Rostrocaudal Distinction of the Dorsal Premotor Area Based on Oculomotor Involvement

To investigate functional differences between the rostral and caudal parts of the dorsal premotor cortex (PMd), we first examined the effects of intracortical microstimulation (ICMS) while monkeys were performing oculomotor and limb motor tasks or while they were at rest. We found that saccades were evoked from the rostral part (PMdr) whereas ICMS in the caudal part (PMdc) predominantly produced forelimb or body movements. Subsequently, we examined neuronal activity in relation to the performance of visually cued and memorized saccades while monkeys reached an arm toward a visual target. We found that roughly equal numbers of PMdr neurons were active during performance of the oculomotor and limb motor tasks. In contrast, the majority of PMdc neurons were related preferentially to arm movements and not to saccades. In the subsequent analysis, we found that the oculomotor effects evoked in the PMdr differ from the effects evoked in either the frontal eye field (FEF) or supplementary eye field (SEF). These findings suggest that the PMdr is involved in oculomotor as well as limb motor behavior. However, the oculomotor involvement of the PMdr seems to have a functional aspect different from that operating in the FEF and SEF.

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Distribution of Eye- and Arm-Movement-Related Neuronal Activity in the SEF and in the SMA and Pre-SMA of Monkeys

Journal of Neurophysiology ◽

10.1152/jn.00867.2001 ◽

2002 ◽

Vol 87 (4) ◽

pp. 2158-2166 ◽

Cited By ~ 68

Author(s):

Naotaka Fujii ◽

Hajime Mushiake ◽

Jun Tanji

Keyword(s):

Neuronal Activity ◽

Supplementary Motor Area ◽

Motor Behavior ◽

Visual Target ◽

Arm Movement ◽

Context Dependency ◽

Motor Area ◽

Motor Tasks ◽

Supplementary Eye Field ◽

Eye Field

We analyzed neuronal activity in the supplementary eye field (SEF), supplementary motor area (SMA), and presupplementary motor area (pre-SMA) during the performance of three motor tasks: capturing a visual target with a saccade, reaching one arm to a target while gazing at a visual fixation point, or capturing a target with a saccade and arm-reach together. Our data demonstrated that each area was involved in controlling the arm and eye movements in a different manner. Saccade-related neurons were found mainly in the SEF. In contrast, arm-movement-related neurons were found primarily in the SMA and pre-SMA. In addition, we found that the activity of both arm-movement- and saccade-related neurons differed depending on the presence or absence of an accompanying saccade or arm movement. Such context dependency was found in all three areas. We also discovered that activity preceding eye or arm movement alone, and eye and arm movement combined, appeared more often in the pre-SMA and SEF, suggesting their involvement in effector-independent aspects of motor behavior. Subsequent analysis revealed that the laterality of arm representation differed in the three areas: it was predominantly contralateral in the SMA but largely bilateral in the pre-SMA and SEF.

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Supplementary eye field contrasted with the frontal eye field during acquisition of conditional oculomotor associations

Journal of Neurophysiology ◽

10.1152/jn.1995.73.3.1122 ◽

1995 ◽

Vol 73 (3) ◽

pp. 1122-1134 ◽

Cited By ~ 107

Author(s):

L. L. Chen ◽

S. P. Wise

Keyword(s):

Primary Motor Cortex ◽

Premotor Cortex ◽

Familiar Stimulus ◽

Frontal Eye Field ◽

Supplementary Eye Field ◽

Significant Difference ◽

Eye Field ◽

Familiar Stimuli ◽

Oculomotor Learning ◽

Selective Activity

1. The companion paper reported that a substantial proportion of cells in the supplementary eye field (SEF) of macaque monkeys show significant evolution of neuronal activity as subjects learn new and arbitrary stimulus-saccade associations. The purpose of the present study was to compare and contrast the activity of the SEF and the frontal eye field (FEF) during such conditional oculomotor learning. 2. In both SEF and FEF, we observed learning-dependent and learning-selective activity, defined as significant evolution of task-related activity as monkeys learned which of four saccades was instructed by a novel stimulus. By definition, in addition to changes as the monkeys learned the instructional significance of a novel instruction stimulus, learning-dependent activity also showed task-related modulation for trials instructed by familiar stimuli, whereas learning-selective activity did not. Of the 186 SEF neurons adequately tested, 81 (44%) showed one of these two categories of learning-related change. By contrast, of the 90 FEF neurons adequately tested, only 14 (16%) showed similar properties. This difference was highly statistically significant (chi 2 = 21.1; P < 0.001). 3. We also observed persistent differences in activity for trials with familiar versus novel instruction stimuli, which we termed learning-static effects. In some cases, the learning-static effect coexisted with learning-dependent or learning-selective changes in activity, although in others it did not. In the former cases, activity changed systematically during learning, but reached a level that differed from that for familiar stimuli instructing the same saccade. In the latter cases, the activity did not change significantly as the monkey learned new conditional oculomotor associations, but did show a significant difference depending upon whether a novel or familiar stimulus instructed a given saccade. Overall, 66 of 186 (35%) cells in the SEF and 17 of 90 (19%) cells in the FEF showed learning-static effects in one or more task periods. This difference was statistically significant (chi 2 = 7.9; P < 0.005). 4. The significant difference in the properties of SEF and FEF cells suggests a functional dissociation of the two areas during conditional oculomotor learning. In this respect, the FEF resembles the primary motor cortex, whereas the SEF resembles the premotor cortex.

