the cerebral cortex of the cebus monkey

47
THE CEREBRAL CORTEX OF THE CEBUS MONKEY GERRARDT VON BONIN Dcparf me,ut of Anato?iijy, L'nw~rsity nf Illiaols, Chicago ELEYEP: FIGURES (A(ceptcd for publication Janunrr 26, 1938) INTRODUCTIOS In important psyliological investigations, Tcliiver ( '33, '37) was able to sliom that the 'intelligence' of the cebus monkey was of about tlie same l e d as that of anthropoid apes. A female capuchin monkey, P.-T.,l with which he workecl used simple tools such as sticks, boxes, gunnysacks or otlLer suitable objects to bring a coveted piece of banana within her reach, and even solved problems in wliicli the food could bc obtained orily by using txo or more objects as tools. Since the cerebral cortex of tlie cebus monkey liad never beeu described in its entirety, tlie writer gladly availed himself of Doctor Rlurer 's kind offer of serial sections through tlie brain of tliis monkey for a cytoarchitectural study. The brain was removed about 24 hours after tlie death of the animal, x-liich occurred when it was ahout 10 to 11 years old. It was fixed in alcohol, embedded in celloidin and cut at 25 p. Every fiftli section mas stained with thionin, and this series forms tlie hasis of the present report. The aiitlior is deeply indebtecl to Doctor TTliiver for placiiig this series at his disposal. The author is further indebted to Dr. 0. El. Kampmeier, iiot only for placing the facilities of the department of anatomy at his disposal, but still more for increasing tliese facilities in tlie most gcnerous manner, re- stricted budgets notwithstailding. The body weight of P.-W. W:IY, on February 13, 1931. 1.9 kg.: at tllc time of death, April 29, 1934. 1.022 kg. 181

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Page 1: The cerebral cortex of the cebus monkey

THE CEREBRAL CORTEX O F THE CEBUS MONKEY

GERRARDT VON BONIN Dcpar f me,ut of Anato?iijy, L ' n w ~ r s i t y nf Illiaols, Chicago

ELEYEP: FIGURES

(A(ceptcd f o r publication Janunrr 2 6 , 1938)

INTRODUCTIOS

In important psyliological investigations, Tcliiver ( '33, '37) was able to sliom that the 'intelligence' of the cebus monkey was of about tlie same l e d as that of anthropoid apes. A female capuchin monkey, P.-T.,l with which he workecl used simple tools such as sticks, boxes, gunnysacks o r otlLer suitable objects to bring a coveted piece of banana within her reach, and even solved problems in wliicli the food could bc obtained orily by using txo or more objects as tools. Since the cerebral cortex of tlie cebus monkey liad never beeu described in its entirety, tlie writer gladly availed himself of Doctor R lu re r 's kind offer of serial sections through tlie brain of tliis monkey for a cytoarchitectural study.

The brain was removed about 24 hours after tlie death of the animal, x-liich occurred when it was ahout 10 to 11 years old. It was fixed in alcohol, embedded in celloidin and cut at 25 p. Every fiftli section mas stained with thionin, and this series forms tlie hasis of the present report.

The aiitlior is deeply indebtecl to Doctor TTliiver for placiiig this series a t his disposal. The author is further indebted to Dr. 0. El. Kampmeier, iiot only for placing the facilities of the department of anatomy at his disposal, but still more for increasing tliese facilities in tlie most gcnerous manner, re- stricted budgets notwithstailding.

The body weight of P.-W. W:IY, on February 13, 1931. 1.9 kg.: at tllc time of death, April 29, 1934. 1.022 kg.

181

Page 2: The cerebral cortex of the cebus monkey

182 GERIIARDT vox BONIS

Our knowledge of the finer structure of the primate cortex is still imperfect. The best known is probably that of man which has been the subject of intensive studies by Campbell ('05), Elliot Smith ('07 b) , Brodmann ('09, '12)' C. and 0. Vogt ( '19-'20), and v. Economo and Koskinas ( '%), to name but a few. Of these, Elliot Smith examined the fresh cross section through the gray matter with a hand lens, the Vogts used mainly stains for myelin sheaths, the others used partly (Campbell) or exclusively Nissl stain or one of i ts modifica- tions. Regarding the anthropoid apes, we possess studies by Campbell ( '05) based on both mpelo- and cytoarchitectural work, and by Mauss ( '12) based on mycloarchitecture. Beck ( '29) has published myeloarchitectural researches on the superior part of the temporal lobe, and Rreht ('36) has studied the comparative cytoarchitecture of the 'speech cen- ters.' Of the lower Old World monkeys, Schuster's study of papio ( ' lo) and Brodmann's of cercopithecus ( '12) are based on cytoarchitecture, while IIauss ( '08) investigated Weigert preparations of the brain of cercopithecus. Among the New World monkeys, Brodmann's ('09) and Mott, Schuster and Halliburton's work ('09) on hapale should be mentioned. Tarsius has recently been described by Woollard ('25). Of lemurs we have information from Mott and Kelley ( '08) and from Brodmann ( '12) ; about microcebus from Le Gros Clark ( '31). Of subprimates which may conceivably present ances- tral stages of man, we may cite the works of Le Gros Clark on tupaia ( '24) and on macroscelides ( '28)' of Rose ( '29 b) on the mouse and of Gray ('24) on the opossum. The gradual increase of complexity as one goes from a lowly mammal to man can be seen at a glance at the brain maps. How cebus fits into the picture which can be constructed from the data just enumerated, we shall discuss later. It should be borne in mind, at any rate, that the genus cebus belongs to the platyr- rhines. These branched off from the catarrhines probably early in tertiary times. The resemblance in the macroscopic configuration of their brains is all the more remarkable. Phylo- genetically speaking, the brain appears to be an exceptionally sluggish organ.

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CORTEX O F CEBTJS 183

Description The gross appearance of P.-Y.'s brain is shown in figures

1 to 3. These are drawings made after plottings from the serial sections.

Even the simplest description cannot altogether avoid tak- ing sides iii questions of comparative anatomy, for most sulci have been given different names by different authors and most of these names were, moreover, chosen with a distinct answer to problems of homology in mind. A synopsis of the various terms used for the snlci and p r i of the pithecus brain which is similar to that of cebus has recently been given by Mcttler ( '33).

A number of figures of cebus brains are to he found in the literature. We givc a list of those which we have been able to use:

Author Species

Anthony, R. ( '28) 3P.

Ariens Kappers, C. U. ( '21) hypoleuens f atuellus

Brodmann, K. ( ' 12 ) sp. Connolly, C. J. ('36) hypoleucus Cunningham, D. J. (1x92) albifrons

capucinus Flatau. R. and capucinus

dacohsohn, I,. (1899 j

Jakob, Chr. ('11) SP. Kukenthal, W. and monachus

Ziehen, Th. (1895) nlbifrons Pansch, A. (1868) cirrhifer Retzius, G. ( '06)

hypoleucus fatuellus

Zuckerkandl, E. ( '04) capucinus

V i e u' 1

1, occ. 1 1

4 m 1, m 1 v v 1 m 1, m, occ. 1 1, ow.

1, m, F

m, occ.

Pnge or plate p. 255 p. 1157 p. 1157 p. 192 p. 308 p. 280 p. 223 p. 222 p. 90 p. 94 pl. 42 p. 23 p. 24

PI. 7 Both from all sides,

pl. I11 and IV. Details on pl. LVII

and LIX p. 422

1 = lateral; o = orbital; m = medial; v = ventral; o w . = occipital view.

The general morphology of the cebus brain is thus well known, and it will be seen that P.-P.'s brain shows no startling devia- t,ions from this pattern.

Page 4: The cerebral cortex of the cebus monkey

The sylviari complex-we follow Anthony ( ’28) in the choice of this term-joins the occipital end of the superior temporal sulcas which continuw but a short way bepond this point in an occipito-dorsal direction. If Elliot Smith’s ( ’03) tlieory of the opercularization of tlic central territory is correct, this would represent tlie primitive condition, and from the pnh- lisliecl figures it appears to he present in most cebus brains.

a,, a,, snlc.us arcnntus (al, 11 of Xettler, liorizontal limb of inferior yreeen- t ra l ; a?, pc of Mettlrr)

a s , Affenspalte (sulcns lunatus) c, fissura calearina em, sulcus calloso-mnrgiiinlis co , fissurn collateralis cr, sulcus ccntralis Rolandi i, sulcus interparietalis o, sulcus orbitalis oi, sulcus oecipitalis inferior os, sulcus occipitalis superior ot, sulcus oceipito-tcruporalis

p, ‘principalis ’ (AriCiis Kappersj : 1’0s- tralis (Anthony, Flatau and Jacob- solin) : inferior frontalis (Mettler) ; rectuv (Eberstaller, Zuckerkandl, Smith, aiid Retzius j

I W , fissura parieto-occipitnlis r, sulcus rostralis s, ‘sglvian complex’ (Anthony) sp, sulcus subparietalis t , suleus teinporalis superior tin, sulcus temporalis iiiedius Y, snmll occipital furrow (coinpare

Kiikentlinl and Ziehen)

Fig. 1 Latcral view of left cerebral Iieiiiisplicqx of P.-Y. (Broken line indi- cates projection of contour of rentricle: s l i add arra, projection of insula).

