scholarly journals FRONTAL EYE FIELD INACTIVATION DIMINISHES SUPERIOR COLLICULUS ACTIVITY, BUT DELAYED SACCADIC ACCUMULATION GOVERNS REACTION TIME INCREASES

2017 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Reaction Time ◽  
Superior Colliculus ◽  
Neural Activity ◽  
Accumulation Rate ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Relevant Parameter ◽  
Intermediate Layers ◽  
Eye Field ◽  
Accumulator Models

AbstractStochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEF) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation, by relating variations in saccade reaction time (SRT) to variations in parameters such as baseline, rate of accumulation of activity, or threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in non-human primates, we causally test which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation.Significance StatementThe superior colliculus (SC) and frontal eye fields (FEF) are two of the best-studied areas in the primate brain. Surprisingly, little is known about what happens in the SC when the FEF is temporarily inactivated. Here, we show that temporary FEF inactivation decreases all aspects of functionally-related activity in the SC. This combination of techniques also allowed us to relate changes in SC activity to concomitant increases in saccadic reaction time (SRT). Although stochastic accumulator models relate SRT increases to reduced rates of accumulation or increases in threshold, such changes were not observed in the SC. Instead, FEF inactivation delayed the onset of saccade-related accumulation, emphasizing the importance of this parameter in biologically-plausible models of saccade initiation.

scholarly journals Frontal Eye Field Inactivation Diminishes Superior Colliculus Activity, But Delayed Saccadic Accumulation Governs Reaction Time Increases

2017 ◽  
Vol 37 (48) ◽  
pp. 11715-11730 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Reaction Time ◽  
Superior Colliculus ◽  
Frontal Eye Field ◽  
Eye Field

scholarly journals Modulation of Presaccadic Activity in the Frontal Eye Field by the Superior Colliculus

2009 ◽  
Vol 101 (6) ◽  
pp. 2934-2942 ◽  
Author(s):  
Rebecca A. Berman ◽  
Wilsaan M. Joiner ◽  
James Cavanaugh ◽  
Robert H. Wurtz
Keyword(s):  
Cerebral Cortex ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Frontal Eye Field ◽  
Visual Response ◽  
Saccadic Eye Movement ◽  
Reversible Inactivation ◽  
Intermediate Layers ◽  
Eye Field ◽  
Neuronal Processing

A cascade of neuronal signals precedes each saccadic eye movement to targets in the visual scene. In the cerebral cortex, this neuronal processing culminates in the frontal eye field (FEF), where neurons have bursts of activity before the saccade. This presaccadic activity is typically considered to drive downstream activity in the intermediate layers of the superior colliculus (SC), which receives direct projections from FEF. Consequently, the FEF activity is thought to be determined solely by earlier cortical processing and unaffected by activity in the SC. Recent evidence of an ascending path from the SC to FEF raises the possibility, however, that presaccadic activity in the FEF may also depend on input from the SC. Here we tested this possibility by recording from single FEF neurons during the reversible inactivation of SC. Our results indicate that presaccadic activity in the FEF does not require SC input: we never observed a significant reduction in FEF presaccadic activity when the SC was inactivated. Unexpectedly, in a third of experiments, SC inactivation elicited a significant increase in FEF presaccadic activity. The passive visual response of FEF neurons, in contrast, was virtually unaffected by inactivation of the SC. These findings show that presaccadic activity in the FEF does not originate in the SC but nevertheless may be influenced by modulatory signals ascending from the SC.

scholarly journals Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

2019 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Superior Colliculus ◽  
Oculomotor System ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Dependent Manner ◽  
Reversible Inactivation ◽  
Ensemble Coding ◽  
Intermediate Layers ◽  
Plausible Model ◽  
The Impact

