Origin, prenatal development and structural organization of layer I of the human cerebral (motor) cortex

Summary

The composition and structural organization of layer I of the human motor cortex were studied throughout the course of prenatal cortical neurogenesis with the rapid Golgi method. The components of layer I are six. The specific afferents of layer I (primitive corticipetal fibers) and the Cajal-Retzius neurons are its essential intrinsic components, while the apical dendritic bouquets of all pyramidal neurons and the axonic terminations of all Martinotti neurons are its essential extrinsic elements. These four components are recognized throughout the entire course of prenatal cortical neurogenesis. The small neurons and terminals from afferent systems of lower cortical strata, which are incorporated into layer I late in cortical neurogenesis, represent its non-essential components. The specific afferents of layer I are the first corticipetal fibers to arrive at the developing telencephalic vesicle marking the beginning of cortical neurogenesis. These primitive fibers extend throughout the surface of the cerebral vesicle establishing an external white matter. They are considered to be the stimulus for the development and maturation of the Cajal-Retzius neurons. Together they form a primitive cortical organization, the primordial plexiform layer, which precedes the appearance of the cortical plate and is considered to be common to and shared by amphibians, reptiles and mammals including man. Layer I evolves from this primordial cortical lamination. The Cajal-Retzius neurons are all characterized by a single descending axonic process which becomes a long horizontal (tangential) fiber in the lower half of layer I. Although the body and main dendrites of these neurons are only found at strategic and old cortical regions (e.g. the motor, acoustic and visual areas) their long horizontal axons extend, anteroposteriorly, throughout the entire surface of the cerebral cortex and establish synaptic connections with the apical dendrites of all pyramidal neurons regardless of location, cortical depth or functional role.

In the course of cortical development, all developing pyramidal neurons ascend through the cortical plate in order to establish primary synaptic contacts with layer I. Only then, do they become ready to be displaced downward by the arrival of the next set of migrating neuroblasts. All pyramidal neurons of the cerebral cortex are actually suspended from layer I anchored to it by their apical dendritic bouquets. The need for all pyramidal neurons to reach and establish original synaptic connections with layer I could explain the remarkable ‘inside-out’ formation of the cortical plate. This fact could also explain the characteristic shape of these neurons, as well as their abundance, structural uniformity and universal radial orientation to layer I. The functional role of layer I seems to be the spreading of the same kind of primitive information to all pyramidal neurons of the cerebral cortex whether they be motor, sensory, acoustic, visual or associational in nature, or whether they be large or small.

The observations presented in this study further corroborate the concept of the dual origin of the mammalian cerebral cortex. The study emphasizes the important role played by layer I in the overall organization of the cerebral cortex. It proposes that in the course of cortical neurogenesis all future pyramidal neurons are attracted to layer I where they establish original synaptic connections and all receive from it the same kind of primitive information needed for their maturation. There seems to be no obvious reason to believe that the original synaptic contacts established between all pyramidal neurons and layer I disappear in the course of cortical neurogenesis. On the contrary, the progressive growth of the apical dendritic bouquets within layer I seems to indicate that they actually expand.