Practice as an intervention to improve speeded motor performance and motor learning in Parkinson’s disease

Journal of the Neurological Sciences 174 (2000) 127–136 www.elsevier.com / locate / jns

Practice as an intervention to improve speeded motor performance and motor learning in Parkinson’s disease a, b a Andrea L. Behrman *, James H. Cauraugh , Kathye E. Light a

b

Department of Physical Therapy, University of Florida, Gainesville, FL 32610 -0154, USA Department of Exercise and Sport Sciences, University of Florida, Gainesville, FL 32611 -8205, USA Received 12 July 1999; received in revised form 4 January 2000; accepted 6 January 2000

Abstract Individuals with Parkinson’s disease have difficulty initiating and performing complex, sequential movements. Practice generally leads to faster initiation and execution of movements in healthy adults, however, whether practice similarly improves motor performance in patients with Parkinson’s disease remains controversial. To assess the effects of practice on motor performance, patients with Parkinson’s disease and control subjects practiced two, rapid arm-reaching tasks with different levels of movement complexity for 120 trials each over 2 days. Response programming was studied by analyzing the overall reaction time latency of each movement and its fractionated sub-components, premotor and motor time. Practice effects were investigated by comparing pretest performance to immediate and delayed retention test performances (10-min and 48-h rest intervals, respectively). Both patients with Parkinson’s disease and control subjects improved speeded performance of sequential targeting tasks by practice and retained the improvement across both retention test intervals. Finding a learning effect for persons with Parkinson’s disease supports practice as an effective rehabilitation strategy to improve motor performance of specific tasks for patients with Parkinson’s disease.  2000 Published by Elsevier Science B.V. All rights reserved. Keywords: Parkinson’s disease; Movement complexity; Practice; Response programming; Reaction time

1. Introduction Parkinson’s disease alters movement capability and generalized aging contributes to loss of motor control [1,2]. In that most individuals with Parkinson’s disease are also in the senior population, the exact differences between the effects of Parkinson’s disease and aging are not clear. A slowdown in movement initiation speed is known to occur both in those with Parkinson’s disease and advanced age [3,4]. When exploring the cause of movement initiation slowdown with the chronometric model of information processing [5], specific deficits are more easily observed. One of the simplest information processing models inAbbreviations: RT, reaction time; MT, movement time *Corresponding author. Tel.: 11-352-395-0085; fax: 11-352-3950731. E-mail address: [email protected] (A.L. Behrman)

cludes the stages of stimulus identification, response selection, and response programming [6]. With progressive aging, all stages of information processing are slowed. Whether the stages are all slowed to the same extent is a controversy in the aging literature [2,4,7]. Response programming is the final stage of information processing and is the stage where the movement response is structured and executed [6,8]. Response programming is defined as a transformation of a selected, cognitive, or abstract idea of a movement response into a code as execution commands for the task [6]. Individuals with Parkinson’s disease are reported to have particular deficits in response programming as compared to the stages of stimulus identification and response selection [3,9–12]. In healthy adults, response programming slowdown is observable as the difficulty of the required movement is increased, such as when multiple steps or directional changes are added [7,13–15]. This manipulation of a movement

0022-510X / 00 / $ – see front matter  2000 Published by Elsevier Science B.V. All rights reserved. PII: S0022-510X( 00 )00267-7

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task leads to an increased time to prepare the initiation or reaction time (RT) of a speeded response. For this study, movement complexity was manipulated to observe and compare response programming capabilities between individuals with Parkinson’s disease and age-matched persons without Parkinson’s disease. Movement complexity effects or increases in the time to prepare a response when the task is more difficult have not been demonstrated in the RTs of subjects with Parkinson’s disease [12,16] as compared to the predicted increased RTs of control subjects. Further, researchers have proposed that a lack of a complexity effect in persons with Parkinson’s disease is due to a deficit in response programming. The benefits of practice to movement training for individuals with Parkinson’s disease is also controversial. Moreover, extensive practice diminishes the response complexity effect in healthy subjects [17,18]. Practice is the primary method used for movement training [19] and re-training, however, its benefits for motor learning in persons with Parkinson’s disease have been limited and task specific [20–22]. To extend the understanding of motor learning relative to Parkinson’s disease, we investigated the response programming stage of information processing and the effects of practice on programming in patients with Parkinson’s disease. To further delineate the central versus peripheral processing, total RT was fractionated by surface electromyography (EMG) into premotor RT and motor RT [23]. Fractionating reaction time provides a microanalysis of response programming which may assist in explaining differences in the central and peripheral contributions to RT. In this study, persons with Parkinson’s disease were tested for response programming and practice effects using two different movement responses based on levels of complexity in a simple RT paradigm. Movement complexity was varied by altering the number of movement components (from one to four) and the number of directional changes (from zero to three) [13–15]. The effect of this practice over 2 days and its interaction with the movement response complexity were examined to differentiate central processing effects from peripheral changes in an analysis of the movement initiation problem in Parkinson’s disease.

