Contribution of the Frontal Eye Field to Gaze Shifts in the Head-Unrestrained Monkey: Effects of Microstimulation

2007 ◽  
Vol 97 (1) ◽  
pp. 618-634 ◽  
Author(s):  
Thomas A. Knight ◽  
Albert F. Fuchs
Keyword(s):  
Eye Movements ◽  
Stimulus Duration ◽  
Head Movement ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Threshold Region ◽  
Gaze Shifts ◽  
Eye Field ◽  
Orbital Position

The role of the primate frontal eye field (FEF) has been inferred primarily from experiments investigating saccadic eye movements with the head restrained. Three recent reports investigating head-unrestrained gaze shifts disagree on whether head movements are evoked with FEF stimulation and thus whether the FEF participates in gaze movement commands. We therefore examined the eye, head, and overall gaze movement evoked by low-intensity microstimulation of the low-threshold region of the FEF in two head-unrestrained monkeys. Microstimulation applied at 200 or 350 Hz for 200 ms evoked large gaze shifts with substantial head movement components from most sites in the dorsomedial FEF, but evoked small, predominantly eye-only gaze shifts from ventrolateral sites. The size and direction of gaze and eye movements were strongly affected by the eye position before stimulation. Head movements exhibited little position dependency, but at some sites and initial eye positions, head-only movements were evoked. Stimulus-evoked gaze shifts and their eye and head components resembled those elicited naturally by visual targets. With stimulus train durations >200 ms, the evoked gaze shifts were more likely to be accomplished with a substantial head movement, which often continued for the entire stimulus duration. The amplitude, duration and peak velocity of the evoked head movement were more strongly correlated with stimulus duration than were those of the gaze or eye movements. We conclude that the dorsomedial FEF generates a gaze command signal that can produce eye, head, or combined eye–head movement depending on the initial orbital position of the eye.

scholarly journals Electrical Stimulation of the Frontal Eye Field in a Monkey Produces Combined Eye and Head Movements

2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Eye Field ◽  
A Site ◽  
Head Rotations ◽  
Stimulation Of

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.

Subcortical contributions to head movements in macaques. I. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus

1994 ◽  
Vol 72 (6) ◽  
pp. 2648-2664 ◽  
Author(s):  
R. J. Cowie ◽  
D. L. Robinson
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Superior Colliculus ◽  
Head Movement ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Reticular Nucleus ◽  
Gaze Shifts ◽  
Gigantocellular Reticular Nucleus ◽  
External Events

1. These studies were initiated to understand the neural sites and mechanisms controlling head movements during gaze shifts. Gaze shifts are made by saccadic eye movements with and without head movements. Sites were stimulated electrically within the brain stem of awake, trained monkeys relatively free to make head movements to study the head-movement components of gaze shifts. 2. Electrical stimulation in and around the gigantocellular reticular nucleus evoked head movements in the ipsilateral direction. Gaze shifts were never evoked from these sites, presumably because the vestibulo-ocular reflex compensated. The rough topography of this region included large head movements laterally, small movements medially, downward movements from dorsal sites, and upward movements more ventrally. 3. The initial position of the head influenced the magnitude of the elicited movement with larger movements produced when the head was directed to the contralateral side. Attentive fixation was associated with larger and faster head movements when compared with those evoked during spontaneous behavior. 4. The superior colliculus makes a significant contribution to gaze shifts and has been shown to contribute to head movements. Because the colliculus is a major source of afferents to the gigantocellular reticular nucleus, comparable stimulation studies of the superior colliculus were conducted. When the colliculus was excited, shifts of gaze in the contralateral direction were predominant. These were most often accomplished by saccadic eye movements, however, we frequently elicited head movements that had an average latency 10 ms longer than those elicited from the reticular head movement region. Sites evoking head movements tended to be deeper and more caudal than loci eliciting eye movements. Neither the onset latencies, amplitudes, nor peak velocities of head movements and eye movements were correlated. Gaze shifts evoked from the caudal colliculus with the head free were larger than those elicited from the same site with the head fixed. 5. These studies demonstrate that both the superior colliculus and gigantocellular reticular nucleus mediate head movements. The colliculus plays a role in orienting to external events, and so collicular head movements predominantly were associated with gaze shifts, with the eye and head movements uncoupled. The medullary reticular system may play a role in the integration of a wider range of movements. Head movements from the medullary reticular sites probably participate in several forms of head movements, such as those that are related to postural reflexes, started volitionally, and/or oriented to external events.

