T H E STRIATE AREA O F PRIMATES

GERHARDT VON EONIN Department of Anatomy, College of Medicine, University of Illinois, Chicago

TEN PIUURES

The visual or striate area of primates is easy to recognize even with the naked eye, as Gennari and Vicq-d’Azyr dis- covered more than a century ago.

Microscopic studies confirmed that this area has a char- acteristic stratification seemingly all of its own. The problem naturally arose to reconcile this pattern with that discernible elsewhere in the iso-cortex. Brodmann ( ’09) and the majority of those who studied primarily Nissl preparations held that in the striate area of the primates the internal granular layer was split into three sub-layers. Brodmann’s conception was developed further in two directions. It received a theoretical interpretation by v. Volkmann (’28) who considered the split- ting of the fourth layer as an example of “diachoresis.” A functional interpretation was attempted by Biiriinyi (’25) and Kleist ( ’26). These authors postulated that impulses from one eye went into the lowest, those from the other eye into the highest of the three sublayers, to be synthesized into a binocular image in the middle layer. That theory, never definitely proved nor definitely refuted, has exerted a powerful influence on neurological thought.

Other workers in this field, such as Ram6n y Cajal (’ll), Campbell ( ’05) and Lorente de N6 ( ’35) have never accepted Brodmann’s interpretation but rather looked upon that layer which Rrodmann called IVA as a part of the third layer, the cells of which were merely smaller and hence more densely crowded than elsewhere in the cortex.

405

406 GERHARDT VOK BONIX

To convince oneself that this is more than merely a play with words, one has only to go back to the fundamental pattern of the iso-cortex. This has recently been explained in a masterly fashion by Lorente de N6 ( '38 a) to whose description the reader may be referred. Suffice it to point out that only the outer stripe of Baillarger contains terminal ramifications of the specific afferents, i.e., of the thalamo-cortical radiations and that this stripe is situated mainly in layer iv of Lorente dc N6. Impulses from the periphery affect therefore most powerfully those cells whose pcrikarya or dendrites are situ- ated in that layer.

We lose much of our labor if we describe the stratification of different areas in identical terms without having made sure that the layers so designated are homologous. Homologous layers have by definition the same relation to the axonal plexus and contain the same type of cells. The former criterion is even more important than the latter, for the functional dignity of a layer is more profoundly affected by its connec- tions or lack of connections with an axonal plexus than by the type of cells it contains. When Brodmann called a certain layer of tlie striate area IVA, he implied therefore - and it is obvious that he was widely understood to imply - that this layer was in direct contact with the incoming impulses, just as it is in any other part of the cortex. When Campbell, Ram6n y Cajal and others called this same layer iii, they implied on the other hand that it was above the axonal plexus of the stripe of Gennari, and was, therefore, subservient to intra-cortical rather than to thalamo-cortical events.

To decide between these two views can obviously only be done by studying silver preparations since these alone are able to show both fibres and cells at the same time and to show tlie cells with their dendrites and axons. Bodian preparations of man, chimpanzee and macaque were available, Golgi preparations were made from man, macaque and mangabee and impregnations after 0. Shultze and Stohr ( '21) of human and macaque material were examined. Thc Golgi impregna- tions were prepared after Bubenaite ('29). The method is

THE STRIATE AREA O F PRIMATES 407

sure to bring out something and can even be used 011 material kept in formalin for 1 to 2 years. Impregnations of axis cylinders were rare, and even then obviously imperfect, hut dendrites and cell bcdies were well demonstrated. The method has been used by the writer for many years in (unpublished) studies, so that enough comparative material was at hand. While the material is still insufficient for an exhaustive study of the striate area, it is adequate for a decision between Brodmann’s and Cajal’s conceptions.

I n the interest of a coherent argument, it is necessary to marshal known facts together with the observations to be recorded in this paper.

The discussion of the next paragraphs will be based mainly on Cajal’s analysis of the stratification of the stria ct t e area. His numbering has the advantage of being purely descriptive, and is, moreover, well enough known to afford a good basis from which to start. Cajal’s scheiiie is indicated in figures 1 and 2.

For greater clarity we shall employ different symbols for the different schemes set forth in the literature. Cajal’s layers will be referred to by Arabic numerals, Rrodmann’s layers by Roman numerals in capital letters and Lorente de N6’s scheme by Roman numerals in small letters. Also, Brodrriann’s sub- divisions will be given in capital letters, and those of Lorente de N6 in small letters.

