Intention tremor and deficits of sensory feedback control in multiple sclerosis: a pilot study.

Megan Heenan,Douglas Woo,Scott A Beardsley,Robert A Scheidt

doi:10.1186/1743-0003-11-170

Abstract

BackgroundIntention tremor and dysmetria are leading causes of upper extremity disability in Multiple Sclerosis (MS). The development of effective therapies to reduce tremor and dysmetria is hampered by insufficient understanding of how the distributed, multi-focal lesions associated with MS impact sensorimotor control in the brain. Here we describe a systems-level approach to characterizing sensorimotor control and use this approach to examine how sensory and motor processes are differentially impacted by MS.MethodsEight subjects with MS and eight age- and gender-matched healthy control subjects performed visually-guided flexion/extension tasks about the elbow to characterize a sensory feedback control model that includes three sensory feedback pathways (one for vision, another for proprioception and a third providing an internal prediction of the sensory consequences of action). The model allows us to characterize impairments in sensory feedback control that contributed to each MS subject’s tremor.ResultsModels derived from MS subject performance differed from those obtained for control subjects in two ways. First, subjects with MS exhibited markedly increased visual feedback delays, which were uncompensated by internal adaptive mechanisms; stabilization performance in individuals with the longest delays differed most from control subject performance. Second, subjects with MS exhibited misestimates of arm dynamics in a way that was correlated with tremor power. Subject-specific models accurately predicted kinematic performance in a reach and hold task for neurologically-intact control subjects while simulated performance of MS patients had shorter movement intervals and larger endpoint errors than actual subject responses. This difference between simulated and actual performance is consistent with a strategic compensatory trade-off of movement speed for endpoint accuracy.ConclusionsOur results suggest that tremor and dysmetria may be caused by limitations in the brain’s ability to adapt sensory feedback mechanisms to compensate for increases in visual information processing time, as well as by errors in compensatory adaptations of internal estimates of arm dynamics.Electronic supplementary materialThe online version of this article (doi:10.1186/1743-0003-11-170) contains supplementary material, which is available to authorized users.

Highlights

Accurate arm and hand movements are the key to performing many daily tasks, but in individuals with Multiple Sclerosis (MS), the processes that control these movements are disrupted due to demyelination of the axonal projections that transmit information within and between brain areas
Tremor and dysmetria are most often associated with lesions in the cerebellum and/or the thalamic nuclei, suggesting impairment of the cortico-cerebellar sensorimotor control loops used for the planning and adaptive control of movement [16,17]; for review see Koch, et al [4]
Within the 2–6 Hz range associated with tremor, maximum power increased with the speed of movement and ranged from 0.22-5.31 cm2-s across MS subjects for their fastest tracings (Figure 3B)

Summary

Introduction

Accurate arm and hand movements are the key to performing many daily tasks, but in individuals with Multiple Sclerosis (MS), the processes that control these movements are disrupted due to demyelination of the axonal projections that transmit information within and between brain areas. Because neural lesions that develop in MS are distributed throughout the central nervous system, similar movement deficits (i.e. tremor) may result from differing impairments in the sensory feedback control pathways. Tremor and dysmetria are most often associated with lesions in the cerebellum and/or the thalamic nuclei, suggesting impairment of the cortico-cerebellar sensorimotor control loops used for the planning and adaptive control of movement [16,17]; for review see Koch, et al [4]. A therapy designed to compensate for one patient’s dysmetria caused by increased sensory processing delays may not be effective for another patient whose dysmetria is due to impaired prediction of limb dynamics. The development of effective therapies to reduce tremor and dysmetria is hampered by insufficient understanding of how the distributed, multi-focal lesions associated with MS impact sensorimotor control in the brain.

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