Gradients of cellular maturation and synaptogenesis in the superior colliculus of the fetal rhesus monkey.

Light (LM) and electron microscopic (EM) qualitative and quantitative analyses were employed to determine the tempo and spatial gradients of synaptogenesis and cellular differentiation in the superficial superior colliculus (SC) of the rhesus monkey between embryonic (E) days E47 and E84. By E47, a majority of the neurons of the prospective superficial gray layer (SGS) have arrived at their final positions and contribute to a uniform band of small, darkly Nissl-stained neurons at the outer surface of the SC. By E54, cells in the middle of the rostral pole of the superficial SC become considerably larger, paler staining, and less densely packed than the more medially or laterally located cells. These regional differences, which extend posteriorly through about the middle of the SC at this age, are evident on both the LM and EM levels and were confirmed by a quantitative EM analysis of the cytodifferentiation and synaptogenesis in the SGS. Several overlapping EM probes made across the medial, middle, and lateral regions of the SGS at each of three coronal levels reveal consistently more developed neuropil and smaller amounts of extracellular space in the middle region than in the medial and lateral portions of the more anterior SC. Further, the densities of synapses, both in terms of synapses/micron2 of total cross-sectional area and synapses/micron2 of neuropil alone, are also higher in the middle than the peripheral regions. Most of the middle-peripheral differences found in the mid-E50s are still evident by the early E60s, but have disappeared by midgestation (E80s). The present results are interpreted to indicate that the middle region of the SGS at a given transverse level begins to mature significantly earlier than the medial or lateral areas. Since our previous 3H-thymidine analysis (Cooper and Rakic, '81a) failed to reveal significant regional variation in the time of neuron origin in the superficial SC, the observed spatiotemporal gradients of neuronal maturation in the primate SGS probably do not arise from underlying gradients of cellular proliferation.