Genesis of the dorsal lateral geniculate nucleus in the rhesus monkey: Site and time of origin, kinetics of proliferation, routes of migration and pattern of distribution of neurons

Abstract

Autoradiograms of the dorsal lateral geniculate body (LGd) in 2‐ to 3‐ month‐old rhesus monkeys, each of which had been exposed to a pulse of H 3‐thymidine (H 3‐TdR) on a specified embryonic (E) or early postnatal (P) day displayed heavily labeled neurons only in animals injected at E36, E38, E40 and E43. In animals exposed to H 3‐TdR during the last four months of gestation or after birth, the LGd contained only an occasional labeled glial cell. In the monkey, therefore, all neurons destined for the LGd are generated during 8 to 9 days at the end of the first quarter of the 165‐day gestational period. An examination of embryos injected with H 3‐TdR around E40 and killed one hour later showed that cells destined for the LGd are generated in two distinct proliferative tiers situated near the surface of the third ventricle. The inner 100‐to 150‐μ‐wide tier consists of pseudostratified columnar cells and corresponds to the ventricular zone. The outer, somewhat narrower tier has cytological features characteristic of the subventricular zone; this zone has not been described previously in the developing diencephalon. It was estimated that the approximately 1.7 × 10 6 neurons that will comprise the fully developed LGd on one side are derived from about 22,000 precursor neurons that are present in the proliferative sector on the corresponding side of the developing diencephalon at E35. The proliferative pool increase 10‐fold in cell number by E41 and becomes exhausted during E44. The number of postmitotic cells leaving the proliferative pool increases exponentially from 2,500 at E36 to a maximum of 350,000 at E43, and then sharply declines to zero by E45. Analysis of embryos exposed to H 3‐TdR around E40 and sacrificed 3, 7, 14 or 42 days later indicate that following their last cell division, young neurons migrate laterally 500–700 μm to the outer aspect of the developing thalamus. Migrating neurons are deployed in distinct cellular fascicles that span the developing diencephalon from the surface of the third ventricle tot he pial surface. Several generations of neurons generated in a restricted location of the germinal zone (proliferative unit) appear to migrate along a single cellular fascicle and accumulate in a column‐shaped aggregate. Neurons generated earliest reach the outermost surface of the diencephalon; neurons generated later accumulate at progressively more inner positions and hence form an “outside‐to‐inside” gradient. The axis of the “outside‐to‐inside” gradient initially oriented latero‐medially later becomes oriented ventro‐dorsally. Thus, in the mature monkey, early generated neurons lie in the ventral magnocellular layers, whereas neurons generated later become part of the dorsal parvocellular layers. Despite these tectogenetic changes, the relationships between early and late generated neurons derived from the same proliferative unit remain preserved and eventually may establish a single “projection column.”