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Experimental Brain Research

, Volume 237, Issue 6, pp 1457–1467 | Cite as

Contribution of corticospinal drive to ankle plantar flexor muscle activation during gait in adults with cerebral palsy

  • Rasmus Feld FriskEmail author
  • Jakob Lorentzen
  • Jens Bo Nielsen
Research Article
  • 65 Downloads

Abstract

Impaired plantar flexor muscle activation during push-off in late stance contributes importantly to reduced gait ability in adults with cerebral palsy (CP). Here we used low-intensity transcranial magnetic stimulation (TMS) to suppress soleus EMG activity during push-off as an estimate of corticospinal drive in CP adults and neurologically intact (NI) adults. Ten CP adults (age 34 years, SD 14.6, GMFCS I–II) and ten NI adults (age 33 years, SD 9.8) walked on a treadmill at their preferred walking speed. TMS of the leg motor cortex was elicited just prior to push-off during gait at intensities below threshold for motor-evoked potentials. Soleus EMG from steps with and without TMS were averaged and compared. Control experiments were performed while standing and in NI adults during gait at slow speed. TMS induced a suppression at a latency of about 40 ms. This suppression was similar in the two populations when differences in control EMG and gait speed were taken into account (CP 18%, NI 16%). The threshold of the suppression was higher in CP adults. The findings suggest that corticospinal drive to ankle plantar flexors at push-off is comparable in CP and NI adults. The higher threshold of the suppression in CP adults may reflect downregulation of cortical inhibition to facilitate corticospinal drive. Interventions aiming to facilitate excitability in cortical networks may contribute to maintain or even improve efficient gait in CP adults.

Keywords

Cerebral palsy Corticospinal drive Plantar flexor muscles Push-off 

Notes

Acknowledgements

The study was supported by the Elsass foundation, Charlottenlund, Denmark. The foundation was not involved in the conduct or decision making regarding the work presented in the paper. We are grateful to all the participants for all their interest in the study.

Compliance with ethical standards

Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the authors.

