (see Bailey arid Boniii, ’51). The first one is roughly the same as Krod- mann’s homotypical cortex, it shows the 6 layers described by so many authors, without undue development of any of them. The koniocortex exhibits a tendency towards an ex- aggerated development of the inner granular layer, towards small size of the constituent cells, and towards a decrease in density in the 5th layer. The agranular cortex shows a poor inner granular layer, so that it is often impossible to recognize it in cell preparations, but a tendency towards large cell size and diminished cell density when compared with eulaminate cortex.

We shall start with the koniocortex, then discuss the eulaminate and finally the agranular varieties.

A. Kowiocortex

There is only one variety of koniocortex in the brain of Tar- sius: the striate area which, as is well known, receives visual impulses from the lateral geniculate body.

Striate oren (fig. 4 B ) . The striate area shows some elaboration over the pattern that is typical for the primates and that was described by LeGros Clark (’42) and by the writer (Ronin, ’42). For the light band iva (in the nomenclature of the writer) is split into three by an inter- vening dark band. Layers ii and iii on the other hand, are

400 GERHARDT VOK BONIN

almost indistinguishable from each other. Layer iii has a very sliarp lower boundaiy. Then follows the thick layer iva which has just been discussed, and then the coniparatively thin layer ivb which again has a very sharp lower boundary.

To state that iva is divided by a dark band rather than tliat ivb is divided by a light band may seem arbitrary at first

A €3

i 11

iii

ivaa

V

vi

Pig. 4 A Parastriate, and B: striate area. The layers of the striate area are tliscussecl in tlic text.

sight. It is based on the fact tliat the large solitary star cells of Meyiiert are fourid in iva a and in iva p, and, in diminished density, also in iva y. The rest of tlic cells are all of approximately the same size, as fa r as can be judged by ordinary observation under high power. Layer v is thick. It contains in its middle and lower reaches very largc cells which are obviously the pyramidal cells of Mcynert. Laycr vi is also


thick, it has an upper dense via and a lower light vib which in turn has a very sharp boundary with the white matter. The sharp lower boundaries of layers iii, iv b and vi b are very striking. The present account differs from that given by the writer some years ago ('42) which was based on a different specimen. It presents a different interpretation, but it shows not only the change of the author's mind but also the vari- ability of the striate area of Tarsius.

B. Eulaminnte cortex

This variety covers by far the greatest part of the liemi- sphere and is found, as should be emphasized, even in those regions which one would expect to receive the radiations from the ventral nucleus of the thalamus and from the medial geniculate body, respectively, i.c., the somesthetic and acoustic radiations.

Subdivisions within the eulaminate cortex can be made only in few instances. But in order to convince the reader photographs and descriptions of several locations are offered.

We begin near the striate margin. Parastriate cortex (fig. 4 A) . As one goes from striate to

eulaniinate cortex abrupt changes occur which, however, af- fect the middle and the inner main layer much more than the outer one. Indeed, layer ii arid iii differ but little from that of the striate area proper. Layer iv, however, becomes tliinner arid homogeneous. Layer iva of the striate area ends abruptly as has been described so often in all sorts of primates. Within the inner main layer the most dramatic change occurs in layer via. I ts cell density decreases abruptly as one leaves the striate area while that of v arid vib remains practically unaltered. Layer vib, however, shows still the curious horizontal arrangement of its cells which can be discerned in the striate area and which is also characteristic of the medial aspect of the frontal lobe in many primates, ~ . g . , the macaque or chimpanzee (FL in particular).

402 GERHARDT VON B O N N

The large cells in layer iiic which are so prominent in the ‘margo magnocellularis” of higher primates (OBy of Ec-

onomo, ’29, arid ORg of Bonin and Bailey, ’47) are missing in Tarsius.

Teinyoro-parietal cortex. As one leaves the parastriate area, mid proceeds in the series towards the ventral side of the hemisphere, the inner granular layer becomes a little thinner and lighter, and the 6th layer loses the tangential arrangement of its cells in the lower reaches as well as the sharpness of its boundary with the white matter. The 5th layer may be a little lighter, but the difierencc is but slight. The outer main layer shows no recognizable changes.

