Download PDF
Klinische Neurophysiologie 2005; 36(4): 165-172
DOI: 10.1055/s-2005-866866
Originalia
© Georg Thieme Verlag KG Stuttgart · New York

Transkranielle Magnetstimulation und funktionelle Bildgebung

Transcranial Magnetic Stimulation and Functional ImagingA.  Flöel1 , C.  Breitenstein1 , 2 , S.  Knecht1 , 2
  • 1Klinik und Poliklinik für Neurologie Münster
  • 2IZKF Münster
Further Information

Publication History

Publication Date:
08 December 2005 (online)

Also available at
    Permissions and Reprints

Zusammenfassung

Die transkranielle Magnetstimulation (TMS) ist eine in den Neurowissenschaften inzwischen weit verbreitete Methode zur Untersuchung neurophysiologischer Prozesse sowie des Zusammenhangs zwischen fokaler Gehirnaktivität und Verhalten. In der folgenden Übersichtsarbeit beschreiben wir zunächst kurz den physikalischen Hintergrund der TMS. Der Hauptteil der Arbeit befasst sich mit den verschiedenen Anwendungsmöglichkeiten einer Kombination aus TMS und funktioneller zerebraler Bildgebung. Die funktionelle Bildgebung kann zum einen genutzt werden, um eine genaue Lokalisation der individuellen TMS-Stimulationsorte zu erhalten. Hierzu haben sich kommerziell erhältliche Neuronavigationsverfahren etabliert (www.brainsight.com; www.nexstim.com). Alternativ kann mit computergestützten Verfahren zur Projektion von Gehirnarealen auf die Kopfoberfläche eine hohe Genauigkeit des Stimulationsortes erzielt werden (http://neurologie.uni-muenster.de/T2T/index.html). Mit der TMS kann dann bestimmt werden, welche funktionelle Relevanz eine regionale kortikale Aktivierung für die Durchführung einer bestimmten Aufgabe hat. In einem weiteren Abschnitt wird beschrieben, wie die funktionelle Bildgebung zeitnah zur Darstellung der durch die TMS induzierten Blutfluss-/Erregbarkeitsänderungen genutzt werden kann. Dies kann sowohl nach der eigentlichen TMS-Stimulation erfolgen als auch (technisch jedoch erheblich aufwändiger) während der Stimulation. Abschließend erfolgt eine Zusammenfassung, wie die Kombination aus TMS und funktioneller Bildgebung zum Verständnis kortikaler Plastizität und therapeutischer Effekte der TMS beitragen kann.

Abstract

Transcranial magnetic stimulation (TMS) is an important tool in neuroscience for the study of neurophysiology and the relationship between focal brain activity and behaviour. In this contribution, we give first a brief description of the physical background of TMS, and then provide an overview of the combined application of TMS and functional imaging. Initially we describe how imaging can be used to determine the exact localisation for TMS in each individual subject, using commercially available neuronavigational systems (www.brainsight.com; www.nexstim.com) or computer-assisted tools that project brain areas onto the scalp with high precision (http://neurologie.uni-muenster.de/T2T/index.html). TMS is subsequently applied to investigate the functional relevance of the cortical activation in a given task, as assessed by functional imaging. Next, we discuss how functional imaging can be used to visualise TMS-induced changes in blood flow and cortical activity, either at the end of stimulation or, technically more challenging, during stimulation. Finally, we sum up how the combined use of TMS and functional imaging may contribute to the understanding of plasticity in the human cortex and to the therapeutic effects of TMS in various neuropsychiatric disorders.

