Macaque Frontal Eye Field Input to Saccade-Related Neurons in the Superior Colliculus

2003 ◽  
Vol 90 (2) ◽  
pp. 1046-1062 ◽  
Author(s):  
Janet O. Helminski ◽  
Mark A. Segraves
Keyword(s):  
Superior Colliculus ◽  
Rhesus Monkeys ◽  
Frontal Eye Field ◽  
Specific Class ◽  
Related Activity ◽  
Deep Layers ◽  
Eye Field ◽  
Visuomotor Tasks ◽  
Superior Colliculus Neurons ◽  
Made In

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.

Functional properties of corticotectal neurons in the monkey's frontal eye field

1987 ◽  
Vol 58 (6) ◽  
pp. 1387-1419 ◽  
Author(s):  
M. A. Segraves ◽  
M. E. Goldberg
Keyword(s):  
Superior Colliculus ◽  
Visual Stimulation ◽  
Visual Stimuli ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Minimum Threshold ◽  
Strong Activity ◽  
Visual Component ◽  
Behavioral Tasks ◽  
Eye Field

1. We examined the activity of identified corticotectal neurons in the frontal eye field of awake behaving rhesus monkeys (Macaca mulatta). Corticotectal neurons were antidromically excited using biphasic current pulses passed through monopolar microelectrodes within the superior colliculus. The activity of single corticotectal neurons was studied while the monkey performed behavioral tasks designed to test the relation of the neuron's discharge to visual and oculomotor events. 2. Fifty-one frontal eye field corticotectal neurons were examined in two monkeys. Current thresholds for antidromic excitation ranged from 6 to 1,200 microA, with a mean of 330 microA. Antidromic latencies ranged from 1.2 to 6.0 ms, with a mean of 2.25 ms. 3. Fifty-three percent of the identified corticotectal neurons were classified as having movement-related activity. They had little or no response to visual stimuli, but very strong activity before both visually guided and memory-guided saccades. An additional 6% of corticotectal neurons had visuomovement activity, combining both a visual- and a saccade-related response. In each case, visuomovement neurons antidromically excited from the superior colliculus had movement-related activity, which was much stronger than the visual component of their response. 4. Twenty-two percent of the corticotectal neurons were primarily responsive to visual stimulation of the fovea. These included both neurons responding to the onset and neurons responding to the disappearance of a light flashed on the fovea. 5. The remaining 20% of the corticotectal neurons were a heterogeneous group whose activity could not be classified as movement, visuomovement or foveal. Their responses included postsaccadic, anticipatory, and reward-related activity, as well as activity modulated during certain directions of smooth-pursuit eye movements. One neuron was unresponsive during all of the behavioral tasks used. There were no corticotectal neurons that could be classified as primarily responsive to peripheral visual stimuli. 6. Histological reconstructions of electrode penetrations localized corticotectal neurons to layer V of the frontal eye field. For 22 corticotectal neurons tested, each had its minimum threshold for antidromic excitation within the superior colliculus, as judged by either histological confirmation, or surrounding neuronal responses recorded through the stimulation microelectrode. The majority of these neurons had minimum threshold sites within the intermediate layers, a few minimum threshold sites were located within the superficial or deep collicular layers.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Acute activation and inactivation of macaque frontal eye field with GABA-related drugs

1995 ◽  
Vol 74 (6) ◽  
pp. 2744-2748 ◽  
Author(s):  
E. C. Dias ◽  
M. Kiesau ◽  
M. A. Segraves
Keyword(s):  
Injection Site ◽  
Rhesus Monkeys ◽  
Frontal Eye Field ◽  
Surgical Removal ◽  
Gamma Aminobutyric Acid ◽  
Eye Field ◽  
Distribution Of Points ◽  
Direction Opposite ◽  
Voluntary Saccades

1. This project tests the behavioral effects of reversible activation and inactivation of sites within the frontal eye field of rhesus monkeys with microinjections of the gamma-aminobutyric acid (GABA)-related drugs bicuculline and muscimol. 2. Muscimol injections impaired the monkeys' ability to make both visually and memory-guided saccades to targets at the center of the area represented by the injection site. The latencies of saccades to targets in regions flanking the injection were increased. For memory-guided saccades, saccades in the direction opposite to that represented by the injection site, were made with shorter latency than controls and often occurred before the movement cue. 3. Bicuculline injections produced irrepressible saccades equivalent to the saccade vector represented by the injection site, often in a staircase of several closely spaced movements. 4. Both substances decreased the accuracy of fixation of a central light. The distribution of points of fixation on different trials was diffuse, and the angle of gaze tended to deviate towards the side of the injection. 5. The results of these acute injections are similiar to those observed in the superior colliculus and are much more substantial than the effects observed in the long term after surgical removal of the frontal eye field. The results of this study promote a central role for the frontal eye field in the generation of all voluntary saccades and in the control of fixation.

Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons

1992 ◽  
Vol 68 (6) ◽  
pp. 1967-1985 ◽  
Author(s):  
M. A. Segraves
Keyword(s):  
Electrical Stimulation ◽  
Visual Stimulation ◽  
Saccadic Eye Movements ◽  
Frontal Eye Field ◽  
Related Activity ◽  
Burst Neurons ◽  
Eye Field ◽  
Movement Field ◽  
Omnipause Neurons ◽  
Stimulation Of

1. This study identified neurons in the rhesus monkey's frontal eye field that projected to oculomotor regions of the pons and characterized the signals sent by these neurons from frontal eye field to pons. 2. In two behaving rhesus monkeys, frontal eye field neurons projecting to the pons were identified via antidromic excitation by a stimulating microelectrode whose tip was centered in or near the omnipause region of the pontine raphe. This stimulation site corresponded to the nucleus raphe interpositus (RIP). In addition, electrical stimulation of the frontal eye field was used to demonstrate the effects of frontal eye field input on neurons in the omnipause region and surrounding paramedian pontine reticular formation (PPRF). 3. Twenty-five corticopontine neurons were identified and characterized. Most frontal eye field neurons projecting to the pons were either movement neurons, firing in association with saccadic eye movements (48%), or foveal neurons responsive to visual stimulation of the fovea combined with activity related to fixation (28%). Corticopontine movement neurons fired before, during, and after saccades made within a restricted movement field. 4. The activity of identified corticopontine neurons was very similar to the activity of neurons antidromically excited from the superior colliculus where 59% had movement related activity, and 22% had foveal and fixation related activity. 5. High-intensity, short-duration electrical stimulation of the frontal eye field caused omnipause neurons to stop firing. The cessation in firing appeared to be immediate, within < or = 5 ms. The time that the omnipause neuron remained quiet depended on the intensity of the cortical stimulus and lasted up to 30 ms after a train of three stimulus pulses lasting a total of 6 ms at an intensity of 1,000 microA. Low-intensity, longer duration electrical stimuli (24 pulses, 75 microA, 70 ms) traditionally used to evoke saccades from the frontal eye field were also followed by a cessation in omnipause neuron firing, but only after a delay of approximately 30 ms. For these stimuli, the omnipause neuron resumed firing when the stimulus was turned off. 6. The same stimuli that caused omnipause neurons to stop firing excited burst neurons in the PPRF. The latency to excitation ranged from 4.2 to 9.8 ms, suggesting that there is at least one additional neuron between frontal eye field neurons and burst neurons in the PPRF. 7. The present study confirms and extends the results of previous work, with the use of retrograde and anterograde tracers, demonstrating direct projections from the frontal eye field to the pons.(ABSTRACT TRUNCATED AT 400 WORDS)

Glutamate-like immunoreactivity in the cat superior colliculus and visual cortex: Further evidence that glutamate is the neurotransmitter of the corticocollicular pathway

1997 ◽  
Vol 14 (1) ◽  
pp. 27-37 ◽  
Author(s):  
Chang-Jin Jeon ◽  
Michael K. Hartman ◽  
R. Ranney Mize
Keyword(s):  
Visual Cortex ◽  
Superior Colliculus ◽  
Optical Density ◽  
Retrograde Tracing ◽  
Biochemical Studies ◽  
Deep Layers ◽  
Dense Band ◽  
Cat Superior Colliculus ◽  
Made In ◽  
In Cells

AbstractBiochemical studies provide evidence that the pathway from visual cortex to the superior colliculus (SC) utilizes glutamate as a neurotransmitter. In the present study, we have used immunocytochemistry, visual cortex lesions, and retrograde tracing to show directly by anatomical methods that glutamate or a closely related analog is contained in corticocollicular neurons and terminals. A monoclonal antibody directed against gamma-L-glutamyl-L-glutamate (gamma glu glu) was used to localize glutamate-like immunoreactivity in both the superior colliculus (SC) and visual cortex (VC). Unilateral lesions of areas 17–18 were made in four cats to determine if gamma glu glu labeling was reduced in SC by this lesion. WGA-HRP was injected into the SC of 10 additional cats in order to determine if corticocollicular neurons were also labeled by the gamma glu glu antibody. A distinctive dense band of gamma glu glu immunoreactivity was found within the deep superficial gray and upper optic layers of SC where many corticotectal axons are known to terminate. Both fibers and cells were labeled within the band. Immunoreactivity was also found in cells and fibers throughout the deep layers of SC. Measures of total immunoreactivity (i.e. optical density) in the dense band were made in sections from the SC both ipsilateral to and contralateral to the lesions of areas 17–18. A consistent reduction in optical density was found in both the neuropil and in cells within the dense band of the SC ipsilateral to the lesion. A large percentage of all corticocollicular neurons that were retrogradely labeled by WGA-HRP also contained gamma glu glu. These results provide further evidence that the corticocollicular pathway in mammals is glutamatergic. The results also suggest that visual cortex ablation alters synthesis or storage of glutamate within postsynaptic SC neurons, presumably as a result of partial deafferentation.

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)

Responses of rabbit superior colliculus neurons to repeated visual stimuli

1975 ◽  
Vol 38 (2) ◽  
pp. 301-312 ◽  
Author(s):  
C. W. Oyster ◽  
E. S. Takahashi
Keyword(s):  
Superior Colliculus ◽  
Visual Stimulus ◽  
Decay Time ◽  
Spontaneous Recovery ◽  
Receptive Fields ◽  
Stimulus Frequency ◽  
Habituation Rate ◽  
Rate Dependent ◽  
Superior Colliculus Neurons ◽  
Made In

It has been shown that cells in the superficial layers of the superior colliculus exhibit response decrements when a visual stimulus is repeated. These response decrements have some of the properties associated with habituation, in particular, 1) spontaneous recovery and 2) habituation rate dependent on stimulus frequency. These observations have been made in two classes of neurons; direction-selective cells and so-called modified concentric cells. All of these neurons had small receptive fields and well-defined response properties. Some neurons in both the direction-selective and modified concentric groups do not show habituation. On the basis of area-threshold curves and other observations, it is suggested that those neurons which habituate possess strong inhibitory inputs which are weak or lacking in thenonhabituating neurons. This generalization leads to a hypothesis that inhibition in the superior colliculus has a long decay time and that a response to a given stimulus is affected by inhibition activated by preceding stimuli.

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