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Cerebral Cortex 769 Cerebral Cortex 769 Cerebral Cortex the cortex is, at the routine histological level seen E G Jones, University of California, Davis, CA, USA with the Nissl stain (which stains only cell somata), ã 2004 Published by Elsevier Ltd. a lamination of cell bodies. Stains such as that of Golgi show that processes of the cells can extend This article is reproduced from the previous edition ã 2004, Elsevier B.V. across laminae. In most parts of the mammalian cortex, a six-layered pattern first introduced by the anatomist Brodmann and The mammalian cerebral cortex is an enormous sheet based upon Nissl staining, has come to be accepted as the of cells covering in the human brain approximately standard, though five- and seven-layered patterns have 250 000 mm2 and containing 1 109 or more nerve also been in vogue. Layer I is the layer immediately Â3 cells in a volume of about 300 cm . The human cere- beneath the pia mater and contains very few cell bodies, bral cortex is by no means the largest – it is exceeded belonging mainly to neuroglial cells and to a few non- in area by that of the whales – but it is probably the pyramidal neurons – hence its name, ‘molecular layer’. most highly differentiated. Differentiation, in this Layer II consists of small, tightly packed cell bodies, sense, means the subdivision of the cortex into the most of which are small pyramidal neurons, but never- largest number of histologically distinct subareas theless is called the ‘external granular layer’. Layer III is a each of which has a known or suspected function. thick layer in which pyramidal cell somata increase pro- The fundamental divisions of the cerebral cortex in gressively in size from superficial to deep. It is referred to mammals are the hippocampal formation (or archi- as the pyramidal or ‘external pyramidal layer’. Layer IV cortex), the olfactory cortex and associated areas is thin but densely packed with the somata of small such as the entorhinal and periamygdaloid area in pyramidal and nonpyramidal cells. It is called the ‘inter- the piriform lobule (paleocortex), and the remainder nal granular layer’. Layer V consists primarily of large, (neocortex). The three parenthetical names indicate loosely dispersed pyramidal cell somata. It is referred to the phylogenetic assumptions of past generations of as the ganglionic or ‘internal pyramidal layer’. Layer VI neuroscientists who regarded the neocortex as the is composed of relatively tightly packed, small, round hallmark of mammalian evolution. In nonmammalian cell somata that belong mostly to a modified form of brains, a hippocampal formation and an olfactory- pyramidal cell. It is called the ‘multiform’ or ‘polymorph related cortex can readily be identified, whereas a layer’. In certain areas, some of these layers can be neocortex is probably absent or if present, is extre- reduplicated or further subdivided. mely small. The remainder of this article deals only The features of the Nissl-stained laminar pattern with mammals and only with the neocortex. are superficial. Each layer defined in the terms given, The neocortex develops on the surface of the cere- apart from layer I, contains pyramidal and non- bral hemispheres as a series of waves of newly gener- pyramidal cells of varying types. All these cells have ated cells many of which migrate radially outward dendrites and axons that can extend into or through from the proliferative ventricular and subventricular other layers. The majority of the pyramidal cells- zones lining the primitive lateral ventricles while with somata in any layer send their apical dendrites others invade by migration from the region of the through all the supervening layers to end, commonly developing basal ganglia. The earliest arriving cells in a tuft of branched dendrites, in layer I. When form a primordial cortex which is invaded by succes- stained with the Golgi method, therefore, the lamina- sive waves of other cells. Each successive wave pushes tion of the cortex is far less clear than in a Nissl- through its predecessors and comes to lie external to stained preparation. them. In this is the beginnings of one of the overt The cerebral cortex is also laminated in terms of histological features of the neocortex: lamination. the distribution of afferent axons and of some of its Cells in a particular lamina are born during the same intrinsic axonal systems. Traditionally, these layers limited time window and aggregate together in the have been described from myelin-stained prepara- cortex. In all but the most superficial layer of the tions, but they can also be discerned in well-stained cortex of a fully developed mammal there are two Golgi and reduced silver preparations which stain major neuronal classes (and, of course, neuroglial axons and dendrites. In these preparations, a tangen- cells). The two neuronal types are called pyramidal tial fiber plexus is revealed in layer I which is conse- and