Effect of eye position within the orbit on electrically elicited saccadic eye movements: a comparison of the macaque monkey's frontal and supplementary eye fields

1993 ◽  
Vol 69 (3) ◽  
pp. 800-818 ◽  
Author(s):  
G. S. Russo ◽  
C. J. Bruce

1. We quantitatively compared the effects of eye position within the orbit on saccadic eye movements electrically elicited from two oculomotor areas of the macaque monkey's frontal lobe cortex: the frontal eye field (FEF) and the supplementary eye field (SEF). 2. The effect of eye position on electrically elicited saccades was studied by delivering 70-ms trains of intracortical microstimulation while the monkeys fixated a spot of light. Tests of different fixation points located across a rectangular array were randomly intermixed. Complete experiments were carried out on 38 sites in three FEFs of two monkeys and 59 sites from three SEFs of the same two monkeys. Stimulation currents for the array experiments were usually 10–20 microA above the site threshold; the average current used was 36 microA for FEF and 49 microA for SEF. 3. The magnitude of effect of the initial eye position on the elicited saccade's dimensions was quantified at each site by computing the linear regression of saccadic eye movement displacement on the eye position within the orbit when stimulation was applied. This computation was done separately for the horizontal and vertical axes. We call the resulting pair of regression coefficients “orbital perturbation indexes.” Indexes of 0.0 represent elicited saccades that do not change their trajectory with different initial eye positions (constant-vector saccades), whereas indexes of -1.0 represent elicited saccades that end at the same orbital position regardless of initial eye position (goal-directed saccades). 4. The effect of eye position varied across sites. In both FEF and SEF, the orbital perturbation indexes were distributed between approximately 0.0 and -0.5, with the horizontal and vertical indexes highly correlated across sites. 5. The average orbital perturbation indexes were small for both eye fields and were not significantly different. The mean horizontal indexes were -0.13 and -0.16 for SEF and FEF, respectively. The mean vertical indexes were -0.16 and -0.13. Neither SEF versus FEF difference was statistically significant. 6. In both SEF and FEF, sites yielding larger-amplitude saccades generally had larger orbital effects than sites yielding smaller saccades. This relationship accounted for the majority of the variability of the orbital perturbation indexes across sites in both SEF and FEF. 7. These results indicate that SEF and FEF are not distinguished from each other by the orbital dependence of their electrically elicited saccades. Thus they do not confirm the previously hypothesized dichotomy that FEF codes constant-vector saccades and SEF codes goal-directed saccades.(ABSTRACT TRUNCATED AT 400 WORDS)

1996 ◽  
Vol 76 (2) ◽  
pp. 825-848 ◽  
Author(s):  
G. S. Russo ◽  
C. J. Bruce

1. We investigated whether neurons in the supplementary eye field (SEF) of macaque monkeys code saccadic eye movements in oculocentric coordinates (relative to the current direction of fixation) or in craniocentric coordinates (relative to the head). Craniocentric coding in SEF had been previously suggested by the convergent appearance of electrically elicited saccades originating at different orbital positions. 2. We primarily studied SEF neurons that started responding before the beginning of saccades because such presaccadic activity is likely related to saccade generation and metrics. Using a memory-saccade task, we classified the presaccadic activity of each neuron as either purely visual related, purely movement related, or both visual and movement related. 3. We then mapped the response fields (receptive fields and movement fields) of SEF neurons from different orbital positions. When mapped relative to a central fixation point, the strongest responses for a given SEF neuron invariably occurred for a particular polar direction with fairly symmetrical declines for departures from that direction. When tested using other fixation point locations, their strongest responses almost always continued to occur for stimuli having the same polar direction relative to each fixation point tested, and thus they appeared to code both stimulus direction and saccade direction in an oculocentric coordinate system. 4. The effect of eye position on SEF presaccadic activity was quantified in two ways by computing, for each neuron, 1) an "intersection distance," the eccentricity of the point where extensions of the neuron's optimal polar directions measured at two eccentric orbital positions converged, and 2) an "orbital perturbation index" such that an index of 0 corresponded to no change in the neuron's optimal polar direction across different orbital positions (i.e., perfectly oculocentric response fields) and an index of 1 corresponded to optimal polar directions that converged to the same craniocentric goal regardless of initial eye position (i.e., perfectly craniocentric response fields). For neurons with both visual and movement responses, these measures were calculated separately for each type of activity using tasks that temporally separated the visual cue presentation and the saccade to it. 5. Almost all of the intersection distances were well beyond the oculomotor range (+/- 50 degrees) of the monkey (38/39 for movement activity and 62/66 for visual activity). The median intersection distance for visual activity was very large (274 degrees), and the median for movement activity was slightly divergent (beyond infinity). Thus SEF neurons rarely showed a conspicuous convergence of response field direction. 6. Likewise, the mean orbital perturbation indexes were very small (-0.04 +/- 0.21, mean +/- SD, for movement activity and 0.09 +/- 0.15 for visual activity), also indicating that SEF neurons code stimuli and saccades in an oculocentric manner. 7. For neurons with both visual and movement activities, the orbital perturbation indexes of the two activities were not significantly correlated (r = 0.16), even though their characteristic directions (optimal polar direction estimated from the center of the screen) were almost the same (circular correlation, r+ = 0.97). The lack of a significant correlation between the visual and movement activity orbital perturbation indexes is consistent with the hypothesis that most of the variation in this index represents statistically independent errors of measurement. Conversely, the strong covariation of visual and movement activity characteristic directions indicates that directional preference is a fundamental functional property of SEF presaccadic activity.(ABSTRACT TRUNCATED)