Page 5: The cerebral cortex of the cebus monkey

CORTEX O F CEBUS 185

Only Kiikenlhal and Ziehen (1895) sliow the two furrows as remaining separate. Coiinolly ( '36) meiitioils a submerged sulcus at this place. Tlie extent of the irisula has beeii indi- cated on figure 1. Tlie irisula itself is entirely smooth, no trace of the pseudusylvin of non-primates caii be found. From Retzius' ('06) plates 59 and 60-the only- good figures of the insula of primates-it map be gathered that this is tlie rule for cebus. (The furi-ow shomii in figure 3 on plate 60 looks more like the groove fo r a blood vessel.) Cuiiningliam (1892)

Fig. 2 Medial vie\+ of I r f t eercbral hemisphere of P:Y. (Shaded area, eoipus callosunl).

found the irisula of Cebus smooth in two, \\-it11 one furrow in two, and with two furrows in one case.

The frontal lobe is bounded occipitad by tlie central sulcus, that characteris tic landmark of tlie primate hraiii. There are two sulei on the lateral side of the frontal lobe: one consists of two branches (a, and a2), wliich come together posteriorly in an acute angle forming a figure resembling the letter T. We shall call this the arcuate sulcus and shall distinguish between its upper branch a, and its lower branch a,. Its phylogenetic development has been described by AriGiis Rap- pers, Huber and Crosby ( '36, pp. 1531-1542). According to

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186 tiEIIHARDT vON B O X I N

the same authors, the horizontal limb, a t (fig. l), is homolo- gous to the midfrontal fissure (sulcus?) described on endo- cranial casts as no. 7 by AriGns Kappers ('29, '33). The other limb, a2, is generally believed to be homologous to the inferior precentral sulcus. Within the two limbs of the arcu- ate sulcus we find a sulcus ( p ) which runs straight toward the frontal pole and which we propose to call, followiiig again Ariijns Kappers, the principalis. Few sulci have given rise to greater confusion than this innocent and simple looking structure. It has been labelled 'sulcus rostralis' by Flatau and Jacobsohn (1899) as well as by Anthony ( '28) who evi- dently overlooked the fact that Kiikenthal and Ziehen (1895) had already given this name to a short sulcus on the medial side of the hemisphere. Ebcrstaller (1890) has called it 'sulcus rectus, ' and several authors have followed him. Mett- ler ('33) follows Cunningham (1892) in calling this sulcus 'inferior frontal,' thus putting a definite and by no means unanimously accepted interpretation on it. That the princi- palis is homologous to Wernicke 's (1876) fronto-marginal sulcus has-we think, rightly-been claimed both by Briijns Kappers, IIuber and Crosby ( '36) and by Connolly ( '36). M7e entirely agree with hiettler that Wernicke himself did not think so.

In the parietal region a curved sulcus (i) is the only land- mark. With Cunningham (1892) and Elliot Smith ( '03) we shall call i t the interparietal in its whole length. It is gen- erally assumed that its anterior and inferior par t is homolo- gous to the inferior postcentral of higher primates, while its posterior part develops into the interparietal sulcus s.str. of the human brain. The interparietal sulcus touches the occipito-parietal fissure (po) and then swings ventrad again to merge with the sulcus lunatus (as). It is impossible to reconstruct with precision the behavior of the caudal end of the interparietal sulcus. According to Ingalls ('14) it gener- ally becomes submerged under the occipital operculum of the

This is a misnomer. It should be intraparietal. The suleus is not between two parietal lobes, but within the parietal lobe.

Page 7: The cerebral cortex of the cebus monkey

CORTEX O F CEBUS 187

lunate sulcus. This latter, mentioned by Ingalls as being particularly variable i r k cebus, extends over the dorsal half of the surface of the occipital lobe. The occipital operculum, of which it forms the outward sign, is not very large in P.-Y.; the bottom of the ‘fossa simiarum’ is only about 1 mm. occipi- tad of the sulcus lunatus. The smaller sulci on the convexity of the occipital lobe arc hardly of great importance, and we can carry over at once the description to the medial side where we shall go back from the occipital to the frontal pole.

The calcarine fissure (fig. 2, c) runs from a point very close to the splenium corporis callosi (less than 0.5 mm.) toward the occipital pole and forks near it into two branches, one of them going dorsofrontal, the other one ven trooccipital. Shortly before this branching there is another short sulcus (co) joining the calcarina from the ventral side. Zucker- kandl’s study (’04) has made i t clear that this is a short col- lateral fissure. Regarding cebus, lie found (’06) this coni- munication of the collateral and calcarine fissure present in nine out of ten hemisphercs which he could examine. Ventral to this and running well forward toward the temporal pole, the occipito-temporal sulcus (ot) is prominent. Going back to the territory dorsal of the calcarine fissure, the parieto- occipital fissure runs parallel to the superior branch of the calcarine, stopping well before joining it. In the parietal and froiital region there is, apart from a n inconspicuous suh- parietal suIcus, oiily the long calloso-marginal sulcus (em) d i i c h appears to run a sti*aight course ell beyond the genu corporis callosi. Near the pole, however, there is a short rostra1 sulcus ( r ) . This term leads to no misunderstanding here. The configuration of the orbital sulcus (0) is shown in figure 3. A single sulcus near the frontal pole, it branches as one goes occipitad, the lateral branch continuing in a sagittal direction, the medial branch curving over toward the medial side, i.e., toward the root of the olfactory tract. Figure 1 gives also the contours of the ventricle. No comparative studies of the ventricles have come to the writer’s attention, hut the human ventricles are well known. We may compare

Page 8: The cerebral cortex of the cebus monkey

188 GERHAKUT l o x BONIK

the length of the posterior and of the infwior horn with that of man by means of the measurements devised by Torkildsen ( ’34). Taking (loc. cit., fig. 7 ) liis measurements D, A and F from encephalograms, we obtaiii in P.-P.’s hraiii for the in- dices 100 F n : 24.0 a id 100 A D: 33.6. Both these ralues are within the range of Torkildseii’s figures w-liic.Ii work out

be forgotten that P.-Y. was eonsitlcrably emaciated when slie died, that hey ventricles were tlierefoi*e pi*obably rnlargccl.

f o r 100 A/D: 2 ~ ~ x 1 , for 100 F /r) : 00-24.7. It Si1ouici ]lot

Fig. 3 Orbital surface of frontal lotre of l’.-Y7. lieducr F3.

Some peculiarities of the cortex of Cebus are kiiowii from iiicicleiital remarks. Brodmaiiii ( ’05, ’09, ’ la) and ?Ilaper (’12) studied sections through 1-arious areas of the cebus hraiii, and it is also mentioned by v w i t’Hoog (’18) and by Bucy ( ’35). llapw’s studies s h o ~ ~ ~ e d that the cortex of cebus was very rich in cells. Brodmaiiii pointed out that oiily in cebus the large stellate cells in layer ivK of the striate area form a darker band in the middle of this layer, thus making it possible to subdivide this sub-layer once more into three sub-sub-layers. I n 1912 the same author published photo- graphs of the cehns brain showing the extent of the striate as well as of the motor arid premotor area. The last two areas have also been figured by Bucy ( ’35). Van t’Hoog’s paper

Page 9: The cerebral cortex of the cebus monkey

CORTEX OF CEBUS 189

contains data on the thickness of the cortical layers in the postcentral region.

As far as cortical areas are concerned it bas probably been felt that the close macroscopic rcsemblaiiec of the ccbus and cereopitliccus brain was iiiclicative of a similarly close archi- tectural resemblance.

PlearlJ- the present study is by no means filial; it concerns itself onl? with cytoarchitecture and it is based o n one hraiii onlr.

It will be our first task to describe tlic areas we have been able to cliflerentiate as objectively arid as briefly as possible. To be 'as objective as possible' implies to stay away from any nomenclat~ii*e derived from the human brain. F o r in so doing, judgment would be passed on questions of homology easily barriiig tlic way to more thorough morpliological investiga- tions. One can, of course, err oil the other side as well and liouiid a perfectly sound principle to death. The homologies of areas such as the area striata (OC, 171, thc area liinbica anterior ( T A , 24), the area 1-etrospleiiialis (LE, 29) and sev- eral others are beyond doubt, and there is no justification to invent cumbersome new names f o r them. Since both letters ancl numbers arc piwluclcd, the nomenclature will he clumsy enough as it is, and the writer lias no intention to irritate his waders more than lie call help.

111 order to he as brief as possilnle, some of tlic data, naniel>- those 011 re la t iw cell numbers and those on relative tliiclriiess of layers hare been collectecl in tables 1 and 2 (pp. 190 and 101). The '1-elatiw cell ~~urnbe r s ' of table 1 give the number of nerve cells in a cube of 100 p length of edge. These numbers are i*oughly eoniparable to those giwn b ~ - v. Economo ancl TCos- kinas ('a;), who write '0.1 mm."' but explain in the text that they mean (0.1 mm.)';. T h y are, liowc'ver, not comparable to those given by Mayer who couiited not only ncrvc cells, but all cells. This is a perfectly legitimate procedure in itself, hut since a choice had to be made, it was thought that the mow complete data of v. Economo and Koskinas woultl be of greater value. The relative cell number was determined by means of

TIC6 J O Z ' R S h l . OF C O \ I P A X A T I Y E N H r R O I . O G Y , \01.. 6 3 , KO. 2

Page 10: The cerebral cortex of the cebus monkey

190 GERHhHDT VOK EONIS

an ocular net micrometer, used in coiijuiictioii with a Leitz objective 6 arid ocular 6 X. For each determination ten counts were made. In two instances, the lowest a id tlie liighest count, the standard deviation and the staiiclard error of tliesc counts were computed. The standard errors of the fignrcs appearing in tlic table are roughly equal to 10. It i s well to

TABLE 1

Cebzrs ~ f l l l t b e v of cells per ( IOU $ ) 3 , for Ul"L'(l.9 urtcl layers

precentr. gig. p: r. precentr. simp]. front.-operc. front. gran. post. front. gran. ant. front.-orbitalis insul. ant. insul. post. post. eentr. gig. yyr. post. centr. gran. post. centr. simp]. interparietalis pariet. post. pariet. front. striata parastriata peristria ta temp. sup. temp. inf, temp. gran. temp. magno cell. limb. ant. limb. post. Average (limbic

areas excepted)

z i I t i A B

257 107 64 168 68 68 199 136 149 7.5 193 9.5 157 86 112 80 204 126 234 111 7 3 322 169 239 105 264 107 183 92 254 108 454 229 314 189 257 12 3- ,039 124 183 106 271 104 258 138

62 152 89

333.8 119.0

C

09 1 3 99

73 74 72 7 8 34

104 7 ,i

8X 88

145 97 75 87

114 84

64

92.4

-- <)I)

9n

321

i U

118 109 102 173 8 1

165 121 148 18,i 306 170 149 14-5 318 301 267 138 "02 214 162

J 38

172.7

78

V

.i 7 36 71 63 77

107 Tr 3 60 .i 8 92 89 96 68 78

231 163 101 74 98 84 82

74

88.5

T i

.17 29 99 72

119 9 1 3 3 68 94 99 95 98 9 9 92

13 166 98 97 78 8.7 6.7 80 7"

90.6

For computations, irA has been taken with iiiC, and iyB and i rC habe both been taken for iv.

