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

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)

1992 ◽  
Vol 68 (6) ◽  
pp. 1967-1985 ◽  
Author(s):  
M. A. Segraves

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)


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.


1998 ◽  
Vol 80 (6) ◽  
pp. 3331-3335 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz

Sommer, Marc A. and Robert H. Wurtz. Frontal eye field neurons orthodromically activated from the superior colliculus. J. Neurophysiol. 80: 3331–3333, 1998. Anatomical studies have shown that the frontal eye field (FEF) and superior colliculus (SC) of monkeys are reciprocally connected, and a physiological study described the signals sent from the FEF to the SC. Nothing is known, however, about the signals sent from the SC to the FEF. We physiologically identified and characterized FEF neurons that are likely to receive input from the SC. Fifty-two FEF neurons were found that were orthodromically activated by electrical stimulation of the intermediate or deeper layers of the SC. All the neurons that we tested ( n = 34) discharged in response to visual stimulation. One-half also discharged when saccadic eye movements were made. This provides the first direct evidence that the ascending pathway from SC to FEF might carry visual- and saccade-related signals. Our findings support a hypothesis that the SC and the FEF interact bidirectionally during the events leading up to saccade generation.


2001 ◽  
Vol 85 (4) ◽  
pp. 1673-1685 ◽  
Author(s):  
Marc A. Sommer ◽  
Robert H. Wurtz

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.


2000 ◽  
Vol 83 (1) ◽  
pp. 625-629 ◽  
Author(s):  
Stefano Ferraina ◽  
Martin Paré ◽  
Robert H. Wurtz

Information about depth is necessary to generate saccades to visual stimuli located in three-dimensional space. To determine whether monkey frontal eye field (FEF) neurons play a role in the visuo-motor processes underlying this behavior, we studied their visual responses to stimuli at different disparities. Disparity sensitivity was tested from 3° of crossed disparity (near) to 3° degrees of uncrossed disparity (far). The responses of about two thirds of FEF visual and visuo-movement neurons were sensitive to disparity and showed a broad tuning in depth for near or far disparities. Early phasic and late tonic visual responses often displayed different disparity sensitivity. These findings provide evidence of depth-related signals in FEF and suggest a role for FEF in the control of disconjugate as well as conjugate eye movements.


2008 ◽  
Vol 100 (2) ◽  
pp. 796-814 ◽  
Author(s):  
Xinmiao Peng ◽  
Margaret E. Sereno ◽  
Amanda K. Silva ◽  
Sidney R. Lehky ◽  
Anne B. Sereno

Previous neurophysiological studies of the frontal eye field (FEF) in monkeys have focused on its role in saccade target selection and gaze shift control. It has been argued that FEF neurons indicate the locations of behaviorally significant visual stimuli and are not inherently sensitive to specific features of the visual stimuli per se. Here, for the first time, we directly examined single cell responses to simple, two-dimensional shapes and found that shape selectivity exists in a substantial number of FEF cells during a passive fixation task or during the sample, delay (memory), and eye movement periods in a delayed match to sample (DMTS) task. Our data demonstrate that FEF neurons show sensory and mnemonic selectivity for stimulus shape features whether or not they are behaviorally significant for the task at hand. We also investigated the extent and localization of activation in the FEF using a variety of shape stimuli defined by static or dynamic cues employing functional magentic resonance imaging (fMRI) in anesthetized and paralyzed monkeys. Our fMRI results support the electrophysiological findings by showing significant FEF activation for a variety of shape stimuli and cues in the absence of attentional and motor processing. This shape selectivity in FEF is comparable to previous reports in the ventral pathway, inviting a reconsideration of the functional organization of the visual system.


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)


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