Hereditary Cerebellar Ataxia Progressively Impairs Force Adaptation During Goal-Directed Arm Movements

Abstract

We investigated how humans with hereditary cerebellar degeneration [spinocerebellar ataxia (SCA) type 6 and 8, n = 9] and age- and sex-matched healthy controls (n = 9) adapted goal-directed arm movements to an unknown external force field. We tested whether learning could be generalized to untrained regions in the workspace, an aspect central to the idea of an internal model, and if any learning could be retained. After removal of the force field, SCA patients showed little or no learning-related aftereffects indicating that repeated force-field exposure never led to successful force compensation. In contrast, healthy control subjects quickly adapted their movements to the new force field. The difference in force adaptation was significant for movements to targets that required both the shoulder and elbow joint (P < 0.001). Moreover, the generalization of learned movements to targets outside the learned workspace was prevented by the cerebellar degeneration (P < 0.01). Retention of force adaptation was significantly lower in SCA patients (P = 0.003). The severity of ataxia in SCA patients correlated negatively with the extent of learning (r = -0.84, P = 0.004). Our findings imply that progressive loss of cerebellar function gradually impairs force adaptation. The failure to generalize learning suggests that cerebellar degeneration prevents the formation of an internal representation of the limb dynamics.

Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

“…However, visuomotor adaptation is known to be subserved by both explicit and implicit processes (Mazzoni and Krakauer 2006;Taylor et al 2014), while adjustment of grip and load forces during lifting seems to be largely implicit, evidenced by the fact that the size-weight illusion persists after appropriate motor adjustments have been made (Flanagan and Beltzner 2000). These tasks also differ in their dependence on the cerebellum; patients with cerebellar degeneration are impaired in adapting to visuomotor rotations (Martin et al 1996;Maschke et al 2004;Smith and Shadmehr 2005;Chen et al 2006;Tseng et al 2007;Rabe et al 2009b) but show no apparent deficit in adjusting grip and load forces to objects of unusual densities (Rabe et al 2009a).…”

Does a basic deficit in force control underlie cerebellar ataxia?

“…This coordination requirement was greater than in our pretests and may explain why deficits were observed even in a 1-DOF task. Given that cerebellar patients have difficulty adapting to novel environments Maschke et al 2004;Smith and Shadmehr 2005), a deficit in cerebellar performance in our main experiment might be due to an inability to understand the mapping between force and the visual display of force instead of an inability to control force. The two pretests were intended to test patients' ability to control the two aspects of this mapping (magnitude and direction).…”

The effect of cerebellar cortical degeneration on adaptive plasticity and movement control

“…The cerebellum has also been implicated in a more complex form of motor learning, namely, sensorimotor adaptation to visual and mechanical distortions. This view is supported by clinical studies, which found that adaptation is often reduced or abolished in patients with cerebellar disease (Deuschl et al 1996;Diedrichsen et al 2005;Gauthier et al 1979;Martin et al 1996;Maschke et al 2004;Tseng et al 2007;Weiner et al 1983). Further support comes from functional neuroimaging studies, which observed an increase of cerebellar activity during an adaptation task (e.g., Flament et al 1996;Graydon et al 2005;Imamizu et al 2000;Krakauer et al 2004;Krebs et al 1998;Lang et al 1988).…”