Advertisement

Gait bradykinesia: difficulty in switching posture/gait measured by the anatomical y-axis vector of the sole in Parkinson’s disease

Abstract

This study in Parkinson’s disease examined how spatiotemporal parameters in gait bradykinesia link to difficulty in terminating posture and initiating gait locomotion. 41 idiopathic Parkinson’s disease patients and 15 age-matched healthy subjects participated in this study. After the patients fixated on a visual-fixation-target, gait was triggered by visual or vocal cue-stimulus. The LED instructed subjects to quickly achieve their own comfortable walking speed on a level floor. The posterior-anterior force of the y-axis vectors of sole relating to soleus and tibialis-anterior EMGs were examined. Step-gain was defined as the duration of the swing-phase relative that of the contralateral stance-phase. Dynamic-ratio was defined as the duration the fore-foot phase relative to that of the ipsilateral stance-phase as forward-oriented movement in each step. The pause in tonic soleus EMG was defined as the off-latency of posture (termination) and the onset of a tibialis-anterior EMG-burst as the on-latency of gait. In Parkinson’s disease, soleus off-latencies were prolonged, whereas tibialis-anterior on-latencies were less prolonged. Unsynchronized off/on-latency differences correlated with spatiotemporal parameters of dynamic-ratios, step-gains, gait-initiation, and gait speed in gait bradykinesia. Delayed EMG off-latencies correlated with prolonged motor-latencies in gait bradykinesia as delayed initial backward body-shift. A delayed and deficient initial backward body-shift of y-axis vector was linked to each difficulty in terminating posture and initiating gait, changing to random gait akinesia. Gait bradykinesia in Parkinson’s disease stemmed from unsynchronized off/on-latency EMG activities, linking to each difficulty in terminating posture and initiating gait synergic movement through an initial backward body-shift.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

ANOVA:

Analysis of variance

BS:

Body-shift

DAT:

Dopamine transporters

EMG:

Electromyogram

GPi:

Globus pallidus pars interna

GPe:

Globus pallidus pars externa

H–Y:

Hoehn and Yahr

LED:

Light-emitting diodes

No-gap:

No-gap task

SNr:

Substantia nigra pars reticulate

STN:

Subthalamic nucleus

Off-latency:

Off-EMG latency

Off-motor program:

Off-EMG latency motor program

On-latency:

On-EMG latency

On-motor program:

On-EMG latency motor program

Off/on-latency difference:

Off/on-EMG latency difference

Off/on-latency motor program:

Off/on-EMG latency motor program

References

  1. Agostino R, Berardelli A, Formica A, Accornero N, Manfredi M (1992) Sequential arm movements in patients with Parkinson’s disease, Huntington’s disease and dystonia. Brain 115:1481–1495

  2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuit links basal ganglia and cortex. Ann Rev Neurosci 9:357–381

  3. Basmajian JV (1974) Muscles alive; their functions revealed by electromyography, 3rd edn. William & Wilkins Co, Baltimore, p p173

  4. Bawa P, Chalmers GS, Stewart H, Eisen AA (2002) Responses of ankle extensor and flexor motoneurons to transcranial magnetic stimulation. J Neurophysiol 88:124–132

  5. Benecke R, Rothwell JC, Dock JPR, Day BL, Marsden CD (1987) Performance of simultaneous movements in patients with Parkinson’s disease. Brain 109:739–757

  6. Brain WR, Walton JN (1969) The parkinsonian syndrome. Brain’s Disease of the Nervous System. London Oxford University Press, New York, p 522

  7. Brotchie P, Iansek R, Horne MK (1991a) Motor function of the monkey globus pallidus. 1. Neuronal discharge and parameters of movement. Brain 114:1667–1683

  8. Brotchie P, Iansek R, Horne MK (1991b) Motor function of the monkey globus pallidus. 2. Cognitive aspects of movement and phasic neuronal activity. Brain 114:1685–1702

  9. Carpinella I, Crenna P, Calabrese E, Rabuffetti M, Mazzoleni P, Nemni R et al (2007) Locomotor function in the early stage of Parkinson’s disease. IEEE Trans Neural Sys Rehab Eng 15:543–551

