Boston University, Neuromuscular Research Center, Boston, Massachusetts 02215
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ABSTRACT |
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Gottlieb, Gerald L. Muscle activation patterns during two types of voluntary single-joint movement. J. Neurophysiol. 80: 1860-1867, 1998. We examined the systematic variations in the EMG patterns during two types of single joint elbow movements. These patterns may be interpreted as exhibiting rules by which the CNS controls movement parameters. Normal human subjects performed two series of fast elbow flexion movements of 20-100° in a horizontal plane manipulandum. The first series consisted of pointing movements (PMs) from an initial position to a target; the second series consisted of reversal movements (RMs) to the same targets with an immediate return to the starting position. Both series showed kinematic and electromyographic (EMG) patterns that followed our previously described speed-insensitive strategy for controlling movement distance. Kinematic patterns of PMs and RMs were identical to about the time of peak PM deceleration. Agonist EMG bursts were also initially the same, but RM bursts ended abruptly in a silent period, whereas PM bursts declined more gradually. Antagonist EMG bursts of RMs were later than those of PMs but were not larger, contrary to our prior expectation and despite the larger net extension torque during RMs. The increase in net RM extension-directed torque that takes the limb back to its initial position appears to be a consequence of reduced flexor muscle torque rather than increased extensor muscle torque. We propose that rules for movement control may be similar for different kinds of movements as long as they are functionally sufficient for the task. However, even in a single-joint movement paradigm, physics alone, that is, the knowledge of net muscle torque and limb kinematics, is not adequate to fully predict those rules or the muscle activation patterns they produce. These must be discovered by experiment. The simplest expression of such rules may not be in terms of torque or kinematic variables but rather explicitly in terms of muscle activation patterns.
Rotation of a single joint is a common paradigm for understanding how the brain controls voluntary movement. The most frequently studied movement is simple flexion of the elbow from one stationary position to another, an action we will refer to as a "pointing" movement (PM). PMs can be described in terms of their mechanical features and the associated patterns of muscle activation or, more specifically, in terms of the modulation of the timing and amplitude of sequential bursts of electromyographic (EMG) activity in agonist and antagonist muscles, the so-called triphasic pattern (Hallett et al. 1975 Nine subjects performed sets of PMs and RMs over four distances. We recorded elbow angle from a capacitative transducer mounted on the axis of rotation of the manipulandum and tangential acceleration from a piezoresistive transducer mounted near the end of the manipulandum and computed velocity.1 DELSYS model DE2.2L surface EMG electrodes with total gain of 2,000 and band pass of 20-450 Hz recorded bicep and lateral tricep EMGs. All data were digitized at 1,000/s with a 12-bit, ±10 V A/D converter.
Data analysis
We aligned individual records to the onset of the agonist EMG burst. Data for each distance were averaged for plotting the time series shown in the next section. Seven parameters were calculated from the individual records. Accelerating impulse (Ia) was the time integral of the joint torque from movement onset to peak velocity, and decelerating impulse (Id) was the time integral of the torque from peak velocity for the same duration as for acceleration or until the torque reversed sign, whichever was first.
Forming conservative hypotheses
We assumed a conservative philosophy that PM muscle activation rules will be used to perform RMs, except when we reason from physics that they must be modified to perform the different task. This suggests specific predictions about how EMG and torque patterns will be preserved or modified across movement types.
Figure 1, A and B, shows average PMs and RMs over the four distances. Both movements demonstrate the same distinguishing characteristics in their kinematic and EMG patterns: the initially distance-independent rate of rise of the acceleration, peak velocities, accelerations, and decelerations that scale with distance. Because the muscles must move the inertia of the limb and manipulandum, we can infer from the acceleration curves that the impulse will increase with distance over both the accelerating and decelerating intervals. The early distance independence of the acceleration/torque is matched by a similar distance independence in the rate of rise of the flexor EMG burst, the muscle that is the agonist for this movement. The area of the agonist burst increases with distance but that of the antagonist burst does not show a clear correlation. Although visual inspection of Fig. 1 suggests that the flexor EMG peaks may be more strongly modulated by distance for PMs than for RMs, this was not a consistent difference. Across the nine subjects, both kinds of patterns were seen for both kinds of movements. Both the rising phase of the acceleration and the duration of the agonist burst are prolonged for longer distance movements while the latency of the antagonist burst increases.
These experiments compare reversal and PMs to test whether generalization of the standard rules is possible. The data demonstrate that for both tasks the process by which the CNS specifies the distance over which a limb segment will move preserves the initial rate of increase of the agonist EMG while the duration of that activation is scaled with distance. In comparison with PMs, the tail of the RM agonist burst is reduced. Rapid reduction of agonist activation is mechanically important because flexor muscle torque outlasts the EMG signal. Fully shutting off the agonist muscle after it accelerated the limb not only allows its flexing torque to decay more rapidly but it presumably increases the muscle's compliance, thereby allowing the antagonist muscle to more easily restretch it.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Hannaford and Stark 1985
).
