Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis

1995 ◽  
Vol 103 (1) ◽  
Author(s):  
DougP. Hanes ◽  
KirkG. Thompson ◽  
JeffreyD. Schall
1996 ◽  
Vol 75 (5) ◽  
pp. 2187-2191 ◽  
Author(s):  
H. Mushiake ◽  
N. Fujii ◽  
J. Tanji

1. We studied neuronal activity in the supplementary eye field (SEF) and frontal eye field (FEF) of a monkey during performance of a conditional motor task that required capturing of a target either with a saccadic eye movement (the saccade-only condition) or with an eye-hand reach (the saccade-and-reach condition), according to visual instructions. 2. Among 106 SEF neurons that showed presaccadic activity, more than one-half of them (54%) were active preferentially under the saccade-only condition (n = 12) or under the saccade-and-reach condition (n = 45), while the remaining 49 neurons were equally active in both conditions. 3. By contrast, most (97%) of the 109 neurons in the FEF exhibited approximately equal activity in relation to saccades under the two conditions. 4. The present results suggest the possibility that SEF neurons, at least in part, are involved in signaling whether the motor task is oculomotor or combined eye-arm movements, whereas FEF neurons are mostly related to oculomotor control.


1987 ◽  
Vol 57 (1) ◽  
pp. 179-200 ◽  
Author(s):  
J. Schlag ◽  
M. Schlag-Rey

Electrical microstimulation and unit recording were performed in dorsomedial frontal cortex of four alert monkeys to identify an oculomotor area whose existence had been postulated rostral to the supplementary motor area. Contraversive saccades were evoked from 129 sites by stimulation. Threshold currents were lower than 20 microA in half the tests. Response latencies were usually longer than 50 ms (minimum: 30 ms). Eye movements were occasionally accompanied by blinks, ear, or neck movements. The cortical area yielding these movements was at the superior edge of the frontal lobe just rostral to the region from which limb movements could be elicited. Depending on the site of stimulation, saccades varied between two extremes: from having rather uniform direction and size, to converging toward a goal defined in space. The transition between these extremes was gradual with no evidence that these two types were fundamentally different. From surface to depth of cortex, direction and amplitude of evoked saccades were similar or changed progressively. No clear systematization was found depending on location along rostrocaudal or mediolateral axes of the cortex. The dorsomedial oculomotor area mapped was approximately 7 mm long and 6 mm wide. Combined eye and head movements were elicited from one of ten sites stimulated when the head was unrestrained. In the other nine cases, saccades were not accompanied by head rotation, even when higher currents or longer stimulus trains were applied. Presaccadic unit activity was recorded from 62 cells. Each of these cells had a preferred direction that corresponded to the direction of the movement evoked by local microstimulation. Presaccadic activity occurred with self-initiated as well as visually triggered saccades. It often led self-initiated saccades by more than 300 ms. Recordings made with the head free showed that the firing could not be interpreted as due to attempted head movements. Many dorsomedial cortical neurons responded to photic stimuli, either phasically or tonically. Sustained responses (activation or inhibition) were observed during target fixation. Twenty-one presaccadic units showed tonic changes of activity with fixation. Justification is given for considering the cortical area studied as a supplementary eye field. It shares many common properties with the arcuate frontal eye field. Differences noted in this study include: longer latency of response to electrical stimulation, possibility to evoke saccades converging apparently toward a goal, and long-lead unit activity with spontaneous saccades.


