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Report
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110
Submitted 3 June 2003; accepted in final form 15 July 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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; Stein 1986; Stein and Glickstein 1992). Cerebellar lesions result in a characteristic ipsilateral limb ataxia (Holmes 1939); impaired coordination and a loss of control over the parameters of movement (Bastian et al. 1996; Diener and Dichgans 1992; Goodkin and Thach 2003; Hore et al. 1991; Miall et al. 1987). Electrophysiological recordings from the cerebellar cortex of the anterior lobe and the intermediate zone of the posterior lobe have demonstrated correlations between simple spike firing and movement parameters of the ipsilateral limb; specifically, limb position, movement direction, and movement speed (Coltz et al. 1999; Fortier et al. 1989, 1993; Fu et al. 1997; Mano and Yamamoto 1980; Marple-Horvat and Stein 1987; Thach 1968, 1970, 1978). Imaging studies have lent further support to the cerebellum's role in ipsilateral motor control by showing a correlation between increased activity in the anterior lateral cerebellum and motor parameters of the ipsilateral limb (Grodd et al. 2001; Turner et al. 1998).
However, several studies indicate that the observed correlations with ipsilateral limb movement cannot completely explain the role of the cerebellar hemisphere. Lesions in humans that were restricted to the posterior and lateral cerebellar hemisphere impaired visuo-motor adaptation but resulted in little or no ataxia (Martin et al. 1996). Electrophysiological recordings in nonhuman primates revealed that complex spikes in the intermediate and lateral cerebellar cortex encoded motor error relative to the target (Kitazawa et al. 1998), whereas simple spike firing in the lateral cerebellum was correlated with visual feedback rather than movement direction (Liu et al. 2003). A functional imaging study has shown bilateral activation of the lateral cerebellar cortex on unilateral limb reaching (Cui et al. 2000), whereas other imaging studies have suggested numerous nonmotor functions for this region of the cerebellar cortex (Allen et al. 1997; Bischoff-Grethe et al. 2002; Gao et al. 1996).
We found that the spike firing in the lateral aspect of the cerebellar hemisphere was significantly modulated by reaching with either the ipsilateral or the contralateral arm. Further, spike firing was correlated with motor parameters during reaching with either the ipsilateral or the contralateral arm. On the basis of these finding, we suggest that, similar to what has been observed in anterior and medial regions of the cerebellar cortex during ipsilateral limb movements, spike firing in the lateral cerebellar cortex was also correlated with movement and motor parameters. But unlike what has been observed in the anterior and medial regions (Thach 1968), spike firing in the lateral cerebellar cortex was correlated with movement and motor parameters irrespective of the effector limb used to perform the reach.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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We trained two adult male macaque monkeys to perform a visually guided reaching task with either arm (Fig. 1). A 15-in touch-sensitive video screen, placed directly in front of the animal 20 cm distant from two capacitance switches, displayed visual targets and registered touches of the monkey's finger. A white rectangle placed in either the upper right- or left-hand corner of the screen continuously indicated which arm was to be used for reaching throughout a block of trials. At the start of a trial, both hands had to remain on the capacitance switches for a variable time period (500-1,500 ms) to complete the initial hold period. A visual target, consisting of a gray dot with a radius of 6 mm, then appeared at a random location on the video screen. The monkey had 300 ms from the start of movement to reach with its hand and touch the screen. The target disappeared when the monkey removed its hand from the switch and then reappeared in the same location 50 ms later while the monkey was in the midst of its reach. This brief target flash was included so that the current paradigm could be directly compared with another paradigm under investigation. A white dot with a radius of 6 mm appeared when and where the monkey touched the screen. For a trial to be considered a success, the target dot and touch dot had to overlap. The reaching hand had to be returned to its switch within 400 ms of touching the screen. Once the reaching hand had been returned to the start position, a final hold period (500-1,500 ms) had to be completed.
