Direction of saccadic and smooth eye movements induced by electrical stimulation of the human frontal eye field: effect of orbital position

The present study reports on the direction of saccadic and smooth eye movements, which were induced electrically from the human dorsolateral frontal cortex including the human frontal eye field (FEF). The eye position prior to stimulation was varied in order to examine its effect on induced eye movement direction. The five patients of the study underwent invasive presurgical evaluation for pharmacoresistant epilepsy. The present data show that the direction of electrically induced eye movements was always contralateral and either horizontal or oblique upward if the eye started from the primary position. The elicited direction was changed if the eyes started from an eccentric position. The frequency of oblique eye movements was increased and oblique downward responses were induced, which were not observed if the eye started from the primary position. This was found for saccades and, especially, for smooth eye movements. Head movements, which were almost exclusively induced with saccades, did not depend on initial orbital position. Four conclusions can be drawn. Firstly, saccades and smooth eye movements induced from the human dorsolateral cortex including the human FEF have the same directional bias. Secondly, the frequent upward responses and the absence of downward responses induced from the primary position suggests either a more numerous or a more superficial representation of neurons that code for the former direction. Thirdly, at some sites the direction of saccades and smooth eye movements varies depending on the initial orbital position. Since these directional changes were observed without changes in eye-head coordination, our data suggest that stimulation of the FEF might evoke goal-directed saccades or interferes with a resettable saccade integrator. Fourthly, human studies that investigate eye movements induced from the lateral frontal cortex need to control eye position prior to stimulation. Electronic Publication     

The frontal eye field provides the goal of saccadic eye movement

Summary Microstimulation of oculomotor regions in primate cortex normally evokes saccadic eye movements of stereotypic directions and amplitudes. The fixed-vector nature of the evoked movements is compatible with the creation of either an artificial retinal or motor error signal. However, when microstimulation is applied during an ongoing natural saccade, the starting eye position of the evoked movement differs from the eye position at stimulation onset (due to the latency of the evoked saccade). An analysis of the effect of this eye position discrepancy on the trajectory of the eventual evoked saccade can clarify the oculomotor role of the structure stimulated. The colliding saccade paradigm of microstimulation was used in the present study to investigate the type of signals conveyed by visual, visuomovement, and movement unit activities in the primate frontal eye field. Colliding saccades elicited from all sites were found to compensate for the portion of the initial movement occurring between stimulation and evoked movement onset, plus a portion of the initial movement occurring before stimulation. This finding suggests that activity in the frontal eye field encodes a retinotopic goal that is converted by a downstream structure into the vector of the eventual saccade. Offprint requests to: J. Schlag, Department of Anatomy and Cell Biology     

Attention-related neurons in the supplementary eye field of the macaque monkey

This study investigated whether the neuronal activity of a cortical area involved in the control of eye fixation is affected by the covert orienting of attention. We recorded single-unit activity from the supplementary eye field (SEF) of two macaque monkeys performing fixation and peripheral-attention tasks. Ninety-nine out of four hundred and fifteen cells were related to eye movements. The other neurons showed relationship with postural adjustments, and arm and ear movements. Fifty-five neurons were active during fixation (fixation cells) and 44 discharged in relation to saccades. The experiments reported here primarily concern the fixation cells. The activity of 64% (35/55) of fixation cells started with the onset of visual stimulus, before the visual input reached the fovea, and continued during active fixation. The activity of 27% (15/55) of fixation cells started with the onset of fixation. The activity of 9% (5/55) of fixation cells modified their timing trial by trial. Sixty-four percent of the fixation cells (35/55) were position-dependent, showing a selective spatial field of activity, 36% (20/55) were position-independent and characterized by a full spatial field. None of the 55 cells showed a visual receptive field. We tested both types of fixation cells by means of a peripheral attention task. When attention was oriented peripherally toward a target located in the selective spatial field, the cells discharged as if the gaze was held toward it. When attention was oriented peripherally toward a target, lying outside the selective spatial field, the cells were inactive as if gaze was held in that position. These results suggest that the supplementary eye field neurons may code for oriented attention in space and might be involved in the preparation of motor action. Preliminary results were presented at the 1994 ENA meeting in abstract form     

