Analysis of the step response of the saccadic feedback: system behavior

We used prolonged stimulation of the monkey superior colliculus to elicit staircase eye movements. By changing the parameters of the stimulating current we were able to obtain movements with different dynamics. An increase in the current frequency resulted in the shortening of the intersaccadic interval and a decrease of the amplitudes in the staircase. In cases of high stimulation, after an initial saccade of fixed metrics, the eyes moved in an apparently smooth fashion. The movement was conjugate and in the same direction as the first saccade. By analyzing the velocity trace we found that the movement consisted of a chain of small saccades, each of which started before the previous one ended. We conducted a quantitative analysis of the staircase movements including the cases of apparently smooth movement of the eyes. We conclude that all of the movements elicited by prolonged SC stimulation were generated by the saccadic feedback circuitry. The dynamic profiles of the elicited movements changed continuously with the stimulating current parameters. On one end of the continuum we observed the classically described staircase movements with individual movements separated in time. On the other end of the continuum we saw the apparent smooth movement as the limit case produced by high stimulation of the SC.     

Stimulation of the caudate nucleus induces contraversive saccadic eye movements as well as head turning in the cat.

The effects of stimulation of the caudate nucleus were investigated in alert cats, with special reference to the induction of eye and head movements. Stimulation of caudal portions of the caudate nucleus on one side with trains of current pulses induced gaze shifts towards the contralateral side. When the head of the animal was restrained, the majority of evoked eye movements were single conjugate saccades. The amplitude and direction of the evoked saccade varied depending on the initial eye position. The amplitude of the horizontal component tended to be larger for saccades initiated from more ipsilateral positions, and became gradually smaller as the initial eye position shifted to the contralateral side. If the eye was far into the contralateral positions, no saccades were induced. Furthermore, the saccades tended to have a downward component when the eye was initially focused upward, and an upward component when the eye was focused downward. When the head was made free to move, the same stimulation induced a sequence of contraversive staircase gaze shifts composed of coordinated eye and head movements. The eye movements in the orbit resembled nystagmus, consisting of contraversive saccades followed by reverse compensatory movements. The head turning, though smooth and continuous, was also suggested to consist of a series of movements coupled with saccadic eye movements. This study indicates a potential role of the caudate nucleus in the control of orienting reflexes.     

Smooth eye movements evoked by electrical stimulation of the cat's superior colliculus

Head-fixed gaze shifts were evoked by electrical stimulation of the deeper layers of the cat superior colliculus (SC). After a short latency, saccades were triggered with kinematics similar to those of visually guided saccades. When electrical stimulation was maintained for more than 150–200 ms, postsaccadic smooth eye movements (SEMs) were observed. These movements were characterized by a period of approximately constant velocity following the evoked saccade. Depending on electrode position, a single saccade followed by a slow displacement or a staircase of saccades interspersed by SEMs were evoked. Mean velocity decreased with increasing deviation of the eye in the orbit in the direction of the movement. In the situation where a single evoked saccade was followed by a smooth movement, the duration of the latter depended on the duration of the stimulation train. In the situation where evoked saccades converged towards a restricted region of the visual field (goal-directed or craniocentric saccades), the SEMs were directed towards the centre of this region and their mean velocity decreased as the eye approached the goal. The direction of induced SEMs depended on the site of stimulation, as is the case for saccadic eye movements, and was not modified by stimulation parameters (place code). On the other hand, mean velocity of the movements depended on the site of stimulation and on the frequency and intensity of the current (rate code), as reported for saccades in the cat. The kinematics of these postsaccadic SEMs are similar to the kinematics of slow, postsaccadic correction observed during visually triggered gaze shifts of the alert cat. These results support the hypothesis that the SC is not exclusively implicated in the control of fast refixation of gaze but also in controlling postsaccadic conjugate slow eye movements in the cat.     

Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey

Recent work has shown that humans and monkeys utilize both retinal error and eye position signals to compute the direction and amplitude of saccadic eye movements (Hallett and Lightstone 1976a, b; Mays and Sparks 1980b). The aim of this study was to examine the role the frontal eye fields (FEF) and the superior colliculi (SC) play in this computation. Rhesus monkeys were trained to acquire small, briefly flashed spots of light with saccadic eye movements. During the latency period between target extinction and saccade initiation, their eyes were displaced, in total darkness, by electrical stimulation of either the FEF, the SC or the abducens nucleus area. Under such conditions animals compensated for the electrically induced ocular displacement and correctly reached the visual target area, suggesting that both a retinal error and eye position error signal were computed. The amplitude and direction of the electrically induced saccades depended not only on the site stimulated but also on the amplitude and direction of the eye movement initiated by the animal to acquire the target. When the eye movements initiated by the animal coincided with the saccades initiated by electrical stimulation, the resultant saccade was the weighted average of the two, where one weighing factor was the intensity of the electrical stimulus. Animals did not acquire targets correctly when their eyes were displaced, prior to their intended eye movements, by stimulating in the abducens nucleus area. After bilateral ablation of either the FEF or the SC monkeys were still able to acquire visual targets when their eyes were displaced, prior to saccade initiation, by electrical stimulation of the remaining intact structure. These results suggest that neither the FEF nor the SC is uniquely responsible for the combined computation of the retinal error and the eye position error signals.     

Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey

The synaptic organization of the saccade-related neuronal circuit between the superior colliculus (SC) and the brainstem saccade generator was examined in an awake monkey using a saccadic, midflight electrical-stimulation method. When microstimulation (50–100 A, single pulse) was applied to the SC during a saccade, a small, conjugate contraversive eye movement was evoked with latencies much shorter than those obtained by conventional stimulation. Our results may be explained by the tonic inhibition of premotor burst neurons (BNs) by omnipause neurons that ceases during saccades to allow BNs to burst. Thus, during saccades, signals originating from the SC can be transmitted to motoneurons and seen in the saccade trajectory. Based on this hypothesis, we estimated the number of synapses intervening between the SC and motoneurons by applying midflight stimulation to the SC, the BN area, and the abducens nucleus. Eye position signals were electronically differentiated to produce eye velocity to aid in detecting small changes. The mean latencies of the stimulus-evoked eye movements were: 7.9±1.0 ms (SD; ipsilateral eye) and 7.8±0.9 ms (SD; contralateral eye) for SC stimulation; 4.8±0.5 ms (SD; ipsilateral eye) and 5.1±0.7 ms (SD; contralateral eye) for BN stimulation; and 3.6±0.4 ms (SD; ipsilateral eye) and 5.2±0.8 ms (SD; contralateral eye) for abducens nucleus stimulation. The time difference between SC- and BN-evoked eye movements (about 3 ms) was consistent with a disynaptic connection from the SC to the premotor BNs.     

Analysis of the step response of the saccadic feedback: computational models

 We present results of theoretical analysis and computational simulations of two models of the saccadic burst generator: the Scudder model and the Jurgens model. We used the experimental paradigm of prolonged stimulation in monkey superior colliculus (SC) to compare the performance of the two models. We excluded the Scudder model since it was not capable of reproducing the experimentally observed staircase movements. We modified the Jurgens model by replacing the originally proposed feedback integrator with an active reset mechanism by a leaky integrator. With this modification we have shown that the staircase movement elicited by prolonged stimulation in the SC can be modeled as a damped oscillatory step response of this model. Furthermore, to replicate the changes in the kinetic profiles of the staircase movements with increased stimulation we modified the functionality of the model. Our results suggest that prolonged stimulation of the SC dynamically changes the gains and time constant of the saccadic feedback. Received: 6 September 1996 / Accepted: 19 February 1997     

Competition between saccade goals in the superior colliculus produces saccade curvature

