Dissociation of Visual Discrimination From Saccade Programming in Macaque Frontal Eye Field

1997 ◽  
Vol 77 (2) ◽  
pp. 1046-1050 ◽  
Author(s):  
Kirk G. Thompson ◽  
Narcisse P. Bichot ◽  
Jeffrey D. Schall

Thompson, Kirk G., Narcisse P. Bichot, and Jeffrey D. Schall. Dissociation of visual discrimination from saccade programming in macaque frontal eye field. J. Neurophysiol. 77: 1046–1050, 1997. To determine whether visual discrimination in macaque frontal eye field (FEF) is contingent on saccade planning, unit activity was recorded in two monkeys during blocked go and no-go visual search trials. The eye movements made by monkeys after correct no-go trials, in addition to an attenuation of the visual responses in no-go trials compared with go trials, indicated that covert saccade planning was effectively discouraged. During no-go search trials, the activity of the majority of neurons evolved to signal the location of the oddball stimulus. The degree and time course of the stimulus discrimination process observed in no-go trials was not different from that observed in go trials. We conclude that the discrimination of a salient visual stimulus reflected by FEF neurons is not contingent on saccade production but rather may reflect the outcome of an automatic visual selection process.

2001 ◽  
Vol 86 (5) ◽  
pp. 2634-2637 ◽  
Author(s):  
Aditya Murthy ◽  
Kirk G. Thompson ◽  
Jeffrey D. Schall

Previous studies of visually responsive neurons in the frontal eye fields have identified a selection process preceding saccades during visual search. The goal of this experiment was to determine whether the selection process corresponds to the selection of a conspicuous stimulus or to preparation of the next saccade. This was accomplished with the use of a novel task, called search-step, in which the target of a singleton visual search array switches location with a distracter on random trials. The target step trials created a condition in which the same stimulus yielded saccades either toward or away from the target. Visually responsive neurons in frontal eye field selected the current location of the conspicuous target even when gaze shifted to the location of a distractor. This dissociation demonstrates that the selection process manifest in visual neurons in the frontal eye field may be an explicit interpretation of the image and not an obligatory saccade command.


2017 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall

AbstractBalancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus, and description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys, but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. Visually-responsive neurons modulated baseline firing rate and the time course of salience evidence. Unlike FEF, the magnitude of visual responses in SC did not vary across SAT conditions, but the time to locate the target was longer in Accurate as compared to Fast trials. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Search errors occurred when visual salience neurons in FEF and SC treated distractors as targets, even in the Accurate condition. Saccade-related neural activity in SC but less FEF varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT.Significance statementNeurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This paper reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision-making.


2000 ◽  
Vol 83 (1) ◽  
pp. 625-629 ◽  
Author(s):  
Stefano Ferraina ◽  
Martin Paré ◽  
Robert H. Wurtz

Information about depth is necessary to generate saccades to visual stimuli located in three-dimensional space. To determine whether monkey frontal eye field (FEF) neurons play a role in the visuo-motor processes underlying this behavior, we studied their visual responses to stimuli at different disparities. Disparity sensitivity was tested from 3° of crossed disparity (near) to 3° degrees of uncrossed disparity (far). The responses of about two thirds of FEF visual and visuo-movement neurons were sensitive to disparity and showed a broad tuning in depth for near or far disparities. Early phasic and late tonic visual responses often displayed different disparity sensitivity. These findings provide evidence of depth-related signals in FEF and suggest a role for FEF in the control of disconjugate as well as conjugate eye movements.


1996 ◽  
Vol 76 (6) ◽  
pp. 4040-4055 ◽  
Author(s):  
K. G. Thompson ◽  
D. P. Hanes ◽  
N. P. Bichot ◽  
J. D. Schall

1. The latency between the appearance of a popout search display and the eye movement to the oddball target of the display varies from trial to trial in both humans and monkeys. The source of the delay and variability of reaction time is unknown but has been attributed to as yet poorly defined decision processes. 2. We recorded neural activity in the frontal eye field (FEF), an area regarded as playing a central role in producing purposeful eye movements, of monkeys (Macaca mulatta) performing a popout visual search task. Eighty-four neurons with visually evoked activity were analyzed. Twelve of these neurons had a phasic response associated with the presentation of the visual stimulus. The remaining neurons had more tonic responses that persisted through the saccade. Many of the neurons with more tonic responses resembled visuomovement cells in that they had activity that increased before a saccade into their response field. 3. The visual response latencies of FEF neurons were determined with the use of a Poisson spike train analysis. The mean visual latency was 67 ms (minimum = 35 ms, maximum = 138 ms). The visual response latencies to the target presented alone, to the target presented with distractors, or to the distractors did not differ significantly. 4. The initial visual activation of FEF neurons does not discriminate the target from the distractors of a popout visual search stimulus array, but the activity evolves to a state that discriminates whether the target of the search display is within the receptive field. We tested the hypothesis that the source of variability of saccade latency is the time taken by neurons involved in saccade programming to select the target for the gaze shift. 5. With the use of an analysis adapted from signal detection theory, we determined when the activity of single FEF neurons can reliably indicate whether the target or distractors are present within their response fields. The time of target discrimination partitions the reaction time into a perceptual stage in which target discrimination takes place, and a motor stage in which saccade programming and generation take place. The time of target discrimination occurred most often between 120 and 150 ms after stimulus presentation. 6. We analyzed the time course of target discrimination in the activity of single cells after separating trials into short, medium, and long saccade latency groups. Saccade latency was not correlated with the duration of the perceptual stage but was correlated with the duration of the motor stage. This result is inconsistent with the hypothesis that the time taken for target discrimination, as indexed by FEF neurons, accounts for the wide variability in the time of movement initiation. 7. We conclude that the variability observed in saccade latencies during a simple visual search task is largely due to postperceptual motor processing following target discrimination. Signatures of both perceptual and postperceptual processing are evident in FEF. Procrastination in the output stage may prevent stereotypical behavior that would be maladaptive in a changing environment.


