Metaplasticity in human cortex

Neuroscientist

Volumn 21, Issue 2, 2015, Pages 185-202

  Müller Dahlhaus, Florian ^a   Ziemann, Ulf ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

long term depression; long term potentiation; metaplasticity; motor cortex; motor learning; non invasive brain stimulation; transcranial direct current stimulation; transcranial magnetic stimulation

Indexed keywords

ANIMAL EXPERIMENT; BRAIN CORTEX; BRAIN DEPTH STIMULATION; HUMAN; LEARNING; MENTAL DISEASE; METAPLASTICITY; MOTOR ACTIVITY; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; MOTOR CORTEX; PHYSIOLOGY; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; CEREBRAL CORTEX; HUMANS; LEARNING; MOTOR CORTEX; NEURONAL PLASTICITY; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84924962646     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858414526645     Document Type: Review

References (135)

1. Abraham WC, Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 1996 ; 19 (4). 126-30
2. Abraham WC, Mason-Parker SE, Bear MF, Webb S, Tate WP. Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP. Proc Natl Acad Sci U S A. 2001 ; 98 (19). 10924-9
3. Ackerley SJ, Stinear CM, Barber PA, Byblow WD. Combining theta burst stimulation with training after subcortical stroke. Stroke. 2010 ; 41 (7). 1568-72
4. Ackerley SJ, Stinear CM, Barber PA, Byblow WD. Priming sensorimotor cortex to enhance task-specific training after subcortical stroke. Clin Neurophysiol. 2013 ;:
5. Ahn KC, Bernier BE, Harnett MT, Morikawa H. IP3 receptor sensitization during in vivo amphetamine experience enhances NMDA receptor plasticity in dopamine neurons of the ventral tegmental area. J Neurosci. 2010 ; 30 (19). 6689-99
6. Antal A, Begemeier S, Nitsche MA, Paulus W. Prior state of cortical activity influences subsequent practicing of a visuomotor coordination task. Neuropsychologia. 2008a ; 46 (13). 3157-61
7. Antal A, Lang N, Boros K, Nitsche M, Siebner HR, Paulus W. Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura. Cereb Cortex. 2008b ; 18 (11). 2701-5
8. Avenanti A, Coccia M, Ladavas E, Provinciali L, Ceravolo MG. Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology. 2012 ; 78 (4). 256-64
9. Barr MS, Farzan F, Wing VC, George TP, Fitzgerald PB, Daskalakis ZJ. Repetitive transcranial magnetic stimulation and drug addiction. Int Rev Psychiatry. 2011 ; 23 (5). 454-66
10. Barria A, Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron. 2005 ; 48 (2). 289-301
11. Berardelli A, Inghilleri M, Rothwell JC, Romeo S, Curra A, Gilio F. Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp Brain Res. 1998 ; 122 (1). 79-84
12. Berger TW. Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science. 1984 ; 224 (4649). 627-30
13. Bernier BE, Whitaker LR, Morikawa H. Previous ethanol experience enhances synaptic plasticity of NMDA receptors in the ventral tegmental area. J Neurosci. 2011 ; 31 (14). 5205-12
14. Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982 ; 2 (1). 32-48
15. Bliem B, Müller-Dahlhaus JF, Dinse HR, Ziemann U. Homeostatic metaplasticity in the human somatosensory cortex. J Cogn Neurosci. 2008 ; 20 (8). 1517-28
16. Bocci T, Caleo M, Tognazzi S, Francini N, Briscese L, Maffei L. Evidence for metaplasticity in the human visual cortex. J Neural Transm. 2014 ; 121 (3). 221-31
17. Bolognini N, Pascual-Leone A, Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil. 2009 ; 6: 8
18. Buschler A, Manahan-Vaughan D. Brief environmental enrichment elicits metaplasticity of hippocampal synaptic potentiation in vivo. Front Behav Neurosci. 2012 ; 6: 85
19. Butler AJ, Shuster M, O'Hara E, Hurley K, Middlebrooks D, Guilkey K. A meta-analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors. J Hand Ther. 2013 ; 26 (2). 162-70
