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1Department of Neurophysiology, Doctoral Program in Kansei Behavioral and Brain Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan; and 2Department of Biological Structure and National Primate Research Center, University of Washington, Seattle, Washington
Submitted 18 May 2007; accepted in final form 29 October 2007
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ABSTRACT |
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INTRODUCTION |
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; Scudder and McGee 2003). In particular, recent studies have shown that the cerebellar oculomotor vermis is at least one of the sites for plasticity (Robinson and Noto 2005; Robinson et al. 2002). Previous work indicates that the reason saccade size changes during adaptation is that saccade-related output from the cerebellum changes (Inaba et al. 2003; Scudder and McGee 2003). How does this change in cerebellar output alter saccade size?
The neuronal mechanism for saccades, including the cerebellum, is well described (e.g., Scudder et al. 2002). Figure 1 shows a schematic summary of the brain stem saccade mechanism. A saccade motor command descends from the superior colliculus (SC) to activate excitatory burst neurons (EBNs). EBNs, together with tonic neurons (not shown in Fig. 1), drive abducens motoneurons that in turn contract extraocular muscles, causing a saccade. At the same time, the saccade motor command from SC also enters the cerebellum by a relay in a major precerebellar nucleus, the nucleus reticularis tegmenti pontis. The cerebellum uses this incoming saccade signal to create its saccade-related output. This signal exits the cerebellum in the axons of neurons in the saccade-related part of the fastigial nucleus, the fastigial oculomotor region (FOR). It is the signals carried by FOR neurons that change during adaptation. No previous work demonstrates how changes in FOR signals cause the changes in motoneuron activity that decrease saccade size during adaptation.
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; Gonzalo-Ruiz et al. 1988, 1990; May et al. 1990; Noda et al. 1990; Sato and Noda 1991). The axons of FOR neurons terminate in areas containing the saccade-related premotor network that drives motoneurons (Noda et al. 1990; Scudder et al. 2000). This premotor network contains saccade burst neurons, that is, excitatory burst neurons (EBNs) and inhibitory burst neurons (IBNs). The largest FOR output, as judged by synaptic terminal density (Noda et al. 1990) and neural responses to electrical stimulation of the FOR (Scudder et al. 2000), is to contralateral IBNs. Modifying IBN discharge could change saccade size. The IBNs on one side of the brain discharge vigorously for ipsiversive saccades. This is the neurons' on-direction. IBNs discharge minimally or not at all for contraversive saccades (the off-direction). The axons of IBNs cross the midline to terminate on and inhibit motoneurons in the contralateral abducens nucleus (Scudder et al. 1988).
We propose that IBNs are a significant link between the FOR and abducens motoneurons. Further, we propose that adaptation-related changes in FOR activity alter saccade size, at least in part, by changing IBN activity. If so, then IBN activity will change during adaptation. Specifically, there will be a significant increase in IBN activity during off-direction saccades as adaptation decreases the size of these saccades (Fig. 1). This increase in IBN activity during off-direction saccades would decrease saccade size by decreasing the activity of neurons in the contralateral abducens nucleus during these saccades. We tested this proposal by recording IBN activity during adaptation in monkeys. Preliminary data of the present study have been reported (Kojima et al. 2005, 2006).
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METHODS |
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We prepared two rhesus monkeys (Macaca mulatta, male, 4.5 and 3.2 kg) for eye movement recording with the magnetic search coil method (Fuchs and Robinson 1966). Experiments were conducted in two separate laboratories, one in the University of Tukuba and one in the University of Washington in Seattle. We collected data from one monkey in each laboratory. Anesthesia was introduced with ketamine hydrochloride (15–20 mg/kg, administered intramuscularly) and maintained by inhalation of isoflurane. Electrocardiogram and blood oxygen level were monitored. In surgery, we implanted each monkey with a three-turn coil of fine Teflon-coated stainless steel wire around one eye. The ends of the wire terminated in a small connector fixed to the top of the skull with stainless steel screws and dental acrylic. In the same surgery, we attached three or four receptacles to the monkey's skull so we could stabilize the head during eye-movement recordings. After recovery from the surgery, each monkey was trained to follow a small visual target with its eyes. When the training was complete, we again induced general anesthesia and implanted a recording chamber (Crist Instrument or custom made) over the posterior part of the skull aimed at the abducens nucleus. The chamber tilted 15° laterally at the top in one monkey (Tsukuba) and was directed straight down in the other (Seattle). After each surgery, antibiotics were given intramuscularly for 3 days to prevent infection. All surgical and experimental protocols were approved by the Animal Care and Use Committee at the University of Tsukuba and the Animal Care and Use Committee at the University of Washington.
