1 Research Service (151S), Veterans Affairs Medical Center; 2 Department of Neurosurgery and 3 Department of Neuroscience and Physiology, State University of New York Health Science Center at Syracuse, Syracuse, New York 13210
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ABSTRACT |
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Hoffman, Donna S. and Peter L. Strick. Step-tracking movements of the wrist. IV. Muscle activity associated with movements in different directions. J. Neurophysiol. 81: 319-333, 1999. We examined the patterns of muscle activity associated with multiple directions of step-tracking movements of the wrist in humans and monkeys. Human subjects made wrist movements to 12 different targets that required varying amounts of flexion-extension and radial-ulnar deviation. Wrist muscles displayed two patterns of electromyographic (EMG) modulation as movement direction changed: amplitude graded and temporally shifted. The amplitude-graded pattern was characterized by modulation of the quantity of muscle activity that occurred during two distinct time periods, an agonist burst interval that began before movement onset and an antagonist burst interval that began just after movement onset. The timing of muscle activity over the two intervals showed little variation with changes in movement direction. For some directions of movement, EMG activity was present over both time intervals, resulting in "double bursts." Modulation of activity during the agonist burst interval was particularly systematic and was well fit by a cosine function. In contrast, the temporally shifted pattern was characterized by a gradual change in the timing of a single burst of muscle activity. The burst occurred at a time intermediate between the agonist and antagonist burst intervals. The temporally shifted pattern was seen less frequently than the amplitude-graded pattern and was present only in selected wrist muscles for specific directions of movement. Monkeys made wrist movements to 8-16 different targets that required varying amounts of flexion-extension and radial-ulnar deviation. These movements were performed more slowly than those of human subjects. The wrist muscles of the monkeys we examined displayed the amplitude-graded pattern of activity but not the temporally shifted pattern. Stimulation of individual wrist muscles in monkeys resulted in wrist movements that were markedly curved, particularly for the wrist extensors. These results indicate that step-tracking movements of the wrist are generated mainly by using the amplitude-graded pattern to modulate muscle activity. We propose that this pattern reflects a central process that decomposes an intended movement into an agonist, "propulsive" component and an antagonist, "braking" component. Separate bursts of muscle activity then are generated to control each component. On the other hand, we argue that the temporally shifted pattern may function to reduce the amount of movement curvature associated with the activation of wrist muscles.
A central question in systems neuroscience is how the nervous system generates the complex spatiotemporal commands needed to vary the speed, amplitude and direction of limb movement. We have chosen to investigate this issue by studying the generation of step-tracking movements of the wrist. Step-tracking movements are of interest because the muscle activity associated with them occurs in distinct bursts. Furthermore there is evidence that initial bursts in agonist and antagonist muscles are centrally generated (see Hoffman and Strick 1990 Our results are based on an examination of patterns of muscle activity in six normal human subjects (2 males, 4 females, aged 24-43 yr) and in three nonhuman primates (monkey A: Macaca mulatta, 5.4 kg; monkey B: M. nemestrina, 5.8 kg; monkey C: M. mulatta, 4.2 kg). The same three monkeys also were used for the results reported in Hoffman and Strick (1993) Experimental setup and task
Each human subject sat in a chair that supported the forearm and elbow of the dominant (right) limb. The forelimb was held in the neutral position, midway between full pronation and full supination. The subject grasped the handle of a two-axis manipulandum. This device was described and illustrated in a prior study (Fig. 1 of Hoffman and Strick 1986b
Data acquisition
We obtained electromyographic (EMG) recordings from four wrist muscles: extensor carpi radialis longus (ECRL); extensor carpi radialis brevis (ECRB); extensor carpi ulnaris (ECU); and flexor carpi radialis (FCR) (see Table 1). EMG activity was recorded with surface electrodes (Liberty Mutual Myoelectrodes, Boston, MA) that have contact surfaces spaced 1.3 cm apart. The electrodes were positioned until they recorded large responses with wrist movement and minimal activity with finger movement. Three subjects were examined in two or more separate recording sessions to verify that the pattern of activity for single muscles was repeatable. One subject was examined using both surface electrodes and intramuscular fine-wire electrodes in ECRL and ECRB to verify the reliability of surface recordings from these muscles. The technical details for fine-wire electrodes are described below (see, Experiments in nonhuman primates). An analysis of activity in flexor carpi ulnaris is not included in this study because we were not convinced that surface recordings from this muscle provided a reliable indication of its activity.
