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.

Interaction of the Frontal Eye Field and Superior Colliculus for Saccade Generation

2001 ◽  
Vol 85 (2) ◽  
pp. 804-815 ◽  
Author(s):  
Doug P. Hanes ◽  
Robert H. Wurtz
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Neural Plasticity ◽  
Recovery Of Function ◽  
Frontal Eye Field ◽  
Indirect Pathway ◽  
Compensatory Mechanisms ◽  
Eye Field ◽  
The Brain ◽  
Saccade Generation

Both the frontal eye field (FEF) in the prefrontal cortex and the superior colliculus (SC) on the roof of the midbrain participate in the generation of rapid or saccadic eye movements and both have projections to the premotor circuits of the brain stem where saccades are ultimately generated. In the present experiments, we tested the contributions of the pathway from the FEF to the premotor circuitry in the brain stem that bypasses the SC. We assayed the contribution of the FEF to saccade generation by evoking saccades with direct electrical stimulation of the FEF. To test the role of the SC in conveying information to the brain stem, we inactivated the SC, thereby removing the circuit through the SC to the brain stem, and leaving only the direct FEF–brain stem pathway. If the contributions of the direct pathway were substantial, removal of the SC should have minimal effect on the FEF stimulation, whereas if the FEF stimulation were dependent on the SC, removal of the SC should alter the effect of FEF stimulation. By acutely inactivating the SC, instead of ablating it, we were able to test the efficiency of the direct FEF–brain stem pathway before substantial compensatory mechanisms could mask the effect of removing the SC. We found two striking effects of SC inactivation. In the first, we stimulated the FEF at a site that evoked saccades with vectors that were very close to those evoked at the site of the SC inactivation, and with such optimal alignment, we found that SC inactivation eliminated the saccades evoked by FEF stimulation. The second effect was evident when the FEF evoked saccades were disparate from those evoked in the SC, and in this case we observed a shift in the direction of the evoked saccade that was consistent with the SC inactivation removing a component of a vector average. Together these observations lead to the conclusion that in the nonablated monkey the direct FEF–brain stem pathway is not functionally sufficient to generate accurate saccades in the absence of the indirect pathway that courses from the FEF through the SC to the brain stem circuitry. We suggest that the recovery of function following SC ablation that has been seen in previous studies must result not from the use of an already functioning parallel pathway but from neural plasticity within the saccadic system.

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 Integration of Eye-Centered and Landmark-Centered Codes in Frontal Eye Field Gaze Responses

2020 ◽  
Vol 30 (9) ◽  
pp. 4995-5013 ◽  
Author(s):  
Vishal Bharmauria ◽  
Amirsaman Sajad ◽  
Jirui Li ◽  
Xiaogang Yan ◽  
Hongying Wang ◽  
...  
Keyword(s):  
Frontal Cortex ◽  
Visual Information ◽  
Target Position ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Cellular Mechanisms ◽  
Behavioral Experiments ◽  
The Gaze ◽  
Field Activity ◽  
Eye Field

Abstract The visual system is thought to separate egocentric and allocentric representations, but behavioral experiments show that these codes are optimally integrated to influence goal-directed movements. To test if frontal cortex participates in this integration, we recorded primate frontal eye field activity during a cue-conflict memory delay saccade task. To dissociate egocentric and allocentric coordinates, we surreptitiously shifted a visual landmark during the delay period, causing saccades to deviate by 37% in the same direction. To assess the cellular mechanisms, we fit neural response fields against an egocentric (eye-centered target-to-gaze) continuum, and an allocentric shift (eye-to-landmark-centered) continuum. Initial visual responses best-fit target position. Motor responses (after the landmark shift) predicted future gaze position but embedded within the motor code was a 29% shift toward allocentric coordinates. This shift appeared transiently in memory-related visuomotor activity, and then reappeared in motor activity before saccades. Notably, fits along the egocentric and allocentric shift continua were initially independent, but became correlated across neurons just before the motor burst. Overall, these results implicate frontal cortex in the integration of egocentric and allocentric visual information for goal-directed action, and demonstrate the cell-specific, temporal progression of signal multiplexing for this process in the gaze system.

