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1Department of Health Sciences and 2Department of Physiology, Hokkaido University School of Medicine, Sapporo 060-8638, Japan; and 3Department of Physiology and Biophysics and Washington National Primate Research Center, University of Washington, Seattle, Washington 98195
Submitted 24 November 2003; accepted in final form 3 January 2004
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ABSTRACT |
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1 Hz). These results, together with the robust vestibular-related discharge of most SEF neurons, show that the discharge of the majority of SEF pursuit-related neurons is quite distinct from that of caudal FEF neurons in identical task conditions, suggesting that the two areas are involved in different aspects of pursuit-vestibular interactions including predictive pursuit. |
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INTRODUCTION |
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; Keller and Heinen 1991; Leigh and Zee 1999; Lisberger et al. 1987).
The primate frontal cortex contains two areas related to smooth-pursuit: the caudal parts of the frontal eye fields (FEFs) in the fundus and posterior bank of the arcuate sulcus and the supplementary eye fields (SEFs) in the dorso-medial cortex (Leigh and Zee 1999; Tehovnik et al. 2000). Although potential differences in the roles of the two cortical areas in smooth-pursuit have been suggested (Tehovnik et al. 2000), published reports do not address certain questions regarding the unique discharge characteristics of SEF pursuit neurons (Heinen 1995; Heinen and Liu 1997). This is in contrast to the detailed studies on discharge characteristics of pursuit neurons in the caudal FEFs (Fukushima et al. 2000, 2002a,b; Gottlieb et al. 1994; MacAvoy et al. 1991; Tanaka and Fukushima 1998; Tanaka and Lisberger 2002a,b; Tian and Lynch 1996). Examples of such questions are as follows. First, do pursuit-related SEF neurons code parameters of tracking eye movements such as eye velocity? Second, because the pursuit system must maintain target images near the foveae during head or whole body movement, this system must interact with the vestibular system, which also has an important role in stabilizing visual images on the retina. It is still unknown whether the SEF participates in this interaction to match the eye-velocity-in-space (i.e., gaze velocity) to target velocity and/or codes gaze velocity during whole body movement. Because the vestibuloocular reflex (VOR) is referenced to the eye and not to the head and because the vestibular organs and eyeballs are separated in the head, the precise control of the gain of the VOR depends on the viewing distance of the target and is essential in primates for maintaining clear foveal images of targets close to the observer during movement (Paige and Tomko 1991; Wilson and Melvill Jones 1979). Third, although motor performance during predictive pursuit has been well documented (see review by Barnes 1993), efficient performance of smooth-pursuit requires prediction of target velocity. Indeed, the majority of caudal FEF pursuit neurons respond during tasks requiring visual prediction (Fukushima et al. 2002a), but it is not known whether SEF pursuit-related neurons carry similarly predictive target velocity information. Fourth, in daily life, targets move not only in fronto-parallel planes but also in depth. To track such target motion in the three-dimensional (3D) visual world, we must use not only conjugate smooth-pursuit to move both eyes in the same direction but also disconjugate vergence eye movements to move the two eyes in opposite directions. Although the vergence and smooth-pursuit systems are thought to have separate neural substrates (see Leigh and Zee 1999), recent studies indicate that the majority of caudal FEF pursuit neurons respond during vergence tracking as well as fronto-parallel pursuit, thus coding smooth eye movements in 3D space (Fukushima et al. 2002b). It is unknown whether SEF pursuit-related neurons respond during vergence tracking as well. Answers to these questions are necessary to understand the specific role of the SEF in pursuit eye movements. In this study, we therefore examined discharge properties of pursuit-related SEF neurons using identical tasks to those that we had used previously for caudal FEF pursuit neurons (Fukushima et al. 2000, 2002a,b). Although some neurons showing similar discharge characteristics are present in each area, the majority of pursuit-related neurons discharged differently. Some of these results have been presented in preliminary form (Fukushima et al. 2003a).
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METHODS |
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Three Japanese male monkeys (Macaca fuscata; C, M, and K; 4.5–6.0 kg) were used. One of them (monkey C) was used for caudal FEF recording in our previous study (Fukushima et al. 2002a). All experiments were performed in strict compliance with the Guide for the Care and Use of Laboratory Animals (DHEW Publication, NIH85-23, 1985). Specific protocols were approved by the Animal Care and Use Committee of Hokkaido University School of Medicine. Our methods for animal preparation, training, and recording were described in detail previously (Fukushima et al. 2000, 2002a,b). Briefly, each monkey was sedated with ketamine hydrochloride (5 mg/kg, im) and anesthetized with pentobarbital sodium (25 mg/kg, ip), and additional anesthesia (0.5–1.0% halothane mixed with 50% nitrous oxide and 50% oxygen) was administered as necessary. Under aseptic conditions, two head-holders were installed over the skull. A scleral search coil was implanted on one eye in one monkey (monkey C) and on both eyes in the other two (monkeys M and K) to record vertical and horizontal components of eye movement (Fuchs and Robinson 1966; Judge et al. 1980). Analgesics (pentazocine, 0.2 mg/kg) and antibiotics (penicillin G sodium, 20,000 U) were administered post-surgically to reduce pain and prevent infection.
