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

2007 ◽  
Vol 97 (3) ◽  
pp. 2159-2173 ◽  
Author(s):  
David E. Moorman ◽  
Carl R. Olson

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.

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.


2007 ◽  
Vol 97 (5) ◽  
pp. 3554-3566 ◽  
Author(s):  
David E. Moorman ◽  
Carl R. Olson

Neurons in the macaque supplementary eye field (SEF) fire at different rates in conjunction with planning saccades in different directions. They also exhibit object-centered spatial selectivity, firing at different rates when the target of the saccade is at the left or right end of a horizontal bar. To compare the rate of incidence of the two kinds of signal, and to determine how they combine, we recorded from SEF neurons while monkeys performed a task in which the target (a dot or the left or right end of a horizontal bar) could appear in any visual field quadrant. During the period when the target was visible on the screen and the monkey was preparing to make a saccade, many neurons exhibited selectivity for saccade direction, firing at a rate determined by the direction of the impending saccade irrespective of whether the target was a dot or the end of a bar. On bar trials, many of the same neurons exhibited object-centered selectivity, firing more strongly when the target was at the preferred end of the bar regardless of saccade direction. The rate of incidence of object-centered selectivity (33%) was lower overall than that of saccade-direction selectivity (56%). Signals related to saccade direction and the object-centered location of the target tended to combine additively. The results suggest that the SEF is at a transitional stage between representing the object-centered command and specifying the parameters of the saccade.


2004 ◽  
Vol 14 (11) ◽  
pp. R416-R418 ◽  
Author(s):  
R.H.S. Carpenter

1999 ◽  
Vol 81 (5) ◽  
pp. 2340-2346 ◽  
Author(s):  
Carl R. Olson ◽  
Sonya N. Gettner

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.


2005 ◽  
Vol 94 (2) ◽  
pp. 1385-1391 ◽  
Author(s):  
Yong-Guk Kim ◽  
Jeremy B. Badler ◽  
Stephen J. Heinen

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.


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.


1992 ◽  
Vol 68 (5) ◽  
pp. 1913-1916 ◽  
Author(s):  
J. C. Lynch

1. Monkeys were trained to perform horizontal visually guided saccades. Latency was measured before and after bilateral lesions of the frontal eye field (FEF) and after combined lesions of both the FEF and the posterior eye field. Destruction of either of these regions alone causes only modest deficits of eye movement, but destruction of both together produces profound oculomotor impairment. The results support the proposal that purposeful eye movements are controlled by a distributed corticocortical network that includes nodes in frontal and parieto-occipital regions.


1997 ◽  
Vol 78 (2) ◽  
pp. 1166-1169 ◽  
Author(s):  
Longtang L. Chen ◽  
Steven P. Wise

Chen, Longtang L. and Steven P. Wise. Conditional oculomotor learning: population vectors in the supplementary eye field. J. Neurophysiol. 78: 1160–1163, 1997. We have shown previously that the activity levels and preferred directions of supplementary eye field neurons change as monkeys learn to associate nonspatial visual information with a saccade (or the spatial target of that saccade). The present report describes changes in neuronal population vectors (PV) during such learning. PVs based on neuronal activity shortly before and after saccades predicted movement direction poorly in the earliest stage of learning, but as monkeys mastered novel stimulus-response mappings, PV accuracy and magnitude increased significantly.


2004 ◽  
Vol 91 (4) ◽  
pp. 1672-1689 ◽  
Author(s):  
Nelly Amador ◽  
Madeleine Schlag-Rey ◽  
John Schlag

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.


2011 ◽  
Vol 106 (6) ◽  
pp. 2992-3000 ◽  
Author(s):  
S. J. Heinen ◽  
H. Hwang ◽  
S. N. Yang

Since the environment is in constant flux, decision-making capabilities of the brain must be rapid and flexible. Yet in sensory motion processing pathways of the primate brain where decision making has been extensively studied, the flexibility of neurons is limited by inherent selectivity to motion direction and speed. The supplementary eye field (SEF), an area involved in decision making on moving stimuli, is not strictly a sensory or motor structure, and hence may not suffer such limitations. Here we test whether neurons in the SEF can flexibly interpret the rule of a go/nogo task when the decision boundary in the task changes with each trial. The task rule specified that the animal pursue a moving target with its eyes if and when the target entered a visible zone. The size of the zone was changed from trial to trial in order to shift the decision boundary, and thereby assign different go/nogo significance to the same motion trajectories. Individual SEF neurons interpreted the rule appropriately, signaling go or nogo in compliance with the rule and not the direction of motion. The results provide the first evidence that individual neurons in frontal cortex can flexibly interpret a rule that governs the decision to act.


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