The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition

Physiological studies in monkeys have shown that the frontal eye field (FEF) is involved in the preparation and triggering of purposive saccades. However, several questions of FEF function remain unclear: the role of the FEF in visual short-term memory, its ability to update its spatial map and its role in reflexive saccade inhibition. We have addressed these issues in a patient with a small acute ischemic lesion whose location corresponded very accurately to the region of the left FEF according to the most recent cerebral blood flow studies. An initial study was conducted on days 7 and 8 after the stroke, i.e., before substantial recovery. A first group of paradigms (smooth pursuit, simple saccade tasks) was performed to assess FEF dysfunction. In a second group of paradigms, (1) visual short-term memory was tested by means of memory-guided saccade paradigms with short and long delays (1 and 7 s), (2) spatial updating abilities were tested by a double-step saccade task and two memory-guided saccade tasks in which the central fixation point was displaced during the memorization delay, and (3) reflexive saccade inhibition was tested by the antisaccade task. Results show that the FEF is involved in short-term memorization of the parameters of the forthcoming memory-guided saccade encoded in oculocentric coordinates. Normal results in the antisaccade task suggest that the FEF is not involved in reflexive saccade inhibition. Received: 26 January 1999 / Accepted: 3 June 1999     

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

The purpose of this study was to investigate the temporal relationship between presaccadic neuronal discharges in the frontal eye fields (FEF) and supplementary eye fields (SEF) and the initiation of saccadic eye movements in macaque. We utilized an analytical technique that could reliably identify periods of neuronal modulation in individual spike trains. By comparing the observed activity of neurons with the random Poisson distribution generated from the mean discharge rate during the trial period, the period during which neural activity was significantly elevated with a predetermined confidence level was identified in each spike train. In certain neurons, bursts of action potentials were identified by determining the period in each spike train in which the activation deviated most from the expected Poisson distribution. Using this method, we related these defined periods of modulation to saccade initiation in specific cell types recorded in FEF and SEF. Cells were recorded in SEF while monkeys made saccades to targets presented alone. Cells were recorded in FEF while monkeys made saccades to targets presented alone or with surrounding distractors. There were no significant differences in the time-course of activity of the population of FEF presaccadic movement cells prior to saccades generated to singly presented or distractor-embedded targets. The discharge of presaccadic movement cells in FEF and SEF could be subdivided quantitatively into an early prelude followed by a high-rate burst of activity that occurred at a consistent interval before saccade initiation. The time of burst onset relative to saccade onset in SEF presaccadic movement cells was earlier and more variable than in FEF presaccadic movement cells. The termination of activity of another population of SEF neurons, known as preparatory set cells, was time-locked to saccade initiation. In addition, the cessation of SEF preparatory set cell activity coincided precisely with the beginning of the burst of SEF presaccadic movement cells. This finding raises the possibility that SEF preparatory set cells may be involved in saccade initiation by regulating the activation of SEF presaccadic movement cells. These results demonstrate the utility of the Poisson spike train analysis to relate periods of neuronal modulation to behavior.     

Reversible inactivation of macaque frontal eye field

 The macaque frontal eye field (FEF) is involved in the generation of saccadic eye movements and fixations. To better understand the role of the FEF, we reversibly inactivated a portion of it while a monkey made saccades and fixations in response to visual stimuli. Lidocaine was infused into a FEF and neural inactivation was monitored with a nearby microelectrode. We used two saccadic tasks. In the delay task, a target was presented and then extinguished, but the monkey was not allowed to make a saccade to its location until a cue to move was given. In the step task, the monkey was allowed to look at a target as soon as it appeared. During FEF inactivation, monkeys were severely impaired at making saccades to locations of extinguished contralateral targets in the delay task. They were similarly impaired at making saccades to locations of contralateral targets in the step task if the target was flashed for ≤100 ms, such that it was gone before the saccade was initiated. Deficits included increases in saccadic latency, increases in saccadic error, and increases in the frequency of trials in which a saccade was not made. We varied the initial fixation location and found that the impairment specifically affected contraversive saccades rather than affecting all saccades made into head-centered contralateral space. Monkeys were impaired only slightly at making saccades to contralateral targets in the step task if the target duration was 1000 ms, such that the target was present during the saccade: latency increased, but increases in saccadic error were mild and increases in the frequency of trials in which a saccade was not made were insignificant. During FEF inactivation there usually was a direct correlation between the latency and the error of saccades made in response to contralateral targets. In the delay task, FEF inactivation increased the frequency of making premature saccades to ipsilateral targets. FEF inactivation had inconsistent and mild effects on saccadic peak velocity. FEF inactivation caused impairments in the ability to fixate lights steadily in contralateral space. FEF inactivation always caused an ipsiversive deviation of the eyes in darkness. In summary, our results suggest that the FEF plays major roles in (1) generating contraversive saccades to locations of extinguished or flashed targets, (2) maintaining contralateral fixations, and (3) suppressing inappropriate ipsiversive saccades. Received: 2 February 1996 / Accepted: 26 February 1997     