20. Byl NN, Merzenich MM, Jenkins WM. A primate genesis model of focal dystonia and repetitive strain injury: I. Learning-induced dedifferentiation of the representation of the hand in the primary somatosensory cortex in adult monkeys. Neurology. 1996 ; 47 (2). 508-20
21. Cantarero G, Lloyd A, Celnik P. Reversal of long-term potentiation-like plasticity processes after motor learning disrupts skill retention. J Neurosci. 2013a ; 33 (31). 12862-9
22. Cantarero G, Tang B, O'Malley R, Salas R, Celnik P. Motor Learning Interference Is Proportional to Occlusion of LTP-Like Plasticity. J Neurosci. 2013b ; 33 (11). 4634-41
23. Carmichael ST. Brain excitability in stroke: the yin and yang of stroke progression. Arch Neurol. 2012 ; 69 (2). 161-7
24. Cassidy JM, Gillick BT, Carey JR. Priming the brain to capitalize on metaplasticity in stroke rehabilitation. Phys Ther. 2014 ; 94 (1). 139-50
25. Castro-Alamancos MA, Donoghue JP, Connors BW. Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J Neurosci. 1995 ; 15 (7). 5324-33
26. Cheeran B, Talelli P, Mori F, Koch G, Suppa A, Edwards M. A common polymorphism in the brain derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol. 2008 ; 586 (23). 5717-25
27. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997 ; 48: 1398-403
28. Christie BR, Abraham WC. Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron. 1992 ; 9 (1). 79-84
29. Christie BR, Stellwagen D, Abraham WC. Reduction of the threshold for long-term potentiation by prior theta-frequency synaptic activity. Hippocampus. 1995 ; 5 (1). 52-9
30. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature. 2010 ; 468 (7321). 305-9
31. Cummings JA, Mulkey RM, Nicoll RA, Malenka RC. Ca2+ signaling requirements for long-term depression in the hippocampus. Neuron. 1996 ; 16 (4). 825-33
32. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Chen R. Dysfunctional neural plasticity in patients with schizophrenia. Arch Gen Psychiatry. 2008 ; 65 (4). 378-85
33. Delvendahl I, Jung NH, Mainberger F, Kuhnke NG, Cronjaeger M, Mall V. Occlusion of bidirectional plasticity by preceding low-frequency stimulation in the human motor cortex. Clin Neurophysiol. 2010 ; 121 (4). 594-602
34. Di Lazzaro V, Profice P, Pilato F, Capone F, Ranieri F, Pasqualetti P. Motor cortex plasticity predicts recovery in acute stroke. Cereb Cortex. 2010 ; 20 (7). 1523-8
35. Di Lazzaro V, Rothwell JC, Talelli P, Capone F, Ranieri F, Wallace AC. Inhibitory theta burst stimulation of affected hemisphere in chronic stroke: a proof of principle, sham-controlled study. Neurosci Lett. 2013 ; 553: 148-52
36. Di Lazzaro V, Ziemann U, Lemon RN. State of the art: Physiology of transcranial motor cortex stimulation. Brain Stimulation. 2008 ; 1 (4). 345-62
37. Doeltgen SH, Ridding MC. Modulation of cortical motor networks following primed theta burst transcranial magnetic stimulation. Exp Brain Res. 2011 ; 215 (3-4). 199-206
38. Edwards DA, Zhang L, Alger BE. Metaplastic control of the endocannabinoid system at inhibitory synapses in hippocampus. Proc Natl Acad Sci U S A. 2008 ; 105 (23). 8142-7
39. Fischer TM, Blazis DEJ, Priver NA, Carew TJ. Metaplasticity at identified inhibitory synapses in aplysia. Nature. 1997 ; 389 (6653). 860-5
40. Frantseva MV, Fitzgerald PB, Chen R, Moller B, Daigle M, Daskalakis ZJ. Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill leaning. Cereb Cortex. 2008 ; 18 (5). 990-6
41. Fricke K, Seeber AA, Thirugnanasambandam N, Paulus W, Nitsche MA, Rothwell JC. Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation (tDCS) of the human motor cortex. J Neurophysiol. 2011 ; 105 (3). 1141-9
42. Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG. Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron. 2010 ; 66 (2). 198-204
