Gaze control in the cat: studies and modeling of the coupling between orienting eye and head movements in different behavioral tasks

Abstract

1. Orienting movements, consisting of coordinated eye and head displacements, direct the visual axis to the source of a sensory stimulus. A recent hypothesis suggests that the CNS may control gaze position (gaze = eye-relative-to-space = eye-relative-to-head + head-relative-to-space) by the use of a feedback circuit wherein an internally derived representation of gaze motor error drives both eye and head premotor circuits. In this paper we examine the effect of behavioral task on the individual and summed trajectories of horizontal eye- and head-orienting movements to gain more insight into how the eyes and head are coupled and controlled in different behavioral situations. 2. Cats whose heads were either restrained (head-fixed) or unrestrained (head-free) were trained to make orienting movements of any desired amplitude in a simple cat-and-mouse game we call the barrier paradigm. A rectangular opaque barrier was placed in front of the hungry animal who either oriented to a food target that was visible to one side of the barrier or oriented to a location on an edge of the barrier where it predicted the target would reappear from behind the barrier. 3. The dynamics (e.g., maximum velocity) and duration of eye- and head-orienting movements were affected by the task. Saccadic eye movements (head-fixed) elicited by the visible target attained greater velocity and had shorter durations than comparable amplitude saccades directed toward the predicted target. A similar observation has been made in human and monkey. In addition, when the head was unrestrained both the eye and head movements (and therefore gaze movements) were faster and shorter in the visible- compared with the predicted-target conditions. Nevertheless, the relative contributions of the eye and head to the overall gaze displacement remained task independent: i.e., the distance traveled by the eye and head movements was determined by the size of the gaze shift only. This relationship was maintained because the velocities of the eye and head movements covaried in the different behavioral situations. Gaze-velocity profiles also had characteristic shapes that were dependent on task. In the predicted-target condition these profiles tended to have flattened peaks, whereas when the target was visible the peaks were sharper. 4. Presentation of a visual cue (e.g., reappearance of food target) immediately before (less than 50 ms) the onset of a gaze shift to a predicted target triggered a midflight increase in first the eye- and, after approximately 20 ms, the head-movement velocity.(ABSTRACT TRUNCATED AT 400 WORDS)

Vestibulo-Ocular Reflex Suppression during Head-Fixed Saccades Reveals Gaze Feedback Control

“…Importantly, we also found that gaze remained accurate despite the head perturbations, even though the VOR was suppressed. These findings are compatible with a series of models that suggest that the brain uses feedback control of gaze trajectory, and not eye trajectory to change the line of sight (Laurutis and Robinson, 1986;Guitton and Volle, 1987;Pelisson et al, 1988;Guitton et al, 1990;Tomlinson, 1990;Lefèvre and Galiana, 1992;Goossens and Van Opstal, 1997;Daye et al, 2014). Our results imply further that the passively induced VOR is modulated by a gaze rather than an eye velocity signal.…”

“…Despite the modification of the saccade trajectory, the gaze ended on target, demonstrating feedback control that compensates for the perturbation. Two possibilities have been proposed for the control of head-free saccades: either the CNS controls the gaze trajectory with feedback (Laurutis and Robinson, 1986;Guitton and Volle, 1987;Pelisson et al, 1988;Guitton et al, 1990;Tomlinson, 1990;Lefèvre and Galiana, 1992;Goossens and Van Opstal, 1997;Daye et al, 2014), or it controls the eye and the head separately without gaze feedback (Freedman, 2001(Freedman, , 2008Freedman and Cecala, 2008;Kardamakis and Moschovakis, 2009;Kardamakis et al, 2010). A separate control of eye and head based on a prior decomposition of the gaze command, with no feedback of the gaze and an imperfect VOR, could not compensate for the head perturbation be- cause the eye controller would have no information about how the perturbation might have affected gaze.…”

Evidence for on-line visual guidance during saccadic gaze shifts

“…The ¢ring rates of the tectoreticular spinal neurons (TR(S)Ns), which are found in the deep layers of the SC, are thought to encode gaze as opposed to eye or head movements alone (Munoz & Guitton 1991). Munoz & Guitton (1989) and Guitton et al (1990) discovered that the appearance of a visual target just prior to a gaze movement caused a sudden increase in the orientating TR(S)N discharge frequency and a modi¢cation in the acceleration of the subsequent gaze movement. This alteration in the acceleration of the gaze started ca.…”

Human eye-head coordination in two dimensions under different sensorimotor conditions

“…However, it was proposed, on the basis of gaze control studies in the cat, that both the oculomotor system and the head motor system are controlled by the same internally created gaze motor-error signal (Galiana and Guitton 1992; Guitton et al 1990). Several behavioural and neurophysiological studies provide support for this so-called common gaze model (reviewed by Guitton 1992).…”

“…According to the common drive hypothesis, the eye and head are both controlled by the same oculocentric gazeerror command (Galiana and Guitton 1992; Guitton et al 1990). Thus, both motor systems are expected to move in similar directions throughout the gaze saccade.…”