Data analysis
All trials were examined individually and occasional odd trials (i.e., trials that were slow or were inaccurate in direction or amplitude) were eliminated from the database. The potentiometer and EMG signals were aligned on movement onset (defined by the computer as a 1.2° change in either x or y) and averaged for each direction of movement. Further analysis was performed using averaged data.
Experiments in nonhuman primates
Each monkey sat in a primate chair with its forearm supported and grasped the handle of a scaled-down version of the two-axis manipulandum described above. Monkeys naturally displayed considerable tonic activity in ECRL and ECRB when holding the manipulandum handle in the neutral position even though no weight was added to the handle. The task that the monkeys performed was similar to that in the human study. They initiated a trial by placing the cursor in the target, which was centered on the screen. The inside diameter of the target measured ~3.5° of wrist movement. After a variable hold period, the target was stepped from the central position to one of 8 or 16 different locations equally spaced around the central position (see Fig. 1, right). The monkey was required to place the cursor in the new target location with a movement time <200 ms to receive a small juice reward. The required change in wrist angle was 20°. Monkeys received considerable training in this task (800-1,500 trials per day for 2-7 yr) so that their performance was quite stable.
Our findings will be presented in three sections. In the first, we will briefly describe the kinematics of step-tracking movements of the wrist in the human and the monkey. Because we previously have reported our studies of the kinematics of movements in a single plane (Hoffman and Strick 1986b Kinematics
When human subjects performed step-tracking movements in different directions, the initial 50-70 ms of movement occurred in a nearly straight line and was well directed toward the target (Fig. 1, left, Patterns of wrist muscle activity in humans
Each of the four prime movers of the wrist joint (ECRL, ECRB, ECU, FCR) displayed a well-defined agonist burst for movements close to the muscle's "pulling direction" (Fig. 2, A, target 12; C, target 12) (see also Hoffman and Strick 1990
Modulations with changes in movement direction
When subjects generated wrist movements in directions that differed from the "best" agonist or antagonist direction for a muscle, the activity was modulated in either of two spatiotemporal patterns, termed amplitude graded and temporally shifted. The key feature of the amplitude-graded pattern (Hoffman and Strick 1986a
Temporally shifted
In some instances, when movements differed from the best agonist and best antagonist directions, we observed a second pattern of muscle activity, termed "temporally shifted" (Fig. 2C, target 9). This pattern was characterized by a single burst of activity, the peak of which lagged that of a normal agonist burst but led that of a normal antagonist burst. We defined a temporally shifted burst as a burst with a peak that occurred in the interval after peak acceleration and before peak velocity.1 This interval is indicated by the cross-hatching in Fig. 7. Single bursts in this interval displayed a gradual and systematic shift in their timing from just after the agonist burst interval to just before the antagonist burst interval (Figs. 3, C and F; and 7, B, targets 8-11; C, targets 9-12; and D, targets 6-9). Temporally shifted bursts have been described previously in studies of shoulder and elbow muscle activity during pointing movements (Flanders et al. 1994 Patterns of wrist muscle activity in monkeys
The basic patterns of EMG activity associated with wrist movements of monkeys differed from those of humans in three respects. First, agonist bursts in the wrist extensor muscles of monkeys were prolonged and sometimes lasted 300 ms (Hoffman and Strick 1993
Electrical stimulation of muscle in monkey
We stimulated each wrist muscle to determine its "pulling direction." Stimulation was tested while the monkey held the manipulandum in the central hold position. This required tonic activity in ECRL and ECRB. However, this muscle tension was the same as that needed for normal performance of the step-tracking task. Overall, the movements produced by muscle stimulation were markedly curved (Fig. 13). The initial evoked movement was followed by a marked deviation of the wrist toward extension or flexion, depending on whether the muscle was a flexor or extensor. Because a variety of factors could produce the later curved portion of the evoked movement, we defined the pulling direction of a muscle as the direction of the initial 40-50 ms of evoked movement.
In humans, movement direction is controlled by modulating muscle activity in two distinct patterns, termed amplitude graded and temporally shifted. Our results indicate that the amplitude-graded pattern is the one used most frequently by humans to generate step-tracking movements of the wrist. The amplitude-graded pattern is characterized by modulation of the quantity of muscle activity during two distinct time periods, corresponding to agonist and antagonist burst intervals. As a result, for some directions of movement, EMG activity appears as double bursts because it is present during both time intervals. Examples of double bursts have been observed previously not only in wrist muscles (Hoffman and Strick 1986a Central generation of muscle activity
How does the CNS generate the complex spatiotemporal patterns of muscle activity that are necessary for determining the direction of wrist movement? Although many central sites may participate in this process, it is likely that the primary motor cortex (M1) plays a key role. Lesions or inactivation of M1 lead to disruption of the normal patterns of muscle activity associated with limb movements (e.g., Hoffman and Strick 1995
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
for discussion of this issue). Thus an examination of the timing and modulation of these bursts provides a "window" into the motor commands generated by the CNS. The wrist joint has the added complexity of rotating in two axes; this makes it particularly interesting for investigations into the neural control of movement direction.
