Paired associative stimulation increases motor cortex excitability more effectively than theta-burst stimulation

Clinical Neurophysiology

Volumn 123, Issue 11, 2012, Pages 2220-2226

  Player, Michael J ^a,b   Taylor, Janet L ^a,c   Alonzo, Angelo ^a,b   Loo, Colleen K ^a,b,d  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b BLACK DOG INSTITUTE   (Australia)

^c NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^d ST GEORGE HOSPITAL   (Australia)

Author keywords

Metaplasticity; Motor learning; Paired associative stimulation (PAS); Plasticity; Theta burst stimulation (TBS); Transcranial magnetic stimulation (TMS)

Indexed keywords

ARTICLE; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FEMALE; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NORMAL HUMAN; PAIRED ASSOCIATE LEARNING; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE; THETA BURST STIMULATION;

ADULT; CROSS-OVER STUDIES; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; NEURONAL PLASTICITY; THETA RHYTHM; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84867021189     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2012.03.081     Document Type: Article

References (53)

1. Abraham W.C., Bear M.F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 1996, 19:126-130.
2. Abraham W.C., Mason-Parker S.E., Bear M.F., Webb S., Tate W.P. Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP. Proc Natl Acad Sci 2001, 98:10924-10929.
3. Bienenstock E.L., Cooper L.N., Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 1982, 2:32-48.
4. Bolognini N., Pascual-Leone A., Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuro Eng Rehab 2009, 6.
5. Cárdenas-Morales L., Nowak D.A., Krammer T., Wolf R.C., Schonfeldt-Lecuouna C. Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr 2010, 22:294-306.
6. Cheeran B., Talelli P., Mori F., Koch G., Suppa A., Edwards M., et al. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol 2008, 586:5717-5725.
7. Cho K., Aggleton J.P., Brown M.W., Bashir Z.I. An experimental test of the role of postsynaptic calcium levels in determining synaptic strength using perirhinal cortex of rat. J Physiol 2001, 532:459-466.
8. Cirillo J., Lavender A.P., Ridding M.C., Semmler J.G. Motor cortex plasticity induced by paired associative stimulation is enhanced in physically active individuals. J Physiol 2009, 587:5831-5842.
9. Conte A., Gilio F., Iezzi E., Frasca V., Inghilleri M., Berardelli A. Attention influences the excitability of cortical motor areas in healthy humans. Exp Brain Res 2007, 182:109-117.
10. Delvendahl I., Jung N.H., Mainberger F., Kuhnke N.G., Cronjaeger M., Mall V. Occlusion of bidirectional plasticity by preceding low-frequency stimulation in the human motor cortex. Clin Neurophysiol 2010, 121:594-602.
11. Di Lazzaro V., Pilato F., Saturno E., Oliviero A., Dileone M., Mazzone P., et al. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 2005, 565:945-950.
12. Di Lazzaro V., Pilato F., Dileone M., Profice P., Oliviero A., Mazzone P., et al. The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 2008, 586:3871-3879.
13. Di Lazzaro V., Dileone M., Pilato F., Profice P., Oliviero A., Mazzone P., et al. Associative motor cortex plasticity: direct evidence in humans. Cereb Cortex 2009, 19:2326-2330.
14. Di Lazzaro V., Dileone M., Pilato F., Capone F., Musumeci G., Ranieri F., et al. Modulation of motor cortex neuronal networks by rTMS: comparison of local and remote effects of six different protocols of stimulation. J Neurophysiol 2011, 105:2150-2156.
15. Duman R.S., Malberg J., Thome J. Neural plasticity to stress and antidepressant treatment. Biol Psychiatry 1999, 46:1181-1191.
16. Duffau H. Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J Clin Neurosci 2006, 13:885-897.
17. Frantseva M., Fitzgerald P.B., Chen R., Moller B., Daigle M., Daskalakis Z.J. Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill leaning. Cereb Cortex 2008, 18:990-996.
18. Fratello F., Veniero D., Curcio G., Ferrara M., Marzano C., Moroni F., et al. Modulation of corticospinal excitability by paired associative stimulation: reproducibility of effects and intraindividual reliability. Clin Neurophysiol 2006, 117:2667-2674.
19. Gamboa O.L., Antal A., Laczo B., Moliadze V., Nitsche M.A., Paulus W. Impact of repetitive theta burst stimulation on motor cortex excitability. Brain Stimulat 2011, 4:145-151.
20. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45:201-206.
21. Huang Y.Z., Chen R.S., Rothwell J.C., Wen H.Y. The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 2007, 118:1028-1032.
22. Huang Y.Z., Rothwell J.C., Edwards M.J., Chen R.S. Effects of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 2008, 18:563-570.
23. Huang Y.Z., Rothwell J.C., Chin-Song L., Wen-Li C., Wey-Li L., Chen R.S. Reversal of plasticity-like effects in the human motor cortex. J Physiol 2010, 588:3683-3693.
