Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study

The three-dimensional structural organization of layer I of the developing and adult human cerebral cortex has been investigated by using sagittal, transverse, and tangential rapid Golgi and Klüver-Barrera preparations. The actual morphology of its fundamental neuron--the Cajal-Retzius cell (C-R)--is established. These large and solitary cells are horizontal multipolar neurons characterized by: (1) long horizontal dendrites that radiate in all directions within a tangential plane parallel to the pial surface, (2) long horizontal axonic collaterals that radiate in all directions within layer I middle level, and (3) a descending axonic process that reaches the lower level, becomes a long tangential fiber--and eventually a myelinated one--and projects in any direction within this level. In cortical ontogenesis, its dendrites, axonic collaterals and terminal axon undergo a progressive multipolar "horizontalization" extending throughout the surface of the expanding cerebral cortex. The neuron's body and main dendrites will be found only in some areas, whereas its axonic collaterals and terminal tangential axon should be found throughout the cerebral cortex. This developmental feature explains the presence of two--middle and lower--plexuses in layer I, composed of the axonic collaterals and the terminal tangential axons of C-R cells, respectively. It is emphasized that the basic morphology of the C-R cell remains essentially unchanged in the course of cortical ontogenesis and that the neuron persists in the adult cerebral cortex. Whereas the C-R cell is the basic neuron of layer I, the pyramidal cells dendritic bouquets represent its larger and main receptive surface (the only one early in development). By the 30th week of gestation, a C-R cell could establish: (1) proximal contacts, through its axonic collaterals, with all dendritic bouquets within a approximately 350 microns radius, and (2) distant contacts, through its tangential axon, with dendritic bouquets within a narrow sagittal, transverse, or diagonal territory several mm long. In cortical ontogenesis, the C-R cells' functional territories continue to expand throughout the surface of the cerebral cortex and possibly overlap with each other. It is proposed that the C-R cell receives inputs from primitive (mesencephalic?) corticipetal fibers and that it transmits the same kind of information (perhaps a basal tone?) to the dendritic bouquets of all pyramidal neurons throughout the cerebral cortex regardless of their location, cortical depth, or functional role.