Supplementary Eye Field: Keeping an Eye on Eye Movement

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.

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Macaque SEF Neurons Encode Object-Centered Directions of Eye Movements Regardless of the Visual Attributes of Instructional Cues

Journal of Neurophysiology ◽

10.1152/jn.1999.81.5.2340 ◽

1999 ◽

Vol 81 (5) ◽

pp. 2340-2346 ◽

Cited By ~ 43

Author(s):

Carl R. Olson ◽

Sonya N. Gettner

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Macaque Monkey ◽

Direction Selectivity ◽

Visual Attributes ◽

Supplementary Eye Field ◽

Eye Field ◽

The Right

Macaque SEF neurons encode object-centered directions of eye movements regardless of the visual attributes of instructional cues. Neurons in the supplementary eye field (SEF) of the macaque monkey exhibit object-centered direction selectivity in the context of a task in which a spot flashed on the right or left end of a sample bar instructs a monkey to make an eye movement to the right or left end of a target bar. To determine whether SEF neurons are selective for the location of the cue, as defined relative to the sample bar, or, alternatively, for the location of the target, as defined relative to the target bar, we carried out recording while monkeys performed a new task. In this task, the color of a cue-spot instructed the monkey to which end of the target bar an eye movement should be made (blue for the left end and yellow for the right end). Object-centered direction selectivity persisted under this condition, indicating that neurons are selective for the location of the target relative to the target bar. However, object-centered signals developed at a longer latency (by ∼200 ms) when the instruction was conveyed by color than when it was conveyed by the location of a spot on a sample bar.

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Trajectory Interpretation by Supplementary Eye Field Neurons During Ocular Baseball

Journal of Neurophysiology ◽

10.1152/jn.00109.2005 ◽

2005 ◽

Vol 94 (2) ◽

pp. 1385-1391 ◽

Cited By ~ 16

Author(s):

Yong-Guk Kim ◽

Jeremy B. Badler ◽

Stephen J. Heinen

Keyword(s):

Eye Movement ◽

Neuronal Activity ◽

Target Motion ◽

Moving Object ◽

Movement Initiation ◽

Sensory Signals ◽

Task Rule ◽

Supplementary Eye Field ◽

Eye Field

Good performance in the sport of baseball shows that humans can determine the trajectory of a moving object and act on it under the constraint of a rule. We report here on neuronal activity in the supplementary eye field (SEF) of monkeys performing an eye movement task inspired by baseball. In “ocular baseball,” a pursuit eye movement to a target is executed or withheld based on the target’s trajectory. We found that a subset of neurons in the SEF interpreted the trajectory according to the task rule. Other neurons specified at a later time the command to pursue the target with the eyes. The results suggest that the SEF can interpret sensory signals about target motion in the context of a rule to guide voluntary eye movement initiation.

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Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys

Journal of Neurophysiology ◽

10.1152/jn.1996.76.4.2754 ◽

1996 ◽

Vol 76 (4) ◽

pp. 2754-2771 ◽

Cited By ~ 90

Author(s):

J. R. Tian ◽

J. C. Lynch

Keyword(s):

Eye Movement ◽

Frontal Eye Field ◽

Adjacent Area ◽

Saccadic Eye Movement ◽

Temporal Area ◽

Macaque Monkeys ◽

Supplementary Eye Field ◽

Eye Field ◽

Cebus Monkeys ◽

The One

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.