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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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Evidence for a supplementary eye field

Journal of Neurophysiology ◽

10.1152/jn.1987.57.1.179 ◽

1987 ◽

Vol 57 (1) ◽

pp. 179-200 ◽

Cited By ~ 369

Author(s):

J. Schlag ◽

M. Schlag-Rey

Keyword(s):

Unit Activity ◽

Cortical Neurons ◽

Cortical Area ◽

Head Movements ◽

Frontal Eye Field ◽

Unit Recording ◽

Electrical Microstimulation ◽

Preferred Direction ◽

Supplementary Eye Field ◽

Eye Field

Electrical microstimulation and unit recording were performed in dorsomedial frontal cortex of four alert monkeys to identify an oculomotor area whose existence had been postulated rostral to the supplementary motor area. Contraversive saccades were evoked from 129 sites by stimulation. Threshold currents were lower than 20 microA in half the tests. Response latencies were usually longer than 50 ms (minimum: 30 ms). Eye movements were occasionally accompanied by blinks, ear, or neck movements. The cortical area yielding these movements was at the superior edge of the frontal lobe just rostral to the region from which limb movements could be elicited. Depending on the site of stimulation, saccades varied between two extremes: from having rather uniform direction and size, to converging toward a goal defined in space. The transition between these extremes was gradual with no evidence that these two types were fundamentally different. From surface to depth of cortex, direction and amplitude of evoked saccades were similar or changed progressively. No clear systematization was found depending on location along rostrocaudal or mediolateral axes of the cortex. The dorsomedial oculomotor area mapped was approximately 7 mm long and 6 mm wide. Combined eye and head movements were elicited from one of ten sites stimulated when the head was unrestrained. In the other nine cases, saccades were not accompanied by head rotation, even when higher currents or longer stimulus trains were applied. Presaccadic unit activity was recorded from 62 cells. Each of these cells had a preferred direction that corresponded to the direction of the movement evoked by local microstimulation. Presaccadic activity occurred with self-initiated as well as visually triggered saccades. It often led self-initiated saccades by more than 300 ms. Recordings made with the head free showed that the firing could not be interpreted as due to attempted head movements. Many dorsomedial cortical neurons responded to photic stimuli, either phasically or tonically. Sustained responses (activation or inhibition) were observed during target fixation. Twenty-one presaccadic units showed tonic changes of activity with fixation. Justification is given for considering the cortical area studied as a supplementary eye field. It shares many common properties with the arcuate frontal eye field. Differences noted in this study include: longer latency of response to electrical stimulation, possibility to evoke saccades converging apparently toward a goal, and long-lead unit activity with spontaneous saccades.

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Role of Supplementary Eye Field in Saccade Initiation: Executive, Not Direct, Control

Journal of Neurophysiology ◽

10.1152/jn.00221.2009 ◽

2010 ◽

Vol 103 (2) ◽

pp. 801-816 ◽

Cited By ~ 80

Author(s):

Veit Stuphorn ◽

Joshua W. Brown ◽

Jeffrey D. Schall

Keyword(s):

Discharge Rate ◽

Stop Signal ◽

Stop Signal Task ◽

Frontal Eye Field ◽

Signal Trial ◽

Visually Guided ◽

Supplementary Eye Field ◽

Task Requirements ◽

Gaze Holding ◽

Eye Field

The goal of this study was to determine whether the activity of neurons in the supplementary eye field (SEF) is sufficient to control saccade initiation in macaque monkeys performing a saccade countermanding (stop signal) task. As previously observed, many neurons in the SEF increase the discharge rate before saccade initiation. However, when saccades are canceled in response to a stop signal, effectively no neurons with presaccadic activity display discharge rate modulation early enough to contribute to saccade cancellation. Moreover, SEF neurons do not exhibit a specific threshold discharge rate that could trigger saccade initiation. Yet, we observed more subtle relations between SEF activation and saccade production. The activity of numerous SEF neurons was correlated with response time and varied with sequential adjustments in response latency. Trials in which monkeys canceled or produced a saccade in a stop signal trial were distinguished by a modest difference in discharge rate of these SEF neurons before stop signal or target presentation. These findings indicate that neurons in the SEF, in contrast to counterparts in the frontal eye field and superior colliculus, do not contribute directly and immediately to the initiation of visually guided saccades. However the SEF may proactively regulate saccade production by biasing the balance between gaze-holding and gaze-shifting based on prior performance and anticipated task requirements.

