Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.     

Incomplete suppression of distractor-related activity in the frontal eye field results in curved saccades

Saccades in the presence of distractors show significant trajectory curvature. Based on previous work in the superior colliculus (SC), we speculated that curvature arises when a movement is initiated before competition between the target and distractor goals has been fully resolved. To test this hypothesis, we recorded frontal eye field (FEF) activity for curved and straight saccades in search. In contrast to the SC, activity in FEF is normally poorly correlated with saccade dynamics. However, the FEF, like the SC, is involved in target selection. Thus if curvature is caused by incomplete target selection, we expect to see its neural correlates in the FEF. We found that saccades that curve toward a distractor are accompanied by an increase in perisaccadic activity of FEF neurons coding the distractor location, and saccades that curve away are accompanied by a decrease in activity. In contrast, for FEF neurons coding the target location, there is no significant difference in activity between curved and straight saccades. To establish that the distractor-related activity is causally related to saccade curvature, we applied microstimulation to sites in the FEF before saccades to targets presented without distractors. The stimulation was subthreshold for evoking saccades and the temporal structure of the stimulation train resembled the activity recorded for curved saccades. The resulting movements curved toward the location coded by the stimulation site. These results support the idea that saccade curvature results from incomplete suppression of distractor-related activity during target selection.     

Control of fixation and saccades during an anti-saccade task: an investigation in humans with chronic lesions of oculomotor cortex

Fourteen patients with a chronic, unilateral lesion restricted to the frontal lobe (twelve involving the frontal eye field (FEF)), nine patients with a chronic, unilateral lesion restricted to posterior association cortex (eight involving the intraparietal sulcus (IPS)), and twelve neurologically normal control subjects were studied in an anti-saccade task. A combination of manipulating cuing and fixation offset enabled us to examine the effects of chronic oculomotor lesions on both saccade preparation and voluntary control over ocular fixation. Patients with lesions of the FEF made more errors (reflexive glances) toward contralesional targets, whereas patients with IPS lesions made fewer errors toward contralesional targets. Patients with IPS lesions had increased latencies to initiate saccades away from contralesional targets. For FEF patients, the presence of a fixation point inhibited the initiation of contralesionally directed saccades less than those directed ipsilesionally. Saccade preparation in response to a cue did not reduce the inhibitory effect of a fixation point on initiating anti-saccades directed either ipsilesionally or contralesionally for either patient group. We conclude that chronic IPS lesions result in a reduced contralesional visual grasp reflex (VGR) and delayed utilization of visual signals in the contralesional field for planning voluntary eye movements. In contrast, patients with chronic FEF lesions are impaired in inhibiting the VGR toward contralesional signals, and manifest an asymmetry in the balance between fixation and saccade activity. Moreover, voluntary control of fixation is compromised after chronic damage to either frontal or parietal oculomotor cortex.     

The effects of microstimulation of the dorsomedial frontal cortex on saccade latency

Neural regions in the dorsomedial frontal cortex (DMFC), including the supplementary eye field (SEF) and the presupplementary motor area (pre-SMA), are likely candidates for generating top-down control of saccade target selection. To investigate this, we applied electrical microstimulation to these structures while saccades were being planned to visual targets. Stimulation administered to superficial and lateral DMFC sites that were within or close to the SEF delayed ipsilateral and facilitated contralateral saccades. Facilitation was limited to saccades made toward targets in a narrow, contralateral movement field that had endpoints consistent with the goal of evoked saccades. Facilitation occurred with current delivered before target onset and delay with current applied after this time. Stimulation at deeper, medial sites that encompassed the pre-SMA resulted in mostly bilateral delay. The amount of delay at these sites was usually greater for ipsilateral saccades and increased with current amplitude. Changes in saccade latency were not accompanied by altered endpoint, trajectory, or peak velocity. The spatial specificity of SEF stimulation in inducing latency changes suggests that the SEF participates in selecting saccade goals. The less specific delay with pre-SMA stimulation suggests that it is involved in postponing visually guided saccades, thus likely permitting other oculomotor structures to select saccade goals.     

