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Monkeys and humans can easily make accurate saccades to stimuli that appear and disappear before an intervening saccade to a different location. We used the flashed-stimulus task to study the memory processes that enable this behavior, and we found two different kinds of memory responses under these conditions. In the short-term spatial memory response, the monkey fixated, a stimulus appeared for 50 ms outside the neuron's receptive field, and from 200 to 1,000 ms later the monkey made a saccade that brought the receptive field onto the spatial location of the vanished stimulus. Twenty-eight of 48 visuomovement cells and 21/32 visual cells responded significantly under these circumstances even though they did not discharge when the monkey made the same saccade without the stimulus present or when the stimulus appeared and the monkey did not make a saccade that brought its spatial location into the receptive field. Response latencies ranged from 48 ms before the beginning of the saccade (predictive responses) to 272 ms after the beginning of the saccade. After the monkey made a series of 16 saccades that brought a stimulus into the receptive field, 21 neurons demonstrated a longer term, intertrial memory response: they discharged even on trials in which no stimulus appeared at all. This intertrial memory response was usually much weaker than the within-trial memory response, and it often lasted for over 20 trials. We suggest that the frontal eye field maintains a spatially accurate representation of the visual world that is not dependent on constant or continuous visual stimulation, and can last for several minutes.

We frequently reposition our gaze by making rapid ballistic eye movements that are called saccades. Saccades pose problems for the visual system, because they generate rapid, large-field motion on the retina and change the relationship between the object position in external space and the image position on the retina. The brain must ignore the one and compensate for the other. Much progress has been made in recent years in understanding the effects of saccades on visual function and elucidating the mechanisms responsible for them. Evidence suggests that saccades trigger two distinct neural processes: (1) a suppression of visual sensitivity, specific to the magnocellular pathway, that dampens the sensation of motion and (2) a gross perceptual distortion of visual space in anticipation of the repositioning of gaze. Neurophysiological findings from several laboratories are beginning to identify the neural substrates involved in these effects.

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 coordinate system.

Efferents from the frontal eye fields (FEF) to the ipsilateral frontal lobe were studied by autoradiography of tritiated tracers (leucine, proline, and fucose) in seven macaque monkeys that were used previously to describe subcortical connections. In four of the cases, tracer injection sites were confirmed by low thresholds for the electrical elicitation of saccadic eye movements. Cases were grouped as lFEF of sFEF cases according to large or small saccades that were characteristic of the injection site. Projections from the FEF terminated in five frontal regions: 1) area FD on the dorsomedial convexity; 2) area FC (containing SEF) medial to the upper limb of the arcuate sulcus; 3) areas FD and FD delta along the walls of the principal sulcus; 4) area FCBm on the deep, posterior wall of the arcuate sulcus inferior to the sulcal spur; and 5) the inferolateral cortex (area FDi) on the convexity and lateral two thirds of the anterior wall of the arcuate sulcus. Projections in sFEF cases tended to be confined to medial parts of dorsomedial FD and FC and the lateral wall of the principal sulcus and inferolateral convexity. Neither lFEF nor sFEF appeared to project to the SMA or pericingulate cortex. Label in these areas was found only in the cases in which tracer spread into non-FEF areas. FEF projections terminated in column-like patches of about 500-600 microns in diameter. Labeled axons and terminals were seen in all cortical layers regardless of location in the frontal lobe.