When saccadic eye movements are made in a search task that requires selecting a target from distractors, the movements show greater curvature in their trajectories than similar saccades made to single stimuli. To test the hypothesis that this increase in curvature arises from competitive interactions between saccade goals occurring near the time of movement onset, we performed single-unit recording and microstimulation experiments in the superior colliculus (SC). We found that saccades that ended near the target but curved toward a distractor were accompanied by increased presaccadic activity of SC neurons coding the distractor site. This increased activity occurred approximately 30 ms before saccade onset and was abruptly quenched on saccade initiation. The magnitude of increased activity at the distractor site was correlated with the amount of curvature toward the distractor. In contrast, neurons coding the target location did not show any significant difference in discharge for curved versus straight saccades. To determine whether this pattern of SC discharge is causally related to saccade curvature, we performed a second series of experiments using electrical microstimulation. Monkeys made saccades to single visual stimuli presented without distractors, and we stimulated sites in the SC that would have corresponded to distractor sites in the search task. The stimulation was subthreshold for evoking saccades, but when its temporal structure mimicked the activity recorded for curved saccades in search, the subsequent saccades to the visual target showed curvature toward the location coded by the stimulation site. The effect was larger for higher stimulation frequencies and when the stimulation site was in the same colliculus as the representation of the visual target. These results support the hypothesis that the increased saccade curvature observed in search arises from rivalry between target and distractor goals and are consistent with the idea that the SC is involved in the competitive neural interactions underlying saccade target selection.     

Convergence eye movements evoked by microstimulation of the rostral superior colliculus in the cat

Results of our previous studies suggest that the circumscribed area in the rostral superior colliculus (SC) of the cat is involved in the control of accommodation. Accommodation is closely linked with vergence eye movements. In this study, we investigated whether or not vergence eye movements are evoked by microstimulation of the rostral SC in the cat. In addition, we studied the effect of chemical inhibition of the rostral SC on visually guided vergence eye movements. This study was conducted on three cats, weighing 2.5-3.5 kg. The animals were trained to carry out visually guided saccade and convergence tasks. Eye movements were measured using search coils placed on both eyes. We recorded eye movements evoked by microstimulation of the rostral SC in the alert cats. Muscimol was injected into the rostral SC, and the effect of SC inactivation on visually guided vergence eye movements was investigated. Convergence eye movements were evoked by low-current stimulation (< 30 microA) of a circumscribed area in the intermediate layers of the rostral SC on one side. Spontaneous saccades were interrupted by the stimulation of the low-threshold area for evoking convergence. Visually guided convergence eye movements were severely diminished by the injection of muscimol into the low-threshold area for evoking convergence of the SC. The rostral SC is related to the control of vergence eye movements as well as accommodation. The rostral SC may be involved in the functional linkage between accommodation, convergence and visual fixation.     

Discharge properties of monkey tectoreticular neurons

The intermediate layers of the superior colliculus (SC) contain neurons that clearly play a major role in regulating the production of saccadic eye movements: a burst of activity from saccade neurons (SNs) is thought to provide a drive signal to set the eyes in motion, whereas the tonic activity of fixation neurons (FNs) is thought to suppress saccades during fixation. The exact contribution of these neurons to saccade control is, however, unclear because the nature of the signals sent by the SC to the brain stem saccade generation circuit has not been studied in detail. Here we tested the hypothesis that the SC output signal is sufficient to control saccades by examining whether antidromically identified tectoreticular neurons (TRNs: 33 SNs and 13 FNs) determine the end of saccades. First, TRNs had discharge properties similar to those of nonidentified SC neurons and a proportion of output SNs had visually evoked responses, which signify that the saccade generator must receive and process visual information. Second, only a minority of TRNs possessed the temporal patterns of activity sufficient to terminate saccades: Output SNs did not cease discharging at the time of saccade end, possibly continuing to drive the brain stem during postsaccadic fixations, and output FNs did not resume their activity before saccade end. These results argue against a role for SC in regulating the timing of saccade termination by a temporal code and suggest that other saccade centers act to thwart the extraneous SC drive signal, unless it controls saccade termination by a spatial code.     

Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets

Neurons in the rostral superior colliculus (SC) of alert cats exhibit quasi-sustained discharge patterns related to the fixation of visual targets. Because some SC neurons also respond to auditory stimuli, we investigated whether there is a population of neurons in the rostral SC which is active in relation to fixation of both auditory and visual targets. We identified cells which were active with visual fixation and which continued to discharge if the fixation stimulus was briefly extinguished. The population of neurons exhibited similar discharge characteristics when the fixation stimulus was auditory. Few neurons were significantly more active during fixation of visual targets than during fixation of auditory targets. Most fixation neurons showed a diminished discharge rate during spontaneous (self-generated) saccadic eye movements away from a visual fixation stimulus, regardless of the direction of the saccade. this diminished discharge rate (or pause) typically began, on average, 12.2 ms before saccade onset and the duration of the pause was Ionger than the duration of the saccade. These observations are consistent with the hypothesis that increased discharge of these neurons is related to active fixation and that reductions in their activity are important for the generation of saccades. However, the lack of a precise relationship between pause duration and saccade duration implies that these neurons would be unlikely to project directly to the saccadic burst generator. The mean interval from the beginning of the pauses of fixation neurons to be beginning of the saccades away from fixation targets is also shorter than has been found in brainstem omnipause neurons. By analogy with the concept of a receptive field, agaze position error field depicts the range of gaze position error for which a cell is active. Although fixation neurons appear to encode the magnitude and direction of the error between visual targets and the visual axis, visual error fields at the end of fixating eye movements were significantly larger than those at stimulus onset. For auditory stimuli, this difference was not significant. These observations are compatible with a number of recent experiments indicating that neural signals of eye position are damped or delayed with respect to current eye position.     

Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey

The cortical area V6A, located in the dorsal part of the anterior bank of the parieto-occipital sulcus, contains retino- and craniocentric visual neurones together with neurones sensitive to gaze direction and/or saccadic eye movements, somatosensory stimulation and arm movements. The aim of this work was to study the dynamic characteristics of V6A saccade-related activity. Extracellular recordings were carried out in six macaque monkeys performing a visually guided saccade task with the head restrained. The task was performed in the dark, in both the dark and light, and sometimes in the light only. The discharge of certain neurones during saccades is due to their responsiveness to visual stimuli. We used a statistical method to distinguish responses due to visual stimulation from those responsible for saccadic control. Out of 597 V6A neurones tested, 66 (11%) showed responses correlated with saccades; 26 of 66 responded also to visual stimulation and 31 of 66 did not; the remaining 9 were not visually tested. We calculated the response latency to saccade onset and its inter-trial variance in 24 of 66 neurones. Saccade neurones could respond before, during or after the saccade. Neurones responding before saccade-onset or during saccades had much higher latency variance than neurones responding after saccades. The early-responding cells had a mean latency (±SD) of –64±62 ms, while the late-responding cells a mean latency of +89±20 ms. The responses to saccadic eye movements were directionally sensitive and varied with the amplitude of the saccade. Responses of late-responding cells disappeared in complete darkness. We suggest that the activity of early-responding cells represents the intended saccadic eye movement or the shift of attention towards another part of the visual space, whereas that of late-responding cells is a visual response due to retinal stimulation during saccades. Electronic Publication     

Expression of a re-centering bias in saccade regulation by superior colliculus neurons

