The Superior Colliculus and the Cognitive Control of Movement

Normal vision consists of an alternation of saccadic eye movements and periods of visual fixation. This is a relatively simple alternation of movement and nonmovement, but the control of this alternation involves many of the cognitive issues underlying the performance of more complex actions. The superior colliculus (SC) is a nexus in the brain system controlling these saccades and fixations, and recent experiments have shown how this structure and its cortical inputs contribute to their control. Activity on the SC movement map shows that the amplitude and direction of the impending saccade is most likely to be represented by the vector average across a large population of neurons. The control of the alternation of movement and nonmovement, which in the case of the saccadic system is the alternation of saccades and fixation, involves the balance of competition between SC neurons tonically active during visual fixation (fixation neurons) and those active long before saccades (buildup neurons). The preparation to move may be represented by the long lead or delay activity of buildup neurons because, as the probability that a saccade will be made increases, this delay activity increases. Whether the processing preceding movement initiation is discrete for each area or is distributed across areas can be answered by comparing neuronal activity in the SC with that of the neurons in frontal and parietal cortices that project to the SC. The processing is distributed with overlap between neuronal activity in cortex and SC and a shift in the SC toward movement preparation. Rapid or saccadic eye movements shift our line of sight from one part of the visual field to another and allow us to direct the higher visual acuity provided by the fovea toward successive points in the field. We make these eye movements as frequently as two times per second during such tasks as scanning the visual scene or reading. Just as important as the saccades, however, is the lack of movement between them because it is in these periods of fixation when almost all vision occurs. Thus, saccades and fixations can be regarded as an integrated system that both moves the eye rapidly to the next target and then holds the eye steadily on that target. This alternation of saccades and fixation is particularly evident during reading (figure 40.1). Even given that saccades and fixation are necessary for normal vision, why should such a relatively mechanistic system be of any relevance to cognitive neuroscience? There are at least three reasons. First, saccades are relatively simple movements, and they therefore offer the opportunity to understand a simple system within the brain for generating actions. The saccades involve rotation of each eye by the coordinated activation of only six muscles, have no variation of load—and therefore have no need for load compensation—and have no complexity introduced by the movement of joints (Robinson, 1968). These relatively simple movements do, however, involve most of the cognitive issues underlying the performance of more complex actions. For example, a saccadic eye movement to a visual stimulus requires shifting attention and selecting a target, transforming input from a sensory map to the output on a movement map, and then coordinating the appropriate muscles to execute the movement and hold the eye in the new position. Second, we have a superb animal model of the human saccadic-fixation system in the old-world monkey, which allows us to study the brain mechanisms controlling the movement. Since the introduction of the now standard techniques for recording neuronal activity from awake behaving monkeys (Evarts, 1966), the accurate recording of eye movements (Fuchs and Robinson, 1966; Judge, Richmond, and Chu, 1980), the training of monkeys to control eye movements (Fuchs, 1967), and the visual stimuli that guide them (Wurtz, 1969), the regions of the monkey brain active before visually guided saccades have been identified. The visual pathway to the striate cortex, to extrastriate areas, and then to the regions of the parietal and frontal cortices have been identified and are included in figure 40.2A. Just as the elaboration of the changes in visual processing at each step in this pathway has contributed to our understanding of the visual input on which further cognitive processing is built, the extensive understanding of the brainstem oculomotor centers for saccade generation (Hepp et al., 1989; Moschovakis and Highstein, 1994) has led to greater understanding of what output is required of cognitive ROBERT H. WURTZ, MICHELE A. BASSO, MARTIN PARÉ, and MARC A. SOMMER Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Md.