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Of a New Concept of Neocortex Evolution*

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Of a New Concept of Neocortex Evolution* Functional Architecture of Motor and Sensory Cortices in Primates in the Light of a New Concept of Neocortex Evolution* FRIEDRICH SANlDES Department of Ana/om'}', University of OUawa, Canada. The Concept of Duality of the Neocortex The dual structure of the neopallium-a parapiriform moiety and a parahippocampal moiety-was first conceived by Dart t 1'J::~4 \ as a resull of painstaking architectonic and stimulation studies on various South African reptiles. These studies were an out· growth of the principal investigations of Johnston (1915), Crosby (1917), and Elliot Smith (1919) on the forebrain of reptiles. Dart already anticipated the principle of duality to be valid for the mammalian neo~ortex. Actuallv, it \\as Abbie who suc­ ceeded in presenting architectonic evidence of the dualin' of the neocortex. first' in monotremes (1940) and later. in marsupials (19 ~2). In cytoarchitectonic terms Abbie subdivided the entire neocortex of echidna and platvpus into two major components~ one related to and adjacent to the hippocampus (archicortex'l, the other one to the piriform cortex (paleocortex). Both moieties show a differentiation into several stages. Within the parahippocampal neocortex Abbie distinguished four successive stages of differentiation and within the parapiriform neocortex three stages. This progressive differentiation takes place in both major components by thickening of the cortex, accentuation of the lamination, and eventually appearance of granular cells (granu­ ~~rization), In the marsupial Perameles, Abbie (1942) found the principle of the dual nature of the neopallium" fully sustained. He concluded that the different architectonic fields represent successive waves of circumferential differentiation in e.\<olution, commencing from the hippocampus and from the piriform cortex, respec­ hl·ely. These important works of Abbie did not receive the attention they'merit. Thus, ~IT~li' work Was supported by grants from the Medical Researcll Council of Canada.. Piil!· 'lurhor wi~hc5 to thank Dr, W. Hendelman for prMfreading the manuscript and for his helpful . IlHlU'nts on English usage. and Mrs. E. Barany"k for the preparation of the hi~tological material. 137 133 FRIEDRICH SAN IDES FU';CTIQl"AL 20 years later, m 1962, on the basis of cytoarchitectonic and myeloarchitectonic data whereas the in the extensive human frontal lobe, we independently proposed the same principle. the depth of the dual origin of the neocortex. The combination of the cytoarchitectonic and myelo­ simian prim: architectonic methods proved to be particularly valuable, not only in outlining the of the front. coinciding areas more reliably but also in tracing differential trends in several suc­ equivalent fl cessive areas. The myeloarchitectonic method is advantageous because, operating at cortex but r, lower magnification. a series of architectonic areas can be surveyed simultaneously Table 1 for a (Fig. 5). It appe, Since our initial fmdings in the frontal lobe of man (l962a, b, 1964) we found archi tecture. the principle of a dual origin of neocortical differentiation confirmed in a series of (1909) and primates (ArClicebus, Sairmri, Macaca. Panl, in Carnivora (cat, raccoon), in Roden­ laminated pI tia (rat), ill Insectivora (Erinaceusl, and in Chiroptera (MYOlis luci/ugusl. older cortiC! A diagrammatic presentation of this principle is illustrated in the frontal lobes the lateral p of man and monkey I Fig:. 1). It is important to recall that the greatly expanded neo­ tics in additi cortical lobes of higher mammals still are bordered ventromedially and ventrolater­ tex). Howe\ ally by the old protocortices, the archicortex and the paleocortex. In the coronal 19-!-7: Sanid, sections of primates' frontal lobes (Fig. 1"1 the archicortex is represented by the tex and the supracallosal hyppocampus (vH, the vestigia hippocampi of Elliot Smith, 1919), primitive aIle The most pr (Fig. 1 L The cha areal arcliite Medially, adj laterally. adj: formerly calh The insular c· phylogenctic rior insular c It was Mey exposed brain surface and t' --~-~--~- AI AlI All FmZ Figu.re 1. Coronal diagrams of frontal lobe of man (a) and monkey (b). The arrows FoZ indicate the differential trends from the cingular proisocortex (Pro) medially and FpZ the insular proisocortex laterally. Becau:;e of the le"ser vault of the frontal lobe of the G g monkey the plane at the level of the sulcus principalis does not pass through the paleo­ Gig a cortex (Pal) -the last source of insulolimbie differentiation-but only through the caudo· H h i, orbital c1austroeortex (Pro). The paleocortex is present in the section through the rsm Ka a human brain. The dashed line through sulcus frontali~ inferior (fi) in man and sulcus Ks $' prineipalis (prine) in monkey marks the basic medio/limbic hordedine of the two pre· lam. dis;;. 