1. The ability of the central nervous system to compensate for saccadic dysmetria was demonstrated in rhesus monkeys. The behavior of this adaptive mechanism after cerebellar ablations was examined. 2. Monkeys were trained to fixate small target lights. Eye movements were monitored while the animals were seated, with their heads fixed, in a rotating magnetic field. The horizontal recti muscles of one eye were weakened by tenectomy. Saccades made by this weakened eye were hypometric and followed by postsaccadic drift. 3. When the patch was switched so that the weak eye was viewing, the hypometric saccades made by the weak eye gradually became larger, until after 3 days they were essentially orthometric. This indicated that the central nervous system could compensate for a peripheral weakness. 4. The tenectomy operation reduced the strength of the muscles, creating hypometria, and upset the ratio of viscosity to elasticity in the orbit, creating postsaccadic drift in the weak eye. The innervation required to make a saccade has both phasic and tonic components, the so-called pulse and step. The sacccadic repair mechanism increased both the pulse and the step to compensate for the hypometria and also adjusted the ratio of the pulse to the step to eliminate postsaccadic drift. 5. Total cerebellectomies were performed on two monkeys, each of which had one tenectomized eye. These ablations created an enduring saccadic hypermetria and postsaccadic drift in the unoperated eye of both animals. The total cerebellectomy abolished all adaptive repair of the saccadic system. 6. Partial cerebellectomies were performed on two monkeys, each of which had one tenectomized eye. Lesions of the vermis and paravermis (lobes IV-IX) and the fastigial nuclei created an enduring saccadic hypermetria without postsaccadic drift in the unoperated eye of both animals. These lesions abolished adaptive control of the pulse of innervation. Adaptive changes in the step of innervation still occurred, so that postsaccadic drift was always eliminated in the experienced, viewing eye. Thus the midline cerebellum (vermis, paravermis, and fastigial nuclei) appears to be important for repair of saccadic dysmetria, but not for repair of postsaccadic drift. Additional evidence that postsaccadic retinal slip cannot be compensated for in flocculectomized monkeys suggest that the adaptive control of the step may depend on the flocculus. 7. After cerebellar lesions the monkeys were able to make saccades of all amplitudes and directions. The principal deficit in these animals seemed to be that the pulse and step of innervation were no longer appropriate to the target displacement. We conclude that the cerebellum's principal contribution to saccadic eye movements is the adjustment of the gains of the pulse- and step-generating mechanisms. Hence this study supports the hypothesis that repair of dysmetria is a general function of the cerebellum.

1. We recorded eye movements in four normal human subjects during refixations between targets calling for various combinations of saccades and vergence. We confirmed and extended prior observations of 1) transient changes in horizontal ocular alignment during both pure horizontal saccades (relative divergence followed by relative convergence) and pure vertical saccades (usually divergence for upward and convergence for downward saccades); 2) occasional, high-frequency (20-25 Hz), conjugate oscillations along the axis orthogonal to the main saccade; and 3) the speeding up of horizontal vergence by both horizontal and vertical saccades. 2. To interpret these findings, we developed a hypothesis for the generation of vergence to step changes in target depth, both with and without associated saccades. The essential features of this hypothesis are 1) the transient changes in horizontal ocular alignment during pure horizontal saccades reflect asymmetries in the mechanical properties of the lateral and medial rectus muscles causing adduction to lag abduction; 2) pure vergence movements in response to step changes in target depth are generated by a neural network that uses a desired change in vergence position as its input command and instantaneous vergence motor error (the difference between the desired change and the actual change in vergence) to drive vergence premoter neurons; and 3) the facilitation of horizontal vergence by saccades arises from nonlinear interactions in central premotor circuits. 3. The hypothetical network for generating pure vergence to step changes in target depth is analogous in structure to the local feedback model for the generation of saccades and has the same conceptual appeal. With the assumption of a single nonlinearity describing the relationship between a vergence motor error signal and the output of the neurons that generate promoter vergence velocity commands, this model generates pure vergence movements with peak velocity-amplitude relationships and trajectories that closely match those of experimental data. 4. Several types of models are proposed for the central, nonlinear interaction that occurs when saccades and vergence are combined. Common to all models is the idea that omnidirectional pause neurons (OPN), which are thought to gate activity for saccade burst neurons, also gate activity for saccade-related vergence. In one model we hypothesize the existence of a separate class of saccade-related vergence burst neurons, which generate premotor horizontal vergence commands but only during saccades. In a second model we hypothesize separate right eye and left eye saccadic burst neurons that receive not only conjugate, but also equal but oppositely directed vergence error signals.(ABSTRACT TRUNCATED AT 400 WORDS)

