Exp Brain Res (1992) 91:509-519

Experimental BrainResearch 9 Springer-Verlag1992

Effects of weak antagonist on fast elbow flexion movements in man M. Margaret Wierzbicka and Allen W. Wiegner Spinal Cord Injury Service, Brockton/WestRoxburyVA Medical Center, i400 VFW Parkway, Boston, MA 02132, USA and Department of Neurology, Harvard Medical School, Boston, MA 02132, USA Received October 4, 1991 / Accepted May 12, 1992

Summary. By using a mathematical model and experiments involving electrical simulation of antagonistic muscles, we have formed the hypothesis (Wierzbicka et al. 1986) that in one-joint movements the antagonist muscle not only provides braking torque but also controis movement time. To get additional experimental support for this hypothesis, we studied elbow flexion movements performed by patients with spinal cord injury at the C 5 6 level who had relatively normal strength in their biceps muscle and little or no voluntary control of the triceps. Seven quadriplegic patients and six control subjects performed elbow flexion movements of 10~, 20~, and 30~ "as fast and accurately as possible". Despite the lack of antagonist, patients used the same "pulse height" strategy as control subjects to scale their responses with movement amplitude. However, patients' movement time was on average twice that of control subjects, and durations of both accelerative and decelerative phases of movement were increased. Movement speed and acceleration were reduced to 20-50% of the corresponding values of control subjects. Patients tended to overshoot the target to a larger extent than control subjects, particularly 10~ targets, with nearly twice the error. We performed the same experiments using an external torque motor to assist the weak triceps. When a constant extensor torque of 2.5 or 5 Nm was provided by the motor, patients were able to move faster, and movement accuracy improved to within the normal range. These results provide direct evidence that the lack of an antagonist has an important effect on completion time and accuracy of fast goal-directed movements. Key words: Voluntary movements - Antagonist muscle - Quadriplegia - Human

Correspondence to:

M. Margaret Wierzbicka

Introduction It is obvious why we need our triceps muscle, the primary elbow extensor, to extend our arm and reach overhead, but it is more difficult to ascertain the full role of the extensor muscle in controlling fast flexion movements. This problem has been widely investigated by examining relatively simple goal-directed movements or isometric contractions at one joint. Studies of movements under different load conditions have supported the hypothesis that the antagonist muscle provides the torque necessary to brake a rapid movement on reaching a target (Lestienne 1979; Flament et al. 1984; Meinck et al. 1984; Stein et al. 1988). However, it has also been shown that antagonist torque often exceeds the level needed for braking (Karst and Hasan 1987). A number of quantitative studies have been performed to relate parameters of the antagonist electromyogram (EMG) burst, such as size and timing, to parameters of movement trajectories (displacement, velocity, acceleration) under varied task conditions. Attempts to correlate the antagonist EMG burst size to single kinematic parameters have shown inconsistent results, indicating that the underlying relationship is not simple (Hallett and Marsden 1979; Brown and Cooke 1981; Hoffman and Strick 1990). Marsden et al. (1983) showed that the antagonist EMG burst is a function of two kinematic parameters, the amplitude and the speed of movement, and varies in a nonlinear fashion with joint rotation angle. The direct effect of the antagonist on a movement is difficult to assess because the recorded motion of the arm is a complex integrated function of the activation of both agonist and antagonist muscles. Furthermore, the antagonist is usually activated when the limb is already moving, invoking the different muscle mechanics involved in "lengthening'' or eccentric contractions. In view of the above limitations on assessing the role of the antagonist in voluntary movements, exploratory studies of antagonist function have been undertaken using mathematical models (Hannaford and

