Parallel programming of saccades in the macaque frontal eye field: are sequential motor plans coactivated?

2020 ◽  
Vol 123 (1) ◽  
pp. 107-119 ◽  
Author(s):  
Debaleena Basu ◽  
Aditya Murthy
Keyword(s):  
Parallel Programming ◽  
Neural Control ◽  
Target Selection ◽  
Saccadic Eye Movements ◽  
Oculomotor System ◽  
Frontal Eye Field ◽  
Movement Activity ◽  
Concurrent Processing ◽  
Electrophysiological Recordings ◽  
Eye Field

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.

scholarly journals Concurrent neural representations of the current and forthcoming movement plans in the frontal eye field during a saccade sequence

2018 ◽  
Author(s):  
Debaleena Basu ◽  
Aditya Murthy
Keyword(s):  
Parallel Programming ◽  
Target Selection ◽  
Saccadic Eye Movements ◽  
Oculomotor System ◽  
Frontal Eye Field ◽  
Movement Activity ◽  
Concurrent Processing ◽  
Electrophysiological Recordings ◽  
Measured Time ◽  
Eye Field

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.

Electrical Stimulation of the Frontal Eye Fields in the Head-Free Macaque Evokes Kinematically Normal 3D Gaze Shifts

2010 ◽  
Vol 104 (6) ◽  
pp. 3462-3475 ◽  
Author(s):  
Jachin A. Monteon ◽  
Alina G. Constantin ◽  
Hongying Wang ◽  
Julio Martinez-Trujillo ◽  
J. Douglas Crawford
Keyword(s):  
Target Selection ◽  
Three Dimensional ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Velocity Amplitude ◽  
Eye Field ◽  
Head Rotations ◽  
Stimulation Of

The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30–100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity–amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listing's law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listing's plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye–head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye–head coordination are likely specified by downstream mechanisms.

scholarly journals Predictive Activity in Macaque Frontal Eye Field Neurons During Natural Scene Searching

2010 ◽  
Vol 103 (3) ◽  
pp. 1238-1252 ◽  
Author(s):  
Adam N. Phillips ◽  
Mark A. Segraves
Keyword(s):  
Visual Search ◽  
Target Selection ◽  
Cell Activity ◽  
Early Time ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Natural Scenes ◽  
Eye Field ◽  
Intermediate Time ◽  
And Performance

Generating sequences of multiple saccadic eye movements allows us to search our environment quickly and efficiently. Although the frontal eye field cortex (FEF) has been linked to target selection and making saccades, little is known about its role in the control and performance of the sequences of saccades made during self-guided visual search. We recorded from FEF cells while monkeys searched for a target embedded in natural scenes and examined the degree to which cells with visual and visuo-movement activity showed evidence of target selection for future saccades. We found that for about half of these cells, activity during the fixation period between saccades predicted the next saccade in a sequence at an early time that precluded selection based on current visual input to a cell's response field. In addition to predicting the next saccade, activity during the fixation prior to two successive saccades also predicted the direction and goal of the second saccade in the sequence. We refer to this as advanced predictive activity. Unlike activity indicating the upcoming saccade, advanced predictive activity occurred later in the fixation period, mirroring the order of the saccade sequence itself. The remaining cells without advanced predictive activity did not predict future saccades but reintroduced the signal for the upcoming saccade at an intermediate time in the fixation period. Together these findings suggest that during natural visual search the timing of FEF cell activity is consistent with a role in specifying targets for one or more future saccades in a search sequence.

Neural mechanisms underlying the temporal control of sequential saccade planning in the frontal eye field

2021 ◽  
Vol 118 (40) ◽  
pp. e2108922118
Author(s):  
Debaleena Basu ◽  
Naveen Sendhilnathan ◽  
Aditya Murthy
Keyword(s):  
Neural Control ◽  
Saccadic Eye Movements ◽  
Neural Mechanisms ◽  
Visual Environment ◽  
Frontal Eye Field ◽  
Neural Responses ◽  
Capacity Sharing ◽  
Eye Field ◽  
Saccade Task ◽  
Neural Underpinnings

Sequences of saccadic eye movements are instrumental in navigating our visual environment. While neural activity has been shown to ramp up to a threshold before single saccades, the neural underpinnings of multiple saccades is unknown. To understand the neural control of saccade sequences, we recorded from the frontal eye field (FEF) of macaque monkeys while they performed a sequential saccade task. We show that the concurrent planning of two saccade plans brings forth processing bottlenecks, specifically by decreasing the growth rate and increasing the threshold of saccade-related ramping activity. The rate disruption affected both saccade plans, and a computational model, wherein activity related to the two saccade plans mutually and asymmetrically inhibited each other, predicted the behavioral and neural results observed experimentally. Borrowing from models in psychology, our results demonstrate a capacity-sharing mechanism of processing bottlenecks, wherein multiple saccade plans in a sequence compete for the processing capacity by the perturbation of the saccade-related ramping activity. Finally, we show that, in contrast to movement-related neurons, visual activity in FEF neurons is not affected by the presence of multiple saccade targets, indicating that, for perceptually simple tasks, inhibition within movement-related neurons mainly instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.