2021 ◽  
pp. 153-190
Author(s):  
Richard E. Passingham

The caudal prefrontal (PF) cortex supports the visual search for objects such as foods both through eye movements and covert attention, and its connections explain how it can do this. The caudal PF cortex, which includes the frontal eye field, has connections with both the dorsal and ventral visual streams. The direction of eye movements depends on its connections with the superior colliculus and oculomotor nuclei. Covert attention depends on enhanced sensory responses that are mediated through top-down interactions with posterior sensory areas. Along with the granular parts of the orbital PF cortex, the caudal PF cortex evolved in early primates. Together, these two new areas led to improvements in searching for and evaluating objects that are hidden in a cluttered environment.


2018 ◽  
Vol 120 (1) ◽  
pp. 372-384 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall

Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. NEW & NOTEWORTHY Neurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This article reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision making.


2004 ◽  
Vol 91 (6) ◽  
pp. 2765-2769 ◽  
Author(s):  
Jeffrey D. Schall ◽  
Takashi R. Sato ◽  
Kirk G. Thompson ◽  
Amanda A. Vaughn ◽  
Chi-Hung Juan

Previous research has shown that visually responsive neurons in the frontal eye field of macaque monkeys select the target for a saccade during efficient, pop-out visual search through suppression of the representation of the nontarget distractors. For a fraction of these neurons, the magnitude of this distractor suppression varied with the proximity of the target to the receptive field, exhibiting more suppression of the distractor representation when the target was nearby than when the target was distant. The purpose of this study was to determine whether the variation of distractor suppression related to target proximity varied with target-distractor feature similarity. The effect of target proximity on distractor suppression did not vary with target-distractor similarity and therefore may be an endogenous property of the selection process.


1986 ◽  
Vol 55 (4) ◽  
pp. 696-714 ◽  
Author(s):  
J. van der Steen ◽  
I. S. Russell ◽  
G. O. James

We studied the effects of unilateral frontal eye-field (FEF) lesions on eye-head coordination in monkeys that were trained to perform a visual search task. Eye and head movements were recorded with the scleral search coil technique using phase angle detection in a homogeneous electromagnetic field. In the visual search task all three animals showed a neglect for stimuli presented in the field contralateral to the lesion. In two animals the neglect disappeared within 2-3 wk. One animal had a lasting deficit. We found that FEF lesions that are restricted to area 8 cause only temporary deficits in eye and head movements. Up to a week after the lesion the animals had a strong preference to direct gaze and head to the side ipsilateral to the lesion. Animals tracked objects in contralateral space with combined eye and head movements, but failed to do this with the eyes alone. It was found that within a few days after the lesion, eye and head movements in the direction of the target were initiated, but they were inadequate and had long latencies. Within 1 wk latencies had regained preoperative values. Parallel with the recovery on the behavioral task, head movements became more prominent than before the lesion. Four weeks after the lesion, peak velocity of the head movement had increased by a factor of two, whereas the duration showed a twofold decrease compared with head movements before the lesion. No effects were seen on the duration and peak velocity of gaze. After the recovery on the behavioral task had stabilized, a relative neglect in the hemifield contralateral to the lesion could still be demonstrated by simultaneously presenting two stimuli in the left and right visual hemifields. The neglect is not due to a sensory deficit, but to a disorder of programming. The recovery from unilateral neglect after a FEF lesion is the result of a different orienting behavior, in which head movements become more important. It is concluded that the FEF plays an important role in the organization and coordination of eye and head movements and that lesions of this area result in subtle but permanent changes in eye-head coordination.


2010 ◽  
Vol 10 (7) ◽  
pp. 518-518
Author(s):  
F. Ostendorf ◽  
J. Kilias ◽  
C. Ploner

Author(s):  
Agnes Wong

■ A small saccade of 0.5–3° that takes the eye away from fixation, followed by a saccade that returns the eye back to fixation after about 200 msec (i.e., presence of intersaccadic interval during which visual feedback occurs) ■ So named because of its appearance in eye movement tracings ■ Normal subjects often have square wave jerks (SWJ), but the rate is only 4–6 per minute. ■ Pathologic SWJ occurs at a rate of >15 per minute. ■ Cerebellar diseases Square wave jerks result from damage of projections from the frontal eye field, rostral pole of the superior colliculus, and the central mesencephalic reticular formation to the omnipause cells in the pons. If symptomatic, SWJ may be treated with methylphenidate, diazepam, phenobarbital, or amphetamines. ■ Burst of saccades with defective steps of innervation (i.e., stepless saccades) ■ Conjugate or monocular Saccadic pulses are associated with multiple sclerosis. Saccadic pulses result from damage of omnipause cells or the neural integrator.


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