ParietaE cortex; (fig. 5 A) . Here again, the outer main layer can only arbitrarily be divided into layer ii and iii. There may be a thin band in which the cells are arranged more densely than in the deeper part of the outer main layer, but the thickness of this band varies from place to place, and it is not distinguishable everywhere with equal clearness. The “third” layer contains a few larger cells but it would be an exaggeration to speak of a cell gradient. The inner granular layer stands out distinctly and contains, besides a wealth of granules, a few larger cells. These are mainly found in its lower reaches and become still more nunierous as one enters the 5th layer where the large cells form a fairly def- inite band “va.” The lower part of the 5th layer is much poorer in cells, and the individual cells are smaller. The 6th layer shows a subdivision into three layers: A fairly thick layer via, rich in medium sized cells, a layer vilo of about the same thickness, but very light because poor in cells, and a narrow dark band of small, densely packed cells which has a fairly sharp boundary against the white matter. Layers via and vib show a columnar arrangement of their cells. The boundary with the white matter is blurred.

Postcei&aZ cortex; (fig. 5 B ) . Postcentral and parietal cortex differ only in a few minor points. The distinction between layers ii and iii is still more uncertain in the former than


in the latter. In layer iii of the postcentral cortex, there are more small cells than elsewhere, although cells of medium size still prevail. Layer iv is thick, but there are large cells in its lower reaches just as in the parietal lobe. Layer v is

A B

Fig. 5. A : Parietal cortex, R: postcentral cortex.

emptier than in the parietal cortex, but contains more cells than in the temporal region. Layer vi can easily be s~ib- divided into a via, richer, arid a vih, poorer in cells. There is further a narrow band of cells, just as in the parietal cortex, layer vie. The boundary with the white matter is quite sharp.


Temporal cor tex (fig. 6 A) . The outer main layer does not differ niucli from that of thc parietal cortex. The iiiiier grann- 1ar layer is well developed, and is densely filled with small cells. The ganglionic layer is much emptier than in the

a B

Fig. G . A : Tenipoial cortrx, H : posterior liinliie cortclx.

parietal cortex. Oiily quite sporadically can one see a sorne- what larger cell, most cells are small aiid scattered rather sparsely but evenly throughout this layer. The 6th layer shows a higher cell dcnsity tliaii the prccctling oiic, its cells are fairly


large, the boundary against the white matter is blurred. A subdivision of layer vi is scarcely possible.

Posterior limbic cortes (fig. 6 23). (The photograph is taken in such a way that the corpus callosum is towards the right side.) The most noticeable clmnge from the parietal cortex (and even that is not very conspicuous) is that the 4th layer becomes a little lighter. The second layer, too, appears to light up every so slightly, and to become a trifle broader, but these changes are all so subtle that they would go unnoticed but for the comparison with the adjacent parietal cortex. The 5th layer is thick, but that is mostly due, so it would seem, to the bending of the cortex around tlie dorsal margin. The boundary between 5th and 6th layer is blurred. When drawn so as to be in the continuation of these layers on tlie eonvex aspect of the hemisphere, the 6th layer appears very thick, and to be subdivided into an upper denser via, a middle, light vib, and a lower denser vie. The boundary against the white matter is sharp.

Insular cortex (fig. 7). I f the insula is defined (see Hal- ler von Hallerstein, ’34) as that part of the cortex which lies over the claustrum, then in Tarsius the island looks ventrad and is almost completely on the free surface of the hemisphere. The “cortex elaustralis” can be divided into three parts. Medially there is a short stretch in which the claustrum merges with the cortex and where the differentiation of the various layers is not well pronounced. Then comes a middle part in which the second layer shows fairly large cells arranged in a somewhat frayed manner, as one finds it in juxtallocortical formations. Here the 4th layer is empty and stands out as a narrow clear zone. Fifth and 6th layer are not well differentiated and there is fairly sharp boundary against the capsula extrema. In the lateral third, which is partly hidden in the furrow which forms the lateral boundary of the island, the second layer loses its juxtallocortical char- acteristics, and the 4th layer becomes well filled with granules and rather broad. Also the division between the 5th

406 GERHARDT v m BONlN

Fig. 7 Insular cortex. Note the “Sylvian fissure.’’ The upper margin of the photograph corresponds to the lateral, the left side t o the medial side of the hemisphere.


and the 6th layer becomes fairly clear, although a further subdivision, so obvious in other parts of the cortex, is not apparent. This is the insular isocortex.

