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Express saccades are rapid saccadic eye movements that can accurately redirect gaze to behaviorally relevant stimuli in the visual environment. This behavior can be commonly observed when the fixation spot disappears at a consistent, short interval before a target spot appears at a repeated location. While seemingly automatic, whether cognitive control can govern express saccade production has not been investigated. Here we report the production and manipulation of express saccades under unfavorable conditions in a saccade countermanding task necessitating cognitive control. To perform this task, we trained two monkeys to fixate a central spot and, following a variable amount of time, saccade to a target stimulus at one of two fixed locations (no-stop trials) presented simultaneously with the disappearance of the fixation dot. On a minority of trials, the fixation point reappeared instructing the monkeys to cancel their planned saccade to the peripheral target (stop-signal trials). Monkeys earned fluid reward for generating saccades to targets on no-stop trials and for maintaining fixation on stop-signal trials. Monkeys and humans adapt to the stop-signal trials by increasing saccade latencies. However, in two macaque monkeys we observed a significant fraction of trials with saccade latencies < 100 ms, resulting in a bimodal distribution of saccadic latencies. Target timing derived from regularities of the fixation interval (foreperiod) was used by some monkeys in some sessions to adapt regular but not express saccade latencies. Furthermore, simulations revealed by varying express saccade production, monkeys could maximize the opportunity for reward. To determine whether monkeys exploited this opportunity, reward contingencies for express saccade were changed. When unrewarded, significantly fewer express saccades were produced. This was confirmed in two other monkeys. This study highlights an unexpected manifestation of cognitive control through release of very short latency responses.

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.

We investigated the chronometry of neural processes in frontal eye fields of macaques performing double-step saccade visual search in which a conspicuous target changes location in the array on a random fraction of trials. Durations of computational processes producing a saccade to original and final target locations (GO1 and GO2, respectively) are derived from response times (RT) on different types of trials. In these data, GO2 tended to be faster than GO1, demonstrating that inhibition of the initial saccade did not delay production of the compensated saccade. Here, we measured the dynamics of visual, visuomovement, and movement neuron activity in relation to these processes by examining trials when neurons instantiated either process. First, we verified that saccades were initiated when the discharge rate of movement neurons reached a threshold that was invariant across RT and trial type. Second, the time when visual and visuomovement neurons selected the target and when movement neuron activity began to accumulate were not significantly different across trial type. Third, the interval from the beginning of accumulation to threshold of movement-related activity was significantly shorter when instantiating the GO2 relative to the GO1 process. Differences observed between monkeys are discussed. Fourth, random variation of RT was accounted for to some extent by random variation in both the onset and duration of selective activity of each neuron type but mostly by variation of movement neuron accumulation duration. These findings offer new insights into the sources of control of target selection and saccade production in dynamic environments.

Neocortex is striking in its laminar architecture. Tracer studies have uncovered anatomical connectivity among laminae, but the functional connectivity between laminar compartments is still largely unknown. Such functional connectivity can be discerned through spontaneous neural correlations during rest. Previous work demonstrated a robust pattern of mesoscopic resting-state connectivity in macaque primary visual cortex (V1) through interlaminar cross-frequency coupling. Here we investigated whether this pattern generalizes to other cortical areas by comparing resting-state laminar connectivity between V1 and the supplementary eye field (SEF), a frontal area lacking a granular layer 4 (L4). Local field potentials (LFPs) were recorded with linear microelectrode arrays from all laminae of granular V1 and agranular SEF while monkeys rested in darkness. We found substantial differences in the relationship between the amplitude of gamma-band (>30 Hz) LFP and the phase of alpha-band (7–14 Hz) LFP between these areas. In V1, gamma amplitudes in L2/3 and L5 were coupled with alpha-band LFP phase in L5, as previously described. In contrast, in SEF phase-amplitude coupling was prominent within L3 and much weaker across layers. These results suggest that laminar interactions in agranular SEF are unlike those in granular V1. Thus the intrinsic functional connectivity of the cortical microcircuit does not seem to generalize across cortical areas.

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.

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.

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.

Numerous studies have described different functional cell types in the frontal eye field (FEF), but the reliability of the distinction between these types has been uncertain. Studies in other brain areas have described specific differences in the width of action potentials recorded from different cell types. To substantiate the functionally defined cell types encountered in FEF, we measured the width of spikes of visual, movement, and visuomovement types of FEF neurons in macaque monkeys. We show that visuomovement neurons had the thinnest spikes, consistent with a role in local processing. Movement neurons had the widest spikes, consistent with their role in sending eye movement commands to subcortical structures such as the superior colliculus. Visual neurons had wider spikes than visuomovement neurons, consistent with their role in receiving projections from occipital and parietal cortex. These results show how structure and function of FEF can be linked to guide inferences about neuronal architecture.