Functional properties of corticotectal neurons in the monkey's frontal 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)     

Unilateral ablation of the frontal eye field of the rat affects the beating field of ocular nystagmus

Spontaneous saccadic orientation and compensatory eye movements in response to optokinetic and vestibular velocity steps were studied in head-restrained, pigmented rats before and 1–2 weeks after unilateral ablation of the frontal eye field (FEF). One group of rats (n=5) received a deep lesion and another group of rats (n=4) received a superficial lesion of the left FEF. Postoperative response parameters such as the duration of slow buildup of eye velocity, the steady state velocity gain, the duration of optokinetic afternystagmus and of per- and postrotatory vestibular nystagmus were similar in the two groups of rats and did not differ from preoperative values measured in the same individuals. Superimposed upon these velocity components of nystagmus was a transient orienting response that expressed itself by a shift of the beating field of nystagmus in quick phase direction (gaze shift). The amplitudes of this gaze shift in quick phase direction were asymmetric in rats with a deep FEF lesion. Gaze shift amplitudes toward the side of the lesion were significantly enhanced and gaze shift amplitudes toward the intact side were significantly reduced. Similar asymmetries were observed in the distribution of spontaneous orienting movements of these rats in the light. Spontaneous saccadic eye movements of the same animals in darkness, however, were symmetric in amplitude to either side. These deficits suggest a partial sensory hemineglect after a deep unilateral lesion of the FEF and an involvement of this structure in the selective attention for targets in visual space. Thus the FEF orients the gaze at rest by means of saccades toward points of interest and during simulated circular locomotion by means of a shift of the beating field of nystagmus toward the visual sector that will be approached next.     

Eye movement disorders after frontal eye field lesions in humans

Eye movements were recorded electro-oculographically in three patients with a small ischemic lesion affecting the left frontal eye field (FEF) and in 12 control subjects. Reflexive visually guided saccades (gap and overlap tasks), antisaccades, predictive saccades, memory-guided saccades, smooth pursuit and optokinetic nystagmus (OKN) were studied in the three patients. Staircase saccades and double step saccades were also studied in one of the three patients. For both leftward and rightward saccades, latency in the overlap task (but not in the gap task) and that of correct antisaccades and of memory-guided saccades was significantly increased, compared with the results of controls. There was a significant decrease in the amplitude gain of all rightward saccades programmed using retinotopic coordinates (gap and overlap tasks, predictive and memory-guided saccades), whereas the amplitude gain of corresponding leftward saccades was preserved. Such an asymmetry between leftward and rightward saccades was significant. In the staircase paradigm as well as for the first saccade in the double step paradigm (with the use of retinotopic coordinates in both cases), the amplitude gain of rightward saccades was also significantly lower than that of leftward saccades. Moreover, in the double step paradigm, the amplitude gain of the first rightward saccade was significantly lower than that of the second rightward saccade (programmed using extraretinal signals), which was preserved. The percentage of errors in the antisaccade task did not differ significantly from that of normal subjects. In the predictive saccade paradigm, the percentage of predictive rightward saccades was significantly decreased. The left smooth pursuit gain for all tested velocities, the right smooth pursuit gain for higher velocities, and the left OKN gain were significantly decreased. The results show, for the first time in humans, that the FEF plays an important role in (1) the disengagement from central fixation, (2) the control of contralateral saccades programmed using retinotopic coordinates, (3) saccade prediction and (4) the control of smooth pursuit and OKN, mainly ipsilaterally. In contrast, the left FEF did not appear to be crucial for the control of the only type of saccades programmed using extraretinal signals studied here.     