Frogatal eularnimate cortex is practically non-existent. I n the sagittal series, the agranular area can be traced clear to the tip of the hemisphere. The transverse series is cut too obliquely a t the frontal pole to be of much use. I n any event, it is impossible to give a satisfactory photograph of any frontal eulaminate cortex which, if it exists at all, is clearly confined to the orbital aspect of the hemisphere.

The descriptions just given lead one to recognize but few varieties of eularninate coy tex : there is tlic general type, i~eprcsented by parietal, postcentral and insular cortex, there is the “ parastriate” type, obviously molded under the influence of the visual (striate) area, and there is the temporal type which may well represent the acoustic area. Histologi- cally a separate somesthetic area cannot be recognized.

G. Agranukar cortex

The brains of most primates show two types of agranular cortex: the precentral motor cortex and the anterior limbic formation. Strictly speaking, there can be no precentral cortex in Tarsius f o r its brain is lissencephalic. Yet the homologies with larger gyrencephalic brains are beyond doubt. It is also not entirely justified to speak of “agranular” cortex, for it is actually no more than dysgranular, as the description will make clear. Yet when scrutinized sufficiently, even the human preceiitral cortex is only dysgranular, and the term “agranular” can only be used loosely at best.

Precentrcxl cortex (fig. 8). The preceiitral cortex is thick as a whole. I ts outer main layer shows a slightly diminished cell density as compared with the rest of the isocortex. There is a very thin but easily recognized inner granular layer, followed by a thick 5th layer in the upper reaches of which the cells of Betz are found. The 6th layer shows a subdivision


into via and vib. The boundary against the white matter is blurred.

The size of the pyramidal cells of Betz is relatively small us compared with the size of the surrounding cells. They are fairly evenly spaced.

A B

Fig. 8. A : Anterior linibic cortex, R : motor cortex.

There is no clearly definable simple agranular area (comparable to area 6 of Brodmanii or FB of Economo) as in highel* primates. The Betz cells may become a little more scarce as one goes forward in the frontal lobe, but they arc found almost up to the tip of the lobe. Any division into “motor” and “premotor” area mould be quite artificial.


Amterior limbic cortex; (fig. 8 A). The cortex covering the anteromedial aspect of the hemisphere above the corpus callosum does not look very different from the rest of the eulaminate cortex. The 4th layer is, however, thinner than on the lateral side, and immediately beneath it there is a layer of fairly large cells, followed again by a stripe of smaller cells. Layer vi, with its two subdivisions does not look much different from that of the precentral cortex.

It is only quite close to the corpus callosum that the small cells of the 4th layer vanish as it were, and that something resembling the mesocortex (Rose, ’27) of other primates appears. It is only here that the inner granular layer iv is replaced by a narrow strip of rather large cells, convention- ally but mistakenly called va (see Bonin, ’49, see also below, section 200).

The cd l /grny cocficieii f

To gain some further insight, the cell/gray coefficients of samples from eulaminate, agranular and koniocortex were determined by the method of Chalkley ( ’43). An ocular is armed with several hairs (we used 4), and the slide is shifted many times from field to field under high power (oil immersion). For each observation the number of hairs which point on a cell and the number which point on intercellular space is recorded, until a sufficient number of observations have been made. The percentage of the times hairs point on a cell gives then a measure of the space occupied by the cells as against the intercellular space. For each determina- tion. 100 fields were observed. thus 400 “throws” were made, and the sampling errors were computed on that basis. The superior parietal area, the striate area, and the giganto- pyramidal area were selected. I n order to have some comparative material, the homologous areas of the human brain were also measured.

Table 1 gives the results.

410 GERHARDT VON BOXIN

Tlie supragranular layer shows in Tarsius a markedly lo.lr.er c*cll/gray coefficient in the agranular as coinpared with the eulaminate cortex (9.5 -+ 3.4), but does not show a significant increase from eulaminate to koniocortex. Tn man, 011 the other hand, agranular and eularninate cortes differ only iasig- nificantly, while the visual koniocortex shows a n increase by 30 t- 3.7% so that its cell/gray coefficient approaches that of Tarsius within the limits of sampling 0 errors.

hTRlATR BULAMISATE A(4RANGLiR

1,ayer ii + iii Tarsius 1 2 & 2.,j 3 9 2 2 . 4 29.5 i 2.4 Man 40 i 2.4 20 & 2.0 16.5 2 1.8

Layer v Tarsius 2G i 2.2 31 i “ 3 22 i 2.1 &fan 22.5 & 2.1 1 7 -+ 1.9 I 6 5 1.8

I,:iyer vi Tarsius 39 i 2.4 3 2 t 2.3 32 & 2.3 Man 32.3 2 2.3 23 i 2.1 20 i- 2.0

__ -. - __

The middle main layer can only be compared between eulaininate a i d koniocortex since, by definition, it is negligible in the cell preparations of the “agranular” cortex. While the koniocoi*te\- of Tarsius does not differ significantly from the eulaminate cortex, the granular layer of the human koniocor- tcx shows a significantly higher cell/gray coefficient (9 2 3.2%) than the eulaminate cortex.