We turn first to the architecture of the striate area (fig. 1). The first or molecular layer was mainly studied in prepara- tions after Schultze-Stohr. The inyeloarchitectural subdivi- sions described by 0. and C. Vogt (’19) can be recognized without difficulty. A thin outermost layer is almost free of formed elements. Then follows a fairly dense plexus ib of coarser “ground fibers.” The inner half of the first layer is occupied by a sparse feltwork of finer fibers, intermingled with the end tirborizations of the apical dendrites of pyramidal and other cells situated in the deeper layers of the cortex.

There is little to he adcled to Cajal’s description of layers 2 and 3. In both, pyramidal cells are the prevailing elements.

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THE STRIATE AREA O F YRIMATES 409

They are smaller in the “outer granular” layer, but the difference in size is not as great as it is in most other parts of the cortex. The differentiation between these two layers is fa r less pronounced than in many other cortical areas. The same impression is given by the myeloarchitectural pattern which shows an almost homogeneous, rather sparse feltwork of ground fibers without a conspicuous stripe of Kaes- Bechterew.

The lower part of Cajal’s third layer is that which Brod- mann and many others called IVA. As explained in the intro- duction, its composition is o€ special interest. Unfortunately, the Spanish master merely states that this layer does not differ much from the pyramidal layer elsewhere in the cortex. That it does contain pyramids was noticed by v. Economo and Koskinas ( ’ 2 5 ) in Nissl preparations and was verified by Lorente do N6 ( ’ 3 5 ) a few years ago in Golgi preparations. The pyramids of this layer can be divided into two classes by paying attention to the development of their basal dendrites. Those belonging to the first class (cf. fig. 1, 1) have short basal dendrites. These processes are few in num- ber, and show comparatively few branches, which do not leave the third layer. Some cells of this class have one or several dendrites coming off from the perikaryon or from the apical dendrite near the perikaryon, and ramifying in the lower and upper part of the third layer. The pyramids of the second class (fig. 1, 2) have long and well-developed basal dendrites which dive into the subjacent fourth layer. Aside from pyramidal cells, the third layer contains double bush cells and others of Golgi type 11.

Cajal’s fourth layer contains, according to his description, giant star cells, middle-sized pyramidal cells and small star cells with short and ascending axon. He considers the giant star cells as the typical element of this layer. Our own observa- tions confirm the presence of these cells in the fourth layer. The dendrites of the giant star cells (fig. 1, 3 ) branch out mainly in a tangential direction. They may be quite long, but they rarely leave the fourth layer. Only those cells which

410 GI!!R,HARDT VON BONIX

are situated in the lowest part of layer 4 send some of their dendrites into the fifth layer. No dcndrite has been observed to run into the third layer. This behavior of the dendrites of the giant star cells is shown in Cajal’s figure (383) biit is not especially emphasized in the text.

The pyramidal cells of layer 4 possess comparatively short basal dendrites. Again two types can be differentiated. The cells of the first class (fig. 1, 4) h a w numeroiis and fairly long dendrites coursing within the fourth and fifth layers. These processes are given off from the base and thc sides of the perikaryon and from the lowest par t of the apical dendrite. X o branches appear to be given off by the apical dendrite in layers 2 and 3. It is probably a fine point whether these cells should be considered as pyramidal cells o r as star pyramids in the sense of Lorente de N6. The other type ( f i g 1, 5 ) gives off few and short basal and “lateral" dendrites in thc fourth layer and has an apical dcndrite which sends off side branches into the third arid second layer. These pyramids resemble most closely thc “border pyramids ” described by O’Leary (’41) in the striate area of the cat. The dendrites of the small s tar cells, Cajal’s third catcgory, appcar to ramifv exclusively within the fourth layer. We have nothing to add to t’ajal’s description of them.

The fifth layer of Cajal, or the layer of small star cells shows a much greater cell density than the preceding one. T t is filled mostly with small cells which, according to Cajal, send their axoiis in a tangential or an ascending direction. It is largely from these cells, as well as from the cells in t’lajal’s sixth layer that the association fibcrs within the stria of Gennari take their origin.

The layer of small pyramidal cells with ascending asons, Cajal’s sixth layer, contains ordinary as well as “short” pyramids (Lorente de N6, ’38a). The latter (fig. 1, f;), havc an apical dendrite which ramifies within the fourth or fifth layers. These cells send their basal dendrites in a strictly tanqential direction so as to ramify exclusivcly within the sixth layer. The course of their axon, as described by Cajal,

TUB S’I*RTATE AREA OF PHIMATES 411

suggcsts that some of the irripulses sent. out by them rcacli thc stria. of Gcnnari.

