Pattern formation in the developing superior colliculus: ontogeny of the periodic architecture in the intermediate...

The superior colliculus of mammals contains a striking neurochemical architecture in which histochemically identifiable compartments are distributed in an iterative arrangement in the intermediate layers. We used stains for acetylcholinesterase activity as a compartment marker to trace ontogenesis of this architecture during pre- and postnatal development in the domestic cat. We found that compartmentation in the intermediate collicular layers is virtually absent at birth, and only gradually emerges during the first weeks of postnatal life. Over the same postnatal period, acetylcholinesterase activity shifts from a predominantly perikaryal expression pattern immediately postnatally to a nearly exclusive localization in the neuropil at maturity. Remarkably, a striking compartmentation of the superior colliculus was readily apparent with acetylcholinesterase histochemistry prenatally. The first appearance of a periodic architecture in the superior colliculus was observed at embryonic day 34, a time at which the collicular plate had not yet become laminated. The compartments characterized by high levels of acetylcholinesterase activity then gained in prominence until late in the prenatal period, when they receded and disappeared. The loss of the acetylcholinesterase-positive compartments in the perinatal period did not reflect a loss of compartmentation altogether. Neonatally, there was a distinct compartmental architecture visible with enkephalin immunohistochemistry. The virtual absence of acetylcholinesterase-positive compartments in the superior colliculus at birth therefore reflects developmental regulation of enzyme expression in the compartments, not regulation of the compartments as structural entities. We conclude that the periodic architecture, which characterizes the intermediate collicular layers in the adult cat, arises early in ontogenesis. These observations raise the possibility that the histochemical compartments are ontogenetic units that undergo remodeling as the superior colliculus matures.