The inner main layer shows no consistent trends. Tlie cell density of the ganglionic layer of the koniocortcs decreases


in Tarsius, and increases in man when compared with the eulaiiiiiiate cortex, although the differences are not statis- tically significant. It shows a significantly lower cell/gray coefficient in the agranular cortex as compared with the eulaniinate cortex in Tarsius (9 -t 3.1), but not in man. Layer via has a higher coefficient in man’s koniocortex than in his eulaniinate cortex (9 t 3.1) but the difference between these two types in Tarsius ( 7 3.3) is not significant “on the 1 ”/. level. ’

By and large, of course, the cell/gray coefficient is lower in man than in Tarsius. That could have been ascertained without elaborate measurements. It is unexpected, however, to find the cell/gray coefficient almost the same (within the error of random sampling) in the outer main layer of the striate area of man and of Tarsius, but to find the inner granular layer of that area definitely “lighter” in man.

SURVEY BY SERIAL SECTIONS

A brief survey of selected serial sections of the transverse series will, it is hoped, help the reader to understand the rela- tive positions of the cortical areas to each other. We shall start near the frontal pole. Approximately every 50th section will be described. But in some instances odd sections were selected because they showed certain points better than the even 50th section would have done.

SPctimz 2200 (fig. .9) goes through the germ of the corpus callosum and through the deepest part of the “fissura Sylvii.”

On the medial aspect, close to the corpus callosum there is a short stretch, almost hidden in the SU~CLM corporis callosi, ~ h i c h has no inner granular layer, but shows a band of rather large cells in its place. This is clearly anterior limbic cortex ( JA) . But most of the dorsomedial wall is covered by eulaminate cortex which, however, shows a slight attcnua- tioii of the inner granular laycr noticeable perhaps only wlicii compared on the same slide with the cortex on the lateral side.


The cortex on the lateral side shows a well developed inner granular layer, and a broad 5th layer the upper part of wliich contains a fairly dense population of large pyramidal cells. Near the veiitrolateral margin and in the depth of the fissure the cortex is cut too obliquely to read. The cortex on the ventral aspcct, medial to the fissure, is covered by insular cortex. On the veiitromedial side the cortex shows an orderly arrangement of the cells of thc inner main layer.

The caudate nucleus is large. it can be followed on to the medial side of the ventricle into a nucleus accumbens. The lentiforni nucleus is just cut, it presents a hoinogeneous mass of cells connected by irregular strands with the caudate nucleus across the internal capsule. Evidently we are dcal- ing with the putamen. Opposite the cortex near the Sylvian fissure, the claustrum can be discernccl. I ts lateral extremity fornis a distinct bulge, towards the medial side it tapers into a iiarrow band which fuses with the cortex.

RPcfion 250 (fi.g. 9) goes through the corpus callosum and tlirough tlic aiiterior part of tlic internal capsule. Beneath thc corpus callosuni, the thick septum impresses tlie observer. I ts lateral part contains the nucleus accumbens. I n the medial part of the septum there a rc some lai-ger cells.

ARBHEVTATTOX8 FOR BlGtTRE8 9 ,4SD 1 0

A, llllcieus anlygdalne To, isocortex oreipitalis A c. 1111 cleu s a ccunihni s C, iinrluus raudatns

JA, juxtalloeortes 11, substautia nigra

ca, anterior conmiissure ~ a l , calcxrine fissure cc, corpus rallosuni C1, claustrum rp, roiliniissiira posterior E, rula~niuate cortex (1, niir leus niedialis tlialaiiii I?, fornis V, lateral rentrirlr (s1i:idetl in all gl, corims geuiculatuin laterille sketrhes) T, internal rapsule

460 mark hippocampus and su1)stantia nigra.