Training procedures
Monkeys' heads were firmly restrained in the primate chair in the stereotaxic plane. The monkeys were trained using two different training booths; in one, they learned to track a target spot with smooth-pursuit eye movements during chair rotation, and in the other, they learned both smooth-pursuit and vergence (depth) tracking using a stereo spot. Unfortunately, the latter was not equipped for vestibular stimulation. Monkey C was trained only in the vestibular booth, and the two others (monkeys M and K) were trained in both booths. In the vestibular booth, the monkey chair was fixed to a turntable that had two degrees of freedom of motion. The interaural axis of the animals' head and its midpoint were brought close to the axis of pitch and yaw rotation, respectively. The chair was rotated sinusoidally in the pitch or yaw plane and also along oblique planes by combining pitch and yaw rotations. A tangent screen was positioned 75 cm in front of the animals' eyes and subtended 60 by 80° of visual angle. The monkeys were trained to track, in darkness, a laser spot (0.2° diam) back-projected onto the tangent screen for apple juice reward. The target moved sinusoidally in either vertical, horizontal, or two oblique directions at 45 and 135° polar angles (Fig. 1, bottom). Target position signals were first calibrated before a recording session by placing the target at known horizontal and vertical locations. Eye position signals were calibrated to the target by requiring the animal to fixate the stationary target or pursue a slowly moving one. In the monkeys with coils in both eyes, each eye was calibrated separately.
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; Kurkin et al. 2003). The target moved either in the frontal plane at 0.5 Hz (±5°) or depth from 65 to 10 cm apparent distance from the eyes in the midsagittal plane, requiring vergence eye movements of 10°. After the animals were trained, a recording chamber was installed over a hole cut in the skull at anterior 21–25 and lateral 1–5 to allow single cell recording in the dorsomedial cortical areas.
Recording procedures and behavioral paradigms
To identify the SEFs, we applied microstimulation (50–100 µA, 20–30 cathodal pulses, 0.2-µs duration, 333 Hz) to the dorso-medial frontal cortex while the monkeys fixated a stationary spot or performed smooth-pursuit. Low-threshold areas (
50 µA) for evoking eye movements were located, and we started searching for responsive neurons in those areas. In the vestibular booth, the target was moved obliquely (at 0.5 Hz, ±5 or 10°) in the frontal plane in association with chair rotation at the same frequency either in the yaw or pitch planes to search for neurons responding to target and/or vestibular stimulation. Once responsive single neurons were encountered, smooth-pursuit responses were tested in four planes (vertical, horizontal, and 2 oblique planes at 45° angles) to determine the preferred direction for pursuit activation without chair rotation. For many neurons, responses to a variety of frequencies were examined (0.1–1.0 Hz) to assess velocity sensitivity.
To examine the importance of a visual target during pursuit, the target was briefly (500–800 ms) extinguished ("blanked"). In particular, we blanked the visual target shortly before it changed direction during its sinusoidal movement. The monkeys were required to continue smooth-pursuit by reversing tracking direction in the absence of a visual target.
To dissociate eye movement in the orbit from that in space (i.e., gaze), we employed two tracking conditions (Lisberger and Fuchs 1978; Miles and Fuller 1975). In the VOR cancellation task, the monkeys tracked a target that moved in space with the same amplitude, direction, and phase as the chair. This condition required the monkeys to cancel the VOR so that the eyes remained virtually motionless in the orbit and gaze therefore moved with the chair. The driving signal for the laser spot on the tangent screen during VOR cancellation was obtained from a position signal derived from the chair motion. We calibrated target amplitudes during chair rotation by matching back-projected target motion to motion of another laser spot fixed to the chair at the monkey's eye level. The error between the two was <0.25°. In the second condition (VOR x 1), the target stayed stationary in space during chair rotation, and the monkeys were required to fixate the stationary spot, which required a perfect VOR and no gaze movement. Chair rotation was applied first in the plane closest to the smooth-pursuit preferred direction for individual neurons. For many neurons, yaw, pitch, or rotation in an oblique axis was tested. For some neurons, responses to a variety of frequencies were examined (0.1–1.0 Hz) for each of the tracking conditions. To examine vestibular responses, chair rotation was also applied in complete darkness without a target. The monkeys were not required to perform any particular task during this condition but were kept alert by occasional random drops of apple juice.
