Threshold mechanism for saccade initiation in frontal eye field and superior colliculus

2013 ◽  
Vol 109 (11) ◽  
pp. 2767-2780 ◽  
Author(s):  
Jay J. Jantz ◽  
Masayuki Watanabe ◽  
Stefan Everling ◽  
Douglas P. Munoz
Keyword(s):  
Superior Colliculus ◽  
Discharge Rate ◽  
Population Level ◽  
Threshold Level ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Variable Threshold ◽  
Discharge Rates ◽  
Fixed Threshold ◽  
Eye Field

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.

scholarly journals What the Brain Stem Tells the Frontal Cortex. I. Oculomotor Signals Sent From Superior Colliculus to Frontal Eye Field Via Mediodorsal Thalamus

2004 ◽  
Vol 91 (3) ◽  
pp. 1381-1402 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz
Keyword(s):  
Superior Colliculus ◽  
Frontal Cortex ◽  
Brain Stem ◽  
Signal Transmission ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Mediodorsal Thalamus ◽  
Visual Activity ◽  
Eye Field ◽  
The Brain

Neuronal processing in cerebral cortex and signal transmission from cortex to brain stem have been studied extensively, but little is known about the numerous feedback pathways that ascend from brain stem to cortex. In this study, we characterized the signals conveyed through an ascending pathway coursing from the superior colliculus (SC) to the frontal eye field (FEF) via mediodorsal thalamus (MD). Using antidromic and orthodromic stimulation, we identified SC source neurons, MD relay neurons, and FEF recipient neurons of the pathway in Macaca mulatta. The monkeys performed oculomotor tasks, including delayed-saccade tasks, that permitted analysis of signals such as visual activity, delay activity, and presaccadic activity. We found that the SC sends all of these signals into the pathway with no output selectivity, i.e., the signals leaving the SC resembled those found generally within the SC. Visual activity arrived in FEF too late to contribute to short-latency visual responses there, and delay activity was largely filtered out in MD. Presaccadic activity, however, seemed critical because it traveled essentially unchanged from SC to FEF. Signal transmission in the pathway was fast (∼2 ms from SC to FEF) and topographically organized (SC neurons drove MD and FEF neurons having similarly eccentric visual and movement fields). Our analysis of identified neurons in one pathway from brain stem to frontal cortex thus demonstrates that multiple signals are sent from SC to FEF with presaccadic activity being prominent. We hypothesize that a major signal conveyed by the pathway is corollary discharge information about the vector of impending saccades.

scholarly journals Neural mechanisms of speed-accuracy tradeoff of visual search: Saccade vigor, targeting errors, superior colliculus and frontal eye field

2017 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Superior Colliculus ◽  
Time Course ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Response Preparation ◽  
Eye Field ◽  
Neurophysiological Mechanisms ◽  
Speed Accuracy ◽  
Accuracy Tradeoff

AbstractBalancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus, and description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys, but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. Visually-responsive neurons modulated baseline firing rate and the time course of salience evidence. Unlike FEF, the magnitude of visual responses in SC did not vary across SAT conditions, but the time to locate the target was longer in Accurate as compared to Fast trials. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Search errors occurred when visual salience neurons in FEF and SC treated distractors as targets, even in the Accurate condition. Saccade-related neural activity in SC but less FEF varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT.Significance statementNeurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This paper reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision-making.

scholarly journals Radial motion bias in macaque frontal eye field

2006 ◽  
Vol 23 (1) ◽  
pp. 49-60 ◽  
Author(s):  
QUAN XIAO ◽  
ANDREI BARBORICA ◽  
VINCENT P. FERRERA
Keyword(s):  
Receptive Field ◽  
Optic Flow ◽  
Posterior Parietal Cortex ◽  
Population Level ◽  
Direction Selectivity ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Eye Field ◽  
Outward Motion ◽  
Random Dot Patterns

The visual responsiveness and spatial tuning of frontal eye field (FEF) neurons were determined using a delayed memory saccade task. Neurons with visual responses were then tested for direction selectivity using moving random dot patterns centered in the visual receptive field. The preferred axis of motion showed a significant tendency to be aligned with the receptive-field location so as to favor motion toward or away from the center of gaze. Centrifugal (outward) motion was preferred over centripetal motion. Motion-sensitive neurons in FEF thus appear to have a direction bias at the population level. This bias may facilitate the detection or discrimination of expanding optic flow patterns. The direction bias is similar to that seen in visual area MT and in posterior parietal cortex, from which FEF receives afferent projections. The outward motion bias may explain asymmetries in saccades made to moving targets. A representation of optic flow in FEF might be useful for planning eye movements during navigation.

scholarly journals Composition and Topographic Organization of Signals Sent From the Frontal Eye Field to the Superior Colliculus