, 1993
). Here we will report on the muscle activity associated with movements in different directions. In preliminary experiments, we observed that wrist movements in different directions were produced by agonist and antagonist bursts that were graded in amplitude but relatively fixed in time (Hoffman and Strick 1986a
). We proposed that during the programming of movement direction, the nervous system could perform a vector analysis, decomposing "intended" movement vectors into agonist and antagonist components for each muscle (pg. 290, Hoffman and Strick 1986a
). In other experiments, we provided evidence that the two components are generated separately (Hoffman and Strick 1990
, 1993
; Waters and Strick 1981
). However, they are ultimately summed so that, for some directions of movement, single muscles show "double bursts," i.e., muscle activity over both the agonist and antagonist burst intervals. Thus our prior results suggested that the nervous system determines the direction of wrist movement by modulating the amplitude of two bursts of muscle activity whose time course is relatively fixed.
and Flanders et al. (1994
, 1996)
proposed an alternative hypothesis. These authors observed that individual shoulder and elbow muscles displayed a single burst of activity, the timing of which shifted gradually with the direction of a pointing movement. The burst could occur later than a normal agonist burst but earlier than a normal antagonist burst. These authors proposed that modification of the timing of a single burst of activity in individual muscles is the primary mechanism used by the nervous system to specify movement direction.
, 1997
).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
. The experiments were conducted according to National Institutes of Health guidelines and were approved by the relevant institutional committees overseeing human and animal experiments. All of the human subjects gave their informed consent. We first will describe the procedures for the human experiments and then describe those for the monkey studies.
). It is a lightweight, low-friction device with a moment of inertia of ~0.0025 kg × m2 in the radial-ulnar direction. The handle of the manipulandum rotates in the vertical and horizontal axes. Two potentiometers are coupled to the device to measure the angles of the wrist in the planes of radial-ulnar deviation and flexion-extension.
,b
, 1990
). To initiate a trial, the subject placed the cursor inside the target, which was positioned at the center of the screen. This target location caused the wrist to be in the neutral position for the start of each trial. After a variable hold period, the target jumped to 1 of 12 different locations on the screen, arranged like the numerals on a clock (see Fig. 1, left). The subject was required to perform a "step-tracking" movement of the wrist; this placed the cursor in the new target location. Subjects were instructed to move as rapidly and accurately as possible to the new location. Different targets were presented in clockwise order, starting with target 12 and ending with the same target. Data were collected for 25 successive movements to each target. In different experiments, target locations could require a 5, 15, 20, or 25° change in wrist angle. In this report, we will focus on the patterns of muscle activity for the intermediate amplitudes of movement (15 or 20°). Subjects were allowed a small amount of practice (~5 trials to several of the targets) before the initiation of data collection.
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FIG. 1.
Trajectories of wrist movements for humans and monkeys. Left: average trajectories of subject 1. Movements were performed as fast and as accurately as possible from the central target location to 12 different peripheral target locations, arranged like the numerals on a clock. Acquisition of the peripheral targets required a 15° change in the angle of the wrist joint. Each trace is the average of 20-25 movements to the same target location. Tick marks indicate 30 and 50 ms after movement onset. , 25-75% of the distance between the central and peripheral targets. Right: average trajectories of monkey C. Monkey was trained to make rapid movements (movement time <200 ms) from the central target location to 8 different peripheral targets. Acquisition of the targets required a 20° change in the angle of the wrist joint. Each trace is the average of 12-29 movements to the same target location. Tick marks indicate 50 and 100 ms after movement onset.
, 25-75% of the distance between the central and peripheral targets. Ext, extension; Flx, flexion; Rad, radial deviation; Uln, ulnar deviation.
View this table:
TABLE 1.
Experimental subjects
= 10 ms) (see Gottlieb and Agarwal 1970
). Rectified and filtered EMG signals, along with the two position signals from the two-axis manipulandum, were digitized at 1.25 kHz and stored on a DEC PDP 11/34 computer.
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FIG. 8.
