Identifying corollary discharges for movement in the primate brain

The brain keeps track of the movements it makes so as to process sensory input accurately and coordinate complex movements gracefully. In this chapter we review the brain's strategies for keeping track of fast, saccadic eye movements. One way it does this is by monitoring copies of saccadic motor commands, or corollary discharges. It has been difficult to identify corollary discharge signals in the primate brain, although in some studies the influence of corollary discharge, for example on visual processing, has been found. We propose four criteria for identifying corollary discharge signals in primate brain based on our experiences studying a pathway from superior colliculus, in the brainstem, through mediodorsal thalamus to frontal eye field, in the prefrontal cortex. First, the signals must originate from a brain structure involved in generating movements. Second, they must begin just prior to movements and represent spatial attributes of the movements. Third, eliminating the signals should not impair movements in simple tasks not requiring corollary discharge. Fourth, eliminating the signals should, however, disrupt movements in tasks that require corollary discharge, such as a double-step task in which the monkey must keep track of one saccade in order to correctly generate another. Applying these criteria to the pathway from superior colliculus to frontal eye field, we concluded that it does indeed convey corollary discharge signals. The extent to which cerebral cortex actually uses these signals, particularly in the realm of sensory perception, remains unknown pending further studies. Moreover, many other ascending pathways from brainstem to cortex remain to be explored in behaving monkeys, and some of these, too, may carry corollary discharge signals.