Interactions between natural and electrically evoked saccades

Summary Fixed-vector saccades evoked by electrical stimulation may result from the elicitation of a retinal error signal directing the eyes toward a goal, or from the elicitation of a motor error signal determining the vector itself. Theoretically, the two mechanisms can be differentiated by delivering the stimulation while the eyes are already in motion (colliding saccade paradigm), thereby changing the eye position from which the evoked saccade starts. Only in the first case is the trajectory of the evoked saccade expected to be modified to compensate for part of the ongoing eye movement. An attempt was made to distinguish retinal vs. motor error mechanisms by applying the colliding saccade paradigm of stimulation to 29 sites throughout the superior colliculus (SC) of two trained monkeys. Compensatory evoked saccades, as predicted by the retinal error hypothesis, were obtained consistently in the superficial layers and at deeper sites where visual unit responses could be recorded. Conversely, in deep layers where only presaccadic activity was found, evoked saccades either were not affected by collision or summed their vectors with that of the ongoing movement. These last observations are both consistent with the hypothesis that the signal produced from deep sites was an initial motor error. A second observation was incidentally made: when stimulation was applied to the most superficial SC region, it definitively erased the goal of the ongoing saccade, and the latter did not resume its interrupted course. The colliding saccade paradigm may be useful in clarifying the role of structures involved in oculomotor function.     

On the gap effect for saccades evoked by electrical microstimulation of frontal eye fields in monkeys

To investigate the mechanisms of fixation disengagement and saccade initiation, we electrically stimulated the macaque frontal eye fields (FEF) while monkeys performed a visual fixation task. We tested the effect of introducing a temporal gap between fixation target offset and the onset of the electrical stimulus. We found that the duration of the gap had a pronounced effect on the probability of producing electrically evoked saccades at a given current level. The highest probability was found for gaps of 200 ms duration. There were also effects of gap duration on saccade latency and amplitude for most of the stimulation sites. The increase in saccade probability may be associated with lower current thresholds for evoking saccades.     

Rostrocaudal distinction of the dorsal premotor area based on oculomotor involvement

To investigate functional differences between the rostral and caudal parts of the dorsal premotor cortex (PMd), we first examined the effects of intracortical microstimulation (ICMS) while monkeys were performing oculomotor and limb motor tasks or while they were at rest. We found that saccades were evoked from the rostral part (PMdr) whereas ICMS in the caudal part (PMdc) predominantly produced forelimb or body movements. Subsequently, we examined neuronal activity in relation to the performance of visually cued and memorized saccades while monkeys reached an arm toward a visual target. We found that roughly equal numbers of PMdr neurons were active during performance of the oculomotor and limb motor tasks. In contrast, the majority of PMdc neurons were related preferentially to arm movements and not to saccades. In the subsequent analysis, we found that the oculomotor effects evoked in the PMdr differ from the effects evoked in either the frontal eye field (FEF) or supplementary eye field (SEF). These findings suggest that the PMdr is involved in oculomotor as well as limb motor behavior. However, the oculomotor involvement of the PMdr seems to have a functional aspect different from that operating in the FEF and SEF.     

Blink-perturbed saccades in monkey. I. Behavioral analysis

Saccadic eye movements are thought to be influenced by blinking through premotor interactions, but it is still unclear how. The present paper describes the properties of blink-associated eye movements and quantifies the effect of reflex blinks on the latencies, metrics, and kinematics of saccades in the monkey. In particular, it is examined to what extent the saccadic system accounts for blink-related perturbations of the saccade trajectory. Trigeminal reflex blinks were elicited near the onset of visually evoked saccades by means of air puffs directed on the eye. Reflex blinks were also evoked during a straight-ahead fixation task. Eye and eyelid movements were measured with the magnetic-induction technique. The data show that saccade latencies were reduced substantially when reflex blinks were evoked prior to the impending visual saccades as if these saccades were triggered by the blink. The evoked blinks also caused profound spatial-temporal perturbations of the saccades. Deflections of the saccade trajectory, usually upward, extended up to approximately 15 degrees. Saccade peak velocities were reduced, and a two- to threefold increase in saccade duration was typically observed. In general, these perturbations were largely compensated in saccade mid-flight, despite the absence of visual feedback, yielding near-normal endpoint accuracies. Further analysis revealed that blink-perturbed saccades could not be described as a linear superposition of a pure blink-associated eye movement and an unperturbed saccade. When evoked during straight-ahead fixation, blinks were accompanied by initially upward and slightly abducting eye rotations of approximately 2-15 degrees. Back and forth wiggles of the eye were frequently seen; but in many cases the return movement was incomplete. Rather than drifting back to its starting position, the eye then maintained its eccentric orbital position until a downward corrective saccade toward the fixation spot followed. Blink-associated eye movements were quite rapid, albeit slower than saccades, and the velocity-amplitude-duration characteristics of the initial excursions as well as the return movements were approximately linear. These data strongly support the idea that blinks interfere with the saccade premotor circuit, presumably upstream from the neural eye-position integrator. They also indicated that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensatory behavior. The tight latency coupling between saccades and blinks is consistent with an inhibition of omnipause neurons by the blink system, suggesting that the observed changes in saccade kinematics arise elsewhere in the saccadic premotor system.     