OK, ocripital koiiiocortex P, putanleu + glohus pallidus pp, pes pedunruli r, zona reticulata tlialaini Rsg, area retrosplenialis granifern T, thalamus

17, nucleus veil t ra lis . t h a la ini Heavy bars in sections 250-340 mark islands of Callcja, in sections 400 and

CORTEX OF TAR.SIUS 413

Caudate nucleus and leritiform nucleus are both large, the latter appears still to consist exclusively of the putamen.

The medial aspect of the hemisphere is covered by anterior limbic cortex. The inner granular layer begins almost es- actly at the dorsal margin, and the whole lateral aspect is covered by essentially the same type of eulaminate cortex The 5th layer may be slightly better filled with cells in the

200 W

300 3 4 0

Fig. 9 Serial transverse sections through the brain.

414 GERHARDT VON BOKIN

dorsal part, between dorsal margin and the arrow, than further ventrally.

The cortex on the ventral side cannot be read, the medial half of the ventral aspect is covered by prepiriform allocortex.

4 00 4 6 0

5 4 0

Fig. 10 Serial transrerse sections through the brain.


Sectioiz 300 (fig. 9 ) cuts through the corpus callosum and through the anterior comniissure which, in Tarsius, crosses at the level of the thalamus. Ventral to the anterior commissure the septa1 region can still be made out. The nucleus of the diagonal band of Broca is conspicuous by virtue of its large cells. Streamers of such cells can be followed, as has been described f o r the macaque (Lauer, ’45), towards the globus pallidus and towards the amygdala.

The thalamus is cut a t about the level of Clark’s (’30) text figure 3. The lateral, the paratenialis and the anterior nuclei can easily be made out. I n the corner between anterior and paratenialis there is a conspicuous group of large cells not shown by LeGros Clark, obviously an intralamellar iiucleus. The reticular nucleus, next to the internal capsule, is large, particularly in its anterior portion.

Caudate and putamen appear again, but there is now a group of large cells medial to the putamen, perhaps repre- seiiting the globus pallidus. It may be followed far mediad and corresponds to Ziehen’s (’03b) description of the “zona re ticulata. ’ ’

The anterior end of the supracallosal part of the c o r ~ ~ u amrnonis has been cut. Going laterad from here, in the fissura corposis callosi, one comes first to a small clump of cells representing the subiculum and then to the retrosplenial graniferous formation which fills most of the hidden part of the cortex. On the medial aspect of the hemisphere, the posterior limbic formation is encountered. The upper part of the lateral aspect, as far as the arrow, is covered by eulaminate cortex which shows the elaborate lamination of the 6th layer described above f o r the parietal formation (p. 402). The lower part of the lateral aspect is covered by eulaminate cortex described as tpmporal cortex (TI. 404). This cortex can be followed as fa r as the lateral third of the ventral aspect. There it goes over into allocortex, and its deeper layers merge almost imperceptibly with the ampgclalar nucleus.

416 GERHARDT VON BOXIN

Section ,340 (f ig. 9) corresponds roughly to Clark's ('30) text figure 4. It is occipitad to the corpus callosum and cuts the ventricle just in the plane where it goes over into the inferior horn.

The various nuclei of the thalamus can be recognized. Yet their outlines are not nearly as precise as they are in man o r other higher primates. The medullary laminae are difficult to discern in cell preparations so that the boundaries of the thalamic nuclei remain vague. This is especially true of the medial (dorsomedial) nucleus whose size is almost impossible to estimate. While the caudate nucleus is not in the plane of section, the amygdalar nucleus looms large in the ventromedial part of the hemisphere.

The cornu ammonis is fairly far laterad, but in a position comparable to that in which it was found in the previous section. From the hippocampal formation, one can follow the fascia dentata and subiculum into the retrosplenial area, again completely hidden in the depth of the sulcus corporis callosi the prolongation of which is still in the plane of section. Both medial and lateral aspect of the hemisphere are covered by eulaininate cortex. Just as in the previous section, the dorsal part of the cortex shows a tripartite 6th layer while the ventral part conforms to the usual pattern. The ventral aspect bears still a fairly broad strip of prepiriform allocortex, covering the amygdalar nucleus.