NOTE: Standard error for precentr. gig.-pyr., iiiC : 8.7, for area striata, ii = 13.2. For purposes of comparison the standard error of a determination may roughly be takcn to be = 10.0, the standard error of a difference as = 14.1. A difference may therefore tie considered significant if larger than about 40.0. The error of a mean is about 10/\/"1 = 2.18. A difference of the means i s significant if larger than about 7.

Page 11: The cerebral cortex of the cebus monkey

CORTEX O F CEBUS 191

keep this in mind when comparing dif'ferent counts. The thickness of the layers given in table 2 mas measured on pliotogi*aphs. Since riot all areas were cut pcrpendicularly to tlie pial surface, only the relative numbers are given, assum- ing the total thickness to be 1. It would undoubtedly have beeii desirable to have data on tlie surface or the volume of the various cortical fields. But owing to tlie fluent nature of

TABLE 2

AcPrage ?elatice /l&.A"ners of 1ngc.r~ t i t Cebits

Area p e e . giganto-p! rani. preeentr. sinipl. front.-opere. front. gran. post. front. gran. ant. orbitalis insul. ant. insul. post. posteentralis gig.-pyr. posteentralis gran. par. ant. simp]. par. post. par. front. striata parastriata perifitriata temp. sup. temp. inf . temp. gran. temp. magnocell. interparietalis limb. ant. limb. post.

Average

1

0.07 0.06 0.06 0.06 0.10 0.06 0.16 0.12 0.04 0.01 0.05 0.06 0.11 0.06 0.0.5 0.07 0.07

0.08 0.08 0.08 0.12 0.07 0.07

om

t i iii

0.08 (1.50 0.07 0.41 0.09 0.3.5 0.06 0.30 0.08 0.40 0.08 0.39 0.10 0.32 0.0s 0.36 0.06 0.38 0.04 0.35 0.08 0.29 0.06 0.36 0.09 0.39 0.05 0.13 0.08 0.27 0.08 0.35 0.06 0.33 0.06 0.31 0.05 0.39 0.07 0.37 0.07 0.22

0.38 0.0x 0.31 0.07 0.3.5

iv

0.00 0.00 0.11 0.06 0.09 0.11 0.12 0.13 0.16 0.13 0.10 0.11 0.12 0.47 ' 0.18 0.12 0.16 0.11 0.10 0.11 0.13

U

0.21 0.33 0.1 H 0.29 0.18 0.17 0.13 0.17 0.15 0.24 0.25 0.22 0.15 0.14 0.22 0.22 0.21 0.26 0.20 0.23 0.43

0.23 0.10 0.28 0.12 0.22

v i

0.14 0.12 0.21 0.22 0.15 0.19 0.17 0.14 0.21 0.20 0.23 0.19 0.14 0.15 0.20 0.16 0.17 0.20 0.1 8 0.14 0.17 0.25 0.16 0.17

*irA4 = 0.10; iTB - 0.18; iyC = 0.19.

many of the changes from field to field, tliese measurements cannot attain a high degree of precision.

Turning now to tlie description of the iiidividual fields, wc sliall start with the precentral or motor area. This area agranularis gigantopyramidalis (fig. 4) can easily be recog- nized by the absence of an inner granular layer arid by the presence of Betz' giant pyramidal cells in the ganglionic layer. THFl .TOlTRN*I. O F COXfPARATI\E NFrROT.O(?Y \OL 69, N O 2

Page 12: The cerebral cortex of the cebus monkey

The outer granular layer coiltailis some granules, lout mostly small pyramidal cells, forming a fairly even band, rich in cells, and dernarcatecl clearly from the pyramidal layer. This third layer is much poorer in cells. Most cclls are of the pyramidal type; as one goes deeper they increase iii size to 40 hp 25 p.

Figlire 4

The boundary against the ganglionic layer can be estahlislied fairly well : there are some granules present, although not enough to form a distiiict inner granular layer. The pprami- dal cells in vA are slightly smaller than i n iiiC’. But as one goes further down in v they become larger again. The lower part of v contains the giant pyramidal cells. They are fairly fa r apart , generally single, but occasioiially in nests of three

Page 13: The cerebral cortex of the cebus monkey

CORTEX O F CEBCS 193

or four. ‘l’hey are all at about the same depth (iniilamellar 8irrangemenl of Brodmann), but they are far from forming a continuous lamella. Jlost of them have three to four, some as many as seven, satellite cells. The sixth layer finally con- sists mostly of small spindle cells; its border toward the medulla is indistinct. Throughout this area the ai*rangement of the cells is rather helter-skelter; there are no columns of cells to he discerned.

Frontal to the gigailto-pyramidal area, the cortex shows w r y much tlie same cytoarchitecture, except that the giant pyramidal cells a re missing. This part, the area frontalis agranularis simplex (fig. 4) is still characterized by a com- plete absence of any columnar arrangement of its cells. The second la:-er is distinctly lighter than in tlie giganto-pyramidal area; it also contains more granular cells. Layers iii and 1- have perhaps blended more completely into one layer than in the giganto-pyramidal region, arid the bouiidar>- toward the sixth layer is again indistinct.

These two fields together may be called the agranular pre- central or yrerolaiidic area. Their posterior boundary is given by the central snlcus of Rolando, excepting, however, its most dorsal portion. Here, the central sulcus bends dis- tinctly backwurd, but the boundary line of the prerolandic area runs straight on and is therefore found i n front of the centi*al sulcus. Ventrad the prcrolaiidic area does not extend beyoricl the lower end of the central sulcus, hence it does not cover the operc*ulum of the island of Reil. The frontal boun. bary runs from the lower end of tlie central sulcus almost straight to a point on the superior margin a little frontad of the halfway mark between the central sulcus arid the frontal pole. Thus on the lateral side the prerolaiidic area is tri- angular. On the medial side it extends as fa r as the sulcus calloso-marginalis. The giganto-pyramidal formation takes up ahout the occipital half of this space, and the simple ayi-anular formation the frontal half (fig. 10).

The anterior part of the frontal lobe is covered by a dis- tinctly gi*anular cortex, arid this whole area may therefore

Page 14: The cerebral cortex of the cebus monkey

194 GEHHARDT VON BONIN

he called the area frontalis granularis (fig. 4). This area map further be subdivided into three parts : an area frontalis granularis posterior on the convexity, an area orbitalis on the posterior part of the orbital surface, and an area frontalis polaris 01- granularis anterior covcring the frontal pole like a cap. All these areas hare much in common. Throughout, the external granular layer is thin and dense, containing mostly noit-pyramidal cells, some of them showing a cork- screw-shaped process toward tlie upper layer (v. Economo’s ‘ f(orkzieherzel1eii’). The pyramidal layer contains mostly rather broad pyramidal cells of medium size. OnIy now and then a conspicuously slender cell can be seen, a little more frequently in tlie fronto-polar part. The inner granular layer. increases in thickness toward the frontal pole, but shows the same cell density throughout. The ganglionic layer is par- ticularly prominent and contains particularly large cells, mostly of pyramidal shape, in thc orbital area. The fusiform layer contains comparatively small cells ; its boundary against the medulla is sharp.

Ventrad to the precentral formation, i.e., on the posterior part of the operculum of thc insula, there is the area parieto- frontalis (fig. 5 ) . I t is thinner than the agranular precentral area but in it the cells of iii and 1- are arranged in fairly clear columns. Both granular layers contain mostly granule cells. The pyramidal layer shows, particularly in its lower strata, large pyramidal cells. The ganglionic layer s l iom agaiit fairly large cells and is rich in cells at the same time. The boundary against the mcdulla is sharp. This a i ~ a bears at least as much resemblance to the parietal as to the frontal cortex, hencc tlie clioice of its name.

There is an interesting field, just in front of it, the area frontalis opercularis (fig. 5 ) . It sliows agairl a curious blend, this time of the parieto-frontal and the precentral type. The inner granular layer thiiis out, the boundary between ii and iii becomes less distinct (there are fewer cells in ii but mo1-e in iii than in the fronto-parietal area) ailcl the large pyrami- dal cells both in iii a i d v are larger tlian in tlie frol1to-parietal

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CORTEX OF CEBYS 195

part. All these symptoms exhibit some tenclcncy toward an agranular type. On the other hand, there prevails a columnar arrangement of the cells from vi to about the miclclle of iii which is distinctly more parietal than frontal. It reminds one forcibly of the structure found in Broca’s area of the human brain (F(’Bm, 44).