Key words

Magnetic stimulation - functional imaging - brain - cortical plasticity - therapy

Literatur

  • 1 Amedi A, Flöel A, Knecht S, Zohary E, Cohen L G. Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects.  Nat Neurosci. 2004;  7 1266-1270
    CrossrefPubMedGoogle Scholar
  • 2 Amedi A, Raz N, Pianka P, Malach R, Zohary E. Early „visual” cortex activation correlates with superior verbal memory performance in the blind.  Nat Neurosci. 2003;  6 758-766
    CrossrefPubMedGoogle Scholar
  • 3 Barker A T, Jalinous R, Freeston I L. Non-invasive magnetic stimulation of human motor cortex.  Lancet. 1985;  1 1106-1107
    PubMedGoogle Scholar
  • 4 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
    CrossrefPubMedGoogle Scholar
  • 5 Bohning D E, Pecheny A P, Epstein C M, Speer A M, Vincent D J, Dannels W, George M S. Mapping transcranial magnetic stimulation (TMS) fields in vivo with MRI.  Neuroreport. 1997;  8 2535-2538
    PubMedGoogle Scholar
  • 6 Bohning D E, Shastri A, McConnell K A, Nahas Z, Lorberbaum J P, Roberts D R, Teneback C, Vincent D J, George M S. A combined TMS/fMRI study of intensity-dependent TMS over motor cortex.  Biol Psychiatry. 1999;  45 385-394
    CrossrefPubMedGoogle Scholar
  • 7 Buckner R L, Raichle M E, Petersen S E. Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups.  J Neurophysiol. 1995;  74 2163-2173
    PubMedGoogle Scholar
  • 8 Cappa S F, Sandrini M, Rossini P M, Sosta K, Miniussi C. The role of the left frontal lobe in action naming: rTMS evidence.  Neurology. 2002;  59 720-723
    CrossrefPubMedGoogle Scholar
  • 9 Chen R, Classen J, Gerloff C, Celnik P, Wassermann E M, Hallett M, Cohen L G. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation.  Neurology. 1997;  48 1398-1403
    CrossrefPubMedGoogle Scholar
  • 10 Cohen L G, Roth B J, Nilsson J, Dang N, Panizza M, Bandinelli S, Friauf W, Hallett M. Effects of coil design on delivery of focal magnetic stimulation. Technical considerations.  Electroencephalogr Clin Neurophysiol. 1990;  75 350-357
    PubMedGoogle Scholar
  • 11 Deppe M, Knecht S, Papke K, Lohmann H, Fleischer H, Heindel W, Ringelstein E B, Henningsen H. Assessment of hemispheric language lateralization: a comparison between fMRI and fTCD.  J Cereb Blood Flow Metab. 2000;  20 263-268
    PubMedGoogle Scholar
  • 12 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
    CrossrefPubMedGoogle Scholar
  • 13 Dressler D, Voth E, Feldmann M, Benecke R. Safety aspects of transcranial brain stimulation in man tested by single photon emission-computed tomography.  Neurosci Lett. 1990;  119 153-155
    CrossrefPubMedGoogle Scholar
  • 14 Duning T, Rogalewski A, Steinstraeter O, Kugel H, Jansen A, Breitenstein C, Knecht S. Repetitive TMS temporarily alters brain diffusion.  Neurology. 2004;  62 2144; author reply 2144-2145
    PubMedGoogle Scholar
  • 15 Epstein C M, Lah J J, Meador K, Weissman J D, Gaitan L E, Dihenia B. Optimum stimulus parameters for lateralized suppression of speech with magnetic brain stimulation.  Neurology. 1996;  47 1590-1593
    PubMedGoogle Scholar
  • 16 Epstein C M, Meador K J, Loring D W, Wright R J, Weissman J D, Sheppard S, Lah J J, Puhalovich F, Gaitan L, Davey K R. Localization and characterization of speech arrest during transcranial magnetic stimulation.  Clin Neurophysiol. 1999;  110 1073-1079
    CrossrefPubMedGoogle Scholar
  • 17 Epstein C M, Schwartzberg D G, Davey K R, Sudderth D B. Localizing the site of magnetic brain stimulation in humans.  Neurology. 1990;  40 666-670