References

  1. Achache V, Roche N, Lamy JC, Boakye M, Lackmy A, Gastal A, Quentin V, Katz R (2010) Transmission within several spinal pathways in adults with cerebral palsy. Brain 133:1470–1483CrossRefGoogle Scholar
  2. Andersson C, Mattsson E (2001) Adults with cerebral palsy: a survey describing problems, needs, and resources, with special emphasis on locomotion. Dev Med Child Neurol 43:76–82CrossRefGoogle Scholar
  3. Barber L, Carty C, Modenese L, Walsh J, Boyd R, Lichtwark G (2017) Medial gastrocnemius and soleus muscle-tendon unit, fascicle, and tendon interaction during walking in children with cerebral palsy. Dev Med Child Neurol 59:843–851CrossRefGoogle Scholar
  4. Barthelemy D, Nielsen JB (2010) Corticospinal contribution to arm muscle activity during human walking. J Physiol 588:967–979CrossRefGoogle Scholar
  5. Barthelemy D, Willerslev-Olsen M, Lundell H, Conway BA, Knudsen H, Biering-Sorensen F, Nielsen JB (2010) Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons. J Neurophysiol 104:1167–1176CrossRefGoogle Scholar
  6. Barthelemy D, Knudsen H, Willerslev-Olsen M, Lundell H, Nielsen JB, Biering-Sorensen F (2013) Functional implications of corticospinal tract impairment on gait after spinal cord injury. Spinal Cord 51:852–856CrossRefGoogle Scholar
  7. Belmonti V, Cioni G, Berthoz A (2016) Anticipatory control and spatial cognition in locomotion and navigation through typical development and in cerebral palsy. Dev Med Child Neurol 58(Suppl 4):22–27CrossRefGoogle Scholar
  8. Benner JL, Hilberink SR, Veenis T, Stam HJ, van der Slot WM, Roebroeck ME (2017) Long-term deterioration of perceived health and functioning in adults with cerebral palsy. Arch Phys Med Rehabil 98:2196–2205.e2191CrossRefGoogle Scholar
  9. Berweck S, Walther M, Brodbeck V, Wagner N, Koerte I, Henschel V, Juenger H, Staudt M, Mall V (2008) Abnormal motor cortex excitability in congenital stroke. Pediatr Res 63:84–88CrossRefGoogle Scholar
  10. Bütefisch CM, Netz J, Wessling M, Seitz RJ, Homberg V (2003) Remote changes in cortical excitability after stroke. Brain 126:470–481CrossRefGoogle Scholar
  11. Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M (1999) Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol 81:129–139CrossRefGoogle Scholar
  12. Chan JH, Lin CS, Pierrot-Deseilligny E, Burke D (2002) Excitability changes in human peripheral nerve axons in a paradigm mimicking paired-pulse transcranial magnetic stimulation. J Physiol 542:951–961CrossRefGoogle Scholar
  13. Darekar A, McFadyen BJ, Lamontagne A, Fung J (2015) Efficacy of virtual reality-based intervention on balance and mobility disorders post-stroke: a scoping review. J Neuroeng Rehabil 12:46CrossRefGoogle Scholar
  14. Davey NJ, Romaiguere P, Maskill DW, Ellaway PH (1994) Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. J Physiol 477:223–235CrossRefGoogle Scholar
  15. Davey NJ, Smith HC, Wells E, Maskill DW, Savic G, Ellaway PH, Frankel HL (1998) Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury. J Neurol Neurosurg Psychiatry 65:80–87CrossRefGoogle Scholar
  16. Di Lazzaro V, Oliviero A, Profice P, Saturno E, Pilato F, Insola A, Mazzone P, Tonali P, Rothwell JC (1998a) Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 109:397–401CrossRefGoogle Scholar
  17. Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998b) Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits. Exp Brain Res 119:265–268CrossRefGoogle Scholar
  18. Di Lazzaro V, Oliviero A, Profice P, Meglio M, Cioni B, Tonali P, Rothwell JC (2001) Descending spinal cord volleys evoked by transcranial magnetic and electrical stimulation of the motor cortex leg area in conscious humans. J Physiol 537:1047–1058CrossRefGoogle Scholar
  19. Dietz V, Harkema SJ (2004) Locomotor activity in spinal cord-injured persons. J Appl Physiol (1985) 96:1954–1960CrossRefGoogle Scholar
  20. Drew T, Jiang W, Kably B, Lavoie S (1996) Role of the motor cortex in the control of visually triggered gait modifications. Can J Physiol Pharmacol 74:426–442Google Scholar