Figure 5

The structure of the parietal lobe is comparatire1)- simple : the interparietal sulcus delimits two large areas, the area parietalis anterior dorsad, and the area parietalis posterior ventrad to it. Just occipitad to the area frontalis agr-arm- l a rk giganto-pyramidalis is the area postcentralis giganto- pyramidalis (fig. 5 ) . I t is a narrow strip, to a large part

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196 GBRHARDT VON BOSIN

1iicldc.n in the depth of the central sulcus, but a t the surface near the dorsal margin of the hemisphere. This area show* a crowded outer granular lager containing some pyamidal cells. Tlie pyramidal layer can be subdivided into three strata (just as in tlie agranular frontal areas) containing pyramidal cells of increasing size as one goes deeper. The fourth laver contains mostlx granules, but some larger pyramids ;ire fonncl here and there. I n the ganglionic layer which in fact is an inner pyramidal layer in this field, there are giant cells of Betz, arranged much in the same way as ill the precentral field. The fusiform layer is sharply marked off against the medulla.

Caudal to this field lies the area postcc'nli*alis granulosa (fig. 5). Here almost all cells throughout tlie cortex are very small, of the granular type. Rome pyramiclal cells, Iiowevei~, are present both in tlie iii aiicl v layer.

Occipital to this area we find the area postcentralis inter- media (fig. 5). Here the second layer is relatively thin aid poor iii cells. The third, as well as the fifth layer, is peculiarly light. The third layer contains mostly smaller cells, and rather slender pyramidal cells are seen here and there. The fourth layer is massive, both broad and deiisc. The fifth layer contains larger cells than the pyramidal layer, mostly of stellate shape. The cells of the multiform layer are agaiii smaller. The boundary toward the medulla is shncp. Througli- out, tlie cells are arranged in good columnar order.

The cortex dorsal to the horizontal part of tlie interparictal SIIICUS, tlie area parietalis anterior simplex (fig. i), diff ers but slightly from the area postcentralis intermedia. Here, too, the cells are arranged in regular columns, extending from iiiA to vB arid showing well-developed pyramidal cells both in iii and in v, a broad inner granular layer and a sharp boundary toward the medulla.

There is a peculiar formation at the dorsal border of thc interparietal sulcus (fig. 6) . Jus t at the lip of the sulcus the ganglionic layer shows a large iiumber of rather large pyrami- dal cells, of about the same size as those in the limbus magmo- c e h l a r i s parastriatus wliich we shall describe presentl?. This

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CORTEX O F CEUI'S 19'7

formation in the dorsal lip of the interpayietal sulcus can be followed a11 along the anterior part of tliis sulcus, up to the parieto-occipital fissure. It thus forms a magiiocellular rirn around the greatest part of the area parietalis simples. TTe shall discuss the importancc of tliis formation later on; pro- visionally we shall refer to it by tlie name given to R similar formation in the liuman brain by Elliot Smith as the visno- sensory band.

The area parietalis posterior (fig. 7) could well be used as a paradigma of the cerebral corlex. All the layers stand out clearly, iiorie appear uiiduly overdeveloped arid tlie cells are arranged not only in a good horizontal, but in H good vertical, i.e., columnar, order as well. The external granular layer is thin arid contains maiiily granular cells. I t is possible to chicle the pyramidal layer into two strata, the lower one of which contains re ry large pyramiclal cells. The inner granu- lar layer is thiiincr tliaii in the anterior parietal region. The colnmiiar arrangement of the cells, distinct in iii, is still noticeable, al t hougli less cl ear-cu t. It disappea 1's compl e t cly in v which coiltailis comparatively few cells of medium size,

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7 98 OERHARDT vox H O S T S

mostly of pyramidal shape. The multiform layer. coiltairls smaller, irregularly scattered cells, and is sIiarp1)- separated from the medulla.

The cortical architecture of the occipital lobe is the same as that of most other primates. The area striata (fig. 7) to which we turn first, clisregarding for. the moment the topo- graphical principle which we have follo\~-ecl so far, sliows the characteristic increase in the number of layers which has been described so often.

Figure i

We will not go into the question of the homology of thesc various layers ; mwelj- for descriptive purposes we have ad- hered in our tablcs to the usual classification iii layer ivA, ivE and ivC, fully aware that ivA contains pyramidal cells aiid is on a level with iiiC in the parastriate area. This has already been pointed out by v. Ecoiiomo and Roskinas. Lorente de N6 has recently ( ' 3 5 ) sliois-n this even more c1earl;v in his excellent Qolgi preparations. For computations we

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COBTEX OF CEBUS 199

have often adopted a different interpretation-including ivA with layer iii. This has been explained on each occasion. In layer ivB giant stellate cells are fairly frequent. In a short survey about 588 per square millimeter cortical surface were found, as against 400 to 600 in man, according to I-. Economo and Roskinas. The giant pyramidal cells of Jleyncrt arc not situated in the ganglionic but in the upperlllost part of the fusiform laver. The same behavior was noted by Schuster (’10) in Papio. The striate area covers the occipital pole like a cap, reaching distinctly farther frontad on the dorsal than on tlie ventral side, and it extends on the medial side along the bottom of the calcarine fissure almost as far as tlie splen- ium corporis callosi (fig. 10). A cross section through the main stem of the fissure shows that the striate area extends much higher on the dorsal than on the ventral lip. However, it appears on the outer surface ventrally at a point a few millimeters anterior to the bifurcation of the calcarine, dor- sally only occipital to that point. Thus, only the superior brancdi forms for about half its length a limiting sulcus to the calcarine area. The lower hranch as well as the stem of the calcaririe are both ‘axial sulci.’ The boundaries of the striate area can be seen from the brain map. That these boundaries are precisely defined need hardly be mentioned. On the lateral side it is well removed from the lunate sulcus or ‘Affenspalte.’ The whole surface of tlic striate area of the left hemisphere is 534 mm.? It is thus about 11% of the surface of the whole hemisphere ( 4 i O O mm.2, see p. 205), a figure which is probably only insignificantly different from 10th given by Filimonoff ( ’ 3 2 ) for cercopithecus.

I t is difficult to delimit precisely the para- arid the peri- striate area. The striato-parastriate boundary is as sharp as in any brain. The limbus parastriatus magno-cellularis (fig. 7) nest to tlie striate area is well marked. The cell counts given in table 1 are taken from that area. As compared with the striate area, the parastriate area contains less cells per unit volume in tlie outer granular, the pyramidal layer, the inner granular (depending on the ‘homology’ of the structure in the striate and parastriatc area) and the ganglionic layer.

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200 GERHBRDT VON E O S I N

The fusiform layer, on tlie other hand, contains practically the same number of cells in both areas. The large pyramidal cells in layer iiiC” are coiispicuous. T h e average of their nuclear volume, determined 011 the basis of only a few meas- iirements, is 638 p3, i.e., about half illat of the giaiit pyramidal ccblls of the precentral area.

Beyond the limbus the cortex assumes very gradually that beautiful columnar appearance with a light gailglioriic layer,

Figure 8

which is typical of the peristriatc area (fig. 7 ) . This in its turn blends almost imperceptibly into the posterior parietal and into the temporal formation.

In the terriporal lobe we shall start from its pole, then de- scribe its lateral and finally its dorsal side. Near the temporal pole the inner granular layer is somewhat attenuated, thus rendering the cortex ‘dysgranular. ’ But this formation is only found in a small area on the lateral side. It soon shades into the true temporal type (fig. S), and is found witli but

Page 21: The cerebral cortex of the cebus monkey

miiioi. differences on both superior and inferior temporal g;pr~. It is a very orderly looking type. The layers stand out clearly, and the cells a re arranged in regularly spaced columns (v. Economo’s ‘Orgelpfeifenformation’). The second Iaye1’ contains almost exclusively granular cells. In the third l a y x two substrata can be distinguished, the lower containing, as would be expected, larger cells than the upper one. The fourth layer is fairly prominent; it is broken up into column^ in accord with the general pattern of this part of the cortex. The ganglionic layer contains large well-formed cells, man:, of them of pyramidal shape. The cells in the sixth la>-ei* appear a little smaller than those in the ganglionic layer. The medullary boundary is sharp.

There are minor differences between the superior and the inferior temporal gyre. In the first place, iririer and outer principal layers are about equally thick in the superior tem- poral area, while in the inferior area the inner layer is dis- tinctly broader than the outer one. The conversion of the cells into pyramidal shape has gone further in the inferior area. Even in the outer granular layer there arc more small pyramidal cells than in many other parts of the cortex.

Both in iiiC and in v there are mell-formed, large pyranii- clal cells. For the volume of their nuclei we find on the basis of ten to fiftccri individual determinations for each mean tlic following figures :

Tn the superior : Inferior temporal mc.1 : iiiC 397.2 p’ 379.2 p*

V 293.1 p7 40.5.1 p 3

There is no significant difference between any of these fig- ures if duc regard is paid to the standard errors of their diameters (which have hcre been omitted). The cell density varies significantly only for the two granular layers. Tlic outer one contains more cells in the superior, the inner one in the inferior temporal area. On the ~ l d e the differences between the two areas are slight, pet they seemed sufficient to warrant the differentiation into distinct areas which lias here been adopted.

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202 GEKI-IARDT YON B O X I N

The boundaries of the area temporalis superior a re clear dorsally arid ventrally; they are given by the lower margin of the sylvian complex and by the depth of the superior tem- poral sulcus. Frontacl it extends about as far as the superior temporal sulcus, occipitad its boundary is indistinct.