2. Methods

2.1. Subjects Fifteen adults diagnosed with Parkinson’s disease, aged 57–82 (mean, 74 years) and 15 age- and gender-matched adults, aged 58–83 (mean, 73 years) without Parkinson’s disease participated in this study. Each group consisted of 10 male and 5 female participants. Table 1 presents descriptive data for group comparisons. Analysis of the age data for the Parkinson’s disease and control groups by a one-way ANOVA revealed no significant group differ-

Table 1 Clinical data for the Parkinson’s disease and control group subjects Variable

Age Duration of PD Box and block ADL Depression Mini-mental state

Group Parkinson’s disease

Control

M

S.D.

Range

M

S.D.

Range

74 7 56 5.5 1.9 28

7 4 11 1 1.6 1.6

56–82 1–15 38–74 2–6 0–5 25–30

73 – 64 6 0.5 29

7 – 12 0 0.8 1.1

57–83 – 40–80 6–6 0–3 26–30

ences. Six patients with Parkinson’s disease were in Stage II and nine were in Stage III of the Hoehn and Yahr disability rating scale [24]. All patients with Parkinson’s disease were on medication to diminish the symptoms of Parkinson’s disease and maintained their routine medication schedule and dosage during the course of the study. Tests and practice sessions were conducted during medication ‘on’ periods for patients with Parkinson’s disease as verified by the patients. All participants were community dwellers, right-hand preferred, and were evaluated for upper extremity motor skill impairment [25], cognitive state and memory [26,27], depression [28], and activities of daily living [29]. The mean score for the control group (64 blocks) on the Box and Block test, a standardized timed test of manual dexterity, is consistent with normative, age-matched data [30]. The PD group, however, demonstrated significantly poorer scores (56 blocks; t-test analysis, P,0.05) indicating motor impairment. Three participants with Parkinson’s disease having scores below standardized normal values for mental state were not included in the study, thus 16 individuals with Parkinson’s disease met the entry criteria and were included in the study. Separate Mann–Whitney U tests were performed to compare ADL, depression, and mini-mental state scores between the groups. A significant difference was found only for the Geriatric Depression scale indicating that the Parkinson’s disease group had higher scores than the control group (P,0.05). Further review of the scores revealed that only three of the patients with Parkinson’s disease were categorized as depressed on the Geriatric Depression Scale, whereas no subject in the control group attained a level of depression on the scale [28]. All subjects in the study demonstrated adequate visual and hearing ability to perform the experimental tasks. No control subjects had a history of neurologic dysfunction. All subjects received $50.00 for completing the study. The University of Florida’s Institutional Review Board provided approval to conduct this study and all subjects provided informed written consent for the study.

2.2. Apparatus The response time data collection system consisted of a

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simple-RT auditory stimulus to indicate response initiation and five microswitches to record the initial release time and subsequent parts in movement time completion. Total response time is comprised of RT and movement time (MT) components. RT is the interval of time from the onset signal to initiation of the movement and MT is the interval of time from the initiation of the response to completion of the movement. The microswitches (AbleNet 100) required a minimum of 20–30 g of force for closure and were 6.35 cm in diameter. These switches were connected to a Lafayette Performance-Pack sequential-movement timer (Model 63520) which provided immediate visual digital readouts for the RTs and response times. Activation of the auditory response onset signal simultaneously initiated the clocks of the sequential timer to record RTs, MTs, and response times. A signal converter assigned specific signal amplitudes to the response stimulus and switch onset signals for identification during acquisition and analysis. The RT, MT, and EMG signals were collected simultaneously on videotape via a 4-channel, Vetter Scientific Instrumentation Recorder. EMG signals were collected via surface electrodes and an EMG signal-amplification system (Therapeutics Unlimited Inc.) Pre-amplified, active surface electrodes with an amplification of 353 consisted of two silver–silver chloride 1 cm diameter electrodes in an epoxy-mounted pre-amplifier with centers 2 cm apart. During data acquisition, input of all timing and EMG signals was monitored with a 2channel digital storage oscilloscope (Hitachi-VC 6023). The videotape data were transferred to a Biopac / AcqKnowledge data acquisition and software analysis program.

