Evarts, E. V.; Kimura, M.; Wurtz, R. H., and Hikosaka, O. Behavioral correlates of activity in basal ganglia neurons. Trends in Neurosci. 1984:447-453.
Abstract:  Changes of neuronal discharge in the striatum, globus pallidus and substantia nigra pars reticulata (SNr) precede movement in certain behavioral situations but not in others.  A given SNr neuron may pause in advance of a saccade to a remembered target but not in relation to the same saccade directed to a target that is present.  A click or a visual stimulus may evoke a response in SNr, globus pallidus, or striatum when the stimulus is behaviorally significant but not when the same stimulus is delivered without such significance.  On the basis of these and other observations it is suggested that the 'internal' initiation of movement in the absence of sensory guidance may be a unique contribution of a system that includes the basal ganglia.  In light of the close anatomical connections between frontal cortex and basal ganglia, such a system may include the frontal cortex.

Hikosaka, O. Role of basal ganglia in saccades. Rev.Neurol.(Paris.). 1989; 145:580-586.
Abstract:  The basal ganglia, substantia nigra pars reticulata (SNr) and caudate nucleus, contribute to the suppression and initiation of saccadic eye movements by imposing a tonic inhibition on the superior colliculus (SC) and by removing it. The tonic inhibition originates from the SNr where neurons show continuous, high frequency discharges. With its inhibitory connection to the SNr, the caudate nucleus transiently suppresses the SNr activity thereby removing the tonic inhibition on the SC. Signals carried by neurons in the SNr and the caudate nucleus are both heavily dependent on or selective for different aspects of learned paradigms. Such task-specific, learned information originating from the basal ganglia may open or close the gate for a variety of excitatory inputs to the SC.

Hikosaka, O.; Sakamoto, M., and Usui, S. Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. J.Neurophysiol. 1989; 61:780-798.
Abstract:  1. We recorded single cell activities in the caudate nucleus of the monkeys trained to perform a series of visuomotor tasks. In the first part of this paper, we summarize the types and locations of neurons in the monkey caudate nucleus. In the second part, we report the characteristics of neurons related to saccadic eye movements. 2. Neurons were classified into two types in terms of spontaneous discharge pattern. A majority of the neurons (2,287/2,559, 89%) had very low-frequency discharges (mostly less than 1 Hz). The rest (n = 272) showed irregular-tonic discharges (3-8 Hz) with broad spikes. 3. Of 2,559 neurons tested, 867 showed spike activity related to some aspects of the tasks; 502 neurons showed discharges in response to environmental changes outside, not in relation to, the tasks. None of the neurons responsive in or outside the tasks belonged to the irregular-tonic type. 4. The task-related activities were classified as: Saccade-related, Visual, Auditory, Cognitive, Fixation-related, and Reward-related. The activities detected outside the tasks were classified into: Visual, Auditory, Movement-related, Reward-related, and Other. Few neurons had both task-related and task-unrelated activities. 5. The locations of recorded neurons were determined using a coordinate system based on the anterior and posterior commissures. Task-related neurons were clustered longitudinally in the central part of the caudate. Neurons responsive outside the tasks were more widely distributed; specifically, auditory neurons were in the medial part, whereas movement-related neurons were in the lateral part. The irregular-tonic neurons were dispersed all over the caudate. 6. The monkey was trained to fixate on a spot of light on the screen and, when the spot moved, to follow it by making a saccade. A visually guided saccade occurred when the spot moved to another location without a time gap (saccade task). A memory-guided saccade occurred when the spot first disappeared and after a time gap reappeared at a fixed location (saccade with gap task). By delivering a cue stimulus while the monkey was fixating, a memory-guided saccade was elicited to a randomly chosen location (delayed saccade task).  7.  Among 306 neurons with saccade-related activities, 266 were further classified into 4 subtypes: neurons related preferentially to memory-guided saccade (SAC/MEM, n = 102); neurons related preferentially to visually guided saccades (SAC/VIS, n = 64), neurons related to both types of saccade (SAC/V&M, n = 80), and neurons showing tonic, preparatory activity increasing toward a saccade (SAC/PRP, n = 27).  8.  The neurons related preferentially to memory-guided saccade also showed discharges before saccades that the monkey made to search for a spot of light.  Only a small number of these neurons showed discharges with spontaneous saccades made in the darkness.  9.  The neurons related preferentially to visually guided saccade could, in addition, show a visual response to the target.  10.  Onsets of saccade-related activities preceded onsets of saccades by 0-300 ms in most cases.  The memory-guided, saccade-related activity tended to start earlier than other activity types.  11.  The saccade-related neurons had movement fields that were large and usually centered in the contralateral visual field.  The centers of movement fields were distributed almost uniformly in the contralateral visual field, regardless of the activity types.  12.  The results suggest that the caudate nucleus contains a part of the neural mechanism by which saccadic eye movement is initiated in the specific context of learned behaviors, either based on memory/anticipation or in response to visual information.

