Abstract
Objectives
To improve the diagnosis of damaged spinal motor pathways in incomplete spinal cord injury (iSCI) by assessing the facilitation of lower limbs motor evoked potentials (MEP).
Methods
Control subjects (n = 12) and iSCI patients (n = 21) performed static and dynamic isometric foot dorsiflexions. MEPs induced by transcranial magnetic stimulation and EMG background of tibialis anterior muscle (TA) were analyzed. Static and dynamic muscle activation was performed at comparable levels of maximal voluntary contraction (MVC). The influence of the motor tasks on the excitability and facilitation of MEPs was compared between controls and iSCI patients.
Results
In the controls an increased facilitation of TA MEP at lower levels of dynamic compared with static activation (10–20% MVC) could be shown. At matched EMG background level the MEP responses were significantly increased. In the iSCI patients at a comparable level of TA activation the MEP responses were significantly reduced and 3 different patterns of MEP responses could be distinguished: i) preserved increment of TA MEP in the dynamic motor task, ii) unchanged MEP size in the dynamic and static motor task, and iii) elicitable MEPs in the dynamic motor task,which were abolished in the static motor task.
Conclusions
Static and dynamic motor tasks have different effects on TA MEP facilitation. The task–dependent modulation of TA MEPs is comparable to that described for upper limb muscles. Complementary to the MEP delay this approach allows for an estimation of the severity of spinal tract damage. The task–dependent modulation of TA MEPs is an additional diagnostic tool to improve the assessment and monitoring of motor function in iSCI.
Similar content being viewed by others
References
Aranyi Z, Mathis J, Hess CW, Rosler KM (1998) Task–dependent facilitation of motor evoked potentials during dynamic and steady muscle contractions. Muscle Nerve 21(10):1309–1316
Bawa P, Chalmers GR, Stewart H, Eisen AA (2002) Responses of ankle extensor and flexor motoneurones to transcranial magnetic stimulation. J Neurophysiol 88(1):124–132
Brouwer B, Ashby P, Midroni G (1989) Excitability of corticospinal neurons during tonic muscle contractions in man. Exp Brain Res 74(3):649–652
Buhler R, Magistris MR, Treffert A, Hess CW, Rosler KM (2001) The triple stimulation technique to study central motor conduction to the lower limbs. Clin Neurophysiol 112(5):938–949
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(1):129–139
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(2):545–557
Clamann HP (1993) Motor unit recruitment and the gradation of muscle force. Phys Ther 73(12):830–843
Claus D, Weis M, Spitzer A (1991) Motor potentials evoked in tibialis anterior by single and paired cervical stimuli in man. Neurosci Lett 125(2):198–200
Curt A, Keck ME, Dietz V (1998) Functional outcome following spinal cord injury: Significance of motor–evoked potentials. Arch Phys Med Rehab 79:81–86
de Noordhout AM, Pepin JL, Gerard P, Delwaide PJ (1992) Facilitation of responses to motor cortex stimulation: effects of isometric voluntary contraction. Ann Neurol 32(3):365–370
de Noordhout AM, Rapisarda G, Bogacz D, Gerard P, De Pasqua V, Pennisi G, Delawaide PJ (1999) Corticomotoneuronal synaptic connections in normal man: an electrophysiological study. Brain 122:1327–1340
Di Lazzaro V, Oliviero A, Proficue P, Insola A, Mazzone P, Tonali P, Rothwell JC (1999) Effects of voluntary contraction on descending volleys evoked by transcranial electrical stimulation over the motor cortex hand area in conscious humans. Exp Brain Res 124:525–528
Di Lazzaro V, Oliviero A, Profice P, Ferrara L, Saturno E, Pilato F, Tonali P (1999) The diagnostic value of motor evoked potentials. Clin Neurophysiol 110(7):1297–1307
Ellaway PH, Davey NJ, Maskill DW, Rawlinson SR, Lewis HS, Anissimova NP (1998) Variability in the amplitude of skeletal muscle responses to magnetic stimulation of the motor cortex in man. Electroencephalogr Clin Neurophysiol 109(2):104–113
Enoka RM (1995) Morphological features and activation patterns of motor units. J Clin Neurophysiol 12(6):538–559
Flament D, Goldsmith P, Buckley CJ, Lemon RN (1993) Task dependence of responses in first dorsal interosseus muscle to magnetic brain stimulation in man. J Physiol 464:361–378
Funase K, Miles TS, Gooden BR (1999) Trial–to–trial fluctuations in H–reflexes and motor evoked potentials in human wrist flexors. Neurosci Lett 271(1):25–28
Hasegawa Y, Kasai T, Tsuji T, Yahagi S (2001) Further insight into the taskdependent excitability of motor evoked potentials in first dorsal interosseus muscle in humans. Exp Brain Res 140(4):387–396
