Executive control of countermanding saccades by the supplementary eye field (original) (raw)
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Stevenson SA, Elsley JK, Corneil BD. A "Gap effect" on stop signal reaction times in a human saccadic countermanding task. . The "gap effect" describes a phenomenon whereby saccadic reaction times are expedited by the removal of a visible fixation point prior to target presentation. Here we investigated whether processes controlling saccade cancellation are also subjected to a gap effect. Human subjects performed a countermanding experiment that required them to try to cancel an impending saccade in the presence of an imperative visual stop signal, across different fixation conditions. We found that saccadic cancellation latencies, estimated via derivation of the stop signal reaction time (SSRT), were ϳ40 ms shorter on trials with a 200-ms gap between fixation point removal and target presentation compared with when the fixation point remained illuminated. Follow-up experiments confirmed that the reduction in SSRTs were primarily due to removal of a foveal fixation point (as opposed to a generalized warning effect) and persisted with an auditory stop signal that controlled for potential differences in stop signal saliency across different fixation conditions. Saccadic RTs exhibited a gap effect in all experiments with reductions in RTs being due to both removal of a foveal fixation point and a generalized warning effect. Overall, our results demonstrate that processes controlling saccade cancellation can be expedited by a 200-ms gap. The simultaneous priming of both saccade cancellation and generation is of particular interest considering the mutually antagonistic relationship between the saccade fixation and generation networks in the oculomotor system.
Role of Supplementary Eye Field in Saccade Initiation: Executive, Not Direct, Control
Journal of Neurophysiology, 2010
Isoda, Masaki and Jun Tanji. Cellular activity in the supplementary eye field during sequential performance of multiple saccades. J Neurophysiol 88: 3541-3545, 2002; 10.1152/jn.00299.2002. To investigate how single neurons in the supplementary eye field (SEF) participate in sequential performance of multiple saccades, we analyzed presaccadic activity while monkeys were performing three saccades in six different orders from memory. The saccades in each sequence were separated by a fixation period and initiated from the same fixation point with intervening return saccades. We found that the majority of the presaccadic activity of the SEF neurons differed significantly depending on the numerical position of saccades in each sequence (rank order). This rank-order selectivity was found in parallel with the selectivity for the sequence of three saccades. Our data suggest a role for SEF neurons in the coding of temporally ordered saccadic eye movements.
In the previous studies on the neural control of saccade initiation using the countermanding paradigm, movement and visuomovement neurons in the frontal eye field were grouped as movement-related neurons. The activity of both types of neurons was modulated when a saccade was inhibited in response to a stop signal, and this modulation occurred early enough to contribute to the control of the saccade initiation. We now report a functional difference between these two classes of neurons when saccades are produced. Movement neurons exhibited a progressive accumulation of discharge rate following target presentation that triggered a saccade when it reached a threshold. When saccades were inhibited with lower probability in response to a stop signal appearing at longer delays, this accumulating activity was interrupted at levels progressively closer to the threshold. In contrast, visuomovement neurons exhibited a maintained elevated discharge rate following target presentation that was followed by a further enhancement immediately before saccade initiation. When saccades were inhibited in response to a stop signal, the late enhancement was absent and the maintained activity decayed regardless of stop signal delay. These results demonstrate that the activity of movement neurons realizes the progressive commitment to saccade initiation modeled by the activation of the GO unit in computational models of countermanding performance. The lack of correspondence of the activity of visuomovement neurons with any elements of these models indicates that visuomovement neurons perform a function other than saccade preparation such as a corollary discharge to update visual processing.
Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field
Journal of neurophysiology, 1997
Patients with frontal lobe damage have difficulty suppressing reflexive saccades to salient visual stimuli, indicating that frontal lobe neocortex helps to suppress saccades as well as to produce them. In the present study, a role for the frontal eye field (FEF) in suppressing saccades was demonstrated in macaque monkeys by application of intracortical microstimulation during the performance of a visually guided saccade task, a memory prosaccade task, and a memory antisaccade task. A train of low-intensity (20-50 microA) electrical pulses was applied simultaneously with the disappearance of a central fixation target, which was always the cue to initiate a saccade. Trials with and without stimulation were compared, and significantly longer saccade latencies on stimulation trials were considered evidence of suppression. Low-intensity stimulation suppressed task-related saccades at 30 of 77 sites tested. In many cases saccades were suppressed throughout the microstimulation period (usu...
