Experimental Brain Research

, Volume 194, Issue 2, pp 259–283 | Cite as

Velocity control in Parkinson’s disease: a quantitative analysis of isochrony in scribbling movements

  • Paolo Viviani
  • Pierre R. Burkhard
  • Sabina Catalano Chiuvé
  • Corrado Corradi dell’Acqua
  • Philippe Vindras
Research Article

Abstract

An experiment was conducted to contrast the motor performance of three groups (N = 20) of participants: (1) patients with confirmed Parkinson Disease (PD) diagnose; (2) age-matched controls; (3) young adults. The task consisted of scribbling freely for 10 s within circular frames of different sizes. Comparison among groups focused on the relation between the figural elements of the trace (overall size and trace length) and the velocity of the drawing movements. Results were analysed within the framework of previous work on normal individuals showing that instantaneous velocity of drawing movements depends jointly on trace curvature (Two-thirds Power Law) and trace extent (Isochrony principle). The motor behaviour of PD patients exhibited all classical symptoms of the disease (reduced average velocity, reduced fluency, micrographia). At a coarse level of analysis both isochrony and the dependence of velocity on curvature, which are supposed to reflect cortical mechanisms, were spared in PD patients. Instead, significant differences with respects to the control groups emerged from an in-depth analysis of the velocity control suggesting that patients did not scale average velocity as effectively as controls. We factored out velocity control by distinguishing the influence of the broad context in which movement is planned—i.e. the size of the limiting frames—from the influence of the local context—i.e. the linear extent of the unit of motor action being executed. The balance between the two factors was found to be distinctively different in PD patients and controls. This difference is discussed in the light of current theorizing on the role of cortical and sub-cortical mechanisms in the aetiology of PD. We argue that the results are congruent with the notion that cortical mechanisms are responsible for generating a parametric template of the desired movement and the BG specify the actual spatio-temporal parameters through a multiplicative gain factor acting on both size and velocity.

Keywords

Parkinson’s disease Movement control Isochrony Two-thirds Power Law 

References

  1. Adamovich SV, Berkinblit MB, Hening W, Sage J, Poizner H (2001) The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets in Parkinson’s disease. Neuroscience 104:1027–1041PubMedGoogle Scholar
  2. Ashe J (1997) Force and the motor cortex. Behav Brain Res 87:255–269PubMedGoogle Scholar
  3. Baldissera F, di Loreto S, Florio T, Scarnati E (1994) Short-latency excitation of hindlimb motoneurons induced by electrical stimulation of the pontomesencephalic tegmentum in the rat. Neurosci Lett 169:13–16PubMedGoogle Scholar
  4. Benecke R, Rothwell JC, Dick JPR, Day BL, Marsden CD (1986) Performance of simultaneous movements in patients with Parkinson’s disease. Brain 109:739–757PubMedGoogle Scholar
  5. Benecke R, Rothwell JC, Dick J, Day BL, Marsden CD (1987) Simple and complex movements off and on treatment in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 50:296–303PubMedGoogle Scholar
  6. Berardelli A, Dick JPR, Rothwell JC, Day BL, Marsden CD (1986a) Scaling of the size of the first agonist EMG burst during rapid wrist movements in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 49:1273–1279PubMedGoogle Scholar
  7. Berardelli A, Accornero N, Argenta M, Meco G, Manfredi M (1986b) Fast complex arm movements in Parkinson’s disease. J Neurol Neurosurg Psychiatry 49:1146–1149PubMedGoogle Scholar
  8. Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146PubMedGoogle Scholar