Cajal’s scveiith layer is a t.hin st.rat.um, defined as the layer of tho giant pyramidal cells. These cells, the so-called solitary cells of Mcynert (fig. 3, 7 a.nd 8 ) , arc geiicrally considered to give rise to yrojcctiori fibers from t.he stria.te area. They can riot rightly be called giant cells if thc calls o f Betx arc! t.akeii as ti staiiclard, for iii man, the iiuclear volume of thc? latter mas foiind (v. Boiiiii, ’38 h aid ’39) to be 2330 % 62 p,” while the size of the cells of 3Cejmrt was 607 32 H.“ We sliall thcrefore call these cells “large” rather than “giant” pJ-ramidal cells. The xhapo of t.he pcrikargozi of the cells of M e p e r t does not appear to he different from that of otlicr dccp 1~yraiiiicla I cells in comparahlc locations. Tlic apical dcntlritc wtis described hy Cajal t is ascending to the iiiolccular lilyel*, a stateirient that c w i unlicsita.tiiigly be accepted. The dcndritc gives off rami in tho sixth, third and scconci layor~s, but iiot in tlic fifth aiid fourtli. (hjal st.atcd that the basal dendrites spread out “rigorously parallcl to the aurfacc. ’’ We tire mitiblc lo confirm this stuteiricnt. 111 our own prcpirti- tions, tho long arid tliiek basal dendritcs arc clctirly stxm to iiivado tho eighth aiid some1 imcs even the ninth laycr, rcacliiiig almost to the white matter. Tliei*e is a curious asymmetry. While the basal clendritn of one sidc will go toward tlic white niat.tcr, its fellow of the otliei* sidc of the pei*ikiir-yoii will sprc?ad in a s1ightl-j- npvr.ard direction to branch out in tlie serenth and sixth layers (fig. 1, 7). Additional shorter clcndiites, going iriaiiily to the sixth layer, arise from .the porikaryon. ‘I’hc basal dendritos ttre of vary considcrablc langth. Tlicir total spread may amount to 1 nini. 01: cven more.

Little is to be added to (lajal’s descript.ioii of the last two luycrs. Tn the dcnsc cightli layer wliich is charticterized hy pyramids, short pyramids sending their apical dcndrjtes no fartlior tlitiri the sixth layer have heen ohscr.vcd. After lesion of the corpus ctillosum iiegcnerated cells appcared within the st.riatc area only in this layer, whilc sirriilar cclls werc found in the parastrittte area i n Chc? tlii.rd, fifth and sixth layers.

A description of thc behavior of the spccific dfcrcnts and their mode of eiidiiig withiii t.hc cortex litis h e n furiii.shcd I)?- (.’a jtil ( ’11) tuid Polyttk ( ’38). Tlic fihxs uscciicl through the cortex in ail abliquc, often tortuous course ant1 cnd most.ly within (”ajal’s fourth t i i d fifth layers (cf. Cajd, loc. cit. ’11, fig. 391). Aceording to Polyak, the amount of Narclii granules is smaller in the fourth than in the fifth laycr. S o libcrti npl)ettr to go 1)cyontl this fitraturn, ia (rantrtist to the hchzlvior of tho

Pig. 2 Pliotograpii of a I3odian prep:wation of tlii? human striate :ire&. On tho left, tlic plan o f stratification of IlamBn y Cajnl (KyC)) is indicated in Arabic and t h t of Rrodmunn (KB) in capital Kornan nuiiiornls. On the rigtit, tlic plan of strlztifieutioii given in this paper (Gvl3) is iudieatrd in srut\ll Roinnn numerals.

thalamic radiation in thc “sensory ” cortex (of. Polyak, loc. cit. ’32, figs. 57 to 65). A11 optic radiat.ions end strictly in the stripe of Geiiuari. Tlic experiments of Le Gros Clark and Sundcrlaiid (’39), to cite hut one papcr, have niade it quite clear, however, that this stripe contains also abimdant intra- cortical assoc.iaCiori fibers. Ti1 Rodian preparations the stripe of Gcniiari is seen as a thick ha.iid in tibout the middlc of the cortex, filling Cajal’s fourth aiicl fifth layer (fig. 2).

