Influence of basal ganglia on upper limb locomotor synergies. Evidence from deep brain stimulation and L-DOPA treatment in Parkinson's disease

Brain

Volumn 131, Issue 12, 2008, Pages 3410-3420

  Crenna, P ^a   Carpinella, I ^b   Lopiano, L ^c   Marzegan, A ^a   Rabuffetti, M ^b   Rizzone, M ^d   Lanotte, M ^c   Ferrarin, M ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d OSPEDALE NIGUARDA CA GRANDA   (Italy)

Author keywords

Arm swing; Deep brain stimulation; Parkinson's disease; Subthalamic nucleus; Walking

Indexed keywords

DOPAMINE RECEPTOR STIMULATING AGENT; LEVODOPA;

ADULT; AGED; ARM MOVEMENT; ARTICLE; BASAL GANGLION; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; HUMAN; LOCOMOTION; PARKINSON DISEASE; PRIORITY JOURNAL; RANGE OF MOTION; SUBTHALAMIC NUCLEUS;

AGED; ARM; BASAL GANGLIA; COMBINED MODALITY THERAPY; DEEP BRAIN STIMULATION; EXERCISE TEST; GAIT DISORDERS, NEUROLOGIC; HUMANS; LEVODOPA; MIDDLE AGED; PARKINSON DISEASE; PSYCHOMOTOR PERFORMANCE; THIGH;

EID: 58149114772     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn272     Document Type: Article

References (93)