During recording sessions, the monkey sat in a primate chair in a darkened booth with its head restrained. The animal was required to make saccades toward a small (0.3°) target spot. Whenever the monkey aimed its eye to within 2.0° of the target continuously for 0.8–1.2 s, the target moved rapidly to another position and the animal was rewarded with a small amount of apple juice or applesauce.
Behavioral procedure
We elicited saccade adaptation with the conventional intrasaccadic target step method (McLaughlin 1967). The target jumped along the horizontal meridian and then, during the saccade, moved rapidly backward by 35% of the initial target movement size. This intrasaccadic step (ISS) created a visual error at the end of the movement as if the saccade had been too large, requiring the animal to make a corrective saccade to catch the target. This procedure, when repeated over several hundreds of movements, gradually decreased the saccade amplitude. After recording about 30 preadaptation saccades to 10° horizontal and vertical target movements as well as 5, 8, 10, 15, and 20° horizontal target movements, we adapted saccades to 10° target movements in one horizontal direction. The target moved along the horizontal meridian pseudorandomly within 15° of the straight-ahead position.
Neuronal recording
Single-unit neuronal activity was recorded with a glass-coated or Epoxylite-coated tungsten electrode and amplified (band width 0.1/8 kHz or 0.2/10 kHz) by conventional circuits. The electrode was placed through a guide tube (23 gauge) that had been inserted through the dura, cerebral tissue, and tentorium cerebelli. In each animal, we first located the abducens nucleus identifiable by the characteristic burst-tonic unit discharge and the high-frequency firing of the neurons there (Fuchs and Luschei 1970). To locate the IBNs we made electrode penetrations in the region caudal and ventral to the abducens nuclei. The waveform of unit spikes was carefully observed to judge whether recordings were being made extracellularly from the cell body. Only negative/positive spikes were regarded as action potentials of the soma.
Data analysis
The unit activity was digitized at 50 kHz to observe the entire waveform of individual spikes. Eye and target position signals were digitized at 1 kHz and stored on a hard disk with an interface (Micro 1401, CED). Data were analyzed off-line on a computer using custom programs that ran on an analysis software (Spike2, CED). Saccade onset and end were defined by an eye velocity threshold criterion of 20°/s. Targeting saccades elicited by an initial (not intrasaccadic) target movement were selected for analysis. We rejected saccades for analysis if their latencies were <60 ms because we regarded these movements as anticipatory. We also rejected saccades with trajectories that had a vertical component of >3°. Parameters of neuronal discharge, saccades, and target movements were exported to statistics programs (StatView or JMP, SAS) to measure other characteristics of neural activity and movements. We defined the gain of a saccade to a horizontally displaced target as the horizontal saccade size divided by the horizontal distance from the initial eye position to the target.
Histology
In the last experiment in one monkey (monkey I), two electrolytic lesions were made along the same track by passing DC cathodal current (20 µA for 30 s). The dorsal and ventral lesions were made immediately dorsal to left burst-tonic units and 1.5 mm ventral to a left burst neuron, respectively (Fig. 2, horizontal arrows). Later on the same day, the animal was killed with an overdose of pentobarbital and perfused intracardially first with 2 L of saline and then with 3 L of 4% paraformaldehyde. The brain was removed, postfixed for several days, and cut into serial frontal sections (100 µm thick). The sections were mounted on slide glasses, dehydrated, stained with cresyl violet, and coverslipped for histological examination. Locations of recording sites were estimated with reference to the marking lesions on the basis of the rostrocaudal and mediolateral coordinates of the track and the depth reading.
