Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-22T05:21:10.235Z Has data issue: false hasContentIssue false
  • English
  • Français

Interhemispheric compensation: A hypothesis of TMS-induced effects on language-related areas

Published online by Cambridge University Press:  16 April 2020

Jamila Andoh  and
Jean-Luc Martinot
Jamila Andoh
Affiliation:
INSERM, U797, Research Unit “Neuroimaging and Psychiatry”, IFR49, Orsay, France CEA, “Neuroimaging and Psychiatry” U797 Unit, Hospital Department Frédéric Joliot and Neurospin, I2BM, Orsay, France Paris Sud University, UMR U797, Orsay, France Paris Descartes University, UMR U797, Paris, France Brain and Body Centre, University of Nottingham, UK
Jean-Luc Martinot*
Affiliation:
INSERM, U797, Research Unit “Neuroimaging and Psychiatry”, IFR49, Orsay, France CEA, “Neuroimaging and Psychiatry” U797 Unit, Hospital Department Frédéric Joliot and Neurospin, I2BM, Orsay, France Paris Sud University, UMR U797, Orsay, France Paris Descartes University, UMR U797, Paris, France
*
∗Corresponding author. INSERM – CEA, Research Unit U797 “Neuroimaging and Psychiatry”, Université Paris Sud, Service Hospitalier Frédéric Joliot, 4 place du Général Leclerc, 91401 Orsay, France. Tel.: +33 (0)1 69 86 77 57; fax: +33 (0)1 69 86 78 10. E-mail address: [email protected] (J.-L. Martinot).
Get access

Abstract

Repetitive transcranial magnetic stimulation (rTMS) applied over brain regions responsible for language processing is used to curtail potentially auditory hallucinations in schizophrenia patients and to investigate the functional organisation of language-related areas. Variability of effects is, however, marked across studies and between subjects. Furthermore, the mechanisms of action of rTMS are poorly understood.

Here, we reviewed different factors related to the structural and functional organisation of the brain that might influence rTMS-induced effects. Then, by analogy with aphasia studies, and the plastic-adaptive changes in both the left and right hemispheres following aphasia recovery, a hypothesis is proposed about rTMS mechanisms over language-related areas (e.g. Wernicke, Broca). We proposed that the local interference induced by rTMS in language-related areas might be analogous to aphasic stroke and might lead to a functional reorganisation in areas connected to the virtual lesion for language recovery.