1. Allert N, Volkmann J, Dotse S, Hefter H, Sturm V, Freund HJ. Effects of bilateral pallidal or subthalamic stimulation on gait in advanced Parkinson's Disease. Mov Disord 2001; 16: 197-201.
2. Alstermark B, Isa T, Ohki Y, Saito Y. Disynaptic pyramidal excitation in forelimb motoneuron mediated via C3-C4 propriospinal neurons in the Macaca fuscata. J Neurophysiol 1999; 82: 3580-95.
3. Alstermark B, Isa T, Petterson LG, Sasaki S. the C3-C4 propriospinal system in the cat and monkey: a spinal premotoneuronal centre for voluntary motor control. Acta Physiol 2007; 189: 123-40.
4. Aravamuthan BR, Muthusamy KA, Stein JF, Aziz TZ, Johansen Berg H. Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage 2007; 37: 694-705.
5. Baev KV, Greene KA, Marciano FF, Samanta JES, Shetter AG, Smith KA, et al. Physiology and pathophysiology of cortico-basal-ganglia-thalamo-cortical loops: theoretical and practical aspects. Progr Neuro-Psychopharmacol Biol Psychiat 2002; 26: 771-804.
6. Ballion B, Morin D, Viala D. Forelimb locomotor generators and quadrupedal locomotion in the neonatal rat. Eur J Neurosci 2001; 14: 1727-38.
7. Braak H, Del Tredici K. Cortico-basal ganglia-cortical circuitry in Parkinson's disease reconsidered. Exp Neurol 2008; 212: 226-29.
8. Brown P, Williams D. Basal ganglia local field potential activity: character and functional significance in the human. Clin Neurophysiol 2005; 116: 2510-9.
9. Buchthal F, Fernandez-Ballestreros ML. Electromyographyc study of the muscles of the upper arm and shoulder during walking in patients with Parkinson's disease. Brain 1965; 88: 875-96.
10. Carpinella I, Crenna P, Marzegan A, Rabuffetti M, Rizzone M, Lopiano L, et al. Effect of L-dopa and subthalamic nucleus stimulation on arm and leg swing during gait in Parkinson's disease. Conf Proc IEEE Eng Med Biol Soc 2007; 6665-8.
11. Carrol TJ, Baldwin ERL, Collins DF, Zehr EP. Corticospinal excitability is lower during rhythmic arm movements than during tonic contraction. J Neurophysiol 2005; 95: 914-21.
12. Chen R, Lemon R. Subthalamic nucleus and gait disturbance. Interaction between basal ganglia and brainstem and spinal pathways? Neurology 2004; 63: 1150-1.
13. Craik R, Herman R, Finley FR. Human solutions for locomotion: interlimb coordination. In: Herman RM, Grillner S, Stein PSG, Stuart DG, editors. Neural control of locomotion. New York: Plenum Press; 1976. p. 51-64.
14. Crenna P, Carpinella I, Rabuffetti M, Rizzone M, Lopiano L, Lanotte M, et al. Impact of subthalamic nucleus stimulation on the initiation of gait in Parkinson's disease. Exp Brain Res 2006; 172: 519-32.
15. D'Amico M, Ferrigno G. Technique for the evaluation of derivatives from noisy biomechanical displacement data using a model-based bandwidth-selection procedure. Med Biol Eng Comput 1990; 28: 407-15.
16. Davidson AG, Budford JA. Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging. Exp Brain Res 2006; 173: 25-39.
17. Delwaide P, Crenna P. Cutaneous nerve stimulation and motoneuronal excitability II: evidence for non-segmental influences. J Neurol Neurosurg Psychiatr 1984; 47: 190-6.
18. Dietz V. Do human bipeds use quadrupedal coordination? Trends Neurosci 2002; 25: 462-7.
19. Donker SF, Daffertshofer A, Beek PJ. Effects of velocity and limb loading in the coordination between limb movements during walking. J Motor Behav 2005; 37: 217-30.
20. Eke-Okoro ST, Gregoric M, Larsson LE. Alteration in gait resulting from deliberate changes of arm-swing amplitude and phase. Clin Biomech 1997; 12: 516-21.
21. Faist M, Kie J, Kurz D, Berger W, Maurer C, Pollak P, et al. Effects of bilateral subthalamic nucleus stimulation on gait in Parkinson's disease. Brain 2001; 124: 1590-600.
22. Fernandez Ballestreros ML, Buchthal F, Rosenfalck P. The pattern of muscular activity during the arm swing of natural walking. Acta Physiol Scand 1965; 63: 296-310.