In previous studies of saccadic eye movement reaction time, the manipulation of initial eye position revealed a behavioral bias that facilitates the initiation of movements towards the central orbital position. An interesting hypothesis for this re-centering bias suggests that it reflects a visuo-motor optimizing strategy, rather than peripheral muscular constraints. Given that the range of positions that the eyes can take in the orbits delimits the extent of visual exploration by head-fixed subjects, keeping the eyes centered in the orbits may indeed permit flexible orienting responses to engaging stimuli. To investigate the influence of initial eye position on central processes such as saccade selection and initiation, we examined the activity of saccade-related neurons in the primate superior colliculus (SC). Using a simple reaction time paradigm wherein an initially fixated visual stimulus varying in position was extinguished 200 ms before the presentation of a saccadic target, we studied the relationship between initial eye position and neuronal activation in advance of saccade initiation. We found that the magnitude of the early activity of SC neurons, especially during the immediate pre-target period that followed the fixation stimulus disappearance, was correlated with changes in initial eye position. For the great majority of neurons, the pre-target activity increased with changes in initial eye position in the direction opposite to their movement fields, and it was also strongly correlated with the concomitant reduction in reaction time of centripetal saccades directed within their movement fields. Taking into account the correlation with saccadic reaction time, the relationship between neuronal activity and initial eye position remained significant. These results suggest that eye-position-dependent changes in the excitability of SC neurons could represent the neural substrate underlying a re-centering bias in saccade regulation. More generally, the low frequency SC pre-target activity could use eccentric eye position signals to regulate both when and which saccades are produced by promoting the emergence of a high frequency burst of activity that can act as a saccadic command. However, only saccades initiated within ~200 ms of target presentation were associated with SC pre-target activity. This eye-dependent pre-target activation mechanism therefore appears to be restricted to the initiation of saccades with relatively short reaction times, which specifically require the integrity of the SC. Electronic Publication     

Interaction of the frontal eye field and superior colliculus for saccade generation

Both the frontal eye field (FEF) in the prefrontal cortex and the superior colliculus (SC) on the roof of the midbrain participate in the generation of rapid or saccadic eye movements and both have projections to the premotor circuits of the brain stem where saccades are ultimately generated. In the present experiments, we tested the contributions of the pathway from the FEF to the premotor circuitry in the brain stem that bypasses the SC. We assayed the contribution of the FEF to saccade generation by evoking saccades with direct electrical stimulation of the FEF. To test the role of the SC in conveying information to the brain stem, we inactivated the SC, thereby removing the circuit through the SC to the brain stem, and leaving only the direct FEF-brain stem pathway. If the contributions of the direct pathway were substantial, removal of the SC should have minimal effect on the FEF stimulation, whereas if the FEF stimulation were dependent on the SC, removal of the SC should alter the effect of FEF stimulation. By acutely inactivating the SC, instead of ablating it, we were able to test the efficiency of the direct FEF-brain stem pathway before substantial compensatory mechanisms could mask the effect of removing the SC. We found two striking effects of SC inactivation. In the first, we stimulated the FEF at a site that evoked saccades with vectors that were very close to those evoked at the site of the SC inactivation, and with such optimal alignment, we found that SC inactivation eliminated the saccades evoked by FEF stimulation. The second effect was evident when the FEF evoked saccades were disparate from those evoked in the SC, and in this case we observed a shift in the direction of the evoked saccade that was consistent with the SC inactivation removing a component of a vector average. Together these observations lead to the conclusion that in the nonablated monkey the direct FEF-brain stem pathway is not functionally sufficient to generate accurate saccades in the absence of the indirect pathway that courses from the FEF through the SC to the brain stem circuitry. We suggest that the recovery of function following SC ablation that has been seen in previous studies must result not from the use of an already functioning parallel pathway but from neural plasticity within the saccadic system.     

Role of the rostral superior colliculus in active visual fixation and execution of express saccades.

