Representation of averaging saccades in the superior colliculus of the monkey

We tested the hypothesis that averaging saccades occur when two different saccades are prepared and executed simultaneously. The activity of saccade-related burst neurons (SRBNs) in the primate superior colliculus was recorded while monkeys made both non-averaging saccades to single targets and averaging saccades which directed the gaze between two simultaneously presented visual targets. For movements of comparable direction and amplitude, the activity measured during averaging and non-averaging saccades was statistically indistinguishable. These results are not consistent with the hypothesis that averaging saccades result from the simultaneous execution of two different saccades at the level of the collicular SRBNs. Instead, these findings indicate that averaging saccades are represented as single intermediate movements within the topographically organized map of these collicular cells.     

Role of monkey superior colliculus in saccade averaging

Summary We have investigated the involvement of collicular movement cells in the monkey in the execution of averaging saccades, elicited by a visual double-step stimulus. We found that, qualitatively, most (12/14) movement cells were recruited during averaging saccades in roughly the same way as for comparable visually-elicited saccades to single targets (V-saccades). However, movement-cell responses during averaging saccades in trials where the target suddenly changed direction were often less intense than for a comparable V-saccade. In these cases, the averaging responses were observed to be also slower than V-saccades of the same amplitude. Firing rate and double-step saccade dynamics were found to be significantly correlated in 9/14 cells tested. Several hypotheses for the collicular role in the generation of averaging saccades are discussed.     

Neurons with complex visual properties in the superior colliculus of the macaque monkey

Summary Single neurons were recorded from the superficial layers of the superior colliculus of immobilized monkeys (Macaca mulatta and Macaca irus). Two main functional types of neurons were found. The neurons of the first type (Type I neurons) responded well to simple stationary and moving stimuli such as spots, bars or slits of light. The latency of their response was 41 ± 6 ms. They were not directionally selective and responded to a large range of velocities.The neurons of the second type (Type II neurons) responded very poorly to simple visual stimuli and their activation required real objects or certain two-dimensional patterns. The mean latency of response of these units was 66 ± 26 ms. Habituation was always present. Type II neurons were located in the lower part of the superficial layers.The characteristics of Type II neurons suggest that in the primate superior colliculus there is a mechanism that allows the recognition of the complexity and the novelty of a stimulus and guides orienting responses to those stimuli that are worth analyzing in detail.This study was supported in part by NIH Grant 2 ROI EY00577 and in part by a grant from the Italian CNR. H.A.B. was supportet by a grant from Cassa di Risparmio di Parma     

Recovery of saccadic dysmetria following localized lesions in monkey superior colliculus

Damage to the monkey superior colliculus (SC) produces deficits in the generation of saccadic eye movements. Recovery of the accuracy of saccades is rapid, but saccadic latency and peak velocity recover slowly or not at all. In the present experiments we revisited the issue of recovery of function following localized lesions of the SC using three methodological advances: implantation of wire recording electrodes into the SC for the duration of the experiment to ensure that we were recording from the same site on the SC map on successive days; quantification of changes in saccadic accuracy, latency, and velocity using a standard grid of target points in the visual field contralateral to the SC lesion; measurement of movement field size to quantitatively determine any changes following the lesion. We confirmed a decrease in saccadic accuracy following electrolytic lesions of the SC, and we found that this dysmetria recovered within about 4 days. Saccadic latency increased for saccades to the lesion area and this deficit persisted. Peak saccadic velocity decreased immediately after the lesion and decreased further during the 10 days to 2 weeks of the experiment. We found no indication of an expansion of the movement fields of neurons adjacent to the lesion area. This lack of reorganization suggests that movement field changes within the SC cannot mediate the recovery in accuracy of the saccade. The persistence of the latency and velocity deficits despite the recovery of amplitude deficits indicates that saccadic latency and peak velocity are dependent upon the SC whereas saccadic amplitude is not.     

Eye and head movements evoked by electrical stimulation of monkey superior colliculus

Summary In unrestrained animals of many species, electrical stimulation at sites in the superior colliculus evokes motions of the head and eyes. Collicular stimulation in monkeys whose heads are rigidly fixed is known to elicit a saccade whose characteristics depend on the site stimulated and are largely independent of electrical stimulation parameters and initial eye position.This study examined what role the colliculus plays in the coding of head movements. A secondary aim was to demonstrate the effects of such electrical stimulation parameters as pulse frequency and intensity. Rhesus monkeys were free to move their heads in the horizontal plane; head and eye movements were monitored. As in previous studies, eye movements evoked by collicular stimulation were of short latency, repeatable, had a definite electrical threshold, and did not depend on the initial position of the eye in the orbit. By contrast, evoked head movements were extremely variable in size and latency, had no definite electrical threshold, and did depend on initial eye position. Thus when the eyes approached positions of extreme deviation, a head movement in the same direction became more likely. These results suggest that the superior colliculus does not directly code head movements in the monkey.     