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

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


1995 ◽  
Vol 73 (3) ◽  
pp. 1122-1134 ◽  
Author(s):  
L. L. Chen ◽  
S. P. Wise

1. The companion paper reported that a substantial proportion of cells in the supplementary eye field (SEF) of macaque monkeys show significant evolution of neuronal activity as subjects learn new and arbitrary stimulus-saccade associations. The purpose of the present study was to compare and contrast the activity of the SEF and the frontal eye field (FEF) during such conditional oculomotor learning. 2. In both SEF and FEF, we observed learning-dependent and learning-selective activity, defined as significant evolution of task-related activity as monkeys learned which of four saccades was instructed by a novel stimulus. By definition, in addition to changes as the monkeys learned the instructional significance of a novel instruction stimulus, learning-dependent activity also showed task-related modulation for trials instructed by familiar stimuli, whereas learning-selective activity did not. Of the 186 SEF neurons adequately tested, 81 (44%) showed one of these two categories of learning-related change. By contrast, of the 90 FEF neurons adequately tested, only 14 (16%) showed similar properties. This difference was highly statistically significant (chi 2 = 21.1; P < 0.001). 3. We also observed persistent differences in activity for trials with familiar versus novel instruction stimuli, which we termed learning-static effects. In some cases, the learning-static effect coexisted with learning-dependent or learning-selective changes in activity, although in others it did not. In the former cases, activity changed systematically during learning, but reached a level that differed from that for familiar stimuli instructing the same saccade. In the latter cases, the activity did not change significantly as the monkey learned new conditional oculomotor associations, but did show a significant difference depending upon whether a novel or familiar stimulus instructed a given saccade. Overall, 66 of 186 (35%) cells in the SEF and 17 of 90 (19%) cells in the FEF showed learning-static effects in one or more task periods. This difference was statistically significant (chi 2 = 7.9; P < 0.005). 4. The significant difference in the properties of SEF and FEF cells suggests a functional dissociation of the two areas during conditional oculomotor learning. In this respect, the FEF resembles the primary motor cortex, whereas the SEF resembles the premotor cortex.


2014 ◽  
Vol 111 (12) ◽  
pp. 2644-2655 ◽  
Author(s):  
Shun-nan Yang ◽  
Stephen Heinen

Single-unit recording in monkeys and functional imaging of the human frontal lobe indicate that the supplementary eye field (SEF) and the frontal eye field (FEF) are involved in ocular decision making. To test whether these structures have distinct roles in decision making, single-neuron activity was recorded from each structure while monkeys executed an ocular go/nogo task. The task rule is to pursue a moving target if it intersects a visible square or “go zone.” We found that most SEF neurons showed differential go/nogo activity during the delay period, before the target intersected the go zone (delay period), whereas most FEF neurons did so after target intersection, during the period in which the movement was executed (movement period). Choice probability (CP) for SEF neurons was high in the delay period but decreased in the movement period, whereas for FEF neurons it was low in the delay period and increased in the movement period. Directional selectivity of SEF neurons was low throughout the trial, whereas that of FEF neurons was highest in the delay period, decreasing later in the trial. Increasing task difficulty led to later discrimination between go and nogo in both structures and lower CP in the SEF, but it did not affect CP in the FEF. The results suggest that the SEF interprets the task rule early but is less involved in executing the motor decision than is the FEF and that these two areas collaborate dynamically to execute ocular decisions.


2010 ◽  
Vol 104 (3) ◽  
pp. 1239-1248 ◽  
Author(s):  
Stan Van Pelt ◽  
Ivan Toni ◽  
Jörn Diedrichsen ◽  
W. Pieter Medendorp

The path from perception to action involves the transfer of information across various reference frames. Here we applied a functional magnetic resonance imaging (fMRI) repetition suppression paradigm to determine the reference frame(s) in which the cortical activity is coded at several phases of the sensorimotor transformation for a saccade, including sensory processing, saccade planning, and saccade execution. We distinguished between retinal (eye-centered) and nonretinal (e.g., head-centered) coding frames in three key regions: the intraparietal sulcus (IPS), frontal eye field (FEF), and supplementary eye field (SEF). Subjects ( n = 18) made delayed saccades to one of five possible peripheral targets, separated at intervals of 9° visual angle. Target locations were chosen pseudorandomly, based on a 2 × 2 factorial design, with factors retinal and nonretinal coordinates and levels novel and repeated. In all three regions, analysis of the blood oxygenation level dependent dynamics revealed an attenuation of the fMRI signal in trials repeating the location of the target in retinal coordinates. The amount of retinal suppression varied across the three phases of the trial, with the strongest suppression during saccade planning. The paradigm revealed only weak traces of nonretinal coding in these regions. Further analyses showed an orderly representation of the retinal target location, as expressed by a contralateral bias of activation, in the IPS and FEF, but not in the SEF. These results provide evidence that the sensorimotor processing in these centers reflects saccade generation in eye-centered coordinates, irrespective of their topographic organization.


