Effects of Transcranial Magnetic Stimulation on Cognitive Function

경두개 자기 자극이 인지 기능에 미치는 영향

  • Lee, Sang Min (Department of Biomedical & Health Science, The Catholic University of Korea) ;
  • Chae, Jeong-Ho (Department of Biomedical & Health Science, The Catholic University of Korea)
  • 이상민 (가톨릭대학교 의생명건강과학과) ;
  • 채정호 (가톨릭대학교 의생명건강과학과)
  • Received : 2016.04.26
  • Accepted : 2016.06.03
  • Published : 2016.08.31

Abstract

Transcranial magnetic stimulation (TMS) is a safe, noninvasive and useful technique for exploring brain function. Especially, for the study of cognition, the technique can modulate a cognitive performance if the targeted area is engaged, because TMS has an effect on cortical network. The effect of TMS can vary depending on the frequency, intensity, and timing of stimulation. In this paper, we review the studies with TMS targeting various regions for evaluation of cognitive function. Cognitive functions, such as attention, working memory, semantic decision, discrimination and social cognition can be improved or deteriorated according to TMS stimulation protocols. Furthermore, potential therapeutic applications of TMS, including therapy in a variety of illness and research into cortical localization, are discussed.

Keywords

References

  1. Walsh V, Cowey A. Transcranial magnetic stimulation and cognitive neuroscience. Nat Rev Neurosci 2000;1:73-79. https://doi.org/10.1038/35036239
  2. Rossi S, Hallett M, Rossini PM, Pascual-Leone A; Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009;120:2008-2039. https://doi.org/10.1016/j.clinph.2009.08.016
  3. Luber B, Lisanby SH. Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS). Neuroimage 2014;85 Pt 3:961-970. https://doi.org/10.1016/j.neuroimage.2013.06.007
  4. Lefaucheur JP, Andre-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 2014;125:2150-2206. https://doi.org/10.1016/j.clinph.2014.05.021
  5. Robertson EM, Theoret H, Pascual-Leone A. Studies in cognition: the problems solved and created by transcranial magnetic stimulation. J Cogn Neurosci 2003;15:948-960. https://doi.org/10.1162/089892903770007344
  6. Chen R. Studies of human motor physiology with transcranial magnetic stimulation. Muscle Nerve Suppl 2000;9:S26-S32.
  7. Hoogendam JM, Ramakers GM, Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul 2010;3:95-118. https://doi.org/10.1016/j.brs.2009.10.005
  8. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 1994;117(Pt 4):847-858. https://doi.org/10.1093/brain/117.4.847
  9. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997;48:1398-1403. https://doi.org/10.1212/WNL.48.5.1398
  10. Vlachos A, Muller-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;32:17514-17523. https://doi.org/10.1523/JNEUROSCI.0409-12.2012
  11. Trippe J, Mix A, Aydin-Abidin S, Funke K, Benali A. ${\theta}$ burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex. Exp Brain Res 2009;199:411-421. https://doi.org/10.1007/s00221-009-1961-8
  12. Speer AM, Kimbrell TA, Wassermann EM, D Repella J, Willis MW, Herscovitch P, et al. Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol Psychiatry 2000;48:1133-1141. https://doi.org/10.1016/S0006-3223(00)01065-9
  13. Larson J, Wong D, Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 1986;368:347-350. https://doi.org/10.1016/0006-8993(86)90579-2
  14. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 2005;45:201-206. https://doi.org/10.1016/j.neuron.2004.12.033
  15. Barbas H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 2000;52:319-330. https://doi.org/10.1016/S0361-9230(99)00245-2
  16. Wood JN, Grafman J. Human prefrontal cortex: processing and representational perspectives. Nat Rev Neurosci 2003;4:139-147. https://doi.org/10.1038/nrn1033
  17. Wassermann EM, Lisanby SH. Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol 2001;112:1367-1377. https://doi.org/10.1016/S1388-2457(01)00585-5
  18. Skrdlantova L, Horacek J, Dockery C, Lukavsky J, Kopecek M, Preiss M, et al. The influence of low-frequency left prefrontal repetitive transcranial magnetic stimulation on memory for words but not for faces. Physiol Res 2005;54:123-128.
