scholarly journals Functional Distinction Between Visuomovement and Movement Neurons in Macaque Frontal Eye Field During Saccade Countermanding

2009 ◽  
Vol 102 (6) ◽  
pp. 3091-3100 ◽  
Author(s):  
Supriya Ray ◽  
Pierre Pouget ◽  
Jeffrey D. Schall

In the previous studies on the neural control of saccade initiation using the countermanding paradigm, movement and visuomovement neurons in the frontal eye field were grouped as movement-related neurons. The activity of both types of neurons was modulated when a saccade was inhibited in response to a stop signal, and this modulation occurred early enough to contribute to the control of the saccade initiation. We now report a functional difference between these two classes of neurons when saccades are produced. Movement neurons exhibited a progressive accumulation of discharge rate following target presentation that triggered a saccade when it reached a threshold. When saccades were inhibited with lower probability in response to a stop signal appearing at longer delays, this accumulating activity was interrupted at levels progressively closer to the threshold. In contrast, visuomovement neurons exhibited a maintained elevated discharge rate following target presentation that was followed by a further enhancement immediately before the saccade initiation. When saccades were inhibited in response to a stop signal, the late enhancement was absent and the maintained activity decayed regardless of stop-signal delay. These results demonstrate that the activity of movement neurons realizes the progressive commitment to the saccade initiation modeled by the activation of the go unit in computational models of countermanding performance. The lack of correspondence of the activity of visuomovement neurons with any elements of these models indicates that visuomovement neurons perform a function other than the saccade preparation such as a corollary discharge to update visual processing.

2010 ◽  
Vol 103 (2) ◽  
pp. 801-816 ◽  
Author(s):  
Veit Stuphorn ◽  
Joshua W. Brown ◽  
Jeffrey D. Schall

The goal of this study was to determine whether the activity of neurons in the supplementary eye field (SEF) is sufficient to control saccade initiation in macaque monkeys performing a saccade countermanding (stop signal) task. As previously observed, many neurons in the SEF increase the discharge rate before saccade initiation. However, when saccades are canceled in response to a stop signal, effectively no neurons with presaccadic activity display discharge rate modulation early enough to contribute to saccade cancellation. Moreover, SEF neurons do not exhibit a specific threshold discharge rate that could trigger saccade initiation. Yet, we observed more subtle relations between SEF activation and saccade production. The activity of numerous SEF neurons was correlated with response time and varied with sequential adjustments in response latency. Trials in which monkeys canceled or produced a saccade in a stop signal trial were distinguished by a modest difference in discharge rate of these SEF neurons before stop signal or target presentation. These findings indicate that neurons in the SEF, in contrast to counterparts in the frontal eye field and superior colliculus, do not contribute directly and immediately to the initiation of visually guided saccades. However the SEF may proactively regulate saccade production by biasing the balance between gaze-holding and gaze-shifting based on prior performance and anticipated task requirements.


2010 ◽  
Vol 103 (5) ◽  
pp. 2433-2445 ◽  
Author(s):  
Tadashi Ogawa ◽  
Hidehiko Komatsu

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.


2010 ◽  
Vol 104 (5) ◽  
pp. 2433-2441 ◽  
Author(s):  
Richard P. Heitz ◽  
Jeremiah Y. Cohen ◽  
Geoffrey F. Woodman ◽  
Jeffrey D. Schall

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.


Author(s):  
Takashi Sato ◽  
Kirk Thompson ◽  
Jeffrey Schall ◽  
Aditya Murthy ◽  
Narcisse Bichot

2004 ◽  
Vol 16 (6) ◽  
pp. 1060-1067 ◽  
Author(s):  
Jacinta O'Shea ◽  
Neil G. Muggleton ◽  
Alan Cowey ◽  
Vincent Walsh

Frontal eye field (FEF) neurons discharge in response to behaviorally relevant stimuli that are potential targets for saccades. Distinct visual and motor processes have been dissociated in the FEF of macaque monkeys, but little is known about the visual processing capacity of FEF in humans. We used double-pulse transcranial magnetic stimulation [(d)TMS] to investigate the timing of target discrimination during visual conjunction search. We applied dual TMS pulses separated by 40 msec over the right FEF and vertex. These were applied in five timing conditions to sample separate time windows within the first 200 msec of visual processing. (d)TMS impaired search performance, reflected in reduced d′ scores. This effect was limited to a time window between 40 and 80 msec after search array onset. These parameters correspond with single-cell activity in FEF that predicts monkeys' behavioral reports on hit, miss, false alarm, and correct rejection trials. Our findings demonstrate a crucial early role for human FEF in visual target discrimination that is independent of saccade programming.