1996 ◽  
Vol 76 (4) ◽  
pp. 2754-2771 ◽  
Author(s):  
J. R. Tian ◽  
J. C. Lynch

1. The locations and connections of the smooth and saccadic eye movement subregions of the frontal eye field (FEFsem and FEFsac, respectively) were investigated in seven hemispheres of five Cebus monkeys. The supplementary eye field was also mapped in seven hemispheres and the hand/arm regions of the dorsal and ventral premotor areas were localized in five hemispheres. Monkeys were immobilized during experiments with Telazol, a dissociative anesthetic agent that has no significant effect on microstimulation-induced eye movement parameters (threshold, velocity, and duration). The functional subregions were defined with the use of low threshold intracortical microstimulation (current < or = 50 microA). Then different retrogradely transported fluorescent tracers were placed into these functionally defined regions. 2. The FEFsac in Cebus monkey is in the same location as the one in macaque monkeys, which is in Walker's areas 8a and 45. The FEFsem is located in the posterior shoulder of the superior arcuate sulcus near its medial tip and is therefore more accessible for tracer injections than the one in macaque monkeys. This subregion is within cytoarchitectural area 6a beta, which is distinct from the adjacent area 6a alpha (dorsal premotor area). This smooth eye movement subregion may be comparable with the one in macaque monkeys. 3. Cortical connection patterns of the FEFsac and FEFsem are similar and parallel to each other. The predominant neural input to these two subregions originates in other cortical eye fields, including the supplementary eye field, the parietal eye field, the middle superior temporal area, and the principal sulcus region. These cortical eye fields each contain two separate, almost non-overlapping, distributions of labeled neurons that project to the corresponding frontal eye field (FEF) subregions. These results suggest that there may be similar, but relatively independent, parallel corticocortical networks to control pursuit and saccadic eye movements. The weak connections between the middle temporal area (MT) and FEF suggest that the MT may not provide the major source of visuomotion inputs to the FEF, but that it rather plays a role in mediating visual information that is relayed from the striate and extrastriate cortices via MT to the parietal cortex and then to the FEF. In addition to the well-known neural connections between the lateral intraparietal area and the FEF, additional parietal projections have been demonstrated from the dorsomedial visual area area specifically to the FEFsac and from area 7m specifically to the FEFsem.


2000 ◽  
Vol 83 (3) ◽  
pp. 1764-1769 ◽  
Author(s):  
Naotaka Fujii ◽  
Hajime Mushiake ◽  
Jun Tanji

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.


Author(s):  
R. John Leigh ◽  
David S. Zee

This chapter reviews the behavioral properties of rapid eye movements, ranging from quick phases of nystagmus to cognitively controlled saccades, and their neural substrate. Properties of various types of saccades are described, including express saccades, memory-guided saccades, antisaccades, and saccades during visual search and reading. Current concepts of regions important for the generation of saccades are reviewed, integrating results of functional imaging and electrophysiology, including brainstem burst neurons and omnipause neurons, the superior colliculus, frontal eye field, supplementary eye field, dorsolateral prefrontal cortex, cingulate cortex, posterior parietal cortex, parietal eye field, thalamus, pulvinar, caudate, substantia nigra pars reticulata, subthalamic nucleus, cerebellar dorsal vermis, and fastigial nucleus. Saccade adaptation to novel visual demands is discussed, and the interaction between saccades and eyelid movements (blinks). Mathematical models of saccades are discussed. Clinical and laboratory evaluation of saccades and the pathophysiology of saccadic disorders, from slow saccades to opsoclonus, are reviewed.


2007 ◽  
Vol 98 (3) ◽  
pp. 1751-1762 ◽  
Author(s):  
Matthew R. G. Brown ◽  
Tutis Vilis ◽  
Stefan Everling

Several current models hold that frontoparietal areas exert cognitive control by biasing task-relevant processing in other brain areas. Previous event-related functional magnetic resonance imaging (fMRI) studies have compared prosaccades and antisaccades, which require subjects to look toward or away from a flashed peripheral stimulus, respectively. These studies found greater activation for antisaccades in frontal and parietal regions at the ends of long (≥6 s) preparatory periods preceding peripheral stimulus presentation. Event-related fMRI studies using short preparatory periods (≤4 s) have not found such activation differences except in the frontal eye field. Here, we identified activation differences associated with short (1-s) preparatory periods by interleaving half trials among regular whole trials in a rapid fMRI design. On whole trials, a colored fixation dot instructed human subjects to make either a prosaccade toward or an antisaccade away from a peripheral visual stimulus. Half trials included only the instruction and not peripheral stimulus presentation or saccade generation. Nonetheless, half trials evoked stronger activation on antisaccades than on prosaccades in the frontal eye field (FEF), supplementary eye field (SEF), left dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex (ACC), intraparietal sulcus (IPS), and precuneus. Greater antisaccade response-related activation was found in FEF, SEF, IPS, and precuneus but not in DLPFC or ACC. These results demonstrate greater preparatory activation for antisaccades versus prosaccades in frontoparietal areas and suggest that prefrontal cortex and anterior cingulate cortex are more involved in presetting the saccade network for the antisaccade task than generating the actual antisaccade response.


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