  19. Turriziani P, Smirni D, Zappala G, Mangano GR, Oliveri M, Cipolotti L. Enhancing memory performance with rTMS in healthy subjects and individuals with Mild Cognitive Impairment: the role of the right dorsolateral prefrontal cortex. Front Hum Neurosci 2012;6:62.
  20. Chambers CD, Bellgrove MA, Gould IC, English T, Garavan H, Mc-Naught E, et al. Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. J Neurophysiol 2007;98:3638-3647. https://doi.org/10.1152/jn.00685.2007
  21. Kalbe E, Schlegel M, Sack AT, Nowak DA, Dafotakis M, Bangard C, et al. Dissociating cognitive from affective theory of mind: a TMS study. Cortex 2010;46:769-80 https://doi.org/10.1016/j.cortex.2009.07.010
  22. Krause L, Enticott PG, Zangen A, Fitzgerald PB. The role of medial prefrontal cortex in theory of mind: a deep rTMS study. Behav Brain Res 2012;228:87-90. https://doi.org/10.1016/j.bbr.2011.11.037
  23. Goh HT, Lee YY, Fisher BE. Neural correlates of dual-task practice benefit on motor learning: a repetitive transcranial magnetic stimulation study. Eur J Neurosci 2013;37:1823-1829. https://doi.org/10.1111/ejn.12192
  24. Drager B, Breitenstein C, Helmke U, Kamping S, Knecht S. Specific and nonspecific effects of transcranial magnetic stimulation on picture-word verification. Eur J Neurosci 2004;20:1681-1687. https://doi.org/10.1111/j.1460-9568.2004.03623.x
  25. Knoch D, Brugger P, Regard M. Suppressing versus releasing a habit: frequency-dependent effects of prefrontal transcranial magnetic stimulation. Cereb Cortex 2005;15:885-887. https://doi.org/10.1093/cercor/bhh196
  26. Basso D, Lotze M, Vitale L, Ferreri F, Bisiacchi P, Olivetti Belardinelli M, et al. The role of prefrontal cortex in visuo-spatial planning: A repetitive TMS study. Exp Brain Res 2006;171:411-415. https://doi.org/10.1007/s00221-006-0457-z
  27. Bahlmann J, Beckmann I, Kuhlemann I, Schweikard A, Munte TF. Transcranial magnetic stimulation reveals complex cognitive control representations in the rostral frontal cortex. Neuroscience 2015;300:425-431. https://doi.org/10.1016/j.neuroscience.2015.05.058
  28. Camus M, Halelamien N, Plassmann H, Shimojo S, O'Doherty J, Camerer C, et al. Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex decreases valuations during food choices. Eur J Neurosci 2009;30:1980-1988. https://doi.org/10.1111/j.1460-9568.2009.06991.x
  29. Buckholtz JW, Martin JW, Treadway MT, Jan K, Zald DH, Jones O, et al. From Blame to Punishment: Disrupting Prefrontal Cortex Activity Reveals Norm Enforcement Mechanisms. Neuron 2015;87:1369-1380. https://doi.org/10.1016/j.neuron.2015.08.023
  30. Sandrini M, Rossini PM, Miniussi C. Lateralized contribution of prefrontal cortex in controlling task-irrelevant information during verbal and spatial working memory tasks: rTMS evidence. Neuropsychologia 2008;46:2056-2063. https://doi.org/10.1016/j.neuropsychologia.2008.02.003
  31. Manenti R, Cappa SF, Rossini PM, Miniussi C. The role of the prefrontal cortex in sentence comprehension: an rTMS study. Cortex 2008;44:337-344. https://doi.org/10.1016/j.cortex.2006.06.006
  32. Gaudeau-Bosma C, Moulier V, Allard AC, Sidhoumi D, Bouaziz N, Braha S, et al. Effect of two weeks of rTMS on brain activity in healthy subjects during an n-back task: a randomized double blind study. Brain Stimul 2013;6:569-575. https://doi.org/10.1016/j.brs.2012.10.009
  33. Preston G, Anderson E, Silva C, Goldberg T, Wassermann EM. Effects of 10 Hz rTMS on the neural efficiency of working memory. J Cogn Neurosci 2010;22:447-456. https://doi.org/10.1162/jocn.2009.21209