2.3. Experimental tasks All subjects were familiarized with the right arm-reaching tasks. The experimenter demonstrated the tasks, manually guided the participant through each movement pattern, and allowed two practice trials of each movement pattern. The fast, arm-reaching test movements were: (1) a simple lateral movement from right to left (12.7 cm) and (2) a more complex, four-part movement consisting of the simple movement segment and three additional movements requiring directional changes (Fig. 1). The testing and practice schedule consisted of pretests for simple reaction times (SRTs) on the two movements on Day 1, followed by 2 days of practice (Day 1 and 2), and immediate and delayed retention tests (Day 2 and 3). The three test sessions occurred in a Monday, Wednesday, Friday or a Tuesday, Thursday, Saturday sequence. For the arm-reaching tasks, the right fingers were positioned flat on the first switch, wrist supported by the table, and arm relaxed with surface EMG electrodes applied and secured over the right biceps brachii muscle. The electrodes recorded EMG activity prior to (baseline activity) and during the movement response. A reference electrode was attached to the opposite lateral tibia. The

129

Fig. 1. Simple and complex arm-reaching movements.

EMG signals were led to a high-impedance (15 mV at 100 Hz) differential amplifier (Therapeutics Unlimited Inc.). The resultant amplification allowed a gain of 1000–10 000 with a bandwidth of 20 Hz–4 kHz. The common mode rejection ratio was 87 dB at 60 Hz. EMG activity was recorded on videotape during the testing and practice sessions of Day 1, 2, and 3. Testing and practice were conducted in a quiet room with the participant sitting in an adjustable-height chair such that their right arm was supported on the standard-height table with the testing apparatus. For the simple movement, following presentation of a verbal ‘ready’ signal, then an auditory, variable (1–3 s) response onset signal, the participant released the first switch and moved laterally to the left 12.7 cm to tap the second switch (Fig. 1). RT was the time between the onset of the response stimulus (auditory buzzer) and the release of the first switch, whereas MT was the time interval from the release of the first switch to the tap of the second switch. Premotor time was the interval of time from the presentation of the response stimulus to onset of EMG activity. EMG onset was defined as a three standard deviation change in EMG activity from baseline EMG activity [31,32]. Motor time was the interval from onset of EMG to the initiation of the movement response (release of the first switch). Response time was the time between the onset of the response stimulus and the tap of the second switch (completion of the simple movement). Fig. 2 illustrates the time intervals (RT, premotor time, motor time, and MT) within the total response time (see interval 1–4) for the simple task as designated by switch and EMG onsets. The more complex movement consisted of the initial and identical simple movement but with the addition of three subsequent movement segments with directional changes (Fig. 1). RT measurements were identical to the simple movement condition. MT was the total time required to complete the four-part movement sequence

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Fig. 2. Response movement component times for the right biceps during performance of the complex arm-reaching movement. The upper channel indicates response stimulus onset and switch contact times. The lower channel indicates biceps electromyographic (EMG) activity. The numbers identify stimulus, switch component, and EMG onsets: 15response stimulus onset, 2 (and triangle marker)5EMG onset, 35reaction time release switch, 45first switch, 55last switch. Premotor time5interval 1–2. Motor time5interval 2–3. Reaction time5interval 1–3. Movement time5interval 3–5. Total response time5interval 1–5. Note that the simple arm-reaching task has the same designated time intervals and fractionated reaction time components, however the total response time5interval 1–4.

