Dynamic Control of Eye-Head Gaze Shifts by a Spiking Neural Network Model of the Superior Colliculus

To reorient gaze (the eye in space) towards a target can be achieved by infinitely many combinations of eye- and head movements. However, behavioral measurements show that the primate gaze-control system selects specific contributions of eye- and head to the saccade, which depend on the initial eye-in-head orientation. Single-unit recordings in the primate superior colliculus (SC) during head-unrestrained gaze shifts have further suggested that cells may encode the instantaneous trajectory of a desired straight gaze path in a feedforward way by the total cumulative number of spikes in the neural population, and that the instantaneous gaze kinematics are determined by the neural firing rates. The recordings also indicated that the latter depended strongly on the initial eye position as well. We recently proposed a conceptual model that accounts for many of the observed properties of eye-head gaze shifts and on the potential role of the SC. Here, we extend and test the model by incorporating a spiking neural network of the SC motor map, the output of which drives the eye-head motor control circuitry by linear cumulative summation of individual spike effects of each recruited SC neuron. We propose a simple neural mechanism on SC cells that explains the modulatory influence of feedback from an initial eye-in-head position signal on their spiking activity. The same signal also determines the onset delay of the head movement with respect to the eye. The downstream eye- and head burst generators were taken to be linear, as our earlier work had suggested that much of the nonlinear kinematics of saccadic eye movements may be due to neural encoding at the collicular level, rather than at the brainstem. We show that the spiking activity of the SC population drives gaze to the intended target location within a dynamic local gaze-velocity feedback circuit that yields realistic eye- and head-movement kinematics and dynamic SC gaze-movement fields.