  34. Koch G, Oliveri M, Torriero S, Carlesimo GA, Turriziani P, Caltagirone C. rTMS evidence of different delay and decision processes in a fronto-parietal neuronal network activated during spatial working memory. Neuroimage 2005;24:34-39. https://doi.org/10.1016/j.neuroimage.2004.09.042
  35. Herwig U, Abler B, Schonfeldt-Lecuona C, Wunderlich A, Grothe J, Spitzer M, et al. Verbal storage in a premotor-parietal network: evidence from fMRI-guided magnetic stimulation. Neuroimage 2003;20:1032-1041. https://doi.org/10.1016/S1053-8119(03)00368-9
  36. Hamidi M, Tononi G, Postle BR. Evaluating the role of prefrontal and parietal cortices in memory-guided response with repetitive transcranial magnetic stimulation. Neuropsychologia 2009;47:295-302. https://doi.org/10.1016/j.neuropsychologia.2008.08.026
  37. Manenti R, Cotelli M, Calabria M, Maioli C, Miniussi C. The role of the dorsolateral prefrontal cortex in retrieval from long-term memory depends on strategies: a repetitive transcranial magnetic stimulation study. Neuroscience 2010;166:501-507. https://doi.org/10.1016/j.neuroscience.2009.12.037
  38. Hawco C, Berlim MT, Lepage M. The dorsolateral prefrontal cortex plays a role in self-initiated elaborative cognitive processing during episodic memory encoding: rTMS evidence. PLoS One 2013;8:e73789. https://doi.org/10.1371/journal.pone.0073789
  39. Sole-Padulles C, Bartres-Faz D, Junque C, Clemente IC, Molinuevo JL, Bargallo N, et al. Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cereb Cortex 2006;16:1487-1493. https://doi.org/10.1093/cercor/bhj083
  40. Viggiano MP, Giovannelli F, Borgheresi A, Feurra M, Berardi N, Pizzorusso T, et al. Disruption of the prefrontal cortex function by rTMS produces a category-specific enhancement of the reaction times during visual object identification. Neuropsychologia 2008;46:2725-2731. https://doi.org/10.1016/j.neuropsychologia.2008.05.004
  41. Smith DT, Jackson SR, Rorden C. Repetitive transcranial magnetic stimulation over frontal eye fields disrupts visually cued auditory attention. Brain Stimul 2009;2:81-87. https://doi.org/10.1016/j.brs.2008.07.005
  42. Vanderhasselt MA, De Raedt R, Baeken C, Leyman L, D'haenen H. The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance. Exp Brain Res 2006;169:279-282. https://doi.org/10.1007/s00221-005-0344-z
  43. Kim SH, Han HJ, Ahn HM, Kim SA, Kim SE. Effects of five daily high-frequency rTMS on Stroop task performance in aging individuals. Neurosci Res 2012;74:256-260. https://doi.org/10.1016/j.neures.2012.08.008
  44. Hwang JH, Kim SH, Park CS, Bang SA, Kim SE. Acute high-frequency rTMS of the left dorsolateral prefrontal cortex and attentional control in healthy young men. Brain Res 2010;1329:152-158. https://doi.org/10.1016/j.brainres.2010.03.013
  45. Wagner M, Rihs TA, Mosimann UP, Fisch HU, Schlaepfer TE. Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex affects divided attention immediately after cessation of stimulation. J Psychiatr Res 2006;40:315-321. https://doi.org/10.1016/j.jpsychires.2005.06.001
  46. Vanderhasselt MA, De Raedt R, Baeken C, Leyman L, D'haenen H. The influence of rTMS over the right dorsolateral prefrontal cortex on intentional set switching. Exp Brain Res 2006;172:561-565. https://doi.org/10.1007/s00221-006-0540-5
  47. Pobric G, Hamilton AF. Action understanding requires the left inferior frontal cortex. Curr Biol 2006;16:524-529. https://doi.org/10.1016/j.cub.2006.01.033
  48. Stadler W, Ott DV, Springer A, Schubotz RI, Schutz-Bosbach S, Prinz W. Repetitive TMS suggests a role of the human dorsal premotor cortex in action prediction. Front Hum Neurosci 2012;6:20.