To examine whether SEF pursuit-related neurons receive retinal information about target movement, the stationary monkeys were rewarded for fixating a stationary laser spot (1st target, 0.2° diam) while a second laser spot (0.6° diam) moved sinusoidally along one of the four directions (Fukushima et al. 2000, 2002a). The first target was occasionally extinguished, whereas the second laser spot was presented continuously, and the monkeys were required to track the second spot. This procedure was used to insure that the monkeys attended to the second spot so that the second spot would not become behaviorally meaningless.
For our search stimulus in the stereo target booth, the target moved in oblique trajectories in virtual 3D space that were generated by combinations of the frontal and depth target motion at 0.5 Hz. Once responsive single neurons were encountered, responses were tested during smooth-pursuit in four frontal planes (vertical, horizontal, and 2 oblique planes along the 45° angles) to determine the preferred direction for pursuit activation and also during vergence tracking in the midsagittal plane. As before, visual responses were tested while the monkeys fixated this spot as it remained stationary while presenting another 0.6° spot moving in the frontal plane in different directions.
For some pursuit-related neurons, we examined the response to saccades as described previously for FEFs (Fukushima et al. 2000). The monkeys first fixated a stationary target at the center of the screen. After 1–2 s, the target jumped to a new position 5 or 10° away from the center, and the monkeys made a saccade to the visible target.
Data analysis
The data were analyzed off-line as previously described (Fukushima et al. 2000, 2002a,2002b). Cell discharge was discriminated with a dual time-amplitude window discriminator and digitized together with eye position, chair position, and target position signals at 500 Hz using a 16-bit A/D board. Eye position signals were differentiated by analog circuits (DC, 100 Hz; -12 dB/octave) to obtain eye velocity. All position signals except for eye positions were differentiated by software to obtain velocity. Gaze velocity was calculated as the sum of eye velocity and chair velocity. During smooth-pursuit and chair rotation in monkeys M and K, after confirming that the signals from the two eyes were virtually identical, we analyzed eye movement signals only from the left eye. Vergence eye movements were calculated as the difference between the horizontal components of the left and right eyes. The traces were displayed, and saccades were marked with a cursor on eye and gaze velocity traces and were removed using our interactive computer program (Fukushima et al. 2000). None of the SEF neurons analyzed exhibited clear bursts associated with saccades. Although two neurons exhibited pauses during saccades (see RESULTS), the pause was apparent in histograms but not in single trials. Therefore we did not manipulate spike data for purposes of analysis in any of the SEF neurons analyzed in this study.
Rasters and histograms were constructed by averaging between 10 and 30 cycles. Each cycle was divided into 64 equal bins together with averaged velocity. To quantify responses, a sine function was fitted to the cycle histograms of cell discharge, exclusive of the bins with zero spike rate, by means of a least-squared error algorithm. Responses that had a harmonic distortion (HD) of more than 50% or a signal-to-noise ratio (S/N) of <1.0 were discarded. S/N was defined as the amplitude of the fundamental frequency component divided by the amplitudes of the third through eighth harmonic, and HD was defined as the amplitude of the second harmonic divided by that of the fundamental (Wilson et al. 1984). The phase shift of the peak of the fitted function relative to (re) upward or rightward stimulus velocity or convergent target velocity was calculated as a difference in degrees. Sensitivity (re stimulus velocity) was calculated as the peak amplitude of the fundamental component fitted to the cycle histogram divided by the peak amplitude of the fitted stimulus velocity (i.e., target velocity for pursuit in the frontal and depth tracking and chair velocity for other tasks during chair rotation). Sensitivity 
0.10 spikes/s/° /s was taken as significant modulation. For responses with oblique stimulus directions, radial stimulus velocity was first calculated by the Pythagorean theorem—the square root of the sum of the squares of the vertical and horizontal components. Radial eye and gaze velocities were similarly calculated, and sensitivity (re stimulus velocity) was calculated by dividing amplitude of modulation of cell activity by the radial stimulus velocity. The phase shift of cell response with oblique preferred directions was calculated relative to the rightward component of eye, gaze, or stimulus velocity. Eye, gaze, and vergence velocity responses were calculated similarly using fitted functions after deleting saccades. Sensitivity (re eye velocity) of neuron responses was also calculated by dividing peak discharge modulation by peak eye velocity during pursuit or peak vergence eye velocity.
