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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.

Neurons in the superior colliculus (SC) are organized as maps of visual and motor space. The companion paper showed that muscimol injections into intermediate layers of the SC alter the trajectory of the movement and confirmed previously reported effects on latency, amplitude, and speed of saccades. In this paper we analyze the pattern of these deficits across the visual field by systematically comparing the magnitude of each deficit throughout a grid of targets covering a large fraction of the visual field. We also translate these deficits onto the SC map of the visual/movement fields to obtain a qualitative estimate of the extent of the deficit in the SC. We found a consistent pattern of substantially increased saccadic latency to targets in the contralateral visual hemifield, accompanied by slight and inconsistent increases and decreases for saccades to the ipsilateral hemifield. The initial and peak speed of saccades was reduced after the injection. The postinjection amplitude of the saccades were either hypometric or normometric, but rarely hypermetric. Although errors in the initial direction of the postinjection saccades were small, they consistently formed a simple pattern: an initial direction with minimal errors (a null direction) separating regions with clockwise and counterclockwise rotations of the initial direction. However, the null direction did not go through the center of the inactivated zone, as would be expected if the SC alone were determining saccade direction, e.g., with a population code. One hypothesis that can explain the misalignment of the null direction with the lesion site is that another system, acting in parallel with the SC, contributes to the determination of saccadic trajectory.

During oblique saccades, the durations of the horizontal and vertical components are stretched until they are approximately equal. Models of the saccadic system have been proposed that provide a mechanism for that stretching. However, they fail to simulate the pattern of activity recorded from premotor medium lead burst neurons (MLBNs) in the brain stem. A new model of the saccadic system is proposed that accounts for both the component stretching of oblique movements and the pattern of activity recorded in MLBNs. MLBNs that project to horizontal (or vertical) motoneurons actually have a wide span of on-directions (the direction associated with the largest discharge) around the cardinal direction. We infer from the wide span of their on-directions that, at the level of individual MLBNs, the vectorial signal present in spatially organized structures (e.g., the superior colliculus) is not decomposed into the separate horizontal and vertical components represented by the motoneurons. Nonetheless, all prior models of the saccadic system have decomposed the vectorial premotor command into horizontal and vertical commands at the level of the MLBNs. That decomposition was explicit, because individual MLBNs, with a sine- or cosine-shaped directional tuning curve, were used. We propose here that the decomposition into horizontal and vertical commands is carried out only at the level of the motoneurons. This decomposition is implicit, because no single MLBN encodes the horizontal or vertical command; the command only exists implicitly in the activity of the population of MLBNs. The new vectorial burster model correctly simulates the pattern of activity recorded in primate MLBNs, and the components of its oblique saccades are stretched. Two mechanisms contribute to this stretching: the distribution of MLBN tuning curves and the inhibition exerted by the contralateral population of MLBNs. In contrast, feedback control of the saccade contributes negligibly to the stretching. Even though the vectorial burster model predicts a component stretching, it is not constrained to produce perfectly straight oblique saccades because no trajectory control is implemented. The amount of curvature depends on the similarity of the horizontal and vertical systems (both neural and mechanical). In this model, stretching is interpreted simply as a side effect of the properties of the MLBNs' tuning curves. The distributed MLBNs of the vectorial burster model forces the general organization of the saccadic system to be reconsidered. We propose that a distributed architecture in which several different neural systems cooperate is needed.

Recent models have placed the superior colliculus inside the local feedback loop that generates the pulse of innervation needed to make a saccade. Such closed-loop models need to take into account the different coordinate systems of visual and motor signals. This paper presents a computational model showing how the superior colliculus can bring the visual and motor information together in a common reference frame.

Recent experiments on the cat and monkey have revealed several different cell types within the superior colliculus, including fixation, burst, and build up cells. During primate saccades, activity remains fixed at one location in burst cells, but spreads across the colliculus in build up cells. New models based on the activity of these cell types suggest their functional roles in saccade generation.

1. The locus of activity within the superior colliculus (SC) is related to the desired displacement of the eye. Current hypotheses suggest that the location of this locus of activity determines the amplitude of the saccade and that the level of activity at this locus determines eye velocity. We present evidence that suggests that, although the locus determines the amplitude of the saccade, the level of activity in the colliculus encodes dynamic motor error (the difference between desired and current eye displacement). 2. We categorized 86 neurons in the intermediate and deep layers of the superior colliculus of two rhesus monkeys by their activity in relation to the end of saccadic eye movements. In 36% of the cells (n = 31), activity was completely cut off by the end of the saccade (clipped cells). For 53% of cells (n = 46), the major burst of activity ceased by the end of the saccade, but activity continued for 30-100 ms after the end of the movement (partially clipped cells). The remaining 10% of the cells (n = 9) had no clear burst of activity (unclipped cells) but rather had activity that increased gradually before the saccade and then slowly decreased for up to 100 ms after the saccade. These categories were part of a continuum of cell types rather than discrete classes of cells. 3. We first determined whether this new categorization of cells revealed a special relation between the discharge of clipped and partially clipped cells and saccadic amplitude and peak velocity. As expected, we found a steady increase in spike count as saccadic amplitude increased up to the center of the movement field, and an increase in peak spike discharge as peak velocity increased up to a maximum radial eye velocity. Variability in the cell discharge was substantially greater than the variability of saccadic amplitude or peak velocity. We concluded that these single point or averaged measures did not reveal any new functional relationship of these cells. 4. We then examined the relationship of the temporal pattern of discharge of clipped and partially clipped cells to instantaneous changes in radial error and radial velocity. There was a monotonic decay in spike discharge with declining radial error. In contrast, there was a complex, multivalued relationship between spike discharge and radial velocity; collicular cells produced two different values of spike discharge for the same velocity, one during acceleration and the other during deceleration of the eye during a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

Studies of the intermediate layers of the superior colliculus have suggested that it provides a desired change in eye position signal (delta E) for the generation of saccadic eye movements. Recent evidence, however, has shown that some neurons in these layers may be related to the velocity of saccades. We present single cell recordings from the intermediate layers of monkey superior colliculus that are consistent with the hypothesis that many superior colliculus neurons provide instead a motor error signal, em. Our hypothesis about the function of these cells places them inside the local feedback loop controlling the waveform of the saccade.