Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades

Abstract

1. The behavior of the combined eye-head gaze saccade mechanism was investigated in the rhesus monkey under both normal circumstances and in the presence of perturbations delivered to the head by a torque motor. Animals were trained to follow a target light that stepped at regular intervals through an angle of 68 degrees (+/- 34 degrees with respect to the midsagittal plane). Thus all primary saccades were center crossing. On randomly occurring trials the torque motor was pulsed so as to perturb the trajectory of the head, thus allowing us to assess both the functional state of the vestibuloocular reflex (VOR) and the effects of such perturbations on gaze saccade accuracy (gaze is defined as the sum of eye-in-head plus head-in-space, and a gaze saccade as a combined eye-head saccadic gaze shift). 2. Gaze shifts can be divided into two discrete sections: the portion during which the gaze angle is changing (the saccadic portion), and the portion during which the gaze is stationary but the head continues to move (the terminal head-movement portion). For the system to accurately acquire eccentric targets, at least two criteria must be met: 1) the saccadic portion must be accurate, and 2) the compensatory eye movement that occurs during the terminal head-movement portion must be equal and opposite to the head movement, thereby maintaining gaze stability. Perturbations delivered during the terminal head-movement portion of the gaze shift indicated that VOR was functioning normally, and thus we concluded that the compensatory eye movements that accompany head movements were vestibular in origin. 3. As reported previously, during the saccadic portion of large-amplitude gaze saccades, the VOR ceases to function. In spite of this observation, the accuracy of the gaze saccade is not affected by perturbations delivered to the head. Gaze accuracy is maintained both by changing the duration of the saccadic portion and by altering the head trajectory. 4. Because rhesus monkeys often make very rapid head movements (1,200 degrees/s), we wished to discover the velocity range over which the monkey VOR might be expected to operate. Accordingly, in a second series of experiments, VOR function was assessed during passive whole-body rotations with the head fixed. By the use of spring-assisted manual rotations, peak velocities up to 850 degrees/s were achieved. When VOR gain was measured during such rotations, it was found to be equal to 0.9 up to the maximum velocities used.(ABSTRACT TRUNCATED AT 400 WORDS)

Premotor Correlates of Integrated Feedback Control for Eye–Head Gaze Shifts

“…2 A, gray traces). As observed previously, perturbed gaze shifts remained accurate following head perturbations ( p ϭ 0.46; paired t test, matched perturbed vs control trials) (Laurutis and Robinson, 1986;Guitton and Volle, 1987;Tomlinson, 1990;Tabak et al, 1996;Cullen et al, 2004) Importantly, the applied transient head perturbations did not completely interrupt the gaze shift (i.e., gaze velocity was not driven to zero velocity for a sustained time interval). Rather, they modified ongoing gaze shifts in two critical ways: (1) gaze shift durations increased significantly ( p Ͻ 0.05) (Fig.…”

“…This has been a controversial issue with respect to eye-head coordination during gaze shifts, and two general classes of models had been proposed to account for the available data: gaze feedback models (Tomlinson 1990;Galiana and Guitton, 1992;Goossens and Van Opstal, 1997) and separate feedback models (Phillips et al, 1995;Freedman, 2001;Sparks et al, 2002). In the first class of models, gaze accuracy is maintained by comparing the desired change in gaze position with the actual gaze displacement, which is calculated from feedback of the ongoing eye and head movements.…”

Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity

“…Gaze saccades, composed of coordinated eye-head movements, may be driven by a gaze-position error (GPE) signal (GPE ϭ desired minus current gaze positions) produced by a comparator within a neurally encoded feedback loop (Laurutis and Robinson, 1986;Guitton and Volle, 1987;Pélisson et al, 1988Pélisson et al, , 1995Tomlinson, 1990;Coimbra et al, 2000;Guitton et al, 2004;Choi and Guitton, 2006;Sylvestre and Cullen, 2006). Feedback assures accuracy by driving gaze until GPE ϭ 0, a process that compensates for variability in the trajectories of the eye-in-head and head-onbody platforms.…”

“…In cat, to show that the hill of activity is moved by feedback, we perturbed gaze shifts (Matsuo et al, 2004) by mechanically braking head movements, a procedure that mimics the natural occurrence of variable transient loads to the head (Laurutis and Robinson 1986;Guitton and Volle, 1987;Tomlinson, 1990;Choi and Guitton, 2006;Sylvestre and Cullen, 2006). We use the same approach here in monkey to show short-latency responses on the map to gaze trajectory perturbations and a gaze saccade amplitude-dependent moving hill.…”

Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

“…Coordinated eye-head movements are made during everyday activities to rapidly redirect the axis of gaze between two targets of interest (humans: André-Deshays et al 1988;Barnes 1979;Guitton and Volle 1987;Pélisson et al 1988;Zangemeister and Stark 1982a,b, and monkeys: Bizzi et al 1971, 1972Dichgans et al 1973;Freedman and Sparks 1997;Lanman et al 1978;Morasso et al 1973;Tomlinson 1990;Tomlinson and Bahra 1986a,b). When the head is immobilized, gaze is redirected by high-velocity saccadic movements for which the relationship between gaze shift amplitude and eye velocity as well as movement duration is predictable (Bahill et al 1975;Baloh et al 1975;Van Gisbergen et al 1984).…”