    CrossrefPubMedGoogle Scholar
  • 18 Ettinger G J, Leventon M E, Grimson W E, Kikinis R, Gugino L, Cote W, Sprung L, Aglio L, Shenton M E, Potts G, Hernandez V L, Alexander E. Experimentation with a transcranial magnetic stimulation system for functional brain mapping.  Med Image Anal. 1998;  2 133-142
    PubMedGoogle Scholar
  • 19 Flitman S S, Grafman J, Wassermann E M, Cooper V, O'Grady J, Pascual-Leone A, Hallett M. Linguistic processing during repetitive transcranial magnetic stimulation.  Neurology. 1998;  50 175-181
    PubMedGoogle Scholar
  • 20 Flöel A, Breitenstein C, Knecht S. The role of the left frontal lobe in action naming: rTMS evidence.  Neurology. 2003;  60 1052; author reply 1052
    PubMedGoogle Scholar
  • 21 Flöel A, Poeppel D, Buffalo E A, Braun A, Wu C W, Seo H J, Stefan K, Knecht S, Cohen L G. Prefrontal cortex asymmetry for memory encoding of words and abstract shapes.  Cereb Cortex. 2004;  14 404-409
    CrossrefPubMedGoogle Scholar
  • 22 Fox P, Ingham R, George M S, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P. Imaging human intra-cerebral connectivity by PET during TMS.  Neuroreport. 1997;  8 2787-2791
    CrossrefPubMedGoogle Scholar
  • 23 Hess G, Donoghue J P. Long-term potentiation and long-term depression of horizontal connections in rat motor cortex.  Acta Neurobiol Exp (Wars). 1996;  56 397-405
    PubMedGoogle Scholar
  • 24 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
    CrossrefPubMedGoogle Scholar
  • 25 Ilmoniemi R J, Virtanen J, Ruohonen J, Karhu J, Aronen H J, Naatanen R, Katila T. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity.  Neuroreport. 1997;  8 3537-3540
    PubMedGoogle Scholar
  • 26 Iriki A, Pavlides C, Keller A, Asanuma H. Long-term potentiation in the motor cortex.  Science. 1989;  245 1385-1387
    CrossrefPubMedGoogle Scholar
  • 27 Knecht S, Flöel A, Drager B, Breitenstein C, Sommer J, Henningsen H, Ringelstein E B, Pascual-Leone A. Degree of language lateralization determines susceptibility to unilateral brain lesions.  Nat Neurosci. 2002;  5 695-699
    PubMedGoogle Scholar
  • 28 Krings T, Chiappa K H, Foltys H, Reinges M H, Cosgrove G R, Thron A. Introducing navigated transcranial magnetic stimulation as a refined brain mapping methodology.  Neurosurg Rev. 2001;  24 171-179
    PubMedGoogle Scholar
  • 29 Krings T, Foltys H, Reinges M H, Kemeny S, Rohde V, Spetzger U, Gilsbach J M, Thron A. Navigated transcranial magnetic stimulation for presurgical planning - correlation with functional MRI.  Minim Invasive Neurosurg. 2001;  44 234-239
    Article in Thieme ConnectPubMedGoogle Scholar
  • 30 Kujirai T, Caramia M D, Rothwell J C, Day B L, Thompson P D, Ferbert A, Wroe S, Asselman P, Marsden C D. Corticocortical inhibition in human motor cortex.  J Physiol. 1993;  471 501-519
    CrossrefPubMedGoogle Scholar
  • 31 Li X, Nahas Z, Lomarev M, Denslow S, Shastri A, Bohning D E, George M S. Prefrontal cortex transcranial magnetic stimulation does not change local diffusion: a magnetic resonance imaging study in patients with depression.  Cogn Behav Neurol. 2003;  16 128-135
    PubMedGoogle Scholar
  • 32 Maeda F, Gangitano M, Thall M, Pascual-Leone A. Inter- and intra-individual variability of paired-pulse curves with transcranial magnetic stimulation (TMS).  Clin Neurophysiol. 2002;  113 376-382
    CrossrefPubMedGoogle Scholar
  • 33 Maeda F, Keenan J P, Tormos J M, Topka H, Pascual-Leone A. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability.  Exp Brain Res. 2000;  133 425-430