Effects of frontal eye field stimulation upon activities of the lateral geniculate body of the cat

Summary Effects of electrical stimulation of the frontal eye field (FEF) upon activities of the lateral geniculate body (LG) were studied in encéphale isolé cats. In some experiments the effects were examined by recording field responses of the dorsal nucleus of LG (LGd) and the visual cortex (VC) to electrical stimulation of the optic chiasm (OX). Conditioning repetitive stimulation of FEF exerted no significant effects on the r₁ wave of LGd responses but had a facilitatory effect on the r₂ wave. FEF-induced facilitation of VC responses was prominent in the late postsynaptic components. These effects had latencies of 50–100 msec and durations of 200–500 msec. Transection of the midbrain showed that most of the FEF-effect was not mediated via the brainstem reticular formation.Extracellular unitary recordings were made from 125 neurons, of which 91 were LGd neurons, 23 neurons of the caudal part of the thalamic reticular nucleus (TRc) and 11 neurons of the ventral nucleus of LG (LGv). In 30 of 87 LGd relay neurons FEF stimuli increased response probabilities to OX stimuli and their spontaneous discharges. These FEF-facilitated LGd neurons were distinguished from the non-affected ones in that the former had longer OX-latencies than the latter. The FEF-facilitated neurons probably correspond to X neurons of LGd.In 17 TRc neurons the effects were inhibitory. Their time courses were similar to those of the facilitation in the LGd relay neurons. Seven LGv neurons received facilitatory effects from FEF. Among them 5 neurons showed short-latency (6.7–17 msec) responses to FEF single shocks.The FEF sites inducing conjugate lateral eye movements exerted stronger facilitatory effects than those inducing upward or centering eye movements did.It is suggested that the effects may subserve to cancel the inhibitory convergence onto X-cells just after saccadic eye movements so as to improve visual information transmission through LGd during the eye fixation.     

Gaze-related mimic word activates the frontal eye field and related network in the human brain: An fMRI study

This is an fMRI study demonstrating new evidence that a mimic word highly suggestive of an eye gaze, heard by the ear, significantly activates the frontal eye field (FEF), inferior frontal gyrus (IFG), dorsolateral premotor area (PMdr) and superior parietal lobule (SPL) connected with the frontal–parietal network. However, hearing a non-sense words that did not imply gaze under the same task does not activate this area in humans. We concluded that the FEF would be a critical area for generating/processing an active gaze, evoked by an onomatopoeia word that implied gaze closely associated with social skill. We suggest that the implied active gaze may depend on prefrontal–parietal interactions that modify cognitive gaze led by spatial visual attention associated with the SPL.     

Anatomical organization of the eye fields in the human and non-human primate frontal cortex

There are several eye fields in the primate frontal cortex. The number and location of these oculomotor control zones remain controversial, especially in the human brain. In the monkey, the frontal eye field (FEF) is located in the rostral bank of the arcuate sulcus at approximately the level of the posterior end of the sulcus principalis, the supplementary eye field (SEF) is located on the dorsomedial frontal cortex, and the cingulate eye field (CEF) in the dorsal bank of the cingulate sulcus. In the human frontal cortex, the location of the FEF varies depending on the method used, electrical stimulation or functional neuroimaging, to establish it. Some investigators have argued that the SEF is located on the medial wall of the frontal lobe but its presumed location remains controversial. The location of the CEF in the human brain is not known. The present article reviews electrophysiological and functional neuroimaging evidence regarding the location of these frontal oculomotor areas in the macaque monkey and human brains and, in light of new findings in the human brain, attempts to reconcile the differences observed in the location of these eye fields using the different techniques. Together, these data suggest the existence of at least four eye fields in the frontal cortex, i.e. the FEF, the SEF, the CEF, and a premotor eye field, and suggest that their anatomical relationships are preserved from monkey to human brain.     

On the gap effect for saccades evoked by electrical microstimulation of frontal eye fields in monkeys

To investigate the mechanisms of fixation disengagement and saccade initiation, we electrically stimulated the macaque frontal eye fields (FEF) while monkeys performed a visual fixation task. We tested the effect of introducing a temporal gap between fixation target offset and the onset of the electrical stimulus. We found that the duration of the gap had a pronounced effect on the probability of producing electrically evoked saccades at a given current level. The highest probability was found for gaps of 200 ms duration. There were also effects of gap duration on saccade latency and amplitude for most of the stimulation sites. The increase in saccade probability may be associated with lower current thresholds for evoking saccades.     

