Parkinsonian arm movements as altered by task difficulty

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Parkinmnism 6 Related Disorders Vol. 2, No. 4, pp. 215-223, 19% Copyright 6 19% Published by Ekvier Science Ltd. AB rights reserved Printed in Great Britain S1353-8020(96)00026-O 135~Lwo/% $15.00 + o.ccl

Parkinsonian Arm Movements as Altered by Task Difficulty I’WEISSt, . G.E. STELMACHt, C.H. ADLERj AND C. WATERMANt Accepted 25 March 1996

A discrete elbow movement to targets with different indexes of difficulty (ID) was used to determine the kinematic organization of arm movements in a young, an elderly and a Parkinson’s disease (PD) group (n = 14). Target size and movement amplitude changes led to expected modifications of the kinematics in all three groups according to Fitts’ law. Increased task demands by changing target size produced not only differences between the age-groups, but affected the modulation of velocity and acceleration in the parkinsonian patients differentially. For large amplitude movements, the PD patients were less able to increase velocity and acceleration magnitudes when target accuracy constraints were reduced. These findings, when taken together with the observation that speed scaling was preserved for small movement amplitudes, suggest that a reduced capability to initiate and regulate force is the cause for the observed slowness in PD. Copyright 0 1996 Published by Elsevier Science Ltd. Parkinson’s disease

Fitts’ law

Motor programming

Speed scaling

Force control

greater the slowing. His results suggest that the transformation process of task requirements into a motor program is qualitatively preserved in PD patients, but the movement parameterization is slowed. Other investigators have approached the problem of bradykinesia from a more physiological perspective. Hallett and Khoshbin [3] found impaired muscle activation patterns in PD patients for simple elbow flexion movements that had precise target constraints. While normals exhibited a three-phasic agonistantagonist-agonist-pattern, the PD patients did not fully saturate their initial EMG burst, resulting in additional muscle activation cycles to achieve the target position. Using similar movements, abnormal saturation was not observed by Teasdale et al. [4], when accuracy constraints were removed. Nevertheless, their PD patients still needed multiple muscle activation bursts to achieve a target position. The time necessary for these additional activation cycles may be responsible for the prolonged movement durations observed in PD. Berardelli et al. [5] found in rapid wrist flexion movements that PD patients were generally able to modify the size and the duration of the first agonist burst with changes in movement distance, but the patients’ overall slowness revealed that they seem to be unable to scale such parameters adequately for specific types of movements. Berardelli et al. [6], therefore, did not consider inadequate muscle activation as the underlying cause

INTRODUCTION A common clinical observation in Parkinson’s disease (PD) is that patients are able to execute both simple movements quickly and complex movements with reasonable accuracy, but show marked movement slowness (bradykinesia) in tasks where both accuracy and speed requirements are combined. To determine the underlying cause of such slowness, Sanest11 examined alternating arm movements to targets with different accuracy constraints in PD and control subjects. By analyzing information processing capacity based on Fitts’law [2], he stressed the importance of deficits in the central mechanisms. Sanes found that the performance of PD patients was generally sensitive to task difficulty. In addition, he showed that the deficits in the parkinsonians were not constant, but increased with accuracy constraints (index of difficulty, ID). Since the PD patients performed as well as controls under conditions with low difficulty level, he assumed the observed deficit was caused by a reduced capability to rapidly process movement related information. The more demanding a movement was the tMotor Control Laboratory, Arizona State University, Tempe, AZ 852874404, U.S.A. $Department of Neurology, Mayo Clinic, Scottsdale, AZ 85259, U.S.A. Address correspondence to: G. E. Stelmach, Motor Control Laboratory, Arizona State University, Box 870404, Tempe, AZ 852870404, U.S.A. Tel.: (602) 965-9847, Fax: (602) 9658108 *Current address: Department of Neurology, Heinrich-Heine-University, Moorenstr. 5, D-40225 Diisseldorf, Germany. 215