THE STRIATE AREA OF PH1IvIATF.S 413

Thus the two layers which contain tlie stripe of Geiinari are lioiiiologous to the layers i r a and ivb of the parietal cortex. The homologies of the “outer niaiii layer” follow almost immediately. Layer i is so obvious as to require 110 discnssion. Layer ii coiricides with Cajal’s layer 2 aiid can also be dis- missed without further comment. Cajal’s third layer is again clearly the homologue of Lorente de N6’s layer iii. It is pos- sible, however, to differentiate iii the primate striate area between an upper substratum which is light arid a lower one which shows a greater cell density and which appears to contain an increased number of small cells of Qolgi type 11. This is the layer which l3rodmaiin aiid many others called IVA. It is, however, as we have seen a moment ago, riot homologous to Loreritc de N6’s iva, but belongs without a doubt to iii. We could then subdivide iii into two sublayers iiia aiid iiib. That has been done in niany other parts of the cortex. The reasons for these subdivisions are, however, different in the two cases. I n the striate area, greater cell density prevails in the lower substratum, in other parts of the cortcx the cell density is greater in the higher substratum. Moreover the cells of iiiR in the striate area a rc not in iiitiniatc contact with tlic ontcr stripe of Haillarger 1101’ do they send many dendrites into tliat plexus, while the cells of iiib or iiic in other areas are in fairly close contact with the upper fringe of the stripe of Baillarger and send their basal dendrites definitely into that plexus. We shall digerentiate therefore between an upper iiiA and a lower iiiB, indicating by the use of capital letters that these substrata are not homologous to the subdivisions iiia, iiib arid iiic which can be made elsewhere in the parietal cortex. Cajal’s sixth layer is also clearly homologous to Lorente de N6’s va, while Cajal’s 7 corresponds equally obviously to Lorente de N6’s vb which that author defined as the substratum containing the large pyramids giv- ing rise to projection fibers. It would then follow further that Cajal’s 8 corresponds to Lorente de K6’s vc, while Cajal’s 9 corresponds t o Lorente de N6’s vi. Evidently this layer can- not be further subdivided in the striate area.

414 GEXFIARDT VON BONIN

The scheme given here is represented in the labelling of figures 1 and 2 for co~npai.ison with tlie other schemes. It is then used exclusively foia tlic rest of the figures accoinpany- iiig this paper.

It is not only the striate area itself which exhibits a char- acteristic structure in tlie brain of prirtiates but also the mar- gin of the parastriate area iminediately surrounding the former. A “margo magnoccllularis ” is present in all higher primates arid appears to be just as characteristic of their brains as the striate area proper. There has been much dis- cussioii among students of cortical architecture whether this itiargin is a typical formation sui geiieris or whether it is an inconstant feature, not worthy to be recorded on a forrnal brain map. 11. Vogt ( W ) , Filimonoff (’33) and Reek ( ’34) inclined to the latter, v. Ikonorno arid Koskinas (’25), Solis (’36), and, on differcnl grounds, Pfeifer (’40) inclined to the former alternative. I T e have carefully gone through serial sections of the brains of chimpanzee, macaque and Cebus, and have found a margo riiagriocellularis in all three of them. The number of large cells in tlie parastriate area may differ from section to section so that sometimes there are only a few cells close to the stiiate bomiclary while clscwlicre many cells a re present cvcii quite f a r away from that boundary. v. Econonio called this iiiargiri, as is well known, OB y. He also speaks of F A Y or PA y, symbolizing by the letter y the presence of giant pyraniidal cells in the fifth layer. Hc does not differentiate between large (or giant) pyramids in the fifth layer (which give origin to projection fibers) and between similar cells in tlic third layer which do not give rise to projection fibcrs and which in some cases probably betray the area in whicli they are found as a suppressor area. It appears advisable therefore to introduce a new symbol, g, for areas showing conspicuously large cells in iii, and we propose therefore to write as heretofore F A y and P A y, but to change to PEg, OBg, etc. In Golgi preparations, a few peculiarities can be made out which appear to confirm v. Economo’s conception of “OBg” as a separate entity. The

THE STRIATE AREA O F PRIMATES 415

general plan of stratification is here the same as elsewhere in the parietal cortex. The large cells in iiic (fig. 1, 9), riiariy of which were stained satisfactorily, send off dendrites from tlic basc as well as from the sidc of their perikaryoii which show r2 very dense ramification within iiic arid iva. Their. basal dendrites dip deep into iva, and it is instructive to compare their dciise arid widespread arborizatiori with those of the lowest pyramids in iiiB of the striate area on the oiic, aiid with the large pyramids in vh of the striate area on the other hand. I n the first instance the clendritic roots are poorly developed in every respect, tlic latter have a much wider spread, but much fewer l)ra~ichc~s witliiii a giver1 space. Tlic apical deiidrites of tlicl cells iii iiie of OBg hehave in tlie usual manner, giving off somc raiiii iii the npper par t of the t1iii.d and in the second layer. The RSOIIS of some cells could be followed a certain distance. Tlicy make for the white matter; collaterals were ohservcd to come off within iv arid to take an ascendirid 0 course.

