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Disruptions in joint control during drawing arm movements in Parkinson’s disease

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Abstract

Impairments in control of multi-joint arm movements in Parkinson’s Disease (PD) were investigated. The PD patients and age-matched elderly participants performed cyclical arm movements, tracking templates of a large circle and four differentially oriented ovals on a horizontal table. The wrist was immobilized and the movements were performed with shoulder and elbow rotations. The task was performed with and without vision at a cycling frequency of 1.5 Hz. Traces of the arm endpoint, joint-motion parameters represented by range of motion and relative phase, and joint-control characteristics represented by amplitude and timing of muscle torque were analyzed. The PD patients provided deformations of the template shapes that were not observed in movements of elderly controls. The deformations were consistent for each shape but differed across the shapes, making quantification of impairments in the endpoint movement difficult. In contrast, the characteristics of joint control and motion demonstrated systematic changes across all shapes in movements of PD patients, although some of these changes were observed only without vision. A specification of the PD influence was observed at the level of joint control and it was not distinguishable in joint and endpoint motion, because of the property of multi-joint movements during which control at each joint influences motion at the other joints. The results suggest that inability of PD patients to provide fine muscle torque regulation coordinated across the joints contributes to the altered endpoint trajectories during multi-joint movements. The study emphasizes the importance of the torque analysis when deficits in multi-joint movements are investigated, because specific impairments that can be detected in joint-control characteristics are difficult to trace in characteristics of joint and endpoint kinematics, because of interactions between joint motions.

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References

  • Alberts JL, Tresilian JR, Stelmach GE (1998) The co-ordination and phasing of a bilateral prehension task. The influence of Parkinson’s disease. Brain 121:725–742

    Article  PubMed  Google Scholar 

  • Amrhein PC (1996) Age-related slowing in movement parameterization studies: not what you might think. In: Fernandez AM, Teasdale N (eds) Changes in sensory motor behavior in aging, vol 114. Elsevier Science BV: North Holland, pp 1–25

    Google Scholar 

  • Barbeau A (1980) Biochemical aging in Parkinson’s disease. In: Amadocci L, Davison AN, Antuono P (eds) Aging of the brain and dementia, vol 13. Raven Press, New York, pp 275–285

    Google Scholar 

  • Bejjani B, Damier P, Arnulf I, Bonnet AM, Dormont D, Pidoux B, Cornu P (1997) Pallidal stimulation for Parkinson’s disease. Two targets?. Neurology 49:1564–1569

    CAS  PubMed  Google Scholar 

  • Benecke R, Rothwell JC, Dick JPR, Day BL, Marsden CD (1987) Simple and complex movements off and on treatment in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 50:296–303

    CAS  PubMed  Google Scholar 

  • Birren JE (1974) Translations in gerontology—from lab to life. Psychophysiology and speed of response. Am Psychol 29:808–815

    CAS  PubMed  Google Scholar 

  • Buchanan JJ (2004) Learning a single limb multijoint coordination pattern: the impact of a mechanical constraint on the coordination dynamics of learning and transfer. Exp Brain Res 156:39–54

    Article  PubMed  Google Scholar 

  • Burleigh A, Horak F, Nutt J, Frank J (1995) Levodopa reduces muscle tone and lower extremity tremor in Parkinson’s disease. Can J Neurol Sci 22:280–285

    CAS  PubMed  Google Scholar 

  • Calne D, Snow B, Lee C (1992) Criteria for diagnosing Parkinson’s disease. Ann Neurol 32:125–127

    Article  Google Scholar 

  • Castiello U, Bennett KMB, Bonfiglioli C, Peppard RF (2000) The reach-to-grasp movement in Parkinson’s disease before and after dopaminergic medication. Neuropsychologia 38:54–59

    Article  Google Scholar 

  • Chaffin DB, Andersson GBJ (1984) Occupational Biomechanics. Wile, New York, pp 64–65

    Google Scholar 

  • Cooke JD, Brown JD, Brooks VB (1978) Increased dependence on visual information for movement control in patients with Parkinson’s disease. Can J Neurol Sci 5:413–415

    CAS  PubMed  Google Scholar 

  • Dounskaia N (2005) The internal model and the leading joint hypothesis: implications for control of multi-joint movements. Exp Brain Res. DOI 10.1007/s00221-005-2339-1 (in press)

    Google Scholar 

  • Dounskaia N, Swinnen SP, Walter CB, Spaepen AJ, Verschueren SMP (1998) Hierarchical control of different elbow-wrist coordination patterns. Exp Brain Res 121:239254

    Article  Google Scholar 

  • Dounskaia N, Swinnen SP, Walter CB (2000) A principle of control of rapid multijoint movements: the leading joint hypothesis. In: Winter JM, Crago PE (eds) Biomechanics and neural control of posture and movement. Springer-Verlag, New York, Inc, pp 390–403