  49. Wipfli M, Felblinger J, Mosimann UP, Hess CW, Schlaepfer TE, Muri RM. Double-pulse transcranial magnetic stimulation over the frontal eye field facilitates triggering of memory-guided saccades. Eur J Neurosci 2001;14:571-575. https://doi.org/10.1046/j.0953-816x.2001.01671.x
  50. Gagnon G, Blanchet S, Grondin S, Schneider C. Paired-pulse transcranial magnetic stimulation over the dorsolateral prefrontal cortex interferes with episodic encoding and retrieval for both verbal and non-verbal materials. Brain Res 2010;1344:148-158. https://doi.org/10.1016/j.brainres.2010.04.041
  51. Gagnon G, Schneider C, Grondin S, Blanchet S. Enhancement of episodic memory in young and healthy adults: a paired-pulse TMS study on encoding and retrieval performance. Neurosci Lett 2011;488:138-142. https://doi.org/10.1016/j.neulet.2010.11.016
  52. Blumenfeld RS, Lee TG, D'Esposito M. The effects of lateral prefrontal transcranial magnetic stimulation on item memory encoding. Neuropsychologia 2014;53:197-202. https://doi.org/10.1016/j.neuropsychologia.2013.11.021
  53. Debarnot U, Crepon B, Orriols E, Abram M, Charron S, Lion S, et al. Intermittent theta burst stimulation over left BA10 enhances virtual reality-based prospective memory in healthy aged subjects. Neurobiol Aging 2015;36:2360-2369. https://doi.org/10.1016/j.neurobiolaging.2015.05.001
  54. Kalla R, Muggleton NG, Cowey A, Walsh V. Human dorsolateral prefrontal cortex is involved in visual search for conjunctions but not features: a theta TMS study. Cortex 2009;45:1085-1090. https://doi.org/10.1016/j.cortex.2009.01.005
  55. Cattaneo L, Sandrini M, Schwarzbach J. State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices. Cereb Cortex 2010;20:2252-2258. https://doi.org/10.1093/cercor/bhp291
  56. Sakai KL, Noguchi Y, Takeuchi T, Watanabe E. Selective priming of syntactic processing by event-related transcranial magnetic stimulation of Broca's area. Neuron 2002;35:1177-1182. https://doi.org/10.1016/S0896-6273(02)00873-5
  57. Mattavelli G, Zuglian P, Dabroi E, Gaslini G, Clerici M, Papagno C. Transcranial magnetic stimulation of medial prefrontal cortex modulates implicit attitudes towards food. Appetite 2015;89:70-76. https://doi.org/10.1016/j.appet.2015.01.014
  58. Clower DM, Hoffman JM, Votaw JR, Faber TL, Woods RP, Alexander GE. Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 1996;383:618-621. https://doi.org/10.1038/383618a0
  59. Demonet JF, Price C, Wise R, Frackowiak RS. Differential activation of right and left posterior sylvian regions by semantic and phonological tasks: a positron-emission tomography study in normal human subjects. Neurosci Lett 1994;182:25-28. https://doi.org/10.1016/0304-3940(94)90196-1
  60. Seghier ML. The angular gyrus: multiple functions and multiple subdivisions. Neuroscientist 2013;19:43-61. https://doi.org/10.1177/1073858412440596
  61. Sack AT, Sperling JM, Prvulovic D, Formisano E, Goebel R, Di Salle F, et al. Tracking the mind's image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery. Neuron 2002;35:195-204. https://doi.org/10.1016/S0896-6273(02)00745-6
  62. Hirnstein M, Bayer U, Ellison A, Hausmann M. TMS over the left angular gyrus impairs the ability to discriminate left from right. Neuropsychologia 2011;49:29-33. https://doi.org/10.1016/j.neuropsychologia.2010.10.028