Two types of large pyr;uiiids were seen in the fifth layer. In vb cells a re situated which resemble very much tlie cells of Meynert in the striate area (fig. 1, 10). Their strong basal dendrites show an enormous spread, giving off but few side- branches. Cells of another type (fig. 1, 11) send off some basal dendrites which spread in thc manner just described for the first typc. I n additiori they possess other branches which come off from tlie ul’pcr part of the perikaryon and which ascend towards the fourth layer. These branches are strong and numerons, and could be followed into ivb. Still others ramify within v. The apical dendrite ascends to the molecular layer as usually. Thej- a re the only cells in v which stand, by virtue of their dendiitcs, in direct contact with the outer stripe of Baillargei.. I t should be reiiiembercd, liowevei., that this plexus does not contain specific afierents in the parastriate area, since this area has no tlialarno-cortical cori- riectioris (Walker, ’38).

Within the striate area there is an extremely sharp boundary of the axonal plexus of specific afferents both against the upper

416 GERHSR,I)T VON KONTN

arid the lower layers. Elsewhere, the pyraiiiids in the lower part of iii dip into tliis plexus. In layer iiiB of the striate area tlie cells have beconic so small and tlieir dendrites havc become so poorly developed that they rarely reach into this plexus. The cells within layer iv show a like tendency to avoid trespassing beyond tlic confines of their “own” layer. The large star pyramids, fairly abundant elsewhere, are reduced in number (if Golgi preparations can be trusted) thus decreas- ing the probability that irripulses from the supragranular layer may influence tlie granular layer itself. On the other hand the “supragraiiular” layers (i.e., i to 5;) receive a11

whundan t supply of i l l tiwortical impulses by way of asceiiding NXOIIS froni layer iv, as ell as from T’H and vc. Tlie f o r m ~ r source probably iiiore than makes up for tlie lack of direct iiiflueiices of the thalamic impulses upon the supragranular layers. To realize this shift in relation between incoming messages and tlie cells of layer iii niay be of importance from a functional point of view.

Within OBg the large cells ii: iiic as well as tlie pyramidal cells with ascending dendrites (fig. 1, 11) in vb iiiap both bc more important to “kill” impulses coming within their “basal dendritic field,” to borrow an expression from Bok ( ’36 ) , tliaii to serve as relay stations for efferent impulses. Fo r a cell will only fire if all synapses contained within a given region are activated (within a given short period of time). Some of the intracortical association fibers in the outer stripe of Baillarger undoubtedly t r a w l beyond the striate area into the parastriate margin, ORg. Here, they encounter tlie large pyramids. It is reasonable to assuiiie although riot yet proven that the synaptic fields on these cells arc heterogeneous, in the sense defined bv Lorentc de N6 ( ’38 b). N o further relay of impulses from the stripe of Geiinari could take place with- out “support” froin other sources of excitation. This hypothesis would help to explain the finding recorded by v. Bonin, Crarol and JfcCullocli (’42) that optic impulses led

‘We hnve carefully studied Dodian preparations hut were unable to comr t n definite results ahout the synapses on the pyramidal cells of ORg.

THE STBIATE -4RE-4 OF PlUMATES 417

to no electrical activity in OBg while they could clearly be observed in OC. T n short, OBg may serve to isolate the striate area from tlic rest of the cortex. What effect that would have 011 visual function (or functions) cannot be analyzed in a few sentences.

On the basis of these results it is interesting to pass in review thc cytoarchitecture of soriic primates. F o r this purpose, prcpara tions of a Lemur galago, of Tarhius spectrum, of Cebus, Macaca, llaiigabee (Cercocebus), orang, chimpanzee aiid man were available. To gather this material was only possible through the generosity oi' 1)r. John F. Fnltoii, Dr. !Margaret Kcriiiard, I)r. Ileinricli Kliiver, Dr. TTarren S. Alc('ulloc1i a i d tlie late Doctor Fantus, who sup- plied brains o r even finished series. To all of these, as well a s to Dr. 0. F. Kanipnieier, Head of the 1)epartiiient of Anatomy, who supported the wri tt'r 's endeavors in the most liberal way, the writer wislies to exprcss liis sincerest gratitude.

111 comparing tlie "striate area" of diff'ereiit species, i t is to he i-einerribei*ed that this area is not hnilt identicallr iii all of i ts parts. Beck ('34) has ilio.cr.11 this f o r the niacaqne, aiid stated (but, so fa r a s the writer is a~vai'c, not yet p~ihlishetl in cxtenso) that the humair striate a r m sliowecl similar sub- divisions, and Ngowyang ( '34) actually gave an a ~ a l ? sib of the subclivisions of the huniaii str iate area baied, ho~ve\-er, on only one brain. l ' h c differences found are, of roiirse, 1-8 tlier subtle, a i d tlirlir fnnctional significance is a t the moment far from clear. TTc shall, noi~etliel , hca t' these rcgioiial dif- ferences in mind and take '*ai.c~ as much a s pussihlc to coni- pare onl;v homologous subdivisions.