Temporal shift and double bursts in ECRL. A: amplitude-graded pattern in subject 2 (see also Fig. 7A). Red area at time = 0-25 indicates the occurrence of agonist bursts (Ag). Several orange peaks at time = 50-75 indicate the occurrence of antagonist bursts (Ant). Note that a sudden transition occurs between the 2 areas, with double bursts (Db) in the transitional area. B: amplitude-graded and temporally shifted patterns in subject 6 (see also Figs. 3, A-C, and 7B). Note that a sudden transition occurs between agonist and antagonist bursts near wrist extension and is marked by double bursts (Db). Gradual transition occurs between agonist and antagonist bursts for wrist flexion and is marked by temporally shifted bursts (Sh). Ag (arrow) and Antag (arrow) indicate the best agonist and antagonist directions for each muscle. Db (bracket) indicates movement directions with double bursts. Sh (bracket) indicates movement directions with temporally shifted bursts. Time scale is in ms; 0 = onset of movement. EMG scale: 100 = maximum EMG observed, 0 = EMG level during hold period.
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FIG. 9.
Temporal shift and double bursts in several wrist muscles. A: amplitude-graded pattern in flexor carpi radialis of subject 3. Note that a sudden transition occurs between agonist and antagonist bursts and is marked by double bursts (Db). B: amplitude-graded and temporally shifted patterns in extensor carpi ulnaris of subject 6 (see also Figs. 3, D-F, and 7D). Dark blue area indicates that muscle activity occurring during the hold period was suppressed for some directions of movement. Note that a gradual transition occurs between agonist and antagonist bursts for combined wrist flexion + ulnar deviation and is marked by temporally shifted bursts (Sh). C: amplitude-graded and temporally shifted patterns in extensor carpi radialis brevis of subject 1 (see also Fig. 7C). Note the occurrence of double bursts for movements near wrist extension and the occurrence of temporally shifted bursts for movements near wrist flexion.
). This method of defining temporal intervals for agonist and antagonist activity avoided the difficulty of determining the onset and endpoint of each burst. Finally, we integrated EMG activity for each movement direction separately during each of the two burst intervals. Occasionally, agonist and antagonist intervals overlapped slightly in time. When this occurred, we shortened the integration interval for the agonist burst and delayed the integration interval for the antagonist burst by equal amounts so that the intervals for agonist and antagonist activity were nonoverlapping.
. The regression equation was: y = a + b*sin x + c*cos x, where x = movement direction (in radians); a, b, and c = regression coefficients. The methodology of Georgopoulos et al. was modified to account for the fact that EMG activity was absent for some directions of movement. When EMG was absent, we decreased the weighting of 1 or 2 near zero values to 0.01, whereas the remaining points had a weighting of 1.0 in the calculation of the regression equation. The decreased weighting of points resulted in a cosine that more accurately fit the larger values of EMG. This adjustment of weights reduced the resulting R2 values slightly. The peak of the cosine defined a "preferred direction" for each muscle's agonist or antagonist activity. The peak was calculated by determining
= tan
1 b/c. Then peak =
if b > 0 and c > 0; peak =
+ 180° if c < 0; peak =
+ 360° if b < 0 and c > 0. The preferred directions obtained in separate recordings from the same muscle in a single subject were averaged to obtain a single value for each muscle in a subject.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
), this section will emphasize the special features of movements in different directions. The next section will describe how the spatiotemporal patterns of EMG activity are modulated to produce different directions of wrist movement in humans. The final section will compare and contrast the EMG patterns observed in monkeys with those of humans.
). All movements overshot the targets considerably and then curved back toward the target. The step-tracking movements of human subjects were quite rapid. Radial and ulnar deviation movements to the 15° targets had mean durations of ~80 ms; flexion and extension to the 15° targets had mean durations of ~110 ms. Mean peak tangential velocities for these movements were 550°/s (radial + ulnar deviation) and 440°/s (flexion + extension). The corresponding peak tangential accelerations were 18,900 and 13,400°/s2.
). Step-tracking movements of monkeys overshot the targets by far less than the movements of humans. The movements of monkeys were rapid, but movement durations were approximately twice those of humans and peak velocities and accelerations were less than half those of humans. Movements of 20° performed by monkeys had mean durations of ~200 ms. Mean peak tangential velocities for these movements were 218°/s (radial + ulnar deviation) and 155°/s (flexion + extension). The corresponding peak tangential accelerations were 4,300 and 2,400°/s2.
). Agonist bursts generally began 30-50 ms before movement onset, peaked before the peak of acceleration, and had a duration of 75-100 ms. However, in some subjects, the agonist bursts recorded from extensor muscles were prolonged (e.g., Fig. 3D) (see also Hoffman and Strick 1993
).
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FIG. 2.