43. Fusco A, Iosa M, Venturiero V, De Angelis D, Morone G, Maglione L. After vs. priming effects of anodal transcranial direct current stimulation on upper extremity motor recovery in patients with subacute stroke. Restor Neurol Neurosci. 2014 ;:
44. Gamboa OL, Antal A, Laczo B, Moliadze V, Nitsche MA, Paulus W. Impact of repetitive theta burst stimulation on motor cortex excitability. Brain Stimul. 2011 ; 4 (3). 145-51
45. Gatica Tossi MA, Stude P, Schwenkreis P, Tegenthoff M, Dinse HR. Behavioural and neurophysiological markers reveal differential sensitivity to homeostatic interactions between centrally and peripherally applied passive stimulation. Eur J Neurosci. 2013 ; 38 (6). 2893-901
46. Gentner R, Wankerl K, Reinsberger C, Zeller D, Classen J. Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex. 2008 ; 18: 2046-53
47. Gerschlager W, Siebner HR, Rothwell JC. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology. 2001 ; 57 (3). 449-55
48. Goldsworthy MR, Müller-Dahlhaus F, Ridding MC, Ziemann U. Resistant against de-depression: LTD-like plasticity in the human motor cortex induced by spaced cTBS. Cereb Cortex. 2014 ;:
49. Goldsworthy MR, Pitcher JB, Ridding MC. The application of spaced theta burst protocols induces long-lasting neuroplastic changes in the human motor cortex. Eur J Neurosci. 2012 ; 35 (1). 125-34
50. Hallett M. The neurophysiology of dystonia. Arch Neurol. 1998 ; 55 (5). 601-3
51. Hamada M, Hanajima R, Terao Y, Arai N, Furubayashi T, Inomata-Terada S. Quadro-pulse stimulation is more effective than paired-pulse stimulation for plasticity induction of the human motor cortex. Clin Neurophysiol. 2007 ; 118 (12). 2672-82
52. Hamada M, Hanajima R, Terao Y, Okabe S, Nakatani-Enomoto S, Furubayashi T. Primary motor cortical metaplasticity induced by priming over the supplementary motor area. J Physiol. 2009 ; 587 (20). 4845-62
53. Hamada M, Terao Y, Hanajima R, Shirota Y, Nakatani-Enomoto S, Furubayashi T. Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J Physiol. 2008 ; 586 (16). 3927-47
54. Harvey CD, Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature. 2007 ; 450 (7173). 1195-200
55. Hasan A, Nitsche MA, Rein B, Schneider-Axmann T, Guse B, Gruber O. Dysfunctional long-term potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation. Behav Brain Res. 2011 ; 224 (1). 15-22
56. Hess G, Aizenman CD, Donoghue JP. Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J Neurophysiol. 1996 ; 75 (5). 1765-78
57. Hsu WY, Cheng CH, Liao KK, Lee IH, Lin YY. Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a meta-analysis. Stroke. 2012 ; 43 (7). 1849-57
58. Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005 ; 45 (2). 201-6
59. Huang YH, Lin Y, Mu P, Lee BR, Brown TE, Wayman G. In vivo cocaine experience generates silent synapses. Neuron. 2009 ; 63 (1). 40-7
60. Huang YY, Colino A, Selig DK, Malenka RC. The influence of prior synaptic activity on the induction of long-term potentiation. Science. 1992 ; 255 (5045). 730-3
61. Hulme SR, Jones OD, Abraham WC. Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci. 2013 ; 36 (6). 353-62
62. Hulme SR, Jones OD, Raymond CR, Sah P, Abraham WC. Mechanisms of heterosynaptic metaplasticity. Philos Trans R Soc Lond B Biol Sci. 2014 ; 369 (1633). 20130148
63. Iezzi E, Conte A, Suppa A, Agostino R, Dinapoli L, Scontrini A. Phasic voluntary movements reverse the aftereffects of subsequent theta-burst stimulation in humans. J Neurophysiol. 2008 ; 100 (4). 2070-6
64. Iezzi E, Suppa A, Conte A, Agostino R, Nardella A, Berardelli A. Theta-burst stimulation over primary motor cortex degrades early motor learning. Eur J Neurosci. 2010 ; 31 (3). 585-92