510 S t a r k 1985) a n d also electrical s t i m u l a t i o n ( W i e r z b i c k a et al. 1986). The present study of elbow flexions in quadriplegics p r o v i d e s a u n i q u e o p p o r t u n i t y to assess flexor f u n c t i o n separately, an assessment that could not be made on t h e basis o f v o l u n t a r y e f f o r t i n n o r m a l subjects. P a t i e n t s w i t h a cervical s p i n a l c o r d i n j u r y a t the C 5 - 6 m o t o r level t y p i c a l l y h a v e m i n i m a l loss o f s t r e n g t h i n t h e b i c e p s muscle, may have some wrist extensor strength, and have little o r n o v o l u n t a r y c o n t r o l o f their triceps m u s c l e . Q u a n t i t a t i v e e v a l u a t i o n o f m o t o r deficits i n these p a t i e n t s c a n h e l p to c l a r i f y s o m e f u n d a m e n t a l issues reg a r d i n g a n t a g o n i s t f u n c t i o n . I n p a r t i c u l a r , will a l a c k o f a n t a g o n i s t : (1) i n c r e a s e m o v e m e n t t i m e i n q u a d r i p l e g ic p a t i e n t s in c o m p a r i s o n w i t h c o n t r o l s u b j e c t s w h e n m o v e m e n t s o f d i f f e r e n t a m p l i t u d e s are p e r f o r m e d " a s fast a n d a c c u r a t e l y as p o s s i b l e " ; (2) affect the a c c u r a c y o f m o v e m e n t s to a t a r g e t , after a n e q u i v a l e n t a m o u n t o f p r a c t i c e i n p a t i e n t s a n d c o n t r o l s u b j e c t s ; (3) r e s u l t in a different pattern of agonist muscle activation from t h a t u s e d b y c o n t r o l s u b j e c t s to p r o d u c e fast m o v e m e n t s o f d i f f e r e n t a m p l i t u d e ? I n a d d i t i o n , we e x a m i n e d t h e effect o f a n " a r t i f i c i a l t r i c e p s " (a c o n s t a n t e x t e n s o r t o r q u e p r o v i d e d at t h e e l b o w j o i n t b y a n e x t e r n a l t o r q u e m o t o r ) o n the t i m i n g a n d a c c u r a c y o f m o v e m e n t s p r o duced by patients.

Materials

and methods

We studied elbow flexion movements in six quadriplegic patients (average age 40) and six control subjects (average age 34). For the purposes of this study we selected quadriplegics with injuries at the C 5-6 level with relatively normal biceps function and little or no voluntary control of triceps (Table 1). One additional subject (number 7) was studied twice: 9 months after the injury, when the triceps strength had recovered from 1/51 to 4/5 (measured as 10 Nm); and 21 months after the injury, when the triceps strength was 5/5 (36 Nm). Because a somewhat different protocol was used the first time subject 7 was studied, the movement-time data have been included in Fig. 5, but the other data from this patient have not been averaged with those of other subjects. During the experiment, subjects were seated in a chair (or their personal wheelchair) with their right arm supported on a table at shoulder height, the forearm, wrist, and hand strapped to the lever arm of a torque motor mounted below the table, its vertical motor shaft coaxial with the elbow. Subjects viewed an oscilloscope which displayed two horizontal lines, one with initial and then final target levels and the other showing the subject's measured elbow angle. The subjects were instructed to align their position with the initial target line at the beginning for each trial and then move "as fast and accurately as possible" to the final target position when the target line shifted. The starting and final target position were controlled by the experimenter at the computer console. Subjects were also asked to refrain from correcting their movements once initiated. Flexion movements of 10~ 20~ and 30~ were performed in blocks of ten trials at each distance in semirandomized order. Final target position was maintained at an angle of 60~ at the elbow joint for all movements; starting position ranged from 70 to 90~ to obtain the desired distance of each movement. More extended (beyond 90~) starting positions were unreachable by patients with no triceps function. All subjects were allowed a period of practice x Clinical motor grading scale: 0/5 = n o n e ; 1/5 =trace; 2/5 = p o o r ; 3/5 = fair; 4/5 = good; 5/5 = normal.

TaMe 1. Patient data Patient

Age (years)

1 2

3 4 5 6 7 7

Time since injury (years)

45

1

64 35 21 38 38 31 32

36 13 0.3 20 16 0.8 1.8

Biceps strength

Triceps strength

(Nm)

(Nm)