  63. Davey J, Cornelissen PL, Thompson HE, Sonkusare S, Hallam G, Smallwood J, et al. Automatic and controlled semantic retrieval: tms reveals distinct contributions of posterior middle temporal gyrus and angular gyrus. J Neurosci 2015;35:15230-15239. https://doi.org/10.1523/JNEUROSCI.4705-14.2015
  64. Kiyonaga A, Korb FM, Lucas J, Soto D, Egner T. Dissociable causal roles for left and right parietal cortex in controlling attentional biases from the contents of working memory. Neuroimage 2014;100:200-205. https://doi.org/10.1016/j.neuroimage.2014.06.019
  65. Uddin LQ, Molnar-Szakacs I, Zaidel E, Iacoboni M. rTMS to the right inferior parietal lobule disrupts self-other discrimination. Soc Cogn Affect Neurosci 2006;1:65-71. https://doi.org/10.1093/scan/nsl003
  66. Ishibashi R, Lambon Ralph MA, Saito S, Pobric G. Different roles of lateral anterior temporal lobe and inferior parietal lobule in coding function and manipulation tool knowledge: evidence from an rTMS study. Neuropsychologia 2011;49:1128-1135. https://doi.org/10.1016/j.neuropsychologia.2011.01.004
  67. Luber B, Kinnunen LH, Rakitin BC, Ellsasser R, Stern Y, Lisanby SH. Facilitation of performance in a working memory task with rTMS stimulation of the precuneus: frequency- and time-dependent effects. Brain Res 2007;1128:120-129. https://doi.org/10.1016/j.brainres.2006.10.011
  68. Ritterband-Rosenbaum A, Karabanov AN, Christensen MS, Nielsen JB. 10 Hz rTMS over right parietal cortex alters sense of agency during self-controlled movements. Front Hum Neurosci 2014;8:471.
  69. Pitcher D, Garrido L, Walsh V, Duchaine BC. Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. J Neurosci 2008;28:8929-8933. https://doi.org/10.1523/JNEUROSCI.1450-08.2008
  70. Babiloni C, Vecchio F, Rossi S, De Capua A, Bartalini S, Ulivelli M, et al. Human ventral parietal cortex plays a functional role on visuospatial attention and primary consciousness. A repetitive transcranial magnetic stimulation study. Cereb Cortex 2007;17:1486-1492. https://doi.org/10.1093/cercor/bhl060
  71. Cattaneo Z, Rota F, Walsh V, Vecchi T, Silvanto J. TMS-adaptation reveals abstract letter selectivity in the left posterior parietal cortex. Cereb Cortex 2009;19:2321-2325. https://doi.org/10.1093/cercor/bhn249
  72. Cattaneo Z, Rota F, Vecchi T, Silvanto J. Using state-dependency of transcranial magnetic stimulation (TMS) to investigate letter selectivity in the left posterior parietal cortex: a comparison of TMS-priming and TMS-adaptation paradigms. Eur J Neurosci 2008;28:1924-1929. https://doi.org/10.1111/j.1460-9568.2008.06466.x
  73. Cooper AC, Humphreys GW, Hulleman J, Praamstra P, Georgeson M. Transcranial magnetic stimulation to right parietal cortex modifies the attentional blink. Exp Brain Res 2004;155:24-29. https://doi.org/10.1007/s00221-003-1697-9
  74. Hartwigsen G, Golombek T, Obleser J. Repetitive transcranial magnetic stimulation over left angular gyrus modulates the predictability gain in degraded speech comprehension. Cortex 2015;68:100-110. https://doi.org/10.1016/j.cortex.2014.08.027
  75. Kirschen MP, Davis-Ratner MS, Jerde TE, Schraedley-Desmond P, Desmond JE. Enhancement of phonological memory following transcranial magnetic stimulation (TMS). Behav Neurol 2006;17:187-194. https://doi.org/10.1155/2006/469132
