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Quadrupedal coordination of bipedal gait: implications for movement disorders

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Abstract

During recent years, evidence has come up that bipedal locomotion is based on a quadrupedal limb coordination. A task-dependent neuronal coupling of upper and lower limbs allows one to involve the arms during gait but to uncouple this connection during voluntarily guided arm/hand movements. Hence, despite the evolution of a strong cortico-spinal control of hand/arm movements in humans, a quadrupedal limb coordination persists during locomotion. This has consequences for the limb coordination in movement disorders such as in Parkinson’s disease (PD) and after stroke. In patients suffering PD, the quadrupedal coordination of gait is basically preserved. The activation of upper limb muscles during locomotion is strong, similar as in age-matched healthy subjects although arm swing is reduced. This suggests a contribution of biomechanical constraints to immobility. In post-stroke subjects a close interactions between unaffected and affected sides with an impaired processing of afferent input takes place. An afferent volley applied to a leg nerve of the unaffected leg leads to a normal reflex activation of proximal arm muscles of both sides. In contrast, when the nerve of the affected leg was stimulated, neither on the affected nor in the unaffected arm muscles EMG responses appear. Muscle activation on the affected arm becomes normalized by influences of the unaffected side during locomotion. These observations have consequences for the rehabilitation of patients suffering movement disorders.

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References

  1. Gans C et al (1997) Vertebrate locomotion. In: Handbook of Physiology, Section 13: Comparative Physiology. Oxford University Press, England, pp 55–213

  2. Duysens J et al (1998) Neural control of locomotion: the central pattern generator from cats to humans. Gait Posture 7:131–141

    Article  PubMed  Google Scholar 

  3. Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Brookhart JMaMVB (ed) Handbook of physiology. The nervous system. Motor control. American Physilogy Society, New York, pp 1179–1236

    Google Scholar 

  4. Cazalets JR et al (2000) Coupling between lumbar and sacral motor networks in the neonatal rat spinal cord. Eur J Neurosci 12:2993–3002

    Article  PubMed  CAS  Google Scholar 

  5. Miller S et al (1975) Coordination of movements of the kindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res 91:217–237

    Article  PubMed  CAS  Google Scholar 

  6. Nathan PW et al (1996) Vestibulospinal, reticulospinal and descending propriospinal nerve fibres in man. Brain 119 (Pt 6):1809–1833

    Article  PubMed  Google Scholar 

  7. Pang MY et al (2000) The initiation of the swing phase in human infant stepping: importance of hip position and leg loading. J Physiol 528 (Pt 2):389–404

    Article  PubMed  CAS  Google Scholar 

  8. Yang JF et al (1998) Transient disturbances to one limb produce coordinated, bilateral responses during infant stepping. J Neurophysiol 79:2329–2337

    PubMed  CAS  Google Scholar 

  9. Dietz V (1992) Human neuronal control of automatic functional movements: interaction between central programs and afferent input. Physiol Rev 72:33–69

    PubMed  CAS  Google Scholar 

  10. Dietz V (1997) Neurophysiology of gait disorders: present and future applications. Electroencephalogr Clin Neurophysiol 103:333–355

    Article  PubMed  CAS  Google Scholar 

  11. Grillner S (1986) Interaction between sensory signals and the central networks controlling locomotion in lamprey, dog fish and cat. In: Grillner S et al (eds) Wenner-Gren international symposium series. Neurobiology of vertebrate locomotion. Macmillan, England, pp 505–512

    Google Scholar 

  12. Herder JG (1785) Ideen zur Philosophie der Geschichte der Menschheit. Hartknoch, Leipzig

    Google Scholar 

  13. McKiernan BJ et al (1998) Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. J Neurophysiol 80:1961–1980

    PubMed  CAS  Google Scholar 

  14. Porter R et al (1993) Corticospinal function and voluntary movement. Clarendon, Oxford

    Google Scholar 

  15. Alstermark B et al (1992) The C3–C4 propriospinal system: target-reaching and food-taking. In: Lea Jami (ed) Muscle afferents ans spinal control of movement. Pergamon, Oxford, pp 327–354

    Google Scholar 

  16. Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462–467

    Article  PubMed  Google Scholar 

  17. Michel J et al (2008) Obstacle stepping involves spinal anticipatory activity associated with quadrupedal limb coordination. Eur J Neurosci 27:1867–1875

    Article  PubMed  CAS  Google Scholar 

  18. Dietz V et al (2001) Neuronal coordination of arm and leg movements during human locomotion. Eur J Neurosci 14:1906–1914