Hess CW, Mills KR, Murray NM (1987) Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol 388:397–419
Humm AM, Z’Graggen WJ, von Hornstein NE, Magistris MR, Rosler KM (2004) Assessment of central motor conduction to intrinsic hand muscles using the triple stimulation technique: normal values and repeatability. Clin Neurophysiol 115(11):2558–2566
Jones KE, Lyons M, Bawa P, Lemon RN (1994) Recruitment order of motoneurons during functional tasks. Exp Brain Res 100(3):503–508
Kasai T, Kawai S, Kawanishi M, Yohagi S (1997) Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery. Brain Res 744(1):147–150
Keck ME, Pijnappels M, Schubert M, Colombo G, Curt A, Dietz V (1998) Stumbling reactions in man: influence of corticospinal input. Electroencephalogr Clin Neurophysiol 109(3):215–223
Kiers L, Cros D, Chiappa KH, Fang J (1993) Variability of motor potentials evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 89(6):415–423
Kimura T, Yamanaka K, Nozaki D, Nakazawa K, Miyoshi T, Akai M, Ohtsuki T (2003) Hysteresis in corticospinal excitability during gradual muscle contraction and relaxation in humans. Exp Brain Res 152:123–132
Kischka U, Fajfr R, Fellenberg T, Hess CW (1993) Facilitation of motor evoked potentials from magnetic brain stimulation in man: a comparative study of different target muscles. J Clin Neurophysiol 10(4):505–512
Lentz M, Nielsen JF (2002) Post–exercise– facilitation and depression of M wave and motor evoked potentials in healthy subjects. Clin Neurophysiol 113(7):1092–1098
Magistris MR, Rosler KM, Truffert A, Landis T, Hess CW (1999) A clinical study of motor evoqued potentials using a triple stimulation technique. Brain 122 (2):265–279
Maton B (1980) Fast and slow motor units: their recruitment for tonic and phasic contraction in normal man. Eur J Appl Physiol Occup Physiol 43(1):45–55
Maynard FM Jr, Bracken MB, Crearey G, Ditunno JF Jr, Donovan WH, Ducke TB (1997) International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 35:266–274
Mills KR, Kimiskidis V (1996) Cortical and spinal mechanisms of facilitation to brain stimulation. Muscle Nerve 19(8):953–958
Nielsen J, Petersen N (1995) Evidence favouring different descending pathways to soleus motoneurones activated by magnetic brain stimulation in man. J Physiol 486(3):779–788
Palmer E, Ashby P (1992) Corticospinal projections to upper limb motoneurones in humans. J Physiol 448:397–412
Romaiguere P, Vedel JP, Pagni S (1989) Fluctuations in motor unit recruitment threshold during slow isometric contractions of wrist extensor muscles in man. Neurosci Lett 103(1):50–55
Rossi F, Triggs WJ, Eisenschenk S (1999) Topographic differences in task–dependent facilitation of magnetic motor evoked potentials. Neurology 52(3):537–540
Rossini PM, Rossi S (1998) Clinical applications of motor evoked potentials. Electroencephalogr Clin Neurophysiol 106(3):180–194
Rothwell JC, Thompson PD, Day BL, Dick JP, Kachi T, Cowan JM, Marsden CD (1987) Motor cortex stimulation in intact man. 1. General characteristics of EMG responses in different muscles. Brain 110(5):1173–1190
Sbriccoli P, Bazzucchi I, Rosponi A, Bernardi M, De Vito G, Felici F (2003) Amplitude and spectral characteristics of biceps Brachii s EMG depend upon speed of isometric force generation. J Electromyogr Kinesiol 13(2):139–147
Schieppati M, Trompetto C, Abbruzzese G (1996) Selective facilitation of responses to cortical stimulation of proximal and distal arm muscles by precision tasks in man. J Physiol 49(12):551–562
Schubert M, Curt A, Jensen L, Dietz V (1997) Corticospinal input in human gait:Modulation of magnetically evoked motor responses. Exp Brain Res 115(2):234–246
Sogaard K (1995) Motor unit recruitment pattern during low–level static and dynamic contractions. Muscle Nerve 18(3):292–300
Thompson PD, Day BL, Rothwell JC, Dressler D, Maertens de Noordhout A, Marsden CD (1991) Further observations on the facilitation of muscle responses to cortical stimulation by voluntary contraction. Electroencephalogr Clin Neurophysiol 81(5):397–402
Turton A, Lemon RN (1999) The contribution of fast corticospinal input to the voluntary activation in normal subjects and in stroke patients. Exp Brain Res 129(4):559–572
Ugawa Y, Terao Y, Hanajima R, Sakai K, Kanazawa I (1995) Facilitatory effect of tonic voluntary contraction on responses to motor cortex stimulation. Electroencephalogr Clin Neurophysiol 97(6):451–454
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Diehl, P., Kliesch, U., Dietz, V. et al. Impaired facilitation of motor evoked potentials in incomplete spinal cord injury. J Neurol 253, 51–57 (2006). https://doi.org/10.1007/s00415-005-0921-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00415-005-0921-x