Preferred direction of a cell's response was estimated by the method of Krauzlis and Lisberger (1996) using a Gaussian function. Responses to eight polar directions along the four stimulus planes were examined. We estimated the Gaussian fit by plotting sensitivities (re stimulus velocity). Sensitivity values were plotted as positive for the increasing discharge and as negative for the direction to which discharge rate decreased, as previously described (Fukushima et al. 2000).
To analyze retinal image motion responses in the frontal plane, all traces were aligned on the motion of the second target. Traces that contained saccades or slow eye movement were removed since they were indicative of the monkeys' failure to fixate the stationary primary target, and only those traces with eye position changes of <1° during each cycle were analyzed, as previously described for FEFs (Fukushima et al. 2000, 2002a).
Histological procedures
Near the conclusion of the recording period in monkey C, the sites of pursuit-related cell activity were marked by iron deposits produced by passing positive current (10–15 µA for 60–100 s; 800–1,200 µCoulombs). This monkey had previously been used for recording in the caudal FEFs (Fukushima et al. 2002a). After recording was completed, the monkey was deeply anesthetized by pentobarbital sodium (50 mg/kg, ip). After histological fixation, the brain was cut in the coronal plane at 100 µm thickness on a freezing microtome. The sections were stained for cell bodies and fibers, and the locations of recording sites were verified microscopically. The two other monkeys are still being used for recording in the dorso-medial frontal cortex and caudal FEFs.
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RESULTS |
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; Heinen and Liu 1997), the responses of many of them varied even during the same task conditions. For example, they might be modulated during the initial two or three cycles and become almost completely unmodulated in the following cycles. Other neurons did not show any clear modulation initially, and variable magnitude modulation appeared during pursuit after several cycles. Of the 135 neurons, 25 showed some form of this type of inconsistent response during smooth-pursuit and 5 neurons during vergence tracking (Table 1, Inconsistent response). In our apparatus, we were unable to find the appropriate condition to evoke consistent responses in such neurons, and we did not analyze them any further. Sixteen neurons in the vestibular booth responded only to chair rotation but not during smooth pursuit (Table 1, Vestibular-only neurons). The remaining 89 neurons responded during smooth-pursuit and/or vergence tracking at least for 10 consecutive cycles at a search frequency of 0.5 Hz. Their discharge characteristics were analyzed further below during different task conditions, although the number of neurons tested varied between tasks due to the limitations of each apparatus and occasional degradation or loss of neural recordings.
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). The discharge characteristics of neurons during fronto-parallel smooth-pursuit were also similar in all monkeys irrespective of whether we used an actual target or a stereo target, so we combined the data for analysis. Response during smooth-pursuit
Consistent with previous studies (Heinen 1995; Heinen and Liu 1997), all pursuit directions are represented in the SEFs. Figure 1 shows representative discharge modulation for two neurons (Fig. 1, A and B) during pursuit in different directions (Fig. 1, a–d). The neuron shown in Fig. 1A had a leftward preferred direction with the peak discharge near peak target/eye velocity, while the neuron shown in Fig. 1B had a rightward preferred direction with the peak discharge lagging peak target/eye velocity. Their modulation was minimal during pursuit in the orthogonal directions (Fig. 1, Ac and Bc). Gaussian fits for sensitivity (re target velocity) confirm their preferred directions (Fig. 1, bottom). Figure 2A summarizes preferred activation directions during smooth-pursuit for all 89 neurons. Although neurons with horizontal preferred directions predominated, preferred directions for individual neurons were distributed across all directions.
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A striking result in this study is the robust vestibular response seen in the majority of pursuit-related SEF neurons. A total of 49 neurons were tested during both smooth-pursuit and whole body rotation. Of these, 33 neurons were modulated during smooth-pursuit, and the great majority (30/33) of them also responded during whole body rotation and VOR cancellation and/or VOR in complete darkness (Table 1). The remaining 16 neurons responded only during whole body rotation.
We classified pursuit-related neurons as "gaze velocity" if they met the following criteria that characterized the horizontal gaze velocity Purkinje cells of Lisberger and Fuchs (1978) (also Fukushima et al. 1999a, 2000; Miles and Fuller 1975; Shinmei et al. 2002): 1) modulation occurred for movements of the eye (smooth-pursuit) and the head (VOR cancellation) in the same direction (see METHODS), 2) modulation during one of these two tasks was less than twice that during the other, and 3) modulation during the VOR x 1 was less than that during VOR cancellation. An example of such a response is shown in Fig. 5. This neuron responded during leftward pursuit (Fig. 5A) and leftward whole body rotation during VOR cancellation, but showed little modulation during VOR x 1 (Fig. 5, B and C, respectively). Thus it satisfies the gaze velocity criteria. The existence of vestibular inputs is also supported by clear modulation during chair rotation in complete darkness (Fig. 5D).