We describe intracranial local field potentials (LFP) recorded in the anterior cingulate cortex (ACC) of macaque monkeys performing a saccade countermanding task. The most prominent feature at ∼70% of sites was greater negative polarity after errors than after rewarded correct trials. This negative polarity was also evoked in unrewarded correct trials. The LFP evoked by the visual target was much less polarized, and the weak presaccadic modulation was insufficient to control the initiation of saccades. When saccades were cancelled, LFP modulation decreased slightly with the magnitude of response conflict that corresponds to the coactivation of gaze-shifting and -holding neurons estimated from the probability of canceling. However, response time adjustments on subsequent trials were not correlated with LFP polarity on individual trials. The results provide clear evidence that error- and feedback-related, but not conflict-related, signals are carried by the LFP in the macaque ACC. Finding performance monitoring field potentials in the ACC of macaque monkeys establishes a bridge between event-related potential and functional brain-imaging studies in humans and neurophysiology studies in non-human primates.

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 approximately 100 ms before saccade onset. The minimum in response variability occurred approximately 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.

It has been proposed that low-threshold Ca2+ (LT)-associated bursts in the lateral geniculate nucleus (LGN) of awake animals communicate significant or unexpected visual events to cortex. The present study investigated this hypothesis by examining the incidence of LT bursts in 146 cells recorded from the LGN of three macaque monkeys. Bursts were defined as clusters of two or more action potentials separated by not more than 4 ms and preceded by a ≥100-ms quiescent interval. The incidence of bursts was examined in several intensive-training Go-NoGo and target selection tasks as well as in training-free tasks where natural scenes with both familiar and novel contents were shown. Our chief findings were as follows. 1) Bursts occur in the majority of cells under every condition tested, 2) burst incidence is very low (

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.

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.

Event-related potentials (ERPs) have provided crucial data concerning the time course of psychological processes, but the neural mechanisms producing ERP components remain poorly understood. This study continues a program of research in which we investigated the neural basis of attention-related ERP components by simultaneously recording intracranially and extracranially from macaque monkeys. Here, we compare the timing of attentional selection by the macaque homologue of the human N2pc component (m-N2pc) with the timing of selection in the frontal eye field (FEF), an attentional-control structure believed to influence posterior visual areas thought to generate the N2pc. We recorded FEF single-unit spiking and local field potentials (LFPs) simultaneously with the m-N2pc in monkeys performing an efficient pop-out search task. We assessed how the timing of attentional selection depends on task demands by direct comparison with a previous study of inefficient search in the same monkeys (e.g., finding a T among Ls). Target selection by FEF spikes, LFPs, and the m-N2pc was earlier during efficient pop-out search rather than during inefficient search. The timing and magnitude of selection in all three signals varied with set size during inefficient but not efficient search. During pop-out search, attentional selection was evident in FEF spiking and LFP before the m-N2pc, following the same sequence observed during inefficient search. These observations are consistent with the hypothesis that feedback from FEF modulates neural activity in posterior regions that appear to generate the m-N2pc even when competition for attention among items in a visual scene is minimal.

Despite nearly a century of electrophysiological studies recording extracranially from humans and intracranially from monkeys, the neural generators of nearly all human event-related potentials (ERPs) have not been definitively localized. We recorded an attention-related ERP component, known as the N2pc, simultaneously with intracranial spikes and local field potentials (LFPs) in macaques to test the hypothesis that an attentional-control structure, the frontal eye field (FEF), contributed to the generation of the macaque homologue of the N2pc (m-N2pc). While macaques performed a difficult visual search task, the search target was selected earliest by spikes from single FEF neurons, later by FEF LFPs, and latest by the m-N2pc. This neurochronometric comparison provides an empirical bridge connecting macaque and human experiments and a step toward localizing the neural generator of this important attention-related ERP component.

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.