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for the bradykinesia in PD. Instead they preferred the hypothesis that a dissociation between perception and action caused incorrect motor program specifications. Utilizing similar simple movements, Montgomery and Nuessen [7] also found impaired target acquisition in PD, which was characterized by a reduced ability of unmedicated PD patients to maximize speed, when moving to targets with minimal accuracy constraints. Proper timing of perturbed movements suggests a target acquisition problem in PD rather than a movement initiation deficit. They viewed target acquisition and movement initiation as parallel processes localized in the putamen and the caudate nucleus, respectively [8,9]. During the course of I’D, the more severe the dopamine loss in the putamen, the more it influences the interaction of the basal ganglia with the somatosensory cortex and leads to an impaired movement parameterization, i.e. force specification. In monkeys, the reversible blockade of the putamen [lo] led to dysmetria and abnormal braking in arm movements, while reaction times remained unaffected. Movement initiation and execution may not be completely separate processes, however, because as Stelmach et al.[ll] have shown the reduced rate of force development in PD can influence reaction time. In normal subjects, reaction time decreases with higher force levels. The long reaction times in the I’D patients could, therefore, be a consequence of their lower rate of force development. This study continues the exploration of PD motor performance by examining the differential deficits of PD patients in a discrete elbow movement task that had different levels of difficulty. While Sanes [l] based his interpretation only on movement time and accuracy error, the present experiment analyses the whole kinematic characteristics of the movement, which can provide information on motor programming processes and how such programming is implemented. Motor programming processes have been conceptualized and described by many [12-151. According to Jeannerod’s stage model for the generation of action, the encoding of external task constraints (e.g. accuracy requirements) takes place at the level of programming and the execution process orchestrates the realisation of the motor program (e.g. force parameterization). The integrity of motor programming processes is revealed by the preserved relative timing of the movement: e.g. the symmetry ratio of the velocity curve (ratio of deceleration by acceleration time). According to Fitts’ law, movements with higher accuracy demands should show reduced peak velocity magnitudes and prolonged movement times. Because of the restricted movement direction as well as the very low friction of the elbow movements in this study, the acceleration values provide a good approximation of the net forces moving the arm. Under the foregoing assumptions, the proper scaling of the velocity and acceleration amplitudes may be considered an index of

force scaling. In particular, the increase of movement amplitude requires a greater generation of force, while the decrease of target size requires a more precise control of the forces generated. A detailed examination of the movement kinematics was undertaken to answer two questions: Do PD patients execute their movements according to the accuracy requirements of the task, which would indicate preserved motor programming? Do PD patients scale the velocity and acceleration features of their movements appropriately indicating efficient force parameterization? By examining the differential influences of target size and movement amplitude changes on movement kinematics, this study also examines whether PD patients demonstrate pronounced slowing with increased task difficulty as predicted by Sanes[l].

METHODS

Subjects The results are based on the examination of 42 righthanded subjects. Fourteen students (7 females, 7 males) from the Arizona State University participated as the young control group (mean age 23.5 +- 3.4 years). Fourteen (7 females, 7 males) spouses of the patients and volunteers served as the elderly control group (mean age 70.3 ? 4.9 years). The PD group (mean age 69.4 + 6.5 years) consisted of 14 subjects (4 females, 10 males), referred by their neurologists or support groups. The disease duration was 1.82 + 1.46years and severity ranged from stage I to III [16]. The patients remained on their regular medication scheme, but were scheduled for the test at the end of their dose-cycle. Additional data about the patient group (stage, medication, symptoms and duration of disease) are listed in Table 1. The comparison between young and elderly subjects examined the effects of aging [17,18], while the comparison between elderly subjects and PD patients revealed the effects of I’D on motor performance. All subjects provided signed informed consent, and the PD and elderly subjects were paid for their participation. Apparatus The experimental set-up consisted of a lever-arm and a personal computer with a monitor mounted on a table. Data was stored on hard disk for subsequent offline analysis. The position data of the lever (i.e. the subject’s arm movements) were recorded with the help of a rotary variable differential transformer (RVDT), while displayed simultaneously in the form of a 2 cm-high cursor line on the screen. The sampling frequency was 100 Hz. In addition, the software automatically registered the time, when the cursor left the home position or entered the target position for each trial. For all subjects the same trial

PARKINSONIAN

ARM MOVEMENTS AS ALTERED BY TASK DIFFICULTY

217

TABLE 1. Clinical data of the 14 Parkinson’s disease patients

Sex

Disease duration

60

m

73 63 79 62

m m m f

6 7 8 9 10

74 71 81 69 60

m m f

11

72

12

69

13 14

68 70

No.

