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.

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 Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements

2016 ◽  
Vol 116 (6) ◽  
pp. 2882-2891 ◽  
Author(s):  
Rebecca M. Krock ◽  
Tirin Moore
Keyword(s):  
Visual Cortex ◽  
Eye Movements ◽  
Saccadic Eye Movements ◽  
Visual Sensitivity ◽  
Saccadic Suppression ◽  
Frontal Eye Field ◽  
Visually Guided ◽  
Visual Neurons ◽  
Saccade Onset ◽  
Eye Field

Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques ( Macaca mulatta). We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining ∼80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression.

Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons

1992 ◽  
Vol 68 (6) ◽  
pp. 1967-1985 ◽  
Author(s):  
M. A. Segraves
Keyword(s):  
Electrical Stimulation ◽  
Visual Stimulation ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Burst Neurons ◽  
Eye Field ◽  
Movement Field ◽  
Omnipause Neurons ◽  
Stimulation Of

1. This study identified neurons in the rhesus monkey's frontal eye field that projected to oculomotor regions of the pons and characterized the signals sent by these neurons from frontal eye field to pons. 2. In two behaving rhesus monkeys, frontal eye field neurons projecting to the pons were identified via antidromic excitation by a stimulating microelectrode whose tip was centered in or near the omnipause region of the pontine raphe. This stimulation site corresponded to the nucleus raphe interpositus (RIP). In addition, electrical stimulation of the frontal eye field was used to demonstrate the effects of frontal eye field input on neurons in the omnipause region and surrounding paramedian pontine reticular formation (PPRF). 3. Twenty-five corticopontine neurons were identified and characterized. Most frontal eye field neurons projecting to the pons were either movement neurons, firing in association with saccadic eye movements (48%), or foveal neurons responsive to visual stimulation of the fovea combined with activity related to fixation (28%). Corticopontine movement neurons fired before, during, and after saccades made within a restricted movement field. 4. The activity of identified corticopontine neurons was very similar to the activity of neurons antidromically excited from the superior colliculus where 59% had movement related activity, and 22% had foveal and fixation related activity. 5. High-intensity, short-duration electrical stimulation of the frontal eye field caused omnipause neurons to stop firing. The cessation in firing appeared to be immediate, within < or = 5 ms. The time that the omnipause neuron remained quiet depended on the intensity of the cortical stimulus and lasted up to 30 ms after a train of three stimulus pulses lasting a total of 6 ms at an intensity of 1,000 microA. Low-intensity, longer duration electrical stimuli (24 pulses, 75 microA, 70 ms) traditionally used to evoke saccades from the frontal eye field were also followed by a cessation in omnipause neuron firing, but only after a delay of approximately 30 ms. For these stimuli, the omnipause neuron resumed firing when the stimulus was turned off. 6. The same stimuli that caused omnipause neurons to stop firing excited burst neurons in the PPRF. The latency to excitation ranged from 4.2 to 9.8 ms, suggesting that there is at least one additional neuron between frontal eye field neurons and burst neurons in the PPRF. 7. The present study confirms and extends the results of previous work, with the use of retrograde and anterograde tracers, demonstrating direct projections from the frontal eye field to the pons.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Suppression of Visually and Memory-Guided Saccades Induced by Electrical Stimulation of the Monkey Frontal Eye Field. II. Suppression of Bilateral Saccades

2004 ◽  
Vol 92 (4) ◽  
pp. 2261-2273 ◽  
Author(s):  
Yoshiko Izawa ◽  
Hisao Suzuki ◽  
Yoshikazu Shinoda
Keyword(s):  
Electrical Stimulation ◽  
Superior Colliculus ◽  
Reticular Formation ◽  
Neural Mechanism ◽  
Frontal Eye Field ◽  
Pontine Reticular Formation ◽  
Visually Guided ◽  
Saccade Onset ◽  
Eye Field ◽  
Stimulation Of

To understand the neural mechanism of fixation, we investigated effects of electrical stimulation of the frontal eye field (FEF) and its vicinity on visually guided (Vsacs) and memory-guided saccades (Msacs) in trained monkeys and found that there were two types of suppression induced by the electrical stimulation: suppression of ipsilateral saccades and suppression of bilateral saccades. In this report, we characterized the properties of the suppression of bilateral Vsacs and Msacs. Stimulation of the bilateral suppression sites suppressed the initiation of both Vsacs and Msacs in all directions during and ∼50 ms after stimulation but did not affect the vector of these saccades. The suppression was stronger for ipsiversive larger saccades and contraversive smaller saccades, and saccades with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for the suppression of ipsilateral and contralateral Vsacs was ∼40–50 ms before saccade onset, indicating that the suppression occurred most likely in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of bilateral saccades were located in the prearcuate gyrus facing the inferior arcuate sulcus where stimulation induced suppression at ≤40 μA but usually did not evoke any saccades at 80 μA and were different from those of ipsilateral saccades where stimulation evoked saccades at ≤50 μA. The bilateral suppression sites contained fixation neurons. The results suggest that fixation neurons in the bilateral suppression area of the FEF may play roles in maintaining fixation by suppressing saccades in all directions.

scholarly journals Frontal Eye Field Neurons Orthodromically Activated From the Superior Colliculus

1998 ◽  
Vol 80 (6) ◽  
pp. 3331-3335 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz
Keyword(s):  
Electrical Stimulation ◽  
Superior Colliculus ◽  
Direct Evidence ◽  
Visual Stimulation ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Anatomical Studies ◽  
Eye Field ◽  
To Receive ◽  
Stimulation Of

Sommer, Marc A. and Robert H. Wurtz. Frontal eye field neurons orthodromically activated from the superior colliculus. J. Neurophysiol. 80: 3331–3333, 1998. Anatomical studies have shown that the frontal eye field (FEF) and superior colliculus (SC) of monkeys are reciprocally connected, and a physiological study described the signals sent from the FEF to the SC. Nothing is known, however, about the signals sent from the SC to the FEF. We physiologically identified and characterized FEF neurons that are likely to receive input from the SC. Fifty-two FEF neurons were found that were orthodromically activated by electrical stimulation of the intermediate or deeper layers of the SC. All the neurons that we tested ( n = 34) discharged in response to visual stimulation. One-half also discharged when saccadic eye movements were made. This provides the first direct evidence that the ascending pathway from SC to FEF might carry visual- and saccade-related signals. Our findings support a hypothesis that the SC and the FEF interact bidirectionally during the events leading up to saccade generation.

Deficits in eye movements following frontal eye-field and superior colliculus ablations

1980 ◽  
Vol 44 (6) ◽  
pp. 1175-1189 ◽  
Author(s):  
P. H. Schiller ◽  
S. D. True ◽  
J. L. Conway
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Superior Colliculus ◽  
Saccadic Eye Movements ◽  
The Other ◽  
Frontal Eye Field ◽  
Saccade Velocity ◽  
Eye Field ◽  
Parallel Channels ◽  
Coil Method

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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