scholarly journals Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets

2017 ◽  
Author(s):  
Christopher K. Hauser ◽  
Dantong Zhu ◽  
Terrence R. Stanford ◽  
Emilio Salinas

In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability, which in spite of extensive research remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, we further characterize the dynamics of this rise-to-threshold process based on computational work and single-neuron recordings from the frontal eye field (FEF) of behaving monkeys. We find that the baseline activity, build-up rate, and threshold level show strong, nonlinear co-dependencies that explain the distinct RT distributions observed experimentally. The results indicate that intrinsic randomness contributes little to saccade variance, which results mainly from an intricate, fundamentally deterministic mechanism of motor conflict resolution that has subtle yet highly characteristic manifestations.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Christopher K Hauser ◽  
Dantong Zhu ◽  
Terrence R Stanford ◽  
Emilio Salinas

In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.



2010 ◽  
Vol 103 (5) ◽  
pp. 2433-2445 ◽  
Author(s):  
Tadashi Ogawa ◽  
Hidehiko Komatsu

Previous studies have suggested that spontaneous fluctuations in neuronal activity reflect intrinsic functional brain architecture. Inspired by these findings, we analyzed baseline neuronal activity in the monkey frontal eye field (FEF; a visuomotor area) and area V4 (a visual area) during the fixation period of a cognitive behavioral task in the absence of any task-specific stimuli or behaviors. Specifically, we examined the temporal storage capacity of the instantaneous discharge rate in FEF and V4 neurons by calculating the correlation of the spike count in a bin with that in another bin during the baseline activity of a trial. We found that most FEF neurons fired significantly more (or less) in one bin if they fired more (or less) in another bin within a trial, even when these two time bins were separated by hundreds of milliseconds. By contrast, similar long time-lag correlations were observed in only a small fraction of V4 neurons, indicating that temporal correlations were considerably stronger in FEF compared with those in V4 neurons. Additional analyses revealed that the findings were not attributable to other task-related variables or ongoing behavioral performance, suggesting that the differences in temporal correlation strength reflect differences in intrinsic structural and functional architecture between visual and visuomotor areas. Thus FEF neurons probably play a greater role than V4 neurons in neural circuits responsible for temporal storage in activity.



2017 ◽  
Vol 37 (48) ◽  
pp. 11715-11730 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil


2009 ◽  
Vol 101 (5) ◽  
pp. 2485-2506 ◽  
Author(s):  
Aditya Murthy ◽  
Supriya Ray ◽  
Stephanie M. Shorter ◽  
Jeffrey D. Schall ◽  
Kirk G. Thompson

The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process—target-step reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys’ response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation.



2013 ◽  
Vol 109 (11) ◽  
pp. 2767-2780 ◽  
Author(s):  
Jay J. Jantz ◽  
Masayuki Watanabe ◽  
Stefan Everling ◽  
Douglas P. Munoz

In an influential model of frontal eye field (FEF) and superior colliculus (SC) activity, saccade initiation occurs when the discharge rate of either single neurons or a population of neurons encoding a saccade motor plan reaches a threshold level of activity. Conflicting evidence exists for whether this threshold is fixed or can change under different conditions. We tested the fixed-threshold hypothesis at the single-neuron and population levels to help resolve the inconsistency between previous studies. Two rhesus monkeys performed a randomly interleaved pro- and antisaccade task in which they had to look either toward (pro) or 180° away (anti) from a peripheral visual stimulus. We isolated visuomotor (VM) and motor (M) neurons in the FEF and SC and tested three specific predictions of a fixed-threshold hypothesis. We found little support for fixed thresholds. First, correlations were never totally absent between presaccadic discharge rate and saccadic reaction time when examining a larger (plausible) temporal period. Second, presaccadic discharge rates varied markedly between saccade tasks. Third, visual responses exceeded presaccadic motor discharges for FEF and SC VM neurons. We calculated that only a remarkably strong bias for M neurons in downstream projections could render the fixed-threshold hypothesis plausible at the population level. Also, comparisons of gap vs. overlap conditions indicate that increased inhibitory tone may be associated with stability of thresholds. We propose that fixed thresholds are the exception rather than the rule in FEF and SC, and that stabilization of an otherwise variable threshold depends on task-related, inhibitory modulation.



2020 ◽  
Author(s):  
Debaleena Basu ◽  
Naveen Sendhilnathan ◽  
Aditya Murthy

SummaryA ramp to threshold activity of frontal Eye Field (FEF) movement-related neurons best explains the reaction time of single saccades. How such activity is modulated by a concurrent saccade plan is not known. Borrowing from psychological theories of capacity sharing that are designed to explain the concurrent planning of two decisions, we show that processing bottlenecks are brought about by decreasing the growth rate and increasing the threshold of saccade-related activity. Further, rate perturbation affects both saccade plans, indicating a capacity-sharing mechanism of processing bottlenecks, where both the saccade plans compete for processing capacity. To understand how capacity sharing was neurally instantiated, we designed a model in which movement fields that instantiate two saccade plans, mutually inhibit each other. In addition to predicting the greater reaction times for both saccades and changes in growth rate and threshold activity observed experimentally, we observed a greater separation of the two neural trajectories in neural state space, which was verified experimentally. Finally, we show that in contrast to movement related neurons, visual activity in FEF neurons are not affected by the presence of multiple saccade targets, indicating that inhibition amongst movement-related neurons 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.



eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Yunshu Fan ◽  
Joshua I Gold ◽  
Long Ding

Many decisions require trade-offs between sensory evidence and internal preferences. Potential neural substrates include the frontal eye field (FEF) and caudate nucleus, but their distinct roles are not understood. Previously we showed that monkeys’ decisions on a direction-discrimination task with asymmetric rewards reflected a biased accumulate-to-bound decision process (Fan et al., 2018) that was affected by caudate microstimulation (Doi et al., 2020). Here we compared single-neuron activity in FEF and caudate to each other and to accumulate-to-bound model predictions derived from behavior. Task-dependent neural modulations were similar in both regions. However, choice-selective neurons in FEF, but not caudate, encoded behaviorally derived biases in the accumulation process. Baseline activity in both regions was sensitive to reward context, but this sensitivity was not reliably associated with behavioral biases. These results imply distinct contributions of FEF and caudate neurons to reward-biased decision-making and put experimental constraints on the neural implementation of accumulation-to-bound-like computations.



2005 ◽  
Vol 94 (1) ◽  
pp. 605-611 ◽  
Author(s):  
Jason D. Connolly ◽  
Melvyn A. Goodale ◽  
Herbert C. Goltz ◽  
Douglas P. Munoz

Variation in response latency to identical sensory stimuli has been attributed to variation in neural activity mediating preparatory set. Here we report evidence for a relationship between saccadic reaction time (SRT) and set-related brain activity measured with event-related functional magnetic resonance imaging. We measured hemodynamic activation time-courses during a preparatory “gap” period, during which no visual stimulus was present and no saccades were made. The subjects merely anticipated appearance of the target. Saccade direction and latency were recorded during scanning, and trials were sorted according to SRT. Both the frontal (FEF) and supplementary eye fields showed pretarget preparatory activity, but only in the FEF was this activity correlated with SRT. Activation in the intraparietal sulcus did not show any preparatory activity. These data provide evidence that the human FEF plays a central role in saccade initiation; pretarget activity in this region predicts both the type of eye movement (whether the subject will look toward or away from the target) and when a future saccade will occur.



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