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Single units were recorded extracellularly with high-impedance glass-coated platinum/iridium microelectrodes (FHC). The electrodes were attached to a custom stereotaxic X-Y drive that was placed on the recording chamber. Electrodes were lowered into cerebellar cortex where either unidentified cortical cells or Purkinje cells, identified by the presence of complex spikes, were isolated and recorded. The signals were sent to an AC-coupled differential amplifier (gain: 10,000; band-pass filter: 0.1-10 kHz). The analog waveform was digitally recorded at 20 kHz (12-bit resolution) for off-line analysis. The digitally recorded waveform was converted to spike time points by template matching using Cambridge Electronic Design's Spike2 software.
EMG and EOG recording
The broadband electromyographic (EMG) signal from surface electrodes was differentially amplified (gain: 10,000) and then digitally recorded (sampling frequency: 2 kHz). The EMG signal was rectified, time aligned on the start of movement, and averaged across 50 trials. EMG data were acquired in the middle of several months of spike data acquisition. Electro-oculography (EOG) was recorded with fine wire electrodes placed subcutaneously at the lateral edge of each orbit. EOG was amplified (gain: 10,000), filtered (band-pass: 0.1-100 Hz) and then digitally recorded (sampling frequency: 2 kHz). Each session of EOG was visually scanned off-line for sharp transients in the signal, indicating that a saccade had occurred. The start time of each saccade was digitally marked for use in further analysis. EOG data were acquired simultaneously with spike data during the last several sessions of recording.
Verification of recording chamber location
Monkey T was killed by an overdose of anesthesia and perfused with 10% formalin. A piece of 28-gauge tubing was coated with dye, stereotaxically positioned at the center of the recording chamber, and lowered throughout the dorsal-ventral extent of the cerebellum in situ. The ink-coated hole served to mark the location of the recording chamber relative to the tissue of the cerebellum. Dissection of the cerebellum verified the location of recording chamber over the lateral cerebellar hemisphere and that electrophysiological recordings were made in its lateral aspect. Monkey R is involved in ongoing experiments; the chamber placement and recording locations have not yet been verified.
Analyses
SIGNIFICANT REACH MODULATION. All cells from which spikes were recorded for 
10 trials during reaching with each arm were analyzed. The mean firing rate during a segment of the initial hold period (750 ms through 250 ms before the start of movement) and during the planning/reaching period (200 ms before through 300 ms after the start of movement) was calculated. A cell was considered to be significantly modulated by reaching if the mean firing rates during these two time periods was significantly different (Wilcoxon rank-sum test: P < 0.05).
CORRELATION WITH REACH DIRECTION. A correlation with reaching direction was tested for by calculating the mean firing rate (200 ms before through 300 ms after the start of movement) for all reaches to ipsilateral side of the touch-screen and for all reaches to contralateral side of the touch-screen for each arm. The Wilcoxon rank-sum test was then used to determine if the firing rate for reaches to ipsilateral space were significantly different (P < 0.05) from the firing rate for reaches to contralateral space.
CORRELATION WITH REACH SPEED. Reach speed was obtained by taking the distance from the start switch to the touch location on the screen and dividing by the reaching time. For each cell the range of reaching speeds for all trials was split into four equally sized bins, and the average reach speed was calculated for each bin. The mean firing rate during the planning/reaching period (200 ms before through 300 ms after the start of movement) was also calculated from all the trials in each of the four reaching speed bins. If these data could be fit by a linear regression with a significantly nonzero slope (ANOVA P < 0.05), then that cell was considered to be correlated with reach speed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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During performance of the task, both monkeys displayed accurate ballistic movements when reaching with either the ipsilateral or contralateral arm. Monkey T's mean reaching speed was 0.72 ± 0.05 (SD) m/s when reaching with the ipsilateral arm and 0.70 ± 0.04 m/s when reaching with the contralateral arm. Monkey R's mean reaching speed was 0.74 ± 0.04 m/s when reaching with the ipsilateral arm and 0.86 ± 0.06 m/s when reaching with the contralateral arm. On average monkey T touched the screen 17 ± 3 (SD) mm, 4.9°, from the target when reaching with the ipsilateral arm, and 18 ± 4 mm, 5.1°, when reaching with the contralateral arm. On average, monkey R touched the screen 11 ± 2 mm, 3.1°, from the target when reaching with the ipsilateral arm and 21 ± 7 mm, 6.0°, when reaching with the contralateral arm. The maximum angle subtended by Monkey T's reaches was 34° for the ipsilateral arm and 35° for the contralateral arm. The maximum angle subtended by monkey R's reaches was 37° for the ipsilateral arm and 33° for the contralateral arm. Monkey T performed at a 57% success rate when reaching with the ipsilateral arm and 50% success rate when reaching with the contralateral arm. Monkey R performed at an 83% success rate when reaching with the ipsilateral arm and a 46% success rate when reaching with the contralateral arm.
