Advertisement

Hand Function pp 133-149 | Cite as

Hand Function in Parkinson’s Disease

  • Jamie R. Lukos
  • Howard Poizner
  • Jacob I. SageEmail author
Chapter

Abstract

Parkinson’s disease (PD) patients have a number of functional hand impairments. The latency and rate of isometric force generation is impaired in PD. Motor dysfunction is also related to impaired integration of sensory feedback and motor output. Moreover, PD patients exhibit sensory deficits such as decreased spatial and temporal tactile discrimination thresholds of the fingertips. Impairments of reaching and grasping are seen as patients tend to exhibit difficulty in movement initiation to a target. There are deficits in hand preshaping to object geometry. There is a lack of coordination between the timing of the reach and grasp components. Patients have an overall dependence on visual cues to control movement. They exhibit impairments in the planning of where to place their digits, resulting in suboptimal performance of object manipulation. It is hypothesized that predictive force control deficits are a result of central impairments associated with the generation and/or retrieval of sensorimotor memories for movement planning.

Clinical aspects of hand function include resting, postural or internal tremor, bradykinesia, and rigidity. Elements of the unified Parkinson’s disease rating scale (UPDRS) are the best way to measure deficits in hand function. Choreiform dyskinesias and dystonia may interfere with hand function.

Keywords

Basal Ganglion Deep Brain Stimulation Visual Feedback Grip Force Hand Function 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Supported in part by NIH grant #2 R01 NS036449 (HP).

References

  1. 1.
    Rodriguez-Oroz MC, Lage PM, Sanchez-Mut J, Lamet I, Pagonabarraga J, Toledo JB, Garcia-Garcia D, Clavero P, Samaranch L, Irurzun C, Matsubara JM, Irigoien J, Bescos E, Kulisevsky J, Perez-Tur J, Obeso JA. Homocysteine and cognitive impairment in Parkinson’s disease: a biochemical, neuroimaging, and genetic study. Mov Disord. 2009;24:1437–44.PubMedGoogle Scholar
  2. 2.
    Rivlin-Etzion M, Marmor O, Heimer G, Raz A, Nini A, Bergman H. Basal ganglia oscillations and pathophysiology of movement disorders. Curr Opin Neurobiol. 2006;16:629–37.PubMedGoogle Scholar
  3. 3.
    Brown P, Marsden CD. Bradykinesia and impairment of EEG desynchronization in Parkinson’s disease. Mov Disord. 1999;14:423–9.PubMedGoogle Scholar
  4. 4.
    Benecke R, Rothwell JC, Dick JP, Day BL, Marsden CD. Disturbance of sequential movements in patients with Parkinson’s disease. Brain. 1987;110(Pt 2):361–79.PubMedGoogle Scholar
  5. 5.
    Flowers KA. Visual “closed-loop” and “open-loop” characteristics of voluntary movement in patients with Parkinsonism and intention tremor. Brain. 1976;99:269–310.PubMedGoogle Scholar
  6. 6.
    Adamovich SV, Berkinblit MB, Hening W, Sage J, Poizner H. The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets in Parkinson’s disease. Neuroscience. 2001;104:1027–41.PubMedGoogle Scholar
  7. 7.
    Poizner H, Feldman AG, Levin MF, Berkinblit MB, Hening WA, Patel A, Adamovich SV. The timing of arm-trunk coordination is deficient and vision-dependent in Parkinson’s patients during reaching movements. Exp Brain Res. 2000;133:279–92.PubMedGoogle Scholar
  8. 8.
    Schettino LF, Adamovich SV, Hening W, Tunik E, Sage J, Poizner H. Hand preshaping in Parkinson’s disease: effects of visual feedback and medication state. Exp Brain Res. 2006;168:186–202.PubMedGoogle Scholar
  9. 9.
    Tunik E, Feldman AG, Poizner H. Dopamine replacement therapy does not restore the ability of parkinsonian patients to make rapid adjustments in motor strategies according to changing sensorimotor contexts. Parkinsonism Relat Disord. 2007;13:425–33.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Castiello U. The neuroscience of grasping. Nat Rev Neurosci. 2005;6:726–36.PubMedGoogle Scholar
  11. 11.
    Prodoehl J, Corcos DM, Vaillancourt DE. Basal ganglia mechanisms underlying precision grip force control. Neurosci Biobehav Rev. 2009;33:900–8.PubMedCentralPubMedGoogle Scholar
  12. 12.
    Clower DM, Dum RP, Strick PL. Basal ganglia and cerebellar inputs to ‘AIP’. Cereb Cortex. 2005;15:913–20.PubMedGoogle Scholar
  13. 13.