Aae

Stage of disease

Additional symptoms

Medication

1.5

II

bilateral tremor, micrographia

1.5 1.5

I II II

slight right hand and arm tremor right hand tremor, micrographia right hand tremor, micrographia left hand tremor

1 0.5 5 0.5

II III II

right sided tremor, micrographia right hand tremor tremor, bradykinesia bilateral hand tremor right hand tremor, micrographia

1.5

II

micrographia, bilateral leg tremor

m

4.5

II

left sided tremor

m m

0.5 2

I

Carbidopa/ L-Dopa, Selegiline Carbidopa/ L-Dopa Carbidopa/ L-Dopa SelegiIine Carbidopa/ L-Dopa, SelegiIine Carbidopal L-Dopa none Carbidopa/ L-Dopa CR Carbidopa/ L-Dopa CR Carbidopa/ L-Dopa, Trihexyphenidyl Carbidopal L-Dopa CR, SelegiIine Carbidopa/ L-Dopa, SelegiIine Carbidopa/ L-Dopa CR Carbidopa/ L-Dopa, SelegiIine

m

3.5

definitions were used. The home position was invariant throughout the experiment: two 6 cm high lines were displayed at the outer right side of the monitor, reflecting a lever-position of 90 degrees. The home position width was 6 mm. Accordingly, the two targets were displayed as pairs of 6 cm-high lines, 70 and 140 mm away (short and long movement amplitude) from the center of the home position on the left side of the screen. These values represented 30 and 60 degrees of lever movement, respectively. The widths of the two different-sized targets were 6 and 16 mm respectively, and they were displayed in a way that their center was always at the above described position. For each movement amplitude (A)-target size (W) combination the index of difficulty was calculated after Fitts’ law [2] ID = log2 (2A/W). For the short amplitude of 70 mm, the ID was 3.13 for the large (16 mm) target and 4.54 for the small (6 mm) target. The increase of the movement amplitude to 140 mm resulted in IDS of 4.13 for the large target size and 5.54 for the small target size. Procedure The subjects sat comfortably at the table in front of the computer screen. The height of the screen and height of the chair were adjusted so that the subjects could see the complete monitor without difficulties. The subjects wore a specially prepared visor, which prevented them from seeing their moving arm during the experiment, but did not disturb the view to the screen. They rested their right arm comfortably on the lever and grasped a handle at its end. The subjects’ arm was secured to the lever with tape, so that the shoulder was half abducted and the forearm was in a 90 degree angle to the upper arm. The elbow was supported above the pivot point of the lever. The subjects kept the arm in this position throughout

right hand tremor

the experiment and the tape prevented any wrist movements. The subjects were given 40 practice trials with different amplitudes and target sizes, which were not used in the actual experiment. During the practice phase, the subjects were required to move as quickly and as accurately as possible in one step into the target. After practice, the subjects performed 120 valid trials under four conditions in a semi-randomized order. Each condition had 30 trials, where the subject moved to one of the two amplitudes in combination with one of the two target sizes, such that each amplitude and each size were repeated twice during the experiment. For each trial, after the subject moved into the home position, the target was displayed after two seconds. The subjects were advised to look at the target position as soon as it was displayed to obtain as much information as possible to prepare the upcoming movement. When the auditory, imperative signal was given, after a random delay of 1000-2500 ms in increments of 500 ms, the subjects moved the cursor (i.e. the lever-arm), as quickly and as accurately as possible in a one-step movement so that the cursor ended between the two target lines on the monitor. The motion performed was a horizontal flexion movement toward the body. After the cursor had remained in the target for 0.5 s, the screen was cleared and the time between leaving the home position and entering the target position (movement time) was displayed as feedback. The analysis software detected error trials during the experimental session on the following basis. (1) Anticipation error: when the subject moved earlier than 100 ms after the imperative stimulus. (2) Reaction error: when the time between stimulus onset and the initiation of the response exceeded 1000 ms. (3) Overshoot and undershoot error: when the subject did not