  76. Stoeckel C, Gough PM, Watkins KE, Devlin JT. Supramarginal gyrus involvement in visual word recognition. Cortex 2009;45:1091-1096. https://doi.org/10.1016/j.cortex.2008.12.004
  77. Lou HC, Luber B, Stanford A, Lisanby SH. Self-specific processing in the default network: a single-pulse TMS study. Exp Brain Res 2010;207:27-38. https://doi.org/10.1007/s00221-010-2425-x
  78. Livingstone M, Hubel D. Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 1988;240:740-749. https://doi.org/10.1126/science.3283936
  79. Cattaneo Z, Vecchi T, Pascual-Leone A, Silvanto J. Contrasting early visual cortical activation states causally involved in visual imagery and short-term memory. Eur J Neurosci 2009;30:1393-1400. https://doi.org/10.1111/j.1460-9568.2009.06911.x
  80. Maunsell JH, Van Essen DC. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 1983; 49:1127-1147. https://doi.org/10.1152/jn.1983.49.5.1127
  81. Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F, Mayer E. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 2003;126(Pt 11):2381-2395. https://doi.org/10.1093/brain/awg241
  82. Tsapkini K, Frangakis CE, Hillis AE. The function of the left anterior temporal pole: evidence from acute stroke and infarct volume. Brain 2011;134(Pt 10):3094-3105. https://doi.org/10.1093/brain/awr050
  83. Cleret de Langavant L, Remy P, Trinkler I, McIntyre J, Dupoux E, Berthoz A, et al. Behavioral and neural correlates of communication via pointing. PLoS One 2011;6:e17719. https://doi.org/10.1371/journal.pone.0017719
  84. Saxe R, Kanwisher N. People thinking about thinking people. The role of the temporo-parietal junction in "theory of mind". Neuroimage 2003;19:1835-1842. https://doi.org/10.1016/S1053-8119(03)00230-1
  85. Campanella F, Fabbro F, Urgesi C. Cognitive and anatomical underpinnings of the conceptual knowledge for common objects and familiar people: a repetitive transcranial magnetic stimulation study. PLoS One 2013;8:e64596. https://doi.org/10.1371/journal.pone.0064596
  86. Pobric G, Jefferies E, Ralph MA. Anterior temporal lobes mediate semantic representation: mimicking semantic dementia by using rTMS in normal participants. Proc Natl Acad Sci U S A 2007;104:20137-20141. https://doi.org/10.1073/pnas.0707383104
  87. Tadin D, Silvanto J, Pascual-Leone A, Battelli L. Improved motion perception and impaired spatial suppression following disruption of cortical area MT/V5. J Neurosci 2011;31:1279-1283. https://doi.org/10.1523/JNEUROSCI.4121-10.2011
  88. Waterston ML, Pack CC. Improved discrimination of visual stimuli following repetitive transcranial magnetic stimulation. PLoS One 2010;5:e10354. https://doi.org/10.1371/journal.pone.0010354
  89. Gallate J, Chi R, Ellwood S, Snyder A. Reducing false memories by magnetic pulse stimulation. Neurosci Lett 2009;449:151-154. https://doi.org/10.1016/j.neulet.2008.11.021
  90. Stolk A, Noordzij ML, Volman I, Verhagen L, Overeem S, van Elswijk G, et al. Understanding communicative actions: a repetitive TMS study. Cortex 2014;51:25-34. https://doi.org/10.1016/j.cortex.2013.10.005
  91. Heinisch C, Dinse HR, Tegenthoff M, Juckel G, Brune M. An rTMS study into self-face recognition using video-morphing technique. Soc Cogn Affect Neurosci 2011;6:442-449. https://doi.org/10.1093/scan/nsq062