S e c t i o n 400 (f ig. 10) goes through the optic chisma, and through about the middle of the lateral geniculate body. It cuts through the beginning of the anterior quadrigeminal body, and hits the ventricle just occipital to the communication between the body of the ventricle and the inferior horn. The hemisphere becomes now quite thin. Beginning at the angle between medial and ventral surface, opposite the anterior tubercle of the midbrain, there is a short stretch of striate area (OK), Going ventrally, the striate area is bor- dered by an ill-defined cortex, marked " ? " which fails to ex- hibit any lamination and which soon goes over into the graniferous retrosplenial formation. Tn its turn, this formation

CORTEX OF TARSIUS 417

borders ventrally on the subiculurn and the fascia dentata, and one is then led to the cornu ammonis, thus rounding the medial hollow of the hemisphere. Ventroniedially the amygdalar nucleus and some allocortex is encountered. But towards the veiitrolateral corner one soon finds again eulaminate cortex, though still with a very dark and pronounced outer granular layer, containing larger cells than usually. Also, the inner main layer seems broader and to contain more, although smaller cells than in the rest of the isocortex. This is temporal juxtallocortex. On the lateral side, eulaminate cortex of the typical appearance predominates except for a small part near the dorsal margin which is covered by striate area.

Section 460 (fig. 10) goes through the aqueduct of Sylvius and the posterior end of the lateral geniculate body.

Dorsal to the anterior quadrigeminal body the calcarine fissure presents a convenient landmark from which to start. The cortex of both walls of this fissure is covered by striate koniocortex and this extends on the lateral surface of the hemisphere as far as the arrow. Ventral to it the cortex turns into eulaminate. I n the dorsal portion the boundary against the white matter appears sharper, and the horizontal arrangement of the cells in layer v and vi are more pronounced than further ventral where the eulaminate cortex takes on its usual appearance (see above, parastriate area). Ventrally the cortex shows a second layer containing astonishingly large cells, somewhat irregularly arranged. This should be considered juxtallocortical. On the medial side the cortex is cut obliquely and cannot with certainty be recognized. Just opposite the lateral geniculate body there seems to be some retrosplenial graniferous formation.

Sectioiz. 488 (fi.9. 10) goes through the occipital region, and shows a deep calcarine fissure. Both walls of the calcarine fissure are covered by the striate area which extends over almost two-fifths of the lateral aspect, and extends on the medial side well below the calcarine fissure. The cortex on the


lateral aspect below the occipital koniocortex is parastriate (see p. 401).

Below the parastriate area the cortex is cut obliquely and is continuous with the cortex of the medial side. Below that spot, there is typical eulaminate cortex. On the ventral side, the large cells in layer ii and the narrow empty stripe below layer iii betray the presence of juxtallocortes. The cortex on the medial aspect of the hemisphere cannot be read. The hrainstem has been omitted from the sketch.

S e c t i o n 540 (f ig. 10) goes through the occipital pole. The ventricle is no more cut. The calcarine fissure is still quite deep. The striate area extends from a point fairly far ventrally on the lateral aspect all over the dorsal margin, on both sides of the calcarine fissure and on the medioventral aspect of the hemisphere. Only the ventrolateral part is covered by the parastriate area.

T H E BRAIN M A P

The map of the cortex of Tarsius which is offered here (see fig. 11) is simpler than that published previously by Wool- lard ( '25a). Although the juxtallocortical formations (6) are fairly large, the olfactory areas proper are so small that Tar- sius can rightly be considered microsmatic. I n contrast, the striate area (1) is large, and contains a fairly deep axial furrow, the calcarine fissure. It is surrounded by a parastriate area (2) which, however, shows not quite the same histologi- cal elaboration as in higher primates. Amidst the rather large expanse of eulaminate cortex (3) which covers the parietal region, there is dimly discernible a temporal region (4) which can be suspected to be the end station of the acoustic radiation, although no proof for this statement has ever been given. It is not possible, however, to recognize by cytoarchitectural criteria a soniesthetic area. The motor area (5) , on the other hand, histologically recognizable by the Betz cells in its 5th layer, can be mapped out easily enough. It covers almost all of the frontal part of the brain. There is a small

Medial side

Loterol side

1. 2. 3. 4. 5. 6. 7.

Pig. 11 Brain map of Tarsius:

Striate area (occipital koniocortex, see fig. 4 B). Parakoniocortex (see fig. 4 A) . Eulaminate cortex (see fig. 5 A and B and fig. 6 B). Temporal cortex (see fig. 6 A) . ' ' Agranular cortex ' ' (see fig. 8 B) . Juxtallocortex (see fig. 2) . Anterior limbic area (see fig. 8 A ) .

