scholarly journals Predictive Activity in Macaque Frontal Eye Field Neurons During Natural Scene Searching

2010 ◽  
Vol 103 (3) ◽  
pp. 1238-1252 ◽  
Author(s):  
Adam N. Phillips ◽  
Mark A. Segraves
Keyword(s):  
Visual Search ◽  
Target Selection ◽  
Cell Activity ◽  
Early Time ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Natural Scenes ◽  
Eye Field ◽  
Intermediate Time ◽  
And Performance

Generating sequences of multiple saccadic eye movements allows us to search our environment quickly and efficiently. Although the frontal eye field cortex (FEF) has been linked to target selection and making saccades, little is known about its role in the control and performance of the sequences of saccades made during self-guided visual search. We recorded from FEF cells while monkeys searched for a target embedded in natural scenes and examined the degree to which cells with visual and visuo-movement activity showed evidence of target selection for future saccades. We found that for about half of these cells, activity during the fixation period between saccades predicted the next saccade in a sequence at an early time that precluded selection based on current visual input to a cell's response field. In addition to predicting the next saccade, activity during the fixation prior to two successive saccades also predicted the direction and goal of the second saccade in the sequence. We refer to this as advanced predictive activity. Unlike activity indicating the upcoming saccade, advanced predictive activity occurred later in the fixation period, mirroring the order of the saccade sequence itself. The remaining cells without advanced predictive activity did not predict future saccades but reintroduced the signal for the upcoming saccade at an intermediate time in the fixation period. Together these findings suggest that during natural visual search the timing of FEF cell activity is consistent with a role in specifying targets for one or more future saccades in a search sequence.

scholarly journals Neural Basis of the Set-Size Effect in Frontal Eye Field: Timing of Attention During Visual Search

2009 ◽  
Vol 101 (4) ◽  
pp. 1699-1704 ◽  
Author(s):  
Jeremiah Y. Cohen ◽  
Richard P. Heitz ◽  
Geoffrey F. Woodman ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Response Time ◽  
Visual Target ◽  
Target Selection ◽  
Target Object ◽  
Frontal Eye Field ◽  
Neural Basis ◽  
Set Size ◽  
Eye Field ◽  
Recorded Activity

Visual search for a target object among distractors often takes longer when more distractors are present. To understand the neural basis of this capacity limitation, we recorded activity from visually responsive neurons in the frontal eye field (FEF) of macaque monkeys searching for a target among distractors defined by form (randomly oriented T or L). To test the hypothesis that the delay of response time with increasing number of distractors originates in the delay of attention allocation by FEF neurons, we manipulated the number of distractors presented with the search target. When monkeys were presented with more distractors, visual target selection was delayed and neuronal activity was reduced in proportion to longer response time. These findings indicate that the time taken by FEF neurons to select the target contributes to the variation in visual search efficiency.

scholarly journals Frontal Eye Field Activity Before Visual Search Errors Reveals the Integration of Bottom-Up and Top-Down Salience

2005 ◽  
Vol 93 (1) ◽  
pp. 337-351 ◽  
Author(s):  
Kirk G. Thompson ◽  
Narcisse P. Bichot ◽  
Takashi R. Sato
Keyword(s):  
Visual Search ◽  
Search Task ◽  
Target Selection ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Top Down ◽  
Bottom Up ◽  
Stimulus Response ◽  
Singleton Search ◽  
Eye Field

We investigated the saccade decision process by examining activity recorded in the frontal eye field (FEF) of monkeys performing 2 separate visual search experiments in which there were errors in saccade target choice. In the first experiment, the difficulty of a singleton search task was manipulated by varying the similarity between the target and distractors; errors were made more often when the distractors were similar to the target. On catch trials in which the target was absent the monkeys occasionally made false alarm errors by shifting gaze to one of the distractors. The second experiment was a popout color visual search task in which the target and distractor colors switched unpredictably across trials. Errors occurred most frequently on the first trial after the switch and less often on subsequent trials. In both experiments, FEF neurons selected the saccade goal on error trials, not the singleton target of the search array. Although saccades were made to the same stimulus locations, presaccadic activation and the magnitude of selection differed across trial conditions. The variation in presaccadic selective activity was accounted for by the variation in saccade probability across the stimulus–response conditions, but not by variations in saccade metrics. These results suggest that FEF serves as a saccade probability map derived from the combination of bottom-up and top-down influences. Peaks on this map represent the behavioral relevance of each item in the visual field rather than just reflecting saccade preparation. This map in FEF may correspond to the theoretical salience map of many models of attention and saccade target selection.

Parallel programming of saccades in the macaque frontal eye field: are sequential motor plans coactivated?

2020 ◽  
Vol 123 (1) ◽  
pp. 107-119 ◽  
Author(s):  
Debaleena Basu ◽  
Aditya Murthy
Keyword(s):  
Parallel Programming ◽  
Neural Control ◽  
Target Selection ◽  
Saccadic Eye Movements ◽  
Oculomotor System ◽  
Frontal Eye Field ◽  
Movement Activity ◽  
Concurrent Processing ◽  
Electrophysiological Recordings ◽  
Eye Field