M-e shall s tar t our survey with the anthropoids. The striate tireti of n i m lias been described so freqnentlv that it appears u~i~iecessi i r~- to go into i ts detailed descr.iption once molx. It is therefore more as a iriatter of record and in order to have a figure for comparison readily available that a pliotoxrapli of the human striate area (fic. 3) is included. Tliis x-as talrcn from the frcw sur fwe of the infwior lip of the calcarine f i s~ui -~ , ie. , of the gyws lingnalis. As the story uiifolds, it nil1 be-

418 GERHARDT voii BONTS

come clear that the following points arc of importance. T l w e is roiy little diffei-encc between ii aiid iiiA, and ncithcr iva nor ivb show a division into subhgcrs. Ngowytmg ( '34) tried to make out two siibla~crs in iva (of our nomenclaturc) but a glance at his photographs will sliow that the difrercmcs arc only very slight. Simila.rly, thc sublapcrs indicated by v. Economo and Koskiiias ('25, loc. cit. p. 647) arc difficult to recognize. It is furthcr to bc Iiotcd that lupcr vh is light, that,

Fig. 3 Photograph of n Sissl preparation of the liuiiian strialo iirct. YOC fiirthcr crplanatiouu sc*c figure 2.

in other words, the large pyrumiiiul ccllv lic above tlict ciciise laycr of vc.

Thc oraiig (fig. 4) shows a structure similar to that of man, pot with some distinctive traits. The external granular laper forms a narrow uiid dcfir1it.c band jiist midcrneath layer i. Thc tliffcrcncc betwcen iiiA and iiil3, on the other h a d , is less obvious in thc anthropoid ape than in man. I;aycr iva i s nari*owci* in the orang but can be much inoro readily sub-

THE ST11TATE AREA OF PJU3lATES 419

divided into two sublaycrs, of which the upper one is lighter than the lower OIIC. The large stellate cells are irregularly distributed iii iva. The filth layer sliows ti slightly greater cell density in the orang. A few large pyraitiids are wit.hin thc lighter layer of vti, but a fairly dense band of large cells is situated in vb which is almost inclist.in~ishahle from the dark band of vc. The striate area as R whole appcars to show a iiioro proiionnced columnization than that of i m 1 1 . B u t that

Figure 4

may be a local diffcreatiation rather than a characteristic of. the species.

The striate area of the chimpanzee (fig. 5) shows little difference between ii ancl iii. La.yer iiiB uppoars to contain a slightly greater number of pyramidal cells tliaii it docs in mail or orang. Layer iva contains rather conspicuous large stellate cells strewn irregularly throughout this layer. A sub- division into iva a and iva /3 is a,s hard to make in this ape as it is in mail. In Rodian preparations, many of the large cells show a stout apical dendrite. Owing to the thinness of the serial sections (10 H) it is rarely possiblc t.o follow this process for any length. A comparison between the hurrrttn and

420 CrEHHAK1)'l' VON WONlS

the cliin~panzcc material distirrct.ly gives the iniprcssion, how- cvei., that star pyramids are relatively IHOPQ frequeiit ill tlic brain of the latter. The stellate cells of thc cliiinpnnzoc! arc distinctly iiiore coiiapiciious in tlie depth of tlic cnlcaritic fissure tliaa on the coiivox surface of the occipital lobc. Wlicther tliore is an actual difforc!iicc in sizo, mid wlicthcr this coiiiciclcs with the territory of the macula zuicl of pcriph- ern1 risioii, wc must lcuvc for future \vork to tlccicle. The

large pyramidal cells of vb arc, just as iii the orang, almost within the dense layer of vc. This layer itself is filled with fairly large cells uiid presents a still coarser appearancc than in the orang.

Among t.he three monkeys on our list we shall describe the niacayuc first (fig. 6). The secoiid laycr rcseinbles that of the orang in that it forms a dense tincl iiarrow hand just underiieath tlic molecular laycr. Thc boundary betwceu ii

THE STRIATE AIIEA OF PRTMATES 421

and iii is iiot precise while t.liat. between ijiA and iiiB can be drawn quite sharply. It is seemingly easy to subdivide iva into two sublayers, a lighter one iva a arid a denser one iva 0. Rodian preparations sliow, homcvor, that the large cells arc restricted to i n a, and it hcconies clcar thorefore that “iva p” should ra.ther be called ivb a, since iva is defined as that layer .which contains lavgc stellar cells. Many of the large star cells shorn? conspicuous and stout apical dciidrites which ofteii can

C’igure 6

be follouwl at least as fur as iiiH. After careful scrutiny of Bodiuii preparations the writer is convinced that many of the large cells in layer ivu are star pyramids o r border pyramids. They are irregularly distributed withiii layer iva, and are frequently found in clusters of three to four or five cells. The fifth layer is light. While most of its cells are small, there are a few medium-sized pyramids, of about half the h e a r dimen- sions of the large solitary pyramids. These large cells are sit.uated well within the dark layer of vc. This shift. in the

422 GERHABDT VOK ROSIN

position of the large solitary pyramids is charactcristic of all loww monkcys.