33

4/5* 51 37 27 61 59 56

Triceps tendon reflex

0

-

0 1.5 0.2 7 4 10 36

+ + + +

* Not measured; clinical assessment

at the start of each experimental condition (0-, 2.5-, and 5-Nm extensor torque), with frequent coaching from the investigators to increase their speed and accuracy, until improvement in their movement times was no longer seen. Five additional practice trials were given each time the distance was changed. Patients performed the first block of trials at each distance without the external torque motor. During the second and third sets of 30 trials, 2.5 and 5 Nm, respectively, of constant extensor torque was provided by the motor, and patients flexed against this torque. The motor was left on continuously throughout each block of 10 trials (unless the subject requested an extra period of rest). Control subjects also performed a block of 30 ~ trials with a "slower, still accurate" instruction. The torque motor was not energized in experiments with control subjects after preliminary measurements in two subjects indicated that it had little effect on their movement parameters (e.g., movement time 186_+ 10 ms with torque, 179__ 9 ms without torque). The angular position of the arm was recorded with a potentiometer attached to the motor shaft. EMG activity of biceps and triceps muscles was recorded with surface electrodes (Liberty Mutual MYO-111 with a --3-dB bandwidth of 120~500 Hz), which were relatively immune to motion artifacts. Data acquisition began when the target shifted to its final position; position and two channels of EMG were sampled for 2 s at a rate of 1 kHz and were stored on a Compaq Deskpro 386/20 computer equipped with a Metrabyte DAS-20 data acquisition board. One second of position and EMG data, starting 100 ms prior to movement onset, was stored in a computer file for further off-line processing. Maximum voluntary contractile strength was measured by having subjects pull (biceps) or push (triceps) against a fixed load cell while in a posture similar to that used for the movement studies. Strength was averaged over a 2-s period. Key kinematic parameters such as peak displacement, velocity, and acceleration; movement time; and duration of accelerative and decelerative phases were evaluated automatically according to predefined criteria. The onset of the movement was defined as when acceleration reached 5% of its maximum. Movement time was defined as the time from movement onset to peak displacement (the point at which velocity returned to 1% of its maximum). Velocity and acceleration trajectories were calculated by numerical differentiation of the position data. Gaussian smoothing (standard deviation, SD = 9; Abeles 1982) was applied after each subsequent differentiation. Errors in subjects' performance were measured as the difference between actual peak displacement and position of the intended target, and were expressed as a percentage of the target amplitude. Constant errors (mean percentage overshoot) and variable errors (SD of within-subject constant errors) were evaluated for each subject. EMG signals were rectified and smoothed (Gaussian filter, SD = 2) before manual evaluation of the burst duration and area.

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Fig. 1. Fast movements of 10% 20~ and 30~ produced by a C5-6 quadriplegic without physiological triceps (patient 1). Averaged displacement, velocity, and acceleration at each target distance

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Fig. 2. Fast movements of 10~ 20~ and 30~ produced by a control subject showing averaged displacement (top) and acceleration (middle) at each target distance. Superimposed averaged, rectified biceps and triceps EMG at each distance (bottom). In this example, biceps burst area increases with distance and triceps burst area decreases with distance

Comparison of patients" movement with those of control subjects

Muscle strength Maximum biceps strength in control subjects ranged from 66 to 91 N m with a mean of 78 N m ; triceps strength ranged from 26 to 66 N m with a mean of 39 Nm. Table 1 shows that patients' biceps strength was about half that of the control group, which may reflect the patients' injury, difficulty in transferring their maximal biceps effort to the apparatus because of their lack of trunk stability, or weakness secondary to lack of exercise against the triceps. Three patients had essentially no triceps strength, three had a small fraction of normal strength, and patient 7 returned to normal strength between the first and second test sessions. The last column of Table 1 indicates whether a palpable triceps tendon jerk could be elicited during examination by a neurologist.

Kinematics. Figure I shows averaged (n = 10) trajectories of fast elbow flexion movements to the three targets produced by a quadriplegic patient with no physiological triceps (patient I in Table 1). A consistent feature of each patient's movements to different targets was that the overall shape of the trajectories was similar, with a small increase in movement time in larger movements. Similar scaling of movement profiles to the different targets was observed in control subjects (Fig. 2), although movement times varied less with target distance. Movement-time parameters for control subjects and patients are compared in Fig. 3 and kinematic parameters in Fig. 4. Patients' movement time, on average (all subjects and distances), was twice that of control subjects and roughly inversely related to the preserved voluntary strength of the triceps muscle (compare Table 1 and Fig. 5). Interestingly, not only was the decelerative phase of the movements extended (on average, by a fac-

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Fig. 3. Movement time parameters of patients and control subjects plotted versus target distance. Different open symbols are used for each patient. Dashed lines indicate mean values for the patient group, solM lines with filled circles show means -t-SD of control subjects

Fig. 4. Kinematic parameters of movements plotted versus target distance. Different open symbols are used for each patient. Dashed lines indicate mean values for the patient group, solid lines with filled circles show means _+SD of control subjects

tor o f 2.8), as could be expected from the weaker braking torque involved, but also the duration of the accelerative phase was increased (on average, 1.6 times) in comparison with control subjects (Fig. 3). Peak velocity of patients' movements was reduced on average (all distances) by a factor of 2; patients were apparently forced to modulate the velocity of their movements according to their ability to recruit braking torque to halt the movement. Peak acceleration was reduced by a factor of 3 and peak deceleration by a factor of 5 (Fig. 4), with the result that the acceleration profiles of patients' movements did not attain the symmetry characteristic of controls' fast movements (Fig. 2). Even those patients with no active antagonist were able to plan movements which stopped near the desired target by relying on the passive viscoelastic torque acting at the elbow joint, but movement speed was greatly reduced.

