Abstract
Force field adaptation of locomotor muscle activity is one way of studying the ability of the motor control networks in the brain and spinal cord to adapt in a flexible way to changes in the environment. Here, we investigate whether the corticospinal tract is involved in this adaptation. We measured changes in motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) in the tibialis anterior (TA) muscle before, during, and after subjects adapted to a force field applied to the ankle joint during treadmill walking. When the force field assisted dorsiflexion during the swing phase of the step cycle, subjects adapted by decreasing TA EMG activity. In contrast, when the force field resisted dorsiflexion, they increased TA EMG activity. After the force field was removed, normal EMG activity gradually returned over the next 5 min of walking. TA MEPs elicited in the early swing phase of the step cycle were smaller during adaptation to the assistive force field and larger during adaptation to the resistive force field. When elicited 5 min after the force field was removed, MEPs returned to their original values. The changes in TA MEPs were larger than what could be explained by changes in background TA EMG activity. These effects seemed specific to walking, as similar changes in TA MEP were not seen when seated subjects were tested during static dorsiflexion. These observations suggest that the corticospinal tract contributes to the adaptation of walking to an external force field.
This is a preview of subscription content,
to check access.









References
Alain S, Cantin B, Bouyer LJ (2005) Human cutaneous reflexes while walking in an elastic force field applied to the ankle. Soc Neurosci Abstr 864.12
Alain S, Barthelemy D, Grey MJ, Bouyer LJ, Richards CL, Nielsen JB (2007) Rapid, task-specific modifications of cortico-spinal excitability during adaptation of human locomotion to elastic force fields applied to the ankle. Soc Neurosci Abstr 924.1
Amos A, Armstrong DM, Marple-Horvat DE (1989) Responses of motor cortical neurones in the cat to unexpected perturbations of locomotion. Neurosci Lett 104:147–151
Armstrong DM, Marple-Horvat DE (1996) Role of the cerebellum and motor cortex in the regulation of visually controlled locomotion. Can J Physiol Pharmacol 74:443–455
Barsi GI, Popovic DB, Tarkka IM, Sinkjaer T, Grey MJ (2008) Cortical excitability changes following grasping exercise augmented with electrical stimulation. Exp Brain Res 191:57–66
Blanchette A, Bouyer LJ (2009) Timing-specific transfer of adapted muscle activity after walking in an elastic force field. J Neurophysiol 102:568–577
Bouyer LJ (2011) Challenging the adaptive capacity of rhythmic movement control: from denervation to force field adaptation. Prog Brain Res 188:119–134
Bouyer L, Rossignol S (2001) Spinal cord plasticity associated with locomotor compensation to peripheral nerve lesions in the cat. In: Patterson MM, Grau JW (eds) Spinal cord plasticity: Alterations in reflex function. Kluwer Academic Publishers, Boston, pp 207–224
Bouyer LJ, Rossignol S (2003a) Contribution of cutaneous inputs from the hindpaw to the control of locomotion. I. Intact cats. J Neurophysiol 90:3625–3639
Bouyer LJ, Rossignol S (2003b) Contribution of cutaneous inputs from the hindpaw to the control of locomotion. II. Spinal cats. J Neurophysiol 90:3640–3653
Bouyer LJ, Whelan PJ, Pearson KG, Rossignol S (2001) Adaptive locomotor plasticity in chronic spinal cats after ankle extensors neurectomy. J Neurosci 21:3531–3541
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 81:129–139
Carrier L, Brustein E, Rossignol S (1997) Locomotion of the hindlimbs after neurectomy of ankle flexors in intact and spinal cats: model for the study of locomotor plasticity. J Neurophysiol 77:1979–1993
Choi JT, Bastian AJ (2007) Adaptation reveals independent control networks for human walking. Nat Neurosci 10:1055–1062
Christensen LO, Morita H, Petersen N, Nielsen J (1999) Evidence suggesting that a transcortical reflex pathway contributes to cutaneous reflexes in the tibialis anterior muscle during walking in man. Exp Brain Res 124:59–68
