Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study

Summary

The neocortex of the cat undergoes a series of fundamental transformations of its fibrillar-neuronal organization during the course of early prenatal cortical ontogenesis. Some of these transformations assume structural chracteristics and neuronal features which resemble those of phylogenetically older cortical organizations. Following the arrival of corticipetal fibers at the marginal zone of the cerebral vesicle a very primitive neocortical organization, the primordial plexiform layer develops. It is characterized by the external location of the white matter with both corticipetal and a few corticofugal fibers and a few immature neurons sandwiched between the fibers. The primitive plexiform layer is present in the cat from the 20th to the 25th day of gestation. The external (superficial) location of the white matter of the primordial plexiform layer of the cat neocortex is reminiscent of the amphibian cortical organization. It also resembles other primitive structures (spinal cord) of the central nervous system. In view of its short duration and because of the immaturity of its fibrillar-neuronal elements, the primordial plexiform layer is considered to be a transient neocortical organization possibly without functional activity in the cat.

The appearance of the cortical plate (25th day of gestation) causes the subdivision of the primordial plexiform layer into an outer and an inner zone. The outer zone becomes layer I and the inner zone layer VI of the neocortex. Both of these layers remain as such throughout cortical development. From the 25th to the 45th day of gestation the fibrillarneuronal structure of layers I and VI develop while the cortical plate grows, passively, by the progressive addition of new cells. The progressive fibrillar-neuronal organization of layers I and VI and the development of structural and functional interactions between them constitutes the primordial neocortical organization of the cerebral cortex of the cat. It is characterized by a superficial (layer I) and a deep (layer VI) plexiform layer composed predominantly of collaterals from the corticipetal fibers arriving at the developing cortex and by three basic types of neurons. The horizontal neurons of layer I with descending axons terminating in layer VI, and the Martinotti neurons of layer VI with ascending axons terminating in layer I, are associative neurons. The large stellate neurons of layer VI are projective neurons. The axons of these cells before entering the white matter send ascending recurrent collaterals to layer I. The fibrillar-neuronal organization of the neocortex during this gestational period (primordial neocortical organization) resembles the organization of the reptilian neocortex. It is postulated that the primordial neocortical organization of the cat is functionally active during this gestational period.

The arrival of new types of afferent fibers at the lower region of the cortical plate (45th day of gestation) causes the maturation of the pyramidal neurons of this region of the neocortex. These neurons are recognized at this age as the pyramidal neurons of layer V of the neocortex of the cat. The appearance of these afferent fibers and the maturation of the pyramidal neurons of layer V marks the transformation of the neocortex from its primitive reptilian structure into a distinctly mammalian organization. It is postulated that the cortical plate (pyramidal plate) is a recent addition in neocortical phylogeny representing a mammalian transformation. An analogy seems to exists among the pyramid-like neurons of the amphibian cortex, the pyramid-like neurons of the reptilian neocortex and the pyramid-like neurons (stellate) of layer VI of the mammalian neocortex. This analogy differs from the classical one postulated by Cajal which includes the pyramidal neurons of the mammalian neocortex, which are here considered as recent additions to neocortical phylogeny and hence as distinct mammalian neurons.