Spike firing was modulated by reaching irrespective of the effector limb
Electrophysiological signals were recorded from 99 cells of 132 penetrations into the posterior and lateral regions of the cerebellar cortex—the lateral aspects of lobules IV, V, VI, and crus I and II of lobule VII (Fig. 1)—in two macaques during the performance of the reaching task. Spike firing in these regions was significantly modulated by reaching with either the ipsilateral or the contralateral arm in 79% of the cells, 78 of 99 (Wilcoxon ranksum test, P < 0.05). Fifty four of these 78 cells were confirmed as Purkinje cells by the presence of complex spikes. Of these 78 significantly modulated cells, 66 were significantly modulated by ipsilateral arm reaching and 65 were significantly modulated by contralateral arm reaching. Spike firing was significantly modulated by both ipsilateral arm and contralateral arm reaching in 68%, 53 of 78, of the cells. Most cells had firing rate peri-stimulus time histograms (PSTHs) that were similar when reaching with either arm. For these cells, the PSTHs could exhibit either increasing firing rates (n = 55) or decreasing firing rates (n = 8) for reaching with the ipsilateral and the contralateral arm (Fig. 2). However, for some cells (n = 15), the PSTHs for the two arms were inversely related. The mean firing rate for ipsilateral arm reaching was plotted against the mean firing rate for the contralateral arm and fit by a linear regression, giving a correlation coefficient of 0.66 and a significantly nonzero slope (P < 0.05; Fig. 3A). Because averaging across a heterogeneous population of firing rates would tend to obscure details in population analyses, two population average PSTHs were constructed, one for PSTHs with increasing firing rates and one for PSTHs with decreasing firing rates (Fig. 3B).
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Spike firing was correlated with motor parameters
A significant (t-test P < 0.05) difference in firing rate for reaches to ipsilateral space versus reaches to contralateral space, was observed in 27% of the cells (21 of 78) when reaching with either arm (Fig. 4A). Thirteen cells exhibited this correlation during ipsilateral arm reaching, whereas 12 cells did so during contralateral arm reaching. When the preferred space—ipsilateral space or contralateral space—was calculated for both the ipsilateral and the contralateral arm for each of the 21 significantly correlated cells, most cells preferred reaching to the same region of space for both arms (n = 15). There was also a bias for both arms to prefer reaches to contralateral space (n = 10) over ipsilateral space (n = 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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). The time course of firing rate modulations we observed in the lateral cerebellar cortex during reaching were much longer, on the order of several hundreds of ms (Figs. 2 and 3B), and when aligned on the occurrence of saccades our data did not reveal sharp transients in firing rate modulation (data not shown). The time course of firing rate modulation during reaching also argues against a correlation with gaze direction as changes in modulation occurred at times when gaze was static (Figs. 2 and 3D). On the basis of these observations, we think that it is unlikely that the correlation of firing rate modulation with bilateral reaching movements can be explained solely in terms of covert ipsilateral muscle contractions or oculomotor factors. However, with the data presented here, these possibilities cannot be absolutely excluded. It is also possible that the results presented here include modulations by oculomotor factors in addition to reaching, as has been observed in several cerebral cortical areas (Batista et al. 1999; Boussaoud et al. 1998; Mushiake et al. 1997).