Keywords

Transcranial magnetic stimulationAphasiaFunctional reorganisationLanguage recovery
Type
Original article
Information
European Psychiatry , Volume 23 , Issue 4 , June 2008 , pp. 281 - 288
Copyright
Copyright © European Psychiatric Association 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abo, M.Senoo, A.Watanabe, S.Miyano, S.Doseki, K.Sasaki, N.et al.Language-related brain function during word repetition in post-stroke aphasics. Neuroreport 2004;15:1891–1894.CrossRefGoogle ScholarPubMed
Aboitiz, F.Garcia, R.The anatomy of language revisited. Biol Res 1997;30:171–183.Google ScholarPubMed
Aleman, A.Sommer, I.E.Kahn, R.S.Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: a meta-analysis. J Clin Psychiatry 2007;68:416–421.CrossRefGoogle ScholarPubMed
Andoh, J.Artiges, E.Pallier, C.Riviere, D.Mangin, J.F.Cachia, A.et al.Modulation of language areas with functional MR image-guided magnetic stimulation. Neuroimage 2006;29:619–627.CrossRefGoogle ScholarPubMed
Andoh, J.Artiges, E.Pallier, C.Riviere, D.Mangin, J.F.Paillere-Martinot, M.L.et al.Priming frequencies of transcranial magnetic stimulation over Wernicke's area modulate word detection. Cereb Cortex 2008;18(1):210–216.CrossRefGoogle ScholarPubMed
Andoh, JCachia, AMangin, JFArtiges, ECointepas, YPaillere-Martinot, ML, et al.A triangulation-based MRI guided method for TMS coil positioning. Brain Stimulation, submitted for publication.Google Scholar
Barrett, J.Della-Maggiore, V.Chouinard, P.A.Paus, T.Mechanisms of action underlying the effect of repetitive transcranial magnetic stimulation on mood: behavioral and brain imaging studies. Neuropsychopharmacology 2004;29:1172–1189.CrossRefGoogle ScholarPubMed
Barta, P.E.Pearlson, G.D.Powers, R.E.Richards, S.S.Tune, L.E.Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 1990;147:1457–1462.Google Scholar
Binder, J.The new neuroanatomy of speech perception. Brain 2000;123(Pt 12):2371–2372.CrossRefGoogle ScholarPubMed
Binder, J.R.Frost, J.A.Hammeke, T.A.Cox, R.W.Rao, S.M.Prieto, T.Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 1997;17:353–362.CrossRefGoogle ScholarPubMed
Bohning, D.E.He, L.George, M.S.Epstein, C.M.Deconvolution of transcranial magnetic stimulation (TMS) maps. J Neural Transm 2001;108:35–52.CrossRefGoogle ScholarPubMed
Bohning, D.E.Shastri, A.McConnell, K.A.Nahas, Z.Lorberbaum, J.P.Roberts, D.R.et al.A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 1999;45:385–394.CrossRefGoogle ScholarPubMed
Catani, M.Howard, R.J.Pajevic, S.Jones, D.K.Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 2002;17:77–94.CrossRefGoogle ScholarPubMed
Catani, M.Jones, D.K.ffytche, D.H.Perisylvian language networks of the human brain. Ann Neurol 2005;57:8–16.CrossRefGoogle ScholarPubMed
Chen, R.Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 2004;154:1–10.CrossRefGoogle ScholarPubMed
Copolov, D.L.Seal, M.L.Maruff, P.Ulusoy, R.Wong, M.T.Tochon-Danguy, H.J.et al.Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study. Psychiatry Res 2003;122:139–152.CrossRefGoogle ScholarPubMed
Crinion, J.Price, C.J.Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. Brain 2005;128:2858–2871.CrossRefGoogle ScholarPubMed
Devlin, J.T.Matthews, P.M.Rushworth, M.F.Semantic processing in the left inferior prefrontal cortex: a combined functional magnetic resonance imaging and transcranial magnetic stimulation study. J Cogn Neurosci 2003;15:71–84.CrossRefGoogle ScholarPubMed
Fernandez, B.Cardebat, D.Demonet, J.F.Joseph, P.A.Mazaux, J.M.Barat, M.et al.Functional MRI follow-up study of language processes in healthy subjects and during recovery in a case of aphasia. Stroke 2004;35:2171–2176.CrossRefGoogle Scholar
Fries, W.Danek, A.Scheidtmann, K.Hamburger, C.Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. Brain 1993;116:369–382.CrossRefGoogle ScholarPubMed
