The mosaic architecture of the superior colliculus

The superior colliculus is a midbrain structure serving visual, multisensory and sensorimotor processing. Throughout various collicular layers, visual afferents are linked together with afferents related to other sensory modalities as well as with afferents from sources not easily subsumed under the term 'sensory'. These inputs are orchestrated in a topographic fashion and led to premotor neurons that are important elements in generating saccadic eye movements and orientation movements of other kinds. Using immunocytochemical techniques to chart the distribution of various substances serving neurotransmission and neuromodulation, it was found that many of them, e.g. acetylcholinesterase (AChE), choline acetyltransferase, the enkephalins, substance P, and parvalbumin, relate to repetitive structural islands, or modules, in the superior colliculus. From studies on the distribution of three further neuroactive substances in rat superior collicular tissue: the calcium binding protein calretinin, the growth and plasticity related protein neuromodulin (GAP-43), and a glutamate receptor of the NMDA-type, we were led to conclude (1) that the intermediate layers of the superior colliculus are composed not of two, but of at least three disjunct types of modules, (2) that not just the intermediate layers but more or less the whole superior colliculus is an assemblage of modules, and (3) that, besides topographic connectivity and laminar structuring, the modules constituting an iterative partitioning represent a third major feature of superior collicular architecture. The origin of the collicular mosaic is considered under an evolutionary perspective, and a hypothesis is presented stating that the pattern of AChE-rich modules on the level of the multimodal collicular layers can be predicted from retinal ganglion cell topography.