  9. Bloxham CA, Mindel TA, Frith CD (1984) Initiation and execution of predictable and unpredictable movements in Parkinson’s disease. Brain 107:371–384PubMedGoogle Scholar
  10. Bock O, Eckmiller R (1986) Goal-directed arm movements in absence of visual guidance: evidence for amplitude rather than position control. Exp Brain Res 62:451–458PubMedGoogle Scholar
  11. Bock O, Arnold K (1992) Motor control prior to movement onset: preparatory mechanisms for pointing at visual targets. Exp Brain Res 90:209–216PubMedGoogle Scholar
  12. Braak H, Rüb U, Sandmann-Keil D, Gai WP, de Vos RAI, Jansen Steur ENH et al (2000) Parkinson’s disease: affection of brain stem nuclei controlling premotor and motor neurons of the somatomotor system. Acta Neuropathol 99:489–495PubMedGoogle Scholar
  13. Braak H, Del Tredici K, Rüb U, de Vos RAI, Jansen Steur ENH, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedGoogle Scholar
  14. Brotchie PR, Iansek R, Horne MK (1991) Motor function of the globus pallidus. 1. Neuronal discharge and parameters of movement. Brain 114:1667–1683PubMedGoogle Scholar
  15. Brown JS, Knauft EB, Rosenbaum G (1948) The accuracy of positioning reactions as a function of their direction and extent. Am J Psychol 61:167–182PubMedGoogle Scholar
  16. Brown RG, Jahanshahi M (1998) An unusual enhancement of motor performance during bimanual movement in Parkinson’s disease. J Neurol Neurosurg Psychiatry 64:813–816PubMedGoogle Scholar
  17. Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y (1990) Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level (Article in French). Acta Neurol Belg 90:207–217PubMedGoogle Scholar
  18. Castiello U, Bennett KMB (1997) The bilateral reach-to-grasp movement of Parkinson’s disease subjects. Brain 120:593–604PubMedGoogle Scholar
  19. Day BL, Dick JP, Marsden CD (1984) Patients with Parkinson’s disease can employ a predictive motor strategy. J Neurol Neurosurg Psychiatry 47:1299–1306PubMedGoogle Scholar
  20. Delwaide PJ, Pepin JL, de Pasqua V, Maertens de Noordhout A (2000) Projections from basal ganglia to tegmentum: a subcortical route for explaining the pathophysiology of Parkinson’s disease signs? J Neurol (suppl 2)II:75–81Google Scholar
  21. Demirci M, Grill S, McShane L, Hallett M (1997) A mismatch between kinaesthetic and visual perception in Parkinson’s disease. Ann Neurol 41:781–788PubMedGoogle Scholar
  22. Desmurget M, Vindras P, Gréa H, Viviani P, Grafton ST (2000) Proprioception does not quickly drift during visual occlusion. Exp Brain Res 134:363–377PubMedGoogle Scholar
  23. Desmurget M, Grafton ST, Vindras P, Gréa H, Turner RS (2003) Basal Ganglia network mediates the control of movement amplitude. Exp Brain Res 153:197–209PubMedGoogle Scholar
  24. Desmurget M, Gaveau V, Vindras P, Turner RS, Broussolle E, Thobois S (2004a) On-line motor control in patients with Parkinson’s disease. Brain 127:1754–1773Google Scholar
  25. Desmurget M, Grafton ST, Vindras P, Gréa H, Turner RS (2004b) The basal ganglia network mediates the planning of movement amplitude. Eur J Neurosci 19:2871–2880PubMedGoogle Scholar
  26. Desmurget M, Turner RS (2008) Testing basal ganglia motor functions through reversible inactivations in the posterior internal globus pallidus. J Neurophysiol 99:1057–1076PubMedGoogle Scholar
  27. Draper IT, Johns RS (1964) The disordered movement in parkinsonism and the effect of drug treatment. Bull Hosp J Hopkins 115:465–480Google Scholar
  28. Evarts EV, Teräväinen H, Calne DB (1981) Reaction times in Parkinson’s disease. Brain 104:167–186PubMedGoogle Scholar
  29. Favilla M, Gordon J, Hening W, Ghez C (1990) Trajectory control in targeted force impulses. VII Independent setting of amplitude and direction in response preparation. Exp Brain Res 79:530–538PubMedGoogle Scholar