65. Iezzi E, Suppa A, Conte A, Li Voti P, Bologna M, Berardelli A. Short-term and long-term plasticity interaction in human primary motor cortex. Eur J Neurosci. 2011 ; 33 (10). 1908-15
66. Iyer MB, Schleper N, Wassermann EM. Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J Neurosci. 2003 ; 23 (34). 10867-72
67. Jeffery KJ, Morris RG. Cumulative long-term potentiation in the rat dentate gyrus correlates with, but does not modify, performance in the water maze. Hippocampus. 1993 ; 3 (2). 133-40
68. Jung P, Ziemann U. Homeostatic and non-homeostatic modulation of learning in human motor cortex. J Neurosci. 2009 ; 29: 5597-604
69. Kang J-S, Terranova C, Hilker R, Quartarone A, Ziemann U. Deficient homeostatic regulation of practice-dependent plasticity in writer's cramp. Cereb Cortex. 2011 ; 21 (5). 1203-12
70. Koch G, Di Lorenzo F, Bonni S, Ponzo V, Caltagirone C, Martorana A. Impaired LTP- but not LTD-like cortical plasticity in Alzheimer's disease patients. J Alzheimers Dis. 2012 ; 31 (3). 593-9
71. Koch G, Mori F, Marconi B, Codeca C, Pecchioli C, Salerno S. Changes in intracortical circuits of the human motor cortex following theta burst stimulation of the lateral cerebellum. Clin Neurophysiol. 2008 ; 119 (11). 2559-69
72. Lang N, Siebner HR, Ernst D, Nitsche MA, Paulus W, Lemon RN. 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 (9). 634-9
73. Li L, Murphy TH, Hayden MR, Raymond LA. Enhanced striatal NR2B-containing N-methyl-d-aspartate receptor-mediated synaptic currents in a mouse model of Huntington disease. J Neurophysiol. 2004 ; 92 (5). 2738-46
74. Li Q, Rothkegel M, Xiao ZC, Abraham WC, Korte M, Sajikumar S. Making synapses strong: metaplasticity prolongs associativity of long-term memory by switching synaptic tag mechanisms. Cereb Cortex. 2014 ; 24 (2). 353-63
75. Li Voti P, Conte A, Rocchi L, Bologna M, Khan N, Leodori1 G. Cerebellar continuous theta-burst stimulation affects motor learning of voluntary arm movements in humans. Eur J Neurosci. 2014 ; 39 (1). 124-31
76. Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci. 2002 ; 3 (3). 175-90
77. Mastroeni C, Bergmann TO, Rizzo V, Ritter C, Klein C, Pohlmann I. Brain-derived neurotrophic factor - a major player in stimulation-induced homeostatic metaplasticity of human motor cortex?. PLoS One. 2013 ; 8 (2). e57957
78. Monfils MH, Teskey GC. Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation. Neuroscience. 2004 ; 125 (2). 329-36
79. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W. Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul. 2013 ; 6 (3). 424-32
80. Monte-Silva K, Kuo MF, Liebetanz D, Paulus W, Nitsche MA. Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J Neurophysiol. 2010 ; 103 (4). 1735-40
81. Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R. Motor cortex plasticity in Parkinson's disease and levodopa-induced dyskinesias. Brain. 2006 ; 129 (4). 1059-69
82. Mori F, Rossi S, Piccinin S, Motta C, Mango D, Kusayanagi H. Synaptic plasticity and PDGF signaling defects underlie clinical progression in multiple sclerosis. J Neurosci. 2013 ; 33 (49). 19112-9
83. Moussawi K, Pacchioni A, Moran M, Olive MF, Gass JT, Lavin A. N-Acetylcysteine reverses cocaine-induced metaplasticity. Nat Neurosci. 2009 ; 12 (2). 182-9
84. Müller-Dahlhaus F, Vlachos A. Unraveling the cellular and molecular mechanisms of repetitive magnetic stimulation. Front Mol Neurosci. 2013 ; 6: 50
85. Müller-Dahlhaus F, Ziemann U, Classen J. Plasticity resembling spike-timing dependent synaptic plasticity: the evidence in human cortex. Front Syn Neurosci. 2010 ; 2 (34). 1-11
86. Müller JF, 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 (11). 3461-8
87. Murakami T, Müller-Dahlhaus F, Lu MK, Ziemann U. Homeostatic metaplasticity of corticospinal excitatory and intracortical inhibitory neural circuits in human motor cortex. J Physiol. 2012 ; 590 (22). 5765-81