23. Ferrarin M, Carpinella I, Rabuffetti M, Rizzone M, Lopiano L, Crenna P. Unilateral and bilateral subthalamic nucleus stimulation in Parkinson's disease: effects on EMG signals of lower limb muscles during walking. IEEE Trans Neural Syst Rehab Engin 2007; 15: 182-9.
24. Ferrarin M, Rizzone M, Bergamasco B, Lanotte M, Recalcati M, Pedotti A, et al. Effects of bilateral subthalamic stimulation on gait kinematics and kinetics in Parkinson's disease. Exp Brain Res 2005; 160: 517-27.
25. Ferrarin M, Rizzone M, Lopiano L, Recalcati M, Pedotti A. Effects of subthalamic nucleus stimulation and L-dopa on trunk kinematics of patients with Parkinson's disease. Gait Posture 2004; 19: 164-71.
26. Frigo C, Rabuffetti M. Multifactorial estimation of hip and knee joint centres for clinical application of gait analysis. Gait Posture 1998; 8: 91-102.
27. Fukuyama H, Ouchi Y, Matsuzaki S, Nagahama Y, Yamauchi H, Ogawa M, et al. Brain functional activity during gait in normal subjects. Neurosci Lett 1997; 228: 183-6.
28. Garcia L, Audin J, D'Alessandro G, Bioulac B, Hammond C. Dual effect of high frequency stimulation on subthalamic neuron activity. J Neurosci 2003; 23: 8743-51.
29. Gatev P, Darbin O, Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord 2006; 21: 1566-77.
30. Georgopoulos AP, Grillner S. Visuomotor coordination in reaching and locomotion. Science 1989; 245: 1209-10.
31. Grillner S. Control of locomotion in bipeds, tetrapods, and fish. In: Brooks V, editor. Handbook of physiology, 2, motor control. Bethesda: American Physiological Society; 1981. p. 1179-236.
32. Gutnik B, Mackie H, Hudson G, Standen C. How close to a pendulum is human upper limb movement during walking. HOMO - J Comp Hum Biol 2005; 56: 35-49.
33. Hallet M, Litivan I. Evaluation of surgery in Parkinson's disease: a report on the therapeutics and technology assessment subcommittee of the American Academy of Neurology. The task force on surgery in Parkinson's disease. Neurology 1999; 53: 1910-21.
34. Hellstrand E. Brain metabolism and human gait - a PET study. Acta Physiol Scand 1985; 125: 555-6.
35. Hinrichs RN. Whole body movement: coordination of arms and legs in walking and running. In: Winters JM, Woo SL-Y, editors. Multiple muscle systems: biomechanical and movement organization. New York: Springer-Verlag; 1990. p. 694-705.
36. Hogue RI. Upper-extremity muscular activity at different cadences and inclines during normal gait. Phys Therapy 1969; 49: 963-72.
37. Ivanenko YP, Grasso R, Zago M, Molinari M, Scivoletto G, Castellano V, et al. Temporal components of the motor patterns expressed by the human spinal cord reflect foot kinematics. J Neurophysiol 2003; 90: 3555-65.
38. Ivanenko YP, Poppele RE, Laquaniti F. Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol (Lond) 2004; 556: 267-82.
39. Jackson KM, Joseph J, Wyard SJ. The upper limb during human walking. Part I. Sagitttal movement. Electromyogr Clin Neurophysiol 1983a; 23: 425-34.
40. Jackson KM, Joseph J, Wyard SJ. The upper limb during human walking. Part II. Function. Electromyogr Clin Neurophysiol 1983b; 23: 435-46.
41. Jahn K, Deutschländer A, Stephan T, Kalla R, Wiesmann M, Strupp M, et al. Imaging human supraspinal locomotor centres in brainstem and cerebellum. Neuroimage 2008; 39: 786-92.
42. Jahn K, Deutschländer A, Stephan T, Strupp M, Wiesmann M, Brandt T. Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. Neuroimage 2004; 22: 1722-31.
43. Jordan LM. Initiation of locomotion in mammals. Ann NY Acad Sci 1998; 860: 83-93.
44. Juvin L, Simmers J, Morin D. Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 2005; 25: 6025-35.
45. Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, et al. Subthalamic nucleus deep brain stimulation: summary and-meta analysis of outcome. Mov Disord 2006; 21 (Suppl 14): S290-304.
46. Kline TL, Schmit BD, Kamper DG. Exaggerated interlimb coupling following stroke. Brain 2007; 130: 159-69.