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RESULTS |
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We recorded the activity of 42 burst neurons in the region ventral and mediocaudal to the abducens nucleus in two monkeys during saccade adaptation (Fig. 2). We held these isolated neurons during adaptation until saccade gain decreased significantly. Nineteen neurons were recorded from monkey I (Tsukuba) and 23 neurons were recorded from monkey T (Seattle). There was no substantial difference in the data recorded from the two monkeys. Consistent with previous descriptions of IBN activity (Scudder et al. 1988), all of the neurons we recorded discharged vigorously for ipsilaterally directed saccades (the on-direction) and discharged minimally or not at all for contralaterally directed saccades (the off-direction). Twenty-seven neurons collected for this study started their spike activity, on the average across saccades, <15 ms earlier than the onset of ipsiversive saccades. They were classified as short lead burst neurons (SLBNs) according to a lead time criterion (15 ms) in previous studies (Scudder et al. 1988; Strassman et al. 1986). The mean lead time from saccade onset for these cells was 5.9 ± 2.7 ms (n = 27). The remaining 15 burst neurons exhibited a prelude of activity (a few to several spikes) before a high-frequency burst for ipsiversive saccades. The prelude started >15 ms earlier than saccade onset. These cells had a mean lead time of 26.2 ± 9.0 ms (n = 15) and were classified as long lead burst neurons (LLBNs). As mentioned in previous reports, such classification was somewhat arbitrary.
The discharge of one SLBN for two horizontal saccades is shown in Fig. 3. This neuron, recorded on the left side of the brain stem, exhibits a high-frequency burst of spikes for the leftward saccade and far fewer spikes for the rightward saccade. Spike activity began about 5 ms before the onset of the on-direction (leftward) saccade and very close to the start of the off-direction saccade. Figure 4 summarizes discharge properties of this neuron. Shown in Fig. 4A is the temporal profile of averaged firing rate for 10° saccades in four directions. The discharge for on-direction (i.e., leftward) saccades started a few milliseconds earlier than did the discharge for saccades in other directions and exhibited a higher rate, nearly 1 kHz, as well as a longer burst duration. The discharge for off-direction (i.e., rightward) saccades was always the smallest among the discharge for saccades in four directions. Its peak frequency was about half that of on-direction discharge. The number of spikes per saccade in the on-direction increased linearly with increasing saccade size (r = 0.91, P < 0.0001). The slope of the regression line was 0.95 spike/°(Fig. 4B, left half). Although the slope of linear regression line for off-directions saccades, 0.097 spike/°, was lower than that for on-direction, it showed a significant positive correlation (P < 0.005, r = 0.28; Fig. 4B, right half). The on-direction burst began about 5 ms before saccade onset regardless of saccade size (y = 0.004x – 4.982, P < 0.95, r = 0.007), whereas the lag of off-direction spike activity relative to saccade onset increased with saccade size (y = 0.590x + 0.917, P < 0.0001, r = 0.621; Fig. 4C). The lead time of spike activity with respect to saccade end increased with increasing size of saccades in both on- and off-directions (on: slope 1.49 ms/°, P < 0.0001, r = 0.85; off: slope –0.949 ms/°, P < 0.0001, r = 0.741; Fig. 4D).
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5 ms) of the on-direction burst relative to saccade onset (Fig. 5C, left). However, this SLBN, unlike the previous one (in Fig. 4), emitted no or only a few spikes for off-direction saccades. Still there was a significant relation between horizontal saccade amplitude and the number of spikes exhibited for off-direction saccades (slope 0.04 spike/°, P < 0.001, r = 0.33; Fig. 5B, right). This unit also showed an increasing time of lag with increasing saccade size in the off-direction (Fig. 5C right, slope 0.96 ms/°, P < 0.0001, r = 0.67). The lead time of spike activity from saccade end increased with increasing saccade size in both the off-direction and the on-direction (Fig. 5D, on: slope 1.34 ms/°, P < 0.0001, r = 0.94; off: slope 0.65 ms/°, P < 0.001, r = 0.51).
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We wanted to document adaptation-related changes in off-direction activity of saccade-related burst neurons, so we preferred to record from the neurons that consistently fired spikes for off-direction saccades. Figure 6 shows the distribution of average number of spikes for off-direction saccades of <20° for each neuron. Among neurons with off-direction spikes, there is a continuous distribution of the number of spikes from few to many. Any division of these cells according to their number of off-direction spikes is somewhat arbitrary. Nonetheless, we divided these neurons into three groups: consistent-off-direction-spike, occasional-off-direction-spike, and no-off-direction-spike neurons. We classified burst neurons as consistent-off-direction-spike if they had an average number of spike 
3.5; as occasional-off-direction-spike if they had an average number of spikes 0.5 and <3.5; and as no-off-direction-spike if they had an average number of spikes <0.5. Neurons shown in Figs. 4 and 5 are indicated by two vertical arrows in Fig. 6.