    Hoover JE, Strick PL. Multiple output channels in the basal ganglia. Science. 1993;259:819–21.PubMedGoogle Scholar
  14. 14.
    Middleton FA, Strick PL. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev. 2000;31:236–50.PubMedGoogle Scholar
  15. 15.
    Nambu A, Yoshida S, Jinnai K. Projection on the motor cortex of thalamic neurons with pallidal input in the monkey. Exp Brain Res. 1988;71:658–62.PubMedGoogle Scholar
  16. 16.
    Holsapple JW, Preston JB, Strick PL. The origin of thalamic inputs to the “hand” representation in the primary motor cortex. J Neurosci. 1991;11:2644–54.PubMedGoogle Scholar
  17. 17.
    DeLong MR, Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch Neurol. 2007;64:20–4.PubMedGoogle Scholar
  18. 18.
    Spraker MB, Yu H, Corcos DM, Vaillancourt DE. Role of individual basal ganglia nuclei in force amplitude generation. J Neurophysiol. 2007;98:821–34.PubMedCentralPubMedGoogle Scholar
  19. 19.
    Vaillancourt DE, Yu H, Mayka MA, Corcos DM. Role of the basal ganglia and frontal cortex in selecting and producing internally guided force pulses. Neuroimage. 2007;36:793–803.PubMedCentralPubMedGoogle Scholar
  20. 20.
    Stelmach GE, Worringham CJ. The preparation and production of isometric force in Parkinson’s disease. Neuropsychologia. 1988;26:93–103.PubMedGoogle Scholar
  21. 21.
    Jordan N, Sagar HJ, Cooper JA. A component analysis of the generation and release of isometric force in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1992;55:572–6.PubMedCentralPubMedGoogle Scholar
  22. 22.
    Vaillancourt DE, Slifkin AB, Newell KM. Intermittency in the visual control of force in Parkinson’s disease. Exp Brain Res. 2001;138:118–27.PubMedGoogle Scholar
  23. 23.
    Mortimer JA, Webster DD. Evidence for a quantitative association between EMG stretch responses and parkinsonian rigidity. Brain Res. 1979;162:169–73.PubMedGoogle Scholar
  24. 24.
    Rothwell JC, Obeso JA, Traub MM, Marsden CD. The behaviour of the long-latency stretch reflex in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1983;46:35–44.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Cantello R, Tarletti R, Varrasi C, Cecchin M, Monaco F. Cortical inhibition in Parkinson’s disease: new insights from early, untreated patients. Neuroscience. 2007;150:64–71.PubMedGoogle Scholar
  26. 26.
    Dietz V, Hillesheimer W, Freund HJ. Correlation between tremor, voluntary contraction, and firing pattern of motor units in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1974;37:927–37.PubMedCentralPubMedGoogle Scholar
  27. 27.
    Milner-Brown HS, Fisher MA, Weiner WJ. Electrical properties of motor units in Parkinsonism and a possible relationship with bradykinesia. J Neurol Neurosurg Psychiatry. 1979;42:35–41.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Berardelli A, Rothwell JC, Thompson PD, Hallett M. Pathophysiology of bradykinesia in Parkinson’s disease. Brain. 2001;124:2131–46.PubMedGoogle Scholar
  29. 29.
    Sainburg RL, Ghilardi MF, Poizner H, Ghez C. Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol. 1995;73:820–35.PubMedGoogle Scholar
  30. 30.
    Sathian K, Zangaladze A, Green J, Vitek JL, DeLong MR. Tactile spatial acuity and roughness discrimination: impairments due to aging and Parkinson’s disease. Neurology. 1997;49:168–77.PubMedGoogle Scholar
  31. 31.
    Artieda J, Pastor MA, Lacruz F, Obeso JA. Temporal discrimination is abnormal in Parkinson’s disease. Brain. 1992;115(Pt 1):199–210.PubMedGoogle Scholar
  32. 32.
    Maschke M, Gomez CM, Tuite PJ, Konczak J. Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. Brain. 2003;126:2312–22.PubMedGoogle Scholar
  33. 33.
    Konczak J, Li KY, Tuite PJ, Poizner H. Haptic perception of object curvature in Parkinson’s disease. PLoS One. 2008;3:e2625.PubMedCentralPubMedGoogle Scholar
  34. 34.
    Konczak J, Corcos DM, Horak F, Poizner H, Shapiro M, Tuite P, Volkmann J, Maschke M. Proprioception and motor control in Parkinson’s disease. J Mot Behav. 2009;41:543–52.PubMedGoogle Scholar
  35. 35.
    Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord. 2003;18:231–40.PubMedGoogle Scholar
  36. 36.