  92. Giardina A, Caltagirone C, Oliveri M. Temporo-parietal junction is involved in attribution of hostile intentionality in social interactions: an rTMS study. Neurosci Lett 2011;495:150-154. https://doi.org/10.1016/j.neulet.2011.03.059
  93. Young L, Camprodon JA, Hauser M, Pascual-Leone A, Saxe R. Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proc Natl Acad Sci U S A 2010;107:6753-6758. https://doi.org/10.1073/pnas.0914826107
  94. Sparing R, Mottaghy FM, Hungs M, Brugmann M, Foltys H, Huber W, et al. Repetitive transcranial magnetic stimulation effects on language function depend on the stimulation parameters. J Clin Neurophysiol 2001;18:326-330. https://doi.org/10.1097/00004691-200107000-00004
  95. Pitcher D, Walsh V, Yovel G, Duchaine B. TMS evidence for the involvement of the right occipital face area in early face processing. Curr Biol 2007;17:1568-1573. https://doi.org/10.1016/j.cub.2007.07.063
  96. Ellison A, Battelli L, Cowey A, Walsh V. The effect of expectation on facilitation of colour/form conjunction tasks by TMS over area V5. Neuropsychologia 2003;41:1794-1801. https://doi.org/10.1016/S0028-3932(03)00180-5
  97. Mottaghy FM, Sparing R, Topper R. Enhancing picture naming with transcranial magnetic stimulation. Behav Neurol 2006;17:177-186. https://doi.org/10.1155/2006/768413
  98. Saad E, Wojciechowska M, Silvanto J. Partial dissociation in the neural bases of VSTM and imagery in the early visual cortex. Neuropsychologia 2015;75:143-148. https://doi.org/10.1016/j.neuropsychologia.2015.05.026
  99. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 2007;55:187-199. https://doi.org/10.1016/j.neuron.2007.06.026
  100. Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng 2007;9:527-565. https://doi.org/10.1146/annurev.bioeng.9.061206.133100
  101. Freitas C, Mondragon-Llorca H, Pascual-Leone A. Noninvasive brain stimulation in Alzheimer's disease: systematic review and perspectives for the future. Exp Gerontol 2011;46:611-627.
  102. Cotelli M, Manenti R, Cappa SF, Zanetti O, Miniussi C. Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline. Eur J Neurol 2008;15:1286-1292. https://doi.org/10.1111/j.1468-1331.2008.02202.x
  103. Cotelli M, Calabria M, Manenti R, Rosini S, Zanetti O, Cappa SF, et al. Improved language performance in Alzheimer disease following brain stimulation. J Neurol Neurosurg Psychiatry 2011;82:794-797. https://doi.org/10.1136/jnnp.2009.197848
  104. Ahmed MA, Darwish ES, Khedr EM, El Serogy YM, Ali AM. Effects of low versus high frequencies of repetitive transcranial magnetic stimulation on cognitive function and cortical excitability in Alzheimer's dementia. J Neurol 2012;259:83-92. https://doi.org/10.1007/s00415-011-6128-4
  105. Haffen E, Chopard G, Pretalli JB, Magnin E, Nicolier M, Monnin J, et al. A case report of daily left prefrontal repetitive transcranial magnetic stimulation (rTMS) as an adjunctive treatment for Alzheimer disease. Brain Stimul 2012;5:264-266. https://doi.org/10.1016/j.brs.2011.03.003
  106. Bentwich J, Dobronevsky E, Aichenbaum S, Shorer R, Peretz R, Khaigrekht M, et al. Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer's disease: a proof of concept study. J Neural Transm (Vienna) 2011;118:463-471. https://doi.org/10.1007/s00702-010-0578-1