    Article  PubMed  CAS  Google Scholar 

  19. Calancie B et al (1996) Central nervous system plasticity after spinal cord injury in man: interlimb reflexes and the influence of cutaneous stimulation. Electroencephalogr Clin Neurophysiol 101:304–315

    Article  PubMed  CAS  Google Scholar 

  20. Brocard F et al (2010) The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. J Neurosci 30:523–533

    Article  PubMed  CAS  Google Scholar 

  21. Baldissera F et al (1998) Cyclic modulation of the H-reflex in a wrist flexor during rhythmic flexion-extension movements of the ipsilateral foot. Exp Brain Res 118:427–430

    Article  PubMed  CAS  Google Scholar 

  22. Wannier T et al (2001) Arm to leg coordination in humans during walking, creeping and swimming activities. Exp Brain Res 141:375–379

    Article  PubMed  CAS  Google Scholar 

  23. De Leon RD et al (1999) Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J Neurophysiol 81:85–94

    PubMed  Google Scholar 

  24. Michel J et al (2007) Facilitation of spinal reflexes assists performing but not learning an obstacle-avoidance locomotor task. Eur J Neurosci 26:1299–1306

    Article  PubMed  CAS  Google Scholar 

  25. Kornhuber HH et al (1965) Changes in the brain potential in voluntary movements and passive movements in man: readiness potential and reafferent potentials. Pflugers Arch Gesamte Physiol Menschen Tiere 284:1–17

    Article  PubMed  CAS  Google Scholar 

  26. Shibasaki H et al (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341–2356

    Article  PubMed  Google Scholar 

  27. Carpinella I et al (2007) 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 2007:6665–6668

    PubMed  CAS  Google Scholar 

  28. Winogrodzka A et al (2005) Rigidity and bradykinesia reduce interlimb coordination in Parkinsonian gait. Arch Phys Med Rehabil 86:183–189

    Article  PubMed  Google Scholar 

  29. Plotnik M et al (2007) A new measure for quantifying the bilateral coordination of human gait: effects of aging and Parkinson’s disease. Exp Brain Res 181:561–570

    Article  PubMed  Google Scholar 

  30. Swinnen SP et al (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

    Article  PubMed  CAS  Google Scholar 

  31. Rogers MW et al (1987) Postural adjustments preceding rapid arm movements in parkinsonian subjects. Neurosci Lett 75:246–251

    Article  PubMed  CAS  Google Scholar 

  32. van Hedel HJ et al (2006) Learning a high-precision locomotor task in patients with Parkinson’s disease. Mov Disord 21:406–411

    Article  PubMed  Google Scholar 

  33. Dietz V et al (1998) Influence of body load on the gait pattern in Parkinson’s disease. Mov Disord 13:255–261

    Article  PubMed  CAS  Google Scholar 

  34. Rogers MW (1996) Disorders of posture, balance, and gait in Parkinson’s disease. Clin Geriatr Med 12:825–845

    PubMed  CAS  Google Scholar 

  35. Dietz V et al (2008) Locomotion in Parkinson’s disease: neuronal coupling of upper and lower limbs. Brain 131:3421–3431

    Article  PubMed  CAS  Google Scholar 

  36. Yang JF et al (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117

    PubMed  CAS  Google Scholar 

  37. Sandrini G et al (2005) The lower limb flexion reflex in humans. Prog Neurobiol 77:353–395

    Article  PubMed  Google Scholar 

  38. Dietz V et al (2009) Human bipeds use quadrupedal coordination during locomotion. Ann N Y Acad Sci 1164:97–103

    Article  PubMed  Google Scholar 

  39. Nieuwenhuijzen PH et al (2006) Startle responses in Parkinson patients during human gait. Exp Brain Res 171:215–224

    Article  PubMed  CAS  Google Scholar 

  40. Grin L et al (2007) The effect of voluntary arm abduction on balance recovery following multidirectional stance perturbations. Exp Brain Res 178:62–78

    Article  PubMed  Google Scholar 

  41. Ford MP et al (2007) Phase manipulation and walking in stroke. J Neurol Phys Ther 31:85–91

    PubMed  Google Scholar 

  42. Reisman DS et al (2007) Locomotor adaptation on a split-belt treadmill can improve walking symmetry post-stroke. Brain 130:1861–1872

