Repetitive activation of the corticospinal pathway by means of rTMS may reduce the efficiency of corticomotoneuronal synapses

Cerebral Cortex

Volumn 25, Issue 6, 2015, Pages 1629-1637

  Taube, Wolfgang ^a   Leukel, Christian ^a,b   Nielsen, Jens Bo ^c,d   Lundbye Jensen, Jesper ^c,d  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

^c Exercise and Sports ^*  (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

corticospinal tract; H reflex conditioning; synaptic plasticity

Indexed keywords

ADULT; ALPHA NERVE FIBER; ARTICLE; CORTICOMOTONEURONAL SYNAPSE; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; HUMAN; NERVE CELL PLASTICITY; NERVE STIMULATION; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL TRACT; SOLEUS MUSCLE; SYNAPTIC TRANSMISSION; TRANSCRANIAL MAGNETIC STIMULATION; ANALYSIS OF VARIANCE; BIOPHYSICS; ELECTROSTIMULATION; FEMALE; HOFFMANN REFLEX; MALE; MOTONEURON; NEUROPHYSIOLOGICAL RECRUITMENT; PERIPHERAL NERVE; PHYSIOLOGY; SYNAPSE; YOUNG ADULT;

ADULT; ANALYSIS OF VARIANCE; BIOPHYSICS; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; H-REFLEX; HUMANS; MALE; MOTOR NEURONS; PERIPHERAL NERVES; PYRAMIDAL TRACTS; RECRUITMENT, NEUROPHYSIOLOGICAL; SYNAPSES; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84930365556     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht359     Document Type: Article

References (43)