  30. Flash T, Inzelberg R, Schechtman E, Korczyn AD (1992) Kinematic analysis of upper limb trajectories in Parkinson’s disease. Exp Neurol 118:215–226PubMedGoogle Scholar
  31. Flowers KA (1975) Ballistic and corrective movements on an aiming task. Neurology 25:413–421PubMedGoogle Scholar
  32. Flowers KA (1976) Visual ‘closed-loop’ and ‘open-loop’ characteristics of voluntary movement in patients with parkisonism and intention tremor. Brain 99:269–310PubMedGoogle Scholar
  33. Flowers KA (1978a) Some frequency response characteristics of Parkinsonism on pursuit tracking. Brain 101:19–34PubMedGoogle Scholar
  34. Flowers KA (1978b) Lack of prediction in the motor behavior of Parkinsonism. Brain 101:35–52PubMedGoogle Scholar
  35. Freeman FN (1914) Experimental analysis of the writing movement. Psychol Rev 17:1–46Google Scholar
  36. Fu QG, Flament D, Coltz JD, Ebner TJ (1995) Temporal encoding of movement kinematics in discharge of primate primary motor and premotor neurons. J Neurophysiol 73:836–854PubMedGoogle Scholar
  37. Fu QG, Suarez JI, Ebner TJ (1993) Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. J Neurophysiol 70:2097–2116PubMedGoogle Scholar
  38. Georgiou N, Iansek R, Bradshaw JL, Phillips JG, Mattingley JB, Bradshaw JA (1993) An evaluation of the role of internal cues in the pathogenesis of parkinsonian hypokinesia. Brain 116:1575–1587PubMedGoogle Scholar
  39. Georgopoulos AP, Caminiti R, Kalaska JF, Massey JT (1983a) Spatial coding of movement: a hypothesis concerning the coding of movement direction by motor cortical populations. Exp Brain Res Suppl 7:327–336Google Scholar
  40. Georgopoulos AP, DeLong MR, Crutcher MD (1983b) Relations between parameters of step-tracking movements and single cells discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J Neurosci 3:1586–1598PubMedGoogle Scholar
  41. Georgopoulos AP (1990) Neurophysiology of reaching. In: Jeannerod M (ed) Attention and performance XIII. Erlbaum, Hillsdale, pp 227–263Google Scholar
  42. Ghilardi MF, Alberoni M, Rossi M, Franceschi M, Mariani C, Fazio F (2000) Visual feedback have differential effects on reaching movements in Parkinson’s and Alzheimer disease. Brain Res 876:112–123PubMedGoogle Scholar
  43. Glickstein M, Stein J (1991) Paradoxical movement in Parkinson’s disease. Trends Neurosci 14:480–482PubMedGoogle Scholar
  44. Godaux E, Koulischer D, Jacquy J (1992) Parkinsonian bradykinesia is due to depression in the rate of rise of muscle activity. Ann Neurol 31:93–100PubMedGoogle Scholar
  45. Gordon J, Ghilardi MF, Ghez C (1994a) Accuracy of planar reaching movements: 1. Independence of direction and extent variability. Exp Brain Res 99:97–111PubMedGoogle Scholar
  46. Gordon J, Ghilardi MF, Cooper SE, Ghez C (1994b) Accuracy of planar reaching movements: 2. Systematic extent errors resulting from inertial anisotropy. Exp Brain Res 99:112–130PubMedGoogle Scholar
  47. Hallett M, Khoshbin S (1980) A physiological mechanism of bradykinesia. Brain 103:301–314PubMedGoogle Scholar
  48. Hallett M, Shahani BT, Young RR (1977) Analysis of stereotyped voluntary movements at the elbow in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 40:1129–1135PubMedGoogle Scholar
  49. Harrington DL, Haaland KY (1991) Sequencing in Parkinson’s disease: abnormalities in programming and controlling movement. Brain 114:99–115PubMedGoogle Scholar
  50. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMedGoogle Scholar
  51. Houk JC, Wise SP (1995) Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action. Cereb Cortex 2:95–110Google Scholar
  52. Inase M, Buford JA, Anderson ME (1996) Changes in the control of arm position, movement, and thalamic discharge during local inactivation in the globus pallidus of the monkey. J Neurophysiol 75:1087–1104PubMedGoogle Scholar