3-Dimensional eye-head coordination in gaze shifts evoked during stimulation of the lateral intraparietal cortex

Coordinated eye-head gaze shifts have been evoked during electrical stimulation of the frontal cortex (supplementary eye field (SEF) and frontal eye field (FEF)) and superior colliculus (SC), but less is known about the role of lateral intraparietal cortex (LIP) in head-unrestrained gaze shifts. To explore this, two monkeys (M1 and M2) were implanted with recording chambers and 3-D eye+ head search coils. Tungsten electrodes delivered trains of electrical pulses (usually 200 ms duration) to and around area LIP during head-unrestrained gaze fixations. A current of 200 μA consistently evoked small, short-latency contralateral gaze shifts from 152 sites in M1 and 243 sites in M2 (Constantin et al., 2007). Gaze kinematics were independent of stimulus amplitude and duration, except that subsequent saccades were suppressed. The average amplitude of the evoked gaze shifts was 8.46° for M1 and 8.25° for M2, with average head components of only 0.36 and 0.62° respectively. The head's amplitude contribution to these movements was significantly smaller than in normal gaze shifts, and did not increase with behavioral adaptation. Stimulation-evoked gaze, eye and head movements qualitatively obeyed normal 3-D constraints (Donders' law and Listing's law), but with less precision. As in normal behavior, when the head was restrained LIP stimulation evoked eye-only saccades in Listing's plane, whereas when the head was not restrained, stimulation evoked saccades with position-dependent torsional components (driving the eye out of Listing's plane). In behavioral gaze-shifts, the vestibuloocular reflex (VOR) then drives torsion back into Listing's plane, but in the absence of subsequent head movement the stimulation-induced torsion was “left hanging”. This suggests that the position-dependent torsional saccade components are preprogrammed, and that the oculomotor system was expecting a head movement command to follow the saccade. These data show that, unlike SEF, FEF, and SC stimulation in nearly identical conditions, LIP stimulation fails to produce normally-coordinated eye-head gaze shifts.     

Expectations can modulate the frequency and timing of multiple saccades: a TMS study

This study was undertaken to determine if target predictability could modulate saccadic planning and timing at the level of the frontal eye fields (FEF). To this end, healthy participants performed two gap saccade tasks in which the targets were displaced left or right of the midline in either a predictable or a random fashion. Additionally, half of the participants were informed about this manipulation. Single pulse transcranial magnetic stimulation (TMS) was applied to the left FEF before, during, or after the target onset. We examined both the saccade latency and the frequency of multiple saccades (MS) (i.e., saccades that covered <90 % of the distance to the target and were subsequently followed by a corrective saccade). Findings revealed that saccadic reaction times were quickest to the more predictable target side and also confirmed that MS were released more quickly than single saccades. Further, the frequency of MS differed between target locations; higher frequencies of MS were found on the unpredictable side, showing more vulnerability to TMS disruption. In conclusion, we have demonstrated that target predictability modulates saccade planning and that this modulation takes place at least in part in the FEF. The influence of FEF in these processes is observed both in the latencies with which saccades are executed and in the timing and characteristics of the multiple saccades that are observed under different task constraints. Finally, the timing of the FEF contribution also appears to be influenced by the manipulation of target predictability. Each of these observations serves to further clarify the role of the human FEF in saccade planning.     