    Seiss E, Praamstra P, Hesse CW, Rickards H. Proprioceptive sensory function in Parkinson’s disease and Huntington’s disease: evidence from proprioception-related EEG potentials. Exp Brain Res. 2003;148:308–19.PubMedGoogle Scholar
  37. 37.
    Lee MS, Lyoo CH, Lee MJ, Sim J, Cho H, Choi YH. Impaired finger dexterity in patients with Parkinson’s disease correlates with discriminative cutaneous sensory dysfunction. Mov Disord. 2010;25:2531–5.PubMedGoogle Scholar
  38. 38.
    Nakamura R, Nagasaki H, Narabayashi H. Disturbances of rhythm formation in patients with Parkinson’s disease: part I. Characteristics of tapping response to the periodic signals. Percept Mot Skills. 1978;46:63–75.PubMedGoogle Scholar
  39. 39.
    Stegemoller EL, Simuni T, MacKinnon C. Effect of movement frequency on repetitive finger movements in patients with Parkinson’s disease. Mov Disord. 2009;24:1162–9.PubMedCentralPubMedGoogle Scholar
  40. 40.
    Stelmach GE, Garcia-Colera A, Martin ZE. Force transition control within a movement sequence in Parkinson’s disease. J Neurol. 1989;236:406–10.PubMedGoogle Scholar
  41. 41.
    Frischer M. Voluntary vs autonomous control of repetitive finger tapping in a patient with Parkinson’s disease. Neuropsychologia. 1989;27:1261–6.PubMedGoogle Scholar
  42. 42.
    O’Boyle DJ, Freeman JS, Cody FW. The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson’s disease. Brain. 1996;119(Pt 1):51–70.PubMedGoogle Scholar
  43. 43.
    Quencer K, Okun MS, Crucian G, Fernandez HH, Skidmore F, Heilman KM. Limb-kinetic apraxia in Parkinson disease. Neurology. 2007;68:150–1.PubMedGoogle Scholar
  44. 44.
    Gebhardt A, Vanbellingen T, Baronti F, Kersten B, Bohlhalter S. Poor dopaminergic response of impaired dexterity in Parkinson’s disease: bradykinesia or limb kinetic apraxia? Mov Disord. 2008;23:1701–6.PubMedGoogle Scholar
  45. 45.
    Stewart KC, Fernandez HH, Okun MS, Alberts JL, Malaty IA, Rodriguez RL, Hass CJ. Effects of dopaminergic medication on objective tasks of deftness, bradykinesia and force control. J Neurol. 2009;256:2030–5.PubMedGoogle Scholar
  46. 46.
    Stegemoller EL, Allen DP, Simuni T, MacKinnon CD. Rate-dependent impairments in repetitive finger movements in patients with Parkinson’s disease are not due to peripheral fatigue. Neurosci Lett. 2010;482:1–6.PubMedCentralPubMedGoogle Scholar
  47. 47.
    Stelmach GE, Worringham CJ, Strand EA. Movement preparation in Parkinson’s disease. The use of advance information. Brain. 1986;109(Pt 6):1179–94.PubMedGoogle Scholar
  48. 48.
    Jahanshahi M, Brown RG, Marsden CD. Simple and choice reaction time and the use of advance information for motor preparation in Parkinson’s disease. Brain. 1992;115(Pt 2):539–64.PubMedGoogle Scholar
  49. 49.
    Desmurget M, Grafton ST, Vindras P, Grea H, Turner RS. Basal ganglia network mediates the control of movement amplitude. Exp Brain Res. 2003;153:197–209.PubMedGoogle Scholar
  50. 50.
    Santello M, Soechting JF. Gradual molding of the hand to object contours. J Neurophysiol. 1998;79:1307–20.PubMedGoogle Scholar
  51. 51.
    Winges SA, Weber DJ, Santello M. The role of vision on hand preshaping during reach to grasp. Exp Brain Res. 2003;152:489–98.PubMedGoogle Scholar
  52. 52.
    Schettino LF, Rajaraman V, Jack D, Adamovich SV, Sage J, Poizner H. Deficits in the evolution of hand preshaping in Parkinson’s disease. Neuropsychologia. 2004;42:82–94.PubMedGoogle Scholar
  53. 53.
    Ansuini C, Begliomini C, Ferrari T, Castiello U. Testing the effects of end-goal during reach-to-grasp movements in Parkinson’s disease. Brain Cogn. 2010;74:169–77.PubMedGoogle Scholar
  54. 54.
    Jackson SR, Jackson GM, Harrison J, Henderson L, Kennard C. The internal control of action and Parkinson’s disease: a kinematic analysis of visually-guided and memory-guided prehension movements. Exp Brain Res. 1995;105:147–62.PubMedGoogle Scholar
  55. 55.
