Frontal Eye Field Contributions to Rapid Corrective Saccades

2007 ◽  
Vol 97 (2) ◽  
pp. 1457-1469 ◽  
Author(s):  
Aditya Murthy ◽  
Supriya Ray ◽  
Stephanie M. Shorter ◽  
Elizabeth G. Priddy ◽  
Jeffrey D. Schall ◽  
...  
Keyword(s):  
Performance Monitoring ◽  
Target Location ◽  
Internal Representation ◽  
Neural Mechanism ◽  
Macaque Monkey ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Original Target ◽  
Corrective Saccades ◽  
Eye Field

Visually guided movements can be inaccurate, especially if unexpected events occur while the movement is programmed. Often errors of gaze are corrected before external feedback can be processed. Evidence is presented from macaque monkey frontal eye field (FEF), a cortical area that selects visual targets, allocates attention, and programs saccadic eye movements, for a neural mechanism that can correct saccade errors before visual afferent or performance monitoring signals can register the error. Macaques performed visual search for a color singleton that unpredictably changed position in a circular array as in classic double-step experiments. Consequently, some saccades were directed in error to the original target location. These were followed frequently by unrewarded, corrective saccades to the final target location. We previously showed that visually responsive neurons represent the new target location even if gaze shifted errantly to the original target location. Now we show that the latency of corrective saccades is predicted by the timing of movement-related activity in the FEF. Preceding rapid corrective saccades, the movement-related activity of all neurons began before explicit error signals arise in the medial frontal cortex. The movement-related activity of many neurons began before visual feedback of the error was registered and that of a few neurons began before the error saccade was completed. Thus movement-related activity leading to rapid corrective saccades can be guided by an internal representation of the environment updated with a forward model of the error.

scholarly journals Neural Control of Visual Search by Frontal Eye Field: Effects of Unexpected Target Displacement on Visual Selection and Saccade Preparation

2009 ◽  
Vol 101 (5) ◽  
pp. 2485-2506 ◽  
Author(s):  
Aditya Murthy ◽  
Supriya Ray ◽  
Stephanie M. Shorter ◽  
Jeffrey D. Schall ◽  
Kirk G. Thompson
Keyword(s):  
Visual Search ◽  
Reaction Time ◽  
Receptive Field ◽  
Target Location ◽  
Visual Selection ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Visual Neurons ◽  
Eye Field ◽  
Saccade Preparation

The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process—target-step reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys’ response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation.

scholarly journals Incomplete Suppression of Distractor-Related Activity in the Frontal Eye Field Results in Curved Saccades

2006 ◽  
Vol 96 (5) ◽  
pp. 2699-2711 ◽  
Author(s):  
Robert M. McPeek
Keyword(s):  
Target Location ◽  
Temporal Structure ◽  
Target Selection ◽  
Neural Correlates ◽  
Frontal Eye Field ◽  
Stimulation Site ◽  
Related Activity ◽  
Distractor Location ◽  
Significant Difference ◽  
Eye Field

Saccades in the presence of distractors show significant trajectory curvature. Based on previous work in the superior colliculus (SC), we speculated that curvature arises when a movement is initiated before competition between the target and distractor goals has been fully resolved. To test this hypothesis, we recorded frontal eye field (FEF) activity for curved and straight saccades in search. In contrast to the SC, activity in FEF is normally poorly correlated with saccade dynamics. However, the FEF, like the SC, is involved in target selection. Thus if curvature is caused by incomplete target selection, we expect to see its neural correlates in the FEF. We found that saccades that curve toward a distractor are accompanied by an increase in perisaccadic activity of FEF neurons coding the distractor location, and saccades that curve away are accompanied by a decrease in activity. In contrast, for FEF neurons coding the target location, there is no significant difference in activity between curved and straight saccades. To establish that the distractor-related activity is causally related to saccade curvature, we applied microstimulation to sites in the FEF before saccades to targets presented without distractors. The stimulation was subthreshold for evoking saccades and the temporal structure of the stimulation train resembled the activity recorded for curved saccades. The resulting movements curved toward the location coded by the stimulation site. These results support the idea that saccade curvature results from incomplete suppression of distractor-related activity during target selection.

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)

Macaque Frontal Eye Field Input to Saccade-Related Neurons in the Superior Colliculus

2003 ◽  
Vol 90 (2) ◽  
pp. 1046-1062 ◽  
Author(s):  
Janet O. Helminski ◽  
Mark A. Segraves
Keyword(s):  
Superior Colliculus ◽  
Rhesus Monkeys ◽  
Frontal Eye Field ◽  
Specific Class ◽  
Related Activity ◽  
Deep Layers ◽  
Eye Field ◽  
Visuomotor Tasks ◽  
Superior Colliculus Neurons ◽  
Made In