The dorsomedial frontal cortex of the rhesus monkey: topographic representation of saccades evoked by electrical stimulation

The dorsomedial frontal cortex (DMFC) of monkeys has been implicated in mediating visually guided saccadic eye movements. The purpose of this study was to determine whether the DMFC has a topographic map coding final eye position, and to ascertain whether this region subserves the maintenance of eye position. The DMFC was stimulated electrically while monkeys fixated a target presented somewhere in visual space. A series of parametric tests was conducted to ascertain the best stimulation parameters to evoke saccades. Electrical stimulation typically produced contraversive saccades that converged onto a region of space, the termination zone. For some stimulation sites, however, stimulation produced ipsiversive saccades. This occurred when the termination zone was located straight ahead of the monkey. Convergence onto an orbital position was never observed during stimulation of the frontal eye fields (FEF), stimulation of which evoked fixed-vector saccades. The latency to evoke a saccade from the DMFC varied with fixation position, such that it increased monotonically the closer the fix spot was to the termination zone. Moreover, the probability of evoking a saccade from the DMFC decreased the closer the fix spot was to the termination zone. The latency for evoking a saccade and the probability of evoking a saccade from the FEF did not vary with fixation position. Horizontal head movements were not evoked from the DMFC while a monkey fixated targets presented in different positions of visual space. Moveover, changing the position of the head with respect to the body did not change the location of a termination zone with respect to the head. The DMFC was found to contain a topographic coding of termination zones, with rostral sites representing zones in extreme contralateral visual space, and caudal sites representing zones straight ahead or ipsilaterally. Furthermore, lateral sites represented zones in upper visual space, whereas medial sites represented zones in lower visual space. Once the eyes were positioned within a termination zone, further stimulation fixed the gaze and inhibited visually evoked saccades. Following release from inhibition, which occurred shortly after the end of stimulation, the saccades reached the visual target accurately. This shows that the stimulation delayed the execution of the saccades without actually aborting their execution. We conclude that the DMFC contains a map representing eye position in craniotopic coordinates, and we argue that this map is utilized to maintain eye position.     

Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. I. Suppression of ipsilateral saccades

When a saccade occurs to an interesting object, visual fixation holds its image on the fovea and suppresses saccades to other objects. Electrical stimulation of the frontal eye field (FEF) has been reported to elicit saccades, and recently also to suppress saccades. This study was performed to characterize properties of the suppression of visually guided (Vsacs) and memory-guided saccades (Msacs) induced by electrical stimulation of the FEF in trained monkeys. For any given stimulation site, we determined the threshold for electrically evoked saccades (Esacs) at < or =50 microA and then examined suppressive effects of stimulation at the same site on Vsacs and Msacs. FEF stimulation suppressed the initiation of both Vsacs and Msacs during and about 50 ms after stimulation at stimulus intensities lower than those for eliciting Esacs, but did not affect the vector of these saccades. Suppression occurred for ipsiversive but not contraversive saccades, and more strongly for saccades with larger amplitudes and those with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for suppression was about 50 ms before saccade onset, which suggests that suppression occurred in the efferent pathway for generating Vsacs at the premotor rather than the motoneuronal level, most probably in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of ipsilateral saccades were distributed over the classical FEF where saccade-related movement neurons were observed. The results suggest that the FEF may play roles in not only generating contraversive saccades but also maintaining visual fixation by suppressing ipsiversive saccades.     

Does microstimulation evoke fixed-vector saccades by generating their vector or by specifying their goal?

Summary Electrical stimulation was performed at several sites of the monkey's forebrain producing fixed-vector saccades when the eyes were steady. When the same stimulation was applied during or immediately after a spontaneous eye movement, the saccade trajectory was considerably modified: the eyes were driven, from wherever they were deviated by the spontaneous movement, to the point where the fixed-vector saccade would have brought them if the spontaneous movement had not occurred. This finding implies first, that saccades evoked from these sites are directed toward a goal and, second, that the goal is defined with respect to an eye position sampled long in advance (before the spontaneous eye movement). This is consistent with the hypothesis that the electrical stimulation evoked the retinotopic representation of a target whose spatial coordinates were then computed at further stages to produce a saccade. Using the present paradigm, it may be possible to distinguish brain sites processing retinal error (at the visual stage) from those processing motor error (at the motor stage).     