Hikosaka, O.; Sakamoto, M., and Usui, S. Functional properties of monkey caudate neurons. II. Visual and auditory responses. J.Neurophysiol. 1989; 61:799-813.
Abstract:  1. Visual responses of caudate neurons were studied in monkeys trained to fixate on a small spot of light. A visual stimulus (another spot of light) was presented in various contexts of behavior using different behavioral paradigms. Visual receptive fields were usually large and centered on the contralateral hemifield. Among 217 neurons with visual responses, 184 were further classified into subtypes. 2. Visual responses in 64 neurons were not modulated by changing the paradigms (unconditional visual responses). In the other neurons, visual responses were dependent on the behavioral contexts in which the stimulus was presented. Three types of behavioral modulation were found. 3. A saccade-enhanced visual response (n = 37) was the one that was enhanced if the monkey made a saccade to the stimulus on its appearance. The enhancement was spatially selective: the response was depressed if the saccade was directed away from the stimulus. 4. Memory-contingent visual responses (n = 36) were present preferentially when the monkey remembered the location of the stimulus and a few seconds later made a saccade to the remembered location. Responses were greater when the location of the stimulus was randomized between trials. 5. Expectation-contingent visual responses (n = 46) were present preferentially when the stimulus came on while the monkey was not fixating another spot, and the stimulus was related directly to a reward. Unlike the other types, its receptive field included both contralateral and ipsilateral hemifields without a particular preference. 6.  A small number of neurons (n = 16) showed a visual response that easily habituated. 7. Latencies of visual responses were usually between 100 and 200 ms. The latencies of the memory-contingent, expectation-contingent, and habituated visual responses tended to be longer than the others and tended to be more variable between trials. 8. Among auditory responsive neurons only a small proportion were related to the tasks. The response was greater to a contralateral sound. It was enhanced if the monkey used the sound as the cue for the future target location. 9. The results suggest that sensory responses of caudate neurons could be used to guide a subsequent sequence of learned behaviors by confirming predicted environmental states, renewing memory, or establishing a motor set.

Hikosaka, O.; Sakamoto, M., and Usui, S. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J.Neurophysiol. 1989; 61:814-832.
Abstract:  1. The present paper reports complex neural activities in the monkey caudate nucleus that precede and anticipate visual stimuli and reward in learned visuomotor paradigms. These activities were revealed typically in the delayed saccade task in which memory and anticipation were required. We classified these activities according to their relationships to the task. 2. Activity related to expectation of a cue (n = 46) preceded the presentation of a spot of light (target cue) that signified the future location of saccade target.  When the target cue was delayed, the activity was prolonged accordingly. The same spot of light was preceded by no activity if it acted as a distracting stimulus. 3. The sustained activity (n = 80) was a tonic discharge starting after the target cue as if holding the spatial information. 4. The activity related to expectation of target (n = 109) preceded the appearance of the target whose location was cued previously. It started with or after a saccade to the cued target location and ended with the appearance of the target. The activity was greater when the target was expected to appear in the contralateral visual field. 5. The activity related to expectation of reward (n = 57) preceded a task-specific reward. It started with the appearance of the final target and ended with the reward. In most cases, the activity was nonselective for how the monkey obtained the reward, i.e., by visual fixation only, by a saccade, or by a hand movement. The activity was dependent partly on visual fixation. 6. A few neurons showed tonic activity selectively before lever release and are thus considered to be related to the preparation of hand movements. 7. The activity related to breaking fixation (n = 33) occurred phasically if the monkey broke fixation, aborting the trial. 8.  Activity related to reward (n = 104) was a phasic discharge that occurred before or after a reward of water was delivered. The activity was not simply related to a specific movement involved in the reward-obtaining behavior (eye, hand, or mouth movement). 9. Fixation-related activity (n = 72) was tonic activity continuing as long as the monkey attentively fixated a spot of light. It was dependent on reward expectancy in most cases. 10. The present results, together with those in the preceding papers, indicate that the activities of individual caudate neurons--sensory, motor, or cognitive--are dependent on specific contexts of learned behavior.  We suggest that the caudate nucleus is part of the neural mechanism for predicting environmental changes and preparing for the next movement in carrying out sequential behaviors.

