Exp Brain Res (2013) 227:323–331 DOI 10.1007/s00221-013-3491-7
RESEARCH ARTICLE
Comparing kinematic changes between a finger‑tapping task and unconstrained finger flexion–extension task in patients with Parkinson’s disease W. P. Teo · J. P. Rodrigues · F. L. Mastaglia · G. W. Thickbroom
Received: 17 October 2012 / Accepted: 14 March 2013 / Published online: 18 May 2013 © Springer-Verlag Berlin Heidelberg 2013
Abstract Repetitive finger tapping is a well-established clinical test for the evaluation of parkinsonian bradykinesia, but few studies have investigated other finger movement modalities. We compared the kinematic changes (movement rate and amplitude) and response to levodopa during a conventional index finger–thumb-tapping task and an unconstrained index finger flexion–extension task performed at maximal voluntary rate (MVR) for 20 s in 11 individuals with levodopa-responsive Parkinson’s disease (OFF and ON) and 10 healthy age-matched controls. Between-task comparisons showed that for all conditions, the initial movement rate was greater for the unconstrained flexion–extension task than the tapping task. Movement rate in the OFF state was slower than in controls for both tasks and normalized in the ON state. The movement amplitude was also reduced for both tasks in OFF and increased in the ON state but did not reach control levels. The rate and amplitude of movement declined significantly for both tasks under all conditions (OFF/ON and controls). The time course of rate decline was comparable for both tasks and was similar in OFF/ON and controls, whereas the tapping task was associated with a greater decline in MA, both in controls and ON, but not OFF. The findings indicate that both finger movement tasks show similar kinematic changes during a 20-s sustained MVR, but that movement amplitude is less well sustained during the tapping task than the unconstrained finger movement task.
W. P. Teo · J. P. Rodrigues · F. L. Mastaglia · G. W. Thickbroom (*) Australian Neuromuscular Research Institute, Centre for Neuromuscular and Neurological Disorders, University of Western Australia, Queen Elisabeth II Medical Centre, Nedlands, WA 6009, Australia e-mail:
[email protected]
Both movement rate and amplitude improved with levodopa; however, movement rate was more levodopa responsive than amplitude. Keywords Parkinson’s disease · Bradykinesia · Finger tapping · Unrestrained finger flexion–extension task · Movement rate · Movement amplitude
Introduction Signs of Parkinson’s disease (PD) such as bradykinesia, hypokinesia and dysrhythmia are clinically assessed within the Unified Parkinson’s Disease Rating Scale (UPDRS) by items 23–25 that comprise repetitive finger-tapping, grasping-releasing and pronation–supination movements of the hand (Goetz et al. 2007). These tasks can demonstrate slowness of movement, reduced amplitude, hesitations and decline in performance that can be assessed and rated by skilled observation. A number of studies have also measured finger-tapping performance quantitatively and have related these measures to UPDRS scores, disease severity and response to levodopa (LD) (Stegemoller et al. 2009; Espay et al. 2010, 2011). Finger–thumb opposition tapping tasks (TT) in PD involve constraint of index finger movement for the flexion phase, spatial alignment of the index finger and the thumb to execute the tap, and thumb movement at the same rate as index finger movement but typically over a small range of movement. These aspects may place additional demands on motor control that could influence the development of bradykinesia. Recently, we characterized the dynamics of a repetitive finger flexion–extension task (FET) that is executed through a comfortable range of movement at maximal voluntary rate (MVR) (Teo et al. 2012a, b).
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This task has parallels with TT, but movement of the index finger is unconstrained throughout the range of movement and does not involve other spatial or compound movement demands. We showed that in healthy controls, movement rate begins to decline within a few seconds of the start of this task and concluded that this decline in performance is central in origin (Rodrigues et al. 2008). In the present study, we have compared the kinematic changes during a conventional index finger TT and a FET performed through a comparable range of movement at MVR in a group of individuals with PD. We measured the movement rate (MR) and movement amplitude (MA) and the sustainability of these aspects of movement throughout the task OFF and ON medication and compared the kinematics of the two tasks in PD with a matched group of healthy control participants.
