Cortical and subcortical contributions to saccade latency in the human brain

An important property of our motor system is the ability to either perform or inhibit an automatic goal-directed reaction. Imagine, for example, how easily we can catch a ball, while at the same time we would never grasp a stinging insect approaching us. The oculomotor system provides a good model to study this ability. Monkey midbrain superior colliculus neurons are responsible for automatic visually evoked saccades, whereas the frontal eye fields can prevent reflexive glances. Little is known about human superior colliculus or the competition between the midbrain and frontal areas controlling saccades. In the present functional magnetic resonance study we used the gap paradigm, where a stimulus fixated with the eyes is removed 200 ms prior to saccade target onset. Subjects were required to either look at the target or prevent an eye movement. From what is known from non-human primate neurophysiology, it is expected that the gap will result in enlarged neuronal activity in the human superior colliculus, disinhibiting the oculomotor system and enhancing automatic reactions. Importantly, we demonstrate that the human superior colliculus homologue is indeed activated by the removal of a fixation target, in either task. The frontal eye fields show a reverse pattern when saccades were suppressed. Furthermore, magnitude of responses in the superior colliculus correlated negatively with saccade latency, and in the frontal eye fields positively. These findings confirm for the first time that the human superior colliculus generates automatic goal-directed saccades, whereas the frontal eye fields can exert volitional control over automatic orienting.