Linear visuomotor transformations in midbrain superior colliculus control saccadic eye-movements

It is well established that a localized population of neurons in the motor map of the midbrain superior colliculus (SC) drives a saccadic eye-head gaze shift. However, there is controversy as to how the brainstem saccade burst generators decode the SC activity. We focus on eye-movement generation by comparing two competing schemes from the recent literature that are both supported by neurophysiological evidence: the vector-averaging scheme versus the vector summation model. Whereas the former contains at least four nonlinearities to explain visuomotor planning and saccade execution, the latter relies predominantly on linear operations. We have demonstrated that the summation model accounts for the nonlinear main sequence of saccade kinematics, and predicted that this results from a spatial gradient in temporal burst profiles of SC cells: rostral cells have higher peak-firing rates and shorter burst durations than caudal cells. Yet, the number of spikes in their saccade-related bursts is identical. In contrast, the averaging model does not predict such activity profiles. We now also show that by incorporating the concept of predictive remapping in the spatial updating of saccade sequences, the phenomenon of target averaging in double-stimulation experiments, and the occurrence of goal-directed, but highly curved saccades in the double-step paradigm, can all be explained by the same linear summation mechanism. We argue that the linear model is more in line with neurophysiological data, while relying on fewer ad-hoc assumptions than the nonlinear vector-averaging scheme.