Disturbance of Sequential Movements in Patients With Parkinson's Disease

Abstract

The following sequences of two single movements were examined in 10 patients with Parkinson's disease and compared with the performance of 9 normal subjects of similar age. Isometric opposition of thumb and fingers to a force of 30 N ('squeeze'), followed by isotonic elbow flexion ('flex') through 15 degrees with the same arm. 'Squeeze' with the left hand followed by 'flex' with the right elbow. Isotonic opposition of thumb and fingers ('cut') through 90 degrees followed by isotonic 'flex' with the same arm. Isotonic elbow 'flex' followed by isometric 'squeeze' with the same arm. All movements were self-paced. Subjects were given instructions to move as rapidly as possible and to start the second movement immediately after the end of the first. Patients were slower than normal when each single movement was performed separately. There was a further decrease in speed when two movements were executed sequentially. This was due to an increase in movement duration of each of the component movements, especially the second, and to an increase in the pause between the first and second movements. In both normals and patients, there was no correlation between the times taken to perform the first and second movements of any of the four sequences that were studied. Because of this we suggest that the two components of the sequence remained under the control of two separate motor programs. When performing the sequential tasks, normal subjects automatically chose an interval between the onsets of the two separate movements of about 230 ms, even in tasks in which the duration of the first movement was less than 200 ms. If normal subjects were instructed to begin the second movement with an interonset interval of less than 200 ms, the speed of the second movement was much slower. Patients with Parkinson's disease automatically chose a much longer interonset interval of 400-500 ms. In addition, they exhibited difficulty in switching from the first to the second movement in the sequence. We suggest that the problems exhibited by patients with Parkinson's disease when they try to perform two rapid sequential movements can be seen as a deficit in the capacity to switch from one motor program to another within an overall motor plan.

Distinct Contribution of the Striatum and Cerebellum to Motor Learning

“…This notion is congruent with a series of studies showing that cerebellar damage impairs the ability to translate a programmed motor sequence into action before the onset of movement (Inhoff & Bisiacchi, 1990;Inhoff et al, 1989;Inhoff & Rafal, 1990). It should be noted that some researchers (Benecke, Rothwell, Dick, Day, & Marsden, 1987;Canavan, Passingham, Marsden, Quinn, Wyke, & Polkey, 1989;Georgiou, Bradshaw, Iansek, Phillips, Mattingley, & Bradshaw, 1994;Harrington & Haaland, 1991;Stelmach, Worringham, & Strand, 1987;Weiss, Stelmach, & Hefter, 1997;see Dominey & Jeannerod, 1997, for a review) have previously investigated the role of the striatum in the sequencing of movements, by examining the performance of patients with PD who were required to switch between two completely different types of motions such as elbow extension and hand squeeze (Benecke et al, 1987), or were asked to shift from one step in the sequence to the next by changing hand postures (Harrington & Haaland, 1991), in situations where patients had explicit knowledge of the sequence of movements they had to perform. By contrast, in this experiment, the notion first proposed by Flourens (1824), Babinski (1899), and Holmes (1939) that damage to the cerebellum produces a ''decomposition of movements'' was further investigated using a new task that did not require switching between separate movements, but instead measured the patients ability to perform a well-articulated sequence of movements in an implicit fashion.…”

“…The fact that patients with PD showed a significant facilitation effect, hence sug-gesting a preserved ability in combining acquired movements into a well-articulated action, may appear to be at variance with the results of recent clinical studies which suggest that PD impairs the smooth transition between two successive movements (Benecke et al, 1987;Canavan et al, 1989;Georgiou et al, 1994;Harrington & Haaland, 1991;Stern, Mayeux, Rosen, & Ilson, 1983;Weiss et al, 1997;see Dominey & Jeannerod, 1997, for a review). Several reasons may explain this apparent divergence of findings.…”

“…First, the difference could be related to the type of movements that were required. Indeed, in previous studies, a deficit in patients with PD was observed, for example, when they were asked to switch between two completely different types of movements such as elbow extension and hand squeeze (Benecke et al, 1987) or when transitions from one step in the sequence to the next required changes in hand posture (Harrington & Haaland, 1991). By contrast, no clear demarcation between the movements to perform while tracing the three juxtaposed simple figures in a triad was required, and thus our task did not elicit as much of the patients' capacity to switch from one motor program (which was learned in Phase III of testing) to another.…”

“…Second, the inconsistency may be due to the explicit vs implicit nature of the sequencing of movements that the patients had to execute. In the other studies, patients with PD acquired declarative knowledge of the sequence of movements they had to perform because (1) they were asked either to memorize the sequence (Rafal, Inhoff, Friedman, & Bernstein, 1987;Stelmach et al, 1987) or to practice it before the experimental testing began (Benecke et al, 1987;Georgiou et al, 1994;Georgiou, Bradshaw, Phillips, Bradshaw, & Chiu, 1995;Georgiou, Iansek, Bradshaw, Phillips, Mattingley, & Bradshaw, 1993;Jones, Phillips, Bradshaw, Iansek, & Bradshaw, 1992;Rafal et al, 1987) or (2) they were allowed to refer to a written version of the sequence they had to produce at all times during the experiment (Harrington & Haaland, 1991). In this study, however, the subjects were unaware that the triads in the Practiced condition were made of the consecutive juxtaposition of the simple figures they had practiced in Phase III, nor that the triads in the Unpracticed condition were composed of novel simple figures that they had never traced individually before.…”

Force related activations in rhythmic sequence production

“…Animal work by Mink (1996) and Boraud et al (2002) has implicated the BG in response selection. Response selection deficits are also evident in work with PD patients, who find it difficult to inhibit competing response alternatives and to initiate a correct response (Praamstra and Plat, 2001;Turner et al, 2003a;Desmurget et al, 2004a underlie problems in performing sequential movements in PD patients (Benecke et al, 1987). Our study revealed bilateral activation of the cerebellum.…”