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). However, the neuron shown in Fig. 6 cannot be classified simply as eye velocity, because its activity during VOR x 1 is almost two times larger than the response during smooth-pursuit, despite only a small difference in the accompanying eye velocity (eye velocity gains 1.0 and 0.88 during VOR x 1 and smooth-pursuit, respectively; Fig. 6, A vs. C). The clear discharge modulation during VOR in complete darkness further supports the existence of vestibular inputs (Fig. 6D). We therefore call these neurons pursuit plus vestibular neurons.
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2 test, P < 0.01, Table 1) (Fukushima et al. 2000). The majority of pursuit-related neurons in the SEFs responded during VOR cancellation during whole body rotation in several planes (15 of 21 neurons tested; 71%). For example, the neuron shown in Fig. 6 was modulated during VOR cancellation in the yaw (Fig. 6B), pitch (Fig. 6E), and oblique planes (data not shown), and also during whole body rotation in complete darkness in various planes (Fig. 6D), suggesting that these neurons receive vestibular inputs from more than one semicircular canal.
Most SEF pursuit-related neurons discharged during brief (500–800 ms) blanking of a tracking target. As illustrated in Fig. 6F, we extinguished the visual target shortly before it changed direction during sinusoidal movement. The monkeys were required to continue tracking by reversing tracking direction. Their responses during blanking were similar or even slightly increased compared with those without blanking (cf. Fig. 6, A and F). Ten neurons were examined; for 7 neurons, the target was blanked for 500 ms, and in 3 neurons, for 800 ms. The results for the two blanking periods were similar. Modulation during target blanking ranged from 61 to 119% (mean, 81.4%) of the modulation without blanking. Activity during predictive pursuit has been noted in the SEFs (Heinen and Liu 1997). The activity during target blanking may reflect such predictive activity (see DISCUSSION).
Comparison of discharge characteristics during pursuit-vestibular interactions
Figure 7 summarizes discharge characteristics of SEF neurons during smooth-pursuit, VOR cancellation, and x1 at 0.5 Hz (Fig. 7, A, C, and E). For comparison, Fig. 7 also shows discharge characteristics of caudal FEF neurons (Fig. 7, B, D, and F) during the same task conditions from our previous study (Fukushima et al. 2000). By definition, the gaze velocity response requires similar preferred directions and similar response magnitudes for smooth-pursuit and VOR cancellation. Although the majority of caudal FEF pursuit neurons show such responses (Fig. 7, B and D; points cluster near the dashed line of slope = 1.0), the great majority of SEF neurons did not (Fig. 7, A and C). If neurons coded eye velocity irrespective of vestibular inputs, the modulation during smooth-pursuit should have been correlated with modulation during VOR x 1, because both required eye movements with the identical magnitude. In caudal FEF eye velocity neurons (filled squares), significant correlation was observed between the two (Fig. 7F), but there was no clear correlation between the two for SEF pursuit plus vestibular neurons (Fig. 7E, filled circles). These comparisons suggest that the majority of SEF neurons do not code parameters of eye or gaze movement during pursuit-vestibular interactions.
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To examine whether SEF pursuit-related neurons respond to retinal image velocity of a target, we tested the responses of 34 neurons to a second spot moving sinusoidally while the monkeys fixated a stationary spot. Only 7 neurons (7/34 = 20%) showed visual responses (4/19 in the vestibular booth and 3/15 in the stereo booth; Table 1; Fig. 10C). Representative discharge is illustrated in Fig. 10A for a neuron with a leftward preferred direction (Fig. 10B). This neuron showed a visual response with a sensitivity of 0.38 (re velocity of 2nd spot) and peak modulation near peak target velocity of the second spot. The monkey fixated the stationary spot well (Fig. 10A: HE and VE), as indicated by the eye gain (re velocity of 2nd spot), which was only 0.03 during this task. During smooth-pursuit, pursuit eye gain was 0.84 and discharge sensitivity was 0.82 spikes/s/° /s (Fig. 10B). If the visual response to the second target during the fixation (Fig. 10A) had been induced by the small residual pursuit sensitivity, the modulation should have been 0.82 x (0.03/0.84) = 0.03 spikes/s /° /s. The fact that we actually observed modulation of 0.38 spikes/s/° /s suggests that the modulation of cell activity during this task cannot reflect residual eye velocity. Visual preferred directions of five of the seven neurons were similar to their pursuit preferred directions, while two neurons showed opposite visual preferred directions (Fig. 10D). The magnitude of the visual response was correlated with the magnitude of the smooth-pursuit response (n = 7, Fig. 10C). Table 1 compares the percentage of visual motion responding neurons in the SEFs and caudal FEFs from previous studies. The percentage is much smaller in the SEFs (7/34 = 20% vs. 21/40 = 53%, 2 test, P < 0.05) (Fukushima et al. 2000).