88. Narayanan R, Johnston D. The h current is a candidate mechanism for regulating the sliding modification threshold in a BCM-like synaptic learning rule. J Neurophysiol. 2010 ; 104 (2). 1020-33
89. Nash JE, Ravenscroft P, McGuire S, Crossman AR, Menniti FS, Brotchie JM. The NR2B-selective NMDA receptor antagonist CP-101,606 exacerbates l-DOPA-induced dyskinesia and provides mild potentiation of anti-parkinsonian effects of l-DOPA in the MPTP-lesioned marmoset model of Parkinson's disease. Exp Neurol. 2004 ; 188 (2). 471-9
90. Nelson SB, Turrigiano GG. Strength through diversity. Neuron. 2008 ; 60 (3). 477-82
91. Nguyen PV, Abel T, Kandel ER. Requirement of a critical period of transcription for induction of a late phase of LTP. Science. 1994 ; 265 (5175). 1104-7
92. Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W. Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol. 2003 ; 114 (4). 600-4
93. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001 ; 57 (10). 1899-901
94. Nitsche MA, Roth A, Kuo M-F, Fischer AK, Liebetanz D, Lang N. Timing-dependent modulation of associative plasticity by general network excitability in the human motor cortex. J Neurosci. 2007 ; 27 (14). 3807-12
95. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J. LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron. 2007 ; 53 (5). 703-17
96. Philpot BD, Cho KK, Bear MF. Obligatory role of NR2A for metaplasticity in visual cortex. Neuron. 2007 ; 53 (4). 495-502
97. Pierelli F, Iacovelli E, Bracaglia M, Serrao M, Coppola G. Abnormal sensorimotor plasticity in migraine without aura patients. Pain. 2013 ; 154 (9). 1738-42
98. Pirulli C, Fertonani A, Miniussi C. The role of timing in the induction of neuromodulation in perceptual learning by transcranial electric stimulation. Brain Stimul. 2013 ; 6 (4). 683-9
99. Popa T, Velayudhan B, Hubsch C, Pradeep S, Roze E, Vidailhet M. Cerebellar processing of sensory inputs primes motor cortex plasticity. Cereb Cortex. 2013 ; 23 (2). 305-14
100. Pötter-Nerger M, Fischer S, Mastroeni C, Groppa S, Deuschl G, Volkmann J. Inducing homeostatic-like plasticity in human motor cortex through converging cortico-cortical inputs. J Neurophysiol. 2009 ; 102 (6). 3180-90
101. Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A. Abnormal associative plasticity of the human motor cortex in writer's cramp. Brain. 2003 ; 126 (12). 2586-96
102. Quartarone A, Rizzo V, Bagnato S, Morgante F, Sant'angelo A, Romano M. Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain. 2005 ; 128: 1943-50
103. Quartarone A, Siebner HR, Rothwell JC. Task-specific hand dystonia: can too much plasticity be bad for you?. Trends Neurosci. 2006 ; 29 (4). 192-9
104. Ragert P, Camus M, Dimyan MA, Vandermeeren Y, Cohen LG. Modulation of iTBS effects applied over primary motor cortex (M1) by conditioning stimulation of the opposite M1. J Neurophysiol. 2009 ; 102 (2). 766-73
105. Raymond CR, Thompson VL, Tate WP, Abraham WC. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J Neurosci. 2000 ; 20 (3). 969-76
106. Richardson AG, Overduin SA, Valero-Cabre A, Padoa-Schioppa C, Pascual-Leone A, Bizzi E. Disruption of primary motor cortex before learning impairs memory of movement dynamics. J Neurosci. 2006 ; 26 (48). 12466-70
107. Ridding MC, Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol. 2010 ; 588 (13). 2291-304
108. Rioult-Pedotti M-S, Friedman D, Hess G, Donoghue JP. Strengthening of horizontal cortical connections following skill learning. Nat Neurosci. 1998 ; 1 (3). 230-4
109. Rioult-Pedotti MS, Friedman D, Donoghue JP. Learning-induced LTP in neocortex. Science. 2000 ; 290 (5491). 533-6