The area temporalis inferior is bounded dorsally by the superior temporal sulcus, rentrally, or better, medially by the entorhirial area. The frontal bordcr lies in the prolongation of that of the superior temporal area, the posterior border is again indistinct. The temporal formations blend here ~vith the peristriate and the posterior parietal area, both of which they resemble fairly closelj-.

The dorsal surfacc of the temporal lobe is, as far as can be made out from the reconstruction, entirely smooth and not very broad. On it the cortex shows a varying architecture. Xear the temporal pole the cortex does not differ from thal 011 the lateral side, but as one goes further occipitad, beyond the region of thc insnla, the cortex becomes increasingly granular without, howerer, completely losing its pyramidal cells (fig. 8) . The inner granular layer is riot much broader. here than in other parts of tlie temporal cortex. The process of becoming granular rather affects the deeper strata of the pyramidal layer where the cells a re small, although mostly still of pyramidal shape. In the innw granular layer there are interspersed vcry large (pyramidal ? ) cells. These cbanges have not affected a larger area to tlie same extent, they are found in spots affecting sometimes only a few cell columns. On its lateral side this granular cortex is lined by a narrow strip, occupying not much more than the curvature from the dorsal to the lateral surface, wliicli shows conspicuously large cells in iii(' with a nuclear volume of about 463 p3. These are the area temporalis granulosa and the area temporalis magno- cellularis (fig. 8) .

Adjacent to the corpus callosum on the medial side of the hemisphere there are three areas which stand out sufficiently clearly. The frontal part of thc gyrus limhicus is covered 13:-

the area 1imbic.a trntc~i~ior. Tlic complete absence of tlic inner

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CORTEX O F CEBUS 203

granular layer renders easy tlie recognition of this formation, described for other species by Rose ( ’ 3 5 ) as ‘cortex quinyue- stratificatus.’ It extends dorsally as far as tlie sulcus calloso- marginalis, frontally about 3 mm. frontacl of the genn corporis callosi, occipitally about as far as does the frontal lobe, and ventrally as fa r as tlie corpus callosum. The occipital part of the limbic gyrus is for the most part covered by the area limbjca posterior. It contains n distinct fourth layer, and

resembles the isocortex in other parts of the hraiii mncli morc closely than the anterior limbic region. The outer granular layer contains numerous g ~ a n u l a r cells of small size. Then f o l l o ~ s a broad pyramidal layer, light, with large pyramidal cells. The fourth layer is broad, contniniiig graiiular cells in which scarcely any pyramidal cclls call be found. Ganglionic and multiform layers merge gradually into each other. Jus t helow the inner granular layer there are large pyramidal cells

Page 24: The cerebral cortex of the cebus monkey

of about the same size as those in ii iV. They are arranged i n columns, although not \-cry distiiictly. The sixth layer contains mostly smaller cells, but some of the large pyrarniclal cells of the fifth layer can still be found. The boundary against the medulla is sharp (fig. 9).

The retrosplenial area is small and situated for the most part ventral to the spleiiium corporis callosi. T t does not differ in its appearance froin that of other animals. A4 cle- tailed description and a photograph of this area seemed there- for superfluous.

The insular cortex (fig. 9) is coiispicuous mainly for its Iiglitriess ; the density of the cells appears here to be less than anydiere else in the cortex. Otherwise the appearance is as typical as one might wish for. All six layers are well devel- oped. The third as well as thc fifth layer coiitain large py- ramidal cells, in both layers of about the same size. Their size appears to decrease somewhat as one goes occipitad, but the difference is slight aiid the change is so gradual that 110

well-defined bouiidary can be given. The structure of the insula is much simpler here than it is in the human brain.

The total area of the isocortcx of tlie left hemisphere was tletermined. Each section was drawn on paper at a magni- fication of X 10, the boniidaries of the isocortex marked, and the outlines measured by means of a cartographer’s wheel, thus fa r following Krauss, Davison aiid Weil (’28). From these data the surface was computed by means of Simpson’s rule for numerical integration. The rationale bcliind this is simple: assuming the sections to have been cut at equal inter- vals and all at the same angle to the longitudinal axis, i.e., parallel to each other, thcii tlie length of the outlines p will be a function of the position of the section on tlic long-ituclinal axis x ; in other words :

y = f ( x )

and tlie surface will be given by tlie equation:

s,,

A - I f(s)ds X,

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CORTEX O F CEBCS 205

where x,, aiid s,, denote tlie frontal and the occipital pole. This integral is not given as an a~lalytical expression, hut its ralues fo r xl, x2, x3, . . . . s,, are known from the measurements, and numerical i 1 1 tegratioii is therefore possible. Two conditions, however, have to be fulfilled to make this a legitimate pro- cedure: firstly, the succeeding points s,, s.,, s$, . . . . x, have to he sufficiently close together; in otlier words, the interval ds has to be sufficiently small. Secondly, the function f ( x ) must not hare any points of discontinuity, as it might happen wlien tlie sections are cnt in the plane of a sulcus (Nayrac, ’30). It should be noted that these conditioiis apply equally to any of the other methods based on serial sections which have b m i explained iii the literature. In the case of the com- pai*ativel>+ simple brain of cebus, the central snlcus is probn- lily the oiily one that might cause a discontinuiiy in our series. The error made in this computation is about ( “‘;,oxn) M, where l r denotes tlie mean of the differences. By ascertaining it, it caii be seen whether the interval chosen was sufficiently small for tlie purpose in hand. For a more detailed explana- tion of this method the reader is referred to the mathematical literature. A useful book is that by R~iiige and Konig ( ’24) .

I n this way the area of the isocortex of the left hemisphere was found to be about 4692 mm.2, with an error of about 100 mm.2. For practical purposes it is proloaid;.\. sufficient to take in round figures 4700 mm.2.

Our result differs widely from Kroclmaiiii’s figure (’12), who found the surface of oiie hemisphere of the cebus brain (of an unknown species) to be 13,682 mni.2 : it agrees tolerably well with the figure given by Popoff (’29) for the macaque ( c53F19 mm.*). It is difficult to explain the discrepancy between our and Brodmaiiii’s value by shrinkage, which TTeil ( ’28) determined for a ccbus brain as 2176. It is more reasonable to suppose that we have had another species than Brodmann. It should, moreover, be kept in mind that we have had a fe- male brain of an emaciated specimen. The total thickness of the cortex is 3 mrn. in the precentral, 1.3 to 1.5 mm. in the occipital, and about 2 mm. in the tempom1 and the parietal

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206 GERHAR,DT VON BONIN

region. All these figures, it should be emphasized, a re taken from stained sections. They are not comparable to similar ones given elsewhere for fresh specimens.

1~18cu881ON

It becomes now our task to compare the cortex of ccbus with that of other species. I n these comparisons, the human brain will play the greatest role, not oiily because it is the best known, but also because in the human brain differentiation has gone furthest. Some general characteristics of the cortex should first be briefly considered.

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CORTEX OF CEBUS 207

The relative thickness of the several layers has aroused much discussion, particularly since many observations point to functional differences of these layers. A receptive and an associative function of the supragranular, and an effective function of the infragranular layer is assumed by Ariens Kappers, Huber and Crosby ('36) and similar views are ex- pressed by v. Economo and Koskinas ( '25) and by many other authors. The anatomical, physiological and clinical argu- ments for such hypotheses received further support from comparative morphology. van t 'Hoog ( '18) determined the thickness of the cortical layers in numerous mammals, and his diagrams are given in Ariens Kappers, Huber and Crosby ( '36). He measured the postcentral area in all brains. Con- fining observations to but one area involves the difficulty of ascertaining morphological homologies, difficulties which are, as we shall see, not always easily surmounted. I t appears safer to take for each species the whole brairi into account, although unfortunately not very many brairis have been de- scribed or pictured in such a way that the thickness of the layers is either directly given or measurable on photographs or drawings. The data we have been able to collect are given in table 3. From these the average thickness was computed by t,aking the mean for all areas for each brain. This, of course, leaves out of account the different sizes of the various areas, but with the existing information we shall have to be content with this rough approximation. In this computation the layer ivA of the striate area has been considered as part of iii. The final results are given in figure 11. The primates and tupaia, a form which is close to the ancestors of pri- mates, have a better developed supragranular layer than the other forms, but the difference is not striking. It is also noteworthy that the first four animals listed have about the same average thickness of the inner granular layer. A re- vision of van t'Hoog's work on the basis of such average figures may be desirable. The correlation between relative thickness of layers and phylogenetic status cannot be very high, and Brodmann's judgment that the two are independent of each other appears still the soundest. THE JOURXAL OF COMPlRATIVE NEUROLOGY, VOL. 69, NO 2

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208 GERHSR.DT VON BONTK

TABLE 3

Relative thickness of layers; comparative material

House (Rose, '89 b )

precentr. grand. precentr. sgranul. postcentr. parietalis occipitalis striata temp. sup. temp. inf. ins. gran. post. Average