1. We studied the activity of single neurons in the monkey frontal eye fields during oculomotor tasks designed to assess the activity of these neurons when there was a dissonance between the spatial location of a target and its position on the retina. 2. Neurons with presaccadic activity were first studied to determine their receptive or movement fields and to classify them as visual, visuomovement, or movement cells with the use of the criteria described previously (Bruce and Goldberg 1985). The neurons were then studied by the use of double-step tasks that dissociated the retinal coordinates of visual targets from the dimensions of saccadic eye movements necessary to acquire those targets. These tasks required that the monkeys make two successive saccades to follow two sequentially flashed targets. Because the second target disappeared before the first saccade occurred, the dimensions of the second saccade could not be based solely on the retinal coordinates of the target but also depended on the dimensions of the first saccade. We used two versions of the double-step task. In one version neither target appeared in the cell's receptive or movement field, but the second eye movement was the optimum amplitude and direction for the cell (right-EM/wrong-RF task). In the other the second stimulus appeared in the cell's receptive field, but neither eye movement was appropriate for the cell (wrong-EM/right-RF task). 3. Most frontal-eye-field cells discharged in the right-EM/wrong-RF version of the double-step task. Their discharge began after the first saccade and continued until the second saccade was made. They usually discharged even on occasional trials in which the monkey failed to make the second saccade. They discharged much less, or not at all, in the wrong-EM/right-RF version of the double-step paradigm. Thus most presaccadic cells in the frontal eye fields were tuned to the dimensions of saccadic eye movements rather than to the coordinates of retinal stimulation. 4. Eleven movement cells (including 1 which also had independent postsaccadic activity for saccades opposite its presaccadic movement field) were studied, and all had significant activity in the right-EM/wrong-RF task. 5. Almost all (28/32) visuomovement cells, including 12 with independent postsaccadic activity, discharged in the right-EM/wrong-RF task. None of the four that failed had independent postsaccadic activity. 6. The majority (26/40) of visual cells were responsive in the right-EM/wrong-RF task.(ABSTRACT TRUNCATED AT 400 WORDS)

1. We recorded from 257 neurons in the banks of the posterior third of the principal sulcus of two rhesus monkeys trained to look at a fixation point and make saccades to stimuli in the visual periphery. Sixty-six percent (220/257) discharged or were suppressed in association with one or more aspects of the tasks we used. 2. Fifty-eight percent (151/257) of the neurons responded to the appearance of a spot of light in some part of the contralateral visual field. Cells did not seem to have absolute requirements for stimulus shape, size, or direction of motion. 3. Thirty-six percent (29/79) of visually responsive neurons tested quantitatively gave an enhanced response to the stimulus in the receptive field when the monkey had to make a saccade to the stimulus when its appearance was synchronous with the disappearance of the fixation point (synchron task). Twenty-nine percent (19/57) of the neurons gave an enhanced response to the stimulus when the monkey had to make a saccade to the stimulus some time after it appeared (delayed-saccade task). In general, enhancement in the synchron task correlated well with enhancement in the delayed-saccade task. 4. Enhancement was spatially specific. It did not occur when the monkey made a saccade to a stimulus outside the receptive field even though there was a stimulus within the receptive field. 5. Twenty-three percent (27/117) of neurons studied in the delayed-saccade task gave two bursts, one at the appearance of the stimulus and a second one around the saccade. This second burst generally did not occur when the monkey made the same saccade to a remembered target, but instead required the presence of the visual stimulus, and so we describe it as a reactivation of the visual response. Reactivation was also spatially specific. 6. The latency from reactivation to the beginning of the saccade ranged from 160 ms before the saccade to the beginning of the saccade. Reactivation usually continued for several hundred milliseconds after the saccade, sometimes for the duration of the trial. 7. Reactivation and enhancement are not the same mechanism. Although some cells showed both phenomena there was no correlation between enhancement and reactivation. 8. Cells that showed reactivation in the saccade task also showed reactivation at a weaker level in a suppressed-saccade task. In this task the monkeys had to hold fixation despite the disappearance of the fixation point and the continued presence of the peripheral stimulus.(ABSTRACT TRUNCATED AT 400 WORDS)