Hikosaka, O. and Wurtz, R. H. Effects on eye movements of a GABA agonist and antagonist injected into monkey superior colliculus. Brain Res. 1983; 272:368-372.
Abstract:  Injection of muscimol, a GABA agonist, into the superior colliculus of awake monkeys produces saccades to visual targets in the movement field of colliculus cells near the injection site that have longer latency and shortened amplitude. Bicuculline, a GABA antagonist, leads to irrepressible saccades towards the movement field. These results are consistent with a tonic inhibition by the substantia nigra on the superior colliculus mediated by GABA which is reduced at the time of saccade initiation.

Hikosaka, O. and Wurtz, R. H. Modification of saccadic eye movements by GABA-related substances. I Effect of muscimol and bicuculline in monkey superior colliculus. J.Neurophysiol. 1985; 53:266-291.
Abstract:  1.  Our previous observations led to the hypothesis that cells in the substantia nigra pars reticulata (SNr) tonically inhibit saccade-related cells in the intermediate layers of the superior colliculus (SC). Before saccades to visual or remembered targets, cells in SNr briefly reduce that inhibition, allowing a burst of spikes of SC cells that, in turn, leads to the initiation of a saccadic eye movement. Since this inhibition is likely to be mediated by gamma-aminobutyric acid (GABA), we tested this hypothesis by injecting a GABA agonist (muscimol) or a GABA antagonist (bicuculline) into the superior colliculus and measured the effects on saccadic eye movements made to visual or remembered targets.  2.  An injection of muscimol selectively suppressed saccades to the movement field of the cells near the injection site. The affected area expanded over time, thus suggesting the diffusion of muscimol in the SC; the area never included the other hemifield, suggesting that the diffusion was limited to one SC. One of the monkeys became unable to make any saccades to the affected area.  3.  Saccades to visual targets following injection of muscimol had longer latency and slightly shorter amplitudes that were corrected by subsequent saccades. The most striking change was a decrease in the peak velocity of the saccade, frequently to less than half the preinjection value.  4.  Saccades to remembered targets following injection of muscimol also showed an increase in latency and decrease in velocity, but in addition, showed a striking decrease in the accuracy of the saccades. The trajectories of saccades became distorted as if they were deflected away from the affected area.  5.  After muscimol injection, the area over which spontaneous eye movements were made shifted toward the side ipsilateral to the injection.  Saccades toward the contralateral side were less frequent and slower. In nystagmus, which developed later, the slow phase was toward the contralateral side.  6.  In contrast to muscimol, injection of bicuculline facilitated the initiation of saccades. Injection was followed almost immediately by stereotyped and apparently irrepressible saccades made toward the center of the movement field of the SC cells at the injection site. The monkeys became unable to fixate during the tasks; the fixation was interrupted by saccadic jerks made to the affected area of the visual field and then back to the fixation point.  7.  After bicuculline injection, eye position shifted toward the side contralateral to the injection, and saccades to the contralateral side increased in frequency.  In subsequent nystagmus the slow phase was toward the ipsilateral side.  8.  These experiments indicate that GABA has a powerful effect on the SC; potentiation or reduction of GABA inhibition alters the execution of saccadic eye movements.  They emphasize that the SC influences the velocity of saccadic eye movements in addition to their latency and accuracy.