Opoaazim (Gray, ' 2 4 )

praeorbitah postorbitah psrietalis striats peristriata temporslis Aver age

l l n r r n r e d ides (LP Gros Clark, ' 8 8 )

sensorimotor parietal insular retrosplenial striate temporal Average

Tupa in minor (La Rros Clark, ' 2 4 )

front. agran. ' postcentral ' striata temporal front. grand. insular Average

1

0.11 0.09 0.07 0.09 0.12 0.14 0.04 0.08 0.06 0.09

I1 and IIl

0.2.5 0.19 0.21 0.35 0.23 0.2 .? 0.25 0.28 0.23 0.24

0.2" 0.32 0.13 0.26 0.23 0.30 0.18 0.21 0.96 0.23 0.14 0.21 0.19 0.26

0.27 0.J3 0.1 n 0.23 0.11 0 2 2 0.24 0.08 0.27 0.14 0.27 0.17 0.23 0.16

0.08 0.36 0.09 0.44

0.09 0.39 0.07 0.53

0.12 0.29 0.10 0.31 0.09 0.39

I r

0.08 0.00 0.16 0.13 0.11 0.19 0.13 0.08 0.0s 0.11

0.00 0.15 0.11 0.28 0.11 0.1 2 0.13

0.08 0.23 0.9s 0.20 0.27 0.28 0.22

0.22

0.20 0.19 0.23 0.20 0.21

0.22

P ond PI

0.56 0.72 0.56 0.53 0.54 0.42 0.58 0.56 0.64 0.57

0.46 0.46 0.36 0.33

0.50 0.42

0.40

0.52 0.35 0.3.9 0.48 0.32 0.28 0.39

0.40 0.25 0.20 0.33 0.37 0.36 0.32

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CORTEX O F CEBUS

Hapale ( M a t t , Schustm, and HaUiburton, ’ 0 9 )

motor A motor B postcentral temporal visual Average

Tarsius (Woollard, ’ 2 5 )

p r er olandic postrolandic parietal occipital striate temp. sup. temp. inf. Average

Papio (Schuster, ‘ 1 0 )

motor anterior precentr. frontal pref rontal postorbital postcentral sup. parietal inf. parietaI calcarine occipital temporal post. limbic Average

TARTJE R-

I

0.09 0.07 0.09 0.08 0.09 0.08

0.08 0.07 0.09 0.10 0.06 0.14 0.07 0.09

0.07 0.07 0.09 0.16 0.13 0.07 0.09 0.07 0.08 0.09 0.10 0.06 0.09 ~-

-Confin U P ~

II and I I I

0.45 0.51 0.47 0.43 0.39 0.46

0.38 0.37 0.47 0.31 0.26 0.30 0.30 0.34

0.41 0.17 0.38 0.41 0.35 0.46 0.41 0.38 0.17 0.39 0.42 0.42 0.39

IT r a n d 81

0.06 0.39 0.00 0.39 0.12 0.32 0.16 0.33 0.26 0.26 0.12 0.31

0.00 0.18 0.14 0.15 0.36 0.24 0.13 0.17

0.00 0.00 0.12 0.06 0.10 0.14 0.11 0.13 0.50 * 0.12 0.15 0.17 0.13

0.54 0.38 0.30 0.44 0.32 0.32 0.50 0.40

0.49 0.46 0.41 0.37 0.42 0.33 0.39 0.42 0.25 0.41 0.32 0.35 0.39

~ ~-

‘ivA = 0.11; ivB = 0.22; ivl: = 0.17.

Another point which has been much discussed is the cell density. As f a r back as 1881, Scliwalbe remarked: “But the differences in intelligence a re bound to show themselves mnch more clearly in differences of the development of the surface relief and of its various parts, even though the two other factors, the thickness of the cortex and the number of the

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210 GERHAR,DT VON BONIN

ganglion cells in the cortex a re still unknown to US."^ Ex- plaining his conception of the nervous gray, Nissl (1898) pointed out that in lower animals (he published photographs of the cortex of man, dog and mole) the cells a re far more crowded than in higher ones, indicating the importance of the nervous gray. Nissl 's conception has probably few adherents nowadays, if a literal interpretation is insisted upon, yet that

Suara- 56 48 49 .54 43 48 39 3 3 45

Papio 1.00

Cebus IOB

Hapale 1.36

n

Man 1.34

Averaee Relative Thickness of Corttcal Layers Figure 11

there is a greater opportunity for processes of the cells to come into mutual contact if the cells are less crowded is almost self-evident. I t is far less evident, however, that a higher development of this 'gray' (whatever its histological inter- pretation) should denote higher intelligence. This supposi- tion is based on certain views on the relation of mind and

a " Vie1 deutlicher miissen sieh aber die Versehiedenheiten der geistigen Begabung in Versehiedenheiten der Oberfliichenentwicklung des Grosshirns und seiner ein- zelnen Abschnitte bemerkbar machen, wenn wir allerdings auch die beiden anderen rnassgebenden Faktoren, die nicke der Grosshirnrinde und die Anzahl der Gang lienzellen in derselben nicht mit in Rechnung bringen konnen. ''

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CORTEX OF CEBUS 211

matter, and on the functioning of nervous ‘networks,’ neither of which is beyond dispute.

But we need not go to this metaphysical depth to meet trouble. Marburg (’07) studied the cell density of the cortex in some primates and arrived at a conclusion diametrically opposite to that of Nissl’s: “The cortex richer in cells is the more highly developed one” (“Die zellreichere Rinde ist die hoher entwickelte”). While this runs counter to one’s im- pressions from casual observations of the cortex of lower and higher mammals, it shows a t any rate that the correlation between phylogenetic status and cell density is fa r from being satisfactory.

This was precisely the conclusion to which Mayer (’12) came on the basis of observations made in the laboratory of Brodmann. Studying various areas in the brains of numer- ous primates, lie stated that there was no correlation between cell density and phylogenetic level. Sugita ( ’18) published a careful study on the number of cells in the cortex of the albino and the Norway rat, unfortunately restricting his measure- ments to but two layers of one area. His paper is very valu- able, however, from a methodological point of view. He dis- cusses the correction coefficient to be applied to the raw measurements in order to allow for shrinkage.

The number of cells per unit volume in the human brain is given for each layer of each area in v. Economo and Koskinas’ work ( ’25, see table 5 ) . But these authors also emphasize that the mere relative number of cells per unit volume leaves out of account the size of the cells. Hence, particularly for comparative purposes, the cell density as defined by these authors (loc. cit., p. 74, et seq.) appears to be a much better measure. It is defined as the relation of the volume of stained cell bodies to the unit volume of the cortex. Later, v. Economo ( ’26) proposed this measure as the gray-cell coefficient which thus far, however, has only been determined for man, where it is about 27: 1.

The anatomist’s determinations of cell size are rendered of somewhat doubtful value by the fact that not always the same

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212 GERHARDT VON B O N I S

methods of fixation and embedding are or hare been employed. Onlp recently G. Hertmig ('31) showed that the amount of shrinkage varies with the method of fixation and that, more- over, the slirinkagc of the nucleus may be quite different from that of the plasma, thus altering artificially the nucleus-plasma relation. Moreover, the time elapsing between death and fixation has a great influence on the size and shape of the cells in the histological picture (Rose, '29 a).

All this goes to show that the practical difficulties of even a reasonably exact determination are almost unsurmountable.

efficient. Even the figures givcn liere for the relative number of cells

are l in t immediately comparahle to those giren by v. Ecoiiomo

IIence, we have not attempted to determine tlic cell-& old>- 1. co-

TABLE 4

K u n i h ~ ~ of cells per ( 1 0 0 ~ ) ~

L n y w Homo C ~ h u - Quotient

ii 98.9 233.8 2.36 iii A 44.4 119.0 2.68 iiiC 3.5.0 92.4 2.69 iv 110.5 172.7 1.56 v 38.3 88.5 2.31 vi 40.6 90.6 2.23

and Koskinas for the human brain. Formalin-paraffin in the latter, alcohol-celloidin in our own case, have distorted the 'true' ( intra vitam) ratio in an unaccountable and presuma- bly quite different way.

No other data on cell density arc available, pet in spite of all that has just been said, table 4 compares the liuman brain with that of cebus. While the arerage cell densities for each layer, taken over all areas, a re in both supra- and infrag. 0 1 anu- lar layers about 2.5 times higher in ccbus, that for the iiiner granular layer itself is only about 1.5 times higher in cehus. This discrepancy between the inner granular and the other layers contains probably more truth than the actual numbers which may, of course, be falsified by differences in the histo- logical techniques.

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Of the various cortical areas we shall first discuss the sen- sory and the motor areas, i.e., the middle level, and then the 'association areas,' i.e., the highest level. Needless to say, this classification has to be taken with a grain of salt, but it appears preferable to a purely topographical principle.

The area striata, 17 or OC, shows an almost more perfect morkmanship than in man. The brain of cebus exhibits a particularly orderly arrangement of the large stellate cells in i\-B. This was first described by Brodmann ('O!,), and Gu Ngoq-ang ('3'7) lias recently called attention to it. Also, the solitary cells in tlie fifth laycr are fouiid rather ill viil. v. Economo and Koskinas mention that in man the giant cells of Neynert are 'not infrequently' dislocated.

The splitting of tlie fourth layer into three sublayers occurs in its fully developed form only in primatcs, although a be- ginning of this process lias been demoiistrated by v. Volkmaiin ('28) already in sciurus. 17. Volkniunii ('28) and Le Gros Clark ('25) have rcceiitly traced the plij-logenesis of thc stri- ate area. Tliether ivR really is a part of the fourth layer, having arisen from it by a process of 'diaclioresis,' as 17.

Volkrriann ('36) believes, o r whether it is homologous to iiiC having undergone n thorough change into granules ('Verkor- neluiig'), as Lorente de K6 ('35) believes, is a question to the solution of m4iich we are unable to contribute. That for prac- tical purposes we have sided with Lorente de N6 has been stated (p. 198).

T t has been pointed out especially by Rleist ( '26) that ivC is thicker than ivA, therefore allotting in his well-known theory the reception of the contralateral impulses to the lower sublaper. It is of some interest in this connection to compare tlie relative tliickriess of' upper and l o x w granular layers (ivA and ivC) in various primates. The material v e have been able to gather is given in table 5. The order in which the quotient ivh/ivC arranges the primates is entirely differ- ent from the natural one. It is all tlie more interesting that cebus is nearer to man than any other primate in the list.

