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

Abstract

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.