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stop inside the defined target lines. Trials with errors were disregarded during the experiment and testing of each condition continued until 30 valid trials were sampled. The duration of the experiment was approximately 1.5 h. After the second condition block, there was a break for the subjects, in which they filled out a health questionnaire. Data processing and analysis The data were processed as follows: the raw position data were filtered at 10 Hz with a dual pass, second order Butterworth filter. Then, the velocity and acceleration values as the first and second derivative of the filtered angular position data were computed (see Fig. 1 for an example trial of a young subject). The following parameters were determined by an algorithm: reaction time (RT), end of the movement as well as time and magnitude of peak velocity, peak acceleration and peak deceleration. For RT, the algorithm detected the first deviation from the initial baseline in the velocity trace of each trial that exceeded 10% of the associated peak velocity magnitude. This is a conservative criterion because it leads to adjusted estimates of movement onset times, especially for trials with low velocity as in the PD patients (complete algorithm in [19]). The end of the movement was defined as the first sign change in the velocity signal after entering the target area. Trials in which such an reversal occurred before the subject had entered the target were disregarded as undershoot-errors. The exclusion of all movements not ending in the target was necessary to fulfill the assumptions of Fitts’ law [2]. The automatically detected kinematic landmarks were double-checked by the experimenter. The obtained kinematic landmarks were used to define the following dependent variables: Movement time (MT): the time interval between movement onset and the end of the movement; time to peak velocity (TN): time after RT to reach peak velocity; deceleration time (DT): time interval between time of peak velocity and end of the movement; time to peak acceleration (TPA): time after movement onset to peak acceleration; and

time to peak deceleration (TPD): time after movement onset to peak deceleration. In addition, deceleration time was expressed as percentage of movement time. The experiment incorporated a 3x2x2 design with group as the between-subjects factor and with movement amplitude (30 and 60 degrees) and target size (6 and 16 mm) as the within-subject factors. An analysis of variance for repeated measures was calculated for the means of each variable per condition, with a priori contrasts for the four conditions and with a p < 0.05 as the probability level. RESULTS

Dfferences between the groups All group data are reported in Table 2. The RT of the young (157 ms) and the elderly (185 ms) subjects was significantly different from that of the PD subjects (204 ms). The difference of MT between the Parkinsonians (716 ms) and both normal groups, the elderly (675 ms) and the young (508 ms), also reached significance. Clear group differences emerged for the other temporal parameters of the movement: there was a progressive ordering of the group means for the parameters time to peak velocity (TN), deceleration time (DT), time to peak acceleration (TPA) and time to peak deceleration (TPD). These five parameter were significantly longer (at the p < 0.01 level) for the PD patients as compared to the elderly subjects, who in turn were slower than the young subjects. Despite the absolute lengthening of these temporal landmarks, the symmetry ratios, indicated by DT expressed as percentage of MT, were similar between all three groups. In addition, the three groups were significantly different for peak velocity, peak acceleration, and peak deceleration, with the young subjects producing the highest values followed by the elderly and then the I’D patients. Similarities between the groups According to Fitts’ law, increasing task difficulty by the lengthening of movement amplitude or a

TABLE 2. Summary of the results for the three groups collapsed over all conditions Group differences Young RT MT TPV DT DT %&IT TPA TPD Peak velocity Peak acceleration Peak deceleration

157 + 508 k 208 2 300 k 58.0 2 99 k 320 k 188 2 1369 2

13 42 14 31 1.8 9 25 19 200

1200 t 184

Elderly 185 675 270 405 59.2 124 415 133 814

k 2 + k k 2 2 2 2

19 50 20 40 2.3 14 28 12 97

810 I 110

PD patients 204 716 297 419 57.4 146 450 121 716

k + ? 2 + 2 % ? k

24 53 19 42 2.1 13 29 11 82

778 k 145

Young vs. Elderly NS F&39) = 21.85 p < F&39) = 16.42 p < F(1,39) = 16.84 p < NS F(1,39) = 9.01 p < F&39) - 18.92 p < F(1,39) = 19.73 p < F(1,39) = 15.22 p <