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The SEF also contained vergence-related neurons. A total of 56 neurons was tested both during smooth-pursuit in the frontal plane and vergence tracking in the midsagittal plane (see METHODS). Figure 11 illustrates the discharge of three representative neurons. The neuron shown in Fig. 11, A1 and A2, responded during horizontal pursuit but not during vergence tracking, whereas the neurons shown in Fig. 11, B1 and B2 and C1 and C2, responded during convergence and vertical pursuit and divergence and vertical pursuit, respectively. Of the 56 neurons examined, 35 responded only during smooth-pursuit (35/56 = 62%), 15 neurons responded both during smooth-pursuit and vergence tracking (15/56 = 27%), and the remaining 6 neurons responded only during vergence tracking (6/56 = 11%). Table 1 summarizes the percentage of vergence-related neurons. The percentage of smooth-pursuit + vergence-related neurons is significantly smaller than that in the caudal FEFs in our previous study (80/122 = 66%, 2 test, P < 0.05, Table 1) (Fukushima et al. 2000).
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To examine whether SEF neurons code vergence velocity, each neuron was tested at different frequencies of vergence target motion at a constant amplitude. Figure 13 plots phase (Fig. 13A) and sensitivity (re vergence target velocity; Fig. 13B) of individual neurons against frequency of vergence target motion. Phases are nearly constant over the range of frequencies. Sensitivity at the higher frequencies of 0.5 and 1.0 Hz was nearly constant (Fig. 13B, right). Indeed, amplitude of modulation plotted against peak vergence eye velocity indicates that many neurons increased discharge modulation as vergence eye velocity increased. This is confirmed in Fig. 13C, which also shows linear regressions for representative neurons. The mean vergence velocity sensitivity for 10 neurons was 0.34 spikes/s/° /s. These neurons code vergence eye velocity.
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We examined activity of 10 pursuit-related SEF neurons during saccades. The majority (8/10) exhibited no clear change in their discharge rate, and the remaining two neurons paused during saccades (Fig. 3C). Although we did not search for saccade-related neurons, in the tracks that we recorded pursuit-related neurons, we also occasionally encountered neurons that discharged bursts during saccades but that did not show clear modulation during smooth-pursuit, suggesting that saccade neurons are separate from pursuit-related neurons in the SEFs.
Recording location
Figure 14 illustrates the reconstructed recording locations (monkey C). We tracked 7 mm rostrocaudally and 7 mm medio-laterally on both sides of the frontal cortex. Pursuit-related neurons were found 1.5 mm rostrocaudally and 2 mm medio-laterally near the caudal edge of the arcuate sulcus (Fig. 14, A and B). They were recorded typically between 2 and 4 mm from the surface. Two other monkeys have not yet provided histology (see METHODS). However, as shown in Fig. 14B, in all monkeys, the stereotaxic anterior-posterior location of "SEF pursuit area" is very similar to the location of the caudal FEF pursuit area of the same monkeys. Therefore we are certain that recordings in these two monkeys also were from similar areas in the dorsomedial frontal cortex.
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DISCUSSION |
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, 2002a,b), they are in the minority; the discharge sensitivities of the majority of neurons in the two cortical areas are quite different. Smooth-pursuit areas in the SEFs
Schall (1991) and Heinen and Liu (1997) reported the location in the SEF where smooth-pursuit and/or eye position–related neurons were recorded. These areas correspond to the locations in the SEF where saccadic or smooth eye movements were induced by electrical stimulation (Fujii et al. 2002; Missal and Heinen 2001; Schall et al. 1993; Tian and Lynch 1996). These locations are generally similar to the areas where we recorded our smooth-pursuit–related neurons (Fig. 14), and the majority of our pursuit-related neurons exhibited discharge characteristics similar to those reported previously (Heinen 1995; Heinen and Liu 1997; Schall 1991). Therefore we conclude that the area we recorded was the SEF. We did not search for saccade neurons in this study and only occasionally encountered saccade-related neurons in the pursuit-related areas. Histological identification of saccade-related neuron locations in previous studies are generally more rostral than our pursuit-related area (Chen and Wise 1995; Fujii et al. 2002; Isoda and Tanji 2003; Schall 1991; Schall et al. 1993). In the areas we recorded, pursuit-related SEF neurons seemed slightly caudal to the saccade-related SEF areas.