beginning with release of the first switch. Premotor and motor times were measured as described for the simple movement. Response time was the time between the onset of the stimulus and the tap of the fifth and final switch (completion of the complex movement). Fig. 2 illustrates the time intervals (RT, premotor time, motor time, and MT) within the total response time for the complex task (see interval 1–5) as designated by switch and EMG onsets. Prior to the study, identical warning signal patterns and testing order were assigned for each age- and gendermatched pair of control subjects and subjects with Parkinson’s disease. Pretests and posttests consisted of 40 SRT trials (20 trials of each of the simple and complex movements), randomly assigned between participant, without feedback. Catch trials were included to prevent anticipatory false starts (4 per 20 trials). If during testing, data indicated a false start, anticipation of the start button by the participant, inattentiveness, or errors in arm-reaching movements, then the trial was immediately repeated. Practice extended over a two-day period to complete 120 SRT trials. Trials were presented in blocks of 10 trials each with the movement types switched between simple

and complex after every block. During the practice trials, summary feedback was provided after every 10 trials and used by the subject for performance evaluation and goal setting. Trials were presented in 10-s intervals and subjects were provided a 30-s rest between every trial block and a 1-min rest after every 6-trial blocks. Upon completion of the practice session on Day 2, subjects rested for 10 min. During this time, subjects responded to questions for mental state and disability rating. Following the rest period, an immediate-retention test was administered. On Day 3, a 48-h delayed-retention test was conducted. The identical procedure for the arm-reaching task, including recording EMG activity was followed for both retention tests with the exception that no performance feedback was provided. Testing and practice schedules remained constant across the 3 days for each subject.

2.4. Analysis The four dependent variables were premotor time, motor time, total RT, and movement time (MT). Before analysis, the raw EMG measures were fully rectified and smoothed.

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131

Table 2 Descriptive data for mean reaction times (ms) for simple and complex arm-reaching tasks for groups: Parkinson’s disease and control a RT

Simple arm-reaching task Pretest

Complex arm-reaching task

Imme retention

Del retention

Pretest

Imme retention

Del retention

PD

CL

PD

CL

PD

CL

PD

CL

PD

CL

PD

CL

Mean

314

297

255

241

250

236

354

337

267

248

262

253

S.D.

64

38

39

29

40

31

67

59

43

39

40

44

220 – 446

243 – 374

173 – 314

191 – 286

175 – 328

192 – 300

264 – 530

243 – 476

192 – 319

191 – 317

196 – 333

187 – 322

Range

a

RT5reaction time; S.D.5standard deviation; PD5Parkinson’s disease group; CL5control group; Imme retention5immediate retention; Del retention5delayed retention.

EMG onsets were indicated by an algorithm of three standard deviations above the baseline mean across the 0.5-s time interval of EMG activity prior to the visuallyidentified deflection of the EMG signal from the baseline [32] using the data analysis software. The time intervals for premotor time, RT, and total response time were identified and recorded from switch-onset recordings. Motor time was calculated by subtracting premotor time from RT, and movement time was calculated by subtracting RT from the total response time. Subject means for each dependent variable: total RT, premotor, motor, movement, and total response time were calculated for 20 trials of each condition for the pre-, immediate-retention, and delayed retention tests. Values two standard deviations above or below each subject’s mean were removed from the data set as nonrepresentative outliers and then the means were re-calculated. One subject was eliminated from the Parkinson’s disease group because of an insufficient number of adequate test trials. The descriptive data are reported by group for each dependent variable: RT, premotor, motor, and movement time in Tables 2–5, respectively. Separate 23233 (Group3Complexity3Test Session) mixed design ANOVAs were performed to analyze the dependent variables (total RT, premotor, motor time, and

movement time) and the effects of practice for RT. Tukey’s Honestly Significant Difference follow-up procedure was performed, when appropriate. All tests were conducted with the alpha level set at 0.05.

3. Results

3.1. Reaction time Analysis of the total RT data revealed a significant Complexity3Test Session interaction, F (2,56)57.36, P, 0.05 (see Fig. 3). Post-hoc analysis determined that the overall RT mean for the simple movements (305 ms) was significantly different than for the complex movement (346 ms). In the immediate-retention test, RTs for both simple and complex movements decreased significantly from the pretest values. The RTs, however, were not significantly different from one another. The delayed-retention test RT means did not change for either the simple or complex movements from the immediate-retention values. These findings indicate that both the Parkinson’s disease and control groups exhibited a movement complexity effect for RT. With practice of each movement (120 trials each)

Table 3 Descriptive data for mean premotor times (ms) for simple and complex arm-reaching tasks for groups: Parkinson’s disease and control a PreTime

Simple arm-reaching task Pretest

Complex arm-reaching task

Imme retention

Del retention

Pretest

Imme retention

Del retention

PD

CL

PD

CL

PD

CL

PD

CL

PD

CL

PD

CL

Mean

172

178

140

133

137

136

195

211

144

140

137

151

S.D.