1. Berardelli A, Inghilleri M, Rothwell JC, Romeo S, Curra A, Gilio F, Modugno N, Manfredi M. 1998. Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp Brain Res. 122:79-84.
2. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. 2003. Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage. 20:1685-1696.
3. Centonze D, Koch G, Versace V, Mori F, Rossi S, Brusa L, Grossi K, Torelli F, Prosperetti C, Cervellino A et al. 2007. Repetitive transcranial magnetic stimulation of the motor cortex ameliorates spasticity in multiple sclerosis. Neurology. 68:1045-1050.
4. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG. 1997. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 48: 1398-1403.
5. Conchou F, Loubinoux I, Castel-Lacanal E, Le TA, Gerdelat-Mas A, Faure-Marie N, Gros H, Thalamas C, Calvas F, Berry I et al. 2009. Neural substrates of low-frequency repetitive transcranial magnetic stimulation during movement in healthy subjects and acute stroke patients. A PET study. Hum Brain Mapp. 30:2542-2557.
6. Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-Deseilligny E. 1990. Sensitivity of monosynaptic test reflexes to facilitation and inhibition as a function of the test reflex size: a study in man and the cat. Exp Brain Res. 81:35-45.
7. Davidson AG, Chan V, O'Dell R, Schieber MH. 2007. Rapid changes in throughput from single motor cortex neurons to muscle activity. Science. 318:1934-1937.
8. Di Lazzaro V, Pilato F, Dileone M, Profice P, Oliviero A, Mazzone P, Insola A, Ranieri F, Tonali PA, Rothwell JC. 2008. Low-frequency repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol. 586: 4481-4487.
9. Di Lazzaro V, Profice P, Pilato F, Dileone M, Oliviero A, Ziemann U. 2010. The effects of motor cortex rTMS on corticospinal descending activity. Clin Neurophysiol. 121:464-473.
10. Fitzgerald PB, Brown TL, Daskalakis ZJ, Chen R, Kulkarni J. 2002. Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol. 113:1136-1141.
11. Fitzgerald PB, Fountain S, Daskalakis ZJ. 2006. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol. 117:2584-2596.
12. Funke K, Benali A. 2011. Modulation of cortical inhibition by rTMS - findings obtained from animal models. J Physiol. 589: 4423-4435.
13. Hallett M. 2007. Transcranial magnetic stimulation: a primer. Neuron. 55:187-199.
14. Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J. 2009. Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol. 120:2040-2054.
15. Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H. 2001. Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin Neurophysiol. 112:250-258.
16. Leukel C, Taube W, Beck S, Schubert M. 2012. Pathway-specific plasticity in the human spinal cord. Eur J Neurosci. 35:1622-1629.
17. Lundbye-Jensen J, Petersen TH, Rothwell JC, Nielsen JB. 2011. Interference in ballistic motor learning: specificity and role of sensory error signals. PLoS One. 6:e17451.
18. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. 2000. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res. 133:425-430.
19. Nielsen J, Petersen N. 1994. Is presynaptic inhibition distributed to corticospinal fibres in man? J Physiol. 477:47-58.
20. Nielsen J, Petersen N. 1995a. Changes in the effect of magnetic brain stimulation accompanying voluntary dynamic contraction in man. J Physiol. 484:777-789.
21. Nielsen J, Petersen N. 1995b. Evidence favouring different descending pathways to soleus motoneurones activated by magnetic brain stimulation in man. J Physiol. 486:779-788.
22. Nielsen J, Petersen N, Ballegaard M. 1995. Latency of effects evoked by electrical and magnetic brain stimulation in lower limb motoneurones in man. J Physiol. 484:791-802.
23. 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.
24. Nitsche MA, Paulus W. 2000. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 527(Pt 3):633-639.
25. Oya T, Hoffman BW, Cresswell AG. 2008. Corticospinal-evoked responses in lower limb muscles during voluntary contractions at varying strengths. J Appl Physiol. 105:1527-1532.
26. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. 1994. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 117(Pt 4):847-858.
27. Perez MA, Lungholt BK, Nielsen JB. 2005. Short-term adaptations in spinal cord circuits evoked by repetitive transcranial magnetic stimulation: possible underlying mechanisms. Exp Brain Res. 162:202-212.
28. Petersen N, Christensen LOD, Nielsen JB. 1998. The effect of transcranial magnetic stimulation on the soleus H reflex during human walking. J Physiol. 513:599-610.
29. 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.
30. Porter R, Lemon RN. 1993. Corticospinal function and voluntary movement. Monographs of the Physiological Society, No. 45. New York: Oxford University Press.
31. Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD. 2000. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res. 131:135-143.
32. Rudomin P, Nunez R, Madrid J. 1975. Modulation of synaptic effectiveness of Ia and descending fibers in cat spinal cord. J Neurophysiol. 38:1181-1195.
33. Schubert M, Beck S, Taube W, Amtage F, Faist M, Gruber M. 2008. Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci. 27:2007-2018.
34. Sommer M, Alfaro A, Rummel M, Speck S, Lang N, Tings T, Paulus W. 2006. Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin Neurophysiol. 117:838-844.
35. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. 2000. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 123(Pt 3):572-584.
36. Taube W, Gruber M, Beck S, Faist M, Gollhofer A, Schubert M. 2007. Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation. Acta Physiol (Oxf). 189:347-358.
37. Taube W, Lundbye-Jensen J, Schubert M, Gollhofer A, Leukel C. 2011. Evidence that the cortical motor command for the initiation of dynamic plantarflexion consists of excitation followed by inhibition. PLoS One. 6:e25657.
38. Taube W, Schubert M, Gruber M, Beck S, Faist M, Gollhofer A. 2006. Direct corticospinal pathways contribute to neuromuscular control of perturbed stance. J Appl Physiol. 101:420-429.
39. Taylor JL. 2006. Stimulation at the cervicomedullary junction in human subjects. J Electromyogr Kinesiol. 16:215-223.
40. Taylor JL, Martin PG. 2009. Voluntary motor output is altered by spike-timing-dependent changes in the human corticospinal pathway. J Neurosci. 29:11708-11716.
41. Tsuji T, Rothwell JC. 2002. Long lasting effects of rTMS and associated peripheral sensory input on MEPs, SEPs and transcortical reflex excitability in humans. J Physiol. 540:367-376.
42. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. 1994. Magnetic stimulation of corticospinal pathways at the foramen magnum level in humans. Ann Neurol. 36:618-624.
43. Valero-Cabré A, Oliveri M, Gangitano M, Pascual-Leone A. 2001. Modulation of spinal cord excitability by subthreshold repetitive transcranial magnetic stimulation of the primary motor cortex in humans. Neuroreport. 12:3845-3848.