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

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.

2003 ◽  
Vol 90 (2) ◽  
pp. 1046-1062 ◽  
Author(s):  
Janet O. Helminski ◽  
Mark A. Segraves

Extracellular recordings were made simultaneously in the frontal eye field and superior colliculus in awake, behaving rhesus monkeys. Frontal eye field microstimulation was used to orthodromically activate the superior colliculus both to locate the depth of the strongest frontal eye field input to the superior colliculus and to identify superior colliculus neurons receiving direct frontal eye field input. The activity of orthodromically driven colliculus neurons was characterized during visuomotor tasks. The purpose of this study was to identify the types of superior colliculus neurons that receive excitatory frontal eye field input. We found that microstimulation of the frontal eye field did not activate the superficial layers of the superior colliculus but did activate the deeper layers. This pattern of activation coincided with the prevalence of visual versus saccade-related activity in the superficial and deep layers. A total of 83 orthodromically driven superior colliculus neurons were identified. Of these neurons, 93% ( n = 77) exhibited a burst of activity associated with the onset of the saccade, and 25% ( n = 21) exhibited prelude/build-up activity prior to the onset of a saccade. In addition, it was common to see some activity synchronized with the onset of a visual target (30%, n = 25). In single neurons, these activity profiles could be observed alone or in combination. Superior colliculus neurons that were exclusively visual, however, were not excited by frontal eye field stimulation. We compared the activity of superior colliculus neurons that received frontal eye field input to descriptions of saccade-related neurons made in earlier reports and found that the distribution of neuron types in the orthodromically driven population was similar to the distribution within the overall population. This suggests that the frontal eye field does not selectively influence a specific class of collicular neurons, but, instead has a direct influence on all preparatory, and saccade-related activity within the deep layers of the superior colliculus.


2009 ◽  
Vol 101 (6) ◽  
pp. 2934-2942 ◽  
Author(s):  
Rebecca A. Berman ◽  
Wilsaan M. Joiner ◽  
James Cavanaugh ◽  
Robert H. Wurtz

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.


2017 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil

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.


1987 ◽  
Vol 57 (4) ◽  
pp. 1033-1049 ◽  
Author(s):  
P. H. Schiller ◽  
J. H. Sandell ◽  
J. H. Maunsell

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)


2004 ◽  
Vol 91 (3) ◽  
pp. 1381-1402 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz

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.


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