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.     

Saccadic eye movements following injection of lidocaine into the superior colliculus

Summary 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. These experiments support the view that the SC normally conveys information on the amplitude and velocity of saccadic eye movements, but that gradual compensation can be made over time by other pathways when damage to the structure occurs.     

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     

Saccadic eye movements following kainic acid lesions of the pulvinar in monkeys

Summary Behavioral and anatomical experiments have suggested that the pulvinar might play a role in the generation of saccadic eye movements to visual targets. To test this idea, we trained monkeys to make visually-guided saccades by requiring them to detect the dimming of a small target. We used three different saccade paradigms. On single-step trials, saccades were made from a central fixation point (FP) to a target at 12, 24 or 36° to the left or right. On overlap trials, the FP remained lit during presentation of a target at 12 or 24°. On double-step trials, the target stepped first to 24°, and then back to 12° on the same side. Animals were trained to criterion, received kainic acid lesions of the pulvinar, and were retested on all three tasks. The lesions were very large, destroying almost all of the visually responsive pulvinar. They also encroached on the lateral geniculate nucleus, thereby producing small foveal scotomas, and this resulted in some behavioral changes, including difficulty in maintaining fixation on the target and in detecting its dimming. Results on the saccade tests suggest that the pulvinar is not crucial for initiation of saccadic eye movements. Saccade latency and amplitude were unimpaired on both single-step and overlap trials. Saccadic performance was also normal on double-step trials. In a second experiment, we measured the average length of fixations during spontaneous viewing of a complex visual scene. Fixation lengths did not differ from those of unoperated control monkeys. We suggest that the neglect, increased saccadic latencies, and prolonged fixations attributed to pulvinar damage in previous studies were probably the result instead of inadvertent damage to tectal afferents. The present results, together with single unit data, point to a role for the pulvinar not in the generation of saccades, but rather in the integration of saccadic eye movements with visual processing.     

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.     

Fusional vergence ranges of the monkey: A behavioral study

Summary Fusional vergence ranges were behaviorally determined for two rhesus monkeys and two human subjects using random dot stereograms as stimuli. The subject performed a two-alternative forced choice form discrimination of discretely presented stimuli and the fusional vergence stimulus was changed during the intertrial intervals. The fusional vergence measurements for the monkey were similar to those for the human subjects.     

Stimulation of the superior colliculus in the alert cat

Summary Electrical stimulation of the cat superior colliculus (SC), in conjunction with the accurate measurement of elicited eye movements and histologically verified electrode positions, has revealed a striking antero-posterior variation in collicular organization. Three zones could be defined in the SC on the basis of eye movement patterns and associated neck muscle EMG activity evoked from the deeper layers. The Anterior zone was coextensive with the central 25 ° of the visual retinotopically coded map contained in the superficial layers. Saccades evoked from this zone were also retinotopically coded, and the latency of EMG activity depended on the position of the eye in the orbit. A similar observation applies to the entire monkey SC. The Intermediate zone was coextensive with the 25 °–70 ° of visual projections. Saccades evoked from this region were goal-directed and were associated with invariant, short latency EMG responses. The Posterior zone was found in the extreme caudo-lateral portion of the SC. Eye movements evoked from this zone were centering saccades associated with constant latency EMG activity. The present results in conjunction with previously demonstrated antero-posterior variations in projections to the SC, suggest that the motor strategies controlling gaze shifts toward visual targets vary depending on the location of the target in the visual field.     

Comparison of the effects of superior colliculus and pulvinar lesions on visual search and tachistoscopic pattern discrimination in monkeys

Summary In order to investigate whether pulvinar lesions produce behavioral impairments similar to those that follow superior colliculus lesions, monkeys were tested on a visual search task before and after receiving radiofrequency lesions of either the superior colliculus or pulvinar. The animals searched for a small target pattern within an array of varying numbers of irrelevant patterns. After receiving colliculus lesions, the animals showed marked postoperative increases in either search time, percent errors, or both. By contrast, pulvinar lesions had little or no effect on visual search performance. Similarly, in learning to search for a target they had not previously seen, animals with colliculus lesions were impaired relative to unoperated controls, whereas pulvinar-lesioned animals did not differ from controls. In an attempt to confirm the finding that pulvinar lesions impair tachistoscopic pattern discrimination, we determined exposure-duration thresholds of pulvinar- and colliculus-lesioned monkeys for performance of a pattern discrimination. The thresholds of the colliculus-lesioned monkeys were elevated 20-fold relative to controls. By contrast, thresholds of the pulvinar-lesioned monkeys were normal. We conclude that the pulvinar is not critical for the attentional processes in which the superior colliculus participates.     