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Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis

Experimental Brain Research ◽

10.1007/bf00241967 ◽

1995 ◽

Vol 103 (1) ◽

Cited By ~ 126

Author(s):

DougP. Hanes ◽

KirkG. Thompson ◽

JeffreyD. Schall

Keyword(s):

Spike Train ◽

Frontal Eye Field ◽

Spike Train Analysis ◽

Supplementary Eye Field ◽

Eye Field ◽

Relationship Of

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Corpus callosum connections of subdivisions of motor and premotor cortex, and frontal eye field in a prosimian primate,Otolemur garnetti

The Journal of Comparative Neurology ◽

10.1002/cne.21706 ◽

2008 ◽

Vol 508 (4) ◽

pp. 565-578 ◽

Cited By ~ 21

Author(s):

Pei-Chun Fang ◽

Iwona Stepniewska ◽

Jon H. Kaas

Keyword(s):

Corpus Callosum ◽

Premotor Cortex ◽

Frontal Eye Field ◽

Eye Field

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Neuronal Activity in the Frontal Eye Field and the Ventral Premotor Cortex around Reaching by Eyes and/or Hand

Neuroscience Research ◽

10.1016/j.neures.2010.07.084 ◽

2010 ◽

Vol 68 ◽

pp. e72

Author(s):

Kiyoshi Kurata

Keyword(s):

Neuronal Activity ◽

Premotor Cortex ◽

Frontal Eye Field ◽

Ventral Premotor Cortex ◽

Eye Field

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Suppression of Task-Related Saccades by Electrical Stimulation in the Primate's Frontal Eye Field

Journal of Neurophysiology ◽

10.1152/jn.1997.77.5.2252 ◽

1997 ◽

Vol 77 (5) ◽

pp. 2252-2267 ◽

Cited By ~ 87

Author(s):

Douglas D. Burman ◽

Charles J. Bruce

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Frontal Lobe ◽

Premotor Cortex ◽

Saccadic Eye Movements ◽

Association Cortex ◽

Frontal Eye Field ◽

Visually Guided ◽

Low Intensity ◽

Eye Field

Burman, Douglas D. and Charles J. Bruce. Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J. Neurophysiol. 77: 2252–2267, 1997. Patients with frontal lobe damage have difficulty suppressing reflexive saccades to salient visual stimuli, indicating that frontal lobe neocortex helps to suppress saccades as well as to produce them. In the present study, a role for the frontal eye field (FEF) in suppressing saccades was demonstrated in macaque monkeys by application of intracortical microstimulation during the performance of a visually guided saccade task, a memory prosaccade task, and a memory antisaccade task. A train of low-intensity (20–50 μA) electrical pulses was applied simultaneously with the disappearance of a central fixation target, which was always the cue to initiate a saccade. Trials with and without stimulation were compared, and significantly longer saccade latencies on stimulation trials were considered evidence of suppression. Low-intensity stimulation suppressed task-related saccades at 30 of 77 sites tested. In many cases saccades were suppressed throughout the microstimulation period (usually 450 ms) and then executed shortly after the train ended. Memory-guided saccades were most dramatically suppressed and were often rendered hypometric, whereas visually guided saccades were less severely suppressed by stimulation. At 18 FEF sites, the suppression of saccades was the only observable effect of electrical stimulation. Contraversive saccades were usually more strongly suppressed than ipsiversive ones, and cells recorded at such purely suppressive sites commonly had either foveal receptive fields or postsaccadic responses. At 12 other FEF sites at which saccadic eye movements were elicited at low thresholds, task-related saccades whose vectors differed from that of the electrically elicited saccade were suppressed by electrical stimulation. Such suppression at saccade sites was observed even with currents below the threshold for eliciting saccades. Pure suppression sites tended to be located near or in the fundus, deeper in the anterior bank of the arcuate than elicited saccade sites. Stimulation in the prefrontal association cortex anterior to FEF did not suppress saccades, nor did stimulation in premotor cortex posterior to FEF. These findings indicate that the primate FEF can help orchestrate saccadic eye movements by suppressing inappropriate saccade vectors as well as by selecting, specifying, and triggering appropriate saccades. We hypothesize that saccades could be suppressed both through local FEF interactions and through FEF projections to subcortical regions involved in maintaining fixation.

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