  21. Drew T, Jiang W, Widajewicz W (2002) Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat. Brain Res Brain Res Rev 40:178–191CrossRefGoogle Scholar
  22. Fisher RJ, Nakamura Y, Bestmann S, Rothwell JC, Bostock H (2002) Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res 143:240–248CrossRefGoogle Scholar
  23. Frisk RF, Jensen P, Kirk H, Bouyer LJ, Lorentzen J, Nielsen JB (2017) Contribution of sensory feedback to plantar flexor muscle activation during push-off in adults with cerebral palsy. J Neurophysiol.  https://doi.org/10.1152/jn.00508.2017 Google Scholar
  24. Graham HK, Rosenbaum P, Paneth N, Dan B, Lin JP, Damiano DL, Becher JG, Gaebler-Spira D, Colver A, Reddihough DS, Crompton KE, Lieber RL (2016) Cerebral palsy. Nat Rev Dis Primers 2:15082CrossRefGoogle Scholar
  25. Honeine JL, Schieppati M, Gagey O, Do MC (2014) By counteracting gravity, triceps surae sets both kinematics and kinetics of gait. Physiol Rep 2:e00229CrossRefGoogle Scholar
  26. Huynh W, Vucic S, Krishnan AV, Lin CS, Kiernan MC (2016) Exploring the evolution of cortical excitability following acute stroke. Neurorehabil Neural Repair 30:244–257CrossRefGoogle Scholar
  27. Jahnsen R, Villien L, Egeland T, Stanghelle JK, Holm I (2004) Locomotion skills in adults with cerebral palsy. Clin Rehabil 18:309–316CrossRefGoogle Scholar
  28. Jensen P, Jensen NJ, Terkildsen CU, Choi JT, Nielsen JB, Geertsen SS (2018) Increased central common drive to ankle plantar flexor and dorsiflexor muscles during visually guided gait. Physiol Rep 6(3):e13598.  https://doi.org/10.14814/phy2.13598 CrossRefGoogle Scholar
  29. Lloyd DP (1951) After-currents, after-potentials, excitability, and ventral root electrotonus in spinal motoneurons. J Gen Physiol 35:289–321CrossRefGoogle Scholar
  30. Lundh S, Nasic S, Riad J (2018) Fatigue, quality of life and walking ability in adults with cerebral palsy. Gait Posture 61:1–6CrossRefGoogle Scholar
  31. Lunenburger L, Colombo G, Riener R, Dietz V (2004) Biofeedback in gait training with the robotic orthosis Lokomat. Conf Proc IEEE Eng Med Biol Soc 7:4888–4891Google Scholar
  32. Morgan P, McGinley J (2014) Gait function and decline in adults with cerebral palsy: a systematic review. Disabil Rehabil 36:1–9CrossRefGoogle Scholar
  33. Morgan P, Murphy A, Opheim A, McGinley J (2016) Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy: an observational study. Gait Posture 48:243–248CrossRefGoogle Scholar
  34. Neptune RR, Kautz SA, Zajac FE (2001) Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. J Biomech 34:1387–1398CrossRefGoogle Scholar
  35. Nielsen JB (2002) Motoneuronal drive during human walking. Brain Res Brain Res Rev 40:192–201CrossRefGoogle Scholar
  36. Nielsen JB (2003) How we walk: central control of muscle activity during human walking. Neuroscientist 9:195–204CrossRefGoogle Scholar
  37. Nielsen J, Petersen N (1995) Changes in the effect of magnetic brain stimulation accompanying voluntary dynamic contraction in man. J Physiol 484:777–789CrossRefGoogle Scholar
  38. Olney SJ, MacPhail HE, Hedden DM, Boyce WF (1990) Work and power in hemiplegic cerebral palsy gait. Phys Ther 70:431–438CrossRefGoogle Scholar
  39. Palmer JA, Hsiao H, Awad LN, Binder-Macleod SA (2016) Symmetry of corticomotor input to plantarflexors influences the propulsive strategy used to increase walking speed post-stroke. Clin Neurophysiol 127:1837–1844CrossRefGoogle Scholar
  40. Palmer JA, Zarzycki R, Morton SM, Kesar TM, Binder-Macleod SA (2017) Characterizing differential poststroke corticomotor drive to the dorsi- and plantarflexor muscles during resting and volitional muscle activation. J Neurophysiol 117:1615–1624CrossRefGoogle Scholar
  41. Parvin S, Taghiloo A, Irani A, Mirbagheri MM (2017) Therapeutic effects of anti-gravity treadmill (AlterG) training on reflex hyper-excitability, corticospinal tract activities, and muscle stiffness in children with cerebral palsy. IEEE Int Conf Rehabil Robot 2017:485–490Google Scholar