Comparison of discharge characteristics of pursuit-related neurons between the SEFs and caudal FEFs
To understand the specific role of each frontal cortical area in smooth-pursuit, it is necessary to compare its activity in identical task conditions. For pursuit-responding neurons, similar discharge characteristics were observed in the two areas. For example, eye velocity sensitivity during smooth-pursuit was similar for the SEF and caudal FEF (mean, 0.56 vs. 0.50–0.53 spies/s/° /s, respectively) (Fukushima et al. 2000). Although the high percentage of neurons with vestibular-related activity in both SEFs and caudal FEFs was strikingly similar (Table 1), the activity of the great majority of SEF pursuit-related neurons did not code gaze (Fig. 6). This is in a sharp contrast to the common, gaze velocity signals found in the caudal FEF in the same task conditions (Table 1). We do not exclude the possibility that gaze velocity signals in the SEFs may become important in different task conditions (see below). Nevertheless, the present results, together with the clear differences in the discharge characteristics between the two areas (Table 1), indicate that the population of pursuit-related neurons in each area is different. In contrast to the majority of caudal FEF neurons that code parameters of smooth-pursuit such as eye velocity, gaze velocity, retinal image motion for target velocity, and smooth eye movements in 3D (Table 1), the majority of SEF pursuit-related neurons did not, despite the fact that they coded eye velocity during smooth-pursuit without vestibular stimulation. These results suggest that the SEFs and caudal FEFs are involved in different aspects of pursuit-vestibular interactions and that eye velocity coding of SEF pursuit neurons is specific to the task conditions.
Heinen and Liu (1997) reported that smooth-pursuit neurons in the SEFs exhibit prediction-related activity before initiation of pursuit. Consistent with this observation, our results show that many pursuit-related neurons exhibited phase leads during sinusoidal target motion (Fig. 2B), and they discharged appropriately during blanking of the target before it changed direction (Fig. 6F). Moreover, individual SEF neurons exhibited virtually constant phase shifts (re target velocity), even at 1 Hz during pursuit in the frontal and depth planes (Figs. 4A and 13A). Such constancy requires accurate prediction to compensate for the long delays involved in processing visual motion information and/or eye velocity commands (Barnes 1993).
Prediction should occur not only on the motor side as preparation and perseverance of ongoing movements (Barnes 1993) but also on the sensory and/or perception side (Umeno and Goldberg 1997). For example, a visual response that anticipates the eventually renewed direction and speed of the target movement of a temporarily occluded visual input. In fact, in addition to vigorous discharge during pursuit of an invisible target, the majority of caudal FEF pursuit neurons receive visual inputs reflecting target motion in the absence of pursuit, and their activity reflects the direction and speed of the reconstructed target image—signals sufficient for estimating target motion (Fukushima et al. 2002a). Using identical tasks in the same animals, this study shows that the majority of SEF pursuit-related neurons do not exhibit visual responses to spot motion (Table 1). This suggests that in the present task conditions SEF neurons do not exhibit visual prediction, despite the fact that the phase invariance of SEF neurons during tracking described above is similar to the phase behavior of caudal FEF pursuit neurons (Fukushima et al. 2000, 2002a). These contrasting results between SEF and caudal FEF pursuit neurons in the present task condition suggest that the SEF involvement in pursuit prediction is more on the motor than sensory or perception side, different from the caudal FEF. Preliminary studies by Kim and Heinen (2001) reported that SEF pursuit neurons discharge vigorously during a task condition that requires prediction. It may well be that pursuit-related neurons in this study would discharge more vigorously to target motion in a predictive manner in the conditions used by Kim and Heinen (2001). Reciprocal connections between the SEF and FEF could transfer the necessary visual signals for task dependent performance including target velocity information (Schall et al. 1993; Stanton et al. 1993).
Olson and his colleagues reported that SEF neurons encode an object-centered frame of reference (Olson and Gettner 1995; Tremblay et al. 2002). Although it is unknown whether SEF neurons could encode a frame of reference of a moving, rather than stationary target, despite a weak visual response to the target alone (Fig. 10, C and D), we do not exclude the possibility that the phase invariance we observed reflected SEF neurons' encoding relative spatial position of the tracking target after training.
