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Introduction: To reorient gaze (the eye's direction in space) towards a target is an overdetermined problem, as infinitely many combinations of eye- and head movements can specify the same gaze-displacement vector. Yet, behavioral measurements show that the primate gaze-control system selects a specific contribution of eye- and head movements to the saccade, which depends 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 thus determined by the neural firing rates. The recordings also indicated that the latter is modulated by the initial eye position. 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 in gaze control. Methods: 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. Moreover, the downstream eye- and head burst generators were taken to be linear, as our earlier work had indicated that much of the non-linear main-sequence kinematics of saccadic eye movements may be due to neural encoding at the collicular level, rather than at the brainstem. Results and discussion: We investigate how 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. [ABSTRACT FROM AUTHOR]

IntroductionTo reorient gaze (the eye’s direction in space) towards a target is an overdetermined problem, as infinitely many combinations of eye- and head movements can specify the same gaze-displacement vector. Yet, behavioral measurements show that the primate gaze-control system selects a specific contribution of eye- and head movements to the saccade, which depends 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 thus determined by the neural firing rates. The recordings also indicated that the latter is modulated by the initial eye position. 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 in gaze control.MethodsHere, 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. Moreover, the downstream eye- and head burst generators were taken to be linear, as our earlier work had indicated that much of the non-linear main-sequence kinematics of saccadic eye movements may be due to neural encoding at the collicular level, rather than at the brainstem.Results and discussionWe investigate how 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.

Tight coupling between eye and head movements has been observed in response to a single visual target offset. On this basis, when the visual stimulus consists of two successive steps in the same (horizontal) direction, either increasing in eccentricity (staircase) or decreasing in eccentricity (pulse-step) gaze should be due to concomitant eye and head angular displacement. That is, the eyes and head should aim at each target displacement so that their combined movement matches target offset. We have tested this hypothesis in five healthy subjects. The measured variables were head and gaze offset, the interval between two consecutive saccades from onset to onset (I) and the response delay between onset of the second step and onset of the first gaze saccade (D). With both staircase and pulse-step stimuli, the eye saccade preceded the head movement, and the gaze response either had the stimulus profile pattern or consisted of one gaze saccade to the final target offset. In response to staircase stimuli, I decreased concomitantly with an increase in D; with pulse-step stimuli, as D increased, I decreased slightly in three subjects and decreased markedly in two subjects. Dissociation between the eye and head movements could clearly be demonstrated with pulse-step stimuli: the first gaze saccade to the target pulse displacement was accompanied by a head movement to the target step offset. We also observed cases in which the gaze saccade to the target step displacement was made simultaneously with the head movement to the target pulse offset. Our study extends previous observations in head fixed condition and illustrates that in the majority of cases, when the head is free and a visual pulse step stimulus is presented, both the saccadic and head systems have the ability to modify or cancel the initial neural command to move to the first target displacement. When this modification takes place in only one system, eye and head movements are dissociated. [ABSTRACT FROM AUTHOR]

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., (© 2019 Elsevier B.V. All rights reserved.)