  53. Jahanshahi M, Brown RG, Marsden CD (1992) Simple and choice reaction time and the use of advance information for motor preparation in Parkinson’s disease. Brain 115:539–564PubMedGoogle Scholar
  54. Johnson MTV, Kipnis AN, Lee MC, Loewenson RB, Ebner TJ (1991) Modulation of the stretch reflex during volitional sinusoidal tracking in Parkinson’s disease. Brain 114:443–460PubMedGoogle Scholar
  55. Kendall MG, Stuart A (1968) The advanced theory of statistics. Griffin, LondonGoogle Scholar
  56. Kurata K (1993) Premotor cortex activity of monkey: set- and movement-related activity reflecting amplitude and direction of wrist movements. J Neurophysiol 9:187–200Google Scholar
  57. Lacquaniti F, Terzuolo CA, Viviani P (1983) The law relating kinematic and figural aspects of drawing movements. Acta Psychol 54:115–130Google Scholar
  58. Lacquaniti F, Terzuolo CA, Viviani P (1984) Global metric properties and preparatory processes in drawing movements. In: Kornblum S, Requin J (eds) Preparatory states and processes. Erlbaum, Hillsdale, pp 357–370Google Scholar
  59. Majsak MJ, Kaminski TR, Gentile AM, Flanagan JR (1998) The reaching movement of patients with Parkinson’s disease under self-determined maximal speed and visually cued conditions. Brain 121:755–766PubMedGoogle Scholar
  60. Marsden CD (1982) The mysterious motor function of the basal ganglia: the Robert Wartenberg lecture. Neurology 32:514–539PubMedGoogle Scholar
  61. Mazzoni P, Hristova A, Krakauer JW (2007) Why don’t we move faster? Parkinson’s disease, movement vigor, and implicit motivation. J Neurosci 27:7105–7116PubMedGoogle Scholar
  62. McLennan JE, Nakano K, Tyler HR, Schwab RS (1972) Micrographia in Parkinson’s disease. J Neurol Sci 15:141–152PubMedGoogle Scholar
  63. Meunier S, Pol S, Houeto JL, Vidailhet M (2000) Abnormal reciprocal inhibition between antagonist muscles in Parkinson’s disease. Brain 123:1017–1026PubMedGoogle Scholar
  64. Michel F (1971) Experimental study of the graphic gesture (Article in French). Neuropsychologia 9:1–13PubMedGoogle Scholar
  65. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425PubMedGoogle Scholar
  66. Mink JW, Thach WT (1991a) Basal ganglia motor control: I. Nonexclusive relation of pallidal discharge to five movement modes. J Neurophysiol 65:273–300PubMedGoogle Scholar
  67. Mink JW, Thach WT (1991b) Basal ganglia motor control: II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. J Neurophysiol 65:301–329PubMedGoogle Scholar
  68. Mink JW, Thach WT (1993) Basal ganglia motor control: III. Pallidal ablation: normal reaction time, muscle cocontraction, and slow movement. J Neurophysiol 65:330–351Google Scholar
  69. Moore AP (1987) Impaired sensorimotor integration in parkinsonism and dyskinesia: a role for corollary discharges? J Neurol Neurosurg Psychiatry 50:544–552PubMedGoogle Scholar
  70. Moore AP (1989) Vibration-induced illusions of movement are normal in Parkinson’s disease: implications for the mechanism of the movement disorders. In: Crossman AR, Sambrook MA (eds) Neural mechanisms in disorders of movement. John Libbey, London, pp 307–311Google Scholar
  71. Moran DW, Schwartz AB (1999) Motor cortical representation of speed and direction during reaching. J Neurophysiol 82:2676–2692PubMedGoogle Scholar
  72. Morris ME, Huxham F, McGinley J, Dodd K, Iansek R (2001) The biomechanics and motor control of gait in Parkinson disease. Clin Biomech 16:459–470Google Scholar
  73. Morris ME, Iansek R, Matyas TA, Summers JJ (1994) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117:1169–1181PubMedGoogle Scholar
  74. Munro-Davies LE, Winter J, Aziz TZ, Stein JF (1999) The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp Brain Res 129:511–517PubMedGoogle Scholar
  75. Ostry DJ, Cooke JD, Munhall KG (1987) Velocity curves of human arm and speech movements. Exp Brain Res 68:37–46PubMedGoogle Scholar