  107. Rabey JM, Dobronevsky E, Aichenbaum S, Gonen O, Marton RG, Khaigrekht M. Repetitive transcranial magnetic stimulation combined with cognitive training is a safe and effective modality for the treatment of Alzheimer's disease: a randomized, double-blind study. J Neural Transm (Vienna) 2013;120:813-819. https://doi.org/10.1007/s00702-012-0902-z
  108. Sitzer DI, Twamley EW, Jeste DV. Cognitive training in Alzheimer's disease: a meta-analysis of the literature. Acta Psychiatr Scand 2006;114:75-90. https://doi.org/10.1111/j.1600-0447.2006.00789.x
  109. Bloch Y, Harel EV, Aviram S, Govezensky J, Ratzoni G, Levkovitz Y. Positive effects of repetitive transcranial magnetic stimulation on attention in ADHD Subjects: a randomized controlled pilot study. World J Biol Psychiatry 2010;11:755-758. https://doi.org/10.3109/15622975.2010.484466
  110. Weaver L, Rostain AL, Mace W, Akhtar U, Moss E, O'Reardon JP. Transcranial magnetic stimulation (TMS) in the treatment of attention-deficit/hyperactivity disorder in adolescents and young adults: a pilot study. J ECT 2012;28:98-103. https://doi.org/10.1097/YCT.0b013e31824532c8
  111. Niederhofer H. Additional biological therapies for attention-deficit hyperactivity disorder: repetitive transcranical magnetic stimulation of 1 Hz helps to reduce methylphenidate. Clin Pract 2011;2:e8. https://doi.org/10.17816/clinpract218-10
  112. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 2001;21:RC157. https://doi.org/10.1523/JNEUROSCI.21-15-j0003.2001
  113. Forbes NF, Carrick LA, McIntosh AM, Lawrie SM. Working memory in schizophrenia: a meta-analysis. Psychol Med 2009;39:889-905. https://doi.org/10.1017/S0033291708004558
  114. Barr MS, Farzan F, Rajji TK, Voineskos AN, Blumberger DM, Arenovich T, et al. Can repetitive magnetic stimulation improve cognition in schizophrenia? Pilot data from a randomized controlled trial. Biol Psychiatry 2013;73:510-517. https://doi.org/10.1016/j.biopsych.2012.08.020
  115. Kohler CG, Walker JB, Martin EA, Healey KM, Moberg PJ. Facial emotion perception in schizophrenia: a meta-analytic review. Schizophr Bull 2010;36:1009-1019. https://doi.org/10.1093/schbul/sbn192
  116. Wolwer W, Lowe A, Brinkmeyer J, Streit M, Habakuck M, Agelink MW, et al. Repetitive transcranial magnetic stimulation (rTMS) improves facial affect recognition in schizophrenia. Brain Stimul 2014;7:559-563. https://doi.org/10.1016/j.brs.2014.04.011
  117. Nestor PJ, Fryer TD, Hodges JR. Declarative memory impairments in Alzheimer's disease and semantic dementia. Neuroimage 2006;30:1010-1020. https://doi.org/10.1016/j.neuroimage.2005.10.008
  118. Beversdorf DQ, Smith BW, Crucian GP, Anderson JM, Keillor JM, Barrett AM, et al. Increased discrimination of “false memories” in autism spectrum disorder. Proc Natl Acad Sci U S A 2000;97:8734-8737. https://doi.org/10.1073/pnas.97.15.8734
  119. Barde LH, Buxbaum LJ, Moll AD. Abnormal reliance on object structure in apraxics' learning of novel object-related actions. J Int Neuropsychol Soc 2007;13:997-1008.
  120. Buxbaum LJ, Kyle KM, Tang K, Detre JA. Neural substrates of knowledge of hand postures for object grasping and functional object use: evidence from fMRI. Brain Res 2006;1117:175-185. https://doi.org/10.1016/j.brainres.2006.08.010
  121. Gold M, Adair JC, Jacobs DH, Heilman KM. Right-left confusion in Gerstmann's syndrome: a model of body centered spatial orientation. Cortex 1995;31:267-283. https://doi.org/10.1016/S0010-9452(13)80362-0