    Google Scholar 

  • Dounskaia N, Ketcham CJ, Stelmach GE (2002a) Commonalities and differences in control of a large set of drawing movements. Exp Brain Res 146:11–25

    Article  CAS  PubMed  Google Scholar 

  • Dounskaia N, Ketcham CJ, Stelmach GE (2002b) Influence of biomechanical constraints on horizontal arm movements. Motor Control 6:366–387

    PubMed  Google Scholar 

  • Fahn S, Elton RL (1987) Members of the UPDRS Development Committee. Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Leiberman A (eds) Recent Developments in Parkinson’s Disease. Florham Park, NJ: Macmillan Health Care Information 2:153–163

  • Flash T, Inzelberg R, Schectman E, Korcyzn AD (1992) Kinematic analysis of upper limb trajectories in Parkinson’s disease. Exp Neurol 118:215–226

    Article  CAS  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state, a practical method for grading the cognitive state of patients for the clinicians. J Psych Res 2:189–198

    Article  Google Scholar 

  • Galloway JC, Koshland GF (2002) General coordination of shoulder, elbow and wrist dynamics during multijoint arm movements. Exp Brain Res 142:163–180

    Article  PubMed  Google Scholar 

  • Gordon J, Ghilardi MF, Cooper SE, Ghez C (1994) Accuracy of planar reaching movements. II. Systematic extent errors resulting from inertial anisotropy. Exp Brain Res 99:112–130

    CAS  PubMed  Google Scholar 

  • Gordon J, Ghilardi MF, Ghez C (1995) Impairments of reaching movements in patients without proprioception. I. Spatial errors. J Neurophysiol 73:347–360

    CAS  PubMed  Google Scholar 

  • Gribble PL, Ostry DJ (1999) Compensation for interaction torques during single- and multi-joint limb movement. J Neurophysiol 82:2310–2326

    CAS  PubMed  Google Scholar 

  • Hallett M, Khoshbin S (1980) A physiological mechanism of bradykinesia. Brain 103:301–304

    CAS  PubMed  Google Scholar 

  • Hirashima M, Kudo K, Ohtsuki T (2003) Utilization and compensation torques during ball-throwing movements. J Neurophysiol 89:1784–1796

    PubMed  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    CAS  PubMed  Google Scholar 

  • Hogan N (1985) The mechanics of multi-joint posture and movement control. Biol Cybern 52:315–331

    Article  CAS  PubMed  Google Scholar 

  • Hollerbach JM, Flash T (1982) Dynamic interactions between limb segments during planar arm movement. Biol Cybern 44:67–77

    Article  CAS  PubMed  Google Scholar 

  • Horak FB, Frank J, Nutt J (1996) Effects of dopamine on postural control in parkinsonian subjects: scaling, set and tone. J Neurophysiol 75:2380–2390

    CAS  PubMed  Google Scholar 

  • Jackson GM, Jackson SR, Hindle JV (2000) The control of bimanual reach-to-grasp movements in hemiparkinsonian patients. Exp Brain Res 132:390–398

    Article  CAS  PubMed  Google Scholar 

  • Jennings PJ (1995) Evidence of incomplete motor programming in Parkinson’s disease. J Mot Behav 27:310–324

    PubMed  Google Scholar 

  • Johnson KA, Cunnington R, Bradshaw JL, Phillips JG, Iansek R, Rogers MA (1998) Bimanual co-ordination in Parkinson’s disease. Brain 121:743–753

    Article  PubMed  Google Scholar 

  • Ketcham CJ, Dounskaia N, Stelmach GE (2004) Age-related differences in the control of multijoint movements. Mot Control 8:422-436

    Google Scholar 

  • Klein CS, Rice CL, March GD (2001) Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91:1341–1349

    CAS  PubMed  Google Scholar 

  • Klockgether T, Borutta M, Rapp H, Spieker S, Dichgans J (1995) A defect of kinesthesia in Parkinson’s disease. Mov Disord 10:450–465

    Article  PubMed  Google Scholar 

  • Latash ML, Anson JG (1996) What are “normal movements” in atypical population? Behav Brain Sci 19:55–106

    Google Scholar 

  • Latash ML, Aruin AS, Shapiro MB (1995) The relation between posture and movement: study of a simple synergy in a two-joint task. Hum Mov Sci 14:79–107

    Article  Google Scholar 

  • Lee G, Dounskaia N, Ketcham CJ, Stelmach GE (2004) Age-related adaptive strategies of joint control during line drawing task. Abstract Viewer/Itinerary Planer. Society for Neuroscience (online)

