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

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.

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

Journal of Neurophysiology ◽

10.1152/jn.1996.75.5.2187 ◽

1996 ◽

Vol 75 (5) ◽

pp. 2187-2191 ◽

Cited By ~ 68

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.

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The effects of reversible inactivation of Frontal Eye Field and Superior Colliculus on saccade target selection

Journal of Vision ◽

10.1167/3.9.694 ◽

2010 ◽

Vol 3 (9) ◽

pp. 694-694

Author(s):

R. M McPeek ◽

E. L Keller

Keyword(s):

Superior Colliculus ◽

Target Selection ◽

Saccade Target ◽

Frontal Eye Field ◽

Reversible Inactivation ◽

Eye Field

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Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys

Journal of Neurophysiology ◽

10.1152/jn.1996.76.4.2754 ◽

1996 ◽

Vol 76 (4) ◽

pp. 2754-2771 ◽

Cited By ~ 90

Author(s):

J. R. Tian ◽

J. C. Lynch

Keyword(s):

Eye Movement ◽

Frontal Eye Field ◽

Adjacent Area ◽

Saccadic Eye Movement ◽

Temporal Area ◽

Macaque Monkeys ◽

Supplementary Eye Field ◽

Eye Field ◽

Cebus Monkeys ◽

The One

1. The locations and connections of the smooth and saccadic eye movement subregions of the frontal eye field (FEFsem and FEFsac, respectively) were investigated in seven hemispheres of five Cebus monkeys. The supplementary eye field was also mapped in seven hemispheres and the hand/arm regions of the dorsal and ventral premotor areas were localized in five hemispheres. Monkeys were immobilized during experiments with Telazol, a dissociative anesthetic agent that has no significant effect on microstimulation-induced eye movement parameters (threshold, velocity, and duration). The functional subregions were defined with the use of low threshold intracortical microstimulation (current < or = 50 microA). Then different retrogradely transported fluorescent tracers were placed into these functionally defined regions. 2. The FEFsac in Cebus monkey is in the same location as the one in macaque monkeys, which is in Walker's areas 8a and 45. The FEFsem is located in the posterior shoulder of the superior arcuate sulcus near its medial tip and is therefore more accessible for tracer injections than the one in macaque monkeys. This subregion is within cytoarchitectural area 6a beta, which is distinct from the adjacent area 6a alpha (dorsal premotor area). This smooth eye movement subregion may be comparable with the one in macaque monkeys. 3. Cortical connection patterns of the FEFsac and FEFsem are similar and parallel to each other. The predominant neural input to these two subregions originates in other cortical eye fields, including the supplementary eye field, the parietal eye field, the middle superior temporal area, and the principal sulcus region. These cortical eye fields each contain two separate, almost non-overlapping, distributions of labeled neurons that project to the corresponding frontal eye field (FEF) subregions. These results suggest that there may be similar, but relatively independent, parallel corticocortical networks to control pursuit and saccadic eye movements. The weak connections between the middle temporal area (MT) and FEF suggest that the MT may not provide the major source of visuomotion inputs to the FEF, but that it rather plays a role in mediating visual information that is relayed from the striate and extrastriate cortices via MT to the parietal cortex and then to the FEF. In addition to the well-known neural connections between the lateral intraparietal area and the FEF, additional parietal projections have been demonstrated from the dorsomedial visual area area specifically to the FEFsac and from area 7m specifically to the FEFsem.

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Polar-angle representation of saccadic eye movements in human superior colliculus

10.1101/169003 ◽

2017 ◽

Author(s):

Ricky R Savjani ◽

Elizabeth Halfen ◽

Jung Hwan Kim ◽

David Ress

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Eye Movement ◽

Visual Stimulation ◽

Polar Angle ◽

Saccadic Eye Movements ◽

List Type ◽

Saccadic Eye Movement ◽

Intermediate Layers ◽

Retinotopic Organization

SummaryThe superior colliculus (SC) is a layered midbrain structure involved in directing eye movements and coordinating visual attention. Electrical stimulation and neuronal recordings in the intermediate layers of monkey SC have shown a retinotopic organization for the mediation of saccadic eye-movements. However, in human SC the topography of saccades is unknown. Here, a novel experimental paradigm and highresolution (1.2-mm) functional magnetic resonance imaging methods were used to measure activity evoked by saccadic eye movements within SC. Results provide three critical observations about the topography of the human SC: (1) saccades along the superior-inferior visual axis are mapped across the medial-lateral anatomy of the SC; (2) the saccadic eye-movement representation is in register with the retinotopic organization of visual stimulation; and (3) activity evoked by saccades occurs deeper within SC than that evoked by visual stimulation. These approaches lay the foundation for studying the organization of human subcortical eye-movement mechanisms.HighlightsHigh-resolution functional MRI enabled imaging from intermediate layers of human SCSaccades along superior-inferior visual field are mapped across medial-lateral SCSaccadic eye movement maps lie deeper in SC and are in alignment with retinotopyeTOC BlurbSavjani et al. found the polar angle representation of saccadic eye movements in human SC. The topography is similar in monkey SC, is in register with the retinotopic organization evoked by visual stimulation, but lies within deeper layers. These methods enable investigation of human subcortical eye-movement organization and visual function.