Relation of frontal eye field activity to saccade initiation during a countermanding task
Experimental Brain Research, 2008
The countermanding (or stop signal) task probes the control of the initiation of a movement by measuring subjects' ability to withhold a movement in various degrees of preparation in response to an infrequent stop signal. Previous research found that saccades are initiated when the activity of movement-related neurons reaches a threshold, and saccades are withheld if the growth of activity is interrupted. To extend and evaluate this relationship of frontal eye field (FEF) activity to saccade initiation, two new analyses were performed. First, we fit a neurometric function that describes the proportion of trials with a stop signal in which neural activity exceeded a criterion discharge rate as a function of stop signal delay, to the inhibition function that describes the probability of producing a saccade as a function of stop signal delay. The activity of movement-related but not visual neurons provided the best correspondence between neurometric and inhibition functions. Second, we determined the criterion discharge rate that optimally discriminated between the distributions of discharge rates measured on trials when saccades were produced or withheld. Differential activity of movement-related but not visual neurons could distinguish whether a saccade occurred. The threshold discharge rates determined for individual neurons through these two methods agreed. To investigate how reliably movement-related activity predicted movement initiation; the analyses were carried out with samples of activity from increasing numbers of trials from the same or from different neurons. The reliability of both measures of initiation threshold improved with number of trials and neurons to an asymptote of between 10 to 20 movement-related neurons. Combining the activity of visual neurons did not improve the reliability of predicting saccade initiation. These results demonstrate how the activity of a population of movement-related but not visual neurons in the FEF contributes to the control of saccade initiation. The results also validate these analytical procedures for identifying signals that control saccade initiation in other brain structures.
Executive control of gaze by the frontal lobes
Cognitive, Affective, & Behavioral Neuroscience, 2007
Current hypotheses about the mechanisms of executive control have been developed largely in the domain of human subjects performing tasks involving response interference (such as Stroop or flanker tasks) or reinforcement learning. Distinguishing between alternative hypotheses about executive control has hinged on articulating the relationship (or lack thereof) between monitoring errors, reinforcement feedback, and response conflict. We will review research on the neurophysiological mechanisms observed in macaque monkeys performing a countermanding (stop signal) task with saccadic eye movements. Key insights include elucidation of how the brain controls whether and when a movement will be initiated, demonstration of the coexistence of error, reinforcement, and conflict signals in the medial frontal lobe, and demonstration of a mechanism by which the medial frontal lobe can influence motor structures to adapt performance. These insights grew out of a synthesis of conceptual frameworks and a coordination of neurophysiological, psychophysical, and mathematical modeling techniques.
2008
The frontal eye field (FEF) is involved in the transformation of visual signals into saccadic eye movements. Although it is often considered an oculomotor structure, several lines of evidence suggest that the FEF also contributes to visual perception and attention. To better understand the range of behaviors to which the FEF can contribute, we tested whether monkeys could detect activation of their FEF by electrical microstimulation with currents below those that cause eye movements. We found that stimulation of FEF neurons could almost always be detected at levels below those needed to generate saccades and that the electrical current needed for detection was highly correlated with that needed to generate a saccade. This relationship between detection and saccade thresholds can be explained if FEF neurons represent preparation to make particular saccades and subjects can be aware of such preparations without acting on them when the representation is not strong.
Effects of electrical microstimulation in monkey frontal eye field on saccades to remembered targets
Vision research, 2005
Spatially selective delay activity in the frontal eye field (FEF) is hypothesized to be part of a mechanism for the transformation of visual signals into instructions for voluntary movements. To understand the linkage between FEF activity and eye movement planning, we recorded neuronal responses of FEF neurons while monkeys performed a memory-saccade task. We then electrically stimulated the same sites
Journal of neurophysiology, 2000
The aim of this study was to determine whether neuronal activity in the macaque supplementary eye field (SEF) is influenced by the rule used for saccadic target selection. Two monkeys were trained to perform a variant of the memory-guided saccade task in which any of four visible dots (rightward, upward, leftward, and downward) could be the target. On each trial, the cue identifying the target was either a spot flashed in superimposition on the target (spatial condition) or a foveally presented digitized image associated with the target (pattern condition). Trials conforming to the two conditions were interleaved randomly. On recording from 439 SEF neurons, we found that two aspects of neuronal activity were influenced by the nature of the cue. 1) Activity reflecting the direction of the impending response developed more rapidly following spatial than following pattern cues. 2) Activity throughout the delay period tended to be higher following pattern than following spatial cues. We...