Two patterns of electromygraphic (EMG) modulation associated with wrist movements in different directions. A: amplitude-graded pattern. An agonist burst occurred for movements to target 12 (solid line). An antagonist burst occurred for movements in the opposite direction (target 6, long dashed line). Two bursts of activity, one at the time of an agonist burst and the other at the time of an antagonist burst, occurred for movements in an orthogonal direction (target 9, short dashed line). ECRL, extensor carpi radialis longus (surface recording). B: tangential velocity traces for the movements associated with the EMGs shown in A. C: temporally shifted pattern. An agonist burst occurred for movements to target 12 (solid line). An antagonist burst occurred for movements in the opposite direction (target 6, long dashed line). A single burst of activity that was shifted in time, compared with agonist and antagonist bursts, occurred for movements in an orthogonal direction (target 9, short dashed line). ECRBi, extensor carpi radialis brevis (intramuscular recording). D: tangential velocity traces for the movements associated with the EMGs shown in C. All EMG traces were full-wave rectified, filtered ( = 10 ms), and averaged (n = 20-25). Time scale is in ms; 0 = onset of movement.
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FIG. 3.
Patterns of EMG modulation for 2 different muscles in a single subject. A: amplitude grading of the agonist burst in ECRL for movements to targets 1 (solid line), 2 (long dashed line), 3 (dot-dashed line), and 4 (short dashed line). Vertical dashed lines indicate the beginning and end of the agonist burst interval for this EMG recording. Note: 2 small bursts, 1 during the agonist burst interval and 1 during the antagonist burst interval, occurred for movements to target 4. B: amplitude grading of the antagonist burst in ECRL for movements to targets 7 (solid line), 5 (long dashed line), and 4 (short dashed line). Vertical dashed lines indicate the beginning and end of the antagonist burst interval. C: temporally shifted burst in ECRL for movements to targets 10 (long dashed line) and 9 (short dashed line). An agonist burst occurred for movements to target 11 (solid line), and an antagonist burst occurred for movements to target 7 (solid line). Vertical dashed lines indicate the agonist and antagonist burst intervals. D: amplitude grading of the agonist burst in ECU for movements to targets 5 (solid line), 4 (long dashed line), and 2 (short dashed line). E: amplitude grading of the antagonist burst in ECU for movements to targets 1 (solid line), 12 (long dashed line), and 11 (short dashed line). Two bursts, 1 during the agonist burst interval and 1 during the antagonist burst interval, occurred for movements to target 1. F: temporally shifted burst in ECU for movements to target 8 (short dashed line). An agonist burst occurred for movements to targets 6 (solid line) and 7 (long dashed line), and an antagonist burst occurred for movements to targets 12 (solid line) and 9 (dot-dashed line). ECU, extensor carpi ulnaris. All EMG traces were full-wave rectified, filtered ( = 10 ms), and averaged (n = 20-25). Open triangles: times of peak acceleration. Closed triangles: times of peak velocity. Time scale is in ms; 0 = onset of movement.
). On average, the agonist burst interval began ~20 ms before movement onset (Fig. 3, A and D). The antagonist burst interval began ~35 ms after movement onset (Fig. 3, B and E). The end of the agonist burst interval usually coincided with the start of the antagonist burst interval.
) was the presence of two bursts of muscle activity: one during the agonist burst interval and the other during the antagonist burst interval (Fig. 2A, target 9). The "double bursts" apparent in averages of EMG activity also were visible in single trials (Fig. 4C) and thus were not an artifact of averaging.
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FIG. 4.
EMG patterns on single trials. A: agonist burst for 2 movements to target 1 (best agonist direction). B: antagonist burst for 2 movements to target 6 (best antagonist direction). C: 2 small bursts, 1 during the agonist burst interval and 1 during the antagonist burst interval, for 2 movements to target 4. Vertical dashed lines indicate the agonist and antagonist burst intervals. EMGs were full-wave rectified and filtered ( = 10 ms). ECRL, extensor carpi radialis longus. Time scale is in ms; 0 = onset of movement. Vertical scale in B and C is twice that in A.
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FIG. 5.
Cosine tuning of agonist burst in human and monkey wrist muscles. A: best cosine fit to the amplitude of the agonist burst in a human subject, R2 = 0.97. B: poorest cosine fit to the amplitude of the agonist burst in a human subject, R2 = 0.84. ECRB, extensor carpi radialis brevis. C: cosine tuning of ECU in monkey C, R2 = 0.94. D: cosine tuning of ECRB in monkey C, R2 = 0.93. *, points that were given a weighting of 0.01 in the regression (see METHODS). , bursts that were temporally shifted. Abscissa: numbers indicate target number. Ordinate: 0 = EMG level during the hold period; 100 = maximum integrated EMG for any direction of movement; negative = decrease in EMG below level during the hold period.