0.001 0.001 0.001 0.01 0.001 0.001 0.001

F(1,39) = 9.4 p < 0.01

Young vs. PD patients F(1,39) = 9.87 p < F(1,39) = 39.04 p < F(1,39) = 36.86 p < F(1,39) = 25.94 p < NS F(1,39) = 32.77 p < F(1,39) = 38.54 p < F(1,39) = 29.12 p < F(1,39) = 21.42 p < F(1,39) = 12.68

0.01 0.001 0.001 0.001 0.001 0.001 0.001 0.001

p < 0.01

Elderly vs. PD patients F&39) = 7.12 p < 0.05 F(1,39) = 20.4 p < 0.001 F(1,39) = 21.82 p < 0.001 F(1,39) = 12.33 p < 0.01 NS F(1,39) - 23.79 p < 0.001 F&39) = 21.68 p < 0.001 F(1,39) = 13.44 p < 0.01 F(1,39) = 9.56 p < 0.01 F(1,39) = 5.48

p < 0.05

PARKINSONIAN

ARM MOVEMENTS AS ALTERED BY TASK DIFFICULTY

219

TABLE 3. Effects of varying movement amplitude Young

Elderly

small

large

small

189 ? 13 442 ? 30

194 * 13

MT

581 5 4P**

TPV

190 ? 12

DT DT %MT TI’A TPD

RT

Peak velocity Peak acceleration Peak deceleration

I’D patients large

small

large

220 + 20

217 2 17

584 + 33

787 ‘- 52*”

239 + 23 635 2 40

236 + 24 829 2 53**’

228 ? 15***

246 2 17

300 rt 20***

274 2 17

328 ? 20***

253 t 21

353 5 35***

338 ? 26

487 * 44-s

360 ? 32

501 t 44***

56.5 ? 1.7 91 2 8 286 5 20 147 f 12

59.8 ? 1.8*** 108 % lo*** 357 + 26*‘”

57.6 + 2.2 116 ? 13 381 I 2

61.1 2 2.3**’ 133 2 15*** 457 + 27-*

56.0 ? 2.0 138 2 12 422 2 28

59.5 % 2.18*‘* 157 2 14** 488 lr 2T**

232 + 18*”

106 ? 7

166 + 11***

97 5 6

156 ? 9***

1416 ? 206

1896 ? 262***

808 ? 99

1092 ? 124***

681 L 72

973 + 85***

1261 2 216

1652 If: 241***

758 2 83

1156 ? 149***

689 + 83

1111 +- 178**’

reduction in target size leads to a prolongation of MT. We observed such significant increases of MT in all three groups. In addition, under increased task difficulty induced by longer movement amplitude (see Table 3 for details), time to peak velocity (TN) and deceleration time (DT) were significantly lengthened for all groups. When the movement amplitude was large, group means showed that all subjects took more time to reach peak acceleration (TPA) and peak deceleration (TPD). Besides the prolongation of the movement components, the symmetry ratio (quotient of DT/TPV) changed with increased movement amplitude similarly in all three groups. The percentage of MT spent in deceleration increased significantly in all three groups. Similar modifications in peak velocity and peak acceleration magnitude were also observed for all groups when task difficulty was increased by lengthening the movement amplitude. The performance of all three groups was also sensitive to increases in task difficulty by reducing

Interaction group by movement amplitude young vs. young vs. PD elderly patients NS F(1,39) = 5.99 p < 0.05 F(1,39) - 4.71 p < 0.05 F(1.39) = 4.63 p < 0.05

NS F(1,39) = 4.75 p < 0.05 F(1,39) = 5.28 p < 0.05 NS(p = 0.08)