11 frontal spheres. Sulci: arc. arcuatus superior: d. cinguli: fm. frontalis medius: fs. !lip] ~! frontalis superior; orhm. orbitali~ mediali~: orbL nrbita!i" lateralis; Ce. corpu" callosulll. ~lsI P ,,\. dUl1gtrum: S. septum; V. ventricle: for furtber abbre\·iations see Table 1. OIllZ ft; FUNCTIONAL AlleHlTEeTl'RE OF ~lOTOH _\:\0 SEi\SORY CORTICES 1:\ I'IU,\lATES I :~9 )hitectonic data whereas the bulk of the primate hippocampus is displaced by 11 sagittal rotation into mme principle: the depth of the temporal lobe. The paleocortex. although reduced in the microsmatic ,nie and myelo­ simian primates, retains its original ventral position ( Pal, Fig_ l11). Because the vault :J. outlining the of the frontal lobe of the monkey is less than in man, a coronal section through the in several ,mc­ equivalent frontal regions of the convexity in the former does not include the paleo­ e, operating at cortex but rather the neocortical proisocortex_ caudo-orbitally (Pro, Ib). (See simultaneously Tnhle 1 for abbreviations.-I It appears necessary to insert some remarks on the nomenclature of the cortical (64) we found architecture_ Most of the terms which \\-e use were orit::inally coined by Brodmann in a series of (1909) and C. and O. Vogt (l919\. The neocortex, insofar as it passes through a six­ on), in Roden­ laminated period during fetal life, is referred to as isogenetic cortex (isocortex). The gus I. older cortices-the medial archicortex Ihippocampal formation of mammaisl and e frontal lobes the lateral paleocortex (olfactory cortex proper) which exhibit peculiar characteris­ expanded neo­ tics in addition to very limited lamination-are called the allogenetic cortex (allocor· nd ventrolater­ tex). However, as we will see, t\\O successive intermediate structural steps (Filimonoff, In the coronal 19-1·7: Sanides, 1962b: Stephan, 1(63) are intercalated between the primitive allocor­ ~scnted by the tex and the mature iSQcortex, namely, the periallocortex (which is adjacent to the Smith, 1919), primitive allocortex) and the proisocortex (which is adjacent to the mature isocortex) . The most primitive types of allocortex are also referred to as allocortex primitivus lfig. 1 L The characteristic periallocortex and proisocortex show different regional and areal architectonic elaborations, in relationship to the bordering isocortical lobes. Medially, adjacent to the archicortex_ they are bound to the limbic lobe. and ventro­ laterally, adjacent to the paleocortex. the\' are bound to the insula Reilii. which was former! y called the stem lobe. Both these "lobes" are phylogenetically old structures. The insular cortex should be designated as part of the limbic cortex for ontogenetic and phylogenetic reasons I Yakovle\'. 1959), The anterior cingulate gyrus and the ante· rior insular cortex exhibit basic architectonic· resemblances. It was Meynert (872) who made the basic ohsen-ation that looking at the freshly exposed brain \\-e can distinguish two major components of cortex, that with a whitish surface and that with a greyish surface. The latter corresponds to the entire isocor- TABLE 1. Explanation of Abbreviations AI primary auditory area Pal paleocortex All secondary auditory area pAll periallocortex All allocortex primitivus parK parakoniocortex FmZ frontomotor zone par:\-r paramotor area l). The arrows FoZ frontopercular zone PiZ parinsular zone medially and FpZ frontopolar zone PIZ paralimbic zone Ital lobe of the G gustatory area PmZ paramotor zone )Ugh the paleo. Gig area gigantopyramidalis PoZ paropercular zone >ugh the caudo­ H hippocampus pre Fr prefrontal cortex Ism intermediate sensorimotor area pre!\f premotor area Ifi through the Ka auditory koniocortex pro~I promotor area nan and sulcus Ks somatic koniocortex proK prokoniocortex )f the two pre­ lam. dies. lamina dissecans Prt parietal cortex lis medius: fs, Mpl supplementary motor area SmI primary somatic area Jrpus callosum, MsI primary motor area SmI£ secondary Eomatic area L OmZ orbitomedial zone FRfEDRfCH SANIDES 14-0 FC:\CTIONA tex, and the former corresponds to the allocortex, including periallocortex. The and the ins whitish color reflects the fact that the cell-poor molecular or zonal layer possesses to the infer here particularly strong tangential fiber plexuses of "hich the striae olfactorii fibers Coneel are one example. This condition corresponds to the primitivity of the allocortex which influenced does not yet depend exclusively on thalamic afferents. key's front( In cytoarchitectonics we can disregard the first cell-poor layer. For example sion, using the so-called second layer of the isocortex forms the first real cellular layer. The experiment; periallocortex (the first architectonic step away from
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