Electrical Stimulation of the Frontal Eye Fields in the Head-Free Macaque Evokes Kinematically Normal 3D Gaze Shifts

2010 ◽  
Vol 104 (6) ◽  
pp. 3462-3475 ◽  
Author(s):  
Jachin A. Monteon ◽  
Alina G. Constantin ◽  
Hongying Wang ◽  
Julio Martinez-Trujillo ◽  
J. Douglas Crawford
Keyword(s):  
Target Selection ◽  
Three Dimensional ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Velocity Amplitude ◽  
Eye Field ◽  
Head Rotations ◽  
Stimulation Of

The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30–100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity–amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listing's law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listing's plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye–head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye–head coordination are likely specified by downstream mechanisms.

Suppression of Task-Related Saccades by Electrical Stimulation in the Primate's Frontal Eye Field

1997 ◽  
Vol 77 (5) ◽  
pp. 2252-2267 ◽  
Author(s):  
Douglas D. Burman ◽  
Charles J. Bruce
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Frontal Lobe ◽  
Premotor Cortex ◽  
Saccadic Eye Movements ◽  
Association Cortex ◽  
Frontal Eye Field ◽  
Visually Guided ◽  
Low Intensity ◽  
Eye Field

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.

Eye-head coordination in cats

1984 ◽  
Vol 52 (6) ◽  
pp. 1030-1050 ◽  
Author(s):  
D. Guitton ◽  
R. M. Douglas ◽  
M. Volle
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Head Movement ◽  
Maximum Velocity ◽  
Head Movements ◽  
Visual Axis ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Rapid Eye Movements ◽  
Motor Strategy

Gaze is the position of the visual axis in space and is the sum of the eye movement relative to the head plus head movement relative to space. In monkeys, a gaze shift is programmed with a single saccade that will, by itself, take the eye to a target, irrespective of whether the head moves. If the head turns simultaneously, the saccade is correctly reduced in size (to prevent gaze overshoot) by the vestibuloocular reflex (VOR). Cats have an oculomotor range (OMR) of only about +/- 25 degrees, but their field of view extends to about +/- 70 degrees. The use of the monkey's motor strategy to acquire targets lying beyond +/- 25 degrees requires the programming of saccades that cannot be physically made. We have studied, in cats, rapid horizontal gaze shifts to visual targets within and beyond the OMR. Heads were either totally unrestrained or attached to an apparatus that permitted short unexpected perturbations of the head trajectory. Qualitatively, similar rapid gaze shifts of all sizes up to at least 70 degrees could be accomplished with the classic single-eye saccade and a saccade-like head movement. For gaze shifts greater than 30 degrees, this classic pattern frequently was not observed, and gaze shifts were accomplished with a series of rapid eye movements whose time separation decreased, frequently until they blended into each other, as head velocity increased. Between discrete rapid eye movements, gaze continued in constant velocity ramps, controlled by signals added to the VOR-induced compensatory phase that followed a saccade. When the head was braked just prior to its onset in a 10 degrees gaze shift, the eye attained the target. This motor strategy is the same as that reported for monkeys. However, for larger target eccentricities (e.g., 50 degrees), the gaze shift was interrupted by the brake and the average saccade amplitude was 12-15 degrees, well short of the target and the OMR. Gaze shifts were completed by vestibularly driven eye movements when the head was released. Braking the head during either quick phases driven by passive head displacements or visually triggered saccades resulted in an acceleration of the eye, thereby implying interaction between the VOR and these rapid-eye-movement signals. Head movements possessed a characteristic but task-dependent relationship between maximum velocity and amplitude. Head movements terminated with the head on target. The eye saccade usually lagged the head displacement.(ABSTRACT TRUNCATED AT 400 WORDS)