Hikosaka, O. and Wurtz, R. H. Modification of saccadic eye movements by GABA-related substances II. Effects of muscimol in monkey substantia nigra pars reticulata. J.Neurophysiol. 1985; 53:292-308.
Abstract:  The preceding study (21) showed that a gamma-aminobutyric acid (GABA) agonist or antagonist injected into the superior colliculus (SC) disrupted saccadic eye movements. The purpose of the present experiments was to determine whether this result was due to altering the inhibitory input to the SC from the substantia nigra pars reticulata (SNr). SNr cells are themselves inhibited by GABA. Injection of muscimol, a GABA agonist, into the SNr should increase the inhibition acting on SNr cells and should reduce the inhibition acting on the SC. If the effects of GABA inhibition in the SC results from terminals originating in the SNr, muscimol in the SNr should act like bicuculline in the SC. Muscimol in the SNr has the same general effect as bicuculline in the SC. The monkey made irrepressible saccades toward the contralateral visual field where cells in the SNr at the injection site had their visual or movement field. During visual fixation saccadic jerks occurred, interspersed with spontaneous saccades, instead of saccades to visual targets or to remembered targets. Saccades to remembered targets were more vulnerable to these saccadic intrusions than were saccades to visual targets. Since muscimol in the SNr acts like bicuculline in the SC, we conclude that a substantial fraction of GABA-mediated inhibitory inputs in the SC originates from the SNr. These experiments, in conjunction with previous experiments, show that the SNr exerts a tonic inhibition on saccade-related cells in SC and that this inhibition is mediated by GABA. The role of the SNr in initiation of saccades to remembered targets is particularly important since these saccades are more severely disrupted by muscimol in the SNr as well as in the SC. We suggest that both of these conclusions about eye movement might apply to skeletal movements as well.  First, the basal ganglia contribute to the initiation of movement by a release of the target structure from tonic inhibition. Second, this mechanism is particularly critical of the movements based on stored or remembered signals that are not currently available as incoming sensory inputs.

Hikosaka, O. and Wurtz, R. H. Saccadic eye movements following injection of lidocaine into the superior colliculus. Exp.Brain Res. 1986; 61:531-539.
Abstract:  Ablation of the superior colliculus (SC) has generally produced limited deficits in the initiation of saccadic eye movements, usually an increase in the latency of saccades. However, recent studies using muscimol, a GABA agonist, to block afferents to the SC showed deficits in not only latency but in amplitude and velocity of saccades as well. These greater deficits might be dependent upon the testing of saccades shortly after the damage of SC before any compensation for the deficits could develop. The present experiments tested this hypothesis by injecting a local anesthetic into SC.  The anesthetic inactivated the cells entirely rather than just deafferenting them, but still allowed testing immediately after the injection. Clear deficits were observed following injection of lidocaine into the SC. The amplitudes of saccades to visual targets were shortened, and the peak velocities of the saccades were reduced even if the reduced amplitude of the saccades was taken into account. Latency of saccades usually increased. The deficits were limited to the area of the visual field that overlapped the movement fields of the cells near the injection site. If the movement fields were in the periphery, saccades to the periphery were shortened following the injection of lidocaine. If the movement fields were near the center of gaze, saccades into the area were shortened, but the monkey was able to make saccades over the visual field related to the affected area to more peripheral targets.(ABSTRACT TRUNCATED AT 250 WORDS)