1999 ◽  
Vol 82 (1) ◽  
pp. 463-471 ◽  
Author(s):  
Laurent Petit ◽  
James V. Haxby

We have investigated the functional anatomy of pursuit eye movements in humans with functional magnetic imaging. The performance of pursuit eye movements induced activations in the cortical eye fields also activated during the execution of visually guided saccadic eye movements, namely in the precentral cortex [frontal eye field (FEF)], the medial superior frontal cortex (supplementary eye field), the intraparietal cortex (parietal eye field), and the precuneus, and at the junction of occipital and temporal cortex (MT/MST) cortex. Pursuit-related areas could be distinguished from saccade-related areas both in terms of spatial extent and location. Pursuit-related areas were smaller than their saccade-related counterparts, three of eight significantly so. The pursuit-related FEF was usually inferior to saccade-related FEF. Other pursuit-related areas were consistently posterior to their saccade-related counterparts. The current findings provide the first functional imaging evidence for a distinction between two parallel cortical systems that subserve pursuit and saccadic eye movements in humans.


1993 ◽  
Vol 10 (2) ◽  
pp. 385-393 ◽  
Author(s):  
Jeffrey D. Schall ◽  
Anne Morel ◽  
Jon H. Kaas

AbstractTwo discrete areas in frontal cortex are involved in generating saccadic eye movements—the frontal eye field (FEF) and the supplementary eye field (SEF). Whereas FEF represents saccades in a topographic retinotopic map, recent evidence indicates that saccades may be represented craniotopically in SEF. To further investigate the relationship between these areas, the topographic organization of afferents to FEF from SEF in Macaco mulatto was examined by placing injections of distinct retrograde tracers into different parts of FEF that represented saccades of different amplitudes. Central FEF (lateral area 8A), which represents saccades of intermediate amplitudes, received afferents from a larger portion of SEF than did lateral FEF (area 45), which represents shorter saccades, or medial FEF (medial area 8A), which represents the longest saccades in addition to pinna movements. Moreover, in every case the zone in SEF that innervated lateral FEF (area 45) also projected to medial FEF (area 8A). In one case, a zone in rostral SEF projected to both lateral area 8A from which eye movements were evoked by microstimulation as well as medial area 8A from which pinna movements were elicited by microstimulation. This pattern of afferent convergence and divergence from SEF onto the retinotopic saccade map in FEF is indicative of some sort of map transformation between SEF and FEF. Such a transformation would be necessary to interconnect a topographic craniotopic saccade representation in SEF with a topographic retinotopic saccade representation in FEF.


1987 ◽  
Vol 57 (4) ◽  
pp. 1033-1049 ◽  
Author(s):  
P. H. Schiller ◽  
J. H. Sandell ◽  
J. H. Maunsell

Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS)


1997 ◽  
Vol 77 (5) ◽  
pp. 2252-2267 ◽  
Author(s):  
Douglas D. Burman ◽  
Charles J. Bruce

Burman, Douglas D. and Charles J. Bruce. Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J. Neurophysiol. 77: 2252–2267, 1997. Patients with frontal lobe damage have difficulty suppressing reflexive saccades to salient visual stimuli, indicating that frontal lobe neocortex helps to suppress saccades as well as to produce them. In the present study, a role for the frontal eye field (FEF) in suppressing saccades was demonstrated in macaque monkeys by application of intracortical microstimulation during the performance of a visually guided saccade task, a memory prosaccade task, and a memory antisaccade task. A train of low-intensity (20–50 μA) electrical pulses was applied simultaneously with the disappearance of a central fixation target, which was always the cue to initiate a saccade. Trials with and without stimulation were compared, and significantly longer saccade latencies on stimulation trials were considered evidence of suppression. Low-intensity stimulation suppressed task-related saccades at 30 of 77 sites tested. In many cases saccades were suppressed throughout the microstimulation period (usually 450 ms) and then executed shortly after the train ended. Memory-guided saccades were most dramatically suppressed and were often rendered hypometric, whereas visually guided saccades were less severely suppressed by stimulation. At 18 FEF sites, the suppression of saccades was the only observable effect of electrical stimulation. Contraversive saccades were usually more strongly suppressed than ipsiversive ones, and cells recorded at such purely suppressive sites commonly had either foveal receptive fields or postsaccadic responses. At 12 other FEF sites at which saccadic eye movements were elicited at low thresholds, task-related saccades whose vectors differed from that of the electrically elicited saccade were suppressed by electrical stimulation. Such suppression at saccade sites was observed even with currents below the threshold for eliciting saccades. Pure suppression sites tended to be located near or in the fundus, deeper in the anterior bank of the arcuate than elicited saccade sites. Stimulation in the prefrontal association cortex anterior to FEF did not suppress saccades, nor did stimulation in premotor cortex posterior to FEF. These findings indicate that the primate FEF can help orchestrate saccadic eye movements by suppressing inappropriate saccade vectors as well as by selecting, specifying, and triggering appropriate saccades. We hypothesize that saccades could be suppressed both through local FEF interactions and through FEF projections to subcortical regions involved in maintaining fixation.


