Preserved and impaired aspects of predictive grip force control in cerebellar patients

Abstract

Objective: To analyze preserved and impaired aspects of feedforward grip force control during cyclic arm movements with a hand-held object after cerebellar damage.

Methods: We tested eight subjects with unilateral or bilateral cerebellar pathologies and eight healthy control subjects. Participants performed cyclic vertical arm movements with a hand held instrumented object at three different speeds.

Results: Compared to controls, patients excerted increased grip forces. The minimum force ratio between grip force and load force was constant across all movement frequencies, suggesting that patients anticipated speed-related changes in load magnitudes by adjusting the grip force. Thus the scaling of grip force level to self-generated load magnitudes was preserved. The coupling between grip and load profiles was assessed by cross correlation analysis. Patients exhibited significantly decreased maximum coefficients of cross correlation implicating impaired anticipation of inertial load fluctuations. However feedforward control could be preserved, as obvious from zero time lags of the maximum cross correlation coefficient.

Conclusions: Our findings suggest that cerebellar lesions affect the processing of predictive grip force modulation in anticipation of inertial loads. Our results add further evidence to the theoretical concept that the cerebellum implements internal feedforward models. However, preserved functions may indicate compensatory mechanisms or extracerebellar aspects of grip and load force regulation.

Significance: The observed dissociation of performance deficits may have direct clinical implication and may guide the development of individual therapeutic strategies for patients with cerebellar disorders.

Introduction

Holding and transporting objects are skilful motor processes, frequently used in daily life. The motor commands for hand and finger forces must be selected and adjusted to the objects' physical properties, such as weight, shape and surface friction as well as to dynamic movement properties such as inertia.

In repetitive vertical movements the summation of gravitational and inertial loads results in a maximum of net load force at the lower turning point of the movement and a minimum at the upper turning point of the movement. It has been found that grip force changes in parallel with load force with a maximum peak in grip force occurring at the lower turning point of the movement and a minimum grip force peak at the upper turning point of the movement (Flanagan, 1993, Flanagan and Wing, 1995). The simultaneous modulation of grip and load forces indicates an anticipatory mode of grip force adjustment to upcoming load changes during object transport (Flanagan, 1993, Johansson and Cole, 1994, Flanagan and Wing, 1995). It has been proposed that such a control mechanism is based on the use of internal models of limb and object dynamics (Flanagan and Wing, 1997, Kawato and Wolpert, 1998, Blakemore and Frith, 2001, Flanagan and Vetter, 2003, Kawato and Kuroda, 2003). In this particular context, internal models may enable grip force anticipation. The cerebellum is considered to be the anatomical correlate of such internal models (Miall and Weir, 1993, Wing and Flanagan, 1998, Kawato and Wolpert, 1998, Kawato and Kuroda, 2003). Thus the cerebellum may play an important role in the prediction of the arm movement and its impact on the object dynamics, which is reflected in the coupling between grip and load force during object manipulation. In addition, single cell recordings in monkeys and imaging studies in healthy volunteers support the idea of a central role of the cerebellum in grip force regulation during object manipulation (Espinoza and Smith, 1990, Dugas and Smith, 1992, Kawato and Kuroda, 2003).

A number of studies investigating cerebellar pathologies documented impairments of grip force control. Holmes (1917) investigated acute cerebellar lesions after gun-shot injuries and showed impairments of the maintenance of near-isometric grip forces, problems of force calibration, increased response latencies to perturbations and lower grip force amplitudes (Holmes, 1917). Mai and Bolsinger investigated grip force behaviour in chronic cerebellar disease and also found an instability of isometric force maintenance, deficits of fast repetitive force changes and impaired force tracking (Mai and Bolsinger, 1988). Maximally generated grip forces were normal. Grip force control during grasping, lifting and holding of an object in patients with cerebellar atrophy was examined by Muller and Dichgans (1994b). Patients showed longer latencies between the onset of grip and lift forces, irregular force output and reduced peak grip forces. Also, Fellows et al. found a deficit in the temporal coordination between proximal arm muscles and finger forces when cerebellar patients lifted an object (Fellows et al., 2001). In contrast to the findings of Muller and Dichgans (1994b), Fellows et al. found exaggerated grip force levels in patients with cerebellar atrophy. When patients with cerebellar atrophy performed vertical point to point movements with a hand held object they applied exaggerated grip force levels to hold and transport the object (Nowak et al., 2002a). In addition, the precision of grip force modulation with the movement induced loads was impaired in patients compared to control subjects.

Müller and Dichgans tested patients with unilateral cerebellar diseases and found similar deficits of grip and load force coordination as found in cerebellar atrophy patients, however the deficits were restricted to the affected side (Muller and Dichgans, 1994a). Fellows et al. showed that focal damage to the dentate nucleus resulted in similar deficits in the control of fingertip forces during object lifting as seen in cerebellar atrophy with lower lifting velocities and elevated grip force levels (Fellows et al., 2001). However, damage to the posterior inferior cerebellar artery (PICA) region did not have any effect on grip force coordination during object manipulation (Fellows et al., 2001).

In order to investigate how cerebellar disease affects predictive grip force adjustments to different inertial loads we examined grip force control during cyclic vertical arm movements with a hand held mass performed at three different speeds. Continuous cyclic movements impose quite vigorous demands on the motor system planning grip force. The rapid fluctuations in load force, both in time and magnitude, have to be compensated by accurate grip force adjustments planned several steps ahead. Patients were asked to move the object at three different frequencies, resulting in different inertial load fluctuations. The question is how cerebellar subjects adjust their force levels to self-induced inertial load variations. For instance, a general increase in grip force is a quite common observation during object manipulation in cerebellar subjects (Babin-Ratte and Sirigu, 1999, Fellows, 2001, Nowak, 2002). Given the results of previous findings, we hypothesize that: (1) Patients use exaggerated grip forces to compensate load force changes in cyclic movements. (2) Patients may nevertheless increase their grip force level with increasing load and keep the ratio between grip and load forces constant across different inertial loads. Such an observation might suggest that grip force scaling is processed differentially to variations in arm movement speed, despite impaired force calibration. (3) The precision of the coupling between grip force and movement induced load fluctuations may be impaired. Our data may shed some light to the understanding how the cerebellum contributes to predictive finger force control during object manipulation.