Gerloff, C.Cohen, L.G.Floeter, M.K.Chen, R.Corwell, B.Hallett, M.Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract. J Physiol 1998;510:249–259.CrossRefGoogle ScholarPubMed
Gernsbacher, M.A.Kaschak, P.A.Neuroimaging studies of language production and comprehension. Annu Rev Psychol 2003;54:91–114.CrossRefGoogle ScholarPubMed
Golding, E.The effect of unilateral brain lesion on reasoning. Cortex 1981;17:31–40.CrossRefGoogle ScholarPubMed
Gugino, L.D.Romero, J.R.Aglio, L.Titone, D.Ramirez, M.Pascual-Leone, A.et al.Transcranial magnetic stimulation coregistered with MRI: a comparison of a guided versus blind stimulation technique and its effect on evoked compound muscle action potentials. Clin Neurophysiol 2001;112:1781–1792.CrossRefGoogle ScholarPubMed
Hausmann, A.Weis, C.Marksteiner, J.Hinterhuber, H.Humpel, C.Chronic repetitive transcranial magnetic stimulation enhances c-fos in the parietal cortex and hippocampus. Brain Res Mol Brain Res 2000;76:355–362.CrossRefGoogle ScholarPubMed
Heiss, W.D.Karbe, H.Weber-Luxenburger, G.Herholz, K.Kessler, J.Pietrzyk, U.et al.Speech-induced cerebral metabolic activation reflects recovery from aphasia. J Neurol Sci 1997;145:213–217.CrossRefGoogle ScholarPubMed
Hilgetag, C.C.Théoret, H.Pascual-Leone, A.Enhanced visual spatial attention ipsilateral to rTMS induced ‘virtual lesions’ of human parietal cortex. Nature 2001;4:953–957.Google ScholarPubMed
Hoffman, R.E.Hawkins, K.A.Gueorguieva, R.Boutros, N.N.Rachid, F.Carroll, K.et al.Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch Gen Psychiatry 2003;60:49–56.CrossRefGoogle ScholarPubMed
Humphries, C.Binder, J.R.Medler, D.A.Liebenthal, E.Time course of semantic processes during sentence comprehension: an fMRI study. Neuroimage 2007;36:924–932.CrossRefGoogle ScholarPubMed
Johansen-Berg, H.Rushworth, M.F.Bogdanovic, M.D.Kischka, U.Wimalaratna, S.Matthews, P.M.The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci U S A 2002;99:14518–14523.CrossRefGoogle ScholarPubMed
Kapur, N.Paradoxical functional facilitation in brain-behaviour research. A critical review. Brain 1996;119:1775–1790.CrossRefGoogle ScholarPubMed
Knecht, S.Floel, A.Drager, B.Breitenstein, C.Sommer, J.Henningsen, H.et al.Degree of language lateralization determines susceptibility to unilateral brain lesions. Nat Neurosci 2002;5:695–699.CrossRefGoogle ScholarPubMed
Kobayashi, M.Hutchinson, S.Théoret, H.Schlaug, G.Pascual-Leone, A.Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology 2004;62:91–98.CrossRefGoogle ScholarPubMed
Lancaster, J.L.Narayana, S.Wenzel, D.Luckemeyer, J.Roby, J.Fox, P.Evaluation of an image-guided, robotically positioned transcranial magnetic stimulation system. Hum Brain Mapp 2004;22:329–340.CrossRefGoogle ScholarPubMed
McIntosh, A.M.Semple, D.Tasker, K.Harrison, L.K.Owens, D.G.Johnstone, E.C.et al.Transcranial magnetic stimulation for auditory hallucinations in schizophrenia. Psychiatry Res 2004;127:9–17.CrossRefGoogle Scholar
Mesulam, M.M.Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 1990;28:597–613.CrossRefGoogle Scholar
Mesulam, M.M.From sensation to cognition. Brain 1998;121:1013–1052.CrossRefGoogle Scholar
Munchau, A.Bloem, B.R.Irlbacher, K.Trimble, M.R.Rothwell, J.C.Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation. J Neurosci 2002;22:554–561.CrossRefGoogle ScholarPubMed
Musso, M.Weiller, C.Kiebel, S.Muller, S.P.Bulau, P.Rijntjes, M.Training-induced brain plasticity in aphasia. Brain 1999;122:1781–1790.CrossRefGoogle ScholarPubMed
Naeser, M.A.Martin, P.I.Nicholas, M.Baker, E.H.Seekins, H.Kobayashi, M.et al.Improved picture naming in chronic aphasia after TMS to part of right Broca's area: an open-protocol study. Brain Lang 2005;93:95–105.CrossRefGoogle ScholarPubMed