110. Rizzo V, Siebner HR, Modugno N, Pesenti A, Münchau A, Gerschlager W. Shaping the excitability of human motor cortex with premotor rTMS. J Physiol. 2004 ; 554: 483-95
111. Rosenkranz K, Kacar A, Rothwell JC. Differential modulation of motor cortical plasticity and excitability in early and late phases of human motor learning. J Neurosci. 2007 ; 27 (44). 12058-66
112. Roze E, Soumare A, Pironneau I, Sangla S, de Cock VC, Teixeira A. Case-control study of writer's cramp. Brain. 2009 ; 132: 756-64
113. Sajikumar S, Li Q, Abraham WC, Xiao ZC. Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1. Learn Mem. 2009 ; 16 (3). 178-86
114. Schambra HM, Sawaki L, Cohen LG. Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clin Neurophysiol. 2003 ; 114 (1). 130-3
115. Shadmehr R, Holcomb HH. Neural correlates of motor memory consolidation. Science. 1997 ; 277 (5327). 821-5
116. Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci. 2004 ; 24 (13). 3379-85
117. Sjöström PJ, Turrigiano GG, Nelson SB. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron. 2001 ; 32 (6). 1149-64
118. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 2000 ; 123: 572-84
119. Stefan K, Wycislo M, Gentner R, Schramm A, Naumann M, Reiners K. Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb Cortex. 2006 ; 16 (3). 376-85
120. Teo JT, Swayne OB, Cheeran B, Greenwood RJ, Rothwell JC. Human theta burst stimulation enhances subsequent motor learning and increases performance variability. Cereb Cortex. 2011 ; 21 (7). 1627-38
121. Todd G, Flavel SC, Ridding MC. Priming theta-burst repetitive transcranial magnetic stimulation with low- and high-frequency stimulation. Exp Brain Res. 2009 ; 195 (2). 307-15
122. Udupa K, Chen R. Motor cortical plasticity in Parkinson's disease. Front Neurol. 2013 ; 4: 128
123. Ueki Y, Mima T, Ali Kotb M, Sawada H, Saiki H, Ikeda A. Altered plasticity of the human motor cortex in Parkinson's disease. Ann Neurol. 2006 ; 59 (1). 60-71
124. Vlachos A, Müller-Dahlhaus F, Rosskopp J, Lenz M, Ziemann U, Deller T. Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. J Neurosci. 2012 ; 32 (48). 17514-23
125. Wankerl K, Weise D, Gentner R, Rumpf JJ, Classen J. L-type voltage-gated Ca2+ channels: a single molecular switch for long-term potentiation/long-term depression-like plasticity and activity-dependent metaplasticity in humans. J Neurosci. 2010 ; 30 (18). 6197-204
126. Ward NS, Cohen LG. Mechanisms underlying recovery of motor function after stroke. Arch Neurol. 2004 ; 61 (12). 1844-8
127. Weise D, Schramm A, Stefan K, Wolters A, Reiners K, Naumann M. The two sides of associative plasticity in writer's cramp. Brain. 2006 ; 129 (10). 2709-21
128. Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol. 2003 ; 89 (5). 2339-45
129. Wolters A, Schmidt A, Schramm A, Zeller D, Naumann M, Kunesch E. Timing-dependent plasticity in human primary somatosensory cortex. J Physiol. 2005 ; 565 (3). 1039-52
130. Woo NH, Nguyen PV. Protein synthesis is required for synaptic immunity to depotentiation. J Neurosci. 2003 ; 23 (4). 1125-32
131. Yang Q, Liao ZH, Xiao YX, Lin QS, Zhu YS, Li ST. Hippocampal synaptic metaplasticity requires the activation of NR2B-containing NMDA receptors. Brain Res Bull. 2011 ; 84 (2). 137-43
132. Yang SN, Tang YG, Zucker RS. Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol. 1999 ; 81 (2). 781-7
133. Ziemann U, Corwell B, Cohen LG. Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci. 1998a ; 18 (3). 1115-23
134. Ziemann U, Hallett M, Cohen LG. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci. 1998b ; 18 (17). 7000-7
135. Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D. Learning modifies subsequent induction of LTP-like and LTD-like plasticity in human motor cortex. J Neurosci. 2004 ; 24 (7). 1666-72