1. The purpose of this study was to describe the response properties of neurons in the supplementary motor area (SMA), including the supplementary eye fields (SEF) of three rhesus monkeys (Macaca mulatta) performing visually guided eye and forelimb movements. Seven hundred thirty single units were recorded in the dorsomedial agranular cortex while monkeys performed a go/no-go visual tracking task. The unit activity associated with rewarded, task-related movements was compared with that associated with unrewarded, spontaneous movements executed in the intertrial interval or when the task was not running. A number of neuronal response types were identified. 2. Sensory cells were characterized by their response to the visual and/or auditory target stimuli combined with no discharge associated with eye or forelimb movements. New information was provided about the receptive fields of the visual cells; they varied in size and, although many included the ipsilateral hemifield, they tended to emphasize the contralateral. A significant proportion of the visually responsive cells had receptive fields restricted to within 8 degrees of the fovea. The response latency was relatively long (greater than 90 ms) and variable. 3. Preparatory set cells were activated from the appearance of the target until the presentation of the go/no-go cue. This subpopulation ceased firing 50-100 ms before the movement was initiated. These cells tended to respond best in relation to contralateral movements. The response latency was similar to that of the sensory cells, although some of these units began to discharge in anticipation of predictable target presentations. These neurons were not active before unrewarded, spontaneous saccades. 4. Sensory-movement cells comprised the largest population of neurons identified in SMA. They were active from the appearance of the target until after the execution of the saccade. These neurons tended to respond preferentially in association with contraversive saccades. The latency of response to the target was significantly longer than that of the sensory cells. There was a large amount of variability in the time to reach the peak level of activation, and this population of units generally became inactivated shortly after the saccade was initiated. Although there were counterexamples, most sensory-movement cells responded equally in association with visually and auditory guided movements. In addition, these neurons were not active in relation to self-generated eye movements made during the intertrial intervals. 5. Pause-rebound cells were identified by their suppression at the appearance of the target and subsequent discharge associated with the saccade. These units tended to respond preferentially to contralateral targets.(ABSTRACT TRUNCATED AT 400 WORDS)

Visually guided movements can be inaccurate, especially if unexpected events occur while the movement is programmed. Often errors of gaze are corrected before external feedback can be processed. Evidence is presented from macaque monkey frontal eye field (FEF), a cortical area that selects visual targets, allocates attention, and programs saccadic eye movements, for a neural mechanism that can correct saccade errors before visual afferent or performance monitoring signals can register the error. Macaques performed visual search for a color singleton that unpredictably changed position in a circular array as in classic double-step experiments. Consequently, some saccades were directed in error to the original target location. These were followed frequently by unrewarded, corrective saccades to the final target location. We previously showed that visually responsive neurons represent the new target location even if gaze shifted errantly to the original target location. Now we show that the latency of corrective saccades is predicted by the timing of movement-related activity in the FEF. Preceding rapid corrective saccades, the movement-related activity of all neurons began before explicit error signals arise in the medial frontal cortex. The movement-related activity of many neurons began before visual feedback of the error was registered and that of a few neurons began before the error saccade was completed. Thus movement-related activity leading to rapid corrective saccades can be guided by an internal representation of the environment updated with a forward model of the error.

The latency and variability of latency of single-unit responses to identical visual stimulation were measured in the frontal eye field (FEF), supplementary eye field (SEF), and anterior cingulate cortex (ACC) of macaque monkeys performing visually guided saccades. The mean visual response latency was significantly shorter in FEF (64 ms) than in SEF (81 ms) or ACC (100 ms), and latency values determined by four methods agreed. The latency variability of the visual response was respectively less in FEF (21 ms) than in SEF (37 ms) or ACC (41 ms). Latency, variability of latency, and magnitude of the visual responses were correlated within FEF and SEF but not ACC. These characteristics of the visual response are consistent with the degree of convergence of visual afferents to these areas and constrain hypotheses about visual processing in the frontal lobe.

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.

REPLY: Several important questions are raised in the recent comparison by Balan and Gottlieb (2009) between the description by Balan et al. (2008) of lateral intraparietal (LIP) neuron activity in monkeys performing visual search with manual responses and our recent report of frontal eye field (FEF) neuron activity in monkeys performing visual search with saccade responses (Cohen et al. 2009). Both studies manipulated the number of distractors in the search display. Balan et al. 2008 reported decreased firing rate with increasing set size, but they reported no delay in the time at which activity for the target exceeded activity for the distractors, referred to as target selection time. Cohen and colleagues (2009) also reported decreased firing rate with increasing set size, but also observed delayed target selection time with increasing set size. How should we interpret the different observations across laboratories, effectors, cortical areas, and task designs? First, we emphasize that this is not a case of one observation being correct and the other incorrect. The results of both studies are valid within their respective contexts. However, the question remains: which difference between studies explains the different outcomes? We argue that task demands are the major factors. In other words, measured under the same task demands, we predict that the same pattern of results would be obtained across effector (manual response vs. saccade) and cortical area (LIP vs. FEF). The first step of the argument is to appreciate that categorical statements about the relationship between target selection time and response time are not possible because these times vary for at least three reasons. First, neuron type matters. Multiple