60° between subjects. All muscles had prominent agonist activity (
25% of the integrated EMG present for the best agonist direction) for movements to six or more targets (i.e., at least one-half of the targets). Thus even though individual muscles displayed a specific preferred direction, muscle activity was broadly tuned during the agonist burst interval (Fig. 6).
View this table:
TABLE 2.
Preferred directions
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FIG. 6.
Directional tuning of the agonist burst in 4 wrist muscles of subject 3. , integral of EMG activity during the agonist burst interval for 12 different directions of movement.
, preferred direction for each muscle. Preferred direction was determined from the cosine fit for each recording. Outer circle indicates the maximum integrated EMG activity observed for any of the 12 directions of movement.
, bursts that were temporally shifted. FCR, flexor carpi radialis.
0.54. Of these nine recordings, six displayed a preferred direction of antagonist activity that was not directly opposite to (i.e., differed by <170° from) the same muscle's preferred direction of agonist activity (Table 2). Restricting comparisons of preferred directions to the six recordings for which antagonist activity was well fit by a cosine function (i.e., R2 > 0.8), four of these had preferred directions of antagonist and agonist activity that were not directly opposite to each other. These observations suggest that activity during the antagonist burst interval is tuned separately from activity during the agonist burst interval. The remaining 8 of 17 EMG recordings had a nonsignificant R2 and showed little variation in the amplitude of EMG during the antagonist burst interval associated with changes in movement direction.
50 ms (Fig. 7, A, targets 3-4, 9-10; B, targets 4-5; C, targets 3-4; and D, targets 1-2). On the basis of all of our observations on the amplitude-graded pattern, we conclude that one strategy used by the nervous system to determine movement direction is to adjust the amplitude, but not the timing, of agonist and antagonist bursts in multiple muscles at a single joint.
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FIG. 7.
Analysis of temporal shift. A: absence of temporal shift in ECRL. B: temporal shift in ECRL for movements to targets 9 and 10. C: temporal shift in ECRB for movements to targets 10 and 11. D: temporal shift in ECU for movements to target 8. Hatched area in each panel indicates the interval between peak acceleration and peak velocity. Ag (arrow) and Antag (arrow) indicate the best agonist and antagonist directions for each muscle. Abscissa: numbers indicate target number. Ordinate is in ms; 0 = onset of movement.
, 1996
).
, 1995
). Second, antagonist bursts were small and were observed consistently only in monkey C. Third, ECRL and ECRB displayed considerable tonic activity (~30% of the maximum agonist burst) during the hold period and had a complex pattern of activity during movement (Fig. 11). These features of the activity of wrist muscles in monkeys made it more difficult to identify double bursts and temporally shifted bursts.
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FIG. 11.
Complex pattern of activity in ECRL and ECRB of monkey C. A: agonist burst for movements in the best agonist direction. Vertical dashed lines indicate the agonist burst interval. B: suppression of tonic activity, followed by an antagonist burst, for movements in the best antagonist direction. Vertical dashed lines indicate the agonist and antagonist burst intervals. C: complex pattern of activity for movements orthogonal to the best agonist direction. Vertical dashed lines indicate the agonist and antagonist burst intervals. D: agonist burst for movements in the best agonist direction. Vertical dashed lines indicate the agonist burst interval. E: suppression of tonic activity, followed by a small antagonist burst, for movements in the best antagonist direction. Vertical dashed lines indicate the agonist and antagonist burst intervals. F: complex pattern of activity for movements orthogonal to the best agonist and antagonist directions. Vertical dashed lines indicate the agonist and antagonist burst intervals. All EMG traces were full-wave rectified, filtered ( = 10 ms), and averaged (n = 10-18). Open triangles: times of peak acceleration. Closed triangles: times of peak velocity. Time scale is in ms; 0 = onset of movement.
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FIG. 10.
Amplitude-graded pattern in monkey C. A: amplitude grading of the agonist burst for movements to target locations 3:45 (solid line), 3 (long dashed line), and 2:15 (short dashed line). Vertical dashed lines indicate the beginning and end of the agonist burst interval. B: amplitude grading of the antagonist burst for movements to target locations 7:30 (solid line), 8:15 (long dashed line), and 9 (short dashed line). Vertical dashed lines indicate the beginning and end of the antagonist burst interval. C: double burst for movements to target location 6:45. EMG traces were full-wave rectified, filtered ( = 10 ms), and averaged (n = 12-29). Open triangles: times of peak acceleration. Closed triangles: times of peak velocity. Time scale is in ms; 0 = onset of movement.