  76. Pahapill PA, Lozano AS (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain 123:1767–1783PubMedGoogle Scholar
  77. Papoulis A (1965) Probability, random variables and stochastic processes. McGraw-Hill, New YorkGoogle Scholar
  78. Pascual-Leone A, Valls-Solé J, Brasil-Neto JP, Cohen LG, Hallett M (1994) Akinesia in Parkinson’s disease. I. Shortening of simple reaction time with focal, single-pulse transcranial magnetic stimulation. Neurology 44:884–891PubMedGoogle Scholar
  79. Pellizzer G (1997) Transformation of the intended direction of movement during motor trajectories. Neuroreport 8:3447–3452PubMedGoogle Scholar
  80. Pfann KD, Buchman AS, Comella CL, Corcos DM (2001) Control of movement distance in Parkinson’s disease. Mov Disord 16:1048–1065PubMedGoogle Scholar
  81. Pine ZM, Krakauer JW, Gordon J, Ghez C (1996) Learning of scaling factors and reference axes for reaching movements. Neuroreport 7:2357–2361PubMedGoogle Scholar
  82. Riehle A, Requin J (1989) Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. J Neurophysiol 61:534–549PubMedGoogle Scholar
  83. Schneider JS, Diamond SG, Markham CH (1987) Parkinson’s disease: sensory and motor problems in arms and hands. Neurology 37:951–956PubMedGoogle Scholar
  84. Schnider A, Gutbrod K, Hess CW (1995) Motion imagery in Parkinson’s disease. Brain 118:485–493PubMedGoogle Scholar
  85. Schwab RS, Chafetz ME, Walker S (1954) Control of two simultaneous voluntary motor acts in normals and parkinsonism. Arch Neurol 72:591–598Google Scholar
  86. Schwartz AB, Georgopoulos AP (1987) Relations between the amplitude of 2-dimensional arm movements and single cell discharge in primate motor cortex (Abstract). Abstr Soc Neurosci 13:244Google Scholar
  87. Schwartz AB (1992) Motor cortical activity during drawing movements: single-unit activity during sinusoid tracing. J Neurophysiol 68:528–541PubMedGoogle Scholar
  88. Schwartz AB (1994) Direct cortical representation of drawing. Science 265:540–542PubMedGoogle Scholar
  89. Schwartz AB, Moran DW (2000) Arm trajectory and representation of movement processing in motor cortical activity. Eur J Neurosci 12:1851–1856PubMedGoogle Scholar
  90. Sheridan MR, Flowers KA, Hurrell J (1987) Programming and execution of movement in Parkinson’s disease. Brain 110:1247–1271PubMedGoogle Scholar
  91. Simonetta-Moreau M, Meunier S, Vidailhet M, Pol S, Galitzky M, Rascol O (2002) Transmission of group II heteronymous pathways is enhanced in rigid lower limb of de novo patients with Parkinson’s disease 125: 2125–2133Google Scholar
  92. Stebbins GT, Goetz CG (1998) Factor structure of the unified Parkinson’s disease rating scale: motor examination scale. Mov Dis 13:633–636Google Scholar
  93. Teasdale N, Phillips JG, Stelmach GE (1990) Temporal movement control in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:862–868PubMedGoogle Scholar
  94. Turner RS, Anderson ME (1997) Pallidal discharge related to the kinematics of reaching movements in two dimensions. J Neurophysiol 77:1051–1074PubMedGoogle Scholar
  95. Turner RS, Grafton ST, Votaw JR, DeLong MR, Hoffman JM (1998) Motor subcircuits mediating the control of movement velocity: a PET study. J Neurophysiol 80:2162–2176PubMedGoogle Scholar
  96. Van Gemmert AWA, Teulings H-L, Contrrras-Vidal JL, Stelmach GE (1999) Parkinson’s disease and the control of size and speed in handwriting. Neuropsychologia 37:685–694PubMedGoogle Scholar
  97. Van Gemmert AWA, Adler CH, Stelmach GE (2003) Parkinson’s disease patients undershoot target size in handwriting and similar tasks. J Neurol Neurosurg Psychiatry 74:1502–1508PubMedGoogle Scholar
  98. Vindras P, Viviani P (1998) Frames of reference and control parameters in visuo-manual pointing. J Exp Psychol Hum Percept Perform 24:569–591PubMedGoogle Scholar