111 Corcoccbus (fig. 7) stratification is inore complex t.hm in the macaque. This statement does riot uppl~7, however, to the strata abovc the stripe of aennari. There is very little difference between layer ii and iii, and even iiiB does not stand out very clearly. On the basis of Nissl proparations layer j\-a can bc subdividod into three strata. Tlic uppcrmost

Figure 7

of these, iva a, is very thin and fornis a somen-hat lighter band just beneath iiiB. It is bettcr pronounced in soine parts of the striate area of this monkey than in others, and it may well be possible to bave a subdivision of that area iri part at least on the behavior of this sublayer. iva p is darker and contains largc cells, arranged in irregularly spaccd clusters. iva y is light arid about as broad as iva a and iva p together. This substruturn, too, shows some large stellate cells. Since only Nissl preparations of the mangabee were available, it is inipossible to sap whether star and border pyramids are frequent or not. ivb might be subdivided into a lighter ivaa

THE STRIATE AREA OF PRIM.4TRS 433

and a darker ivb 0. The colls in thc former secm to bc slightly larger than in the latter. va is light and harbors only few pyramids of medium size. Most of its cclls arc sma.11. The large solitary pyraniids are situated well within the dark baud of vb + vc. This layer is ill-defined against. the thin mid light six3Lrth layer. The boundary aga.iiist thc wliitc matter is sharp.

Figure 8

Thc striate area of Cebus (fig. 8) has been described by Brodmann ('09 and '12) and later by t8hc prcscnt writcr (v. Bonin, '38a). Its most conspicuous peculiarity is the subdivision of layer iva into three sublapers by a relatively dark band in its middle part. This band is formed by granules as well as by the large stcllutc cells. Even more than in the mangabee, the large cells are rcstricted to ivap, although a few of them are found here and there in iva y. To subdivide ivb into an upper lighter ivba and a lower, darker ivbp is feasible just as in the mangabee. Layer oa is light and con-

424 GEKHAEDT vo.1’ ROSTN

t.airis almost exclusively siiitill calls. vh aiid vc cannot be distinguished. The large pyramidal cells a.re situnt.ed at a slightly higlier level t.11a.n they are in thc niangaboo.

A11 the primates discussed so far show n woll-developed margo magnoccllularis OHg surrounding the striate area.

The visual cortex of Tarsius (fig. 9) has heen described mid figured by Woollard ( ’25) and by Le Gros Clark ( ’25). Neither of them saw aiipthiiig beyond the ordiiiary- primate strat,ifica- tion and Lc Gros Clark concluded from his comparative

studies that the “visual cortex of Tarsius iuclicates a position intermediate betweon that of Tuyaitt on the one huizd, and that of the Aiithropoida on tho other.” Pet a glaiice t.lirough the microscope will show a much iiiore complicated pattern than in ally of the primates coilsidered thus far. Ry merely counting the altei-natcly light and dark layers, 14 strata can be observed. I t is easy to identify the first four layers as i , ii, iiiA and iiiB of our scheme. Layer iva consists of t.hree sub- layers, the first and third of which are light and the second of which is dark. The cells contained in iva are all of about the same size; it is impossible to distinguish any large stellate cells. Layer ivb is also divisible into three sublayers. Two

THE BT11LATE AREA OF PRIMATES 425

dark bands, filled with very small, graiiular cells RI’C separatetl from cach othcr by a light band which contains few and irregularly spaced c.ells of somewhat snialler size thum those found in iva. Layei* v consist.s of a light m d a dark layel.. The former is evidently va, the latter vc. It is impossible to make out large pyramidal cells in Xissl prepartitions sirice all cells appear to be of rather uiiiforiti size. Laycr vi is light in its upper part arid fornis a narrow band consist.ing of one to t.lirec rows of cells at the border bet.wecn cortcx and whit.c matter. To identify the various layers in the nianric1r just outlined may appear as an inpssiblc tusk when oiily Sissl preparations are available. However, a study of the border between the strintc and the parastriate area and of some Rodian preparations forcibly suggest the scheme given here.