    Alberts JL, Tresilian JR, Stelmach GE. The co-ordination and phasing of a bilateral prehension task. The influence of Parkinson’s disease. Brain. 1998;121(Pt 4):725–42.PubMedGoogle Scholar
  56. 56.
    Rand MK, Smiley-Oyen AL, Shimansky YP, Bloedel JR, Stelmach GE. Control of aperture closure during reach-to-grasp movements in Parkinson’s disease. Exp Brain Res. 1996;168:131–42.Google Scholar
  57. 57.
    Jackson GM, Jackson SR, Hindle JV. The control of bimanual reach-to-grasp movements in hemiparkinsonian patients. Exp Brain Res. 2000;132:390–8.PubMedGoogle Scholar
  58. 58.
    Negrotti A, Secchi C, Gentilucci M. Effects of disease progression and L-dopa therapy on the control of reaching-grasping in Parkinson’s disease. Neuropsychologia. 2005;43:450–9.PubMedGoogle Scholar
  59. 59.
    Castiello U, Bennett KM, Scarpa M. The reach to grasp movement of Parkinson’s disease subjects. In: Bennett KM, Castiello U, editors. Insights into the reach to grasp movement. Amsterdam, The Netherlands: Elsevier Science B.V.; 1994. p. 215–37.Google Scholar
  60. 60.
    Flowers K. Lack of prediction in the motor behaviour of Parkinsonism. Brain. 1978;101:35–52.PubMedGoogle Scholar
  61. 61.
    Stern Y, Mayeux R, Rosen J, Ilson J. Perceptual motor dysfunction in Parkinson’s disease: a deficit in sequential and predictive voluntary movement. J Neurol Neurosurg Psychiatry. 1983;46:145–51.PubMedCentralPubMedGoogle Scholar
  62. 62.
    Ansuini C, Giosa L, Turella L, Altoe G, Castiello U. An object for an action, the same object for other actions: effects on hand shaping. Exp Brain Res. 2008;185:111–9.PubMedGoogle Scholar
  63. 63.
    Castiello U, Bennett K, Bonfiglioli C, Lim S, Peppard RF. The reach-to-grasp movement in Parkinson’s disease: response to a simultaneous perturbation of object position and object size. Exp Brain Res. 1999;125:453–62.PubMedGoogle Scholar
  64. 64.
    Rand MK, Lemay M, Squire LM, Shimansky YP, Stelmach GE. Control of aperture closure initiation during reach-to-grasp movements under manipulations of visual feedback and trunk involvement in Parkinson’s disease. Exp Brain Res. 2010;201:509–25.PubMedGoogle Scholar
  65. 65.
    Lukos J, Ansuini C, Santello M. Choice of contact points during multidigit grasping: effect of predictability of object center of mass location. J Neurosci. 2007;27:3894–903.PubMedGoogle Scholar
  66. 66.
    Lukos JR, Ansuini C, Santello M. Anticipatory control of grasping: independence of sensorimotor memories for kinematics and kinetics. J Neurosci. 2008;28:12765–74.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Lukos JR, Lee D, Poizner H, Santello M. Anticipatory modulation of digit placement for grasp control is affected by Parkinson’s disease. PLoS One. 2010;5:e9184.PubMedCentralPubMedGoogle Scholar
  68. 68.
    Ingvarsson PE, Gordon AM, Forssberg H. Coordination of manipulative forces in Parkinson’s disease. Exp Neurol. 1997;145:489–501.PubMedGoogle Scholar
  69. 69.
    Fellows SJ, Noth J, Schwarz M. Precision grip and Parkinson’s disease. Brain. 1998;121(Pt 9):1771–84.PubMedGoogle Scholar
  70. 70.
    Nowak DA, Hermsdorfer J. Coordination of grip and load forces during vertical point-to-point movements with a grasped object in Parkinson’s disease. Behav Neurosci. 2002;116:837–50.PubMedGoogle Scholar
  71. 71.
    Muratori LM, McIsaac TL, Gordon AM, Santello M. Impaired anticipatory control of force sharing patterns during whole-hand grasping in Parkinson’s disease. Exp Brain Res. 2008;185:41–52.PubMedGoogle Scholar
  72. 72.
    Santello M, Muratori L, Gordon AM. Control of multidigit grasping in Parkinson’s disease: effect of object property predictability. Exp Neurol. 2004;187:517–28.PubMedGoogle Scholar
  73. 73.
    Gordon AM, Ingvarsson PE, Forssberg H. Anticipatory control of manipulative forces in Parkinson’s disease. Exp Neurol. 1997;145:477–88.PubMedGoogle Scholar
  74. 74.