). In the monkey, the concept of double bursts needs to be modified to include the summation of three elements: the early antagonist suppression (e.g., Fig. 11, B and E) as well as the agonist burst and the antagonist burst. The complete shape of the antagonist suppression is unknown because the absence of EMG activity may not indicate the full extent of motoneuron hyperpolarization that occurs. However, if the early suppression possessed an exponential decay, then the sum of the suppression with an agonist burst might account for the delayed onset of the first burst of EMG activity seen in Fig. 11, C and F.
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FIG. 12.
Directional tuning of muscle activity in monkey C. Closed circles plot increases in muscle activity during the agonist burst interval. Open circles plot decreases in muscle activity during the agonist burst interval. Closed arrows point toward the muscle's preferred direction, which was determined from the cosine fit. Open arrows point toward the muscle's "pulling direction," i.e., the initial direction of movement resulting from intramuscular stimulation. Outer circle indicates the maximum integrated EMG activity observed for any of the 16 directions of movement.
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FIG. 13.
Wrist movements evoked by intramuscular stimulation in monkey A. Each trace represents the average of 8 muscle stimulations (600 µA to 2 mA, 10 pulses at 50/s). Time period illustrated is from movement onset to 105-145 ms later. Tick marks indicate 20-ms intervals, 100 ms after movement onset. Movement amplitude has been rescaled so that the maximum movement amplitude is the same for all muscles.
30° in different sessions in the same monkey. This variation appeared to depend on the specific location of the EMG electrodes within FCR. The initial pulling direction was close to radial deviation for two muscles (ECRB, ECRL), close to ulnar deviation for two muscles (ECU, FCU), and 30° away from flexion for one muscle (FCR). No muscle had an initial pulling direction toward wrist extension.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
) but also in muscles that move the elbow (Fig. 9 in Sergio and Ostry 1995
; Fig. 8A, 4 and 6, in Wadman et al. 1980
) and shoulder (Fig. 5, directions 6 and 8 in Pellegrini and Flanders 1996
). Thus the amplitude-graded pattern of muscle activity appears to be an essential feature of arm movements at proximal as well as distal joints.
). These components are graded individually in amplitude but are relatively fixed in time. Double bursts are created when separate agonist and antagonist components for each muscle are summed at the level of the motoneuron pool. Our hypothesis implies that the signals for agonist and antagonist bursts are, at some level of the nervous system, independently generated (see also Sergio and Ostry 1995
).
; Flanders and Soechting 1990
; Flanders et al. 1996
). We found that the agonist burst was modulated according to a cosine function. In some cases, the antagonist component also was cosine tuned. Surprisingly, in most instances, the preferred directions for agonist and antagonist activity differed by <170° and therefore, were not directly opposite to each other (see also Flanders et al. 1996
). This result provides further support for the proposal that the neural processes that determine the properties of antagonist muscle activity are partially separate from those that determine agonist activity (Hoffman and Strick 1986a
, 1990
).
; Flanders et al. 1994
, 1996
; Karst and Hasan 1991
; Wadman et al. 1980
). Our results demonstrate that this pattern also occurs in distal muscles. The presence of this pattern of activity in both proximal and distal muscles and the size of temporally shifted bursts (i.e., intermediate between agonist and antagonist bursts in the same muscle) highlight the functional importance of this pattern of muscle activity.
). These observations suggest that the temporally shifted pattern is not simply an alternative to the amplitude-graded pattern. Rather, we believe that the temporally shifted pattern serves a unique function that is required for a specific set of movement conditions.
). As a consequence, the anatomic arrangement of single wrist muscles in humans also should produce curved movement trajectories. Finally, in comparing our human and monkey results, there appeared to be an association between the presence or absence of temporally shifted bursts and the extent to which the initial movement trajectories were curved. Human subjects displayed temporally shifted bursts and could make wrist movements that displayed little curvature during the initial portion of the movement trajectory (Fig. 1, left,
). In contrast, monkeys did not display clear examples of temporally shifted bursts, and the trajectories of their movements began to curve ~50 ms after movement onset for some directions of movement (Fig. 1, right,
). With specific and extended training, monkeys might be induced to generate wrist movements that were more similar to those of humans. If so, we predict that a straightening of movement trajectories in monkeys would be associated with the emergence of temporally shifted bursts.
concerning the control of reaching movements. They proposed that straight reaching movements are achieved by "staggered joint interpolation," i.e., by staggering the onset of shoulder and elbow joint movements. This would be accomplished by adjusting the time of onset of EMG activity at these two joints. Wadman et al. (1980)
also proposed that the time shift between activation of elbow and shoulder muscles was an important factor in determining trajectory shape. Our proposal contrasts with the suggestion of Pellegrini and Flanders (1996)
that asynchronous patterns of muscle activity may contribute to hand path curvature during reaching movements. Thus we believe that the exceptional skill of human subjects in generating relatively straight trajectories, whether at the shoulder or the wrist, may depend on their ability to adjust accurately not only the amplitude but also the timing of EMG bursts.