Hikosaka, O. and Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J.Neurophysiol. 1983; 49:1230-1253.
Abstract:  The substantia nigra pars reticulata recently has been shown to represent a major output of the basal ganglia.  The efferent projection of the substantia nigra to the visual and oculomotor layers of the superior colliculus suggests some visual or oculomotor role for the substantia nigra as well.  We have studied the sensory and oculomotor properties of cells in the monkey substantia nigra pars reticulata by recording extracellular unitary spikes of these cells while the monkey was performing behavioral paradigms that allowed the presentation of visual and auditory stimuli and the initiation of saccadic eye movements under different behavioral conditions.  2.  Substantia nigra pars reticulata cells typically showed high background discharge rates (usually 50-100 spikes/s).  The cells that responded in relation to sensory (visual or auditory) stimuli or saccadic eye movements were located primarily in the lateral part of the pars reticulata.  This response was almost always a decrease in discharge rate.  3.  We found that the substantia nigra cells may respond in different ways under different experimental conditions.  We therefore classified response types rather than cell types and were able to identify nine response types based on their temporal correlation with sensory stimulation or eye movement and their behavioral dependency.  4.  Many cells (58% of all cells that showed some type of response) showed a simple visual response:  they decreased their discharge rate in response to visual stimuli while the monkey was fixating on a spot of light.  Latency of visual response ranged from 70 to 167 ms (mean, 120 ms).  Spots of light were usually more effective than larger stimuli.  No preference for moving stimuli or stimuli with particular shapes was present.  5.  Visual response was best to a stimulus in the visual field contralateral to the recording site.  The receptive fields showed a clear gradient of response; the further a stimulus was from the center of the receptive field, the less the visual response.  Cells encountered on the same electrode penetration tended to have receptive fields clustered toghther.  6.  The visual response of some cells (42%) was frequently enhanced when the monkey made a saccade to the stimulus and reduced when the monkey made a saccade away from the stimulus (saccade-modulated visual response).  The enhancement could be explained by the addition of a visual response and another response related to a saccade.  Habituation of the visual response was sometimes seen by repeated stimulation, particularly with short intertrial intervals.  7.  Some cells (32%) showed a visually contingent saccade response, a decrease in discharge rate temporally correlated with a saccade to a visual target:  no change in activity was associated with the same saccade if the target was no longer present or if the saccade occurred in darkness.  The cells that showed this type of response frequently (65%) also had a visual response.  8.  A fraction of the cells (9%) responded to auditory stimuli.  The response was greater to a stimulus contralateral to the recording site and was sometimes enhanced when auditory stimulation was associated with a subsequent saccade toward the sound.  9.  Cell activity in the substantia nigra described in this paper may be related to the monkey's orienting behavior, including shift of gaze to novel stimuli.  This activity may be dependent on input directly from the caudate nucleus and indirectly from the frontal eye fields.

Hikosaka, O. and Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. II. Visual responses related to fixation of gaze. J.Neurophysiol. 1983; 49:1254-1267.
Abstract:  1.  In this study we describe two types of visual responses that are dependent on the monkey's fixation gaze.  To demonstrate these responses, we compared responses of substantia nigra cells to the same visual stimulus with the same retinal location under two different conditions:  one in which the monkey was or had been fixating on a spot of light when the stimulus came on (fixation condition), and the other in which no spot of light was present for the monkey to fixate on when the stimulus came on (nonfixation condition).  2.  The first type of response occurred to a spot of light when the monkey was not fixating on another spot of light (nonfixation-contingent visual response).  Of 155 substantia nigra cells with some sensory or oculomotor responses, 45 cells (29%) showed this type of response.  The response was a decrease in discharge rate that was time-locked to the onset of the stimulus (mean latency, 126 ms).  3.  Visual receptive fields of these substantia nigra cells determined under the nonfixation condition were large, extending both into the contralateral and ipsilateral sides frequently by 40^o of visual angle.  A stimulus in the central part of the visual field was always the most effective; a stimulus in the contralateral visual field was usually more effective than one in the ipsilateral field.  4.  The presence of an overt stimulus on the fovea, which was usually associated with visual fixation, was important for the suppression of the visual response.  5.  The shorter the intertrial interval, the weaker the visual response of these substantia nigra cells under the nonfixation condition.  The response reduction built up over several trials.  6.  The second type of response related to the monkey's fixation of gaze was a response to the offset of a spot of light (mean latency, 131 ms) that the monkey was fixating (fixation-contingent visual off-response).  Of 154 substantia nigra cells with some sensory or oculomotor responses, 36 cells (23%) showed this type of response.  Many of them also had a nonfixation-contingent visual on-response.  7.  This contingent off-response was largely suppressed if another spot of light was present as the fixation spot went off; the response was present only when the fixation spot went off leaving no other overt stimulus.  The response became greater as the period from the offset of the fixation spot to the onset of a visual target increased.  8.  These substantia nigra cells respond to the appearance of a light spot that the monkey is going to fixate or to the disappearance of a light spot that it was fixating.  We suggest that they signal the initiation or the termination of visually guided oculomotor behavior.