Target selection and saccade generation in monkey superior colliculus

The superior colliculus (SC) of the monkey has been shown to be involved in not only initiation of saccades but in the selection of the target to which the saccade can be directed. The present experiments examine whether SC neuronal activity related to target selection is also related to saccade generation. In an asynchronous target task, the monkey was required to make a saccade to the first of two spots of light to appear. Using choice probability analysis over multiple trials, we determined the earliest time at which neurons in the SC intermediate layers indicated target selection. We then determined how closely the neuronal selection was correlated to saccade onset by using our asynchronous reaction time task, which allowed the monkey to make a saccade to the target as soon as the selection had been made. We found that the selection became evident at widely differing times for different neurons. Some neurons indicated target selection just before the saccade (close to the pre-saccadic burst of activity), others did so at the time of the visual response, and some showed an increase in their activity even before the target appeared. A fraction of this pre-stimulus bias resulted from a priming effect of the previous trial; a saccade to the target in the movement field on the previous trial produced both a higher level of neuronal activity and a higher probability for a saccade to that target on the current trial. We found that most of the neurons (76%) showed a correlation between selection time and reaction time. Furthermore, within this 76% of neurons, many indicated a selection very early during the visual response. There was no evidence of a sequence from target selection first and saccade selection later, but rather that target selection and saccade initiation are intertwined and are probably inseparable.     

Adaptive changes in vergence eye movements induced by vergence-vestibular interaction training in monkeys

Clear vision of objects moving in three-dimensional space near an observer is attained by a combination of smooth-pursuit and vergence eye movements. The two systems must interact with the vestibular system to maintain the image of the object on the fovea. Previous studies showed that training with smooth-pursuit vestibular interactions resulted in adaptive changes in the smooth-pursuit response. Although vergence and smooth-pursuit systems are thought to have separate neural substrates, recent studies indicate that the caudal parts of the frontal eye fields that receive vestibular inputs contain neurons that discharge in response to combinations of smooth-pursuit and vergence. This combination of discharge sensitivities suggests the possibility that adaptive changes may be induced in the vergence system by vestibular inputs during vergence-pursuit training. To explore this possibility, we examined the effects of training with conflicting vestibular and vergence tracking in four head-stabilized monkeys. Animals were rewarded for tracking a laser spot that moved towards or away from them at 1 Hz in phase with sinusoidal whole-body rotation (±5°) in the pitch plane; the spot moved closer when the monkeys nose moved downward. From the monkeys point of view, the spot moved sinusoidally 10–66 cm in front of them along the mid-sagittal plane, requiring symmetrical vergence eye movements of 4.8° for each eye. Eye movements induced by equivalent spot motion at 0.3–1.0 Hz with or without chair rotation were examined before and after training for each session (0.5–1.0 h). Before training, pitch rotation alone in complete darkness did not induce vergence eye movements in any of the monkeys tested. Vergence tracking without chair rotation showed decreased gain and increased phase lag (re vergence target velocity) at frequencies above 0.5 Hz. After training, the vergence response during chair rotation with the spot showed significantly higher gains and smaller phase lags at 0.3–1.0 Hz in all monkeys. Pitch rotation alone in complete darkness induced vergence eye movements with gains (eye vergence/chair) of 0.15–0.35 after training in two monkeys. These results suggest that vestibular information can be used effectively to modify vergence tracking.     

Latency of adaptive vergence eye movements induced by vergence-vestibular interaction training in monkeys

Clear vision of objects that move in depth toward or away from an observer requires vergence eye movements. The vergence system must interact with the vestibular system to maintain the object images on the foveae of both eyes during head movement. Previous studies have shown that training with sinusoidal vergence-vestibular interaction improves the frequency response of vergence eye movements during pitch rotation: vergence eye velocity gains increase and phase-lags decrease. To further understand the changes in eye movement responses in this adaptation, we examined latencies of vergence eye movements before and after vergence-vestibular training. Two head-stabilized Japanese monkeys were rewarded for tracking a target spot moving in depth that required vergence eye movements of 10°/s. This target motion was synchronized with pitch rotation at 20°/s. Both target and chair moved in a trapezoidal waveform interspersed with random inter-trial intervals. Before training, pitch rotation in complete darkness without a target did not induce vergence eye movements. Mean latencies of convergence and divergence eye movements induced by vergence target motion alone were 182 and 169 ms, respectively. After training, mean latencies of convergence and divergence eye movements to a target synchronized with pitch rotation shortened to 65 and 53 ms, and vergence eye velocity gains (relative to vergence target velocity) at the normal latencies were 0.68 and 1.53, respectively. Pitch rotation alone without a target induced vergence eye movements with similar latencies after training. These results indicate that vestibular information can be used effectively to initiate vergence eye movements following vergence-vestibular training.     

