Cytogenesis in the monkey retina

Abstract

Time of cell origin in the retina of the rhesus monkey (Macaca mulatto) was studied by plotting the number of heavily radiolabeled nuclei in autoradiograms prepared from 2‐ to 6‐month‐old animals, each of which was exposed to a pulse of 3 H‐thymidine (3 H‐TdR) on a single embryonic (E) or postnatal (P) day. Cell birth in the monkey retina begins just after E27, and approximately 96% of cells are generated by E120. The remaining cells are produced during the last (∼ 45) prenatal days and into the first several weeks after birth. Cell genesis begins near the fovea, and proceeds towards the periphery. Cell division largely ceases in the foveal and perifoveal regions by E56. Despite extensive overlap, a class‐specific sequence of cell birth was observed. Ganglion and horizontal cells, which are born first, have largely congruent periods of cell genesis with the peak between E38 and E43, and termination around E70. The first labeled cones were apparent by E33, and their highest density was achieved between E43 and E56, tapering to low values at E70, although some cones are generated in the far periphery as late as E110. Amacrine cells are next in the cell birth sequence and begin genesis at E43, reach a peak production between E56 and E85, and cease by E110. Bipolar cell birth begins at the same time as amacrines, but appears to be separate from them temporally since their production reaches a peak between E56 and E102, and persists beyond the day of birth. Müller cells and rod photoreceptors, which begin to be generated at E45, achieve a peak, and decrease in density at the same time as bipolar cells, but continue genesis at low density on the day of birth. Thus, bipolar, Müller, and rod cells have a similar time of origin. The maximal temporal separation of cell birth is between cones and amacrine cells so that cell generation exhibits two relatively distinct phases: the first phase gives rise to ganglion, horizontal, and cone cells, and the second phase to amacrine, bipolar, rod, and Müller cells. In addition, cells of the first phase are generated faster than the second phase cells, and there are differences in the topography of spread of labeled cells between the two phases. Each cell class displays a central‐to‐peripheral gradient in genesis, although the spatiotemporal characteristics of the gradients differ between the classes. Heavily labeled ganglion cells, horizontal cells, and cone photoreceptors (phase 1) are found near the retinal margin much sooner than amacrine, bipolar, Müller, and rod photoreceptor cells (phase 2). As a consequence, genesis of phase 1 cells generally occurs over a more extensive retinal area, extending to the retinal margin, while phase 2 cell genesis ceases centrally by the time cell birth begins near the margin. The site of initial cessation of cell division is more variable than it is for the beginning of cytogenesis, although for all cell classes it is roughly centered on the fovea.