We studied single neurons in the frontal eye fields of awake macaque monkeys and compared their activity with the saccadic eye movements elicited by microstimulation at the sites of these neurons. Saccades could be elicited from electrical stimulation in the cortical gray matter of the frontal eye fields with currents as small as 10 microA. Low thresholds for eliciting saccades were found at the sites of cells with presaccadic activity. Presaccadic neurons classified as visuomovement or movement were most associated with low (less than 50 microA) thresholds. High thresholds (greater than 100 microA) or no elicited saccades were associated with other classes of frontal eye field neurons, including neurons responding only after saccades and presaccadic neurons, classified as purely visual. Throughout the frontal eye fields, the optimal saccade for eliciting presaccadic neural activity at a given recording site predicted both the direction and amplitude of the saccades that were evoked by microstimulation at that site. In contrast, the movement fields of postsaccadic cells were usually different from the saccades evoked by stimulation at the sites of such cells. We defined the low-threshold frontal eye fields as cortex yielding saccades with stimulation currents less than or equal to 50 microA. It lies along the posterior portion of the arcuate sulcus and is largely contained in the anterior bank of that sulcus. It is smaller than Brodmann's area 8 but corresponds with the union of Walker's cytoarchitectonic areas 8A and 45. Saccade amplitude was topographically organized across the frontal eye fields. Amplitudes of elicited saccades ranged from less than 1 degree to greater than 30 degrees. Smaller saccades were evoked from the ventrolateral portion, and larger saccades were evoked from the dorsomedial portion. Within the arcuate sulcus, evoked saccades were usually larger near the lip and smaller near the fundus. Saccade direction had no global organization across the frontal eye fields; however, saccade direction changed in systematic progressions with small advances of the microelectrode, and all contralateral saccadic directions were often represented in a single electrode penetration down the bank of the arcuate sulcus. Furthermore, the direction of change in these progressions periodically reversed, allowing particular saccade directions to be multiply represented in nearby regions of cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Electrical stimulation of the frontal eye fields of the rhesus monkey evokes saccadic eye movements. Both the amplitude of electrically elicited saccades and the threshold current for eliciting them are primarily determined by the location of the stimulating electrode within the frontal eye fields; however, threshold and amplitude also are systematically affected by the monkey's behavioral state when the stimulation is applied. If the monkey is alert, but not performing a task, saccade amplitudes are largest and thresholds are lowest. Conversely, if the monkey actively fixates a visual target, elicited saccades are smaller and threshold currents are higher. Saccades evoked during fixation have slower velocities appropriate for their reduced amplitude. Phase plane plots of eye velocity versus eye position indicate that these saccades are originally programmed to be smaller and slower, and hence are not large saccades voluntarily braked in mid-flight. As opposed to their amplitude and threshold, the direction of electrically evoked saccades is unaffected by the state of fixation. The state of attentive fixation, but not the visual fixation target itself, is the responsible factor for these effects. These results suggest that there is a difference between the state of active fixation and the state of having the eye still in the orbit without active fixation. The oculomotor system in the latter case is relatively more susceptible to signals from the cerebral cortex.

1. We examined the activity of identified corticotectal neurons in the frontal eye field of awake behaving rhesus monkeys (Macaca mulatta). Corticotectal neurons were antidromically excited using biphasic current pulses passed through monopolar microelectrodes within the superior colliculus. The activity of single corticotectal neurons was studied while the monkey performed behavioral tasks designed to test the relation of the neuron's discharge to visual and oculomotor events. 2. Fifty-one frontal eye field corticotectal neurons were examined in two monkeys. Current thresholds for antidromic excitation ranged from 6 to 1,200 microA, with a mean of 330 microA. Antidromic latencies ranged from 1.2 to 6.0 ms, with a mean of 2.25 ms. 3. Fifty-three percent of the identified corticotectal neurons were classified as having movement-related activity. They had little or no response to visual stimuli, but very strong activity before both visually guided and memory-guided saccades. An additional 6% of corticotectal neurons had visuomovement activity, combining both a visual- and a saccade-related response. In each case, visuomovement neurons antidromically excited from the superior colliculus had movement-related activity, which was much stronger than the visual component of their response. 4. Twenty-two percent of the corticotectal neurons were primarily responsive to visual stimulation of the fovea. These included both neurons responding to the onset and neurons responding to the disappearance of a light flashed on the fovea. 5. The remaining 20% of the corticotectal neurons were a heterogeneous group whose activity could not be classified as movement, visuomovement or foveal. Their responses included postsaccadic, anticipatory, and reward-related activity, as well as activity modulated during certain directions of smooth-pursuit eye movements. One neuron was unresponsive during all of the behavioral tasks used. There were no corticotectal neurons that could be classified as primarily responsive to peripheral visual stimuli. 6. Histological reconstructions of electrode penetrations localized corticotectal neurons to layer V of the frontal eye field. For 22 corticotectal neurons tested, each had its minimum threshold for antidromic excitation within the superior colliculus, as judged by either histological confirmation, or surrounding neuronal responses recorded through the stimulation microelectrode. The majority of these neurons had minimum threshold sites within the intermediate layers, a few minimum threshold sites were located within the superficial or deep collicular layers.(ABSTRACT TRUNCATED AT 400 WORDS)