AbstractSaccades require a spatiotemporal transformation of activity between the intermediate layers of the superior colliculus (iSC) and downstream brainstem burst generator. The dynamic linear ensemble-coding model (Goossens and Van Opstal, 2006) proposes that each iSC spike contributes a fixed mini-vector to saccade displacement. Although biologically-plausible, this model assumes cortical areas like the frontal eye fields (FEF) simply provide the saccadic goal to be executed by the iSC and brainstem burst generator. However, the FEF and iSC operate in unison during saccades, and a pathway from the FEF to the brainstem burst generator that bypasses the iSC exists. Here, we investigate the impact of large yet reversible inactivation of the FEF on iSC activity in the context of the model across four saccade tasks. We exploit the overlap of saccade vectors generated when the FEF is inactivated or not, comparing the number of iSC spikes for metrically-matched saccades. We found that the iSC emits fewer spikes for metrically-matched saccades during FEF inactivation. The decrease in spike count is task-dependent, with a greater decrease accompanying more cognitively-demanding saccades. Our results show that FEF integrity influences the readout of iSC activity in a task-dependent manner. We propose that the dynamic linear ensemble-coding model be modified so that FEF inactivation increases the gain of a readout parameter, effectively increasing the influence of a single iSC spike. We speculate that this modification could be instantiated by a direct pathway from the FEF to the omnipause region that modulates the excitability of the brainstem burst generator.Significance statementOne of the enduring puzzles in the oculomotor system is how it achieves the spatiotemporal transformation, converting spatial activity within the intermediate layers of the superior colliculus (iSC) into a rate code within the brainstem burst generator. The spatiotemporal transformation has traditionally been viewed as the purview of the oculomotor brainstem. Here, within the context of testing a biologically-plausible model of the spatiotemporal transformation, we show that reversible inactivation of the frontal eye fields (FEF) decreases the number of spikes issued by the iSC for metrically-matched saccades, with greater decreases accompanying more cognitively-demanding tasks. These results show that signals from the FEF influence the spatiotemporal transformation.

How the frontal eye field can impose a saccade goal on superior colliculus neurons

1992 ◽  
Vol 67 (4) ◽  
pp. 1003-1005 ◽  
Author(s):  
M. Schlag-Rey ◽  
J. Schlag ◽  
P. Dassonville
Keyword(s):  
Superior Colliculus ◽  
Frontal Eye Field ◽  
Intermediate Layers ◽  
Eye Field ◽  
Superior Colliculus Neurons

Saccades were electrically evoked from the frontal eye field (FEF) of two trained monkeys while saccade-cells were recorded from the intermediate layers of the superior colliculus (SC). We found that FEF microstimulation, eliciting saccades of a given vector, excited SC saccade-cells encoding the same vector and inhibited all others. Such a mechanism can prevent competing commands from arising simultaneously in different structures.

Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields

1996 ◽  
Vol 75 (5) ◽  
pp. 2187-2191 ◽  
Author(s):  
H. Mushiake ◽  
N. Fujii ◽  
J. Tanji
Keyword(s):  
Eye Movement ◽  
Neuronal Activity ◽  
Motor Task ◽  
Oculomotor Control ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Saccadic Eye Movement ◽  
Visually Guided ◽  
Supplementary Eye Field ◽  
Eye Field

1. We studied neuronal activity in the supplementary eye field (SEF) and frontal eye field (FEF) of a monkey during performance of a conditional motor task that required capturing of a target either with a saccadic eye movement (the saccade-only condition) or with an eye-hand reach (the saccade-and-reach condition), according to visual instructions. 2. Among 106 SEF neurons that showed presaccadic activity, more than one-half of them (54%) were active preferentially under the saccade-only condition (n = 12) or under the saccade-and-reach condition (n = 45), while the remaining 49 neurons were equally active in both conditions. 3. By contrast, most (97%) of the 109 neurons in the FEF exhibited approximately equal activity in relation to saccades under the two conditions. 4. The present results suggest the possibility that SEF neurons, at least in part, are involved in signaling whether the motor task is oculomotor or combined eye-arm movements, whereas FEF neurons are mostly related to oculomotor control.

The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey

1987 ◽  
Vol 57 (4) ◽  
pp. 1033-1049 ◽  
Author(s):  
P. H. Schiller ◽  
J. H. Sandell ◽  
J. H. Maunsell
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Short Latency ◽  
The Other ◽  
Frontal Eye Field ◽  
Express Saccades ◽  
Unimodal Distribution ◽  
Other Hand ◽  
Eye Field ◽  
The Mean

Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS)

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