The influence of mental and motor load on handwriting movements in Parkinsonian patients

Abstract

This experiment tested the hypothesis that Parkinson’s disease (PD) patients are more vulnerable to a moderate level of secondary task load than elderly or young controls due to heightened variability in the motor system. PD patients, elderly, and young adults performed a handwriting task with different secondary tasks. The secondary task imposed motor load (i.e., speech) and/or a mental load (i.e., ignoring, repeating, or subtracting). The findings showed that, in contrast to young and elderly controls, PD patients tended to increase MT, accumulated pause time, and normalized jerk when the secondary task consisted primarily of motor load. Furthermore, it was shown that PD patients did not reduce writing sizes as result of a high level of mental load which finding suggests that writing in an automated fashion does not result in micrographia. The results are discussed in relation to strategies imposed to contend with reduced signal-to-noise levels in the motor system.

Introduction

The handwriting of Parkinson’s disease (PD) patients is more impaired in terms of force amplitude than in terms of force timing when compared to handwriting of the elderly Teulings and Stelmach, 1991a, Teulings and Stelmach, 1991b, Teulings and Stelmach, 1992, Van Gemmert et al., 1998. As a result of impairments in force amplitude, PD patients experience problems with the fine tuning of forces Stelmach and Worringham, 1988, Stelmach et al., 1989, Kunesch et al., 1995 and often report muscle weakness (Shindo and Yanagawa, 1992). The elderly, in turn, make slower and spatially more variable movements as compared to young adults Stelmach et al., 1987, Stelmach et al., 1988, Seidler-Dobrin and Stelmach, 1998, but to a lesser extent than PD patients (Contreras-Vidal et.al., 1995).

It is suggested that slower and more variable movements in the elderly as compared to younger adults are due to reduced signal-to-noise ratios in the motor system of the elderly Welford, 1981, Walker et al., 1997. These impaired signal-to-noise ratios are probably caused by a combination of physiological aging processes, such as loss of motor units (Lexell et al., 1988), and reduced muscle strength as result of a reduction of the number of muscle fibers per muscle (Vandervoort, 1992). Additionally, it is suggested that PD patients have smaller signal-to-noise ratios than the elderly (cf. Teulings and Stelmach, 1991a). This account of movement slowness and variability is based on two assumptions about signal-to-noise ratios in the motor system. Firstly, the motor system is inherently noisy (Fitts, 1954). The noise in the motor system reflects the combined result of the stochastic recruitment process of muscle units due to characteristics of muscle tissue, physiological tremor, stretch reflexes, springlike oscillations of the limbs, and correction servos from feedback processing (Van Galen and Schomaker, 1992). Secondly, noise in the motor system increases with larger force levels resulting in an increase of the variability in peak force Sherwood and Schmidt, 1980, Stelmach et al., 1989, Van Galen and De Jong, 1995. Therefore, rapid movements are generally more noisy than slower movements, because fast movements require higher levels of force.

Recent studies by Van Gemmert and Van Galen, 1994, Van Gemmert and Van Galen, 1996, Van Gemmert and Van Galen, 1997, Van Gemmert et al., 1998 on the effects of different kinds of stress on point-to-point aiming and handwriting movements, suggested that both mental load and physical stress reduce signal-to-noise ratios. Furthermore, these studies showed that subjects can adapt relatively easy to moderate levels of mental load and physical stress. In these studies, it was argued that an increase of noise in the motor system as a consequence of mental load or physical stress is diminished by the filtering properties of the pen–limb system and/or the signal is enhanced by increasing processing time.

The latter view to increase signal-to-noise ratios in the motor system by increasing processing time is based on the notion that as a signal accrues over time, its noise levels off. This principle, which has a long history in detection theory (Tanner and Swets, 1954), leads to prolonged movement duration (i.e., longer movement times and/or pauses). If movement duration is to be kept constant, this adaptation strategy is not optional, because longer pause intervals need to be added between movements to allow for more processing time.

The first option to increase the signal-to-noise ratio in the motor system is to use the filtering properties of the effector system to actively cope with increased levels of neuromotor noise. To this end, subjects may enhance limb stiffness which then suppresses high-frequency components of the movement, these components are thought to produce more variable movement trajectory and end-point outcomes Ghez and Martin, 1982, Hogan, 1984, Van Galen and Schomaker, 1992, Van Galen et al., 1990. To some extent, the latter mechanism may increase signal-to-noise ratios without it needs to reduce movement speed. Active cocontraction of the agonist and antagonist muscle that lead to an increase of tonic limb stiffness is preferred over the detection-theory based option to increase signal-to-noise ratios, because this option requires longer movement durations. However the increase in cocontraction without loss of performance speed requires accurate modulations of muscle force (Seidler-Dobrin et al., in press). In the present experiment, the coping strategies of PD patients, young, and elderly control subjects will be investigated under various levels of mental and motor load by analyses of signal-to-noise ratios of handwriting movements.

Morris et al. (1995) suggested that movement performance of PD patients deteriorates when secondary cognitive or motor tasks are performed. Other studies Gnanalingham et al., 1997, Kuzis et al., 1997 failed to show cognitive deficits in mildly affected PD patients. These findings suggest that as a result of secondary cognitive tasks, neuromotor noise in the motor system of PD patients and elderly controls may be elevated to the same extent. Therefore, we argue that in mildly affected PD patients, a secondary cognitive task should deteriorate motor performance to the same extend as performance of the elderly, which will be less for a task consisting of moderate levels of cognitive load as compared to a task consists moderate levels of motor load. It is predicted that a deterioration of motor performance will be exhibited by a reduction of movement speed. Generally, a reduction in movement speed could either result from an increase in movement duration or a decrease in movement amplitude. Reduction of stroke size (i.e., movement amplitude) in handwriting is one of the characteristic clinical signs of PD often referred to as micrographia Sandyk, 1995, Sandyk and Iacono, 1994, Tetrud, 1991, Helsper et al., 1996. If PD patients would reduce their movement amplitude as a result of a secondary cognitive task (i.e., mental load), but not as result of a secondary motor task (i.e., motor load), this could explain the reduced writing size (micrographia) of PD patients, because handwriting in daily life often occurs in situations where mental load is present, like simultaneous calculations, and memory recall. Evidence supporting this view is given by Oliveira et al. (1997) who showed that PD patients with micrographia benefitted from external cues to increase their writing size. They suggested that the external cues encouraged PD patients to write less automatically. Therefore, secondary tasks that increase mental load during handwriting should reduce writing size, because the writing task must then be performed in a more automated fashion to free resources to fulfil the requirements of the secondary task. To investigate this explanation and test the hypothesis that motor performance of PD patients deteriorates during motor load, an experiment was designed in which a handwriting task was performed under three levels of mental load, induced by a secondary arithmetic task, and two levels of motor load, induced by a secondary speech task. There were three subject groups: PD patients, normal young adults, and normal elderly adults.

We expected that increased motor load would increase the neural noise in the PD patients as manifested by increased variability (jerk), longer movement durations, and reduced writing size. Furthermore, we expected that a high level of mental load would show a similar deterioration of motor performance for PD patients as for the elderly. Finally, we predicted that the higher level of mental load would result in more variable movements and longer movement durations for both the elderly and young adults, but that the movements of the elderly would be more affected than those of the young adults, because signal-to-noise ratios are generally reduced in the elderly due to aging processes.