The relationship of monkey frontal eye field activity to saccade dynamics

1993 ◽  
Vol 69 (6) ◽  
pp. 1880-1889 ◽  
Author(s):  
M. A. Segraves ◽  
K. Park

1. In this study, we compared the temporal waveforms of the activity of monkey frontal eye field movement neurons with the dynamics of saccadic eye movements. 2. Movement neurons in the frontal eye field were selected according to previously published criteria. They had little or no response to visual stimuli in a fixation task, and equivalent activity before visually guided and memory-guided saccades. We studied corticotectal neurons and corticopontine neurons identified by antidromic excitation, as well as neurons whose projections were not identified. 3. These neurons had a peak activation at a mean of 13 ms before the saccade began. However, rather than falling off rapidly as the saccade ended, most neurons continued to fire after the saccade, returning to baseline at a mean of 93 ms after the end of the saccade. 4. We measured the decrement in activity for these neurons during the saccade. Although a few neurons showed decrements of > 60% of their peak activity level, the average activity dropped only 16.9%, with some neurons actually showing a rise in activity during the saccade. If we ignored the latency between peak in activity and saccade start and measured the fall in activity for a period equal to one saccade duration after the peak, the average drop in activity was still only 34.9%. Thus the activity of these neurons did not appear to be closely related to dynamic motor error, which falls from its maximum value to zero over the time course of a saccade. 5. These results suggest that a focus of movement activity within the topographic map in the frontal eye field specifies the amplitude and direction for an impending saccade, whereas the peak of movement activity signals the time to initiate a saccade. 6. Unlike the superior colliculus, the activity of frontal eye field movement neurons does not appear to be related to dynamic events that occur during the saccade, such as motor error.

1997 ◽  
Vol 77 (5) ◽  
pp. 2252-2267 ◽  
Author(s):  
Douglas D. Burman ◽  
Charles J. Bruce

Burman, Douglas D. and Charles J. Bruce. Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J. Neurophysiol. 77: 2252–2267, 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 μA) 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 (usually 450 ms) and then executed shortly after the train ended. Memory-guided saccades were most dramatically suppressed and were often rendered hypometric, whereas visually guided saccades were less severely suppressed by stimulation. At 18 FEF sites, the suppression of saccades was the only observable effect of electrical stimulation. Contraversive saccades were usually more strongly suppressed than ipsiversive ones, and cells recorded at such purely suppressive sites commonly had either foveal receptive fields or postsaccadic responses. At 12 other FEF sites at which saccadic eye movements were elicited at low thresholds, task-related saccades whose vectors differed from that of the electrically elicited saccade were suppressed by electrical stimulation. Such suppression at saccade sites was observed even with currents below the threshold for eliciting saccades. Pure suppression sites tended to be located near or in the fundus, deeper in the anterior bank of the arcuate than elicited saccade sites. Stimulation in the prefrontal association cortex anterior to FEF did not suppress saccades, nor did stimulation in premotor cortex posterior to FEF. These findings indicate that the primate FEF can help orchestrate saccadic eye movements by suppressing inappropriate saccade vectors as well as by selecting, specifying, and triggering appropriate saccades. We hypothesize that saccades could be suppressed both through local FEF interactions and through FEF projections to subcortical regions involved in maintaining fixation.


1999 ◽  
Vol 81 (5) ◽  
pp. 2191-2214 ◽  
Author(s):  
Elisa C. Dias ◽  
Mark A. Segraves

Muscimol-induced inactivation of the monkey frontal eye field: effects on visually and memory-guided saccades. Although neurophysiological, anatomic, and imaging evidence suggest that the frontal eye field (FEF) participates in the generation of eye movements, chronic lesions of the FEF in both humans and monkeys appear to cause only minor deficits in visually guided saccade generation. Stronger effects are observed when subjects are tested in tasks with more cognitive requirements. We tested oculomotor function after acutely inactivating regions of the FEF to minimize the effects of plasticity and reallocation of function after the loss of the FEF and gain more insight into the FEF contribution to the guidance of eye movements in the intact brain. Inactivation was induced by microinjecting muscimol directly into physiologically defined sites in the FEF of three monkeys. FEF inactivation severely impaired the monkeys’ performance of both visually guided and memory-guided saccades. The monkeys initiated fewer saccades to the retinotopic representation of the inactivated FEF site than to any other location in the visual field. The saccades that were initiated had longer latencies, slower velocities, and larger targeting errors than controls. These effects were present both for visually guided and for memory-guided saccades, although the memory-guided saccades were more disrupted. Initially, the effects were restricted spatially, concentrating around the retinotopic representation at the center of the inactivated site, but, during the course of several hours, these effects spread to flanking representations. Predictability of target location and motivation of the monkey also affected saccadic performance. For memory-guided saccades, increases in the time during which the monkey had to remember the spatial location of a target resulted in further decreases in the accuracy of the saccades and in smaller peak velocities, suggesting a progressive loss of the capacity to maintain a representation of target location in relation to the fovea after FEF inactivation. In addition, the monkeys frequently made premature saccades to targets in the hemifield ipsilateral to the injection site when performing the memory task, indicating a deficit in the control of fixation that could be a consequence of an imbalance between ipsilateral and contralateral FEF activity after the injection. There was also a progressive loss of fixation accuracy, and the monkeys tended to restrict spontaneous visual scanning to the ipsilateral hemifield. These results emphasize the strong role of the FEF in the intact monkey in the generation of all voluntary saccadic eye movements, as well as in the control of fixation.