  10. Charcot JM (1880) Leçons sur les maladies du système nerveux faites á la Salpêtrière, vol 1. Delahaye & Lecrosnier, Paris, p 155

  11. Crenna P, Frigo C (1991) A motor programme for the initiation of forward-oriented movement in humans. J Physiol 437:635–653

  12. Crutcher MD, DeLong MR (1984) Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53:244–258

  13. DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20–24

  14. Delval A, Rambour A, Tar C, Dujardin D, Devous D, Bleise S et al (2016) Freezing/Festination during motor tasks in early-stage Parkinson’s disease: a prospective study. Move Disord 31:1837–1845

  15. Evarts EV, Teravainen H, Calone DB (1981) Reaction time in Parkinson’s disease. Brain 104:167–186

  16. Flaherty AW, Graybiel AM (1991) Coriticostiriatal transformations in the primate somatosensory system: projections from physiologically mapped body-part representations. J Neurophysiol 66:1249–1263

  17. Gantchev N, Viallet F, Aurenty R, Massion J (1996) Impairement of posture-kinetic co-ordination during initiation of forward oriented stepping movement in parkinsnian patients. EEG Clin Neurophysiol 101:110–120

  18. Georgopoulos AP, DeLong MR, Crutcher MD (1983) Relation between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J Neurosci 3:1586–1598

  19. Goerendt IK, Mess C, Dawrence AD, Grasby PM, Piccini P, Brooks DJ (2003) Dopamine release during sequential finger movements in health and Parkinson’s disease: a PET study. Brain 126:312–325

  20. Gowars WR (1892) A manual of disease of the nervous system, vol 2. Blankiston, Philadelphia, p 636

  21. Halliday SE, Winter DA, Frank JS, Patla AE, Prince F (1998) The initiation of gait in young, elderly, and Parkinson’s disease subject. Gait Posture 8:8–14

  22. Harrington DL, Haaland KY (1991) Sequencing in Parkinson’s disease: abnormalities in programming and controlling movement. Brain 114:99–115

  23. Hazarati LN, Prent A (1992) The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res 592:213–227

  24. Hikosaka O, Sakamoto M, Usui S (1989) Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. J Neurophysiol 61:780–798

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

  26. Hughes AJ, Daniels SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

  27. Kiriyama K, Warabi T, Kato M, Yoshida T, Kobayashi N (2004) Progression of human body-shift during successive walking studied by recording sole-floor reaction forces. Neurosci Lett 359:130–132

  28. Kiriyama K, Warabi T, Kato M, Yoshida T, Kobayashi N (2005) Medial-lateral balance during stance phase of straight and circular walking of human subjects. Neurosci Lett 388:91–95

  29. Kobayashi N, Warabi T, Kato M, Kiriyama K, Yoshida T, Chiba S (2006) Posterior–anterior body weight shift during stance period studied by measuring solw-floor reaction force during healthy and hemiplegic human walking. Neurosci Lett 399:141–146

  30. Liblois A, Boraud T, Meissner W, Bergman H, Hansel D (2006) Competition between feedback loops underlines normal and pathological dynamics in the basal ganglia. J Neurosci 26:3567–3583

  31. Maertens de Noordhout A, Rapisarda G, Bogacs D, Gerard P, Pasqua VD, Pennisis G, Delwaide PJ (1999) Corticomononeuronal synaptic connections in normal man: an electrophysiological study. Brain 122:1327–1340

  32. Marsden CD, Rothwell JC (1987) The physiology of idiopathic dystonia. Can J Neurol Sci. 14:521–527

  33. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425 (Review)

  34. Mink JW, Thach WT (1991) Basal ganglia motor control. II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. J Neurophysiol 65:301–329

  35. Nambu A, Tokuno H, Takada M (2002a) Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res 43:111–117

  36. Nambu A, Kaneda K, Tokuno H, Takada M (2002b) Organization of corticostriatal motor inputs in monkey putamen. J Neurophysiol 88:1830–1842