Input to the primate frontal eye field from the substantia nigra,superior colliculus,and dentate nucleus demonstrated by transneuronal transport

The purpose of these experiments was to study the subcortical input to the frontal eye field (FEF) and to determine which subcortical structures might project to the FEF via pathways that contain only a single intervening synapse. We used retrograde transneuronal transport of herpes simplex virus type 1 (HSV-1) to label second-order neurons that send information to the FEF of cebus monkeys. The saccade region of the FEF was identified physiologically using intracortical stimulation and then injected with a strain of HSV-1 known to be transported transneuronally in the retrograde direction. Retrograde transport of virus labeled neurons was observed in all the thalamic sites known to innervate the FEF. In addition, we found neurons labeled by transneuronal transport in three subcortical sites: the pars reticulata of the substantia nigra, the optic and intermediate gray layers of the superior colliculus, and a posterior portion of the dentate nucleus of the cerebellum. Each of these sites has been shown in prior studies to project to thalamic regions that innervate the FEF. Moreover, the neurons labeled through transneuronal transport were located in a subregion of each subcortical site that is known to be involved in oculomotor control. These observations demonstrate that signals from the substantia nigra, superior colliculus and dentate nucleus can have a significant influence on the output of the FEF.     

Inhibition of return and the human frontal eye fields

Inhibition of return (IOR) is a bias against reorienting attention to a previously cued location. In this study, using single-pulse transcranial magnetic stimulation (TMS), we show that the human frontal eye fields (FEF) play a crucial role in the generation of IOR. When TMS was applied over the right FEF at a time interval after a visual cue but shortly before the target, IOR was modulated in the hemifield ipsilateral to the TMS such that responses to a previously cued target were no longer slower than responses to uncued targets. Control TMS over the superior parietal lobule, as well as TMS of the FEF shortly after the cue but well before the target, had no influence on IOR. We further show that the FEF is involved with visual selection as responses to targets appearing contralateral to the TMS of the FEF, but not the control site, were delayed. These results suggest that the FEF produces IOR by biasing attention and eye movements away from a previously attended location and facilitating target detection at novel locations. Electronic Publication     

Visual and vergence eye movement-related responses of pursuit neurons in the caudal frontal eye fields to motion-in-depth stimuli

The caudal parts of the frontal eye fields (FEF) contain smooth-pursuit related neurons. Previous studies show that most FEF pursuit neurons carry visual signals in relation to frontal spot motion and discharge before the initiation of smooth-pursuit. It has also been demonstrated that most FEF pursuit neurons discharge during vergence tracking. Accurate vergence tracking requires information about target motion-in-depth. To further understand the role of the FEF in vergence tracking and to determine whether FEF pursuit neurons carry visual information about target motion-in-depth, we examined visual and vergence eye movement-related responses of FEF pursuit neurons to sinusoidal spot motion-in-depth. During vergence tracking, most FEF pursuit neurons exhibited both vergence eye position and velocity sensitivity. Phase shifts (re target velocity) of most neurons remained virtually constant up to 1.5 Hz. About half of FEF pursuit neurons exhibited visual responses to spot motion-in-depth. The preferred directions for visual responses of most neurons were similar to those during vergence tracking. Visual responses of most of these neurons exhibited sensitivity to the velocity of spot motion-in-depth. Phase shifts of most of the responding neurons remained virtually constant up to 2.0 Hz. Neurons that exhibited visual responses in-depth were mostly separate from neurons that showed visual responses in the frontal plane. To further examine whether FEF pursuit neurons could participate in initiation of vergence tracking, we examined latencies of neuronal responses with respect to vergence eye movements induced by step target motion-in-depth. About half of FEF pursuit neurons discharged before the onset of vergence eye movements with lead times longer than 20 ms. These results together with previous observations suggest that the caudal FEF carries visual signals appropriate to be converted into motor commands for pursuit in depth and frontal plane.     

Otolith inputs to pursuit neurons in the frontal eye fields of alert monkeys

The smooth-pursuit system must interact with the vestibular system to maintain the accuracy of eye movements in space during head movement. Maintenance of a target image on the foveae is required not only during head rotation which activates primarily semi-circular canals but also during head translation which activates otolith organs. The caudal part of the frontal eye fields (FEF) contains pursuit neurons. The majority of them receive vestibular inputs induced by whole body rotation. However, it has not been tested whether FEF pursuit neurons receive otolith inputs. In the present study, we first classified FEF pursuit neurons as belonging to one of three groups (vergence + fronto-parallel pursuit, vergence only, fronto-parallel pursuit only) based on their responses during fronto-parallel pursuit and mid-sagittal vergence-pursuit. We, then, tested discharge modulation of these neurons during fore/aft and/or right/left translation by passively moving the whole body sinusoidally at 0.33 Hz (±10 cm, peak velocity 19 cm/s; 0.04g). The majority of FEF pursuit neurons in all three groups were activated by fore/aft and right/left translation without a target in complete darkness. There was no correlation between the magnitude of discharge modulation and translational vestibulo-ocular reflex (VOR). Preferred directions of translational responses were distributed nearly evenly in front of the monkeys. Discharge modulation was also observed when a target moved together with whole body, requiring the monkeys to cancel the translational VOR. These results indicate that the discharge modulation of FEF pursuit neurons during whole body translation reflected otolith inputs.     