2013 ◽  
Vol 109 (11) ◽  
pp. 2767-2780 ◽  
Author(s):  
Jay J. Jantz ◽  
Masayuki Watanabe ◽  
Stefan Everling ◽  
Douglas P. Munoz

In an influential model of frontal eye field (FEF) and superior colliculus (SC) activity, saccade initiation occurs when the discharge rate of either single neurons or a population of neurons encoding a saccade motor plan reaches a threshold level of activity. Conflicting evidence exists for whether this threshold is fixed or can change under different conditions. We tested the fixed-threshold hypothesis at the single-neuron and population levels to help resolve the inconsistency between previous studies. Two rhesus monkeys performed a randomly interleaved pro- and antisaccade task in which they had to look either toward (pro) or 180° away (anti) from a peripheral visual stimulus. We isolated visuomotor (VM) and motor (M) neurons in the FEF and SC and tested three specific predictions of a fixed-threshold hypothesis. We found little support for fixed thresholds. First, correlations were never totally absent between presaccadic discharge rate and saccadic reaction time when examining a larger (plausible) temporal period. Second, presaccadic discharge rates varied markedly between saccade tasks. Third, visual responses exceeded presaccadic motor discharges for FEF and SC VM neurons. We calculated that only a remarkably strong bias for M neurons in downstream projections could render the fixed-threshold hypothesis plausible at the population level. Also, comparisons of gap vs. overlap conditions indicate that increased inhibitory tone may be associated with stability of thresholds. We propose that fixed thresholds are the exception rather than the rule in FEF and SC, and that stabilization of an otherwise variable threshold depends on task-related, inhibitory modulation.


1994 ◽  
Vol 72 (5) ◽  
pp. 2532-2537 ◽  
Author(s):  
E. C. Dias ◽  
C. J. Bruce

1. We recorded from the frontal eye field (FEF) of rhesus monkeys while they performed the gap task in which the fixation point disappears 200 ms before the appearance of the peripheral saccadic target. This gap allows the disengagement of fixation to begin before the acquisition of saccade coordinates, thereby greatly reducing saccade latency (“gap effect”). Very short-latency saccades obtained in this gap task have been called “express saccades”. 2. We studied 145 FEF neurons that had presaccadic activity on conventional saccade tasks. When tested in the gap task with a 200-ms gap, nearly half of these neurons (69) increased their discharge rate in response to the disappearance of the fixation target. We call this increase a fixation-disengagement discharge (FDD). The mean latency of the start of the FDD relative to the fixation light extinction was 149 +/- 36 (SD) ms. 3. Gap-task trials with the saccade target in the cell's response field were randomly intermixed with trials having the target opposite to the cell's field. The FDD was present in both cases: on trials into the response field, the FDD was followed by the cell's presaccadic burst. On trials opposite the cell's field, the FDD activity was suppressed prior to the saccade. 4. The FDD was most likely to be found in cells that had the movement type of presaccadic activity, i.e., movement cells and visuomovement cells. FDD was observed in 57% of visuomovement cells A, B, and C, 50% with movement activity, and 18% purely visual.(ABSTRACT TRUNCATED AT 250 WORDS)


1997 ◽  
Vol 78 (3) ◽  
pp. 1373-1383 ◽  
Author(s):  
Marc M. Umeno ◽  
Michael E. Goldberg