Christensen LO, Andersen JB, Sinkjaer T, Nielsen J (2001) Transcranial magnetic stimulation and stretch reflexes in the tibialis anterior muscle during human walking. J Physiol 531:545–557
Cote MP, Gossard JP (2004) Step training-dependent plasticity in spinal cutaneous pathways. J Neuro sci 24:11317–11327
Cumming G, Finch S (2005) Inference by eye: confidence intervals and how to read pictures of data. Am Psychol 60:170–180
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 537:1047–1058
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 74:426–442
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 40:178–191
Drew T, Kalaska J, Krouchev N (2008) Muscle synergies during locomotion in the cat: a model for motor cortex control. J Physiol 586:1239–1245
Duysens J, Tax AA, Trippel M, Dietz V (1992) Phase-dependent reversal of reflexly induced movements during human gait. Exp Brain Res 90:404–414
Edgerton VR, Tillakaratne NJ, Bigbee AJ, De Leon RD, Roy RR (2004) Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci 27:145–167
Emken JL, Reinkensmeyer DJ (2005) Robot-enhanced motor learning: accelerating internal model formation during locomotion by transient dynamic amplification. IEEE Trans Neural Syst Rehabil Eng 13:33–39
Faist M, Hoefer C, Hodapp M, Dietz V, Berger W, Duysens J (2006) In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading. Brain Res 1076:87–92
Fortin K, Blanchette A, McFadyen BJ, Bouyer LJ (2009) Effects of walking in a force field for varying durations on after effects and on next day performance. Exp Brain Res 199:145–155
Graham-Brown T (1911) The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond B Biol Sci 84:308–319
Grillner S, Wallen P (1985) Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci 8:233–261
Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374
Hultborn H, Nielsen JB (2007) Spinal control of locomotion–from cat to man. Acta Physiol (Oxf) 189:111–121
Jayaram G, Galea JM, Bastian AJ, Celnik P (2011) Human locomotor adaptive learning is proportional to depression of cerebellar excitability. Cereb Cortex. [Epub ahead of print]
Kernell D, Hultborn H (1990) Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507:176–179
Lackner JR, Dizio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313
Lam T, Anderschitz M, Dietz V (2006) Contribution of feedback and feedforward strategies to locomotor adaptations. J Neurophysiol 95:766–773
Loftus GR, Masson MEJ (1994) Using confidence intervals in within-subject designs. Psych Bull Review 1:476–490
Malone LA, Bastian AJ (2010) Thinking about walking: effects of conscious correction versus distraction on locomotor adaptation. J Neurophysiol 103(4):1954–1962
Marchand-Pauvert V, Nielsen JB (2002a) Modulation of heteronymous reflexes from ankle dorsiflexors to hamstring muscles during human walking. Exp Brain Res 142:402–408
Marchand-Pauvert V, Nielsen JB (2002b) Modulation of non-monosynaptic excitation from ankle dorsiflexor afferents to quadriceps motoneurones during human walking. J Physiol 538:647–657
Masson MEJ, Loftus GR (2003) Using confidence intervals for graphically based data interpretation. Can J Exp Psych 57:203–220
Matthews PB (1999) The effect of firing on the excitability of a model motoneurone and its implications for cortical stimulation. J Physiol 518(Pt 3):867–882
McNeil CJ, Martin PG, Gandevia SC, Taylor JL (2009) The response to paired motor cortical stimuli is abolished at a spinal level during human muscle fatigue. J Physiol 587:5601–5612
Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26:9107–9116
Muir GD, Steeves JD (1995) Phasic cutaneous input facilitates locomotor recovery after incomplete spinal injury in the chick. J Neurophysiol 74:358–368
Nielsen JB (2003) How we walk: central control of muscle activity during human walking. Neuroscientist 9:195–204
Nielsen JB, Cohen LG (2008) The olympic brain. Does corticospinal plasticity play a role in acquisition of skills required for high-performance sports? J Physiol 586:65–70
Nielsen J, Petersen N (1995) Evidence favouring different descending pathways to soleus motoneurones activated by magnetic brain stimulation in man. J Physiol 486(Pt 3):779–788
