Dual origin of the mammalian neocortex and evolution of the cortical plate

Abstract

A Golgi study of the structural organization of the early developmental stages of the cerebral cortex of the cat has been presented. It has been demonstrated that the structural organization of the mammalian neocortex undergoes a series of fundamental transformations in the course of its early embryonic development. A clear understanding of these early structural changes is essential to comprehend the multi-layered nature of the mammalian cerebral cortex. In order of appearance the following basic transformations have been recognized in mammalian cortical ontogenesis. A. The first recognizable change in the undifferentiated neuroepithelial structure of the cerebral vesicle is the arrival and penetration of corticipetal fibers through its superficial region. The penetration of these afferent fibers into the cerebral vesicle forms a clear plexiform region under the pial surface just above the matrix zone. This clear plexiform region corresponds to the classical marginal zone and is composed, at first, of corticipetal fibers and their collaterals. B. The arrival of these corticipetal fibers induces maturation of some neurons. Primitive-looking and still-developing neurons begin to appear scattered among the afferent fibers without forming any distinct lamination. This combination of an external white matter of afferent fibers with scattered neurons among the fibers has been named the primordial plexiform layer of the mammalian cerebral cortex. Its structure represents a primitive type of nervous organization which is reminiscent of the amphibian brain. In mammalian cortical ontogenesis this primitive plexiform layer has a short duration and it is established as a distinct structure prior to the appearance of the cortical plate. C. The appearance and the formation of the cortical plate within the primordial plexiform layer results in the separation of its neurons and fibers into a superficial and a deep plexiform lamination. Structural and functional interrelationships soon start to develop between the neuronal elements of the superficial and the deep plexiform laminations establishing the primordial neocortical organization, which is characterized by specific types of neurons and fibers. Its structural organization resembles somewhat that of the cerebral cortex of some reptiles. It is important to emphasize that the neurons and fibers of this primordial neocortical organization persist and become components of the adult cerebral cortex. The superficial plexiform becomes layer I and the deep lamination becomes layer VII of the adult mammalian cerebral cortex. Therefore, the cortical plate represents the primordium of only layers VI, V, IV, III, and II of the adult cerebral cortex. The cortical plate is considered to be a distinct mammalian structure of a more recent phylogenetic origin. D. The last significant transformation consists of the sequential growth and maturation of the cortical plate which follows an "inside-out" progression. The maturation of the neurons of the cortical plate and hence the formation of its laminations seems to be due to the sequential and progressive arrival of corticipetal fibers which takes place during the late embryonic stages of development. According to these observations the mammalian cerebral cortex has a double origin and a possible dual nature. A new interpretation of the basic structural organization of the mammalian neocortex based primarily on this dual nature is introduced and analyzed in this communication. It proposes new ideas concerning the origin, the embryonic development, and the phylogenetic evolution of the mammalian cerebral cortex which differ somewhat from the classical conceptions of cortical development. © 1978 Springer-Verlag.