53

28

36

24

33

17

61

49

35

22

38

24

103 – 305

135 – 235

90 – 208

88 – 174

96 – 206

111 – 160

113 – 378

132 – 315

98 – 208

102 – 168

94 – 220

110 – 195

Range

a

PreTime5premotor time; S.D.5standard deviation; PD5Parkinson’s disease group; CL5control group; Imme retention5immediate retention; Del retention5delayed retention.

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132

Table 4 Descriptive data for mean motor times (ms) for simple and complex arm-reaching tasks for groups: Parkinson’s disease and control a MotorT

Simple arm-reaching task Pretest

Complex arm-reaching task

Imme retention

Del retention

Pretest

Imme retention

Del retention

PD

CL

PD

CL

PD

CL

PD

CL

PD

CL

PD

CL

Mean

139

114

112

108

111

98

156

124

119

105

119

101

S.D.

34

24

27

18

32

20

38

29

28

24

34

26

95 – 193

69 – 152

73 – 189

70 – 144

67 – 179

66 – 136

93 – 226

87 – 185

73 – 168

70 – 164

76 – 179

56 – 162

Range

a

MotorT5motor time; S.D.5standard deviation; PD5Parkinson’s disease group; CL5control group; Imme retention5immediate retention; Del retention5delayed retention. Table 5 Descriptive data for mean movement times (ms) for simple and complex arm-reaching tasks for groups: Parkinson’s disease and control a MT

Simple arm-reaching task Pretest

Complex arm-reaching task Imme retention

Del retention

Pretest

Imme retention

Del retention

PD

PD

PD

Control

PD

Control

PD

Control

PD

Control

Mean

200

183

130

106

134

111

1376

1169

972

831

949

820

S.D.

74

68

32

38

35

41

377

279

233

131

230

134

103 – 368

79 – 350

84 – 195

45 – 195

76 – 197

33 – 194

918 – 2127

708 – 1804

624 – 1474

573 – 1060

654 – 1398

543 – 1034

Range

Control

Control

a

MT5movement time; S.D.5standard deviation; PD5Parkinson’s disease group; CL5control group; Imme retention5immediate retention; Del retention5delayed retention.

followed by a 10-min rest period and immediate-retention test, both groups improved significantly in RTs for both the simple and complex movements. The movement complexity effect for RT diminished with practice across the two days, such that the RT for the complex movement became equal to that of the simple movement. This

Fig. 3. Reaction time means and standard deviations for Complexity3 Test Session interaction. Imme5immediate. Del5delayed.

relationship was sustained across a 48-h rest interval as indicated by the delayed-retention test. These findings were similar for both subjects with and without Parkinson’s disease.

3.1.1. Premotor time A significant Complexity3Test Session interaction was also revealed for premotor times, F (2, 56)56.65, P,0.05 and is displayed in Fig. 4. As was observed in the total RT findings, the difference between mean premotor times for the simple and complex movements was significant only for the pretest session (175 and 203 ms) in both the Parkinson’s disease and control groups. These premotor values decreased significantly at the immediate retention test (137 and 142 ms) and were maintained across the delayed retention test (136 and 144 ms). The premotor times mirror those of RT for the movement complexity effect. In the pretest, the simple movement premotor values were significantly faster than those for the complex movement. However, with practice, this complexity effect was eliminated and it remained stable for both immediate retention and delayed retention intervals. 3.1.2. Motor time A third Group3Test Session interaction was found for motor time analysis, F (2,56)55.79, P,0.05 (see Fig. 5).

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Fig. 4. Premotor time means and standard deviations for Complexity3 Test Session interaction. Imme5immediate. Del5delayed.

Fig. 6. Movement time means and standard deviations for Complexity3 Test Session interaction. Imme5immediate. Del5delayed.

The post-hoc analysis indicated that the group with Parkinson’s disease had significantly slower motor times than the control group. From the pretest to the immediateretention test, motor times decreased by 33 ms for the group with Parkinson’s disease and were sustained across the delayed-retention test interval. Motor time did not significantly change in the group without Parkinson’s disease.

and delayed-retention tests. These results indicate that individuals with Parkinson’s disease, as well as those without Parkinson’s disease, became significantly faster in MTs for the complex task, but no significant change was observed for the MTs in the simple task. Furthermore, both groups maintained the improved MT performance in the complex task when tested for delayed retention 48 h later.

