The modern era of oculomotor research began with the advent of the chronic single-unit recording method in the late 1960s. Research carried out in the intervening years has made it possible to provide a detailed description of the saccadic command signals that are generated by motor neurons and the formation of these signals in premotor brainstem regions. These findings have been assimilated in control-systems models that simulate important behavioural features of saccades. Despite these great advances, key issues, such as the nature of the feedback signal and the location of the comparator, are unresolved and some of the factors that have impeded progress can be identified.

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The brainstem control of saccadic eye movements

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)

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

The behavior of the vestibulo-ocular reflex at high velocities of head rotation.

In this paper, we report a detailed study of the dynamic properties of horizontal, vertical and oblique saccades. These eye movements were measured with an improved version of the double-magnetic induction method in two rhesus monkeys. We found that onsets of orthogonal components of oblique saccades are so well synchronized in the monkey that a common initiation system seems likely. Saccade vectors obeyed a nonlinear peakvelocity/amplitude relationship in all directions. The peak-velocity/duration/amplitude relationship for components was not fixed, but depended on the relative size of the orthogonal component: for a component with a given size, its duration increased and its peak velocity decreased, as the saccade vector to which it contributed turned away from the component direction under consideration. This stretching effect, which reflects a nonlinearity in the system, was negligible for small saccade vectors but became very pronounced in large oblique saccades. These experimental data were confronted with quantitative predictions derived from two different models for the generation of saccades in two dimensions. It appears that a model which assumes the existence of synchronized, but otherwise independent, pulse generators for horizontal and vertical components must be rejected. An alternative model, featuring a nonlinear vectorial pulse generator followed by a decomposition stage which generates component velocity command signals from the vectorial eye velocity signal, provides good fit with the data. According to this common-source model, the two nonlinear phenomena observed, viz., the curvilinear peak-velocity/amplitude relationship of saccades in all directions and component stretching in large oblique saccades, are due to a single nonlinearity in the proposed vectorial pulse generator. A possible neural basis for the common-source model is discussed.

Experimental test of two models for the generation of oblique saccades

The objective of these experiments was to determine whether the trajectories of the horizontal and vertical components of oblique saccades in primates were coupled. Human and monkey eye movements were recorded during a visual tracking task that jumped a small visible target spot to different locations on a tangent screen. For oblique saccades larger than ca. 3 deg, there was coupling between the horizontal and vertical components so that the duration of the smaller component was longer ("stretched") than would have been expected from its amplitude-duration relationship. The duration of a stretched component of an oblique saccade was linearly related to the vector amplitude of the eye movement but not to the amplitude of the stretched component. Stretched components of oblique saccades had lower peak and average velocities than would have occurred with pure horizontal or vertical saccades of the same size. Decreased component velocity was not caused by low-velocity eye movement components inserted at the beginning or end of the saccade, but was a function of the saccade's direction and component amplitude. For any saccade, there was a linear relationship between peak and average component velocity. We compared the discharge of monkey abducens neurons with the characteristics of the on-direction horizontal components of oblique saccades. The burst duration of an abducens neuron was lengthened when the horizontal component of an oblique saccade was stretched. Intraburst firing frequency was also decreased in correspondence with a decrease in horizontal component velocity. For an oblique saccade, the duration of the neuron's burst was correlated with the duration of the horizontal component and with the vector amplitude of the saccade, but was not correlated with the amplitude of the horizontal component itself. The duration of the smaller component of an oblique saccade was proportional but not always equal to the duration of the larger component. Usually, the smaller component began later and ended earlier than the larger component. These results show that the horizontal and vertical components of oblique saccades are coupled centrally so that the velocity of the smaller component is decreased and its duration is increased. For oblique saccades, larger than ca. 3 deg, amplitude-duration and amplitude-velocity relationships based on pure horizontal or vertical saccade data are not applicable. These findings are discussed in relation to three recently proposed models of coupled saccadic burst generators.

Oblique saccadic eye movements of primates.

Oblique saccades of the cat: A comparison between the durations of horizontal and vertical components

A comparison between saccades and quick phases of vestibular nystagmus in the cat.

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Oblique saccades of the cat: A comparison between the durations of horizontal and vertical components

A comparison between saccades and quick phases of vestibular nystagmus in the cat.