  42. Perez MA, Cohen LG (2009) The corticospinal system and transcranial magnetic stimulation in stroke. Top Stroke Rehabil 16:254–269CrossRefGoogle Scholar
  43. Petersen N, Christensen LO, Nielsen J (1998) The effect of transcranial magnetic stimulation on the soleus H reflex during human walking. J Physiol 513:599–610CrossRefGoogle Scholar
  44. Petersen NT, Butler JE, Marchand-Pauvert V, Fisher R, Ledebt A, Pyndt HS, Hansen NL, Nielsen JB (2001) Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J Physiol 537:651–656CrossRefGoogle Scholar
  45. Petersen NT, Pyndt HS, Nielsen JB (2003) Investigating human motor control by transcranial magnetic stimulation. Exp Brain Res 152:1–16CrossRefGoogle Scholar
  46. Petersen TH, Willerslev-Olsen M, Conway BA, Nielsen JB (2012) The motor cortex drives the muscles during walking in human subjects. J Physiol 590:2443–2452CrossRefGoogle Scholar
  47. Petersen TH, Farmer SF, Kliim-Due M, Nielsen JB (2013) Failure of normal development of central drive to ankle dorsiflexors relates to gait deficits in children with cerebral palsy. J Neurophysiol 109:625–639CrossRefGoogle Scholar
  48. Renshaw B (1941) Influence of discharge of motoneurons upon excitation of neighboring motoneurons. J Neurophysiol 4:167–183CrossRefGoogle Scholar
  49. Riad J, Modlesky CM, Gutierrez-Farewik EM, Brostrom E (2012) Are muscle volume differences related to concentric muscle work during walking in spastic hemiplegic cerebral palsy? Clin Orthop Relat Res 470:1278–1285CrossRefGoogle Scholar
  50. Roche N, Pradon D, Cosson J, Robertson J, Marchiori C, Zory R (2014) Categorization of gait patterns in adults with cerebral palsy: a clustering approach. Gait Posture 39:235–240CrossRefGoogle Scholar
  51. Schubert M, Curt A, Jensen L, Dietz V (1997) Corticospinal input in human gait: modulation of magnetically evoked motor responses. Exp Brain Res 115:234–246CrossRefGoogle Scholar
  52. Schubert M, Curt A, Colombo G, Berger W, Dietz V (1999) Voluntary control of human gait: conditioning of magnetically evoked motor responses in a precision stepping task. Exp Brain Res 126:583–588CrossRefGoogle Scholar
  53. Verschuren O, Smorenburg ARP, Luiking Y, Bell K, Barber L, Peterson MD (2018) Determinants of muscle preservation in individuals with cerebral palsy across the lifespan: a narrative review of the literature. J Cachexia Sarcopenia Muscle 9:453–464CrossRefGoogle Scholar
  54. Vry J, Linder-Lucht M, Berweck S, Bonati U, Hodapp M, Uhl M, Faist M, Mall V (2008) Altered cortical inhibitory function in children with spastic diplegia: a TMS study. Exp Brain Res 186:611–618CrossRefGoogle Scholar
  55. Willerslev-Olsen M, Andersen JB, Sinkjaer T, Nielsen JB (2014) Sensory feedback to ankle plantar flexors is not exaggerated during gait in spastic hemiplegic children with cerebral palsy. J Neurophysiol 111:746–754CrossRefGoogle Scholar
  56. Willerslev-Olsen M, Petersen TH, Farmer SF, Nielsen JB (2015) Gait training facilitates central drive to ankle dorsiflexors in children with cerebral palsy. Brain 138:589–603CrossRefGoogle Scholar
  57. Winters TF Jr, Gage JR, Hicks R (1987) Gait patterns in spastic hemiplegia in children and young adults. J Bone Jt Surg Am 69:437–441CrossRefGoogle Scholar
  58. Zewdie E, Damji O, Ciechanski P, Seeger T, Kirton A (2017) Contralesional corticomotor neurophysiology in hemiparetic children with perinatal stroke. Neurorehabil Neural Repair 31:261–271CrossRefGoogle Scholar
  59. Zuur AT (2013) Human locomotion and the motor cortex: drive to the motoneuron and the role of afferent input. PhD Thesis, Aalborg UniversityGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of NeuroscienceUniversity of CopenhagenCopenhagen NDenmark
  2. 2.Professionshøjskolen AbsalonRoskildeDenmark
  3. 3.Elsass InstituteCharlottenlundDenmark

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