Methods Participants Eleven LD-treated patients with PD (patient’s demographic data and clinical features shown in Table 1) were recruited from movement disorder clinics at the Australian Neuromuscular Research Institute, Perth, Western Australia. A control (CTRL) group of 10 right-handed healthy participants age matched to the PD group (55–66 years of age, 6M, 4F) was also recruited. The study was approved by the University of Western Australia Human Research Ethics Committee and was conducted in accordance with the Declaration of Helsinki. All patients and control participants provided informed consent prior to their inclusion in the study. There were no reports of ill effects during or after the procedure. Table 1 PD patient’s demographic data and clinical features Sex (age)
Disease duration (yrs)
Hoehn and Yahr score
Total UPDRS
M (57) M (59) F (59) M (53) F (63) M (54) M (58) M (60) M (61) F (57)
8 5 7 5 9 7 6 8 9 6
3 2 2 1 3 2 1 1 3 2
63 49 51 30 69 55 26 21 68 45
M (59)
8
1
22
13
Kinematic measurements A light-weight goniometer (Single Axis Torsiometer Q150, Biometrics Ltd, UK) was attached across the second metacarpophalangeal joint of the right index finger to measure MR (Hz) and MA (deg). The right hand was secured to a modified hand brace that allowed the index finger and the thumb to have a full range of motion. Data acquisition was performed using a custom written LabVIEW (National Instrument Corporation, Austin, TX, USA) program running on a personal computer. Finger‑tapping task (TT) and finger flexion–extension task (FET) Figure 1 shows the subject’s hand set-up for the TT and FET. Both tasks were executed at MVR for 20 s. For the TT, participants were instructed to tap the index finger to the thumb as fast as possible through a comfortable range of movement of the index finger. For the FET, the index finger was flexed and extended through a similar range, while the thumb was maintained in a neutral position that did not impede finger movement. Verbal encouragement to maintain MVR was provided, and participants were able to observe their hand during the tasks. Experimental procedure The procedure began with a period of familiarization in which the first task to be performed (TT or FET) was demonstrated and participants practiced the movement for a few seconds. Participants self-selected a MA over a comfortable range of motion and were asked to try to maintain this MA at MR throughout the task. Two trials of the task were then recorded with a 5-min inter-trial rest period. This was repeated for the remaining task. The PD and CTRLs were classified into three conditions: PD off LD (OFF), PD on LD (ON) and CTRL. For the OFF condition, the PD group was requested to delay their morning medication on the day of testing, resulting in a 12-h withdrawal of LD. The TT and FET recordings were first made during this OFF condition. PD participants were then requested to consume their medication and given 1 h for the medication to take effect after which the TT and FET tasks were repeated. For all conditions, the TT and FET were performed in a pseudorandomized order. Data and statistical analyses Kinematic data were analysed using a custom-designed LabVIEW program. Each 20 s of kinematic data was divided into ten 2-s epochs, and the mean MR and MA were calculated for each epoch. Each epoch was then
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Fig. 1 A diagram of the hand set-up for the a TT and b FET. The TT was performed by tapping the index finger onto the thumb, while the FET was an unconstraint finger movement with the thumb pointing downwards so as not to impede movement
averaged across the two repeat trials that were performed for each task. The MR and MA values from the first (START) and last (END) epochs were compared to determine overall change within task (TT, FET) and between conditions (OFF, ON, CTRL). Statistical analysis was performed with multivariate analysis of variance (MANOVA) (Factor 1—TIME [START, END]; Factor 2—TASK [TT, FET]; Factor 3—CONDITION [OFF, ON, CTRL]). Post hoc t tests with Bonferroni correction for multiple comparisons were applied to determine where statistical significance occurred. Pearson’s product correlation coefficient was used to determine whether there was a relationship between UPDRS and percentage decline in MR and MA. All data were analysed with SPSS for windows version 19.0 (IBM, USA).
Bonferroni correction revealed significantly higher MR for the FET than the TT for all groups (OFF: 5.65 ± 0.1 vs. 5.31 ± 0.12 Hz; t(19) = 15.45, p