  99. Vindras P, Viviani P (2002) Altering the visuomotor gain: evidence that motor plans deal with vector quantities. Exp Brain Res 147:280–295PubMedGoogle Scholar
  100. Vingerhoets FJ, Schulzer M, Calne DB, Snow BJ (1997) Which clinical sign of Parkinson’s disease best reflects the nigrostriatal lesion? Ann Neurol 41:58–64PubMedGoogle Scholar
  101. Vinter A, Gras P (1998) Spatial features of angular drawing movements in Parkinson’s disease patients. Acta Psychol 100:177–193Google Scholar
  102. Viviani P, Terzuolo CA (1980) Space–time invariance in learned motor skills. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior. North-Holland, Amsterdam, pp 525–533Google Scholar
  103. Viviani P, Terzuolo CA (1982) Trajectory determines movement dynamics. Neuroscience 7:431–437PubMedGoogle Scholar
  104. Viviani P, Terzuolo CA (1983) The organization of movement in handwriting and typing. In: Butterworth B (ed) Language production, vol II. Development, writing and other language processes. Academic Press, New York, pp 103–146Google Scholar
  105. Viviani P, McCollum G (1983) The relation between linear extent and velocity in drawing movements. Neuroscience 10:211–218PubMedGoogle Scholar
  106. Viviani P, Cenzato M (1985) Segmentation and coupling in complex movements. J Exp Psychol Hum Percept Perform 11:828–845PubMedGoogle Scholar
  107. Viviani P (1986) Do units of motor action really exist? In: Heuer H, Fromm C (eds) Generation and modulation of action patterns. Springer, Berlin, pp 201–216Google Scholar
  108. Viviani P, Zanone PG (1988) Spontaneous covariations of movement parameters in 5- to 7-years old boys. J Mot Behav 20:205–216Google Scholar
  109. Viviani P, Flash T (1995) Minimum-jerk, Two-thirds Power Law, and isochrony: converging approaches to movement planning. J Exp Psychol Hum Percept Perform 21:32–53PubMedGoogle Scholar
  110. Viviani P, Schneider R (1991) A developmental study of the relationship between geometry and kinematics in drawing movements. J Exp Psychol Hum Percept Perform 17:198–218PubMedGoogle Scholar
  111. Viviani P, Stucchi N (1992) Biological movements look uniform: evidence of motor-perceptual interactions. J Exp Psychol Hum Percept Perform 18:603–623PubMedGoogle Scholar
  112. Warabi T, Noda H, Yanagisawa N, Tashiro K, Shindo R (1986) Changes in sensorimotor function associated with the degree of bradykinesia in Parkinson’s disease. Brain 109:1209–1224PubMedGoogle Scholar
  113. Weiss P, Stelmach GE, Hefter H (1997) Programming of a movement sequence in Parkinson’s disease. Brain 120:91–102PubMedGoogle Scholar
  114. Wichmann T, DeLong MR (1996) Functional and pathophysiological models of the basal ganglia. Curr Opin Neurobiol 6:751–758PubMedGoogle Scholar
  115. Wiesendanger M (1998) Bernstein’s principle of equal simplicity and related concepts. In: Latash ML (ed) Bernstein’s tradition in movement studies, vol 1. Human Kinetics, Champaign, pp 105–125Google Scholar
  116. Zia S, Cody F, O’Boyle D (2000) Joint position sense is impaired by Parkinson’s disease. Ann Neurol 47:218–228PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Paolo Viviani
    • 1
  • Pierre R. Burkhard
    • 2
  • Sabina Catalano Chiuvé
    • 3
  • Corrado Corradi dell’Acqua
    • 4
  • Philippe Vindras
    • 5
  1. 1.Faculty of Psychology and Educational SciencesUniversity of GenevaGenevaSwitzerland
  2. 2.Department of Neurology, Faculty of MedicineGeneva University HospitalsGenevaSwitzerland
  3. 3.Department of Neurology, Neuropsychology UnitGeneva University HospitalsGenevaSwitzerland
  4. 4.Cognitive Neuroscience SectorSISSA TriesteItaly
  5. 5.Laboratory of Neurophysiology of Perception and MovementInstitute of Cognitive Science, CNRS UMR 5229BronFrance

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