We use sequences of saccadic eye movements to continually explore our visual environments. Previous behavioral studies have established that saccades in a sequence may be programmed in parallel by the oculomotor system. In this study, we tested the neural correlates of parallel programming of saccade sequences in the frontal eye field (FEF), using single-unit electrophysiological recordings from macaques performing a sequential saccade task. It is known that FEF visual neurons instantiate target selection whereas FEF movement neurons undertake saccade preparation, where the activity corresponding to a saccade vector gradually ramps up. The question of whether FEF movement neurons are involved in concurrent processing of saccade plans is as yet unresolved. In the present study, we show that, when a peripheral target is foveated after a sequence of two saccades, presaccadic activity of FEF movement neurons for the second saccade can be activated while the first is still underway. Moreover, the onset of movement activity varied parametrically with the behaviorally measured time available for parallel programming. Although at central fixation coactivated FEF movement activity may vectorially encode the retinotopic location of the second target with respect to the fixation point or the remapped location of the second target, with respect to the first our evidence suggests the possibility of early encoding of the remapped second saccade vector. Taken together, the results indicate that movement neurons, although located terminally in the FEF visual-motor spectrum, can accomplish concurrent processing of multiple saccade plans, leading to rapid execution of saccade sequences. NEW & NOTEWORTHY The execution of purposeful sequences underlies much of goal-directed behavior. How different brain areas accomplish sequencing is poorly understood. Using a modified double-step task to generate a rapid sequence of two saccades, we demonstrate that downstream movement neurons in the frontal eye field (FEF), a prefrontal oculomotor area, allow for coactivation of the first and second movement plans that constitute the sequence. These results provide fundamental insights into the neural control of action sequencing.

Neural basis of saccade target selection in frontal eye field during visual search

Nature ◽  
1993 ◽  
Vol 366 (6454) ◽  
pp. 467-469 ◽  
Author(s):  
Jeffrey D. Schall ◽  
Doug P. Hanes
Keyword(s):  
Visual Search ◽  
Target Selection ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Neural Basis ◽  
Eye Field

scholarly journals Concurrent neural representations of the current and forthcoming movement plans in the frontal eye field during a saccade sequence

2018 ◽  
Author(s):  
Debaleena Basu ◽  
Aditya Murthy
Keyword(s):  
Parallel Programming ◽  
Target Selection ◽  
Saccadic Eye Movements ◽  
Oculomotor System ◽  
Frontal Eye Field ◽  
Movement Activity ◽  
Concurrent Processing ◽  
Electrophysiological Recordings ◽  
Measured Time ◽  
Eye Field

AbstractWe use sequences of saccadic eye movements to continually explore our visual environments. Previous studies have established that saccades in a sequence may be programmed in parallel by the oculomotor system. In this study, we tested the neural correlates of parallel programming of saccade sequences in the frontal eye field (FEF), using single-unit electrophysiological recordings from macaques performing a double-step saccade task. Neurons in the FEF range from visual neurons instantiating target selection, to movement neurons which prepare a saccadic response towards the selected target. The question of whether the FEF movement neurons undertake concurrent processing of multiple goals or saccade plans is yet unresolved. We show that when a peripheral target is foveated by a sequence of two saccades, FEF movement activity for the second saccade can be initiated whilst the first is still underway. Moreover, the onset of the movement activity varied parametrically with the behaviorally measured time available for parallel programming. Finally, the concurrent activity was specific for the final remapped motor vector connecting the first and the second targets and not the goal of the second saccade. In contrast, the upstream FEF visual-related neurons showed concurrent activity related to the goal of the second saccade, but not the remapped vector connecting the first and the second targets. Taken together, the results indicate that movement neurons, although located terminally in the FEF visual-motor spectrum, can accomplish concurrent processing of multiple saccade plans, leading to rapid execution of saccade sequences.

Electrical Stimulation of the Frontal Eye Fields in the Head-Free Macaque Evokes Kinematically Normal 3D Gaze Shifts

2010 ◽  
Vol 104 (6) ◽  
pp. 3462-3475 ◽  
Author(s):  
Jachin A. Monteon ◽  
Alina G. Constantin ◽  
Hongying Wang ◽  
Julio Martinez-Trujillo ◽  
J. Douglas Crawford
Keyword(s):  
Target Selection ◽  
Three Dimensional ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Velocity Amplitude ◽  
Eye Field ◽  
Head Rotations ◽  
Stimulation Of

The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30–100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity–amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listing's law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listing's plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye–head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye–head coordination are likely specified by downstream mechanisms.

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

2018 ◽  
Vol 120 (1) ◽  
pp. 372-384 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Superior Colliculus ◽  
Target Selection ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Response Preparation ◽  
Eye Field ◽  
Neurophysiological Mechanisms ◽  
Speed Accuracy ◽  
Accuracy Tradeoff

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.

scholarly journals Sequential Operations Revealed by Serendipitous Feature Selectivity in Frontal Eye Field

2019 ◽  
Author(s):  
Kaleb A. Lowe ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Search Task ◽  
Visual Search Task ◽  
Target Selection ◽  
Stimulus Orientation ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Eye Field ◽  
Feature Selectivity ◽  
Selection Indexes

ABSTRACTNeurons in macaque frontal eye field contribute to spatial but typically not feature selection during visual search. Using an innovative visual search task, we report a serendipitous discovery that some frontal eye field neurons can develop rapid selectivity for stimulus orientation that is used to guide gaze during a visual search task with pro-saccade and anti-saccade responses. This feature selectivity occurs simultaneously at multiple locations for all objects sharing that feature and coincides with when neurons select the singleton of a search array. This feature selectivity also reveals the distinct, subsequent operation of selecting the endpoint of the saccade in pro-saccade as well as anti-saccade trials. These results demonstrate that target selection preceding saccade preparation is composed of multiple operations. We conjecture that singleton selection indexes the allocation of attention, which can be divided, to conspicuous items. Consequently, endpoint selection indexes the focused allocation of attention to the endpoint of the saccade. These results demonstrate that saccade target selection is not a unitary process.SIGNIFICANCE STATEMENTFrontal eye field is well known to contribute to spatial selection for attention and eye movements. We discovered that some frontal eye field neurons can acquire selectivity for stimulus orientation when it guides visual search. The chronometry of neurons with and without feature selectivity reveal distinct operations accomplishing visual search.

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.

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)

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