Neural control of eye-head coordination during orienting movements: The role of the primate superior colliculus

Movements which change the direction of the line of sight can be made up of movements of the eyes, head, and body. The extent to which each of these mobile segments contributes to orienting gaze shifts depends upon the amplitude and direction of the desired movement, the relative mobility of the structures involved in the movement, and upon their initial positions. In non-primates, microstimulation of the superior colliculus (SC) has implicated this structure in the control of combined eye-head gaze shifts. In contrast the results of microstimulation and single unit recording in the primate SC has led to very different conclusions; the primate SC was generally thought to be involved only in the control of saccadic eye movements. Two head unrestrained rhesus monkeys were trained to make gaze shifts to visual targets. An analysis of these movements revealed several factors which influenced the coordination of the eyes and head: (1) the initial positions of the eyes in the orbits; and (2) the amplitude of the vertical component of the gaze shift. In addition, several conditions were identified in which the relative contributions of the eye, head and gaze components of coordinated gaze shifts were separable. This dissociation of eye, head and gaze movement components allowed differential predictions about the role of the primate SC in the control of orienting movements to be tested. The results of both microstimulation and single unit recording in the primate SC indicate that a signal of desired gaze displacement is derived from the locus of the active population of cells. In addition, the effects of systematically varying the parameters of microstimulation indicate that the SC generates two distinct signals. A level independent signal of the desired gaze displacement is derived from the locus of activity. A level dependent signal derived from the level of SC activity can influence the velocity of gaze shifts without affecting the signal of desired displacement