The relationship between the geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex

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Abstract
To study the prenatal development of connections between the lateral geniculate nucleus (LGN) and the primary visual cortex in the cat, we have examined the relationship between the position of ingrowing afferents from the LGN and their target cells in cortical layers 4 and 6 at various times during the cat''s 65 d gestation period and during the first 3 weeks of postnatal life. In 1 series of experiments, the method of transneuronal transport of intraocularly injected tritiated proline (3H-proline), followed by autoradiography, was used to label the developing geniculocortical pathway. In another series, the tritiated thymidine (3H-thymidine) method was employed to keep track of the cells destined for layers 4 and 6 by labeling them on their birthdates (layer 4: embryonic day (E) 37-43; layer 6: E31-36) (Luskin and Shatz, 1985b) and then charting their locations at subsequent times during development. The results of the 2 sets of experiments were compared at corresponding ages. By E39, many of the cells of cortical layer 6 have completed their migrations and are situated within the cortical plate immediately above the subplate. However, the transneuronal labeling pattern indicates that the geniculocortical afferents have not yet arrived within the vicinity of the future visual cortex, but rather are still en route and confined within the optic radiations of the telencephalon. By E42, a week after the first afferents can be detected in the radiations, substantial transneuronal label is found in the subplate immediately below future visual cortex. However, the overlying cortical plate is free of label. Over the next 2 weeks, geniculocortical axons continue to accumulate in the subplate zone, and, in addition, transneuronal label can be found in the marginal zone. By E55 a faint geniculocortical projection can be detected within the cortical plate, but only within its deeper half (future layers 5 and 6), and even then the major portion of the projection is still confined to the subplate. The absence of a projection to cortical layer 4 at these ages is remarkable in view of the results from our 3H-thymidine experiments, which indicate that by E57 the majority of cells destined to belong to layer 4 have already completed their migrations and assumed positions superficial to the cells of layers 5 and 6. By birth, a substantial geniculocortical projection to cortical layer 4 can be detected in the transneuronal autoradiographs. The cortex is nevertheless very immature with regard to the organization of its afferent input and the laminar arrangement of its constituent cells. 3H-Thymidine studies show that the majority of cells destined for the most superficial cortical layers (layers 2 and 3) have not yet completed their pialwards migrations and instead are still en route through the deeper cortical layers. Neurons belonging to layers 2 and 3 do not assume their final positions within the cortex until about 3 weeks postnatal, and it is just at this time that the segregation of the geniculocortical afferents into the system of ocular dominance columns in layer 4 commences (LeVay et al., 1978). These observations indicate that while the geniculocortical afferents arrive within the telencephalon in the vicinity of the visual cortex early in development, they undergo a prolonged period of waiting in the subplate and only invade their target cortical layers once the neurons comprising those layers have completed their migrations and assumed their final relative positions within the cortex.