Errors. Constant errors (mean percentage overshoot)

and variable errors (SD of within-subject constant errors) of patients and control subjects, expressed as a percentage of target amplitude, are shown in Table 2. Positive constant errors indicate that control subjects overshot the target, on average, at all movement distances. Patients had the most difficulty in controlling the amplitude of smaller movements (10~ as both their constant and variable errors were nearly twice those of control subjects; these differences were statistically significant (Table 2). At 20 ~ the constant error of patients was comparable with that of controls, but the variable error o f their efforts, reflected in the SD, remained statistically greater (P < 0.01). At 30 ~ the differences between controls and patients did not reach statistical significance at the 0.05 level. However, when control subjects performed 30 ~ movements at a speed comparable with that of the patient group (movement time 361 +_86 ms),

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Fig. 5. Patients' average movement time (all trials) for movements without torque (filled circle) and with 2.5-Nm (open triangle) or 5-Nm (plus) external torque. Patient numbering as in Table 1. Solid and dashed lines are mean and mean +2 SD, respectively, of control subjects

their constant error decreased and was significantly less than that of the patient group at the same distance (P < 0.01).

Electromyogram. Averaged surface E M G recorded from flexor and extensor muscles is shown in Fig. 6 for movements made by patient 1, as shown in Fig. 1. The agonist muscle was activated in a clearly defined burst of approximately 100 ms duration, with burst area proportionally adjusted to the distance (Fig. 7). An antagonist burst was not seen, since this patient could not voluntarily activate his triceps, nor was an extensor stretch reflex present during clinical examination. A low level of E M G activity recorded by the triceps electrode paralleled biceps activity and was most likely volume-conducted biceps E M G (cross talk). A second agonist burst in patient 1 (Fig. 8) was seen in 21 of 30 trials and occurred 454_+ 41 ms after movement onset, near the time of peak displacement (443+37 ms). Similar E M G patterns were seen in the other two patients with functionally absent triceps. In patients with some triceps strength, one produced a triphasic E M G pattern (consisting of two agonist bursts separated by a relative silent period in the agonist, Table 2. Movement errors

Percentage error

during which the antagonist burst occurs), one a biphasic pattern (no second agonist burst), and the third a biphasic pattern followed by cocontraction of agonist and antagonist. A m o n g control subjects, E M G patterns ranged from triphasic (Fig. 2) to biphasic with substantial cocontraction. A summary of selected E M G parameters from l0 ~ and 30 ~ movements is given in Table 3 (data from 20 ~ movements are not included since one patient failed to complete these trials). First agonist burst duration in all patients was like that of control subjects making fast movements, and did not show the increased duration characteristic of controls' slower movements. First agonist burst area showed comparable scaling in controls and patients. In patients with a functional but weak triceps, the width of the antagonist burst was increased in a manner similar to that o f control subjects making slower movements, perhaps as an accommodation to the weakness of the muscle. Antagonist burst area appeared to change little with movement distance in both patients and controls. However, because of the unknown spatial distribution of the remaining active fibers within each paretic triceps muscle, and the corresponding unknown impact on the shape of the E M G - force relation, quantitative measures of triceps E M G magnitude in patients are approximate. Thus, both patients and control subjects scaled the amplitude of the first agonist E M G burst, which had relatively constant duration, with distance to produce fast m o t o r responses. However, there were substantial qualitative and quantitative differences in the kinematics of the responses o f patients and control subjects. The lack of a strong antagonist resulted in asymmetry of the accelerative and decelerative phases of patients' movements, with a substantially prolonged decelerative phase (Fig. 1), in contrast to the approximately symmetric acceleration profiles of the fast m o t o r responses of control subjects (Fig. 2).

Comparison of patients' movements with and without triceps support Kinematics. Figure 9 shows the effect of the amplitude of artificial extensor torque on movement time, acceleration time, and deceleration time in patient 1. In this

10~ movements Constant

Patients, 0 Nm Patients, 2.5Nm Patients, 5.0Nm Controls, fast Controls, slower

20~ movements

Variable Constant

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Variable Constant

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All errors expressed as mean 4-SD. Constant error is percentage overshoot; variable error is within-subject variability of measured constant error; SD indicates across-subjects variability of both evaluated errors * Differs from fast movements of controls (P < 0.05, Newman-Keuls test) ** Differs from slower movements of controls (P < 0.05, Newman-Keuls test)

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