419

420 GERHARDT TON BOKIN

insular region, not shown on the map, which is laterally bound- cd by a sulcus, which as we saw, has heeii designated as Sylvian fissure by Ziehen, and “perhaps suprasylvian” by Smith. The medial side shows a rather small anterior limbic region ( 7 ) , which for purposes of demonstration, has been drawn larger on the map than it should have been.

COMMEKTS

The brain of Tarsius exhibits a curious mixture of ad- vanced and primitive traits.

I ts extreme brachencephaly goes counter to Ariens ICap- pers’ findings ( ’27) that animals which have a higher cephalization coefficient are more brachencephalic than those with lower coefficients.

While the brain of Tarsius is microsmatic, as that of all otlicr primates, its prepiriform and juxtallocorticd f orma- tions are relatively larger than in higher primates. Also, the olfactory bulb is not underneath but in front of the frontal lobe. But this may be due to the poor development of the frontal lobe rather than to a good development of the olfactory apparatus.

The septal and parolfactory formations are structurally well developed, but again no better than in other primates. Edinger’s (’08) conception of the parolfactory area as the centey for the “oral sense” comes to mind. He based his ideas, as the reader will remember, on the fact that the parolfactory area received fibers from the pontine region, pre- sumably from the trigeminal nuclei (see Edinger, ’11, fig. 289) as well as from the olfactory regions. Dell’s work (’50) makes it appear likely that vagal impulses which reach the orbital aspect of the frontal lobe may also influence the parolfactory region. Edinger visualized a center which could synthetize infomiation gathered by all the sensory nerves of the muzzle. That the septal region is of some importance in connecting endbrain and hypothalamus, has become evident from the recent experiments by Hess (’48) who could evoke


panting, sneezing, salivation and decrease of respiratory activ- ity by stimulating the septa1 region of the cat. Its I-ole in the primate brain is not yet well documented. I t is largely f o r this reason that a wide definition of the parolfactory area was preferred, although both Johnston (’13) and Young ( ’26) tried to separate the parolfactory area from the septa1 region proper.

While Tarsius would seem to have made the trailsition from olfaction to vision as the main “gnostic” sensory modality, the good development of his muzzle is mirrored in the rda - tively large size of his parolfactory area.

The brain of Tarsius is the smallest primate brain whicli has a posterior horn of the lateral ventricle, and which tlicre- Fore can be described as having that ill-defined part, a posterior lobe. The laminar pattern of its striate area exhibits even better “workmanship” than that of man, particularly in its inner granular layer.

We are unfortunately not well informed about the rest of the visual system of Tarsius. I t s retina contains only rods as Detwiler ( ’39) asserts on anatomical examination. The complicated folds which Woollard ( ’25b) described near the “niacula” and of which Franz (’34) gave a diapram- matic representation look more like distortions than anp- thing else and have not been found in well preserved eyes (Polyak, ’50). It was said by Woollard ( ’25b) that the optic nerves undergo a complete decussation in the chiasma, although Ziehen ( ’03b) had previously mentioned merely the crossing of many fibers. The lateral geniculate body has a structure that is simpler than that of other primates (Ziehen, ’03b ; Clark, ’30).

The arboreal life of Tarsius demands among otlier. abilities precise discrimination of the distance of branches on which to jump. Ever since Wheatstone invented the stereoscope, depth perception has become intimately correlated wit11 hinoen- lar vision in the minds of biologists, and occasioiial difficulties such a s to pour wine into one’s glass under tlie guide


of only one eye have only strengthelled this conviction. Smith’s discussion (’27) is a good example of this attitude. Yet psychology (see Gibson, ’SO) has shown beyond doubt that visual depth perception depends much more on other factors such a s “texture,” than on binocular vision. The reader should inspect the photographs in Gibson’s book in the man- lier demanded by the author, i.e. with one eye shut and slightly closer than he is accustomed to look a t pictures and startle liimself by the sudden appearance of the depth effect. The in terpupillary distance makes it indeed doubtful whether binocular vision, with its convergence and its retinal dis- crepancies can contribute much to the judgment of depth beyond tlie reach of the arm. If Woollard observed the total crossing of the optic fibers in the chiasma correctly, and if it is true that Tarsius is unable to move his eyes in their sockets, Tarsius cannot rely for depth perception on binocular vision. That ability to perceive depth is in some way to be correlated with the peculiar structure of the striate area, may nonetheless be true. The simple hypothesis of Baranyi and Kleist (see Kleist, ’26) receives no support, however, from the anatomy of Tarsius. Whether the close vicinity of the anterior end of the striate area to the retrosplenial granifer- 011s region (see fig. 3) could somehow pave the way for tho shift from olfaction to vision, that central riddle of primate cvolution, cannot be discussed so long as we are ignorant of tlie function of the retrosplenial area.