'As Le Gros Clark ( ' 2 5 ) points out, both the stellate cells in ivB and the 'giant' cells in v were described by Meynert a solitary cells.

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214 GERHARDT VON BONIN

The extent arid the shape of the striate area has recently been discussed by Gu Ngowyang ( '37). On its medial side the cebus brain shows the T-shaped pithecoid type. P.-Y.'s brain closely resembles that shown by Brodmann ( '12, p. 192). In both cases, the upper branch of the calcarine fissure forms a limiting sulcus, and in both brains the striate area reaches almost as far as the splenium. On the lateral side, the striate area does not quite reach the h a t e sulcus.

Both para- and peristriate areas can clearly be recognized. Although difficult to prove, the impression remains with the writer that the peristriate area is not as well developed in cebus as it is in man where it appears to be more sharply differentiated from the neighboring parietal and temporal cortex. By and large, however, there can be no doubt that

TABLE 5

RPlati?le thicknPs8 of Quotient Species ivA ivC ivA/ivC

Man 0.08 0.19 3.4 v. Economo and Koskinas Orang 0.14 0.19 1.4 Own preparation Baboon 0.07 0.11 1.6 Gu Ngowyang ( '37) Macaque 0.08 0.13 1.6 Ibid. Cebus 0.10 0.19 1.9 Present paper Hapale 0.12 0.17 1.4 Brodmann ( '09)

the optic region is as well developed in cebus as in any primate.

The auditory region, studied intensively in man by v. Economo and Horn ( '30) , is definitely better differentiated in cebus than Brodmann's brain maps of other primates would lead one to expect. According to this author, the auditory 'Koniokortex' of the human brain, his area 41, is not present in cercopithecus nor in any other lower form. The phylo- genetic development of the auditory area remained thus shrouded in mystery, although Brodmann's area 22 was gen- erally looked upon as the area of hearing in lower animal^.^

' Field 22 of the mouse, identified by Rose ( '29 b ) and studied by Lorente de N6 ('22) does not coincide with the projection area of the medial geniculate body determined by Pennington ('37) in the rat. On the other hand field 4 1 4 2 of Tsuneda's ( '37) description is much smaller than, but within, Pennington '8 area.

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Reek (’29) was able to show in thorough myeloarchitectural studies that the orang a t any rate possessed the same degree of differentiation as man on the superior temporal planum, but hardly any information regarding the lower monkeys has been forthcoming. Only quite recently Walker (’37 b) has examined the auditory area in the macaque, defined as the area of projection from the medial geniculate body. Without giving pictures he describes mesially to, and distinct from, area 22 in the posterior part of the splviari fissure “a distinct type of cortex,” “which has the characteristics of ‘konio- cortex’ ” and which, according to him, is “very probably the cortical representation of the auditory system.’’ We have seen that cebus has a similar area, and it appears permissible to homologize this with v. Economo and Koskinas’ area TC. It would also appear permissible to postulate a homology between the area temporalis magnocellularis and v. Economo and Koskinas’ TB.e On the other hand, a glance at figure 8 will suffice to show that these two areas are histologically less differentiated than they are in man. The auditory area proper is less granular, medium-sized pyramidal cells are still present, nor is the para-auditory area as clearly characterized by large (giant?) pyramidal cells as it is in man. Further investigations are urgently needed. At present it would appear as though the phylogenetic development of the tem- poral koniocortes lagged behind that of the occipital area.

Both the striate and the supratemporal area are the sole end stations of the sensory radiations leading to them. It is different for what is generally considered as the somesthetic area, for the radiation from the somato-sensory nucleus of the thalamus ends not only there but in a much larger field of the cortex which includes parts of the parietal as well as of the frontal lobe (Poliak, ’32; Le Gros Clark, ’32; Walker, ’37a). Nonetheless, we shall confine our discussion of the somesthetic field to the postcentral area.

‘How far TC and TB are synonymous with Brodrnann’s 42 and 41 has been discussed by v. Eeonomo and Koskinas, loc. eit., pp. 692-693.

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216 GERHARDT VON B O N N

A simple definition of this area based on function or on thalamic connections is a t present impossible. Even about its structure there is no complete agreement among the authors. According to v. Economo and Koskinas (’25) four different areas cover the human postcentral gyrus like narrow hands laid down parallel to the central sulcus. 111 ilie depth of this sulcus there is a strip (PA) still containing giant cells of Betz, but already showing a well-developed inner granular layer. Brodmann (’04, p. 130) considercd this as a transitory formation (eine kurze, die T‘ermischung beirlcr Strukturtypen zeigende obergangszone), and did not give it a special name. Biicy (’35) states that area 4 is in contact with area 3, the juncture being extremely sliarp, evidently not recognizing PA at all. Beyorid this narrow strip there follows, still on the posterior wall of the central siilcus, a strip of ‘koniokortes,’ v. Economo and Koslrinas’ PK, Brodmann’s area 3. The height of the postcentral gyrixs and its posterior all are covered by a cortex characterized by well-developed pyrami- dal cells and an equally well-developed inner granular layer. This is PC, or 1. In the depth and in the posterior wall of the postcentral sulcus there is a iiarrm- strip of cortex char- acterized by small cells, hat also by some conspicnonsly large pyramidal cells in iiiC. This is 17. Economo and Roskinas’ PD, Brodmann’s 2. All these areas extciid almost as f a r as the parietal operculum of the insula. There is a small area occipital to the dorsal quarter of the postcentral sulcns which contains again some giant pyramidal cells. r. Economo and Koskinas consider it continuous with their area PA and con- sequently call it PA2; Brodmann called it field 5 or area praeparietalis. That this area should still he considered a part of the postcentral field is suggested by v. Economo and Koskinas ’ nomenclature, while Brodmann included it in his parietal region.

The nomenclature and the systems used by Brodmann and by v. Economo and Koskinas are again tabulated, together with data about their. presence in cebns.

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2;. E . and K, Rrodmonn Present in rebvi;

PA1 - A. poste. gig. pyr. S n m e

A. postc. gig. pyr.

3 A. postc. granulosa YB2 A. poste. intermedia YC 1 A. postc. intermedia

A. postc. oralis granulosa A. postc. oralis simplex PB1 I A. posttr. caudalis A. praeparietalis

P D 2 P A 2 5

The postcentral field of cebus is simpler than that of man. There can be no doubt about the homologies of the two oral fields P A and PB. It is more clifficult to decide the homology of our area postcentralis intermedia. I t shows perhaps more resemblance to v. Ecoiiomo and Koskinas’ PC, but may also he claimed for their area postceiitralis oralis simples. Tt is safest to assume that we have to do with an undiffercntiated ai’ea homologous perhaps to both, perhaps even t o BB3, P C and PD. The area praeparietalis which Rrodmaiin claims to liave found ‘far down the mammalian line’ is lacking iii the cebus brain, and it is a t present impossible even to guess at its mode of evolution. W e shall have to come back to this arca a t a later stage.

The motor arca which is immediately in front of the central sulcus arid the postcentral field shows a clear distinction into ‘motor’ a id ‘premotor’ area. Brodmanii (’12) has given data on the extent of these two areas for cebus which have been used by Bucy ( ’35). We can mainly confirm his results, but wish especially to call attention to two points, namely, to the relation between the central sulcus and tlie motor area and to tlie ventral extension of the motor and the somcstlietic areas. Owing to the direction of our sections it was impos- sible to determine with precision whether the boundary be- tween the preceiitral (i.e., the motor) and tlie postcentral area ran exactly in the depth of the central sulcus. It can only definitely be stated that near the dorsal margin the central sulcus bends oceipitad, but that the boundary between the motor and the sensory area goes straight on, with the result that a small part of the postcentral (i.e., tlie somesthetic) area comes to lie in front of tlie central sulcus. Vogt has fouiicl

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this behavior in his myeloarchitectural studies of the cerco- pithecus brain where Brodmann, on the basis of cytoarchi- tectural studies, did not mention it. Mott, Schuster and Sherrington ('11) note it in the gibbon (in an otherwise almost certainly erroneous map, as Bucy pointed out), and Bucy ( '35) himself has shown it for lagothrix, ateles (in one hemi- sphere), one rhesus monkey, the baboon and one orang (EE) , but not for cebus (5a, A) . Brodmann ( '12, p. 169) published a horizontal section through the central sulcus showing that F A only reached as far as the anterior lip of the central sul- cus. The most likely inference to be drawn is that there are individual variations, and that the relation between cytoarchi- tectural fields and furrows remains somewhat unsettled even in quite highly developed primates. It is further noteworthy that the somatic areas (by this term we may designate both motor and sensory areas) do not reach as fa r ventrally in cebus as they do in man. Again the reader may be referred to Brodmann's ( '12) or to Bucy's ( '35 ) figures. Brodmann shows a fairly broad strip on the operculum not covered by the motor and premotor area in cebus ; Bucy depicts the same behavior in lagothrix, ateles, papio, one macaque (13A), and in one chimpanzee (16C). Regarding papio he agrees with Schuster ('10). The whole precentral agranular cortex shows only two fields, the occipital one containing giant pyramidal cells, the anterior one devoid of them, but otherwise showing much the same arrangement of cells. This agrees with the findings of the majority of authors, but it should not be over- looked that v. Economo and Koskinas were able to differ- entiate between three fields in man, from the central sulcus forward, field FAY, F A and FB. This raises a problem of homology: which part corresponds to the motor, which to the premotor field, established by Fulton and his co-workers (see Fulton, '36) in the primate brain? Our own observations, being purely anatomical, naturally offer no clues. Stimula- tion of the exposed cortex by neuro-surgeons points, however, to a definite answer.