Nielsen J, Petersen N, Deuschl G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471:223–243
Nielsen J, Petersen N, Fedirchuk B (1997) Evidence suggesting a transcortical pathway from cutaneous foot afferents to tibialis anterior motoneurones in man. J Physiol 501(Pt 2):473–484
Noble JW, Prentice SD (2006) Adaptation to unilateral change in lower limb mechanical properties during human walking. Exp Brain Res 169:482–495
Noel M, Fortin K, Bouyer LJ (2009) Using an electrohydraulic ankle foot orthosis to study modifications in feedforward control during locomotor adaptation to force fields applied in stance. J Neuroeng Rehabil 6:16–17
Pearson KG (2000) Neural adaptation in the generation of rhythmic behavior. AnnuRevPhysiol 62:723–753
Perez MA, Lungholt BK, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205
Petersen N, Christensen LO, Morita H, Sinkjaer T, Nielsen J (1998) Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man. J Physiol 512(Pt 1):267–276
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 537:651–656
Petersen NT, Taylor JL, Butler JE, Gandevia SC (2003) Depression of activity in the corticospinal pathway during human motor behavior after strong voluntary contractions. J Neurosci 23:7974–7980
Pierrot-Deseilligny E (2002) Propriospinal transmission of part of the corticospinal excitation in humans. Muscle Nerve 26:155–172
Press WH (1986) Numerical recipes: the art of scientific computing. Cambridge University Press, New York
Reisman DS, Wityk R, Silver K, Bastian AJ (2007) Locomotor adaptation on a split-belt treadmill can improve walking symmetry post-stroke. Brain 130:1861–1872
Rossignol S, Brustein E, Bouyer L, Barthelemy D, Langlet C, Leblond H (2004) Adaptive changes of locomotion after central and peripheral lesions. Can J Physiol Pharmacol 82:617–627
Rossignol S, Barriere G, Frigon A, Barthelemy D, Bouyer L, Provencher J, Leblond H, Bernard G (2008) Plasticity of locomotor sensorimotor interactions after peripheral and/or spinal lesions. Brain Res Rev 57:228–240
Sawicki GS, Domingo A, Ferris DP (2006) The effects of powered ankle-foot orthoses on joint kinematics and muscle activation during walking in individuals with incomplete spinal cord injury. J Neuroeng Rehabil 3:3–4
Schneider C, Lavoie BA, Barbeau H, Capaday C (2004) Timing of cortical excitability changes during the reaction time of movements superimposed on tonic motor activity. J Appl Physiol 97:2220–2227
Schubert M, Curt A, Jensen L, Dietz V (1997) Corticospinal input of human gait: modulation of magnetically evoked motor responses. Exp Brain Res 115:234–246
Shadmehr R, Holcomb HH (1997) Neural correlates of motor memory consolidation. Science 277:821–825
Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224
Sherrington CS (1906) The integrative action of the nervous system. Charles Scribner’s Sons, New York
Sinkjaer T, Andersen JB, Ladouceur M, Christensen LO, Nielsen JB (2000) Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol 523(3):817–827
Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19:8573–8588
Whelan PJ, Pearson KG (1997) Plasticity in reflex pathways controlling stepping in the cat. JNeurophysiol 78:1643–1650
Widajewicz W, Kably B, Drew T (1994) Motor cortical activity during voluntary gait modifications in the cat. II. Cells related to the hindlimbs. J Neurophysiol 72:2070–2089
Yang JF, Stein RB (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117
Zuur AT, Christensen MS, Sinkjaer T, Grey MJ, Nielsen JB (2009) Tibialis anterior stretch reflex in early stance is suppressed by repetitive transcranial magnetic stimulation. J Physiol 587:1669–1676
Acknowledgments
This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). DB received a Post-Doctoral Fellowship from the Canadian Institutes of Health Research (CIHR).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Barthélemy, D., Alain, S., Grey, M.J. et al. Rapid changes in corticospinal excitability during force field adaptation of human walking. Exp Brain Res 217, 99–115 (2012). https://doi.org/10.1007/s00221-011-2977-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-011-2977-4