Abnormal sensorimotor control,but intact force field adaptation,in multiple sclerosis subjects with no clinical disability

Abstract

In MS subjects with no clinical disability, we assessed sensorimotor organization and their ability to adapt to an unfamiliar dynamical environment. Eleven MS subjects performed reaching movements while a robot generated a speed-dependent force field. Control and adaptation performance were compared with that of an equal number of control subjects. During a familiarization phase, when the robot generated no forces, the movements of MS subjects were more curved, displayed greater and more variable directional errors and a longer deceleration phase. During the force field phase, both MS and control subjects gradually learned to predict the robot-generated forces. The rates of adaptation were similar, but MS subjects showed a greater variability in responding to the force field. These results suggest that MS subjects have a preserved capability of learning to predict the effects of the forces, but make greater errors when actually using such predictions to generate movements. Inaccurate motor commands are then compensated later in the movement through an extra amount of sensory-based corrections. This indicates that early in the disease MS subjects have intact adaptive capabilities, but impaired movement execution. Multiple Sclerosis 2008; 14: 330—342. http://msj.sagepub.com

Keywords

motor adaptation motor control multiple sclerosis robot therapy

Get full access to this article

View all access options for this article.

References

Lublin FD , Baier M. , Cutter G. Effect of relapses on development of residual deficit in multiple sclerosis . Neurology 2003; 61: 1528-32.

Rocca MA , Colombo B. , Falini A. , Ghezzi A. , Martinelli V. , Scotti G. et al. Cortical adaptation in patients with MS: a cross-sectional functional MRI study of disease phenotypes. Lancet Neurol 2005; 4: 618-26.

Wang J. , Hier DB Motor reorganization in multiple sclerosis. Neurol Res 2007; 29: 3-8.

Filippi M. , Rocca MA MRI evidence for multiple sclerosis as a diffuse disease of the central nervous system. J Neurol 2005; 252(Suppl 5): v16-24.

Shadmehr R. , Mussa-Ivaldi FA Adaptive representation of dynamics during learning of a motor task. J Neurosci 1994; 14: 3208-24.

Maschke M. , Gomez CM , Ebner TJ , Konczak J. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol 2004; 91: 230-8.

Smith MA , Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J Neurophysiol 2005; 93: 2809-21.

Martin CL , Phillips BA , Kilpatrick TJ , Butzkueven H. , Tubridy N. , McDonald E. , Galea MP Gait and balance impairment in early multiple sclerosis in the absence of clinical disability. Mult Scler 2006; 12: 620-8.

Solaro C. , Brichetto G. , Casadio M. , Roccatagliata L. , Ruggiu P. , Mancardi GL et al. Subtle upper limb impairment in asymptomatic multiple sclerosis subjects. Mult Scler 2007; 13: 428-32.

10.

Leocani L. , Comi E. , Annovazzi P. , Rovaris M. , Rossi P. , Cursi M. et al. Impaired short-term motor learning in multiple sclerosis: Evidence from virtual reality. Neurorehabil Neural Repair 2007; 21: 273-8.

11.

Poser CM , Paty DW , Scheinberg L. , McDonald WI , Davis FA , Ebers GC et al. New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann Neurol 1983; 13: 227-31.

12.

Kurtzke JF Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33: 1444-52.

13.

Sipe JC et al. A neurologic rating scale (NRS) for use in multiple sclerosis . Neurology 1984; 34: 1368-72.

14.

Casadio M. , Morasso PG , Sanguineti V. , Arrichiello V. Braccio di Ferro: a new haptic workstation for neuromotor rehabilitation. Technol Health Care 2006; 13: 1-20.

15.

Diedrichsen J. , Hashambhoy Y. , Rane T. , Shadmehr R. Neural correlates of reach errors. J Neurosci 2005; 25: 9919-31.

16.

Criscimagna-Hemminger SE , Donchin O. , Gazzaniga MS , Shadmehr R. Learned dynamics of reaching movements generalize from dominant to non-dominant arm. J Neurophysiol 2003; 89: 168-76.

17.

Cheng S. , Sabes PN Modeling sensorimotor learning with linear dynamical systems. Neural Comput 2006; 18: 760-93.

18.

Donchin O. , Francis JT , Shadmehr R. Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control . J Neurosci 2003; 23: 9032-45.

19.

Scheidt RA , Dingwell JB , Mussa-Ivaldi FA Learning to move amid uncertainty. J Neurophysiol 2001; 86: 971-85.

20.

Thoroughman KA , Shadmehr R. Learning of action through adaptive combination of motor primitives. Nature 2000; 407: 742-7.

21.

Gordon J. , Ghilardi MF , Cooper SE , Ghez C. Accuracy of planar reaching movements. II. Systematic extent errors resulting from inertial anisotropy. Exp Brain Res 1994 ; 99: 112-30.

22.

Mainero C. , Pantano P. , Caramia F. , Pozzilli C. Brain reorganization during attention and memory tasks in multiple sclerosis: insights from functional MRI studies. J Neurol Sci 2006; 245: 93-8.

23.

Filippi M. , Rocca MA , Mezzapesa DM , Ghezzi A. , Falini A. , Martinelli V. et al. Simple and complex movement-associated functional MRI changes in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis. Hum Brain Mapp 2004 ; 21: 108-17.

24.

Langkilde AR , Frederiksen JL , Rostrup E. , Larsson HB Functional MRI of the visual cortex and visual testing in patients with previous optic neuritis. Eur J Neurol 2002; 9: 277-86.

25.

Toosy AT , Werring DJ , Bullmore ET , Plant GT , Barker GJ , Miller DH et al. Functional magnetic resonance imaging of the cortical response to photic stimulation in humans following optic neuritis recovery. Neurosci Lett 2002; 330: 255-9.

26.

Filippi M. , Rocca MA , Mezzapesa DM , Falini A. , Colombo B. , Scotti G. et al. A functional MRI study of cortical activations associated with object manipulation in patients with MS. Neuroimage 2004; 21: 1147-54.

27.

Prange GB , Jannink MJ , Groothuis-Oudshoorn CG , Hermens HJ , Ijzerman MJ Systematic review of the effect of robot-aided therapy on recovery of the hemiparetic arm after stroke. J Rehabil Res Dev 2006; 43: 171-84.

28.

Mussa-Ivaldi FA , Hogan N. , Bizzi E. Neural, mechanical and geometric factors subserving arm posture in humans. J Neurosci 1985; 5: 2732-43.

29.

Ghahramani Z. , Hinton GE Parameter estimation for linear dynamical systems. University of Toronto, Toronto, 1996.