3.2. Movement time

4. Discussion

The 23333 (Group3Complexity3Test Session) analysis of mean MTs indicated a significant Complexity3Test Session interaction, F (2,56)594.07, P,0.05 (Fig. 6). After practice, significantly faster MTs were identified only for the complex movement with values changing from the pretest to the immediate-retention test (1.27 s–901 ms). These faster MTs were sustained between the immediate-

4.1. Practice: reaction time and fractionated reaction time

Fig. 5. Motor time means and standard deviations for Group3Test Session interaction. Imme5immediate. Del5delayed.

The significantly decreased RTs at the immediate-retention test for both groups demonstrated the relatively immediate benefits of practice. More importantly, the effect of practice on RTs for both groups was sustained across a 48-h rest interval. Sustaining the performance level across a retention period indicated a learning effect of practice for response programming of the complex armreaching task. The current finding that persons with Parkinson’s disease benefited similarly from practice for response programming when compared to persons without Parkinson’s disease is striking and very important. Previous literature has characterized the benefits of motor skill practice for persons with Parkinson’s disease as limited with a slower rate of improvement and significantly less improvement compared to the outcomes for persons without Parkinson’s disease [33–36], though exceptions have also been found [21,22]. In this study, practice resulted in a parallel decrease in premotor and overall RTs for both the Parkinson’s disease and control groups. This result was expected for the healthy elders and was consistent with the practice literature for healthy individuals [37,38]. Overall mean

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motor times also decreased from the pretest to the immediate-retention test only for persons with Parkinson’s disease and persisted at the delayed retention test. A change in neuromuscular coordination or adaptation may account for the change in motor times in persons with Parkinson’s disease [39], though such a change did not occur in the control subjects [38]. This study of practice on motor learning and response programming relative to fractionated RTs in persons with Parkinson’s disease is a new contribution. Across the practice sessions, persons with Parkinson’s disease improved the cognitive processing component of reaction time in preparing the more complex movement and demonstrated relatively lasting effects on premotor time. Such sustained improvements have significant implications concerning the use of practice for re-training motor behavior in Parkinsonian patients. This work suggests that initiation speeds for simple targeting tasks can be improved in individuals with Parkinson’s disease by practice. This finding is consistent with the conclusion of Agostino et al. [21] that although patients with Parkinson’s disease demonstrate impaired motor control, a parallel impairment in motor learning should not be surmized. In addition, practice did have an immediate and significant effect on decreasing the motor time of patients with Parkinson’s disease but not in the control group and the effect was sustained for the delayed retention test. The literature presents varied findings concerning altered motor times in persons with Parkinson’s disease when compared to controls [39–45]. Our initial motor time findings were comparable to those of Sheridan et al. [40]. Improvements in motor time are attributed to changes in the peripheral neuromuscular and physiological processes required to initiate and develop muscle activity. An improvement in motor time typically accompanies activities enhancing function of the peripheral apparatus, such as strengthening. In this study, subjects simply practiced a motor task. Glendinning and Enoka [39] characterized motor unit behavior in persons with Parkinson’s disease as having inconsistent discharge rates, increased number of motor units activated at low forces of contraction, and increased muscle coactivation. Secondary disuse and weakness may further contribute to altered motor unit activity in persons with Parkinson’s disease. Practice of the experimental tasks may have promoted increased familiarity with the motor task and heightened neuromuscular activity in an already compromised system. Practice may have afforded persons with Parkinson’s disease a change in neuromuscular coordination, improved consistency of motor unit discharge, or possible decreases in muscle coactivation, thus decreasing their motor times. Furthermore, the current study demonstrates that individuals with Parkinson’s disease retain the ability to develop a single motor program and to effectively use that program. This learning ability has previously been observed in individuals with Parkinson’s disease practicing

tracking tasks and repetitions of hand postures and single movement sequences [22,34,46,47]. In comparison, Haaland et al. [22] observed differential deficits in learning by patients with Parkinson’s disease when exposed to randomized practice conditions (i.e. variable and randomized speed practice) for rotary pursuit performance as opposed to beneficial results following blocked conditions (single speeds) of practice. Haaland et al. [22] speculated that practicing under variable practice conditions may hinder the development of a single or generalized motor program by individuals with Parkinson’s disease. This view is consistent with the findings of the present study in which blocked practice of the simple and complex movements may have promoted a similar practice benefit for healthy adults and patients with Parkinson’s disease.