  37. Nigg BM, Herzog W (1999) Biomechanics of the musculo-skeletal system. Wiley, Calgary

  38. Nutt JG et al (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744

  39. Parkinson J (1817) An essay on the shaking palsy. Sherwood, Neely & Jones, London

  40. Poizner H, Feldman AG, Levin ME, Berknblit MG, Hening WA, Patel A, Adamovich SV (2000) The timing of arm-trunk coordination in deficient and visually-dependent in Parkinson’s patients during reaching movement. Exp Brain Res 133:279–292

  41. Richer P (1888) Habitude extèrieure et facies dans la paralysie agitante. Nouv Inconogr. Saplêt 1:213

  42. Sabatini U, Goulaouar K, Fabre N, Martin F, Carel C, Colonnese C et al (2000) Cortical motor reorganization in akinetic patients with Parkinson’s disease A functional MRI stud. Brain 123:394–403

  43. Thach WT (1978) Correlation of neural discharge with pattern and force of muscular activity, joint position and direction of the intended movement in motor cortex and cerebellum. J Neurophysiol 41:654–676

  44. Warabi T, Kato M (2009) A new method to measure sole-floor reaction forces from anatomically discrete points of the sole during human locomotion. Recent Res Dev Neurosci 3:1–23

  45. Warabi T, Noda H, Yanagisawa N, Tashiro K, Shindo R (1986) Changes in sensory- motor function associated with the degree of bradykinesia of Parkinson’s disease. Brain 109:1209–1224

  46. Warabi T, Yanagisawa N, Shindo R (1988) Changes in strategy of aiming tasks in Parkinson’s disease. Brain 111:497–505

  47. Warabi T, Kato M, Kiriyama K, Yoshida T, Kobayashi N (2004) Analysis of human locomotion by recording sole-floor reaction force from anatomically discrete point. Neurosci Res. 50:419–426

  48. Warabi T, Kato M, Kato M, Kiriyama K, Yoshida T, Kobayashi N (2005) Treadmill walking and overground waking of human subjects compared by recording sole-floor reaction force. Neurosci Res. 53:343–348

  49. Warabi T, Fukushima K, Olley PM, Chiba S, Yanagisawa N (2011) Difficulty in terminating the preceding movement/posture explains the impaired initiation of new movements in Parkinson’s disease. Neurosci Lett 496:84–89

  50. Warabi T, Furuyama H, Sugai E, Kato M, Yanagisawa N (2018) Gait bradykinesia in Parkinson’s disease: a change in the motor program which controls the synergy of gait. Exp Brain Res 236:43–57

  51. Wichmann T, Bergmann H, DeLong MR (1994) The primate subthalamic nucleus. I. Functional properties in intact animals. J Neurophysiol 72:496–506

  52. Wilson CJ (1995) The contribution of cortical neurons to the firing pattern of striatal spine neurons. In: Houk JC, Davis JL, Beiser DG (eds) Models of information processing in the basal ganglia. MIT press, Cambridge, pp 29–50

  53. Wilson KSA, Bruce AN (1970) Paralysis agitans neurology, vol II. Hafner Publishing Company, New York, p 787

Download references

Acknowledgements

The authors wish to express their gratitude to Prof. Nobuo Yanagisawa, MD PhD for his valuable comments, and Prof. Mariya A. Niendorf PhD for English language advice. We also wish to thank Mrs. Takako Takita, Eri Sugai, PT, and Kenestu Shimizu OT for skilled technical assistance with the figures and the manuscript.

Funding

The authors received no financial support for the research, authorship, or publication of this article.

Author information

Correspondence to Tateo Warabi.

Ethics declarations

Conflict of interest

The authors declare no potential conflicts of interest with respect to the research, authorship, or publication of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Francesco Lacquaniti.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Warabi, T., Furuyama, H. & Kato, M. Gait bradykinesia: difficulty in switching posture/gait measured by the anatomical y-axis vector of the sole in Parkinson’s disease. Exp Brain Res 238, 139–151 (2020). https://doi.org/10.1007/s00221-019-05704-x

Download citation

Keywords

  • Parkinson’s disease
  • Gait bradykinesia
  • Akinesia
  • Motor program
  • Off-latency