    Nowak DA, Hermsdorfer J. Predictive and reactive control of grasping forces: on the role of the basal ganglia and sensory feedback. Exp Brain Res. 2006;173:650–60.PubMedGoogle Scholar
  75. 75.
    Nowak DA, Tisch S, Hariz M, Limousin P, Topka H, Rothwell JC. Sensory timing cues improve akinesia of grasping movements in Parkinson’s disease: a comparison to the effects of subthalamic nucleus stimulation. Mov Disord. 2006;21:166–72.PubMedGoogle Scholar
  76. 76.
    Wenzelburger R, Zhang BR, Pohle S, Klebe S, Lorenz D, Herzog J, Wilms H, Deuschl G, Krack P. Force overflow and levodopa-induced dyskinesias in Parkinson’s disease. Brain. 2002;125:871–9.PubMedGoogle Scholar
  77. 77.
    Johansson RS. Somatosensory signals and sensorimotor transformations in reactive control. In: Franzen O et al., editors. Somesthesis and the neurobiology of the somatosensory cortex. Switzerland: Birkhäuser Verlag Basel; 1996. p. 271–82.Google Scholar
  78. 78.
    Westling G, Johansson RS. Factors influencing the force control during precision grip. Exp Brain Res. 1984;53:277–84.PubMedGoogle Scholar
  79. 79.
    Rearick MP, Stelmach GE, Leis B, Santello M. Coordination and control of forces during multifingered grasping in Parkinson’s disease. Exp Neurol. 2002;177:428–42.PubMedGoogle Scholar
  80. 80.
    Boecker H, Lee A, Muhlau M, Ceballos-Baumann A, Ritzl A, Spilker ME, Marquart C, Hermsdorfer J. Force level independent representations of predictive grip force-load force coupling: a PET activation study. Neuroimage. 2005;25:243–52.PubMedGoogle Scholar
  81. 81.
    Pope P, Wing AM, Praamstra P, Miall RC. Force related activations in rhythmic sequence production. Neuroimage. 2005;27:909–18.PubMedGoogle Scholar
  82. 82.
    Vaillancourt DE, Mayka MA, Thulborn KR, Corcos DM. Subthalamic nucleus and internal globus pallidus scale with the rate of change of force production in humans. Neuroimage. 2004;23:175–86.PubMedGoogle Scholar
  83. 83.
    Prodoehl J, Yu H, Wasson P, Corcos DM, Vaillancourt DE. Effects of visual and auditory feedback on sensorimotor circuits in the basal ganglia. J Neurophysiol. 2008;99:3042–51.PubMedGoogle Scholar
  84. 84.
    Ehrsson HH, Fagergren A, Johansson RS, Forssberg H. Evidence for the involvement of the posterior parietal cortex in coordination of fingertip forces for grasp stability in manipulation. J Neurophysiol. 2003;90:2978–86.PubMedGoogle Scholar
  85. 85.
    Samuel M, Ceballos-Baumann AO, Blin J, Uema T, Boecker H, Passingham RE, Brooks DJ. Evidence for lateral premotor and parietal overactivity in Parkinson’s disease during sequential and bimanual movements. A PET study. Brain. 1997;120(Pt 6):963–76.PubMedGoogle Scholar
  86. 86.
    Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, Bozzao L, Berry I, Montastruc JL, Chollet F, Rascol O. Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain. 2000;123(Pt 2):394–403.PubMedGoogle Scholar
  87. 87.
    Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, Conrad B, Ceballos-Baumann AO. Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain. 2001;124:558–70.PubMedGoogle Scholar
  88. 88.
    Escola L, Michelet T, Douillard G, Guehl D, Bioulac B, Burbaud P. Disruption of the proprioceptive mapping in the medial wall of parkinsonian monkeys. Ann Neurol. 2002;52:581–7.PubMedGoogle Scholar
  89. 89.
    Rowe J, Stephan KE, Friston K, Frackowiak R, Lees A, Passingham R. Attention to action in Parkinson’s disease: impaired effective connectivity among frontal cortical regions. Brain. 2002;125:276–89.PubMedGoogle Scholar
  90. 90.
    Buhmann C, Glauche V, Sturenburg HJ, Oechsner M, Weiller C, Buchel C. Pharmacologically modulated fMRI—cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain. 2003;126:451–61.PubMedGoogle Scholar
  91. 91.
    Turner RS, Grafton ST, McIntosh AR, DeLong MR, Hoffman JM. The functional anatomy of parkinsonian bradykinesia. Neuroimage. 2003;19:163–79.PubMedGoogle Scholar
  92. 92.
    Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ. Impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Ann Neurol. 1992;32:151–61.PubMedGoogle Scholar
  93. 93.
    Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ. Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain. 1995;118(Pt 4):913–33.PubMedGoogle Scholar
  94. 94.
    Grafton ST. Contributions of functional imaging to understanding parkinsonian symptoms. Curr Opin Neurobiol. 2004;14:715–9.PubMedGoogle Scholar
  95. 95.
    Catalan MJ, Ishii K, Honda M, Samii A, Hallett M. A PET study of sequential finger movements of varying length in patients with Parkinson’s disease. Brain. 1999;122(Pt 3):483–95.PubMedGoogle Scholar
  96. 96.
    Glickstein M, Stein J. Paradoxical movement in Parkinson’s disease. Trends Neurosci. 1991;14:480–2.PubMedGoogle Scholar
  97. 97.
    Pessiglione M, Guehl D, Rolland AS, Francois C, Hirsch EC, Feger J, Tremblay L. Thalamic neuronal activity in dopamine-depleted primates: evidence for a loss of functional segregation within basal ganglia circuits. J Neurosci. 2005;25:1523–31.PubMedGoogle Scholar
  98. 98.
    Raz A, Frechter-Mazar V, Feingold A, Abeles M, Vaadia E, Bergman H. Activity of pallidal and striatal tonically active neurons is correlated in mptp-treated monkeys but not in normal monkeys. J Neurosci. 2001;21:RC128.PubMedGoogle Scholar
  99. 99.
    Raz A, Vaadia E, Bergman H. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J Neurosci. 2000;20:8559–71.PubMedGoogle Scholar
  100. 100.
    Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 2002;25:525–31.PubMedGoogle Scholar
  101. 101.
    Gatev P, Darbin O, Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord. 2006;21:1566–77.PubMedGoogle Scholar
  102. 102.
    Goldberg JA, Rokni U, Boraud T, Vaadia E, Bergman H. Spike synchronization in the cortex/basal-ganglia networks of parkinsonian primates reflects global dynamics of the local field potentials. J Neurosci. 2004;24:6003–10.PubMedGoogle Scholar
  103. 103.
    Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, Vaadia E. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 1998;21:32–8.PubMedGoogle Scholar
  104. 104.
    Bar-Gad I, Bergman H. Stepping out of the box: information processing in the neural networks of the basal ganglia. Curr Opin Neurobiol. 2001;11:689–95.PubMedGoogle Scholar
  105. 105.
    Soikkeli R, Partanen J, Soininen H, Paakkonen A, Riekkinen Sr P. Slowing of EEG in Parkinson’s disease. Electroencephalogr Clin Neurophysiol. 1991;79:159–65.PubMedGoogle Scholar
  106. 106.
    Hammond C, Bergman H, Brown P. Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci. 2007;30:357–64.PubMedGoogle Scholar
  107. 107.
    Filion M, Tremblay L. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced Parkinsonism. Brain Res. 1991;547:142–51.PubMedGoogle Scholar
  108. 108.
    Bergman H, Wichmann T, Karmon B, DeLong MR. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of Parkinsonism. J Neurophysiol. 1994;72:507–20.PubMedGoogle Scholar
  109. 109.
    Nini A, Feingold A, Slovin H, Bergman H. Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of Parkinsonism. J Neurophysiol. 1995;74:1800–5.PubMedGoogle Scholar
  110. 110.
    Hutchison WD, Lozano AM, Tasker RR, Lang AE, Dostrovsky JO. Identification and characterization of neurons with tremor-frequency activity in human globus pallidus. Exp Brain Res. 1997;113:557–63.PubMedGoogle Scholar
  111. 111.
    Merello M, Balej J, Delfino M, Cammarota A, Betti O, Leiguarda R. Apomorphine induces changes in GPi spontaneous outflow in patients with Parkinson’s disease. Mov Disord. 1999;14:45–9.PubMedGoogle Scholar
  112. 112.
    Levy R, Hutchison WD, Lozano AM, Dostrovsky JO. High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci. 2000;20:7766–75.PubMedGoogle Scholar
  113. 113.
    Swann N, Poizner H, Houser M, Gould S, Greenhouse I, Caj W, Strunk J, George J, Aron A. Deep brain stimulation of the subthalamic nucleus alters the cortical profile of response inhibition in the beta frequency band: a scalp EEG study in Parkinson’s disease. J Neurosci. 2011;31:5721–9.PubMedCentralPubMedGoogle Scholar
  114. 114.
    Brown P, Eusebio A. Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Mov Disord. 2008;23:12–20. quiz 158.PubMedGoogle Scholar
  115. 115.
    Flink TA, Stelmach GE. Prehension characteristics in Parkinson’s disease patients. In: Nowak DA, Hermsdorfer J, editors. Sensorimotor control of grasping. Cambridge: Cambridge University Press; 2009. p. 311–25.Google Scholar
  116. 116.