) that describe how the observable variables change as a function of features of the movement task. Movement is smooth with a velocity profile that has a single peak. Joint torque is a biphasic pulse. The acceleration impulse (integral of torque from onset to peak velocity) increases with distance, load, and speed. Changes in distance or loading do not alter the initial rate of rise of the torque, despite the fact that both affect movement speed. There is a proportional change in the initial rate with deliberate changes in speed. The agonist muscle initiates a fast movement with an EMG burst, the area of which is proportional to the accelerating impulse. The rate of rise of the burst is independent of distance or load and scales with intentional changes in speed in the same way as does the initial rise in joint torque. The duration of the agonist EMG burst increases with distance and load but is not directly affected by speed, although burst duration is a difficult parameter to quantify because the end of the burst is often poorly defined. The antagonist muscle first becomes active at a relatively low level shortly after the agonist and then produces a later, more or less distinct burst of EMG activity to slow and arrest the movement at its endpoint. The onset of this burst is delayed for movements over longer distances or with greater loads and is earlier if the movement is intentionally faster. The area of the antagonist burst increases with inertial load or intended speed and decreases with viscous and elastic loads but has only a weak dependence on distance.
; Gottlieb 1993
, 1996
; Gottlieb et al. 1989a
, 1992
, 1995
, 1996
; Pfann et al. 1998
). The rules do not however answer the question of whether the CNS plans such movements in terms of torque patterns or kinematic patterns or, for that matter, in terms of muscle activation patterns themselves. Plausible arguments can be made for all three. The rules are also not complete because there are variations and features of the EMG patterns that are neglected by this very simple pulse-step description. There is more EMG activity than just bursts, and the shapes of the bursts are more complex than the filtered rectangular pulses that are proposed by these rules. These omissions were usually ignored or treated as "second-order" effects that are not essential to the understanding how the CNS controls simple movements.
; Gottlieb et al. 1989b
; Hallett et al. 1975
; LeBozec and Cnockaert 1980; Maton and Cnockaert 1980; Wadman et al. 1979
, 1980
), but few looked at other movements. Schmidt et al. (1988)
and Sherwood et al. (1988)
examined "reversal" movements (RM) that traveled to a target and immediately returned to the starting point. They showed EMG patterns similar to those of PMs but with two clearly separated bursts of activity in the agonist. They made no explicit comparison with PMs. We show here that the PM rules described previously account for many features of and are not violated by RMs but they do not predict all of our findings. The EMG and torque patterns for these different movements require us to pay more attention to the second-order features. These observations have implications for how the CNS plans its movements.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). The visual targets were two vertical poles positioned just beyond the end of the manipulandum. The initial position aligned the forearm with one pole at 50°. The origin (0°) was defined with the forearm perpendicular to the upper arm and extension was positive. For PMs, subjects were instructed to flex quickly and align the manipulandum with the second target. Speed was stressed and accuracy was mentioned. The subjects grasped a vertical handle and were easily able to align the target pole within the width of the fist within a few practice trials. After they felt ready, they made 11 fast and accurate flexion PMs on an audio cue. They were then asked to move to the same target and return to the starting position as quickly as possible. They were allowed to practice and then 11 RMs were recorded. In about one-half of the series, RMs were performed before PMs. Both tasks were easy for the subjects to perform consistently and accurately. The target poles were 20, 40, 60, and 100° into flexion from the starting position. All subjects read and signed Boston University's Human Investigation Consent Form before participating.
).
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FIG. 2.
Dependence of different EMG parameters on movement distance. Data for each subject are normalized to unity for the 8 data points. Open symbols and dashed lines are for PMs. Solid symbols and lines are for reversal movements. A: initial agonist EMG Q30. B: area of the agonist burst during acceleration to peak velocity (Qaga). C: area of the agonist EMG over 75 ms of deceleration after peak velocity (Qagd). D: area of the antagonist burst to 5% of peak velocity (Qant). E: latency of the centroid of antagonist activity (Cant). F: impulse during acceleration (Ia) and deceleration (Id).
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TABLE 1.
Measures to characterize electromyograph, kinematic, and torque patterns
; Sherwood et al. 1988
) although those studies provided no direct comparisons between movement types. Furthermore, on the basis of our expectations of the changes in movement kinematics and joint torque, we also expect that the reversal movement antagonist burst will be delayed2 when it increases in area. Our results confirmed all of the predictions, summarized in Table 1, except the one in italics for Qant.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 1.