NS NS NS F(1,39) = 9.12 p < 0.01 F(1,39) = 6.26 p < 0.05 NS

NS NS NS F(1,39) = 10.61 p < 0.01 F(1,39) - 4.56 p < 0.05 NS

target size (see Table 4 for details). The smaller target size led to significant changes in the acceleration phase (an increase of TPV and TPA) as well as in the deceleration phase (increase of DT and TPD) in all groups. These changes resulted again in a modified symmetry ratio. Finally, all three groups showed similarly reduced peak velocity and peak acceleration magnitudes under increased accuracy requirements caused by decreased target size. interactions between the groups With increasing task difficulty induced by larger movement amplitudes, the differences between the two age groups were more pronounced than those between elderly and I’D subjects (see Table 3 for details). The elderly as well as the PD subjects showed a substantial lengthening of TPV and DT as compared to the young subjects, as indicated by the significant group by movement amplitude interactions. Moreover, peak velocity and peak acceleration magnitudes

TABLE 4. Effects of varying target size Young

Elderly large

‘t * r ?

13 44 14 34 1.8

155 2 12 457 5 33”’ 195 -c 13*** 261 + 24*** 56.5 + l.T**

186 736 283 453 60.7

21 53 20 44 2.2

184 ? 17 623 -+ 43*** 259 2 20** 364 * 33*** 57.8 % 2.3***

Tl’A Tl’D Peak velocity

106 2 10 347 % 27 167 -c 17

93 lr 8,” 297 ? 22”* 205 + 20***

130 + 14 436 2 27 121 2 10

119 * 14** 398 ? 29” 143 + 12***

152 ? 14 473 2 31 112 + 10

Peak acceleration Peak deceleration

1369 2 200

1875 ? 259’**

814 2 97

1038 ? 125**’

716 ? 82

1200 2 184

1655 + 256’*’

810 2 110

1043 + 136*’

778 % 145

RT MT TPV DT DT %MT

161 569 223 346 59.9

small

? 2 2 + t

large

PD patients small large

small

208 770 313 458 58.4

? * 2 ? ?

23 55 21 45 2.2

201 * 24 672 2 47”** 284 2 17** 388 38** 56.7 ? 2.1’

Interaction group by target size young vs. elderly vs. PD elderly patients NS NS NS NS NS

NS NS NS NS F(1,39) = 10.67 p < 0.01 NS 141 2 12** NS NS NS 430 t 26”“” F(1,39) = 9.2 129 -c lo** F(1,39) = 8.16 p < 0.01 p < 0.01 875 ? 86’* F(1,39) = 14.52 F(1,39) = 9.35 p < 0.01 p < 0.001 NS F(1,39) = 5.29 938 2 138 p < 0.05

P. WEISS

-loo ’

pi

’ ’

’

MovementTime

I.

(MT)

I r 200

FIGURE 1. The position, velocity and acceleration traces of a young subject when moving over the large amplitude to the large target are shown. The following kinematic landmarks and times are displayed: reaction time (RT), movement time (MT), peak velocity (PV), time to peak velocity (TPV), deceleration time (DT), peak acceleration amplitude (PA A), time to peak acceleration (TPA), peak deceleration amplitude (PDA) and time to peak deceleration (TPD).

changed differentially in the young group in comparison to the elderly and the I’D group. In contrast, changes in peak velocity [F(1,39) = 4.07, p = 0.51 and peak acceleration [F(1,39) = 1.05, p = 0.311 did not differ between the elderly and PD subjects (Fig. 2). Therefore, I’D led to a similar slowing as observed with age. An increase of task difficulty by reducing target size also influenced the temporal characteristics of the movement differentially (see Table 4 for details). When target size decreased, the I’D patients spent more time decelerating the movement (DT%MT) as

etal. compared to both control groups. Furthermore, in the I’D patients the change of the peak deceleration magnitude failed significance [F(1,13) = 3.73, p = 0.751. When accuracy constraints were increased by decreasing target size, there were greater differences between the velocity and acceleration magnitudes of the three groups compared to a lengthening in movement amplitude. All group by target size interactions were significant (see Table 4 for the statistical values), with the exception of the peak deceleration, for which the young versus elderly interaction just failed to reach significance [F(1,39) = 3.99, p - 0.0531. However, the peak deceleration reduction in the elderly subjects was more pronounced as compared to the I’D patients [F(1,39) = 5.29, p < 0.051. Therefore, alterations in task difficulty by changing target size did not only show differences due to aging, but decreases in peak velocity, peak acceleration and peak deceleration in the PD patients. To illustrate the magnitude differences between the elderly and patient group, the three-way interaction of group, target size and movement amplitude for peak acceleration is shown in Fig. 3. For the short movement amplitude movement, the graph shows that the patients modify their reduced peak acceleration according to changes in target size in a similar manner as the elderly controls. However, their peak acceleration adjustments are minimal in comparison to the elderly subjects for the long movement amplitude condition. The reduced peak acceleration adjustment led to a

