Maps and sensorimotor transformations for eye-head gaze shifts: Role of the midbrain superior colliculus

Single-unit recordings in head-restrained monkeys indicated that the population of saccade-related cells in the midbrain Superior Colliculus (SC) encodes the kinematics of desired straight saccade trajectories by the cumulative number of spikes. In addition, the nonlinear main sequence of saccades (their amplitude-peak velocity saturation) emerges from a spatial gradient of peak-firing rates of collicular neurons, rather than from neural saturation at brainstem burst generators. We here extend this idea to eye-head gaze shifts and illustrate how the cumulative spike-count in head-unrestrained monkeys relates to the desired gaze trajectory and its kinematics. We argue that the output of the motor SC is an abstract desired gaze-motor signal, which drives in a feedforward way the instantaneous kinematics of ongoing gaze shifts, including the strong influence of initial eye position on gaze kinematics. We propose that the neural population acts as a vectorial gaze pulse-generator for eye-head saccades, which is subsequently decomposed into signals that drive both motor systems in appropriate craniocentric reference frames within a dynamic gaze-velocity feedback loop.