The mammalian superior colliculus: laminar structure and connections

Abstract

The superior colliculus is a laminated midbrain structure that acts as one of the centers organizing gaze movements. This review will concentrate on sensory and motor inputs to the superior colliculus, on its internal circuitry, and on its connections with other brainstem gaze centers, as well as its extensive outputs to those structures with which it is reciprocally connected. This will be done in the context of its laminar arrangement. Specifically, the superficial layers receive direct retinal input, and are primarily visual sensory in nature. They project upon the visual thalamus and pretectum to influence visual perception. These visual layers also project upon the deeper layers, which are both multimodal, and premotor in nature. Thus, the deep layers receive input from both somatosensory and auditory sources, as well as from the basal ganglia and cerebellum. Sensory, association, and motor areas of cerebral cortex provide another major source of collicular input, particularly in more encephalized species. For example, visual sensory cortex terminates superficially, while the eye fields target the deeper layers. The deeper layers are themselves the source of a major projection by way of the predorsal bundle which contributes collicular target information to the brainstem structures containing gaze-related burst neurons, and the spinal cord and medullary reticular formation regions that produce head turning.

Introduction

The superior colliculus (SC) is a laminated structure sitting astride the midbrain of the vertebrate brainstem, where it is strategically placed to receive incoming sensory information and to direct brainstem activity. Its primary function is to direct the sensory structures of the head towards objects of interest. In primates, where the foveated eye has become the predominant sensory structure, visual sensory input is the primary drive for the SC, and its outputs primarily direct the line of gaze by initiating saccadic movements of the eyes and orienting movements of the head. In general, the importance of a sensory system for a species is reflected in the density of terminals conveying this modality to the SC; e.g., rats have more trigeminotectal connections than monkeys. In addition, the SC often acts to direct the ears or whiskers, where these sensory structures are important mobile sensory receivers. In some species, the collicular signals may also be used to direct the mouth, either in obtaining food or for defense (rat: Redgrave et al., 1996b). Collicular signals may even be used to direct the limbs at targets (cat: Iwamoto, 1990; monkey: Werner et al., 1997). In conjunction with physically directing gaze at a target through its descending projections, the SC also plays a role in redirecting attention toward analysis of said target through its ascending projections. Finally, the SC has a less well understood role under conditions where an object is perceived to be a threat. In this case, other collicular systems may orient the animal away from the threat. The emphasis of this review¹ of collicular connections will be on collicular gaze control, particularly in commonly used mammalian species. Nevertheless, it should not be forgotten that numerous species specializations exist, and that this core collicular function is not its sole one.