2 ,,,’ Young I

Y

8 P

800 600 I

I

small

large Target size

k..’ J

1

small

large

Movement amplitude FIGURE 2. Interaction of peak velocity amplitude (in degree/s) for the two movement amplitudes (small and large) with the three groups. While the change in peak velocity amplitude is similar in the elderly subjects (circles) and the PD group (triangles), the young subjects (squares) modulate the peak velocity amplitude more strongly with changing movement amplitude (p < 0.01). Given are means and SEM.

FIGURE 3. Interaction of peak acceleration amplitude (in degree/ s2) for the two target sizes (small and large) with the three groups: young subjects (squares), elderly subjects (circles) and PD patients (triangles). Depicted are the mean values and SEM for movements to different sized targets with long (open symbols) and short (filled symbols) movement amplitudes. Note that the significant interaction (p < 0.01, indicated by the arrow) between elderly subjects and PD patients is mainly caused by the reduced amplitude modulation of the patients, when covering the long amplitude (open circles and triangles). In addition, the more pronounced amplitude modiflcations in the young group (squares) interacted significantly (p < 0.01) with both the elderly and the PD group.

PARKLNSONIAN ARM MOVEMENTS AS ALTERED BY TASK DIFFICULTY

significant difference between the elderly and I’D subjects for the large targets, while both groups show similar values for the small targets. A similar pattern of modulation was obtained for peak velocity and peak deceleration. DISCUSSION

Using different movement amplitude and accuracy constraints, the purpose of our study was to investigate the capability of adjusting discrete arm movements in young, elderly and PD subjects. In comparison to the young group, reaction time and movement time revealed a slowness of movement initiation and execution in the elderly subjects and a more pronounced slowness in the I’D patients. In comparison with both control groups, the PD patients showed a prolonged reaction time [20]. Moreover, the movement duration was influenced by age and PD, such that the young control had the shortest MTs followed by the elderly and, finally, the patients. These findings support the postulate that PD patients need more time to either prepare their arm movements or to implement the motor program [12,21]. As mentioned in the introduction, the analysis was directed at two primary questions: Do I’D patients alter the temporal characteristics of their movements similarly as do controls according to the accuracy requirements of the task indicating preserved motor programming? Do PD patients scale velocity and acceleration of their movements appropriately indicating efficient force control? Our data showed that PD patients did execute their movements according to the task demands, since the temporal parameters as well as velocity and acceleration features changed according to Fitts’ law. Increased accuracy requirements caused by the reduction of the target size led to lengthening of the movement components and reduction of the peak velocity and acceleration magnitudes in all subjects. Increasing the index of difficulty (ID) by lengthening the movement amplitude also resulted in systematic increase in time parameters. These effects were similar in both PD patients and control subjects. PD, therefore, does not affect the patients’ ability to alter movement time and speed according to task difficulty. These findings support the notion that motor programming is preserved in I’D [l]. In addition, the similar symmetry ratios (ratio of DT over TPV) across the three groups support the interpretation that for I’D patients the absolute lengthening of the movement time does not affect the overall temporal organization of the movement. For our PD patients, motor programming does not appear to be the primary locus of their motor deficit. The pronounced slowing in the kinematics of the I’D patients was not solely related to the index of difficulty, but is instead dependent on specific move-