47. Knuttson E, Mårtensson A. Posture and gait in parkinsonian patients. In: Bles W, Brandt T, editors. Disorders of posture and gait. Amsterdam: Elsevier Science Publisher (Biomedical Division); 1986. p. 217-29.
48. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. New Engl J Med 2003; 349: 1925-34.
49. Kringelbach ML, Jenkinson N, Owen SL, Aziz TZ. Translational principles of deep brain stimulation. Nat Rev Neurosci 2007; 8: 623-35.
50. Krystkowiak P, Blatt JL, Bourriez JL, Duhamel A, Perina M, Blond S, et al. Effects of subthalamic nucleus stimulation and levodopa treatment on gait abnormalities in Parkinson's disease. Arch Neurol 2003; 60: 80-4.
51. Kubo M, Wegenaar RC, Saltzman E, Holt KG. Biomechanical mechanism for transition in phase and frequency of arm and leg swing during walking. Biol Cybern 2004; 91: 91-8.
52. Kühn A, Kupsch A, Schneider G-H, Brown P. Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement. Eur J Neurosci 2006; 23: 1956-60.
53. Lemon RN, Griffiths J. Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve 2005; 32: 261-79.
54. Li Y, Wang W, Crompton RH, Gunther MM. Free vertical moments and trasverse forces in human walking and their role in relation to arm swing. J Exp Biol 2001; 204: 47-58.
55. Limousin P, Greene J, Pollak P, Rothwell J, Benabid AL, Frackowiak R. Changes in the cerebral activity pattern due to subthalamic nucleus or internal pallidum in Parkinson's disease. Ann Neurol 1997; 42: 283-91.
56. Lopiano L, Rizzone M, Bergamasco B, Tavella A, Torre E, Perozzo P, et al. Deep brain stimulation of the subthalamic nucleus: clinical effectiveness and safety. Neurology 2001; 56: 552-4.
57. Malouin F, Richards CL, Jackson PL, Dumas F, Dojon J. Brain activations during motor imagery of locomotor-related tasks: a PET study. Hum Brain Mapp 2003; 19: 47-62.
58. Matsuyama K, Drew T. Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. II. Walking on an inclined plane. J Neurophysiol 2000; 84: 2257-6.
59. Matsuyama K, Mori F, Nakajima K, Drew T, Aoki M, Mori S. Locomotor role of the corticoreticular-reticulospinal-spinal interneuronal system. Progr Brain Res 2004; 143: 239-49.
60. Maurer C, Mergner T, Xie J, Faist M, Pollak P, Lucking CH. Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson's disease. Brain 2003; 126: 1146-63.
61. Mazzone P, Lozano A, Stanzione P, Galati S, Scarnati E, Peppe A, et al. Implantation of human pedunculopontine nucleus: a safe and clinically relevant target in Parkinson's disease. Neuroreport 2005; 16: 1877-81.
62. Meink HM, Piesiur-Strehlow B. Reflex evoked in leg muscles from arm afferents: a propriospinal pathway in man? Exp Brain Res 1981; 43: 78-86.
63. Meissner W, Leblois A, Hansel D, Bioulac B, Gross CE, Benazzouz A, et al. Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 2005; 128: 2372-82.
64. Morris ME, Mc Ginley J, Huxham F, Collier J, Iansek R. Constraints on the kinetics, kinematic and spatio-temporal parameters of gait in Parkinson's disease. Hum Mov Sci 1999; 18: 461-83.
65. Murray MP, Sepic SB, Barnard EJ. Patterns of sagittal rotation of the upper limbs in walking. Phys Ther 1967; 47: 272-84.
66. Murray MP, Sepic SB, Gardner GM, Downs WJ. Walking patterns of men with parkinsonism. Am J Phys Med 1978; 57: 278-94.
67. Muzii RA, Lamm C, Gentile AM. Coordination of the upper and lower extremities. Hum Mov Sci 1984; 3: 337-54.
68. Nathan PW, Smith MC. The rubrospinal and central tegmental tracts in man. Brain 1982; 105: 223-69.
69. Nathan PW, Smith MC, Deacon P. Vestibulospinal, reticulospinal and descending propriospinal nerve fibers in man. Brain 1996; 119: 1809-33.
70. Nicolas G, Marchand-Pauvert V, Burke D, Pierrot-Deseilligny E. Corticospinal excitation of presumed cervical propriospinal neurones and its reversal to inhibition in humans. J Physiol (Lond) 2001; 533: 903-19.