The striate area of the lemnrs has frequent.ly been described. 1iot.t ant1 Kclley ( ’08) worked on the braiii of Lemur brunxieus, IJ. iiiongoz and L. catta, Brocimann (’09) gave a drawing of the striate area of Lemur ~~iacaco (loc. cii., fig. 72), and Alouf (’29) described the striate area of Lemur catta. All these species belong to the lemnriformes. The striate area of Lemur macaco belongs unquestioiiably to the “trist.riate” type of Brodniunn, while Leniur catta, in spite of Alouf’s labelling a.ppcars to belong to thc bistriate type (cf. Alouf, loc. cit., plate 6, fig. 2). To accept Alouf’s layer N A , even 011 the hasis of Brodmanri’s scheme, appears well nigh impossible. That layer does not show ~icttrly t.he cell density and the relative frequency of granules that is cxhibited in Alouf’s IVC. Mott and Kelley ’s di-awiiigs caniiot be confidently interpreted.

Galago, a rcpresent.ative of the lorisiformes (fig. 10) which the writer was able to examine shows a still Rimpler pattern. The second and third layers are hardly distinguishable from each other, even iii and iv blcad almost impcrceptibly into each other. The snialler size of the cells and their round appearance provide some indication of iv, but the diagnosis of this layer requires more scrutiny than it does in the case of the higher primates. It is easier to recognize in Bodian

426 C;E:KHARIYl! voh' BOXIS

preparations which show thc position of the stripc of Gcunari. The writer has been unable to identify beyond doubt any lnrgc stellate cells. 'Layer va and b are light. It is easy to recognize the large pyramids of vb in Bodian preparations. They are fairly frequent, and their position within the light band may justify an obscrver to sag that in this one respect at least the Galago is closer to man than are many of the higher primates. vc is almost as broad as va and vb together while vi is extreiiiely narrow. The boundary against the white matter is sharp.

Figure 10

It is custoniary to consider man as the proud and finished product of a11 evolutionary line starting from rather imperfect simple forms and gradually approaching hur~irtn standards by illcreasing diff crentiution. T t is clear almost at oncc, how- ever, that this conception is utterly inapplicable to the matc- rial described in this paper. It needs 110 more than a glance at the photographs to see that the lamination of the striate area is more elaborate iri Tarsius than in thc monkeys, and inorc elaborate in thc monkeys than in apes or man. The visual area of man is comparatively primitive in its pattern of lamination, although its supragranular layers show a better dcvclopment than they do in lower primates. It is true, on the other hand, that the class of primates shows a more elaboratc stratification than the lower mamnials, and this is illustrated in our material by Galago.

THE STRIATE AREA OF PRIMATES 427

It is tempting to correlate morphological with psychological facts. Whcii yielding to this t.emptation, however, we are apt to bog doww in R brain mythology no whit better than thc brand offered by the “schciiie-makers” for tbc explanatioii of aphasia. TTe should rather stay within t.he bounds of morpbology aiid note that differentiation of the striate area increases with the ratio which the size of that area bmrs to the size of the wholc cortex. The largcr tlic rclatire size of t.he striate area tlie greater its cornplcxity. We iiiight, with- out liowevcr gaiiiiiig for thc itiomciit a verifiable hypothesis, think of the various strata as a product. of some fonnative gradient, origimting probably from the st.ripc of Gcnnari, supcrposcd oii ti formative gradient at vvork throughout thc iso-cortex aiicl soinehow rriodifyiiig it. Thc largcr the area through which this gradient ctiii s ~ e e p , the more profound i.fs iiifluciicc.

8[: W M A B Y

Thc first part of this paper dovelops a plan of stratificat.ion of thc striate area, ‘bascd nitiinly 011 thc study of silvcr prcparti- tioiis. It is sliowii that .Lorc!iitc tie M6’s sti*atific!titioii of tlie iso-cortcs is fully upplicablc to t.he striate area, aiid Cajal’s arid (:artlpbell ’s ohservtitions wiid coiicctptioiis are lsrgcly coil- fimictd. !I’hc siriatc area is charactcrized by a teridcncy to separatc the various st rata from each other more coiriplctely than elsewhere in the cortcs. ‘Fhe strwture of tlic inargo rnagnoccllularis is briefly described.

The sccoiid part analyses the striate arcas of niaii, orang, chimpanzcc, macaque, riiaiigabcc, Cebus, Tarsius and (Xalago. Stratification is siinplest in Galago, it is most elaborate in tlic tarsius, the onlp two forms in whicli a margo magiioc.cllularis is not clearly discernible. In descendiiig ordcr follow cebus, Inangahec, macaque, the large apes and man. The complexity of it.s pattcru appears t.o bc proportional to tlie relative size of the striate area a.s compared with tlic size of thc vholc cortex

428 GERHARD’I’ VOK HONIN

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