1. In the rostral pole of the monkey superior colliculus (SC) a subset of neurons (fixation cells) discharge tonically when a monkey actively fixates a target spot and pause during the execution of saccadic eye movements. 2. To test whether these fixation cells are necessary for the control of visual fixation and saccade suppression, we artificially inhibited them with a local injection of muscimol, an agonist of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). After injection of muscimol into the rostral pole of one SC, the monkey was less able to suppress the initiation of saccades. Many unwanted visually guided saccades were initiated less than 100 ms after onset of a peripheral visual stimulus and therefore fell into the range of express saccades. 3. We propose that fixation cells in the rostral SC form part of a fixation system that facilitates active visual fixation and suppresses the initiation of unwanted saccadic eye movements. Express saccades can only occur when activity in this fixation system is reduced.     

Dynamic coding of vertical facilitated vergence by premotor saccadic burst neurons

To redirect our gaze in three-dimensional space we frequently combine saccades and vergence. These eye movements, known as disconjugate saccades, are characterized by eyes rotating by different amounts, with markedly different dynamics, and occur whenever gaze is shifted between near and far objects. How the brain ensures the precise control of binocular positioning remains controversial. It has been proposed that the traditionally assumed "conjugate" saccadic premotor pathway does not encode conjugate commands but rather encodes monocular commands for the right or left eye during saccades. Here, we directly test this proposal by recording from the premotor neurons of the horizontal saccade generator during a dissociation task that required a vergence but no horizontal conjugate saccadic command. Specifically, saccadic burst neurons (SBNs) in the paramedian pontine reticular formation were recorded while rhesus monkeys made vertical saccades made between near and far targets. During this task, we first show that peak vergence velocities were enhanced to saccade-like speeds (e.g., >150 vs. <100 degrees/s during saccade-free movements for comparable changes in vergence angle). We then quantified the discharge dynamics of SBNs during these movements and found that the majority of the neurons preferentially encode the velocity of the ipsilateral eye. Notably, a given neuron typically encoded the movement of the same eye during horizontal saccades that were made in depth. Taken together, our findings demonstrate that the brain stem saccadic burst generator encodes integrated conjugate and vergence commands, thus providing strong evidence for the proposal that the classic saccadic premotor pathway controls gaze in three-dimensional space.     

Eye position effects in saccadic adaptation

Saccades are used by the visual system to explore visual space with the high accuracy of the fovea. The visual error after the saccade is used to adapt the control of subsequent eye movements of the same amplitude and direction in order to keep saccades accurate. Saccadic adaptation is thus specific to saccade amplitude and direction. In the present study we show that saccadic adaptation is also specific to the initial position of the eye in the orbit. This is useful, because saccades are normally accompanied by head movements and the control of combined head and eye movements depends on eye position. Many parts of the saccadic system contain eye position information. Using the intrasaccadic target step paradigm, we adaptively reduced the amplitude of reactive saccades to a suddenly appearing target at a selective position of the eyes in the orbitae and tested the resulting amplitude changes for the same saccade vector at other starting positions. For central adaptation positions the saccade amplitude reduction transferred completely to eccentric starting positions. However, for adaptation at eccentric starting positions, there was a reduced transfer to saccades from central starting positions or from eccentric starting positions in the opposite hemifield. Thus eye position information modifies the transfer of saccadic amplitude changes in the adaptation of reactive saccades. A gain field mechanism may explain the eye position dependence found.     

A new local feedback model of the saccadic burst generator

1. To accommodate the finding that the superior colliculus is an important input to the brain stem pathways that generate saccades (the saccadic burst generator), a new model of the burst generator is proposed. Unlike the model of Robinson (61) from which it was derived, the model attempts to match a neural replica of change in eye position, which is the output of the burst generator, to a neural replica of change in target position, which is the output of the colliculus and the input to the model. 2. The elements of the model correspond to neurons known or thought to be associated with the actual primate saccadic burst generator and are mostly connected together in accord with the results of anatomical and physiological experiments. 3. The model was simulated on a digital computer to compare its behavior with that of the actual burst generator under normal and experimental conditions. Simulated peak burst frequency and saccade duration matched that obtained from monkey excitatory burst neurons and inhibitory burst neurons for saccades up to 15 degrees but did not match at larger sizes; stimulation of the omnipause neurons caused an interruption of the saccade, and the saccade resumed at the end of stimulation as in actual data; the model can generate the abnormally long-duration saccades seen under decreased alertness or various pathologies by changing the burst generator inputs and without having to change any properties of the neurons themselves or their connections; a simulated horizontal and vertical burst generator pair connected only through the omnipause neurons can generate realistic oblique saccades. 4. The implications of the model for higher-order control of the saccadic burst generator are discussed.     