2013 ◽  
Vol 109 (8) ◽  
pp. 2129-2144 ◽  
Author(s):  
Robin C. Ashmore ◽  
Marc A. Sommer

The caudal dentate nucleus (DN) in lateral cerebellum is connected with two visual/oculomotor areas of the cerebrum: the frontal eye field and lateral intraparietal cortex. Many neurons in frontal eye field and lateral intraparietal cortex produce “delay activity” between stimulus and response that correlates with processes such as motor planning. Our hypothesis was that caudal DN neurons would have prominent delay activity as well. From lesion studies, we predicted that this activity would be related to self-timing, i.e., the triggering of saccades based on the internal monitoring of time. We recorded from neurons in the caudal DN of monkeys ( Macaca mulatta) that made delayed saccades with or without a self-timing requirement. Most (84%) of the caudal DN neurons had delay activity. These neurons conveyed at least three types of information. First, their activity was often correlated, trial by trial, with saccade initiation. Correlations were found more frequently in a task that required self-timing of saccades (53% of neurons) than in a task that did not (27% of neurons). Second, the delay activity was often tuned for saccade direction (in 65% of neurons). This tuning emerged continuously during a trial. Third, the time course of delay activity associated with self-timed saccades differed significantly from that associated with visually guided saccades (in 71% of neurons). A minority of neurons had sensory-related activity. None had presaccadic bursts, in contrast to DN neurons recorded more rostrally. We conclude that caudal DN neurons convey saccade-related delay activity that may contribute to the motor preparation of when and where to move.


2020 ◽  
Vol 123 (1) ◽  
pp. 107-119 ◽  
Author(s):  
Debaleena Basu ◽  
Aditya Murthy

We use sequences of saccadic eye movements to continually explore our visual environments. Previous behavioral studies have established that saccades in a sequence may be programmed in parallel by the oculomotor system. In this study, we tested the neural correlates of parallel programming of saccade sequences in the frontal eye field (FEF), using single-unit electrophysiological recordings from macaques performing a sequential saccade task. It is known that FEF visual neurons instantiate target selection whereas FEF movement neurons undertake saccade preparation, where the activity corresponding to a saccade vector gradually ramps up. The question of whether FEF movement neurons are involved in concurrent processing of saccade plans is as yet unresolved. In the present study, we show that, when a peripheral target is foveated after a sequence of two saccades, presaccadic activity of FEF movement neurons for the second saccade can be activated while the first is still underway. Moreover, the onset of movement activity varied parametrically with the behaviorally measured time available for parallel programming. Although at central fixation coactivated FEF movement activity may vectorially encode the retinotopic location of the second target with respect to the fixation point or the remapped location of the second target, with respect to the first our evidence suggests the possibility of early encoding of the remapped second saccade vector. Taken together, the results indicate that movement neurons, although located terminally in the FEF visual-motor spectrum, can accomplish concurrent processing of multiple saccade plans, leading to rapid execution of saccade sequences. NEW & NOTEWORTHY The execution of purposeful sequences underlies much of goal-directed behavior. How different brain areas accomplish sequencing is poorly understood. Using a modified double-step task to generate a rapid sequence of two saccades, we demonstrate that downstream movement neurons in the frontal eye field (FEF), a prefrontal oculomotor area, allow for coactivation of the first and second movement plans that constitute the sequence. These results provide fundamental insights into the neural control of action sequencing.


2018 ◽  
Author(s):  
Debaleena Basu ◽  
Aditya Murthy

AbstractWe use sequences of saccadic eye movements to continually explore our visual environments. Previous studies have established that saccades in a sequence may be programmed in parallel by the oculomotor system. In this study, we tested the neural correlates of parallel programming of saccade sequences in the frontal eye field (FEF), using single-unit electrophysiological recordings from macaques performing a double-step saccade task. Neurons in the FEF range from visual neurons instantiating target selection, to movement neurons which prepare a saccadic response towards the selected target. The question of whether the FEF movement neurons undertake concurrent processing of multiple goals or saccade plans is yet unresolved. We show that when a peripheral target is foveated by a sequence of two saccades, FEF movement activity for the second saccade can be initiated whilst the first is still underway. Moreover, the onset of the movement activity varied parametrically with the behaviorally measured time available for parallel programming. Finally, the concurrent activity was specific for the final remapped motor vector connecting the first and the second targets and not the goal of the second saccade. In contrast, the upstream FEF visual-related neurons showed concurrent activity related to the goal of the second saccade, but not the remapped vector connecting the first and the second targets. Taken together, the results indicate that movement neurons, although located terminally in the FEF visual-motor spectrum, can accomplish concurrent processing of multiple saccade plans, leading to rapid execution of saccade sequences.