  • Levin O, Ouamer M, Steyvers M, Swinnen SP (2001) Directional tuning effects during cyclical two-joint arm movements in the horizontal plane. Exp Brain Res 141:471–484

    Article  CAS  PubMed  Google Scholar 

  • Mardia KV (1972) Statistics of directional data. Academic Press, NY

    Google Scholar 

  • Mortimer JA, Pirozzolo FJ, Maletta GJ (1982) Overview of the aging motor system. In: Mortimer JA, Pirozzolo FJ, Maletta GJ (eds) The aging motor system. Praeger, New York

    Google Scholar 

  • Pfann KD, Corcos DM, Moore CG, Hasan Z (2002) Circle-drawing movements at different speeds: role of inertial anisotropy. J Neurophysiol 88:2399–2407

    PubMed  Google Scholar 

  • Poizner H, Feldman AG, Levin MF, Berkinblit MB, Hening WA, Patel A, Adamovich SV (2000) The timing of arm-trunk coordination is deficient and vision-dependent in Parkinson’s patients during reaching movements. Exp Brain Res 133:279–292

    Article  CAS  PubMed  Google Scholar 

  • Putnam CAA (1993) Sequential motions of body segments in striking and throwing skills: descriptions and explanations. J Biomech 26:125–135

    Article  PubMed  Google Scholar 

  • Rand MK, Stelmach GE, Bloedel JR (2000) Movement accuracy constraints in Parkinson’s disease patients. Neuropsychologia 38:203–212

    Article  CAS  PubMed  Google Scholar 

  • Sainburg RL, Kalakanis D (2000) Differences in control of limb dynamics during dominant and nondominant arm reaching. J Neurophysiol 83:2661–2675

    CAS  PubMed  Google Scholar 

  • Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 73:820–835

    CAS  PubMed  Google Scholar 

  • Saling M, Adler CH, Alberts JL, Stelmach GE (1996) Kinematic properties of prehensile movements in Parkinson’s disease patients. Neurology 46:A141

    Google Scholar 

  • Schneider K, Zernicke RF, Ulrich BD, Jensen JL, Thelen E (1990) Understanding movement control in infants through the analysis of limb intersegmental dynamics. J Mot Behav 22:521–535

    PubMed  Google Scholar 

  • Seidler RD, Alberts JL, Stelmach GE (2001) Parkinson’s disease affects the ability to control multijoint movements. Exp Brain Res 140:335–344

    Article  CAS  PubMed  Google Scholar 

  • Sheridan MR, Flowers KA (1990) Movement variability and bradykinesia in Parkinson’s disease. Brain 113:1149–1161

    PubMed  Google Scholar 

  • Sheridan MR, Flowers KA, Hurrel J (1987) Programming and execution of movement in Parkinson’s disease. Brain 110:1247–1271

    PubMed  Google Scholar 

  • Stelmach GE, Teasdale N, Phillips J, Worringham CJ (1989) Force production characteristics in Parkinson’s disease. Exp Brain Res 76:165–172

    Article  CAS  PubMed  Google Scholar 

  • Swinnen SP, Van Langendonk L, Vershueren S, Peeters G, Dom R, De Weert W (1997) Interlimb coordination deficits in patients with Parkinson’s disease during the production of two-joint oscillations in the sagittal plane. Mov Disord 12:958–968

    CAS  PubMed  Google Scholar 

  • Teasdale N, Phillips J, Stelmach GE (1990) Temporal movement control in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:862–868

    CAS  PubMed  Google Scholar 

  • Teulings HL, Contreras-Vidal JL, Stelmach GE, Adler CH (1997) Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Exp Neurol 146:159–170

    Article  CAS  PubMed  Google Scholar 

  • Virji-Babul N, Cooke JD (1995) Influence of joint interactional effects on the coordination of planar two-joint arm movements. Exp Brain Res 103:451–459

    Article  CAS  PubMed  Google Scholar 

  • Wing AM (1988) A comparison of the rate of pinch grip force increases and decreases in Parkinsonian bradykinesia. Neuropsychologia 26:479–482

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The work was supported by NS39352 and NS43502 grant from the National Institute of Neurological Diseases and Strokes. Caroline Ketcham is now with Department of Health and Kinesiology, Texas A&M University, College Station, TX 77843-4243. Berta Leis is now with Booth Gardner Parkinson’s Care Center, Evergreen Hospital Medical Center, Kirkland, WA 98034.

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Correspondence to Natalia Dounskaia.

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Dounskaia, N., Ketcham, C.J., Leis, B.C. et al. Disruptions in joint control during drawing arm movements in Parkinson’s disease. Exp Brain Res 164, 311–322 (2005). https://doi.org/10.1007/s00221-005-2251-8

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  • DOI: https://doi.org/10.1007/s00221-005-2251-8

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