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All in all the projection areas of cebus are on three levels of differentiation. The striate area has even gone beyond the human level as far as stratification is concerned, and it has well-developed para- and peristriate areas surrounding it. The postcentral areas are not far below the human level, while the temporal koniocortex and its magnocellular rim lag con- siderably behind in differentiation. This behavior finds its counterpart in the relationships to the sulci and gyri. The stem of the calcarine fissure forms the axial sulcus for the striate area just as in man’s brain; the central sulcus forms nearly, although not quite the boundary between pre- and postcentral region, but Heschl’s gyrus can hardly be distin- guished from the surrounding supratemporal plane.

The parietal area which we shall discuss first is covered by two fields, di- vided by the interparietal sulcus. An effort to determine their homologies may not lead to much more than a working hypothesis, particularly since our knowledge of these areas in other primates is still very limited. Yet the phylogeny of the parietal lobe is no whit less important or interesting than that of the frontal lobe. In fact we know of more definable functions in man connected with the parietal than with the frontal lobe. F a r more aphasias are a sequence of parietal than of frontal lesions ; ideatory apraxias, many agnosias and the body scheme are somehow bound up with the parietal lobe. Indeed, the form and function of an area which extends be- tween the three most important sensory fields-the visual, the auditory and the somato-sensory-should be of outstanding interest. The morphology of the primate parietal cortex is at present mainly based on Campbell ’ s ( ’05)’ Mauss ’ ( ’08, ’12) and Brodmann’s (’09) maps. On Brodmann’s maps we see in lemur and hapale a beginning differentiation into two distinct fields, a frontal area 5 and an occipital area 7. These ttvo fields are still found in cercopithecus, but with this dif- ference that 5 is now mainly dorsal and 7 ventral of the inter- parietal sulcus. A further differentiation has occurred in man where areas 39 and 40 are now added on the supramarginal

We come to the highest level of the cortex.

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220 GER,HARDT vox BONIN

and the angular u r u s respectively. On Brodmann’s map we find 7 now (in man) dorsal of the interparietal, while 5 has shrunk to a small area near the postcentral region. Rut 5 corresponds to area P92 of v. Economo and Koskinas, and belongs, as me already saw, in all probability to the somes- thetic field. This circumstance as well as the different localiza- tion of 7 relative to the interparietal sulcus makes one hesi- tate to accept Brodmann ’s interpretation. The difficulties are enhanced by the fact that the areas dorsal and ventral to the interparietal sulcus resemble each other very closely in their structure. At first sight one would be inclined to accept the dorsal area as the homologue of area 7 or PE, the ventral area (parietalis posterior) as the homologuc or oriment of the humaii areae 39 and 40, or PF and PG. But merely the iden- iical relation to a sulcus would not be a sufficient argument. Such a view would, however, receive a weighty support if the narrow strip on the clorsal lip of the interparietal sulcus which m-e described in the previous chapter, could be identified as the homologue of the visuo-sensory band in man, Then, identi- cal topographical relations could be adduced as an argument.

The visuo-sensory band or ‘sensory band p’ was first de- scribed by Elliot Smith (’07 b) as extending from a poiiit “aboiit 2-3 mm. from the upper lip of the sulens ” and reaching “exactly to the bottom of the furrow.” He could cite li’lechsig’s myelogenetic observations in support of his conceptions. Brodmann (’09) recognized this band but thought that it mas merely an occipital extension of his field 2 along the inter- parietal sulcus, and did not constitute a separate field. v. Economo and ICoskinas are more inclined to follow Elliot Smith. They describe a formation PE (D) as coursing in the interparietal sulcus, ‘ beide Wande desselben iiberkleidend. ’ Vogt ( ’ l a ) describes an area 87 in his myeloarchitectural studies which, however, is situated ventral of the interparietal sulcus and which therefore hardly corresponds to Elliot Smith’s band. Obviously, anatomists are still fa r from com- plete agreement.

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Confirmation of Elliot Smith's views came from the clinical side. Potzl ( '25) discussed Elliot Smith's visuo-sensory band when reporting on a patient in rhom a glioma of the inter- parietal region had been successfully removed. His co- workers, Hoff ('29) and Hoff and Kamin ('30), studied in two patients the effects upon this area of cooling and heating throngh a mound in the scalp, and Foerster ( '36, p. 386, et seq.) describes in detail the symptoms after electrical stimulation of the upper lip of tlie interparietal sulcus. Foerster states that this region is the cortical end station of vestibular impulses.

The strip of cortex which is found in cebus is by no means identical in structure with the human visuo-sensory band. I n man the visuo-sensory band shows, according to v. Economo and Koskinas, large cells in tlie third layer ; in cebus the dor- sal lip of the interparietal sulcus shows the largest cells in the ganglionic layer. It will need further comparative material from other primates before we can have a clear picture of the morphology of the parietal field. Only provisionally, then, can we put forward the view that the posterior parietal area of cebus is homologous to area 39 (PF) and 40 (Pa) . ?Ve would further have to assume that tlic posterior parietal area gradu- ally differentiated into PF and P G much in the same way in which the primitive postcentral area differentiates into PA, PB and PC, or the precentral area into FA and FB. Oiily further observations, however, to repeat it once more, 1t7ill enable us to reach a verclict on this hypothesis.

Whether field 39 and 40 should be considerecl part of the parietal lobe, as does Brdmaiin, or part of the temporal lobe, as does Campbell, appears to the writer a matter of minor importance which, at any rate, could only be settled by more extensive studies.

The ventral connection between parietal and frontal field on the operculum is of particular intercst. The posterior parie- tal area of cebus extends fairly far forward, changing its appbarance slightly in a very gradual manner. It is thus possible to speak of a parieto-frontal area which shows slightly larger pyramidal cells and a slightly broader inner

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222 GERHARDT VON BONIN

granular layer than the rest of the parietal field but still re- tains that well-ordered columnar appearance we miss else- where in the frontal lobe of cebus. It is not clear whether this area can be homologized with the area opercularis de- scribed by Mauss ( ’08, ’12) in the brain of cercopithecus and of the orang and the gibbon, since Mauss studied only the myeloarchitecture. Moreover, Mauss remarks in his second paper that the homology of field 30 in cercopithecus with field 30 in the orang and the gibbon “ist trotz der topischen uber- einstimmung mehr als zweifelhaft,” basing his criteria for homology obviously more on the microscopic structure than on topographical relations.

The influence of this parietal type, as we may call it, is still seen in the fronto-opercular area which combines the large cells and the slight inner granular layer of the precentral areas with the columnar arrangement of the parietal areas. The similarity between this formation and area FCBm (44) in man is quite striking. It is, of course, clear that cebus does not possess a speech center in the sense in which man has one, but it appears reasonable to suppose that the oriment of this area goes farther back in phylogenesis than most authors formerly believed. Indeed, v. Economo and Koskinas still asserted that the area FCBm was only present in man and missing in all primates. Since then, Icreht (’36) studied the cytoarchitecture of Broca’s area in the anthropoid apes. In the baboon, too, v. Niessl-Mayendorf (’30) asserted its pres- ence, although on somewhat slender grounds.

The ‘prefrontal’ field of cebus, covering, according to Brod- mann (’12) less than 10C;, of the whole cortex, as compared with 29% in the human brain, is remarkably uniform. It has not been possible to differentiate more than three areas. Even so, the orbital area does not differ widely from those on the lateral side of the hemisphere. The anterior granular area contains significantly more cells than the posterior one in the second and in the sixth layer. Computing the standard devia- tions f o r the data given in table 1, a short calculation shows that the fronto-polar area contains about 0.28 0 and the poste- rior area about 0.81 c less cells than the average f o r the whole

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cortex. In a similar way we obtain from v. Economo and Koskinas’ figures, estimating the standard deviations from the ranges, the following figures f o r the frontal areas of man regarding cell density :

FC -0.91 u

FD -0.6; u

FDA -0.44 u

F D r -1.02 u FE -0.2; u

The fronto-polar area of ccbus and of man showr, as far as the single character of cell density is concerned, about the same degree of divcrgeiice from the mean cortex. The poste- rior granular area of cebus is nearest FC, but here the re- semblance is not nearly so close. We arc Iiaidly justified in laying too much stress 011 such sliglitlp specious numerical ah- stractions, but from general considerations it appears reason- able to assume that in phylogenesis the fronto-polar area has assumed its definite form first, and that then a further differ- entiation took place iii the intermediate field, a differentiation which does not appear to have completed its course yet. The posterior granular area in cebus is therefore not strictly homologous to any one field in man, but is an indifferent field out of which the areas F C and FD of the huiriaii brain could have developed by a process of progressive differentiation essentially the same as that which was postulated f o r the parietal lobe.

SUMMARY

Much of what might be said in a summary has been given in the brain map (fig. 10) which accompanies this paper. Apart from this, we saw that the brain of cebus was well tlificrcntiated in its visual area, not quite so well in its somes- thetic, and perhaps still less in its auditory area. We dis- cussed the homologies of the arcas in the parietal and in the frontal lobe. In both lobes we found a much simpler structure than is shown by the human brain, but differentiation was already foreshadowed. I n particular, we found a high degree of specialization on the operculum of the insula where the

T H B JOURXAL OF C O M P A R A T I V E NEUROLOGY, YOL. 69, NO. 2

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human speech centers seemed already discernible. While much of this discussion was of necessity speculative, it is hoped to have given at least a working hypothesis for future cytoarchitectural work.

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