Nixon, P.Lazarova, J.Hodinott-Hill, I.Gough, P.Passingham, R.The inferior frontal gyrus and phonological processing: an investigation using rTMS. J Cogn Neurosci 2004;16:289–300.CrossRefGoogle ScholarPubMed
O'Shea, J.Johansen-Berg, H.Trief, D.Gobel, S.Rushworth, M.F.Functionally specific reorganization in human premotor cortex. Neuron 2007;54:479–490.CrossRefGoogle ScholarPubMed
Parker, E.S.Weingartner, H.Retrograde facilitation of human memory by drugs. In: Weingartner, H.Parker, E.S., editors. Memory consolidation: psychobiology of cognition Hillsdale (NJ): Lawrence Erlbaum; 1984. p. 231–251.Google Scholar
Parker, G.J.Luzzi, S.Alexander, D.C.Wheeler-Kingshott, C.A.Ciccarelli, O.Lambon Ralph, M.A.Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 2005;24:656–666.CrossRefGoogle ScholarPubMed
Pascual-Leone, A.Bartres-Faz, D.Keenan, J.P.Transcranial magnetic stimulation: studying the brain-behaviour by induction of “virtual lesions”. Philos Trans R Soc Lond B Biol Sci 1999;354:1229–1238.CrossRefGoogle Scholar
Paus, T.Inferring causality in brain images: a perturbation approach. Philos Trans R Soc Lond B Biol Sci 2005;360:1109–1114.CrossRefGoogle ScholarPubMed
Paus, T.Castro-Alamancos, M.A.Petrides, M.Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci 2001;14:1405–1411.CrossRefGoogle ScholarPubMed
Paus, T.Jech, R.Thompson, C.J.Comeau, R.Peters, T.Evans, A.C.Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci 1997;17:3178–3184.CrossRefGoogle ScholarPubMed
Paus, T.Wolforth, M.Transcranial magnetic stimulation during PET: reaching and verifying the target site. Hum Brain Mapp 1998;6:399–402.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Peck, K.K.Moore, A.B.Crosson, B.A.Gaiefsky, M.Gopinath, K.S.White, K.et al.Functional magnetic resonance imaging before and after aphasia therapy: shifts in hemodynamic time to peak during an overt language task. Stroke 2004;35:554–559.CrossRefGoogle ScholarPubMed
Plaze, M.Bartrés-Faz, D.Martinot, J.L.Januel, D.Bellivier, F.De Beaurepaire, R.et al.Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients. Schizophr Res 2006;87:109–115.CrossRefGoogle ScholarPubMed
Price, C.J.Crinion, J.The latest on functional imaging studies of aphasic stroke. Curr Opin Neurol 2005;18:429–434.CrossRefGoogle ScholarPubMed
Robertson, E.M.Theoret, H.Pascual-Leone, A.Studies in cognition: the problems solved and created by transcranial magnetic stimulation. J Cogn Neurosci 2003;15:948–960.CrossRefGoogle ScholarPubMed
Rosen, H.J.Petersen, S.E.Linenweber, M.R.Snyder, A.Z.White, D.A.Chapman, L.et al.Neural correlates of recovery from aphasia after damage to left inferior frontal cortex. Neurology 2000;55:1883–1894.CrossRefGoogle ScholarPubMed
Rounis, E.Lee, L.Siebner, H.R.Rowe, J.B.Friston, K.J.Rothwell, J.C.et al.Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage 2005;26:164–176.CrossRefGoogle ScholarPubMed
Sakai, K.L.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.CrossRefGoogle ScholarPubMed
Shergill, S.S.Brammer, M.J.Williams, S.C.Murray, R.M.McGuire, P.K.Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch Gen Psychiatry 2000;57:1033–1038.CrossRefGoogle ScholarPubMed
Sparing, R.Mottaghy, F.M.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.CrossRefGoogle ScholarPubMed
Suzuki, M.Yuasa, S.Minabe, Y.Murata, M.Kurachi, M.Left superior temporal blood flow increases in schizophrenic and schizophreniform patients with auditory hallucination: a longitudinal case study using 123I-IMP SPECT. Eur Arch Psychiatry Clin Neurosci 1993;242:257–261.CrossRefGoogle ScholarPubMed
Theoret, H.Kobayashi, M.Valero-Cabre, A.Pascual-Leone, A.Exploring paradoxical functional facilitation with TMS. Suppl Clin Neurophysiol 2003;56:211–219.CrossRefGoogle ScholarPubMed