Schmolesky, Matthew T., Youngchang Wang, Doug P. Hanes, Kirk G. Thompson, Stefan Leutgeb, Jeffrey D. Schall, and Audie G. Leventhal. Signal timing across the macaque visual system. J. Neurophysiol. 79: 3272–3278, 1998. The onset latencies of single-unit responses evoked by flashing visual stimuli were measured in the parvocellular (P) and magnocellular (M) layers of the dorsal lateral geniculate nucleus (LGNd) and in cortical visual areas V1, V2, V3, V4, middle temporal area (MT), medial superior temporal area (MST), and in the frontal eye field (FEF) in individual anesthetized monkeys. Identical procedures were carried out to assess latencies in each area, often in the same monkey, thereby permitting direct comparisons of timing across areas. This study presents the visual flash-evoked latencies for cells in areas where such data are common (V1 and V2), and are therefore a good standard, and also in areas where such data are sparse (LGNd M and P layers, MT, V4) or entirely lacking (V3, MST, and FEF in anesthetized preparation). Visual-evoked onset latencies were, on average, 17 ms shorter in the LGNd M layers than in the LGNd P layers. Visual responses occurred in V1 before any other cortical area. The next wave of activation occurred concurrently in areas V3, MT, MST, and FEF. Visual response latencies in areas V2 and V4 were progressively later and more broadly distributed. These differences in the time course of activation across the dorsal and ventral streams provide important temporal constraints on theories of visual processing.

Hanes, Doug P., Warren F. Patterson II, and Jeffrey D. Schall. Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J. Neurophysiol. 79: 817–834, 1998. A new approach was developed to investigate the role of visual-, movement-, and fixation-related neural activity in gaze control. We recorded unit activity in the frontal eye fields (FEF), an area in frontal cortex that plays a central role in the production of purposeful eye movements, of monkeys ( Macaca mulatta) performing visually and memory-guided saccades. The countermanding paradigm was employed to assess whether single cells generate signals sufficient to control movement production. The countermanding paradigm consists of a task that manipulates the monkeys' ability to withhold planned saccades combined with an analysis based on a race model that provides an estimate of the time needed to cancel the movement that is being prepared. We obtained clear evidence that FEF neurons with eye movement-related activity generate signals sufficient to control the production of gaze shifts. Movement-related activity, which was growing toward a trigger threshold as the saccades were prepared, decayed in response to the stop signal within the time required to cancel the saccade. Neurons with fixation-related activity were less common, but during the countermanding paradigm, these neurons exhibited an equally clear gaze-control signal. Fixation cells that had a pause in firing before a saccade exhibited elevated activity in response to the stop signal within the time that the saccade was cancelled. In contrast to cells with movement or fixation activity, neurons with only visually evoked activity exhibited no evidence of signals sufficient to control the production of gaze shifts. However, a fraction of tonic visual cells exhibited a reduction of activity once a saccade command had been cancelled even though the visual target was still present in the receptive field. These findings demonstrate the use of the countermanding paradigm in identifying neural signatures of motor control and provide new information about the fine balance between gaze shifting and gaze holding mechanisms.

1. The purpose of this study was to analyze the response properties of neurons in the frontal eye fields (FEF) of rhesus monkeys (Macaca mulatta) and to compare and contrast the various functional classes with those recorded in the supplementary eye fields (SEF) of the same animals performing the same go/no-go visual tracking task. Three hundred ten cells recorded in FEF provided the data for this investigation. 2. Visual cells in FEF responded to the stimuli that guided the eye movements. The visual cells in FEF responded with a slightly shorter latency and were more consistent and phasic in their activation than their counterparts in SEF. The receptive fields tended to emphasize the contralateral hemifield to the same extent as those observed in SEF visual cells. 3. Preparatory set cells began to discharge after the presentation of the target and ceased firing before the saccade, after the go/no-go cue was given. These neurons comprised a smaller proportion in FEF than in SEF. In contrast to their counterparts in SEF, the preparatory set cells in FEF did not respond preferentially in relation to contralateral movements, even though most responded preferentially for movements in one particular direction. The time course of the discharge of the FEF set cells was similar to that of their SEF counterparts, except that they reached their peak level of activation sooner. The few preparatory set cells in FEF tested with both auditory and visual stimuli tended to respond preferentially to the visual targets, whereas, in contrast, most set cells in SEF were bimodal. 4. Sensory-movement cells represented the largest population of cells recorded in FEF, responding in relation to both the presentation of the targets and the execution of the saccade. Although some of these sensory-movement cells resembled their counterparts in SEF by exhibiting a sustained elevation of activity, most of the FEF sensory-movement cells gave two discrete bursts, one after the presentation of the target and another before and during the saccade. Like their counterparts in SEF, the sensory-movement cells tended to be tuned for saccades into the contralateral hemifield, but this tendency was more pronounced in FEF than in SEF. The FEF sensory-movement cells discharged more briskly, with a shorter latency relative to the presentation of the target, than their counterparts in SEF. In addition, the FEF sensory-movement neurons reached their peak activation sooner than SEF sensory-movement neurons. Most FEF sensory-movement cells exhibited different patterns of activation in response to visual and auditory targets.(ABSTRACT TRUNCATED AT 400 WORDS)