Studies in the anterior lobe and intermediate zone of the posterior lobe revealed that in a majority of cells simple spike firing was correlated with reach direction in space (Fortier et al. 1989, 1993) and reach speed (Coltz et al. 1999; Mano and Yamamoto 1980; Marple-Horvat and Stein 1987) during reaching with the ipsilateral arm. We found that spike firing in lateral cerebellar cortical cells exhibited spatial preferences and reach speed tuning during reaches using either the ipsilateral or contralateral arm. These cells tended to prefer reaching to the same region of space and at the same speed for both the ipsilateral and the contralateral arms. In the current study, only a minority of cells were correlated with motor parameters, so it was possible that a large percentage of cells in the lateral cerebellum were encoding nonmotor aspects of task performance such as attention or sensory processing (Allen et al. 1997; Gao et al. 1996). We think it is more likely that the relatively small number of cells observed with direction and speed tuning was related to the limited range of reach directions used. In the studies of Fortier et al. and Coltz et al., reaching subtended a full 360° with preferred directions, and the associated preferred speed, distributed uniformly in this range. In the current study, reaching subtended <45° so that a substantial number of cells with significant motor parameter correlation may have gone undetected. As ipsilateral arm and contralateral arm reaches began in opposite hemi-fields, the visual input would have been different for each arm. We found that in most cells the firing rate modulation was similar for both arms. This argues against the firing rate modulation in these cells being correlated with visual stimuli generated by the reaching movements rather than the reaching movements themselves. However, the possibility that cells which did not encode motor parameters may have been correlated with attention or visual stimuli rather than movement cannot be excluded.
The medial regions—anterior lobe and intermediate zone of the posterior lobe— of the cerebellum have long been known to play a role in motor control of the ipsilateral limbs (Coltz et al. 1999; Fortier et al. 1989, 1993; Fu et al. 1997; Holmes 1939; Mano and Yamamoto 1980; Marple-Horvat and Stein 1987; Thach 1968, 1970, 1978). In light of these reports, the finding of spike firing in the lateral cerebellum being in any way correlated with contralateral arm movements appears anomalous. However, these apparently contradictory finding may simply be the result of the differing anatomical locations explored—medial versus lateral. We suggest that there may be a medial-lateral gradient of function in the cerebellar cortex with direct control of motor parameters of the ipsilateral limbs being represented in medial regions while the lateral regions exert control over motor parameters that are abstracted from the effector limb. This idea is supported by the finding that lesion of the lateral cerebellum resulted in little or no ataxia in human patients (Martin et al. 1996) and the differing anatomical connectivity of these two regions.
The anatomic connectivity of the lateral cerebellum forms a complex closed loop system with large areas of the frontal cortex—including Brodmann's areas 8, 9, 10, 46—and parietal cortex—including inferior and superior parietal lobules (Asanuma et al. 1983; Clower et al. 2001; Dum and Strick 2003; Glickstein et al. 1994; Middleton and Strick 2001; Orioli and Strick 1989; Schmahmann and Pandya 1989, 1990, 1995, 1997). Spike firing in frontal and parietal cortices, specifically primary motor cortex, area 46d, supplementary motor cortex, and the posterior parietal cortex has been correlated with movements and motor parameters of both the ipsilateral and contralateral arms (Cisek et al. 2003; Donchin et al. 2002; MacKay 1992). We found that spike firing in the cerebellar cortex of the lateral hemisphere was correlated with reaching movements and encoded reach parameters irrespective of the effector limb. Taken together these findings suggest that the lateral cerebellar cortex may be working with areas of the frontal and parietal lobes in the planning and coordination of movement at a level of encoding that is abstracted from strictly kinematic or myotopic reference frames.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Present address of B. Greger: Div. of Biology, Caltech, Mail Code 216-76, 1200 E. California St., Pasadena, CA 91125.
GRANTS
This research was funded by National Institute of Neurological Disorders and Stroke Grant R01 NS-12777.
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FOOTNOTES |
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Address for reprint requests and other correspondence: B. Greger, Caltech, Div. of Biology, MC 216-76, 1200 E. California Blvd., Pasadena, CA 91125 (E-mail: greger{at}vis.caltech.edu).
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REFERENCES |
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