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 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.

Overlap of Saccadic and Pursuit Eye Movement Systems in the Brain Stem Reticular Formation

2001 ◽  
Vol 86 (6) ◽  
pp. 3056-3060 ◽  
Author(s):  
Yi-Jun Yan ◽  
Dong-Mei Cui ◽  
James C. Lynch
Keyword(s):  
Eye Movements ◽  
Brain Stem ◽  
Eye Movement ◽  
Saccadic Eye Movements ◽  
Point Of View ◽  
Medial Longitudinal Fasciculus ◽  
Frontal Eye Field ◽  
Neural Pathways ◽  
Eye Field ◽  
The Brain

Recent physiological studies have suggested that there are several sites of interaction between the neural pathways that control saccadic eye movements and those that control visual pursuit movements. To address the question of saccade/pursuit interaction from a neuroanatomical point of view, we have studied the connections from the smooth and saccadic eye movement subregions of the frontal eye field (FEFsem and FEFsac, respectively) to the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) in four Cebus apella monkeys. The riMLF has traditionally been considered to be a premotor center for vertical saccadic eye movements on the basis of single neuron recording experiments, microstimulation experiments, and surgical or chemical lesion experiments. We localized the functional subregions of the FEF with the use of low-threshold (≤50 μA) intracortical microstimulation. Biotinylated dextran amine or lectin from triticum vulgaris (wheat germ), peroxidase labeled, was placed into these functionally defined subregions to label anterogradely the terminals of axons that originated in the FEF. Our results demonstrate that both the FEFsem and FEFsac send direct projections to the ipsilateral riMLF. The distribution and density of labeling from the FEFsem are comparable to those from the FEFsac. The direct FEFsem-to-riMLF projection suggests a possible role of the riMLF in smooth pursuit eye movements and supports the hypothesis that there is interaction between the saccadic and pursuit subsystems at the brain stem level.

scholarly journals Integration of eye-centered and landmark-centered codes in frontal eye field gaze responses

2019 ◽  
Author(s):  
Vishal Bharmauria ◽  
Amirsaman Sajad ◽  
Jirui Li ◽  
Xiaogang Yan ◽  
Hongying Wang ◽  
...  
Keyword(s):  
Frontal Cortex ◽  
Visual Information ◽  
Target Position ◽  
Frontal Eye Field ◽  
Visual Responses ◽  
Cellular Mechanisms ◽  
Behavioral Experiments ◽  
The Gaze ◽  
Eye Field ◽  
Saccade Task

ABSTRACTThe visual system is thought to separate egocentric and allocentric representations, but behavioral experiments show that these codes are optimally integrated to influence goal-directed movements. To test if frontal cortex participates in this integration process, we recorded primate frontal eye field (FEF) activity during a cue-conflict memory delay saccade task. To dissociate egocentric and allocentric coordinates, we surreptitiously shifted a visual landmark during the delay period, causing saccades to deviate by 37% in the same direction. To assess the cellular mechanisms, we fit neural response fields against an egocentric (eye centered target-to-gaze) continuum, and an allocentric shift (eye-to-landmark centered) continuum. Initial visual responses best fit target position. Motor responses (after the landmark shift) predicted future gaze position but embedded within the motor code was a 29% shift toward allocentric coordinates. This shift appeared transiently in memory-related visuomotor activity, and then reappeared in motor activity before saccades. Notably, fits along the egocentric and allocentric shift continua were initially independent, but became correlated just before the motor burst. Overall, these results implicate frontal cortex in the integration of egocentric and allocentric visual information for goal-directed action, and demonstrate the cell-specific, temporal progression of signal multiplexing for this process in the gaze system.

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.

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