Umeno, M. M. and Goldberg, M. E. Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J. Neurophysiol. 78: 1373–1383, 1997. Neurons in the lateral intraparietal area and intermediate layers of the superior colliculus show predictive visual responses. They respond before an impending saccade to a stimulus that will be brought into their receptive field by that saccade. In these experiments we sought to establish whether the monkey frontal eye field had a similar predictive response. We recorded from 100 presaccadic frontal eye field neurons (32 visual cells, 48 visuomovement cells, and 20 movement cells) with the use of the classification criteria of Bruce and Goldberg. We studied each cell in a continuous stimulus task, where the monkey made a saccade that brought a recently appearing stimulus into its receptive field. The latency of response in the continuous stimulus task varied from 52 ms before the saccade to 272 ms after the saccade. We classified cells as having predictive visual responses if their latency in the continuous stimulus task was less than the latency of their visual on response to a stimulus in their receptive or movement field as described in a visual fixation task. Thirty-four percent (11 of 32) of the visual cells, 31% (15 of 48) of the visuomovement cells, and no (0 of 20) movement cells showed a predictive visual response. The cells with predictive responses never responded to the stimulus when the monkey did not make the saccade that would bring that stimulus into the receptive field, and never discharged in association with that saccade unless it brought a stimulus into the receptive field. The response in the continuous stimulus task was almost always weaker than the visual on response to a stimulus flashed in the receptive field. Because cells with visual responses but not cells with movement activity alone showed the effect, we conclude that the predictive visual response is a property of the visual processing in the frontal eye field, i.e., a response to the stimulus in the future receptive field. It is not dependent on the actual planning or execution of a saccade to that stimulus. We suggest that the predictive visual mechanism is one in which the brain dynamically calculates the spatial location of objects in terms of desired displacement. This enables the oculomotor system to perform in a spatially accurate manner when there is a dissonance between the retinal location of a target and the saccade necessary to acquire that target. This mechanism does not require an explicit calculation of target position in some supraretinal coordinatesystem.


2009 ◽  
Vol 102 (6) ◽  
pp. 3656-3672 ◽  
Author(s):  
Ilya E. Monosov ◽  
Kirk G. Thompson

We investigated the link between neuronal activity in the frontal eye field (FEF) and the enhancement of visual processing associated with covert spatial attention in the absence of eye movements. We correlated activity recorded in the FEF of monkeys manually reporting the identity of a visual search target to performance accuracy and reaction time. Monkeys were cued to the most probable target location with a cue array containing a popout color singleton. Neurons exhibited spatially selective responses for the popout cue stimulus and for the target of the search array. The magnitude of activity related to the location of the cue prior to the presentation of the search array was correlated with trends in behavioral performance across valid, invalid, and neutral cue trial conditions. However, the speed and accuracy of the behavioral report on individual trials were predicted by the magnitude of spatial selectivity related to the target to be identified, not for the spatial cue. A minimum level of selectivity was necessary for target detection and a higher level for target identification. Muscimol inactivation of FEF produced spatially selective perceptual deficits in the covert search task that were correlated with the effectiveness of the inactivation and were strongest on invalid cue trials that require an endogenous attention shift. These results demonstrate a strong functional link between FEF activity and covert spatial attention and suggest that spatial signals from FEF directly influence visual processing during the time that a stimulus to be identified is being processed by the visual system.


2012 ◽  
Vol 108 (10) ◽  
pp. 2737-2750 ◽  
Author(s):  
Braden A. Purcell ◽  
Richard P. Heitz ◽  
Jeremiah Y. Cohen ◽  
Jeffrey D. Schall

Discharge rate modulation of frontal eye field (FEF) neurons has been identified with a representation of visual search salience (physical conspicuity and behavioral relevance) and saccade preparation. We tested whether salience or saccade preparation are evident in the trial-to-trial variability of discharge rate. We quantified response variability via the Fano factor in FEF neurons recorded in monkeys performing efficient and inefficient visual search tasks. Response variability declined following stimulus presentation in most neurons, but despite clear discharge rate modulation, variability did not change with target salience. Instead, we found that response variability was modulated by stimulus luminance and the number of items in the visual field independently of attentional demands. Response variability declined to a minimum before saccade initiation, and presaccadic response variability was directionally tuned. In addition, response variability was correlated with the response time of memory-guided saccades. These results indicate that the trial-by-trial response variability of FEF neurons reflects saccade preparation and the strength of sensory input, but not visual search salience or attentional allocation.


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