71. Nielsen JB. How we walk: central control of muscle activity during human walking. Neuroscientist 2003; 9: 195-204.
72. Pahapill AP, Lozano AM. The pedunculopontine nucleus and Parkinson's disease. Brain 2000; 123: 1767-83.
73. Park J. Synthesis of natural arm swing motion in human bipedal walking. J Biomech 2008; 41: 1417-26.
74. Pierrot Deseilligny E. Propriospinal transmission of part of the corticospinal excitation in humans. Muscle Nerve 2002; 26: 155-72.
75. Plaha P, Gill SS. Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson's disease. Neuroreport 2005; 16: 1883-7.
76. Salarian A, Russmann H, Vingerhoets FJG, Dehollain C, Blanc Y, Burkhard PR, et al. Gait assessment in Parkinson's disease: toward an ambulatory system for long-term monitoring. IEEE Trans Biomed Eng 2004; 51: 1434-43.
77. Schepens B, Drew T. Descending signals from the pontomedullary reticular formation are bilateral, asymmetric, and gated during reaching movements in the cat. J Neurophysiol 2006; 96: 2229-52.
78. Shimamura M, Tanaka I, Fuwa T. Supraspinal control mechanisms of coordinated movements among four limbs in cats during stepping. In: Shimamura M, Grillner S, Edgerton VR, editors. Neurobiological basis of human locomotion. Tokyo: Japan Scientific Society Press; 1991. p. 57-74.
79. Siegfrid J, Lippiz B. Bilateral chronic electrostimulation of ventroposterolateral pallidum: a new therapeutic approach for alleviating all parkinsonian symptoms. Neurosurgery 1994; 35: 1126-30.
80. Silberstein P, Pogosyan A, Kühn AA, Hotton G, Tisch S, Kupsch A, Dowsey-Limousin P, et al. Cortico-cortical coupling in Parkinson's disease and its modulation by therapy. Brain 2005; 128: 1277-91.
81. Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jönk K, Illert M, Deuschl G. Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson's disease. J Neurol Neurosurg Psychiat 2001; 70: 289-97.
82. Takakusaki K, Habaguchi T, Ostinata-Sugimoto J, Saitoh K, Sakamoto T. Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: a new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience 2003; 119: 293-308.
83. Turton A, Lemon RN. The contribution of fast corticospinal input to the voluntary activation of proximal muscles in normal subjects and in stroke patients. Exp Brain Res 1999; 129: 559-72.
84. van Emmerik REA, Wagenaar RC, Wegen EH. Interlimb coupling patterns in humans: are we bipeds or quadrupeds? Ann NY Acad Sci 1998; 860: 539-42.
85. Wagenaar RC, van Emmerik REA. Resonant frequencies of arms and legs identify different walking patterns. J Biomech 2000; 33: 853-61.
86. Wannier T, Bastiaanse C, Colombo G, Dietz V. Arm leg coordination in humans during walking, creeping and swimming activities. Exp Brain Res 2001; 141: 375-9.
87. Webb D, Tuttle RH, Baksh M. Pendular activity of human upper limbs during slow and normal walking. Am J Phys Anthropol 1994; 93: 477-89.
88. Winogrodzka A, Wagenaar R, Booij J, Wolters EC. Rigidity and bradikinesia reduce interlimb coordination in Parkinsonian gait. Arch Phys Med Rehabil 2005; 86: 183-9.
89. Wright WG, Gurfinkel VS, Nutt J, Horak FB, Cordo PJ. Axial hypertonicity in Parkinson's disease: direct measurements of trunk and hip torque. Exp Neurol 2007; 208: 38-46.
90. Xiang Y, John P, Yakushin SB, Kunin M, Raphan H, Cohen B. Dynamics of quadrupedal locomotion in monkeys: implication for central control. Exp Brain Res 2007; 177: 551-72.
91. Yamaguchi T. Activity of cervical neurons during forelimb fictive locomotion in decerebrate cats. Jpn J Physiol 1992; 42: 501-14.
92. Zehr EP, Carrol TJ, Chua R, Collins DF, Frigon A, Haridas C, et al. Possible contribution of CPG activity to the control of rhythmic human arm movement. Can J Physiol Pharmacol 2004; 82: 556-68.
93. Zijlmans JCM, Poels PJE, Duysens J, van der Straaten J, Thien T, van't Hof MA, et al. Quantitative gait analysis in patients with vascular parkinsonism. Mov Disord 1996; 11: 501-8.