Repetition Suppression Dissociates Spatial Frames of Reference in Human Saccade Generation

2010 ◽  
Vol 104 (3) ◽  
pp. 1239-1248 ◽  
Author(s):  
Stan Van Pelt ◽  
Ivan Toni ◽  
Jörn Diedrichsen ◽  
W. Pieter Medendorp
Keyword(s):  
Reference Frames ◽  
Target Location ◽  
Blood Oxygenation ◽  
Frontal Eye Field ◽  
Supplementary Eye Field ◽  
Repetition Suppression ◽  
Spatial Frames Of Reference ◽  
Oxygenation Level ◽  
Eye Field ◽  
Saccade Generation

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.

Intracerebral dynamics of saccade generation in the human frontal eye field and supplementary eye field

NeuroImage ◽  
2006 ◽  
Vol 30 (4) ◽  
pp. 1302-1312 ◽  
Author(s):  
Jean-Philippe Lachaux ◽  
Dominique Hoffmann ◽  
Lorella Minotti ◽  
Alain Berthoz ◽  
Philippe Kahane
Keyword(s):  
Frontal Eye Field ◽  
Supplementary Eye Field ◽  
Eye Field ◽  
Saccade Generation

Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields

1996 ◽  
Vol 75 (5) ◽  
pp. 2187-2191 ◽  
Author(s):  
H. Mushiake ◽  
N. Fujii ◽  
J. Tanji
Keyword(s):  
Eye Movement ◽  
Neuronal Activity ◽  
Motor Task ◽  
Oculomotor Control ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Saccadic Eye Movement ◽  
Visually Guided ◽  
Supplementary Eye Field ◽  
Eye Field

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.

Evidence for a supplementary eye field

1987 ◽  
Vol 57 (1) ◽  
pp. 179-200 ◽  
Author(s):  
J. Schlag ◽  
M. Schlag-Rey
Keyword(s):  
Unit Activity ◽  
Cortical Neurons ◽  
Cortical Area ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Unit Recording ◽  
Electrical Microstimulation ◽  
Preferred Direction ◽  
Supplementary Eye Field ◽  
Eye Field

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.

Higher level influences on saccade generation in normals and patients with visual hemineglect

1999 ◽  
Vol 22 (4) ◽  
pp. 688-689
Author(s):  
Wolfgang Heide ◽  
Andreas Sprenger ◽  
Detlef Kömpf
Keyword(s):  
Human Subjects ◽  
Perceptual Processing ◽  
Visual Exploration ◽  
Frontal Eye Field ◽  
Automatic Processes ◽  
Eye Field ◽  
Level 3 ◽  
Normal Human ◽  
Reflexive Saccades ◽  
Saccade Generation

In this commentary we describe findings in normal human subjects and in patients with visual hemineglect that support the importance of higher-level influences on saccade generation during visual exploration. As the duration of fixations increases with increases in the cognitive demand of the task, the timing of exploratory saccades is controlled more by centers of cognitive and perceptual processing at levels 4 and 5 than by reflex-like automatic processes at level 3. In line with this, unilateral frontal eye field lesions impair systematic, intentional saccadic exploration of visual scenes, causing prolonged fixations and contralesional hemineglect, but leave visually triggered reflexive saccades largely intact.

Frontal eye field: A cortical salience map

1999 ◽  
Vol 22 (4) ◽  
pp. 699-700 ◽  
Author(s):  
Kirk G. Thompson ◽  
Narcisse P. Bichot
Keyword(s):  
Visual Attention ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Eye Field ◽  
Salience Map ◽  
Saccade Generation

The concept of a salience map has become important for the development of theories of visual attention and saccade generation. Recent studies have shown that the frontal eye fields have all of the characteristics of a salience map.

scholarly journals Role of Supplementary Eye Field in Saccade Initiation: Executive, Not Direct, Control

2010 ◽  
Vol 103 (2) ◽  
pp. 801-816 ◽  
Author(s):  
Veit Stuphorn ◽  
Joshua W. Brown ◽  
Jeffrey D. Schall
Keyword(s):  
Discharge Rate ◽  
Stop Signal ◽  
Stop Signal Task ◽  
Frontal Eye Field ◽  
Signal Trial ◽  
Visually Guided ◽  
Supplementary Eye Field ◽  
Task Requirements ◽  
Gaze Holding ◽  
Eye Field

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.

scholarly journals Neural Control of Visual Search by Frontal Eye Field: Effects of Unexpected Target Displacement on Visual Selection and Saccade Preparation

2009 ◽  
Vol 101 (5) ◽  
pp. 2485-2506 ◽  
Author(s):  
Aditya Murthy ◽  
Supriya Ray ◽  
Stephanie M. Shorter ◽  
Jeffrey D. Schall ◽  
Kirk G. Thompson
Keyword(s):  
Visual Search ◽  
Reaction Time ◽  
Receptive Field ◽  
Target Location ◽  
Visual Selection ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Visual Neurons ◽  
Eye Field ◽  
Saccade Preparation

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.

Supplementary eye field contrasted with the frontal eye field during acquisition of conditional oculomotor associations

1995 ◽  
Vol 73 (3) ◽  
pp. 1122-1134 ◽  
Author(s):  
L. L. Chen ◽  
S. P. Wise
Keyword(s):  
Primary Motor Cortex ◽  
Premotor Cortex ◽  
Familiar Stimulus ◽  
Frontal Eye Field ◽  
Supplementary Eye Field ◽  
Significant Difference ◽  
Eye Field ◽  
Familiar Stimuli ◽  
Oculomotor Learning ◽  
Selective Activity

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.

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