Thiel, A.Habedank, B.Herholz, K.Kessler, J.Winhuisen, L.Haupt, W.F.et al.From the left to the right: how the brain compensates progressive loss of language function. Brain Lang 2006;98:57–65.CrossRefGoogle ScholarPubMed
Thiel, A.Haupt, W.F.Habedank, B.Winhuisen, L.Herholz, K.Kessler, J.et al.Neuroimaging-guided rTMS of the left inferior frontal gyrus interferes with repetition priming. Neuroimage 2005;25:815–823.CrossRefGoogle ScholarPubMed
Thiel, A.Herholz, K.Koyuncu, A.Ghaemi, M.Kracht, L.W.Habedank, B.et al.Plasticity of language networks in patients with brain tumors: a positron emission tomography activation study. Ann Neurol 2001;50:620–629.CrossRefGoogle ScholarPubMed
Thiel, A.Schumacher, B.Wienhard, K.Gairing, S.Kracht, L.W.Wagner, R.et al.Direct demonstration of transcallosal disinhibition in language networks. J Cereb Blood Flow Metab 2006;26:1122–1127.CrossRefGoogle ScholarPubMed
Thomas, C.Altenmuller, E.Marckmann, G.Kahrs, J.Dichgans, J.Language processing in aphasia: changes in lateralization patterns during recovery reflect cerebral plasticity in adults. Electroencephalogr Clin Neurophysiol 1997;102:86–97.CrossRefGoogle ScholarPubMed
Thulborn, K.R.Carpenter, P.A.Just, M.A.Plasticity of language-related brain function during recovery from stroke. Stroke 1999;30:749–754.CrossRefGoogle Scholar
Topper, R.Mottaghy, F.M.Brugmann, M.Noth, J.Huber, W.Facilitation of picture naming by focal transcranial magnetic stimulation of Wernicke's area. Exp Brain Res 1998;121:371–378.Google ScholarPubMed
Van Petten, C.Luka, B.J.Neural localization of semantic context effects in electromagnetic and hemodynamic studies. Brain Lang 2006;97:279–293.CrossRefGoogle ScholarPubMed
Voets, N.L.Adcock, J.E.Flitney, D.E.Behrens, T.E.Hart, Y.Stacey, R.et al.Distinct right frontal lobe activation in language processing following left hemisphere injury. Brain 2006;129:754–766.CrossRefGoogle ScholarPubMed
Warrington, E.K.Weiskrantz, L.Further analysis of the prior learning effect in amnesic patients. Neuropsychologia 1978;16:169–177.CrossRefGoogle ScholarPubMed
Weiller, C.Chollet, F.Friston, K.J.Wise, R.J.S.Frackowiak, R.S.J.Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol 1992;31:463–472.CrossRefGoogle ScholarPubMed
Woodruff, P.W.Wright, I.C.Bullmore, E.T.Brammer, M.Howard, R.J.Williams, S.C.et al.Auditory hallucinations and the temporal cortical response to speech in schizophrenia: a functional magnetic resonance imaging study. Am J Psychiatry 1997;154:1676–1682.CrossRefGoogle ScholarPubMed
Xu, X.J.Zhang, M.M.Shang, D.S.Wang, Q.D.Luo, B.Y.Weng, X.C.Cortical language activation in aphasia: a functional MRI study. Chin Med J 2004;117:1011–1106.Google ScholarPubMed
Zaidel, E.Auditory vocabulary of the right hemisphere following brain bisection or hemidecortication. Cortex 1976;12:191–211.CrossRefGoogle ScholarPubMed
Gilio, F.Rizzo, V.Siebner, H.R.Rothwell, J.C.Effects on the right motor hand-area excitability produced by low-frequency rTMS over human contralateral homologous cortex. J Physiol. 2003;1;551(Pt 2):563–573.CrossRefGoogle Scholar
Aboitiz, F.García, V.R.The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective. Brain Res Brain Res Rev 1997;25(3):381–396 [Review]CrossRefGoogle Scholar
Price, C.J.Crinion, J.The latest on functional imaging studies of aphasic stroke. Curr Opin Neurol 2005;18(4):429–434 [Review]CrossRefGoogle ScholarPubMed
Winhuisen, L.Thiel, A.Schumacher, B.Kessler, J.Rudolf, J.Haupt, W.F.et al.The right inferior frontal gyrus and poststroke aphasia: a follow-up investigation. Stroke 2007;38(4):1286–1292.CrossRefGoogle ScholarPubMed
Mottaghy, F.M.Hungs, M.Brügmann, M.Sparing, R.Boroojerdi, B.Foltys, H.et al.Facilitation of picture naming after repetitive transcranial magnetic stimulation. Neurology 1999;53(8):1806–1812.CrossRefGoogle ScholarPubMed
Submit a response

Comments

No Comments have been published for this article.