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We summarized the relationship between the number of spikes fired for off-direction saccades and horizontal saccade size for all 42 burst neurons. Figure 7A (top) shows the superimposed regression lines for these neurons. The correlation coefficients for this relationship ranged from 0.01 to 0.90 (mean 0.39). The average slope of relationship was 0.22 spike/°and the range was –0.19 to 1.86 spikes/° (Fig. 7A, bottom). In general, number of spikes for off-direction saccades correlated positively with horizontal saccade size.
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Changes in off-direction activity during adaptation
We examined these 42 units during amplitude-decreasing adaptation of off-direction saccades. Every one of these adaptations significantly reduced saccade size; the gain of the last 20 adaptation saccades was significantly smaller than that of the last 20 preadaptation saccades (P < 0.05, t-test). The mean gain reduction was 0.173 ± 0.072 (mean percentage gain change = 18.0 ± 6.7). Figure 8A shows the activity of an example SLBN during adaptation (same neuron as in Figs. 3 and 4). Illustrated is one off-direction (rightward) saccade recorded early during adaptation (arrow). The off-direction saccade is followed by an on-direction (leftward) corrective saccade. There were 7 spikes for the 10° off-direction saccade and 16 spikes for the 3° on-direction saccade. Figure 8B shows one off-direction saccade late during adaptation. Amplitude of this saccade initiated to a target 10° to the right has been reduced by adaptation and is about 7°. The SLBN exhibited 12 spikes for this saccade.
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We summarized the adaptation-related changes that occurred in the activity of all 42 burst neurons by plotting two points for each neuron (Fig. 11). One represented 20 saccades before each adaptation (filled circle) and one represented the last 20 of that adaptation (open circle). Each point's position on the plot was determined by two values: the mean gain of the saccades (abscissa) and the mean number of spikes fired by the neuron during those off-direction saccades (ordinate). Figure 11, A–C shows three such plots, one for each of the three groups of burst neurons defined according to the consistency of their off-direction response: i.e., consistent, occasional, or no spikes.
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Finally, we examined how a neuron's response changed with the progress of adaptation for two neurons, which were collected during particularly large decreases in saccade gain (25%). Both fired spikes for every off-direction saccade during adaptation (2–19 spikes) and the number of spikes emitted per saccade increased gradually over approximately 600–750 saccades. We calculated the average spikes/saccade and average gain for every sequential group of 10 saccades. Correlation was then tested between the average number of off-direction spikes/saccade and the average gain. Both neurons showed a significant negative correlation (P < 0.0001, r = 0.862, n = 75 and P < 0.0001, r = 0.481, n = 59).
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DISCUSSION |
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It is logically possible that the increases in off-direction IBN spikes we report could result purely from chance and not from adaptation. In this view, the off-direction responses of all IBNs vary and change spontaneously during the time necessary for adaptation. The firing of IBNs with strong preadaptation responses is more likely to decrease during adaptation, whereas that of cells with weak preadaptation responses is more likely to increase.
For the following reasons we think that it is extremely unlikely that random changes in IBN responses significantly influenced our findings. First, contrary to the pattern that chance would cause, none of our least responsive IBNs increased its responses during adaptation and our most responsive IBNs showed an average increase instead of decrease. Second, some IBNs show negative correlations between their off-direction response and saccade gain during the course of adaptation. Third, FOR cells change their saccade-related activity during adaptation and project heavily to IBNs. As we subsequently discuss, the changes in FOR discharge are consistent with those in IBN off-direction discharge. Fourth, on-direction spikes/saccade of our IBNs did not change during adaptation. This precludes some random change in IBN excitability.
A previous lesion study has suggested that "rapid adaptation," like the one induced with intrasaccadic step of the target, "is specifically involved in preventing continuous reduction [in saccade size] caused by fatigue" (Barash et al. 1999). If this were the case and IBNs were involved in the fatigue compensation, one would expect to see some change in IBN activity when the monkey simply repeats hundreds of normal-sized saccades to target movements that are not followed by intrasaccadic steps. It may therefore be argued that the observed changes in our IBN activity could at least partly be related to fatigue. We do not think that it is likely that fatigue compensation influenced our results because the change we observed in IBN activity is in the wrong direction to compensate for fatigue. The off-direction activity of IBNs would have decreased to prevent fatigue-related reduction in saccade size because IBNs inhibit contralateral abducens neurons. Instead, our IBNs showed an increase in their off-direction activity.
