Structural organization of the human cerebral cortex prior to the appearance of the cortical plate

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Abstract
The early development and the structural organization of the human cerebral cortex, prior to the appearanc of the cortical plate (Carnegie stage 22, ca. 54 days), was studied in two embryos: 43 (stage 18) and 50 day old (stage 20), respectively. It has been shown that the human cerebral cortex begins its ontogenetic development around the sixth rather than around the eighth week of gestation as it has been previously assumed. The human cerebral cortex starts to develop soon after the cerebral vesicles have been formed (stage 15) and a primitive internal capsule has been established (stage 17, ca. 41 days). By stage 18 of human development fibres from this primitive internal capsule have reached and probably have penetrated into the developing cerebral vesicle, through its more superficial zone. Fibres from this primitive internal capsule have been traced backward through the ventral thalamus to the mesencephalic tegmentum. The possible existence of primitive ascending fibres from the mid-brain which terminate in the superficial zone of the developing cerebral cortex (tegmento-thalamostriato-cortical tract) is suggested. The arrival of these primitive corticipetal fibres establishes in the outer zone of the cerebral cortex a primordial plexiform lamina or an external white matter. Horizontal-bipolar cells (embryonic Cajal-Retzius neurons) begin to differentiate by stage 18 of human development (43 days in our case). By stage 20 (50 days in our case), the primordial plexiform lamina is well established, extends throughout the entire surface of the developing cerebral cortex, and is considered to be functionally active. It is, by this age, a superficial, 40 μm thick, complex fibrillar neuronal organization composed of numerous horizontal corticipetal fibres (demonstrable with silver methods), horizontal-bipolar Cajal-Retzius neurons and a few other, less defined, cellular elements. This primordial plexiform lamina is considered to represent a primitive “premammalian” cortical organization. The next event in cortical ontogenesis is the appearance of the cortical plate or the mammalian neocortical grey at stage 22 (ca. 54 days). Migrating neuroblasts attracted toward the preexisting primordial plexiform lamina and guided by glial fibres start to accumulate within it. The appearance of the mammalian neocortical grey divides the primordial plexiform lamina into a superficial plexiform or layer I (external white matter) and a deep plexiform or layer VII (subplate zone). Layer I is considered to play a significant role in the overall structural organization of the cerebral cortex by controlling the migration of all its pyramidal neurons. In cortical ontogenesis the mammalian neocortical grey (cortical plate) will only give rise to layers VI, V, IV, III and II of the adult cerebral cortex. These observations further corroborate the concept of the dual origin, composition and nature of the mammalian cerebral cortex including that of man. They also demonstrate that the human cerebral cortex starts to develop much earlier than was previously thought.