Synaptic patterns in the superficial layers of the superior colliculus of the monkey,Macaca mulatta

Summary While the synaptic patterns studied with the electron microscope in the upper layers of the superior colliculus of the monkey are basically similar to those described for the rat, there are notable differences in the terminal patterns of the afferent pathways.The retinotectal pathway in monkeys terminates sparsely near the surface in the caudal part of the colliculus. Most of the terminals undergo an electron dense reaction in degeneration and are rapidly removed from their postsynaptic sites.The corticotectal pathway terminates heavily throughout superficial layers making both axodendritic and serial synaptic connections. The terminals undergo neurofilamentous and dense degenerative reactions.It is suggested from a comparison of the retinotectal and retinogeniculate pathways that terminals which undergo the neurofilamentous degenerative reaction belong to a different population of axons from those undergoing only the dense reaction.     

Contralateral cortical projections to the superior colliculus in the macaque monkey

Summary Cortical projections from the contralateral hemisphere to the superior colliculus (SC) were studied in macaque monkey using retrograde transport of the enzyme horseradish peroxidase (HRP). After single or multiple injections of HRP into SC, labelled cells were found contralaterally in layer V of the anterior bank of the arcuate sulcus, the origin of this contralateral projection being confined to the anterior part of Brodmann's area 6. Only a few labelled cells appeared in adjacent area 8. Labelled cells occured in patches, forming bands which were found to run in a ventromedial direction. A similar pattern was seen homotopically in ipsilateral area 6. Thus, this anterior part of area 6 gives rise to a bilateral projection to the SC. The findings emphasize structural differences in a region of the frontal lobe which has been considered functionally uniform as frontal eye field.Supported by Deutsche Forschungsgemeinschaft (SFB 50/C6 and Di 212/2)     

Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements

The intermediate and deep layers of the monkey superior colliculus (SC) comprise a retinotopically organized map for eye movements. The rostral end of this map, corresponding to the representation of the fovea, contains neurons that have been referred to as "fixation cells" because they discharge tonically during active fixation and pause during the generation of most saccades. These neurons also possess movement fields and are most active for targets close to the fixation point. Because the parafoveal locations encoded by these neurons are also important for guiding pursuit eye movements, we studied these neurons in two monkeys as they generated smooth pursuit. We found that fixation cells exhibit the same directional preferences during pursuit as during small saccades-they increase their discharge during movements toward the contralateral side and decrease their discharge during movements toward the ipsilateral side. This pursuit-related activity could be observed during saccade-free pursuit and was not predictive of small saccades that often accompanied pursuit. When we plotted the discharge rate from individual neurons during pursuit as a function of the position error associated with the moving target, we found tuning curves with peaks within a few degrees contralateral of the fovea. We compared these pursuit-related tuning curves from each neuron to the tuning curves for a saccade task from which we separately measured the visual, delay, and peri-saccadic activity. We found the highest and most consistent correlation with the delay activity recorded while the monkey viewed parafoveal stimuli during fixation. The directional preferences exhibited during pursuit can therefore be attributed to the tuning of these neurons for contralateral locations near the fovea. These results support the idea that fixation cells are the rostral extension of the buildup neurons found in the more caudal colliculus and that their activity conveys information about the size of the mismatch between a parafoveal stimulus and the currently foveated location. Because the generation of pursuit requires a break from fixation, the pursuit-related activity indicates that these neurons are not strictly involved with maintaining fixation. Conversely, because activity during the delay period was found for many neurons even when no eye movement was made, these neurons are also not obligatorily related to the generation of a movement. Thus the tonic activity of these rostral neurons provides a potential position-error signal rather than a motor command-a principle that may be applicable to buildup neurons elsewhere in the SC.     

Extraretinal inputs to neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements.

The intermediate and deep layers of the monkey superior colliculus (SC) are known to be important for the generation of saccadic eye movements. Recent studies have also provided evidence that the rostral SC might be involved in the control of pursuit eye movements. However, because rostral SC neurons respond to visual stimuli used to guide pursuit, it is also possible that the pursuit-related activity is simply a visual response. To test this possibility, we recorded the activity of neurons in the rostral SC as monkeys smoothly pursued a target that was briefly extinguished. We found that almost all rostral SC neurons in our sample maintained their pursuit-related activity during a brief visual blink, which was similar to the maintained activity they also exhibited during blinks imposed during fixation. These results indicate that discharge of rostral SC neurons during pursuit is not simply a visual response, but includes extraretinal signals.