Muscimol-Induced Inactivation of Monkey Frontal Eye Field: Effects on Visually and Memory-Guided Saccades

1999 ◽  
Vol 81 (5) ◽  
pp. 2191-2214 ◽  
Author(s):  
Elisa C. Dias ◽  
Mark A. Segraves
Keyword(s):  
Eye Movements ◽  
Target Location ◽  
Memory Task ◽  
Saccadic Eye Movements ◽  
Spatial Location ◽  
Frontal Eye Field ◽  
Visually Guided ◽  
Field Effects ◽  
Progressive Loss ◽  
Eye Field

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.

scholarly journals Coupling Between Horizontal and Vertical Components of Saccadic Eye Movements During Constant Amplitude and Direction Gaze Shifts in the Rhesus Monkey

2008 ◽  
Vol 100 (6) ◽  
pp. 3375-3393 ◽  
Author(s):  
Edward G. Freedman
Keyword(s):  
Eye Movements ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Horizontal Meridian ◽  
Constant Amplitude ◽  
Saccade Amplitude ◽  
Gaze Shifts ◽  
Horizontal Saccade ◽  
Vertical Saccade ◽  
Saccade Duration

When the head is free to move, changes in the direction of the line of sight (gaze shifts) can be accomplished using coordinated movements of the eyes and head. During repeated gaze shifts between the same two targets, the amplitudes of the saccadic eye movements and movements of the head vary inversely as a function of the starting positions of the eyes in the orbits. In addition, as head-movement amplitudes and velocities increase, saccade velocities decline. Taken together these observations lead to a reversal in the expected correlation between saccade duration and amplitude: small-amplitude saccades associated with large head movements can have longer durations than larger-amplitude saccades associated with small head movements. The data in this report indicate that this reversal occurs during gaze shifts along the horizontal meridian and also when considering the horizontal component of oblique saccades made when the eyes begin deviated only along the horizontal meridian. Under these conditions, it is possible to determine whether the variability in the duration of the constant amplitude vertical component of oblique saccades is accounted for better by increases in horizontal saccade amplitude or increases in horizontal saccade duration. Results show that vertical saccade duration can be inversely related to horizontal saccade amplitude (or unrelated to it) but that horizontal saccade duration is an excellent predictor of vertical saccade duration. Modifications to existing hypotheses of gaze control are assessed based on these new observations and a mechanism is proposed that can account for these data.

Head Movement Evoked By Electrical Stimulation in the Supplementary Eye Field of the Rhesus Monkey

2005 ◽  
Vol 94 (6) ◽  
pp. 4502-4519 ◽  
Author(s):  
L. Longtang Chen ◽  
Mark M. G. Walton
Keyword(s):  
Head Movement ◽  
Direct Evidence ◽  
Head Movements ◽  
Eye Position ◽  
Low Velocity ◽  
Gaze Shifts ◽  
The Gaze ◽  
Supplementary Eye Field ◽  
Combined Movements ◽  
Eye Field

Although the supplementary eye field (SEF) has been implicated in the control of head movements associated with gaze shifts, there is no direct evidence that SEF plays a role in the generation of head movements independent of gaze. If the SEF does, varying the duration of stimulation should selectively alter the head-movement kinematics during the postgaze-shift period. The duration of the stimulation was manipulated while head-unrestrained monkeys maintained stable head forward postures. The initial positions of the eyes in the orbits were systematically varied. Although combined movements of the eyes and head were produced in the majority of the trials, head movements were sometimes evoked in the absence of gaze shifts. These head-alone movements were most frequent when the initial eye position was contralateral to the stimulated side. When the stimulation produced eye and head movements, gaze onset was sometimes preceded by a relatively low-velocity phase of the head movement. Evoked head movements were primarily horizontal, unlike the gaze shifts, which typically had vertical components that varied according to the initial positions of the eyes in the orbits. The postgaze-shift head movements tended to be of low velocity and in many cases persisted until stimulation offset. In general, prolonging the stimulation resulted in improved centering of the eyes in the orbits. These findings suggest that, in addition to its previously described role in the generation of coordinated eye-head gaze shifts, the SEF is also involved in the control of head movements in the absence of a change of gaze.

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