Hikosaka, O. and Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. J.Neurophysiol. 1983; 49:1268-1284.
Abstract:  The three types of responses described in this point were all related to either saccades to remembered targets or to the targets to be remembered.  All the responses were a decrease in discharge rate.  2.  The new paradigm frequently used in this study required the monkey to remember the location of a stimulus presented briefly while it was fixating; a later saccade was rewarded if it was made to the position of the no longer present stimulus.  The three types of responses were revealed by the use of this paradigm; they were less obvious or undetectable in conventional paradigms in which the monkey responded to the stimulus that was still present.  3.  The first type of response was to the visual stimulus that the monkey had to use as the target for a subsequent saccade (memory-contingent visual response); a minimal response occurred if the monkey made a saccade to the stimulus while it was still present or if the monkey continued to fixate.  Latencies and receptive fields for this response were similar to those for simple visual responses (17).  Of 93 substantia nigra cells with some sensory-oculomotor response, 29 cells (31%) showed this type of response.  4.  The second type of response was temporally correlated with a saccade made to the point where a visual stimulus was once present (memory-contingent saccade response).  Nearly half of these cells showed no significant response if the saccade was made to the stimulus while it was still present, whereas others showed a comparable response in both conditions.  None of them showed a change in activity in relation to spontaneous saccades in darkness.  5.  The onset of a memory-contingent saccade response usually preceeded the saccade onsetby up to 280 ms (most frequently by 70 to 240 ms).  The response was usually spatially selective; for most responses, contralateral saccades were associated with an exclusive or greater response compared with ipsilateral saccades.  Movement fields were demonstrated for some cells.  Of 128 cells tested, 41 cells (32%) showed this second type of response.  6.  The third type of response began after the briefly presented stimulus and continued until the saccade made to the stimulus position (memory-contingent sustained response).  Of 95 cells tested, 15 cells (16%) showed this type of response.  These cells frequently also showed a memory-contingent saccade response.  7.  These three types of substantia nigra cell activity are related to the special type of visuooculomotor behavior in which a visual input, particularly its spatial location, must be stored and then used as a target for a saccadic eye movement.  One of their efferent connections, the nigrocollicular pathway, may act as a channel for the stored visual-spatial information to be executed as a saccadic eye movement.  8.  Discussions of basal ganglia function generally emphasize one of three functions:  sensory, motor, or cognitive.  All of these three functional aspects appear to be combined in the substantia nigra pars reticulata, which is presumably a final stage of processing in the basal ganglia.  In single substantia nigra cells, however, they are combined or gated in different ways so that the sensory or motor activities of the cells are specialized for the different contexts in which behavior occurs.

Hikosaka, O. and Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J.Neurophysiol. 1983; 49:1285-1301.
Abstract:  1.  The preceeding studies (18-20) have shown that cells in the monkey substantia nigra pars reticulata have responses that are temporarily correlated with visual or auditory stimuli and saccadic eye movements.  In this study we determined whether these substantia nigra cells project to the superior colliculus.  2.  We first recorded from a substantia nigra cell and identified its sensory and oculomotor properties using the behavioral paradigms developed previously (18-20).  Then we stimulated the ipsilateral superior colliculus while moving the stimulating electrode through the layers of the colliculus to determine whether and from what depth the substantia nigra cell was activated antidromically.  Finally, we identified the visual and oculomotor properties of the colliculus cells located near the points from which the substantia nigra cell was activated antidromically with the lowest thresholds.  3.  Of 180 substantia nigra cells studied, 51 were activated antidromically from the ipsilateral superior colliculus.  Nearly half of the substantia nigra cells that showed some visual- or saccade-related responses were activated antidromically, whereas cells that did not show such responses were rarely activated.  4.  For each of the substantia nigra cells that showed visual- or occulomotor-related responses, we determined the center of the visual receptive or movement field of the cell and compared it with the field center of the superior colliculus cells found at the lowest threshold point.  The closer the two field centers, the more probable the antidromic activation of the substantia nigra cell, which suggests that each substantia nigra cell projects to the superior colliculus so as to match its own field with that of the colliculus cells in its projection area.  5.  The threshold stimulation current for antidromic activation of single substantia nigra cells varied, depending on the depth of the stimulating electrode within the superior colliculus, with several low-threshold points usually seen on a penetration through the colliculus.  Regardless of the type of visual or oculomotor response of the substantia nigra cell, the low-threshold point was most commonly found among colliculus cells that showed a burst of spikes before saccades and, therefore, were probably located in the intermediate layers.  A low-threshold point was also common in the deep layers but was relatively rare in the superficial layers.  The latency of antidromic response ranged from 0.7 to 2.3 ms. The antidromic latency for single substantia nigra cells tended to decrease with the depth of stimulation in the superior colliculus.  6.  We compared the visual and oculomotor activity of antidromically activated substantia nigra cells with that of superior colliculus cells near the point of lowest threshold for stimulation.  An inverse relationship was found between saccade-related activities of such a neuron pair: a decrease in discharge rate of the substantia nigra cell occurred with an increase in discharge rate (frequently a burst of spikes) of the superior colliculus cell.  However, such a relationship depended on how the saccade was initiated because saccade-related response of substantia nigra cells were selective for the mode of saccade initiation (visually contingent or memory contingent; Refs. 18 and 20), whereas superior colliculus cells were usually nonselective.  Correlation of visual responses of substantia nigra cells with activity of superior colliculus cells was less obvious.  7.  The results of these antidromic stimulation experiments suggest a synaptic connection between substantia nigra cells and the superior colliculus, particularly those cells in the intermediate layers of the colliculus that give a burst of spikes before the onset of saccades.  The relationship between cell discharge in the two structures is consistant with the idea that the substantia nigra cells discharge rapidly and inhibit superior colliculus cells tonically.  A release of the tonic inhibition resulting from a decrease in substantia nigra cell activity would contribute to the generation of the burst activity in the colliculus cells and, consequently, would contribute to the initiation of saccadic eye movements.

