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The neocortex

An overview of its evolutionary development, structural organization and synaptology

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Abstract

By way of introduction, an outline is presented of the origin and evolutionary development of the neocortex. A cortical formation is lacking in amphibians, but a simple three-layered cortex is present throughout the pallium of reptiles. In mammals, two three-layered cortical structures, i.e. the prepiriform cortex and the hippocampus, are separated from each other by a six-layered neocortex. Still small in marsupials and insectivores, this “new” structure attains amazing dimensions in anthropoids and cetaceans. Neocortical neurons can be allocated to one of two basic categories: pyramidal and nonpyramidal cells. The pyramidal neurons form the principal elements in neocortical circuitry, accounting for at least 70% of the total neorcortical population. The evolutionary development of the pyramidal neurons can be traced from simple, “extraverted” neurons in the amphibian pallium, via pyramid-like neurons in the reptilian cortex to the fully developed neocortical elements designated by Cajal as “psychic cells”. Typical mammalian pyramidal neurons have the following eight features in common: (1) spiny dendrites, (2) a stout radially oriented apical dendrite, forming (3) a terminal bouquet in the most superficial cortical layer, (4) a set of basal dendrites, (5) an axon descending to the subcortical white matter, (6) a number of intracortical axon collaterals, (7) terminals establishing synaptic contacts of the round vesicle/asymmetric variety, and (8) the use of the excitatory aminoacids glutamate and/or aspartate as their neurotransmitter. The pyramidal neurons constitute the sole output and the largest input system of the neocortex. They form the principal targets of the axon collaterals of other pyramidal neurons, as well as of the endings of the main axons of cortico-cortical neurons. Indeed, the pyramidal neurons constitute together a continuous network extending over the entire neocortex, justifying the generalization: the neocortex communicates first and foremost within itself. The typical pyramidal neurons represent the end stage of a progressive evolutionary process. During further development many of these elements have become transformed by reduction into various kinds of atypical or aberrant pyramidal neurons. Interestingly, none of the six morphological characteristics, mentioned above under 1–6, has appeared to be unassailable; pyramidal neurons lacking spines, apical dendrites, long axons and intracortical axon collaterals etc. have all been described. From an evolutionary point of view the typical pyramidal neurons represent not only the principal neocortical elements, but also the source of various excitatory local circuit neurons. The spiny stellate cells, which are abundant in highly specialized primary sensory areas, form a remarkable case in point. In these elements only two of the six original pyramidal attributes, i.e. spiny dendrites and an intracortical axonal arbor, are retained. The nonpyramidal neurons display a diverse morphology, but share a number of important morphological and functional features: (1) their dendrites bear only a few spines or none, (2) their axons do not leave the cortex, (3) their terminals make synapses of the flat vesicle/symmetric variety, (4) they use the inhibitory neurotransmitter GABA, and (5) almost all types make synaptic contacts with pyramidal neurons. Several subclasses of nonpyramidal neurons are selectively immunoreactive for particular calcium-binding proteins. The widely held notion that the pyramidal neurons constitute the relatively constant basic framework of the cortex, whereas the local circuit neurons are variable and increase during phylogenetic development in number as well as in diversity is untenable. A survey is presented of the structure, synaptology and chemodifferentiation of the various neocortical cell types, allocating them to three groups: pyramidal neurons, excitatory interneurons and inhibitory interneurons. The synaptic relations of the various neocortical neurons are pictorially summarized in two microcircuitry diagrams, which together form the pièce de résistance of the present treatise. The various approaches to the structure of the neocortex are discussed. It is emphasized that correlative structural, ultrastructural and electrophysiological studies of pyramidal neurons known to project to a given cortical or subcortical target form a promising field of interdisciplinary research.

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  1. Rudolf Nieuwenhuys

    Present address: , Papehof 25, NL-1391, BD Abcoude, The Netherlands

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  1. Department of Anatomy and Embryology, University of Nijmegen, P.O. Box 9101, NL-6500, HB Nijmegen, The Netherlands

    Rudolf Nieuwenhuys

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Dedicated to the memory of Hendrik van der Loos.

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Nieuwenhuys, R. The neocortex. Anat Embryol 190, 307–337 (1994). https://doi.org/10.1007/BF00187291

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