nonpyramidal. Among the latter are several sub- quently called the plexiform layer. A condensation of types. The names of the cells reflect their morphology fibers in the deepest part of layer I is called the stria as seen with stains such as that of Golgi which reveal of Kaes or Bechterew (Figure 1). Horizontal plexuses the morphology of the whole cell. The lamination of of fibers in layer IV and deep in layer V are called 770 Cerebral Cortex 10 1a 1b I 1c 2 II 31 III1 32 III2 33 III3 4 IV 5a Va 5b Vb 6aa VI a 6ab 6b VI ba a VI bb 6bb Figure 1 Vogt’s scheme of the fundamental plan of cellular (left) and fiber (right) layering in the cerebral cortex. The cellular layers (I through VI) are those given in the text and Vogt divides them into sublayers. Fiber layers 4 and 5b are the bands of Baillarger; the stria of KaesBechterew, when present, is in layer 1c. From Vogt C and Vogt O (1919) Allgemeinere Ergebnisse unserer Hirnforschung. Journal of Psychology and Neurology 25: 279–462. the inner and outer bands of Baillarger. These are cortex can usually be identified in myelin prepara- probably formed primarily by intrinsic axons of the tions as thick, obliquely running fibers separate cortex (i.e., axons of some nonpyramidal cells and from the radial fasciculi (Figure 1). collateral branches of axons of pyramidal cells). The The laminar patterns seen in Nissl- and myelin- outer band of Baillarger is traditionally thought to be stained preparations vary from mammal to mammal formed by the terminal ramifications of thalamo- and across the surface of the cortex of an individual cortical axons, but this has been disputed in the visual mammalian species. The art of identifying and deter- cortex where the band is referred to as the stria of mining the boundaries of different cortical areas is Gennari and consists mainly of axons arising from known as cytoarchitectonics or myeloarchitectonics, intrinsic cortical sources. depending on whether Nissl or myelin stains are used Vertical bundles of myelinated axons extend as the basis for the delineations made. Cortical areas, through layers III to VI of the cortex, becoming many with known functional characteristics (visual, thicker as they descend and as more axons are added. auditory, motor, etc.) have cyto- and myeloarchitec- The bundles are referred to as radial fasciculi and tonic features and common differences in histochem- contain axons of pyramidal neurons as they proceed ical staining as well, that enable their borders to be to exit the cortex, and the axons of certain non- defined and a distinction to be made between them pyramidal neurons. Afferent axons coming into the and adjacent areas. The basic types of neocortex are: Cerebral Cortex 771 ‘homotypical’, found in the frontal, temporal, and corticotectal, corticostriatal, and corticothalamic fibers parietal lobes; ‘heterotypical’, divided further into to nonspecific thalamic nuclei. There are conflicting granular and agranular cortex. ‘Granular’ or ‘konio- reports about the extent to which axons to one site cortex’ is found in the sensory areas and in it there is a arise as branches of those directed to another and there predominance of small cell bodies in layers II–IV, may be species differences in the degree to which this resulting in a blurring of the borders between the occurs. Pyramidal cells of layers II and III provide most layers; in ‘agranular cortex’, found in the premotor of the axons of the corpus callosum and most of those and motor areas, layer IV disappears during devel- forming ipsilateral corticocortical connections, though opment, and layers III and V form a continuum of some callosal and ipsilateral corticocortical axons can increasing pyramidal cell somal size. In conjunction arise from pyramidal cells with somata in other layers with the changes in the Nissl staining pattern, there as well. The precise constellation of cortical and sub- are changes in the myelin staining pattern. The homo- cortical connections emanating from a cortical area typical cortex shows all the laminated plexuses, in gran- varies, with some types of connection and thus the ular cortex the bands of Baillarger predominate, and parent cell category being absent from some areas. in agranular cortex thick radial fasciculi predominate. Corticorubral fibers, for example, arise only in the With one or two exceptions, mainly in the visual motor and premotor areas. Others, such as the cortico- cortex, the pyramidal cells are the output cells of the striatal and corticopontine, probably arise in all areas. cerebral cortex, sending their axons to subcortical It is probably the variation in pyramidal cell size and targets and to other cortical areas on the same and shape related to these differential connections that opposite sides of the brain (Figure 2). To a large extent helps determine the architectonic characteristics of the pyramidal cells with somata in a particular corti- the individual cortical areas.
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