2007 ◽  
Vol 45 (5) ◽  
pp. 997-1008 ◽  
Author(s):  
Andrew Parton ◽  
Parashkev Nachev ◽  
Timothy L. Hodgson ◽  
Dominic Mort ◽  
David Thomas ◽  
...  

1999 ◽  
Vol 81 (5) ◽  
pp. 2191-2214 ◽  
Author(s):  
Elisa C. Dias ◽  
Mark A. Segraves

Muscimol-induced inactivation of the monkey frontal eye field: effects on visually and memory-guided saccades. Although neurophysiological, anatomic, and imaging evidence suggest that the frontal eye field (FEF) participates in the generation of eye movements, chronic lesions of the FEF in both humans and monkeys appear to cause only minor deficits in visually guided saccade generation. Stronger effects are observed when subjects are tested in tasks with more cognitive requirements. We tested oculomotor function after acutely inactivating regions of the FEF to minimize the effects of plasticity and reallocation of function after the loss of the FEF and gain more insight into the FEF contribution to the guidance of eye movements in the intact brain. Inactivation was induced by microinjecting muscimol directly into physiologically defined sites in the FEF of three monkeys. FEF inactivation severely impaired the monkeys’ performance of both visually guided and memory-guided saccades. The monkeys initiated fewer saccades to the retinotopic representation of the inactivated FEF site than to any other location in the visual field. The saccades that were initiated had longer latencies, slower velocities, and larger targeting errors than controls. These effects were present both for visually guided and for memory-guided saccades, although the memory-guided saccades were more disrupted. Initially, the effects were restricted spatially, concentrating around the retinotopic representation at the center of the inactivated site, but, during the course of several hours, these effects spread to flanking representations. Predictability of target location and motivation of the monkey also affected saccadic performance. For memory-guided saccades, increases in the time during which the monkey had to remember the spatial location of a target resulted in further decreases in the accuracy of the saccades and in smaller peak velocities, suggesting a progressive loss of the capacity to maintain a representation of target location in relation to the fovea after FEF inactivation. In addition, the monkeys frequently made premature saccades to targets in the hemifield ipsilateral to the injection site when performing the memory task, indicating a deficit in the control of fixation that could be a consequence of an imbalance between ipsilateral and contralateral FEF activity after the injection. There was also a progressive loss of fixation accuracy, and the monkeys tended to restrict spontaneous visual scanning to the ipsilateral hemifield. These results emphasize the strong role of the FEF in the intact monkey in the generation of all voluntary saccadic eye movements, as well as in the control of fixation.


1980 ◽  
Vol 44 (6) ◽  
pp. 1175-1189 ◽  
Author(s):  
P. H. Schiller ◽  
S. D. True ◽  
J. L. Conway

1. This study investigated the effects of frontal eye-field and superior colliculus ablations on fixation patterns and saccadic eye movements. Monkeys were trained to pick apple pieces out of a multiple-slotted apple board while their heads were fixed. Eye movement records were obtained using predominantly the implanted search-coil method. 2. Both unilateral and bilateral frontal eye-field lesions produced only temporary deficits in eye movements. Following surgery monkeys tended to neglect the contralateral peripheral visual field and made fewer saccades to peripheral targets. Recovery was virtually completed in 2-4 wk. 3. Superior colliculus ablation reduced fixation accuracy, saccade frequency, and saccade velocity. These deficits showed little recovery with time. 4. Paired frontal eye-field and superior colliculus lesions produced dramatic deficits in visually triggered eye movements. Animals could no longer fixate their eyes on visual targets with any degree of accuracy. The range of eye movements was greatly reduced, as was the frequency and velocity of saccades. These deficits showed little recovery with time. 5. These results suggest that visually triggered saccadic eye movements are controlled by two parallel channels, one involving the superior colliculus and the other the frontal eye field.


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