Kinematics of eye movements of cats to broadband acoustic targets.

Operant conditioning was used to train cats with their heads immobilized to localize sound by directing their eyes to the location of the sources. The kinematics of those eye movements were studied and compared with eye movements to visual targets at the same locations. The main finding of this study is that eye movements to broadband long-duration acoustic targets have two components: an initial slow phase of variable duration and a fast, normal saccade. The slow component is characterized by a persistent, shallow velocity ramp, while the saccadic component of the response falls on the main sequence computed from eye movements to visual targets. The slow component was shorter before saccades to long-duration stimuli performed under the delayed-saccade task and practically absent before saccades to transient acoustic stimuli. The results suggest that the initial slow component is used by cats to deal with uncertainty associated with the location of long-duration broadband targets and that the input to the saccade integrator(s) is similar under both visual and acoustic conditions.     

Effects of eye position on saccades evoked electrically from superior colliculus of alert cats

Electrical stimulation was carried out in the intermediate and deep gray layers of the superior colliculus in alert cats. The heads of the animals were fixed, and their eye movements were recorded with the scleral search coil method. Stimulation in the anterior two-thirds of the colliculus with long-duration pulse trains produced multiple saccades, as in the primate (45, 51), but their directions and amplitudes were influenced significantly by the initial position of the eye. Stimulation in the posterior part of the colliculus evoked saccades that appeared to be "goal-directed," whereas stimulation at the extreme caudal edge of the colliculus yielded centering saccades. These observations confirm previous reports of Roucoux and Crommelinck (48) and Guitton et al. (24). Saccades evoked during bilateral simultaneous stimulation of the superior colliculi were also dependent on the initial position of the eye. At certain relative intensities of stimulation on the two sides, saccades failed to occur when the eye was within a particular part of the oculomotor range. When the eye was outside this region, the same stimuli triggered an eye movement that drove the eye toward the zone of saccade failure. These findings indicate that saccadic commands resulting from focal collicular stimulation in the cat can be modified by information about current eye position. It is not certain where in the brain this occurs or by what neural mechanisms, but a local feedback model of the saccadic control system (46) can account for the main observations. The functional significance of these findings depends in large measure on the degree to which focal collicular stimulation reproduces naturally occurring patterns of neural activity.     

Role of the basal ganglia in the control of purposive saccadic eye movements

In addition to their well-known role in skeletal movements, the basal ganglia control saccadic eye movements (saccades) by means of their connection to the superior colliculus (SC). The SC receives convergent inputs from cerebral cortical areas and the basal ganglia. To make a saccade to an object purposefully, appropriate signals must be selected out of the cortical inputs, in which the basal ganglia play a crucial role. This is done by the sustained inhibitory input from the substantia nigra pars reticulata (SNr) to the SC. This inhibition can be removed by another inhibition from the caudate nucleus (CD) to the SNr, which results in a disinhibition of the SC. The basal ganglia have another mechanism, involving the external segment of the globus pallidus and the subthalamic nucleus, with which the SNr-SC inhibition can further be enhanced. The sensorimotor signals carried by the basal ganglia neurons are strongly modulated depending on the behavioral context, which reflects working memory, expectation, and attention. Expectation of reward is a critical determinant in that the saccade that has been rewarded is facilitated subsequently. The interaction between cortical and dopaminergic inputs to CD neurons may underlie the behavioral adaptation toward purposeful saccades.