Comparisons of average (of 10 movements) angle, velocity (computed from the measured acceleration), acceleration records, and biceps/triceps (inverted) electromyographic (EMG) records for pointing (PM) and reversal movements (RMs) over 4 distances. A: PM. B: RM. C: PM and RM with the same 40° target.
). The RM antagonist burst is delayed, but, in spite of the increase in decelerating torque that muscle would be expected to generate, its area is not larger than that of the PM burst.
; Wadman et al. 1979
). There was a strong linear variation with distance between acceleration and deceleration impulse for both movement types (Fig. 2F). Consequently, there was a statistically significant relationship between the agonist burst (Qaga) and accelerating impulse (Ia) but no statistically significant relationship between antagonist burst (Qant) and decelerating impulse (Id). These data show that column 2 of Table 1 describes RMs and PMs equally well.
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TABLE 2.
Statistical comparison of RM and PM electromyographic and torque patterns
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Lestienne 1979
). We should also note however that the reduction in agonist muscle activity during RM deceleration (i.e., the difference between the 2 lines in Fig. 2C) does scale with movement distance. We might expect from this that the force in the flexor muscle during deceleration declines more for larger than for smaller movements.
; Feldman 1980
; Morasso and Mussa Ivaldi 1982
; Viviani and Flash 1995
). Inspection of Fig. 1 suggests that an RM might be well described in such a manner; as the superposition of two, equal, and opposite PMs, one delayed with respect to the other. We performed such an analysis by subtracting the two waveforms shown in Fig. 1C. Figure 3 shows the PM from Fig. 1C and a "synthetic" PM (sPM), the difference between Fig. 1C's two movements, aligned with the PM. These two PMs differ near the end of the movement, but most of the time the sPM is just a slower version of the PM. Thus, from a kinematic point of view, the RM in Fig. 1C can be constructed from the two parts of Fig. 3 according to the following equation
The process by which we synthesize a complex movement by the superposition of the kinematic trajectories of two simpler movements that are similar to each other cannot be extended to the EMG patterns. The bottom panel of Fig. 3 shows the results of subtracting the PM EMGs from the RM EMGs. It is quite clear that, although the kinematic features of the sPM are similar to those of a real PM, the EMG features are very different. In fact, both synthetic EMGs in Fig. 3 are mostly negative.
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FIG. 3.
A synthetic PM (sPM, solid line) is computed by subtracting the 2 movements of Fig. 1C. When inverted, the angle velocity and acceleration records of this figure are similar to the 40° PM of Fig. 1 (dashed line). When the sPM is delayed by 135 ms and subtracted from the PM, the resulting wave from reproduces the kinematics of the 40° RM of Fig. 1. However, the EMG patterns produced by this manipulation (bottom panel) are unlike those of the Fig. 1 PM EMGs.
). The general validity of this contention cannot be argued on the basis of these data, but the data do show that the earliest differences between the EMG patterns of PMs and RMs precede differences in kinematics, as of course they logically must. This EMG divergence requires different central commands for PMs and RMs that cannot be created by sequential superposition of two similar PM commands. Furthermore, whatever may be the reflex contribution to the EMG patterns, it is quite difficult to explain the difference between PM and RM EMG patterns as consequences of kinematically driven reflexes.
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ACKNOWLEDGEMENTS |
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We thank Dr. D. M. Corcos for suggestions on this manuscript.
This work was supported in part by National Institute of Arthritis and Muscoloskeletal and Skin Diseases Grants RO1-AR-33189 and RO1-AR-44388.
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FOOTNOTES |
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1 The range of our angle transducer is ±50°. As a result, in some movements there was distortion (clipping) of the angle record if the limb position exceeded these limits which distorted the velocity near zero when computed by differentiation. None of our quantitative analyses were affected by these errors. Velocity in Figs. 1 and 3 was computed by integrating the measured acceleration and do not have this distortion.
2 It is necessary to delay the antagonist burst if it is increased. If this is not done, the resulting stronger extension-directed torque will produce zero velocity and then start the limb's return before it reaches the target.
3
Although our review of the literature shows that most single joint EMG studies recorded from only a single agonist and antagonist pair, those that recorded more than that (e.g., Corcos et al. 1989; Gottlieb et al. 1989a
; Wadman et al. 1980
) found only subtle differences among synergists. It is of course possible that the anticipated EMG increase might have been found in other extensor muscles had we had the foresight to record from them. Although the available data do not suggest dramatic differences among synergists for the two movements we studied, we cannot exclude this possibility and would not be able to do so with only surface recording.
Address for reprint requests: Boston University, Neuromuscular Research Center, 44 Cummington St., Boston, MA 02215.
Received 12 March 1998; accepted in final form 15 June 1998.
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REFERENCES |
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