Are the burst neurons IBNs?
The neurons we recorded for this study were saccade-related burst neurons located in the region caudal, medial, and ventral to the abducens nucleus. Previous reports indicate that these burst neurons are inhibitory burst neurons (IBNs), which directly project to contralateral abducens motoneurons. Strassman et al. (1986) examined, using intraaxonal horseradish peroxidase injection in alert squirrel monkeys, the axonal trajectory of burst neurons whose somata were located in this reticular region and found that almost all of them (18/19), including a few LLBNs, terminated in the contralateral abducens nucleus. Scudder et al. (1988) analyzed in detail saccade-related responses of burst neurons in this region of the rhesus monkey. The discharge characteristics of the neurons that we recorded are very similar to those recorded by Scudder et al. (1988).
IBNs are located in the region immediately ventral and mediocaudal to the abducens nucleus. It is usually easy to distinguish IBNs and abducens neurons because only the latter show tonic activity that is related to eye position. However, it is possible to miss the tonic activity of some burst-tonic neurons with high position threshold and mistake them for SLBNs. To avoid this, we looked for tonic activity when the eye was aimed left and right 20° in neurons that, like abducens neurons, did not emit spikes for off-direction saccades.
Distribution of IBNs distinguished by off-direction activity
Our procedure may have caused us to overestimate the proportion of IBNs that consistently fire spikes during off-direction saccades. We were interested in the off-direction activity of IBNs so we searched specifically for such neurons. When the first neuron(s) that we encountered on an electrode penetration produced no off-direction spike, we did not test it (them) and drove the electrode deeper to find another IBN. If, during a subsequent penetration through the IBN area we found no burst neurons, we withdrew the electrode to the cell producing no off-direction spikes and characterized its properties.
Nonetheless, our estimate that about one third of IBNs, including both SLBNs and LLBNs, consistently exhibit off-direction spikes is similar to the findings of the previous study on IBNs in the same species. Scudder et al. (1988) reported that 27% of SLBNs and 32% of LLBNs fired an increasing number of spikes with increasing saccade size in the off-direction.
Role of off-direction IBN activity in saccade adaptation
In the present study, we examined the contribution of IBN off-direction activity to saccade amplitude adaptation by testing whether IBN activity increases during adaptive decrease in saccade gain. About one third of the neurons for which the adapted direction was their off-direction showed a gradual increase in the number of spikes or a shortening of the spike lag as gain decrease adaptation progressed. This result suggests that the increase in off-direction activity of IBNs contributed to the decrease in motoneuron activity and thus in saccade amplitude. IBNs that had been silent during off-direction saccades before adaptation showed no changes and remained silent after adaptation. Because we tested gain reduction of saccades only to 10° target movements, these no-spike IBNs might have fired spikes during adaptation that had reduced the gain of saccades of other amplitudes. Alternatively, the no-spike IBNs simply did not contribute to adaptation.
The intense burst of IBNs for ipsiversive saccades is transmitted to and inhibits contralateral abducens motoneurons, relaxing the antagonist muscles (Scudder et al. 2002). However, IBN activity during contraversive (i.e., off-direction) saccades has not been a focus of attention in previous studies. Van Gisbergen et al. (1981) analyzed premotor SLBN activity in both on- and off-directions. Their analysis suggested that excitatory input from ipsilateral EBNs is not sufficient to accurately describe saccade dynamics and that additional inhibitory input from contralateral IBNs should be taken into account. This supports the idea that off-direction activity of IBNs does influence the activity of target motoneurons. Our data extend this idea by suggesting that changes in IBN activity for contraversive saccades produce substantive changes in the size of these saccades.
Does IBN off-direction activity reflect input from FOR?