4.2. Practice: movement time With practice, persons with Parkinson’s disease, have been reported to improve the speed of buttoning under both single and dual-task interference conditions [36]. In our study, the decrease in movement times for both Parkinson’s disease and control groups practicing the complex movement was consistent with the literature [15]. The fact that improved MT was maintained for both subject groups upon delayed retention is one of the most important findings in this study. Practice of fast movements may be particularly beneficial for increasing the performance speed of persons with Parkinson’s disease and have long-lasting effects on motor performance. Sustained performance at the delayed-retention test is a strong indicator of motor learning effects and the potential for benefits beyond the period of practice. Slowness in the execution of movements has a significant impact on the performance of everyday activities whether such slowness is due to healthy aging or disease processes such as Parkinson’s. Interventions to assist speed of performance are thus advantageous and important for both populations. Practice is a critical variable for improving the speed of a movement response across healthy age groups [15,48] and impacts both RT and MT components. Practice of skills to improve speeded performance may be a viable strategy for increasing speed and function in the rehabilitation of individuals with Parkinson’s disease. These studies were conducted in a period during the day when persons with Parkinson’s disease reported being in an ‘on’ state. The findings are generalizable only to persons on medication to relieve the symptoms of Parkinson’s disease and practicing a motor task during an ‘on’ state. The findings of this study indicate a valuable effect of practice under these specific conditions. Improvements in motor function resulting from practice during the ‘on’ periods may also transfer into the ‘off’ periods, though this was not tested in this study. Many physical therapies are provided during the ‘on’ periods in which the individual with Parkinson’s disease is most mobile and able even to

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participate in the activity as compared to the ‘off’ periods. Improving function during the ‘off’ period is a critical and valuable goal of intervention as this period severely compromises the patients’ abilities to perform activities of daily living and other functional or social tasks. Assessing first, the effect of practice during an ‘off’ state on ‘off’ state motor performance and second, the transfer of practice during an ‘on’ state to ‘off’ state motor performance would both be important next steps in determining the relevance of practice as an intervention strategy for individuals with Parkinson’s disease.

with Parkinson’s disease has been shown to be limited, perhaps task specific, and dependent upon the practice conditions. In this study, practice had beneficial effects on both cognitive and peripheral components of fast movement responses. Everyday lives are filled with tasks requiring the performance of rapid, discrete, aiming movements. Based on the findings of this study, the benefits of practice may be extended to the performance of other movements using a single motor program for execution. The implications from this study encourage the testing of such potential in persons with Parkinson’s disease.

5. Summary

Acknowledgements

The most important finding of this study was that individuals with Parkinson’s disease: (1) improved speeded performance of sequential targeting tasks by practice, and (2) retained the improvement across a 2-day interval. Persons with Parkinson’s disease benefited from practicing two, fast arm-reaching tasks as much as individuals without PD. The particular benefit of practice for the components of a fast, complex movement response were on: (1) premotor time, the cognitive component of information processing, (2) motor time, the peripheral component of RT, and (3) movement execution speed. In particular, response programming and movement execution speed of the more complex task improved with practice. The movement complexity effect was diminished by practice for both the Parkinson’s disease and control groups indicating further evidence for the benefits of practice in response programming for both groups. Persons with Parkinson’s disease were able to use a predictable, environmental stimulus as a cue for programmed responses of rapid aiming. In addition, a learning effect for these improvements was sustained across both a 10-min and 48-h rest intervals. Determining this learning effect for persons with Parkinson’s disease is important in justifying practice as an effective rehabilitation intervention for individuals with Parkinson’s disease to improve motor performance. From a theoretical perspective, this study demonstrates that Parkinson’s disease has not limited the capacity of individuals to improve motor performance of speeded responses by practice. Based on the retention-test findings, blocked practice resulted in a relatively permanent change in behavior for persons with and without Parkinson’s disease. From a clinical and intervention perspective, this study indicates that practice can be viewed as an effective training variable for improving response speed in persons with Parkinson’s disease. These benefits of practice can only be promoted for the performance of rapid, discrete, sequential targeting responses of the arms in individuals with mild to moderate impairments secondary to Parkinson’s disease. In the literature to date, the extent of the benefits of practice on speed of performance in persons

Participation by members of the Ocala, Gainesville, and Sarasota Parkinson’s Disease Support Groups and the Gainesville American Association of Retired Persons in this study is acknowledged and appreciated. This work was supported in part by a grant from the Foundation for Physical Therapy, Inc.

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