Possible relations of SEF pursuit-related neuronal activity to task-dependent pursuit eye movements
Although electrical stimulation of the SEF has been shown to facilitate smooth eye movements (Missal and Heinen 2001), SEF lesions are known to have minimum effects on pursuit (see review by Tehovnik et al. 2000). Consistent with these results, muscimol injection into the SEF pursuit area failed to induce clear effects on smooth-pursuit and VOR cancellation in the same task conditions in our monkeys (Fukushima et al. 2003b; also see review by Tehovnik et al. 2000). These results are in striking contrast to the deficits in smooth-pursuit and VOR cancellation induced by caudal FEF lesions or chemical inactivation (Fukushima et al. 1999b; Keating 1991, 1993; Lynch 1987; MacAvoy et al. 1991; Shi et al. 1998). Those observations and the present results taken together suggest that, with simple ocular tracking tasks, a specific role of the SEF could not be detected.
In addition to the well-known saccade-related activity (Schall 1991; Schlag and Schlag-Rey 1987), the SEF is reported to play an important role in more complex behaviors such as learning-related activity (Chen and Wise 1995; Nakamura et al. 1998), planning of saccades (Olson et al. 2000), decision-making processes (Coe et al. 2002), sequential performance of saccades (Isoda and Tanji 2002, 2003; Lu et al. 2002; Pierrot-Deseilligny et al. 1995; Schiller and Chou 1998), antisaccades (Schlag-Rey et al. 1997), and eye-hand reach coordination (Mushiake et al. 1996). Reward-predicting activity is also reported (Amador et al. 2000), and apparently, SEF neuron activity is task-dependent (Tanji 1996). Furthermore, in our task conditions, if we presented a tracking target that moved across a stationary structured background, after muscimol infusion into the SEF pursuit area our monkeys exhibited impairment of upward smooth-pursuit, despite the fact that the same monkeys did not show impairment in tracking across a homogeneous background after infusion (Fukushima et al. 2003b). Again, this is in contrast to the impairment induced by muscimol infusion into the caudal FEFs. FEF inactivation also impaired vertical pursuit across the textured background, but the effects were less selective, since a similar impairment was observed across the homogeneous background. These results indicate that, as Tanji (1996) clearly states, "the usage of the SEF is more dependent on the behavior or conditional state than the usage of the FEF."
The possible importance of vestibular signals in SEF function has been suggested by clinical studies. De Waele et al. (2001) reported vestibular evoked potentials in the anterior portion of the supplementary motor area with latencies of 6 ms induced by electrical stimulation of the vestibular nerve in patients. Israël et al. (1992, 1995) and Pierrot-Deseilligny et al. (1993) reported that vestibular contingent memory-guided saccades are impaired in patients with SEF lesions, although they did not exhibit abnormalities in memory-guided saccade tasks without vestibular stimulation (Pierrot-Deseilligny et al. 1993). These observations suggest the importance of vestibular information in self-centered spatial representation during the memory-guided saccade tasks. Olson and Gettner (1995) (see also Tremblay et al. 2002) reported that the SEF provides an object-centered frame of reference. Strong vestibular-related activity in the great majority of SEF pursuit-related neurons in this study (Fig. 6; Table 1) may provide that body-centered frame of reference for animal behavior in 3D space (Fukushima 1997). It is possible that vestibular signals may also be used for calculation of gaze velocity during demanding task conditions that require learning. Vestibular signals might facilitate smooth-pursuit and vergence tracking (Fukushima et al. 2001; Sato et al. 2004). Vestibular signals can also be used for pursuit adaptation, and caudal FEF neurons exhibit adaptation-related activity (Fukushima et al. 2001). The SEF may provide adaptation-related vestibular signals to the FEF via their direct projections (Schall et al. 1993). Prediction-related activity of SEF pursuit neurons (Heinen and Liu 1997; Kim and Heinen 2001) should be tested further to examine a specific role of vestibular signals in the SEFs for task-dependent pursuit eye movements.
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ACKNOWLEDGMENTS |
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GRANTS
This research was supported by Japanese Ministry of Education, Culture, Science, Sports and Technology Grants 15016004 and 14658266, Marna Cosmetics, Toyota Riken, and National Institutes of Health Grants EY-06558 and RR-00166.
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. Fukushima, Dept. of Physiology, Hokkaido Univ. School of Medicine, West 7, North 15, Sapporo 060-8638, Japan (E-mail: kikuro{at}med.hokudai.ac.jp).
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ABSTRACT
INTRODUCTION
, neurons with eye position–related activity during saccades.
) with the overlaid fitted sine waves (smooth line), spikes rasters, and histograms of neuron discharge with superimposed fitted sine waves.