; Matsumura et al. 1991
). Specifically, we have shown that removal of the arm area in M1 results in a misdirection of step-tracking movements of the wrist due to changes in the spatial and temporal pattern of muscle activity about the wrist joint (Hoffman and Strick 1995
).
; Fu et al. 1995
; Georgopoulos et al. 1982
; Kalaska et al. 1989
; Schwartz et al. 1988
). The similarities between neuron and muscle activity suggest that grading of the amplitude of agonist activity in wrist muscles may be due, in part, to the directional properties of M1 neurons.
; see, however, Scott 1997
; Scott and Kalaska 1997
). A uniform distribution is a key requirement of the population vector hypothesis. According to this hypothesis, each M1 neuron active for a particular movement makes a vectorial contribution to movement direction based on its preferred direction (Georgopoulos et al. 1988
). The magnitude of the contribution is proportional to the cell's discharge. It will be important to determine the distribution of preferred directions for wrist-related neurons in M1 and to compare this with the distribution of preferred directions for wrist muscles. The differences between these two distributions will provide information about the nature of the transformation that occurs between M1 and motor output from the spinal cord. Any similarities in the two distributions would suggest that the representation of motor output in M1 is not as abstract as the population vector hypothesis suggests (see also Scott 1997
; Scott and Kalaska 1997
).
). Yet our results emphasize that muscle activity occurs in distinct temporal bursts during step-tracking movements. The agonist and antagonist bursts in wrist muscles occur over separate time intervals and appear to be generated independently (see also Hoffman and Strick 1986a
, 1990
, 1993
). The demonstration that, under certain circumstances, the activity of wrist muscles in human subjects shows a temporal shift and occurs over an interval between the agonist and antagonist bursts would make the generation of spatiotemporal patterns of muscle activity even more complex in humans.
; Evarts 1974
; Murphy et al. 1982
; Smith et al. 1975
; Wannier et al. 1991
). Furthermore, M1 neurons with preferred directions close to the intended movement direction (agonist-related) should become active much earlier than neurons with preferred directions opposite to the intended movement direction (antagonist-related) (Georgopoulos et al. 1982
). As a consequence, the population vector for neurons in M1, when measured over small time intervals, would point first in the direction of net agonist activity, then would rotate to the direction of net antagonist activity, and finally would settle in the direction of net activity required to hold the limb in the final position (see Fig. 13.8 in Kalaska and Drew 1993
; Sergio and Kalaska 1998
). This prediction remains to be examined for wrist movements.
; Jamison and Caldwell 1993
; Macpherson 1988
; Schieber 1995
). In addition, we have demonstrated that temporal relations between individual muscles vary with movement direction (Flanders et al. 1996
). For example, the closely related synergists, ECRL and ECRB, are coactivated temporally for some directions of wrist movement but are active over separate time intervals for other directions of movement. Our lesion study indicates that the appropriate temporal coactivation of muscles requires an intact M1 because its removal was associated with incorrect sequencing of synergistic muscles (Hoffman and Strick 1995
). The well-known branching of single corticospinal neurons to influence neurons in multiple motor nuclei may be a mechanism for coactivating muscles (Fetz and Cheney 1980
; Kasser and Cheney 1985
; Shinoda et al. 1979
, 1981
). However, an understanding of how synergists may be activated during distinct time intervals will require greater attention to the temporal patterns of neuron activity (see also Bennett and Lemon 1996
).
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ACKNOWLEDGEMENTS |
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We thank E. Stappenbeck for expert technical assistance.
This work was supported by funds from the Department of Veterans Affairs, Medical Research and Rehabilitation Research and Development Services (PLS).
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FOOTNOTES |
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1 In general, peak acceleration occurred ~25 ms after movement onset and peak velocity occurred ~50 ms after movement onset.
Address for reprint requests: P. L. Strick, Research Service (151S), V.A. Medical Center, Syracuse, NY 13210.
Received 16 January 1998; accepted in final form 21 September 1998.
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REFERENCES |
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