Faculty Opinions recommendation of Feature-based attention in the frontal eye field and area V4 during visual search.

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.

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Differential Temporal Storage Capacity in the Baseline Activity of Neurons in Macaque Frontal Eye Field and Area V4

Journal of Neurophysiology ◽

10.1152/jn.01066.2009 ◽

2010 ◽

Vol 103 (5) ◽

pp. 2433-2445 ◽

Cited By ~ 29

Author(s):

Tadashi Ogawa ◽

Hidehiko Komatsu

Keyword(s):

Neuronal Activity ◽

Storage Capacity ◽

Discharge Rate ◽

Time Lag ◽

Temporal Correlation ◽

Frontal Eye Field ◽

Area V4 ◽

Baseline Activity ◽

Eye Field ◽

V4 Neurons

Previous studies have suggested that spontaneous fluctuations in neuronal activity reflect intrinsic functional brain architecture. Inspired by these findings, we analyzed baseline neuronal activity in the monkey frontal eye field (FEF; a visuomotor area) and area V4 (a visual area) during the fixation period of a cognitive behavioral task in the absence of any task-specific stimuli or behaviors. Specifically, we examined the temporal storage capacity of the instantaneous discharge rate in FEF and V4 neurons by calculating the correlation of the spike count in a bin with that in another bin during the baseline activity of a trial. We found that most FEF neurons fired significantly more (or less) in one bin if they fired more (or less) in another bin within a trial, even when these two time bins were separated by hundreds of milliseconds. By contrast, similar long time-lag correlations were observed in only a small fraction of V4 neurons, indicating that temporal correlations were considerably stronger in FEF compared with those in V4 neurons. Additional analyses revealed that the findings were not attributable to other task-related variables or ongoing behavioral performance, suggesting that the differences in temporal correlation strength reflect differences in intrinsic structural and functional architecture between visual and visuomotor areas. Thus FEF neurons probably play a greater role than V4 neurons in neural circuits responsible for temporal storage in activity.

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

Journal of Neurophysiology ◽

10.1152/jn.2001.86.5.2634 ◽

2001 ◽

Vol 86 (5) ◽

pp. 2634-2637 ◽

Cited By ~ 89

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.

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

Journal of Neurophysiology ◽

10.1152/jn.90824.2008 ◽

2009 ◽

Vol 101 (5) ◽

pp. 2485-2506 ◽

Cited By ~ 40

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.

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

Journal of Neurophysiology ◽

10.1152/jn.00604.2010 ◽

2010 ◽

Vol 104 (5) ◽

pp. 2433-2441 ◽

Cited By ~ 29

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.

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The effects of bilateral frontal eye-field, posterior parietal or superior collicular lesions on visual search in the rhesus monkey

Brain Research ◽

10.1016/0006-8993(78)90216-0 ◽

1978 ◽

Vol 146 (1) ◽

pp. 35-50 ◽

Cited By ~ 70

Author(s):

Richard Latto

Keyword(s):

Visual Search ◽

Rhesus Monkey ◽

Frontal Eye Field ◽

Eye Field ◽

Posterior Parietal

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Effects of frontal eye field microstimulation on the discriminability of visual responses in area V4

Journal of Vision ◽

10.1167/6.6.748 ◽

2010 ◽

Vol 6 (6) ◽

pp. 748-748

Author(s):

K. M. Armstrong ◽

T. Moore

Keyword(s):

Frontal Eye Field ◽

Visual Responses ◽

Area V4 ◽

Eye Field

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

10.1101/212621 ◽

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.

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