2000 ◽  
Vol 83 (4) ◽  
pp. 1979-2001 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz
Keyword(s):  
Superior Colliculus ◽  
Visual Analysis ◽  
Sampling Bias ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Topographic Organization ◽  
Specific Subset ◽  
Cognitive Operations ◽  
Eye Field ◽  
Movement Field

The frontal eye field (FEF) and superior colliculus (SC) contribute to saccadic eye movement generation, and much of the FEF's oculomotor influence may be mediated through the SC. The present study examined the composition and topographic organization of signals flowing from FEF to SC by recording from FEF neurons that were antidromically activated from rostral or caudal SC. The first and most general result was that, in a sample of 88 corticotectal neurons, the types of signals relayed from FEF to SC were highly diverse, reflecting the general population of signals within FEF rather than any specific subset of signals. Second, many neurons projecting from FEF to SC carried signals thought to reflect cognitive operations, namely tonic discharges during the delay period of a delayed-saccade task (delay signals), elevated discharges during the gap period of a gap task (gap increase signals), or both. Third, FEF neurons discharging during fixation were found to project to the SC, although they did not project preferentially to rostral SC, where similar fixation neurons are found. Neurons that did project preferentially to the rostral SC were those with foveal visual responses and those pausing during the gap period of the gap task. Many of the latter neurons also had foveal visual responses, presaccadic pauses in activity, and postsaccadic increases in activity. These two types of rostral-projecting neurons therefore may contribute to the activity of rostral SC fixation neurons. Fourth, conduction velocity was used as an indicator of cell size to correct for sampling bias. The outcome of this correction procedure suggested that among the most prevalent neurons in the FEF corticotectal population are those carrying putative cognitive-related signals, i.e., delay and gap increase signals, and among the least prevalent are those carrying presaccadic burst discharges but lacking peripheral visual responses. Fifth, corticotectal neurons carrying various signals were biased topographically across the FEF. Neurons with peripheral visual responses but lacking presaccadic burst discharges were biased laterally, neurons with presaccadic burst discharges but lacking peripheral visual responses were biased medially, and neurons carrying delay or gap increase signals were biased dorsally. Finally, corticotectal neurons were distributed within the FEF as a function of their visual or movement field eccentricity and projected to the SC such that eccentricity maps in both structures were closely aligned. We conclude that the FEF most likely influences the activity of SC neurons continuously from the start of fixation, through visual analysis and cognitive manipulations, until a saccade is generated and fixation begins anew. Furthermore, the projection from FEF to SC is highly topographically organized in terms of function at both its source and its termination.

scholarly journals Neural mechanisms of speed-accuracy tradeoff of visual search: saccade vigor, the origin of targeting errors, and comparison of the superior colliculus and frontal eye field

2018 ◽  
Vol 120 (1) ◽  
pp. 372-384 ◽  
Author(s):  
Thomas R. Reppert ◽  
Mathieu Servant ◽  
Richard P. Heitz ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Superior Colliculus ◽  
Target Selection ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Response Preparation ◽  
Eye Field ◽  
Neurophysiological Mechanisms ◽  
Speed Accuracy ◽  
Accuracy Tradeoff

Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. NEW & NOTEWORTHY Neurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This article reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision making.

scholarly journals Disparity Sensitivity of Frontal Eye Field Neurons

2000 ◽  
Vol 83 (1) ◽  
pp. 625-629 ◽  
Author(s):  
Stefano Ferraina ◽  
Martin Paré ◽  
Robert H. Wurtz
Keyword(s):  
Eye Movements ◽  
Dimensional Space ◽  
Visual Stimuli ◽  
Three Dimensional ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Motor Processes ◽  
Uncrossed Disparity ◽  
Eye Field ◽  
Three Dimensional Space

Information about depth is necessary to generate saccades to visual stimuli located in three-dimensional space. To determine whether monkey frontal eye field (FEF) neurons play a role in the visuo-motor processes underlying this behavior, we studied their visual responses to stimuli at different disparities. Disparity sensitivity was tested from 3° of crossed disparity (near) to 3° degrees of uncrossed disparity (far). The responses of about two thirds of FEF visual and visuo-movement neurons were sensitive to disparity and showed a broad tuning in depth for near or far disparities. Early phasic and late tonic visual responses often displayed different disparity sensitivity. These findings provide evidence of depth-related signals in FEF and suggest a role for FEF in the control of disconjugate as well as conjugate eye movements.

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 & 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, & 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.

Differential Temporal Storage Capacity in the Baseline Activity of Neurons in Macaque Frontal Eye Field and Area V4

2010 ◽  
Vol 103 (5) ◽  
pp. 2433-2445 ◽  
Author(s):  
Tadashi Ogawa ◽  
Hidehiko Komatsu
Keyword(s):  
Neuronal Activity ◽  
Storage Capacity ◽  
Discharge Rate ◽  
Time Lag ◽  
Temporal Correlation ◽  
Frontal Eye Field ◽  
Area V4 ◽  
Baseline Activity ◽  
Eye Field ◽  
V4 Neurons

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.

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