Extracellular recordings were made simultaneously in the frontal eye field and superior colliculus in awake, behaving rhesus monkeys. Frontal eye field microstimulation was used to orthodromically activate the superior colliculus both to locate the depth of the strongest frontal eye field input to the superior colliculus and to identify superior colliculus neurons receiving direct frontal eye field input. The activity of orthodromically driven colliculus neurons was characterized during visuomotor tasks. The purpose of this study was to identify the types of superior colliculus neurons that receive excitatory frontal eye field input. We found that microstimulation of the frontal eye field did not activate the superficial layers of the superior colliculus but did activate the deeper layers. This pattern of activation coincided with the prevalence of visual versus saccade-related activity in the superficial and deep layers. A total of 83 orthodromically driven superior colliculus neurons were identified. Of these neurons, 93% ( n = 77) exhibited a burst of activity associated with the onset of the saccade, and 25% ( n = 21) exhibited prelude/build-up activity prior to the onset of a saccade. In addition, it was common to see some activity synchronized with the onset of a visual target (30%, n = 25). In single neurons, these activity profiles could be observed alone or in combination. Superior colliculus neurons that were exclusively visual, however, were not excited by frontal eye field stimulation. We compared the activity of superior colliculus neurons that received frontal eye field input to descriptions of saccade-related neurons made in earlier reports and found that the distribution of neuron types in the orthodromically driven population was similar to the distribution within the overall population. This suggests that the frontal eye field does not selectively influence a specific class of collicular neurons, but, instead has a direct influence on all preparatory, and saccade-related activity within the deep layers of the superior colliculus.

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.

Delay-Period Activity in Visual, Visuomovement, and Movement Neurons in the Frontal Eye Field

2005 ◽  
Vol 94 (2) ◽  
pp. 1498-1508 ◽  
Author(s):  
Bonnie M. Lawrence ◽  
Robert L. White ◽  
Lawrence H. Snyder
Keyword(s):  
Spatial Information ◽  
Delay Period ◽  
Frontal Eye Field ◽  
Significant Delay ◽  
Related Activity ◽  
Null Direction ◽  
Preferred Direction ◽  
Canonical Neurons ◽  
Eye Field ◽  
Saccade Direction

In the present study, we examined the role of frontal eye field neurons in the maintenance of spatial information in a delayed-saccade paradigm. We found that visual, visuomovement, and movement neurons conveyed roughly equal amounts of spatial information during the delay period. Although there was significant delay-period activity in individual movement neurons, there was no significant delay-period activity in the averaged population of movement neurons. These contradictory results were reconciled by the finding that the population of movement neurons with memory activity consisted of two subclasses of neurons, the combination of which resulted in the cancellation of delay-period activity in the population of movement neurons. One subclass consisted of neurons with significantly greater delay activity in the preferred than in the null direction (“canonical”), whereas the other subclass consisted of neurons with significantly greater delay activity in the null direction than in the preferred direction (“paradoxical”). Preferred direction was defined by the saccade direction that evoked the greatest movement-related activity. Interestingly, the peak saccade-related activity of canonical neurons occurred before the onset of the saccade, whereas the peak saccade-related activity of paradoxical neurons occurred after the onset of the saccade. This suggests that the former, but not the latter, are directly involved in triggering saccades. We speculate that paradoxical neurons provide a mechanism by which spatial information can be maintained in a saccade-generating circuit without prematurely triggering a saccade.

Comparison of Memory- and Visually Guided Saccades Using Event-Related fMRI

2004 ◽  
Vol 91 (2) ◽  
pp. 873-889 ◽  
Author(s):  
M.R.G. Brown ◽  
J.F.X. DeSouza ◽  
H. C. Goltz ◽  
K. Ford ◽  
R. S. Menon ◽  
...  
Keyword(s):  
Inferior Frontal Gyrus ◽  
Stimulus Presentation ◽  
Delay Period ◽  
Frontal Eye Field ◽  
Peripheral Stimulus ◽  
Precentral Gyrus ◽  
Visually Guided ◽  
Related Activity ◽  
Eye Field ◽  
Sensory Processes

Previous functional imaging studies have shown an increased hemodynamic signal in several cortical areas when subjects perform memory-guided saccades than that when they perform visually guided saccades using blocked trial designs. It is unknown, however, whether this difference results from sensory processes associated with stimulus presentation, from processes occurring during the delay period before saccade generation, or from an increased motor signal for memory-guided saccades. We conducted fMRI using an event-related paradigm that separated stimulus-related, delay-related, and saccade-related activity. Subjects initially fixated a central cross, whose color indicated whether the trial was a memory- or a visually guided trial. A peripheral stimulus was then flashed at one of 4 possible locations. On memory-guided trials, subjects had to remember this location for the subsequent saccade, whereas the stimulus was a distractor on visually guided trials. Fixation cross disappearance after a delay period was the signal either to generate a memory-guided saccade or to look at a visual stimulus that was flashed on visually guided trials. We found slightly greater stimulus-related activation for visually guided trials in 3 right prefrontal regions and right rostral intraparietal sulcus (IPS). Memory-guided trials evoked greater delay-related activity in right posterior inferior frontal gyrus, right medial frontal eye field, bilateral supplementary eye field, right rostral IPS, and right ventral IPS but not in middle frontal gyrus. Right precentral gyrus and right rostral IPS exhibited greater saccade-related activation on memory-guided trials. We conclude that activation differences revealed by previous blocked experiments have different sources in different areas and that cortical saccade regions exhibit delay-related activation differences.

The effects of combined superior temporal polysensory area and frontal eye field lesions on eye movements in the macaque monkey

1997 ◽  
Vol 84 (1-2) ◽  
pp. 31-46 ◽  
Author(s):  
Séamas P. ÓScalaidhe ◽  
Hillary R. Rodman ◽  
Thomas D. Albright ◽  
Charles G. Gross
Keyword(s):  
Eye Movements ◽  
Macaque Monkey ◽  
Frontal Eye Field ◽  
Eye Field
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