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 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 Neurally constrained modeling of speed-accuracy tradeoff during visual search: gated accumulation of modulated evidence

2019 ◽  
Vol 121 (4) ◽  
pp. 1300-1314 ◽  
Author(s):  
Mathieu Servant ◽  
Gabriel Tillman ◽  
Jeffrey D. Schall ◽  
Gordon D. Logan ◽  
Thomas J. Palmeri
Keyword(s):  
Decision Making ◽  
Visual Search ◽  
Response Times ◽  
Frontal Eye Field ◽  
Search Performance ◽  
Model Framework ◽  
Accumulator Model ◽  
Eye Field ◽  
Speed Accuracy ◽  
Accuracy Tradeoff

Stochastic accumulator models account for response times and errors in perceptual decision making by assuming a noisy accumulation of perceptual evidence to a threshold. Previously, we explained saccade visual search decision making by macaque monkeys with a stochastic multiaccumulator model in which accumulation was driven by a gated feed-forward integration to threshold of spike trains from visually responsive neurons in frontal eye field that signal stimulus salience. This neurally constrained model quantitatively accounted for response times and errors in visual search for a target among varying numbers of distractors and replicated the dynamics of presaccadic movement neurons hypothesized to instantiate evidence accumulation. This modeling framework suggested strategic control over gate or over threshold as two potential mechanisms to accomplish speed-accuracy tradeoff (SAT). Here, we show that our gated accumulator model framework can account for visual search performance under SAT instructions observed in a milestone neurophysiological study of frontal eye field. This framework captured key elements of saccade search performance, through observed modulations of neural input, as well as flexible combinations of gate and threshold parameters necessary to explain differences in SAT strategy across monkeys. However, the trajectories of the model accumulators deviated from the dynamics of most presaccadic movement neurons. These findings demonstrate that traditional theoretical accounts of SAT are incomplete descriptions of the underlying neural adjustments that accomplish SAT, offer a novel mechanistic account of decision-making mechanisms during speed-accuracy tradeoff, and highlight questions regarding the identity of model and neural accumulators. NEW & NOTEWORTHY A gated accumulator model is used to elucidate neurocomputational mechanisms of speed-accuracy tradeoff. Whereas canonical stochastic accumulators adjust strategy only through variation of an accumulation threshold, we demonstrate that strategic adjustments are accomplished by flexible combinations of both modulation of the evidence representation and adaptation of accumulator gate and threshold. The results indicate how model-based cognitive neuroscience can translate between abstract cognitive models of performance and neural mechanisms of speed-accuracy tradeoff.

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.

Dissociation of Visual Discrimination From Saccade Programming in Macaque Frontal Eye Field

1997 ◽  
Vol 77 (2) ◽  
pp. 1046-1050 ◽  
Author(s):  
Kirk G. Thompson ◽  
Narcisse P. Bichot ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Eye Movements ◽  
Visual Stimulus ◽  
Visual Discrimination ◽  
Time Course ◽  
Selection Process ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Eye Field ◽  
Saccade Programming

Thompson, Kirk G., Narcisse P. Bichot, and Jeffrey D. Schall. Dissociation of visual discrimination from saccade programming in macaque frontal eye field. J. Neurophysiol. 77: 1046–1050, 1997. To determine whether visual discrimination in macaque frontal eye field (FEF) is contingent on saccade planning, unit activity was recorded in two monkeys during blocked go and no-go visual search trials. The eye movements made by monkeys after correct no-go trials, in addition to an attenuation of the visual responses in no-go trials compared with go trials, indicated that covert saccade planning was effectively discouraged. During no-go search trials, the activity of the majority of neurons evolved to signal the location of the oddball stimulus. The degree and time course of the stimulus discrimination process observed in no-go trials was not different from that observed in go trials. We conclude that the discrimination of a salient visual stimulus reflected by FEF neurons is not contingent on saccade production but rather may reflect the outcome of an automatic visual selection process.

scholarly journals Neural Basis of the Set-Size Effect in Frontal Eye Field: Timing of Attention During Visual Search

2009 ◽  
Vol 101 (4) ◽  
pp. 1699-1704 ◽  
Author(s):  
Jeremiah Y. Cohen ◽  
Richard P. Heitz ◽  
Geoffrey F. Woodman ◽  
Jeffrey D. Schall
Keyword(s):  
Visual Search ◽  
Response Time ◽  
Visual Target ◽  
Target Selection ◽  
Target Object ◽  
Frontal Eye Field ◽  
Neural Basis ◽  
Set Size ◽  
Eye Field ◽  
Recorded Activity

Visual search for a target object among distractors often takes longer when more distractors are present. To understand the neural basis of this capacity limitation, we recorded activity from visually responsive neurons in the frontal eye field (FEF) of macaque monkeys searching for a target among distractors defined by form (randomly oriented T or L). To test the hypothesis that the delay of response time with increasing number of distractors originates in the delay of attention allocation by FEF neurons, we manipulated the number of distractors presented with the search target. When monkeys were presented with more distractors, visual target selection was delayed and neuronal activity was reduced in proportion to longer response time. These findings indicate that the time taken by FEF neurons to select the target contributes to the variation in visual search efficiency.

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 Frontal Eye Field Activity Before Visual Search Errors Reveals the Integration of Bottom-Up and Top-Down Salience

2005 ◽  
Vol 93 (1) ◽  
pp. 337-351 ◽  
Author(s):  
Kirk G. Thompson ◽  
Narcisse P. Bichot ◽  
Takashi R. Sato
Keyword(s):  
Visual Search ◽  
Search Task ◽  
Target Selection ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Top Down ◽  
Bottom Up ◽  
Stimulus Response ◽  
Singleton Search ◽  
Eye Field

We investigated the saccade decision process by examining activity recorded in the frontal eye field (FEF) of monkeys performing 2 separate visual search experiments in which there were errors in saccade target choice. In the first experiment, the difficulty of a singleton search task was manipulated by varying the similarity between the target and distractors; errors were made more often when the distractors were similar to the target. On catch trials in which the target was absent the monkeys occasionally made false alarm errors by shifting gaze to one of the distractors. The second experiment was a popout color visual search task in which the target and distractor colors switched unpredictably across trials. Errors occurred most frequently on the first trial after the switch and less often on subsequent trials. In both experiments, FEF neurons selected the saccade goal on error trials, not the singleton target of the search array. Although saccades were made to the same stimulus locations, presaccadic activation and the magnitude of selection differed across trial conditions. The variation in presaccadic selective activity was accounted for by the variation in saccade probability across the stimulus–response conditions, but not by variations in saccade metrics. These results suggest that FEF serves as a saccade probability map derived from the combination of bottom-up and top-down influences. Peaks on this map represent the behavioral relevance of each item in the visual field rather than just reflecting saccade preparation. This map in FEF may correspond to the theoretical salience map of many models of attention and saccade target selection.

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.

Neural basis of saccade target selection in frontal eye field during visual search

Nature ◽  
1993 ◽  
Vol 366 (6454) ◽  
pp. 467-469 ◽  
Author(s):  
Jeffrey D. Schall ◽  
Doug P. Hanes
Keyword(s):  
Visual Search ◽  
Target Selection ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Neural Basis ◽  
Eye Field
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