    Klockgether T, Dichgans J. Visual control of arm movement in Parkinson’s disease. Mov Disord. 1994;9:48–56.PubMedGoogle Scholar
  117. 117.
    Deuschl G, Fogel W, Hahne M, Kupsch A, Muller D, Oechsner M, Sommer U, Ulm G, Vogt T, Volkmann J. Deep-brain stimulation for Parkinson’s disease. J Neurol. 2002;249 Suppl 3:III/36–9.Google Scholar
  118. 118.
    Deuschl G, Wenzelburger R, Kopper F, Volkmann J. Deep brain stimulation of the subthalamic nucleus for Parkinson’s disease: a therapy approaching evidence-based standards. J Neurol. 2003;250 Suppl 1:I43–6.PubMedGoogle Scholar
  119. 119.
    Ashkan K, Wallace B, Bell BA, Benabid AL. Deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 1993–2003: where are we 10 years on? Br J Neurosurg. 2004;18:19–34.PubMedGoogle Scholar
  120. 120.
    Volkmann J. Deep brain stimulation for the treatment of Parkinson’s disease. J Clin Neurophysiol. 2004;21:6–17.PubMedGoogle Scholar
  121. 121.
    Pahwa R, Lyons KE, Wilkinson SB, Simpson Jr RK, Ondo WG, Tarsy D, Norregaard T, Hubble JP, Smith DA, Hauser RA, Jankovic J. Long-term evaluation of deep brain stimulation of the thalamus. J Neurosurg. 2006;104:506–12.PubMedGoogle Scholar
  122. 122.
    Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schafer H, Botzel K, Daniels C, Deutschlander A, Dillmann U, Eisner W, Gruber D, Hamel W, Herzog J, Hilker R, Klebe S, Kloss M, Koy J, Krause M, Kupsch A, Lorenz D, Lorenzl S, Mehdorn HM, Moringlane JR, Oertel W, Pinsker MO, Reichmann H, Reuss A, Schneider GH, Schnitzler A, Steude U, Sturm V, Timmermann L, Tronnier V, Trottenberg T, Wojtecki L, Wolf E, Poewe W, Voges J. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2006;355:896–908.PubMedGoogle Scholar
  123. 123.
    Boucai L, Cerquetti D, Merello M. Functional surgery for Parkinson’s disease treatment: a structured analysis of a decade of published literature. Br J Neurosurg. 2004;18:213–22.PubMedGoogle Scholar
  124. 124.
    Schettino LF, Van Erp E, Hening W, Lessig S, Song D, Barba D, Poizner H. Deep brain stimulation of the subthalamic nucleus facilitates coordination of hand preshaping in Parkinson’s disease. Int J Neurosci. 2009;119:1905–24.PubMedGoogle Scholar
  125. 125.
    Wenzelburger R, Zhang BR, Poepping M, Schrader B, Muller D, Kopper F, Fietzek U, Mehdorn HM, Deuschl G, Krack P. Dyskinesias and grip control in Parkinson’s disease are normalized by chronic stimulation of the subthalamic nucleus. Ann Neurol. 2002;52:240–3.PubMedGoogle Scholar
  126. 126.
    Nowak DA, Topka H, Tisch S, Hariz M, Limousin P, Rothwell JC. The beneficial effects of subthalamic nucleus stimulation on manipulative finger force control in Parkinson’s disease. Exp Neurol. 2005;193:427–36.PubMedGoogle Scholar
  127. 127.
    Fellows SJ, Kronenburger M, Allert N, Coenen VA, Fromm C, Noth J, Weiss PH. The effect of subthalamic nucleus deep brain stimulation on precision grip abnormalities in Parkinson’s disease. Parkinsonism Relat Disord. 2006;12:149–54.PubMedGoogle Scholar
  128. 128.
    Fregni F, Pascual-Leone A. Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol. 2007;3:383–93.PubMedGoogle Scholar
  129. 129.
    Fregni F, Simon DK, Wu A, Pascual-Leone A. Non-invasive brain stimulation for Parkinson’s disease: a systematic review and meta-analysis of the literature. J Neurol Neurosurg Psychiatry. 2005;76:1614–23.PubMedCentralPubMedGoogle Scholar
  130. 130.
    Lomarev MP, Kanchana S, Bara-Jimenez W, Iyer M, Wassermann EM, Hallett M. Placebo-controlled study of rTMS for the treatment of Parkinson’s disease. Mov Disord. 2006;21:325–31.PubMedGoogle Scholar
  131. 131.