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Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements

Journal of Neurophysiology ◽

10.1152/jn.1995.73.5.1988 ◽

1995 ◽

Vol 73 (5) ◽

pp. 1988-2003 ◽

Cited By ~ 221

Author(s):

M. F. Walker ◽

E. J. Fitzgibbon ◽

M. E. Goldberg

Keyword(s):

Receptive Field ◽

Superior Colliculus ◽

Eye Movement ◽

Receptive Fields ◽

Saccadic Eye Movements ◽

Superficial Layer ◽

Saccade Target ◽

Visual Response ◽

Intermediate Layers ◽

Movement Field

1. Previous experiments have shown that visual neurons in the lateral intraparietal area (LIP) respond predictively to stimuli outside their classical receptive fields when an impending saccade will bring those stimuli into their receptive fields. Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demonstrate similar predictive responses in the monkey colliculus. 2. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. Each of these neurons did not respond to the stimulus unless an eye movement brought it into its receptive field, nor did it discharge in association with the eye movement unless it brought a stimulus into its receptive field. 4. These neurons were located in the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. 5. The predictive responses of most of these neurons (16/18, 89%) did not require that the stimulus be relevant to the monkey's rewarded behavior. However, for some neurons the predictive response was enhanced when the stimulus was the target of a subsequent saccade into the neuron's movement field. 6. Most neurons with predictive responses responded with a similar magnitude and latency to a continuous stimulus that remained on after the saccade, and to the same stimulus when it was only flashed for 50 ms coincident with the onset of the saccade target and thus never appeared within the cell's classical receptive field. 7. The visual response of neurons in the intermediate layers of the colliculus is suppressed during the saccade itself. Neurons that showed predictive responses began to discharge before the saccade, were suppressed during the saccade, and usually resumed discharging after the saccade. 8. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelevant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would not be brought into their receptive fields by a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

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Frontal Eye Field Sends Delay Activity Related to Movement, Memory, and Vision to the Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.2001.85.4.1673 ◽

2001 ◽

Vol 85 (4) ◽

pp. 1673-1685 ◽

Cited By ~ 105

Author(s):

Marc A. Sommer ◽

Robert H. Wurtz

Keyword(s):

Prefrontal Cortex ◽

Superior Colliculus ◽

Visual Memory ◽

Target Location ◽

Visual Stimulation ◽

Visual Space ◽

Frontal Eye Field ◽

Visual Response ◽

Eye Field ◽

Output Neurons

Many neurons within prefrontal cortex exhibit a tonic discharge between visual stimulation and motor response. This delay activity may contribute to movement, memory, and vision. We studied delay activity sent from the frontal eye field (FEF) in prefrontal cortex to the superior colliculus (SC). We evaluated whether this efferent delay activity was related to movement, memory, or vision, to establish its possible functions. Using antidromic stimulation, we identified 66 FEF neurons projecting to the SC and we recorded from them while monkeys performed a Go/Nogo task. Early in every trial, a monkey was instructed as to whether it would have to make a saccade (Go) or not (Nogo) to a target location, which permitted identification of delay activity related to movement. In half of the trials (memory trials), the target disappeared, which permitted identification of delay activity related to memory. In the remaining trials (visual trials), the target remained visible, which permitted identification of delay activity related to vision. We found that 77% (51/66) of the FEF output neurons had delay activity. In 53% (27/51) of these neurons, delay activity was modulated by Go/Nogo instructions. The modulation preceded saccades made into only part of the visual field, indicating that the modulation was movement-related. In some neurons, delay activity was modulated by Go/Nogo instructions in both memory and visual trials and seemed to represent where to move in general. In other neurons, delay activity was modulated by Go/Nogo instructions only in memory trials, which suggested that it was a correlate of working memory, or only in visual trials, which suggested that it was a correlate of visual attention. In 47% (24/51) of FEF output neurons, delay activity was unaffected by Go/Nogo instructions, which indicated that the activity was related to the visual stimulus. In some of these neurons, delay activity occurred in both memory and visual trials and seemed to represent a coordinate in visual space. In others, delay activity occurred only in memory trials and seemed to represent transient visual memory. In the remainder, delay activity occurred only in visual trials and seemed to be a tonic visual response. In conclusion, the FEF sends diverse delay activity signals related to movement, memory, and vision to the SC, where the signals may be used for saccade generation. Downstream transmission of various delay activity signals may be an important, general way in which the prefrontal cortex contributes to the control of movement.

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

10.1101/646604 ◽

2019 ◽

Cited By ~ 1

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.

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The frontal eye field provides the goal of saccadic eye movement

Experimental Brain Research ◽

10.1007/bf00228246 ◽

1992 ◽

Vol 89 (2) ◽

Cited By ~ 34

Author(s):

Paul Dassonville ◽

John Schlag ◽

Madeleine Schlag-Rey

Keyword(s):

Eye Movement ◽

Frontal Eye Field ◽

Saccadic Eye Movement ◽

Eye Field

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

Journal of Neurophysiology ◽

10.1152/jn.1992.67.4.1003 ◽

1992 ◽

Vol 67 (4) ◽

pp. 1003-1005 ◽

Cited By ~ 89

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.

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