2016 ◽  
Vol 116 (6) ◽  
pp. 2882-2891 ◽  
Author(s):  
Rebecca M. Krock ◽  
Tirin Moore

Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques ( Macaca mulatta). We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining ∼80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression.


1994 ◽  
Vol 71 (3) ◽  
pp. 1250-1253 ◽  
Author(s):  
G. S. Russo ◽  
C. J. Bruce

1. We studied neuronal activity in the monkey's frontal eye field (FEF) in conjunction with saccades directed to auditory targets. 2. All FEF neurons with movement activity preceding saccades to visual targets also were active preceding saccades to auditory targets, even when such saccades were made in the dark. Movement cells generally had comparable bursts for aurally and visually guided saccades; visuomovement cells often had weaker bursts in conjunction with aurally guided saccades. 3. When these cells were tested from different initial fixation directions, movement fields associated with aurally guided saccades, like fields mapped with visual targets, were a function of saccade dimensions, and not the speaker's spatial location. Thus, even though sound location cues are chiefly craniotopic, the crucial factor for a FEF discharge before aurally guided saccades was the location of auditory target relative to the current direction of gaze. 4. Intracortical microstimulation at the sites of these cells evoked constant-vector saccades, and not goal-directed saccades. The direction and size of electrically elicited saccades generally matched the cell's movement field for aurally guided saccades. 5. Thus FEF activity appears to have a role in aurally guided as well as visually guided saccades. Moreover, visual and auditory target representations, although initially obtained in different coordinate systems, appear to converge to a common movement vector representation at the FEF stage of saccadic processing that is appropriate for transmittal to saccade-related burst neurons in the superior colliculus and pons.


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.


1992 ◽  
Vol 68 (6) ◽  
pp. 1967-1985 ◽  
Author(s):  
M. A. Segraves

1. This study identified neurons in the rhesus monkey's frontal eye field that projected to oculomotor regions of the pons and characterized the signals sent by these neurons from frontal eye field to pons. 2. In two behaving rhesus monkeys, frontal eye field neurons projecting to the pons were identified via antidromic excitation by a stimulating microelectrode whose tip was centered in or near the omnipause region of the pontine raphe. This stimulation site corresponded to the nucleus raphe interpositus (RIP). In addition, electrical stimulation of the frontal eye field was used to demonstrate the effects of frontal eye field input on neurons in the omnipause region and surrounding paramedian pontine reticular formation (PPRF). 3. Twenty-five corticopontine neurons were identified and characterized. Most frontal eye field neurons projecting to the pons were either movement neurons, firing in association with saccadic eye movements (48%), or foveal neurons responsive to visual stimulation of the fovea combined with activity related to fixation (28%). Corticopontine movement neurons fired before, during, and after saccades made within a restricted movement field. 4. The activity of identified corticopontine neurons was very similar to the activity of neurons antidromically excited from the superior colliculus where 59% had movement related activity, and 22% had foveal and fixation related activity. 5. High-intensity, short-duration electrical stimulation of the frontal eye field caused omnipause neurons to stop firing. The cessation in firing appeared to be immediate, within < or = 5 ms. The time that the omnipause neuron remained quiet depended on the intensity of the cortical stimulus and lasted up to 30 ms after a train of three stimulus pulses lasting a total of 6 ms at an intensity of 1,000 microA. Low-intensity, longer duration electrical stimuli (24 pulses, 75 microA, 70 ms) traditionally used to evoke saccades from the frontal eye field were also followed by a cessation in omnipause neuron firing, but only after a delay of approximately 30 ms. For these stimuli, the omnipause neuron resumed firing when the stimulus was turned off. 6. The same stimuli that caused omnipause neurons to stop firing excited burst neurons in the PPRF. The latency to excitation ranged from 4.2 to 9.8 ms, suggesting that there is at least one additional neuron between frontal eye field neurons and burst neurons in the PPRF. 7. The present study confirms and extends the results of previous work, with the use of retrograde and anterograde tracers, demonstrating direct projections from the frontal eye field to the pons.(ABSTRACT TRUNCATED AT 400 WORDS)


Sign in / Sign up

Export Citation Format

Share Document