Lu, X. F.; Hikosaka, O., and Miyachi, S. Role of monkey cerebellar nuclei in skill for sequential movement. J.Neurophysiol. 1998 May; 79(5):2245-2254.
Abstract:  To examine whether the cerebellum is involved in learning and memory of visuomotor sequences, we trained two monkeys on a sequential button press task and inactivated different portions of the cerebellar nuclei by injecting a small amount of muscimol (gamma-aminobutyric acid agonist). Before the injection experiments started, the monkeys had learned a set of sequences (n = 21 and 12) extensively. After each injection, we had the monkeys perform the learned sequences and, in addition, learn new sequences. We found deficits in learning/memory by the injections into the dorsal and central part of the dentate nucleus. The number of errors increased significantly for the learned sequences but not for the new sequences. This effect was present only when the hand ipsilateral to the muscimol injection was used. Consistent with this result, anticipatory saccades, the occurrence of which is correlated closely with motor skill, also became less frequent particularly when the ipsilateral hand was used. No effect on learning/memory was observed after injections into the ventral or lateral parts of the dentate nucleus, interpositus nucleus, or fastigial nucleus. In contrast, hand movements became slower after ipsilateral injections at all of the injection sites.  These results suggest that, among the cerebellar nuclei, the dentate nucleus, especially its dorsal and central regions, is related to the storage and/or retrieval of long-term memory for motor skill.

Miyachi, S.; Hikosaka, O.; Miyashita, K.; Karadi, Z., and Rand, M. K. Differential roles of monkey striatum in learning of sequential hand movement. Experimental Brain Research. 1997 Jun; 115(1):1-5.
Abstract:  To study the role of the basal ganglia in learning of sequential movements, we trained two monkeys to perform a sequential button-press task (2x5 task).  This task enabled us to examine the process of learning new sequences as well as the execution of well-learned sequences repeatedly. We injected muscimol (a GABA agonist) into different parts of the striatum to inactivate the local neural activity reversibly. The learning of new sequences became deficient after injections in the anterior caudate and putamen, but not the middle-posterior putamen. The execution of well-learned sequences was disrupted after injections in the middle-posterior putamen and, less severely, after injections in the anterior caudate/putamen. These results suggest that the anterior and posterior portions of the striatum participate in different aspects of learning of sequential movements.

Wurtz, R. H.; Goldberg, M. E., and Robinson, D. L. Behavioral modulation of visual responses in the monkey: stimulus selection for attention and movement. Progress in Psychobiology and Physiological Psychology. 1980; 9:43-83.
 

Wurtz, R. H. and Hikosaka, O. Role of the basal ganglia in the initiation of saccadic eye movements. Prog.Brain Res. 1986; 64:175-190.