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
Keyword(s):  
Time Course ◽  
Saccadic Eye Movements ◽  
Activity Level ◽  
Frontal Eye Field ◽  
Topographic Map ◽  
Visually Guided ◽  
Movement Activity ◽  
Dynamic Events ◽  
Motor Error ◽  
Eye Field

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.

Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons

1992 ◽  
Vol 68 (6) ◽  
pp. 1967-1985 ◽  
Author(s):  
M. A. Segraves
Keyword(s):  
Electrical Stimulation ◽  
Visual Stimulation ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Burst Neurons ◽  
Eye Field ◽  
Movement Field ◽  
Omnipause Neurons ◽  
Stimulation Of

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)

scholarly journals Salience by Competitive and Recurrent Interactions: Bridging Neural Spiking and Computation

2021 ◽  
Author(s):  
Gregory Edward Cox ◽  
Thomas Palmeri ◽  
Gordon D. Logan ◽  
Philip L. Smith ◽  
Jeffrey Schall
Keyword(s):  
Decision Making ◽  
Response Times ◽  
Target Selection ◽  
Interaction Model ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Visual Neurons ◽  
Discharge Rates ◽  
Neural Spiking ◽  
Eye Field

Decisions about where to move the eyes depend on neurons in Frontal Eye Field (FEF). Movement neurons in FEF accumulate salience evidence derived from FEF visual neurons to select the location of a saccade target among distractors. How visual neurons achieve this salience representation is unknown. We present a neuro-computational model of target selection called Salience by Competitive and Recurrent Interactions (SCRI), based on the Competitive Interaction model of attentional selection and decision making (Smith &amp; Sewell, 2013). SCRI selects targets by synthesizing localization and identification information to yield a dynamically evolving representation of salience across the visual field. SCRI accounts for neural spiking of individual FEF visual neurons, explaining idiosyncratic differences in neural dynamics with specific parameters. Many visual neurons resolve the competition between search items through feedforward inhibition between signals representing different search items, some also require lateral inhibition, and many act as recurrent gates to modulate the incoming flow of information about stimulus identity. SCRI was tested further by using simulated spiking representations of visual salience as input to the Gated Accumulator Model of FEF movement neurons (Purcell et al., 2010; Purcell, Schall, Logan, &amp; Palmeri, 2012). Predicted saccade response times fit those observed for search arrays of different set size and different target-distractor similarity, and accumulator trajectories replicated movement neuron discharge rates. These findings offer new insights into visual decision making through converging neuro-computational constraints and provide a novel computational account of the diversity of FEF visual neurons.

scholarly journals Shape Selectivity in Primate Frontal Eye Field

2008 ◽  
Vol 100 (2) ◽  
pp. 796-814 ◽  
Author(s):  
Xinmiao Peng ◽  
Margaret E. Sereno ◽  
Amanda K. Silva ◽  
Sidney R. Lehky ◽  
Anne B. Sereno
Keyword(s):  
Functional Organization ◽  
Target Selection ◽  
Visual Stimuli ◽  
Shape Selectivity ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Gaze Shift ◽  
Match To Sample ◽  
Neurophysiological Studies ◽  
Eye Field

Previous neurophysiological studies of the frontal eye field (FEF) in monkeys have focused on its role in saccade target selection and gaze shift control. It has been argued that FEF neurons indicate the locations of behaviorally significant visual stimuli and are not inherently sensitive to specific features of the visual stimuli per se. Here, for the first time, we directly examined single cell responses to simple, two-dimensional shapes and found that shape selectivity exists in a substantial number of FEF cells during a passive fixation task or during the sample, delay (memory), and eye movement periods in a delayed match to sample (DMTS) task. Our data demonstrate that FEF neurons show sensory and mnemonic selectivity for stimulus shape features whether or not they are behaviorally significant for the task at hand. We also investigated the extent and localization of activation in the FEF using a variety of shape stimuli defined by static or dynamic cues employing functional magentic resonance imaging (fMRI) in anesthetized and paralyzed monkeys. Our fMRI results support the electrophysiological findings by showing significant FEF activation for a variety of shape stimuli and cues in the absence of attentional and motor processing. This shape selectivity in FEF is comparable to previous reports in the ventral pathway, inviting a reconsideration of the functional organization of the visual system.

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