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Impact of Experience on the Representation of Object-Centered Space in the Macaque Supplementary Eye Field

Journal of Neurophysiology ◽

10.1152/jn.00848.2006 ◽

2007 ◽

Vol 97 (3) ◽

pp. 2159-2173 ◽

Cited By ~ 5

Author(s):

David E. Moorman ◽

Carl R. Olson

Keyword(s):

Eye Movement ◽

Spatial Selectivity ◽

Match To Sample ◽

Supplementary Eye Field ◽

Neural Representations ◽

Primate Brain ◽

Before And After ◽

Eye Field ◽

Stage 1 ◽

Use Of An Object

Many neurons in the macaque supplementary eye field (SEF) exhibit object-centered spatial selectivity, firing at different rates when the monkey plans a saccade to the left or right end of a horizontal bar. Is this property natural to the SEF or is it a product of specialized training in the laboratory? To answer this question, we monitored the activity of single SEF neurons in two monkeys before and after training to select eye-movement targets by an object-centered rule. During stage 1, the monkeys performed a color delayed-match-to-sample (DMS) task in which a red or green central cue dictated an eye movement to the matching end of a horizontal bar. Many neurons at this stage exhibited object-centered spatial selectivity. During stage 2, the monkeys performed a color-conditional object-centered task in which a green or red central cue instructed an eye movement to the left or right end of a gray bar. More neurons exhibited object-centered spatial selectivity during this stage than during stage 1. During stage 3, the monkeys again performed the color DMS task. The fraction of neurons exhibiting object-centered spatial selectivity remained at a level comparable to that observed during stage 2 and above that observed during stage 1. Thus object-centered spatial selectivity was present before training on an object-centered rule, was enhanced as a product of object-centered training, and outlasted active use of an object-centered rule. We conclude that neural representations of object-centered space, naturally present in the primate brain, can be sharpened by training.

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Primate Antisaccade. II. Supplementary Eye Field Neuronal Activity Predicts Correct Performance

Journal of Neurophysiology ◽

10.1152/jn.00138.2003 ◽

2004 ◽

Vol 91 (4) ◽

pp. 1672-1689 ◽

Cited By ~ 80

Author(s):

Nelly Amador ◽

Madeleine Schlag-Rey ◽

John Schlag

Keyword(s):

Eye Movement ◽

Single Neuron ◽

Peripheral Stimulus ◽

Visual Responses ◽

Supplementary Eye Field ◽

Individual Trial ◽

Eye Field ◽

Saccade Task ◽

Anti Saccades ◽

Initial Instruction

Neuronal activities were recorded in the supplementary eye field (SEF) of 3 macaque monkeys trained to perform antisaccades pseudorandomly interleaved with prosaccades, as instructed by the shape of a central fixation point. The prosaccade goal was indicated by a peripheral stimulus flashed anywhere on the screen, whereas the antisaccade goal was an unmarked site diametrically opposite the flashed stimulus. The visual cue was given immediately after the instruction cue disappeared in the immediate-saccade task, or during the instruction period in the delayed-saccade task. The instruction cue offset was the saccade gosignal. Here we focus on 92 task-related neurons: visual, eye-movement, and instruction/fixation neurons. We found that 73% of SEF eye-movement–related neurons fired significantly more before anti-saccades than prosaccades. This finding was analyzed at 3 levels: population, single neuron, and individual trial. On individual antisaccade trials, 40 ms before saccade, the firing rate of eye-movement–related neurons was highly predictive of successful performance. A similar analysis of visual responses (40 ms astride the peak) gave less-coherent results. Fixation neurons, activated during the initial instruction period (i.e., after the instruction cue but before the stimulus) always fired more on antisaccade than on prosaccade trials. This trend, however, was statistically significant for only half of these neurons. We conclude that the SEF is critically involved in the production of antisaccades.

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Learning-selective and learning-dependent neuronal activity in the supplementary eye field of rhesus monkeys

Neuroscience Research Supplements ◽

10.1016/0921-8696(94)92958-0 ◽

1994 ◽

Vol 19 ◽

pp. S244

Author(s):

Longtang L. Chen ◽

Steven P. Wise

Keyword(s):

Neuronal Activity ◽

Rhesus Monkeys ◽

Supplementary Eye Field ◽

Eye Field

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Evidence for a supplementary eye field

Journal of Neurophysiology ◽

10.1152/jn.1987.57.1.179 ◽

1987 ◽

Vol 57 (1) ◽

pp. 179-200 ◽

Cited By ~ 369

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.

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