Characteristics of contralesional and ipsilesional saccades in hemianopic patients

In order to further our understanding of action-blindsight, four hemianopic patients suffering from visual field loss contralateral to a unilateral occipital lesion were compared to six healthy controls during a double task of verbally reported target detection and saccadic responses toward the target. Three oculomotor tasks were used: a fixation task (i.e., without saccade) and two saccade tasks (eliciting reflexive and voluntary saccades, using step and overlap 600 ms paradigms, respectively), in separate sessions. The visual target was briefly presented at two different eccentricities (5° and 8°), in the right or left visual hemifield. Blank trials were interleaved with target trials, and signal detection theory was applied. Despite their hemifield defect, hemianopic patients retained the ability to direct a saccade toward their contralesional hemifield, whereas verbal detection reports were at chance level. However, saccade parameters (latency and amplitude) were altered by the defect. Saccades to the contralesional hemifield exhibited longer latencies and shorter amplitudes compared to those of the healthy group, whereas only the latencies of reflexive saccades to the ipsilesional hemifield were altered. Furthermore, healthy participants showed the expected latency difference between reflexive and voluntary saccades, with the latter longer than the former. This difference was not found in three out of four patients in either hemifield. Our results show action-blindsight for saccades, but also show that unilateral occipital lesions have effects on saccade generation in both visual hemifields.     

Different memory types for generating saccades at different stages of learning

It has been proposed that positional memories encoded in different types of reference frame are used for the reaching hand movement in different stages of learning. However, the types of reference frame employed for generating behavior at each stage of learning remain unclear, particularly for saccades. To examine the types of reference frame for target positions, we analyzed the saccade of monkeys performing an oculomotor task. The task required the animal to make a learning-based saccade to one of the eight landmark positions specified by the color of a fixation point. According to the color of the fixation point, the target landmark position was fixed in all experimental blocks (FIX trial) or altered to other landmark positions block by block (ALTER trial). Although the monkeys learned the target landmark position in both the FIX and the ALTER trials, once the landmarks became invisible, the success rate remained high only in the FIX trials. These results suggest that the target position was learned on the basis of the landmark positions in the early stage of learning. However, the memory of the target position in space was formed after sufficient training. When the fixation point was shifted horizontally by 5 degrees and the landmarks were invisible, the saccades in the ALTER trials were made to the normal target landmark position whereas those in the FIX trials were made to the point approximately 5 degrees shifted horizontally from the normal target landmark position. These results suggest that the target position in space was initially represented in the head-centered or world-centered reference frame and then in the eye-centered reference frame. Analysis of saccade end-points indicated that a kinematically similar saccade was generated for each FIX trial. These results showed that memories encoded by different reference frames were formed to generate a saccade while the saccade toward the same target was repeatedly executed.     

Reversible inactivation of macaque frontal eye field

 The macaque frontal eye field (FEF) is involved in the generation of saccadic eye movements and fixations. To better understand the role of the FEF, we reversibly inactivated a portion of it while a monkey made saccades and fixations in response to visual stimuli. Lidocaine was infused into a FEF and neural inactivation was monitored with a nearby microelectrode. We used two saccadic tasks. In the delay task, a target was presented and then extinguished, but the monkey was not allowed to make a saccade to its location until a cue to move was given. In the step task, the monkey was allowed to look at a target as soon as it appeared. During FEF inactivation, monkeys were severely impaired at making saccades to locations of extinguished contralateral targets in the delay task. They were similarly impaired at making saccades to locations of contralateral targets in the step task if the target was flashed for ≤100 ms, such that it was gone before the saccade was initiated. Deficits included increases in saccadic latency, increases in saccadic error, and increases in the frequency of trials in which a saccade was not made. We varied the initial fixation location and found that the impairment specifically affected contraversive saccades rather than affecting all saccades made into head-centered contralateral space. Monkeys were impaired only slightly at making saccades to contralateral targets in the step task if the target duration was 1000 ms, such that the target was present during the saccade: latency increased, but increases in saccadic error were mild and increases in the frequency of trials in which a saccade was not made were insignificant. During FEF inactivation there usually was a direct correlation between the latency and the error of saccades made in response to contralateral targets. In the delay task, FEF inactivation increased the frequency of making premature saccades to ipsilateral targets. FEF inactivation had inconsistent and mild effects on saccadic peak velocity. FEF inactivation caused impairments in the ability to fixate lights steadily in contralateral space. FEF inactivation always caused an ipsiversive deviation of the eyes in darkness. In summary, our results suggest that the FEF plays major roles in (1) generating contraversive saccades to locations of extinguished or flashed targets, (2) maintaining contralateral fixations, and (3) suppressing inappropriate ipsiversive saccades. Received: 2 February 1996 / Accepted: 26 February 1997     

Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region

Over the past decade, considerable research efforts have been focused on the role of the rostral superior colliculus (SC) in control of saccades. The most recent theory separates the deeper intermediate layers of the SC into two functional regions: the rostral pole of these layers constitutes a fixation zone and the caudal region comprises the saccade zone. Sustained activity of fixation neurons in the fixation zone is argued to maintain fixation and help prevent saccade generation by exciting the omnipause neurons (OPNs) in the brain stem. This hypothesis is in contrast to the traditional view that the SC contains a topographic representation of the saccade motor map on which the rostral pole of the SC encodes signals for generating small saccades (<2 degrees ) instead of preventing them. There is therefore an unresolved controversy about the specific role on the most rostral region of the SC, and we reexamined its functional contribution by quantifying and comparing spatial and temporal trajectories of 30 degrees saccades perturbed by electrical stimulation of the rostral pole and more caudal regions in the SC and of the OPN region. If the rostral pole serves to preserve fixation, then saccades perturbed by stimulation should closely resemble interrupted saccades produced by stimulation of the OPN region. If it also contributes to saccade generation, then the disrupted movements would better compare with redirected saccades observed after stimulation of the caudal SC. Our experiments revealed two significant findings: 1) the locus of stimulation was the primary factor determining the perturbation effect. If the directions of the target-directed saccade and stimulation-evoked saccade were aligned and if the stimulation was delivered within approximately the rostral 2 mm (<10 degrees amplitude) of SC, the ongoing saccade stopped in midflight but then resumed after stimulation end to reach the original visually specified goal with close to normal accuracy. When stimulation was applied at more caudal sites, the ongoing saccade directly reached the target location without stopping at an intermediate position. If the directions differed considerably, both initial and resumed components were typically observed for all stimulation sites. 2) A quantitative analysis of the saccades perturbed from the fixation zone showed significant deviations from their control spatial trajectories. Thus they resembled redirected saccades induced by caudal SC stimulation and differed significantly from interrupted saccades produced by OPN stimulation. The amplitude of the initial saccade, latency of perturbation, and spatial redirection were greatest for the most caudal sites and decreased gradually for rostral sites. For stimulation sites within the rostral pole of SC, the measures formed a smooth continuation of the trends observed in the saccade zone. As these results argue for the saccade zone concept, we offer reinterpretations of the data used to support the fixation zone model. However, we also discuss scenarios that do not allow an outright rejection of the fixation zone hypothesis.     

Frames of reference for saccadic command tested by saccade collision in the supplementary eye field

In what frame of reference does the supplementary eye field (SEF) encode saccadic eye movements? In this study, the "saccade collision" test was used to determine whether a saccade electrically evoked in the monkey's SEF is programmed to reach an oculocentric goal or a nonoculocentric (e.g., head or body-centered) goal. If the eyes start moving just before or when an oculocentric goal is imposed by electrical stimulation, the trajectory of the saccade to that goal should compensate for the ongoing movement. Conversely, if the goal imposed by electrical stimulation is nonoculocentric, the trajectory of the evoked saccade should not be altered. In head-fixed experiments, we mapped the trajectories of evoked saccades while the monkey fixated at each of 25 positions 10 degrees apart in a 40 x 40 degrees grid. For each studied SEF site, we calculated convergences indices and found that "convergent" and "nonconvergent" sites were separately clustered: nonconvergent rostral to convergent. Then, the "saccade collision" test was systematically applied. We found compensation at sites where saccades were of the nonconvergent type and practically no compensation at sites where saccades were of the convergent type. The results indicate that the SEF can encode saccade goals in at least two frames of reference and suggest a rostrocaudal segregation in the representation of these two modes.     

Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades.

Muscimol-induced inactivation of the monkey frontal eye field: effects on visually and memory-guided saccades. Although neurophysiological, anatomic, and imaging evidence suggest that the frontal eye field (FEF) participates in the generation of eye movements, chronic lesions of the FEF in both humans and monkeys appear to cause only minor deficits in visually guided saccade generation. Stronger effects are observed when subjects are tested in tasks with more cognitive requirements. We tested oculomotor function after acutely inactivating regions of the FEF to minimize the effects of plasticity and reallocation of function after the loss of the FEF and gain more insight into the FEF contribution to the guidance of eye movements in the intact brain. Inactivation was induced by microinjecting muscimol directly into physiologically defined sites in the FEF of three monkeys. FEF inactivation severely impaired the monkeys' performance of both visually guided and memory-guided saccades. The monkeys initiated fewer saccades to the retinotopic representation of the inactivated FEF site than to any other location in the visual field. The saccades that were initiated had longer latencies, slower velocities, and larger targeting errors than controls. These effects were present both for visually guided and for memory-guided saccades, although the memory-guided saccades were more disrupted. Initially, the effects were restricted spatially, concentrating around the retinotopic representation at the center of the inactivated site, but, during the course of several hours, these effects spread to flanking representations. Predictability of target location and motivation of the monkey also affected saccadic performance. For memory-guided saccades, increases in the time during which the monkey had to remember the spatial location of a target resulted in further decreases in the accuracy of the saccades and in smaller peak velocities, suggesting a progressive loss of the capacity to maintain a representation of target location in relation to the fovea after FEF inactivation. In addition, the monkeys frequently made premature saccades to targets in the hemifield ipsilateral to the injection site when performing the memory task, indicating a deficit in the control of fixation that could be a consequence of an imbalance between ipsilateral and contralateral FEF activity after the injection. There was also a progressive loss of fixation accuracy, and the monkeys tended to restrict spontaneous visual scanning to the ipsilateral hemifield. These results emphasize the strong role of the FEF in the intact monkey in the generation of all voluntary saccadic eye movements, as well as in the control of fixation.     

Multisensory interactions in saccade target selection: Curved saccade trajectories

In a series of experiments, we examined the change in saccade trajectories observed when distractors are presented at non-target locations. The primary aim of the experiments was to examine multisensory interaction effects between the visual, auditory and somatosensory modalities in saccade generation. In each experiment observers made saccades to visual targets above and below fixation in the presence of visual, auditory or tactile stimuli to the left or right of fixation. In experiment 1 distractor location indicated which of two stimuli was the target for the saccade. Saccade trajectories showed strong leftward curvature following right-side distractors and showed rightward curvature following left-side distractors. The largest effects on trajectories were observed for visual distractors, but significant curvature was observed with auditory and somatosensory distractors. In experiment 2 saccades were made following the onset of a visual target (reflexive) or following presentation of an arrow at fixation (voluntary), and task-irrelevant crossmodal distractors were presented simultaneously with target onset. Both voluntary and reflexive saccades were found to curve away from task-irrelevant visual distractors, but auditory and somatosensory distractors did not modulate saccade trajectories. In experiment 3 task-irrelevant distractors preceded the onset of the target by 100 ms. Reflexive saccades were found to curve away from visual, auditory and somatosensory distractors, but voluntary saccades curved away from visual distractors only. The modulation of saccade trajectories by distractors from different modalities is interpreted in terms of inhibitory processes operating in neural structures involved in saccade generation. Our findings suggest that visual, auditory and somatosensory distractors can all modulate saccade trajectories. Such effects could be related to the inhibition of populations of neurons, in a common motor map, for the selection of a saccade target.