The ocular following responses elicited by brief unexpected movements of the visual scene were studied in 10 rhesus monkeys. Test patterns were either random dots or sine-wave gratings [spatial frequency (Fs) 0.046-1.06 cycles per degree (c/degree)]. Test stimuli were velocity steps [speed (V) 5-400 degrees/s] of 100-ms duration, applied 50 ms after spontaneous saccades to avoid saccadic intrusions. Eye velocity response profiles were nonmonotonic and idiosyncratic, but consistent and closely time-locked to stimulus onset. Two measures of response amplitude were used: initial peak in eye velocity (ei), and average final eye velocity over the period of 110-140 ms measured from stimulus onset (ef). Using random dot patterns, response latencies were short, e.g., when the criterion for onset was an eye acceleration of 100 degrees/s2, mean latency (+/- SE) for eight monkeys with a 40 degrees/s test ramp was 51.5 +/- 0.6 ms. Using gratings of low spatial frequency (Fs less than 0.5 c/degree), latency was inversely related to, and solely a function of, contrast and temporal frequency, Ft (where Ft = V X Fs). We conclude from the latter that ocular following is triggered by local changes in luminance, and propose a model of the detection mechanism that reproduces all the essential features of these data. Moderate low-pass spatial filtering ("blurring") of the random dot pattern, by interposing a sheet of ground glass between the animal and the scene, progressively increased the response latency and decreased ef, but ei was either little affected or increased. When used with gratings, the ground glass simply reduced the contrast (range: 0.5-0.003), with very similar consequences for ocular following: latency increased and ef decreased, but ei changed little over the first decade of contrast reduction, increased over the second, and began to show attenuation (often pronounced) only at the lowest contrast. We suggest that these anomalous increases in ei with reductions in contrast are secondary to the delay in response onset and might be explained if the motion detectors responsible for triggering ocular following act as a gate for integrated retinal slip inputs to the tracking system proper: the delay in detection causes a buildup in the error signal driving the tracking response. En masse movement of the visual field was not the optimal stimulus for ocular following.(ABSTRACT TRUNCATED AT 400 WORDS)

Experimental evidence indicates that the superior colliculus (SC) is important but neither necessary nor sufficient to produce accurate saccadic eye movements. Furthermore both clinical and experimental evidence points to the cerebellum as an indispensable component of the saccadic system. Accordingly, we have devised a new model of the saccadic system in which the characteristics of saccades are determined by the cooperation of two pathways, one through the SC and the other through the cerebellum. Both pathways are influenced by feedback information: the feedback determines the decay of activity for collicular neurons and the timing of the activation for cerebellar neurons. We have modeled three types of cells (burst, buildup, and fixation neurons) found in the intermediate layers of the superior colliculus. We propose that, from the point of view of motor execution, the burst neurons and the buildup neurons are not functionally distinct with both providing a directional drive to the brain stem circuitry. The fixation neurons determine the onset of the saccade by disfacilitating the omnipause neurons in the brain stem. Excluding noise-related variations, the ratio of the horizontal to the vertical components of the collicular drive is fixed throughout the saccade (i.e., its direction is fixed); the duration of the drive is such that it always would produce hypermetric movements. The cerebellum plays three roles: first, it provides an additional directional drive, which improves the acceleration of the eyes; second, it keeps track of the progress of the saccade toward the target; and third, it ends the saccade by choking off the collicular drive. The drive provided by the cerebellum can be adjusted in direction to exert a directional control over the saccadic trajectory. We propose here a control mechanism that incorporates a spatial displacement integrator in the cerebellum; under such conditions, we show that a partial directional control arises automatically. Our scheme preserves the advantages of several previous models of the saccadic system (e.g., the lack of a spatial-to-temporal transformation between the SC and the brain stem; the use of efference copy feedback to control the saccade), without incurring many of their drawbacks, and it accounts for a large amount of experimental data.