Dynamic control of eye-head gaze shifts by a spiking neural network model of the superior colliculus

Abstract

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.

Neural encoding of instantaneous kinematics of eye-head gaze shifts in monkey superior Colliculus

“…Figure 1b presents a possible scheme for eye-head gaze control by the SC population (after 65 ). Behavioral studies have shown that eyes and head are both driven by their own goals: an oculocentric gaze error for the eye vs. a craniocentric error for the head 14 , 66 , which requires feedback from an eye-in-head position signal (red arrows in Fig.…”

Neural Control of Instantaneous Kinematics of Eye-Head Gaze Shifts in Monkey Superior Colliculus

“…Figure 1B illustrates a possible extension of the model in Fig. 1A to eye-head gaze control by the SC population (after Alizadeh and Van Opstal, 2022b). Behavioral studies have shown that eyes and head are both driven by their own goals: an oculocentric gaze error for the eye, vs. a craniocentric error for the head (Goossens and Van Opstal, 1997;Freedman and Sparks, 2000).…”

“…Recenty, we proposed a quantitative model for the SC and the downstream control circuits for the eyes and head that can account for these behaviors (Kasap and Van Opstal, 2018;Van Opstal and Kasap, 2019;Alizadeh and Van Opstal, 2022b).…”

Neural Control of Instantaneous Kinematics of Eye-Head Gaze Shifts in Monkey Superior Colliculus

“…Recenty, we proposed a quantitative model for the SC and the downstream control circuits for the eyes and head that accounts for these behaviors (Kasap and Van Opstal, 2018;Van Opstal and Kasap, 2019;Alizadeh and Van Opstal, 2022b). The major novelty of our model with respect to earlier proposals (Laurutis and Robinson, 1986;Guitton and Volle, 1987;Guitton, 1992;Galiana and Guitton, 1992;Goossens and Van Opstal, 1997;Freedman, 2001;Kardamakis et al, 2010;Sağlam et al, 2011;Daye et al, 2014) resides in the assumed role of the midbrain Superior Colliculus (SC) in the control of gaze shifts.…”