Several lines of evidence strongly suggest that the saccade-related portion of the fastigial nucleus, FOR, carries key cerebellar output to produce saccade adaptation. Inactivation studies (Robinson et al. 2002) show that FOR activity is necessary for changes in saccade size during adaptation. Recordings from FOR neurons indicate that the FOR activity changes during saccade adaptation in parallel with saccade amplitude (Inaba et al. 2003; Scudder and McGee 2003). In particular, FOR neurons increase their activity and/or exhibit their burst earlier as the size of ipsiversive saccades is adaptively reduced. In addition, both anatomical and electrophysiological studies strongly suggest that FOR neurons project directly to contralateral IBNs (Noda et al. 1990; Scudder et al. 2000). These data make it likely that IBNs are a major recipient of adaptation-related signals that originate from the cerebellum.
It should be recognized that changing the off-direction activity of IBNs may not be the only way for the FOR to elicit adaptation. FOR neurons have been shown to increase their bursts during adaptive increase in the size of contraversive saccades (Scudder and McGee 2003). The FOR thus could contribute to the amplitude-increasing adaptation by increasing the on-direction burst of contralateral IBNs, which in turn would prolong the pause in antagonist motoneurons. No one to date has recorded FOR cells during adaptation to decrease the size of a contraversive saccade. Still, current data allow us to predict that FOR neurons will decrease their firing during such adaptation. This would decrease the on-direction activity of contralateral IBNs and decrease their inhibition of the antagonist muscles opposing the saccade, thereby reducing saccade size. In addition, changes in the saccade-related activity of FOR neurons, through their projection to contralateral EBNs (Noda et al. 1990; Scudder et al. 2000), could also modify the on-direction burst of EBNs and, consequently, that of agonist motoneurons. In the current experiments, we chose to examine contributions of IBN activity to saccade adaptation because the largest FOR output is to these neurons. We reasoned that that this could make adaptation-related changes in IBNs easier to detect than those in other FOR targets like EBNs.
Characteristics of off-direction discharge of our IBNs are similar to those of burst discharge exhibited by neurons in the contralateral FOR. Many of the IBNs emitted more spikes for larger contraversive saccades just as many FOR cells do for larger ipsiversive saccades (Fuchs et al. 1993). The burst latency of FOR cells relative to saccade onset tends to increase with the size of ipsiversive saccades; i.e., their burst starts progressively later as the saccade size increases (Fuchs et al. 1993). The off-direction spikes of our IBNs also began later for larger saccades (Fig. 7B). The lead time relative to saccade end tends to increase with saccade size both in FOR cells (Fuchs et al. 1993) and in our IBNs (Fig. 7C). The burst of FOR cells often lasts well beyond the end of ipsiversive saccades (e.g., Figs. 2 and 8 of Ohtsuka and Noda 1991; Figs. 1, 2, and 5 of Fuchs et al. 1993). Similarly, some of our IBNs exhibited off-direction spike activity that outlasted concurrent saccades (e.g., Fig. 6G). More important, these two classes of cells change their activity in a similar fashion during adaptation. For example, when adaptation reduces the amplitude of rightward saccades, many IBNs on the left side increase the number of spikes/saccade or exhibit spikes at shorter latencies. Many neurons in the right FOR, which project to the left IBN region, show similar changes (Inaba et al. 2003; Scudder and McGee 2003). Thus both preadaptation activity of IBNs and its adaptation-related changes for off-direction saccades appear to reflect those of FOR neurons that project to these IBNs.
We propose that the IBNs that change their activity during adaptation relay adaptation-related changes in cerebellar output to the abducens motoneurons.
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GRANTS |
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ACKNOWLEDGMENTS |
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Present address of Y. Kojima: Department of Physiology and Biophysics, National Primate Research Center, University of Washington, Seattle, WA 98195-7420.
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FOOTNOTES |
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Address for reprint requests and other correspondence: Y. Iwamoto, Department of Neurophysiology, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8574, Japan (E-mail: iwamoto{at}md.tsukuba.ac.jp)
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V. Ethier, D. S. Zee, and R. Shadmehr Spontaneous Recovery of Motor Memory During Saccade Adaptation J Neurophysiol, May 1, 2008; 99(5): 2577 - 2583. [Abstract] [Full Text] [PDF]
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 H. Chen-Harris, W. M. Joiner, V. Ethier, D. S. Zee, and R. Shadmehr Adaptive Control of Saccades via Internal Feedback J. Neurosci., March 12, 2008; 28(11): 2804 - 2813. [Abstract] [Full Text] [PDF]
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