24. Iezzi E., Conte A., Suppa A., Agostino R., Dinapoli L., Scontrini A., et al. Phasic voluntary movements reverse the aftereffects of subsequent theta-burst stimulation in humans. J Neurophysiol 2008, 100:2070-2076.
25. Ilić N.V., Sajić J., MiŠković M., Krstić J., Milanović S., Vesović-Potić V., et al. The efficacy of two protocols for inducing motor cortex plasticity in healthy humans - TMS study. Gen Physiol Biophys 2009, 28:228-234.
26. Iyer M.B., Schleper N., Wassermann E.M. Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J Neurosci 2003, 23:10867-10872.
27. Johnston M. Clinical disorders of brain plasticity. Brain Dev 2004, 26:73-80.
28. Kurijai K., Kurijai T., Sinkjaer T., Rothwell J.C. Associative plasticity in the human motor cortex during voluntary muscle contraction. J Neurophysiol 2006, 96:1337-1346.
29. Lang N., Siebner H.R., Ernst D., Nitsche M.A., Paulus W., Lemon R.N., Rothwell J.C. Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biol Psychiatry 2004, 56:634-639.
30. Lisman J.E. Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J Physiol 2001, 532:285.
31. Li Voti P., Conte A., Suppa A., Iezzi E., Bologna M., Aniello M.S., et al. Correlation between cortical plasticity, motor learning and BDNF genotype in healthy subjects. Exp Brain Res 2011, 212:91-99.
32. Müller J.F., Orekhov Y., Liu Y., Ziemann U. Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation. Eur J Neurosci 2007, 25:3461-3468.
33. Müller-Dahlhaus J.F., Orekhov Y., Liu Y., Ziemann U. Interindividual variability and age-dependency of motor cortical plasticity induced by paired associative stimulation. Exp Brain Res 2008, 187:467-475.
34. Nitsche M.A., Roth A., Kuo M.-F., Fisher A.K., Liebetanz D., Lang N., et al. Timing-dependent modulation of associative plasticity by general network excitability in the human motor cortex. J Neurosci 2007, 27:3807-3812.
35. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
36. Paulus W., Classen J., Cohen L.G., Large C.H., Di Lazzaro V., Nitsche M., et al. State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimulat 2008, 1:151-163.
37. Pötter-Nerger M., Fischer S., Mastroeni C., Groppa S., Deuschl G., Volkmann J., et al. Inducing homeostatic-like plasticity in human motor cortex through converging cortico-cortical inputs. J Neurophysiol 2009, 102:3180-3190.
38. Quartarone A., Bagnato S., Rizzo V., Morgante F., Sant'Angelo A., Battaglia F. Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex. Exp Brain Res 2005, 161:114-124.
39. Ridding M.C., Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 2010, 588:2291-2304.
40. Rosenkranz K., Rothwell J.C. Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex. Eur J Neurosci 2006, 23:822-829.
41. Sale M.V., Ridding M.C., Nordstrom M.A. Factors influencing the magnitude and reproducibility of corticomotor excitability changes induced by paired associative stimulation. Exp Brain Res 2007, 181:615-624.
42. Sale M.V., Ridding M.C., Nordstrom M.A. Cortisol inhibits neuroplasticity induction in human motor cortex. J Neurosci 2008, 2:8285-8293.
43. Stefan K., Kunesch E., Cohen L.G., Benecke R., Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000, 123:572-584.
44. Stefan K., Kunesch E., Benecke R., Cohen L.G., Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 2002, 543:699-708.
45. Stefan K., Wycislo M., Classen J. Modulation of associative human motor cortical plasticity by attention. J Neurophysiol 2004, 92:66-72.
46. Teo J.T.H., Swayne O.B., Rothwell J.C. Further evidence for NMDA-dependence of the aftereffects of human theta burst stimulation. Clin Neurophysiol 2007, 118:1649-1651.
47. Todd G., Flavel S.C., Ridding M. Priming theta-burst repetitive transcranial magnetic stimulation with low- and high-frequency stimulation. Exp Brain Res 2009, 195:307-315.
48. Todd G., Kimber T.E., Ridding M.C., Semmler J.G. Reduced motor cortex plasticity following inhibitory rTMS in older adults. Clin Neurophysiol 2010, 121:441-447.
49. Wankerl K., Weise D., Gentner R., Rumpf J.J., Classen J. L-type voltage-gated Ca21 channels: a single molecular switch for long-term potentiation/long-term depression-like plasticity and activity-dependent metaplasticity in humans. J Neurosci 2010, 30:6197-6204.
50. Wolters A., Sandbrink F., Schlottmann A., Kunesch E., Stefan K., Cohen L.G., et al. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 2003, 89:2339-2345.
51. Zafar N., Paulus W., Sommer M. Comparative assessment of best conventional with best theta burst repetitive transcranial magnetic stimulation protocols on human motor cortex excitability. Clin Neurophysiol 2008, 119:1393-1399.
52. Ziemann U., Ilić T.V., Pauli C., Meintzschel F., Ruge D. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 2004, 24:1666-1672.
53. Ziemann U., Siebner H.R. Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimulat 2008, 1:60-66.