    Gruner U, Eggers C, Ameli M, Sarfeld AS, Fink GR, Nowak DA. 1 Hz rTMS preconditioned by tDCS over the primary motor cortex in Parkinson’s disease: effects on bradykinesia of arm and hand. J Neural Transm. 2010;117:207–16.PubMedGoogle Scholar
  132. 132.
    Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;117(Pt 4):847–58.PubMedGoogle Scholar
  133. 133.
    Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48:1398–403.PubMedGoogle Scholar
  134. 134.
    Duvoisin RD. Parkinson’s disease, a guide for patient and family. New York: Raven; 1984.Google Scholar
  135. 135.
    Duvoisin RC, Sage JI. The spectrum of Parkinson’s disease. In: Chokroverty S, editor. Movement disorders. Yorba Linda, CA: PMA; 1990. p. 159–77.Google Scholar
  136. 136.
    Sage JI, Mark MH, editors. Practical neurology of the elderly, vol. 2. New York: Marcel Dekker; 1996.Google Scholar
  137. 137.
    Sage JI. Fluctuations of nonmotor symptoms. In: Factor SA, Weiner WJ, editors. Parkinson’s disease: diagnosis and clinical management. New York: Demos Medical Publishing; 2002. p. 455–63.Google Scholar
  138. 138.
    Fahn S, Elton RL, Members of the UPDRS Development Committee. Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M, editors. Recent developments in Parkinson’s disease, vol. II. Florham Park, NJ: Macmillan Healthcare Information; 1987. p. 153–63. 293–304.Google Scholar
  139. 139.
    Sage JI. Pain in Parkinson’s disease. In: Reich SG, editor. Current treatment options in neurology, vol. 6. Philadelphia, PA. Current Science, Inc; 2004. p. 191–200.Google Scholar
  140. 140.
    McHale DM, Sage JI, Sonsalla PK, Vitagliano D. Complex dystonia of Parkinson’s disease; clinical features and relation to plasma levodopa profile. Clin Neuropharmacol. 1990;13:164–70.PubMedGoogle Scholar
  141. 141.
    Hillen ME, Sage JI. Nonmotor fluctuations in patients with Parkinson’s disease. Neurology. 1996;47:1180–3.PubMedGoogle Scholar
  142. 142.
    Sage JI, Kortis HI, Sommer W. Evidence for the role of spinal cord systems in Parkinson’s disease associated pain. Clin Neuropharmacol. 1990;13:171–4.PubMedGoogle Scholar
  143. 143.
    Sage JI, Mark MH. Basic mechanisms of motor fluctuations. Neurology. 1994;44 Suppl 6:S10–4.PubMedGoogle Scholar
  144. 144.
    Sage JI, Mark MH, McHale DM, Sonsalla PK, Vitagliano D. Benefits of monitoring plasma levodopa in Parkinson’s disease patients with drug-induced chorea. Ann Neurol. 1991;29:623–8.PubMedGoogle Scholar
  145. 145.
    Walters A, McHale D, Sage J, Hening W, Bergen M. A blinded study of the suppressibility of involuntary movements in Huntington’s chorea, tardive dyskinesia and L-DOPA induced chorea. Clin Neuropharmacol. 1990;13:236–40.PubMedGoogle Scholar
  146. 146.
    Hammon PS, Makeig S, Poizner H, Todorov E, de Sa V. Extracting trajectories and target endpoints from human EEG during a reaching task. IEEE Signal Process. 2008;25:69–77.Google Scholar
  147. 147.
    Brandeis D, Michel CM, Koenig T, Gianotti LRR. Integration of electrical neuroimaging with other functional imaging methods. In: Michel CM et al., editors. Electrical neuroimaging. Cambridge: Cambridge University Press; 2009. p. 215–32.Google Scholar
  148. 148.
    Mulert C, Lemieux L, editors. EEG–fMRI: physiological basis, technique, and applications. Berlin: Springer; 2010.Google Scholar
  149. 149.
    Ullsperger M, Debener S, editors. Simultaneous EEG and fMRI: recording, analysis, and application. New York: Oxford University Press; 2010.Google Scholar
  150. 150.
    Wingeier B, Tcheng T, Koop MM, Hill BC, Heit G, Bronte-Stewart HM. Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson’s disease. Exp Neurol. 2006;197:244–51.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Jamie R. Lukos
    • 1
  • Howard Poizner
    • 2
  • Jacob I. Sage
    • 3
    Email author
  1. 1.Institute for Neural ComputationUniversity of California, San DiegoLa JollaUSA
  2. 2.Institute for Neural ComputationUniversity of California, San DiegoLa JollaUSA
  3. 3.Department of NeurologyRobert Wood Johnson Medical SchoolNew BrunswickUSA

Personalised recommendations