    Article  PubMed  Google Scholar 

  43. Barzi Y et al (2008) Rhythmic arm cycling suppresses hyperactive soleus H-reflex amplitude after stroke. Clin Neurophysiol 119:1443–1452

    Article  PubMed  Google Scholar 

  44. Debaere F et al (2001) Coordination of upper and lower limb segments: deficits on the ipsilesional side after unilateral stroke. Exp Brain Res 141:519–529

    Article  PubMed  CAS  Google Scholar 

  45. Kline TL et al (2007) Exaggerated interlimb neural coupling following stroke. Brain 130:159–169

    Article  PubMed  Google Scholar 

  46. Stephenson JL et al (2010) The effect of arm movements on the lower limb during gait after a stroke. Gait Posture 31:109–115

    Article  PubMed  Google Scholar 

  47. Finley JM et al (2008) Stretch reflex coupling between the hip and knee: implications for impaired gait following stroke. Exp Brain Res 188:529–540

    Article  PubMed  Google Scholar 

  48. Divani AA et al (2009) Risk factors associated with injury attributable to falling among elderly population with history of stroke. Stroke 40:3286–3292

    Article  PubMed  Google Scholar 

  49. Lamontagne A et al (2009) Gaze and postural reorientation in the control of locomotor steering after stroke. Neurorehabil Neural Repair 23:256–266

    PubMed  Google Scholar 

  50. Lamontagne A et al (2007) Physiological evaluation of gait disturbances post stroke. Clin Neurophysiol 118:717–729

    Article  PubMed  Google Scholar 

  51. Marigold DS et al (2006) Altered timing of postural reflexes contributes to falling in persons with chronic stroke. Exp Brain Res 171:459–468

    Article  PubMed  Google Scholar 

  52. Marigold DS et al (2004) Modulation of ankle muscle postural reflexes in stroke: influence of weight-bearing load. Clin Neurophysiol 115:2789–2797

    Article  PubMed  Google Scholar 

  53. Kloter E et al (2011) Locomotion in stroke subjects: interactions between unaffected and affected sides. Brain 134:721–731

    Article  PubMed  Google Scholar 

  54. Lemon RN (2008) Descending pathways in motor control. Annu Rev Neurosci 31:195–218

    Article  PubMed  CAS  Google Scholar 

  55. Faist M et al (1999) Impaired modulation of quadriceps tendon jerk reflex during spastic gait: differences between spinal and cerebral lesions. Brain 122 (Pt 3):567–579

    Article  PubMed  Google Scholar 

  56. Thilmann AF et al (1990) Pathological stretch reflexes on the “good” side of hemiparetic patients. J Neurol Neurosurg Psychiatry 53:208–214

    Article  PubMed  CAS  Google Scholar 

  57. Dietz V et al (2007) Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol 6:725–733

    Article  PubMed  Google Scholar 

  58. Dyer JO et al (2009) Transmission in heteronymous spinal pathways is modified after stroke and related to motor incoordination. PloS One 4:e4123

    Article  PubMed  Google Scholar 

  59. Forrester LW et al (2008) Exercise-mediated locomotor recovery and lower-limb neuroplasticity after stroke. J Rehabil Res Dev 45:205–220

    Article  PubMed  Google Scholar 

  60. Luft AR et al (2008) Treadmill exercise activates subcortical neural networks and improves walking after stroke: a randomized controlled trial. Stroke 39:3341–3350

    Article  PubMed  Google Scholar 

  61. Werner C et al (2002) Treadmill training with partial body weight support and an electromechanical gait trainer for restoration of gait in subacute stroke patients: a randomized crossover study. Stroke 33:2895–2901

    Article  PubMed  CAS  Google Scholar 

  62. Hornby TG et al (2008) Enhanced gait-related improvements after therapist- versus robotic-assisted locomotor training in subjects with chronic stroke: a randomized controlled study. Stroke 39:1786–1792

    Article  PubMed  Google Scholar 

  63. Lamontagne A et al (2004) Faster is better: implications for speed-intensive gait training after stroke. Stroke 35:2543–2548

    Article  PubMed  Google Scholar 

  64. Plummer P et al (2007) Effects of stroke severity and training duration on locomotor recovery after stroke: a pilot study. Neurorehabil Neural Repair 21:137–151

    Article  PubMed  Google Scholar 

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Dietz, V. Quadrupedal coordination of bipedal gait: implications for movement disorders. J Neurol 258, 1406–1412 (2011). https://doi.org/10.1007/s00415-011-6063-4

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