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation

The smooth pursuit system and the vestibular system interact to keep the retinal target image on the fovea by matching the eye velocity in space to target velocity during head and/or whole body movement. The caudal part of the frontal eye fields (FEF) in the fundus of the arcuate sulcus contains pursuit-related neurons and the majority of them respond to vestibular stimulation induced by whole body movement. To understand the role of FEF pursuit neurons in the interaction of vestibular and pursuit signals, we examined the latency and time course of discharge modulation to horizontal whole body rotation during different vestibular task conditions in head-stabilized monkeys. Pursuit neurons with horizontal preferred directions were selected, and they were classified either as gaze-velocity neurons or eye/head-velocity neurons based on the previous criteria. Responses of these neurons to whole body step-rotation at 20 degrees/s were examined during cancellation of the vestibulo-ocular reflex (VOR), VOR x1, and during chair steps in complete darkness without a target (VORd). The majority of pursuit neurons tested (approximately 70%) responded during VORd with latencies <80 ms. These initial responses were basically similar in the three vestibular task conditions. The shortest latency was 20 ms and the modal value was 24 ms. These responses were also similar between gaze-velocity neurons and eye/head-velocity neurons, indicating that the initial responses (<80 ms) were vestibular responses induced by semicircular canal inputs. During VOR cancellation and x1, discharge of the two groups of neurons diverged at approximately 90 ms following the onset of chair rotation, consistent with the latencies associated with smooth pursuit. The shortest latency to the onset of target motion during smooth pursuit was 80 ms and the modal value was 95 ms. The time course of discharge rate difference of the two groups of neurons between VOR cancellation and x1 was predicted by the discharge modulation associated with smooth pursuit. These results provide further support for the involvement of the caudal FEF in integration of vestibular inputs and pursuit signals.     

Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys

Summary The cortical mechanism of eye-movement control was investigated by recording single cell activity from the frontal eye field (FEF) in unanesthetized monkeys seated in a primate chair with head restrained. Two types of cells (I and II) were found. Type I neurons fired during voluntary saccades occurring in a given direction and during the fast phase of nystagmus. Cells of this type were silent during slow pursuit movement. Type II cells showed steady discharge when the eyes were oriented in a specific direction. These cells discharged also during smooth pursuit movements and the slow phase of nystagmus, provided that the eyes were moving across positions which would have been associated with neuronal activity had the eyes come to rest there. All of Type II and a few of Type I neurons were identified by antidromic response to stimulation of the cerebral peduncle. These results indicate that cortical neurons have patterns of discharge distinctly related either to saccadic or to pursuit movements, in line with the view that these two different types of eye movement are generated by distinct neuronal mechanisms.     

Electrically evoked saccades from the dorsomedial frontal cortex and frontal eye fields: a parametric evaluation reveals differences between areas

Using electrical stimulation to evoke saccades from the dorsomedial frontal cortex (DMFC) and frontal eye fields (FEF) of rhesus monkeys, parametric tests were conducted to compare the excitability properties of these regions. Pulse frequency and pulse current, pulse frequency and train duration, and pulse current and pulse duration were varied to determine threshold functions for a 50% probability of evoking a saccade. Also a wide range of frequencies were tested to evoke saccades, while holding all other parameters constant. For frequencies beyond 150 Hz, the probability of evoking saccades decreased for the DMFC, whereas for the FEF this probability remained at 100%. To evoke saccades readily from the DMFC, train durations of greater than 200 ms were needed; for the FEF, durations of less than 100 ms were sufficient. Even though the chronaxies of neurons residing in the DMFC and FEF were similar (ranging from 0.1 to 0.24 ms) significantly higher currents were required to evoke saccades from the DMFC than FEF. Thus the stimulation parameters that are optimal for evoking saccades from the DMFC differ from those that are optimal for evoking saccades from the FEF. Although the excitability of neurons in the DMFC and FEF are similar (due to similar chronaxies), we suggest that the density of saccade-relevant neurons is higher in the FEF than in the DMFC. Received: 14 January 1997 / Accepted: 2 June 1997