In the acoustic system, the medial geniculate body appears to have reached about the same degree of differentiation as in other primates (Clark, ’30). Clark mentions that the caudo- ventral element is smaller in Tarsius than in Cercopithecus. Rut since this element sends its fibers to the zona incerta, it has probably little to do with “conscious” perception of acoustic stimuli. The cortical acoustic area is, on the other Iiand, distiiictly less developed in Tarsius than in higher forms. Indeed, it was only by unproved surmise that it could be located in the cortex at all.


The somesthetic system is astonishingly poorly represented in the cortex of Tarsius. As we learned in the introduction, the posterior furiiculi represent in the cervical cord about 20% of the whole white matter. This compares well with some of the figures given by Brouwer (’15) for other primates (Oedipomidas, 20% ; Callitrix, 215% ; Cebus, 25% ; man, 3974 ; all in round figures).

The motor cortex shows a simpler structure than in higher primates. The differentiation into motor and premotor area, i.e. into area 4 or FA and 6 or FB is not present in Tarsius, nor can anything even remotely resembling area 44 (or FCBm) be found.

It is instructive, finally, to point to the differences between the brains of Tarsius and Galago, Smith’s statement (’03b) that? “the brain of Tarsius exhibits decisive evidence of its lemuroid status ” notwithstanding. Figure 1 2 shows, in sagittal sections for the poorness of which the writer ought to apologize, the medial island of Calleja in the two brains. The island in Tarsius is not only much smaller but shows also a much poorer degree of differentiation than in Galago. On the other hand, the brain of Tarsius shows a much better dcvclopnicnt of the visual area and with it of the occipital lobe than Galago. There is a posterior horn in Tarsius, hut not in Galago (fig. l), the striate area shows the typical primate pattern of the multilaminate type in Tarsius, but, for the most of i ts extent, the simple “subprimate” type in Galago (see Bonin, ’45, lout also Solnitzky and Harman, ’46). P e r contra, Galago has a fairly large frontal cortical field, arid a clearly recognizable inferior horn, while Tarsius is still without a temporal lobe in the true sense of the ~ o i d , thus perhaps lacking that “hierarchy of functions” to which Gibbs (’51) has only recently called attention from a clinical point of view. Since the temporal lobe, and the epileptic disorders which occur in its pole with astonishing frequency (see Bailey and Gibbs, ’51) have become of major clinical in-

424 GERHhKDT VON BONIN

Pig. 12 Medial islands of Calleja, in sagittal sections. Above: Tarsius, below, Galago.


terest, it may not be amiss to point to the seeming parallel evolution of the temporal and the frontal lobe in primates.

Neither Galago nor Tarsius has a brain that could be considered as the ancestral form of the human brain which must have combined quite early a balanced evolution of both occipital and fronto-temporal regions. T h e n studying the cerebral hemisphere one is inclined to concur with the conclusion at which Strauss (’49) arrived on the basis of entirely different evidence, namely that “the stock from which man arose was monkey like,” and “did not evolve directly from tarsi- oids.”

What becomes clear, in any event, by this comparison is that the primate brain differs from that of other mammals in at least two respects: in the structure of its visual areas as well as in the extent of its fronto-temporal regions. It appears also safe to state that frontal and temporal lobes go hand in hand in the degree of their development among primates.

SUMMARY

Tarsius has an extremely brachencephalic brain. The coefficient of encephalieation is low. The rhinencephalon is small, the parolfactory and septa1 regions show the same structure that is found in other mammals, but these parts are smaller than in Galayo.

The cerebral hemisphere has a small occipital lobe, but does not possess a true temporal lobe, as evidenced by the shape of the lateral ventricle.

The isocortex has a very large and well differentiated striate area and an easily recognized although only “dys- qranular” motor area. The rest of the cortex shows poor differentiation, in particular it is almost impossible to recognize a somesthetic and an acoustic area. Frontal (or prefrontal) areas are very small. The poor fronto-temporal development makes it hard to accept the brain of Tarsius as the model of a stage through which the human brain evolved.


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