scholarly journals Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search

1996 ◽  
Vol 76 (6) ◽  
pp. 4040-4055 ◽  
Author(s):  
K. G. Thompson ◽  
D. P. Hanes ◽  
N. P. Bichot ◽  
J. D. Schall
Keyword(s):  
Visual Search ◽  
Search Display ◽  
Saccade Latency ◽  
Frontal Eye Field ◽  
Visual Response ◽  
Response Latencies ◽  
Target Discrimination ◽  
Motor Processing ◽  
Eye Field ◽  
Saccade Programming

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.

Dynamic Dissociation of Visual Selection From Saccade Programming in Frontal Eye Field

2001 ◽  
Vol 86 (5) ◽  
pp. 2634-2637 ◽  
Author(s):  
Aditya Murthy ◽  
Kirk G. Thompson ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Selection Process ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Search Array ◽  
Visual Neurons ◽  
Current Location ◽  
Eye Field ◽  
Saccade Programming ◽  
Selection Of

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.

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
Keyword(s):  
Visual Search ◽  
Eye Movements ◽  
Visual Stimulus ◽  
Visual Discrimination ◽  
Time Course ◽  
Selection Process ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Eye Field ◽  
Saccade Programming

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.

Effects of unilateral frontal eye-field lesions on eye-head coordination in monkey

1986 ◽  
Vol 55 (4) ◽  
pp. 696-714 ◽  
Author(s):  
J. van der Steen ◽  
I. S. Russell ◽  
G. O. James
Keyword(s):  
Visual Search ◽  
Search Task ◽  
Visual Search Task ◽  
Peak Velocity ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Behavioral Task ◽  
Direct Gaze ◽  
Relative Neglect ◽  
Eye Field

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.

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 Neural Correlates of Correct and Errant Attentional Selection Revealed Through N2pc and Frontal Eye Field Activity

2010 ◽  
Vol 104 (5) ◽  
pp. 2433-2441 ◽  
Author(s):  
Richard P. Heitz ◽  
Jeremiah Y. Cohen ◽  
Geoffrey F. Woodman ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Visual Processing ◽  
Neural Correlates ◽  
Event Related Potential ◽  
Covert Attention ◽  
Extrastriate Cortex ◽  
False Alarms ◽  
Frontal Eye Field ◽  
Physiological Basis ◽  
Eye Field

The goal of this study was to obtain a better understanding of the physiological basis of errors of visual search. Previous research has shown that search errors occur when visual neurons in the frontal eye field (FEF) treat distractors as if they were targets. We replicated this finding during an inefficient form search and extended it by measuring simultaneously a macaque homologue of an event-related potential indexing the allocation of covert attention known as the m-N2pc. Based on recent work, we expected errors of selection in FEF to propagate to areas of extrastriate cortex responsible for allocating attention and implicated in the generation of the m-N2pc. Consistent with this prediction, we discovered that when FEF neurons selected a distractor instead of the search target, the m-N2pc shifted in the same, incorrect direction prior to the erroneous saccade. This suggests that such errors are due to a systematic misorienting of attention from the initial stages of visual processing. Our analyses also revealed distinct neural correlates of false alarms and guesses. These results demonstrate that errant gaze shifts during visual search arise from errant attentional processing.

scholarly journals Neural mechanisms of speed-accuracy tradeoff of visual search: Saccade vigor, targeting errors, superior colliculus and frontal eye field

2017 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Superior Colliculus ◽  
Time Course ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Response Preparation ◽  
Eye Field ◽  
Neurophysiological Mechanisms ◽  
Speed Accuracy ◽  
Accuracy Tradeoff

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.

scholarly journals Difficulty of Visual Search Modulates Neuronal Interactions and Response Variability in the Frontal Eye Field

2007 ◽  
Vol 98 (5) ◽  
pp. 2580-2587 ◽  
Author(s):  
Jeremiah Y. Cohen ◽  
Pierre Pouget ◽  
Geoffrey F. Woodman ◽  
Chenchal R. Subraveti ◽  
Jeffrey D. Schall ◽  
...  
Keyword(s):  
Multivariate Analysis ◽  
Visual Search ◽  
Search Task ◽  
Response Variability ◽  
Frontal Eye Field ◽  
Search Tasks ◽  
Saccade Onset ◽  
Neuronal Interactions ◽  
Eye Field ◽  
Spiking Activity

The frontal eye field (FEF) is involved in selecting visual targets for eye movements. To understand how populations of FEF neurons interact during target selection, we recorded activity from multiple neurons simultaneously while macaques performed two versions of a visual search task. We used a multivariate analysis in a point process statistical framework to estimate the instantaneous firing rate and compare interactions among neurons between tasks. We found that FEF neurons were engaged in more interactions during easier visual search tasks compared with harder search tasks. In particular, eye movement–related neurons were involved in more interactions than visual-related neurons. In addition, our analysis revealed a decrease in the variability of spiking activity in the FEF beginning ∼100 ms before saccade onset. The minimum in response variability occurred ∼20 ms earlier for the easier search task compared with the harder one. This difference is positively correlated with the difference in saccade reaction times for the two tasks. These findings show that a multivariate analysis can provide a measure of neuronal interactions and characterize the spiking activity of FEF neurons in the context of a population of neurons.

scholarly journals Effect of Inactivation of the Cortical Frontal Eye Field on Saccades Generated in a Choice Response Paradigm

2008 ◽  
Vol 100 (5) ◽  
pp. 2726-2737 ◽  
Author(s):  
Edward L. Keller ◽  
Kyoung-Min Lee ◽  
Se-Woong Park ◽  
Jessica A. Hill
Keyword(s):  
Alternative Interpretation ◽  
Saccade Latency ◽  
Frontal Eye Field ◽  
Choice Response ◽  
Visually Guided ◽  
Eye Field ◽  
Saccade Direction ◽  
Response Task ◽  
Bilateral Lesions

Previous studies using muscimol inactivations in the frontal eye fields (FEFs) have shown that saccades generated by recall from working memory are eliminated by these lesions, whereas visually guided saccades are relatively spared. In these experiments, we made reversible inactivations in FEFs in alert macaque monkeys and examined the effect on saccades in a choice response task. Our task required monkeys to learn arbitrary pairings between colored stimuli and saccade direction. Following inactivations, the percentage of choice errors increased as a function of the number of alternative (NA) pairings. In contrast, the percentage of dysmetric saccades (saccades that landed in the correct quadrant but were inaccurate) did not vary with NA. Saccade latency increased postlesion but did not increase with NA. We also made simultaneous inactivations in both FEFs. The results following bilateral lesions showed approximately twice as many choice errors. We conclude that the FEFs are involved in the generation of saccades in choice response tasks. The dramatic effect of NA on choice errors, but the lack of an effect of NA on motor errors or response latency, suggests that two types of processing are interrupted by FEF lesions. The first involves the formation of a saccadic intention vector from associate memory inputs, and the second, the execution of the saccade from the intention vector. An alternative interpretation of the first result is that a role of the FEFs may be to suppress incorrect responses. The doubling of choice errors following bilateral FEF lesions suggests that the effect of unilateral lesions is not caused by a general inhibition of the lesioned side by the intact side.

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