221

ment amplitude and target size configurations. For changes in movement amplitude, the influence of aging on the movement parameters was prominent, while for changes in target size, the velocity and the acceleration of the PD patients were differentially affected. These differential effects are not in accordance with Sanes’ postulation [l], because they did depend on specific movement amplitudes and target sizes combinations rather than the index of difficulty per se. Indeed, Sanes predicted a direct relationship between I’D impairment and movement difficulty irrespective of whether an increased movement amplitude or a reduced target size contributed to the increased movement difficulty. On the surface, the strong influence of target size on the peak velocity and acceleration magnitudes in I’D patients compared with elderly subjects seems to support Sanes’ hypothesis. However, further inspection reveals that the patients are able to increase the velocity and acceleration properties of their movements as target size increases, when moving over a the short amplitude (see Fig. 3 for peak acceleration). In contrast, for the long movement amplitude I’D patients do not increase their peak acceleration magnitudes as much, when the target size constraints were reduced. Previous studies from our laboratory have also shown that I’D subjects are able to modulate speed, but only to a limited extent [11,22]). One possible interpretation for these findings is that the PD patients are performing at their speed limits in the long amplitude condition, independent of target size. This interpretation parallels the finding that PD subjects had only one slow speed strategy available to achieve different complex arm movements [23]. As a consequence, movement amplitude appears to be a more crucial variable than target size in PD. This is supported by Stelmach and Worringham’s findings [24] for an isometric force task, in which I’D affected the force magnitude, but not force accuracy of the patients. Reduced speed scaling in the I’D patients with large amplitude movements suggests that they have a reduced capability to increase their rate of force production when accuracy constraints are minimized. As reported in the literature, force initiation and regulation deficits are prominent in I’D [23-251 and may account for deficits observed in simple as well as complex motor tasks. However, I’D patients have a well preserved internal model of force requirements [11,27]. In the task used in the present experiment, problems with accurate force control cannot completely account for the reduced speed scaling observed in the PD patients. The demands on precise force control are the greatest for the long movement amplitudesmall target-condition (ID = 5.54), where I’D patients performed similarly to the elderly control subjects. When greater force levels were required, as in the large movement amplitude-large target size condition, PD patients produced only marginal increases in

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speed. Because our task required fast movements, a slow force generation [28,29] and/ or a slow force release [30-321 may contribute to the inability to appropriately modulate movement speed. For example, when comparing the capability to produce small and large force levels, Muller and Stelmach [22] found for the small force levels similar force rates in I’D and control subjects. At the high force level, a different pattern emerged. Controls kept the time to achieve a given force level constant by increasing the rate of force development. In contrast, PD patients were unable to scale their rate of force development to maintain a constant time. An inefficient motor unit recruitment may be the neural substrate that causes the reduced scaling capability [33]. In PD patients who exhibited reduced force levels, Wierzbecka et al. [26] observed a tendency of motor unit activity to switch from the normal high frequency, continuous discharge patterns to a low frequency, synchronized patterns of activity. Besides a general undershooting in the PD patients, Wierzbicka et aZ.‘sfindings are especially appealing, because force generation capabilities are reduced when higher force levels were required, which parallels our findings for the large amplitude movements. Our findings are also consistent with other results [34,35] that examined large, fast movements in PD patients. Studies on motor units (MU) summarized by Glendinning and Enoka[36] revealed that MU activation is delayed in PD in comparison to elderly subjects. Other findings on MUs in PD patients compared to age-matched controls are the highly variable discharge rates, increased recruitment of low threshold MUs and increased co-activation [37]. On the one hand, the higher variability in the MU discharge cannot explain sufficiently our current results because the deficit of the PD patients is greatest in the condition with lesser force accuracy demands. On the other hand, in PD the selective involvement of fast-twitch muscle fibers may be the reason that large MUs, necessary for fast movements as in this study, are not well accessed. In summary, for the elderly and PD subjects in comparison to the young subjects the temporal characteristics of a discrete arm movement were similarly affected by the task difficulty requirements. Parkinson’s disease patients, like normals, had the general ability to modify velocity and acceleration, but did not appropriately scale movement speed for the larger movement amplitude possibly due to lower rates of force development.

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Acknowledgements-This study was supported by grants from the Arizona Disease Control Research Commission (82-0377) and National Institutes of Neurological Disorders and Stroke (NS 17421). The authors would Iike to thank Dr H. Hefter and Dr Y Rossetti for valuable discussions.