    CrossrefPubMedGoogle Scholar
  • 34 Maeda F, Keenan J P, Tormos J M, Topka H, Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation.  Clin Neurophysiol. 2000;  111 800-805
    CrossrefPubMedGoogle Scholar
  • 35 Mottaghy F M, Gangitano M, Horkan C, Chen Y, Pascual-Leone A, Schlaug G. Repetitive TMS temporarily alters brain diffusion.  Neurology. 2003;  60 1539-1541
    PubMedGoogle Scholar
  • 36 Mottaghy F M, Gangitano M, Krause B J, Pascual-Leone A. Chronometry of parietal and prefrontal activations in verbal working memory revealed by transcranial magnetic stimulation.  Neuroimage. 2003;  18 565-575
    CrossrefPubMedGoogle Scholar
  • 37 Mottaghy F M, Hungs M, Brugmann M, Sparing R, Boroojerdi B, Foltys H, Huber W, Topper R. Facilitation of picture naming after repetitive transcranial magnetic stimulation.  Neurology. 1999;  53 1806-1812
    PubMedGoogle Scholar
  • 38 Mottaghy F M, Keller C E, Gangitano M, Ly J, Thall M, Parker J A, Pascual-Leone A. Correlation of cerebral blood flow and treatment effects of repetitive transcranial magnetic stimulation in depressed patients.  Psychiatry Res. 2002;  115 1-14
    CrossrefPubMedGoogle Scholar
  • 39 Mottaghy F M, Krause B J, Kemna L J, Topper R, Tellmann L, Beu M, Pascual-Leone A, Muller-Gartner H W. Modulation of the neuronal circuitry subserving working memory in healthy human subjects by repetitive transcranial magnetic stimulation.  Neurosci Lett. 2000;  280 167-170
    CrossrefPubMedGoogle Scholar
  • 40 Mottaghy F M, Pascual-Leone A, Kemna L J, Topper R, Herzog H, Muller-Gartner H W, Krause B J. Modulation of a brain-behavior relationship in verbal working memory by rTMS.  Brain Res Cogn Brain Res. 2003;  15 241-249
    CrossrefPubMedGoogle Scholar
  • 41 Muellbacher W, Ziemann U, Boroojerdi B, Hallett M. Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior.  Clin Neurophysiol. 2000;  111 1002-1007
    CrossrefPubMedGoogle Scholar
  • 42 Pascual-Leone A, Valls-Sole J, Wassermann E M, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex.  Brain. 1994;  117 (Pt 4) 847-858
    CrossrefPubMedGoogle Scholar
  • 43 Paus T. Imaging the brain before, during, and after transcranial magnetic stimulation.  Neuropsychologia. 1999;  37 219-224
    PubMedGoogle Scholar
  • 44 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
    PubMedGoogle Scholar
  • 45 Paus T, Jech R, Thompson C J, Comeau R, Peters T, Evans A C. Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex.  J Neurophysiol. 1998;  79 1102-1107
    PubMedGoogle Scholar
  • 46 Rossi S, Cappa S F, Babiloni C, Pasqualetti P, Miniussi C, Carducci F, Babiloni F, Rossini P M. Prefrontal [correction of Prefontal] cortex in long-term memory: an „interference” approach using magnetic stimulation.  Nat Neurosci. 2001;  4 948-952
    CrossrefPubMedGoogle Scholar
  • 47 Rossi S, Miniussi C, Pasqualetti P, Babiloni C, Rossini P M, Cappa S F. Age-related functional changes of prefrontal cortex in long-term memory: a repetitive transcranial magnetic stimulation study.  J Neurosci. 2004;  24 7939-7944
    CrossrefPubMedGoogle Scholar
  • 48 Rothwell J, Burke D, Hicks R, Stephen J, Woodforth I, Crawford M. Transcranial electrical stimulation of the motor cortex in man: further evidence for the site of activation.  J Physiol. 1994;  481 (Pt 1) 243-250
    CrossrefPubMedGoogle Scholar
  • 49 Rudiak D, Marg E. Finding the depth of magnetic brain stimulation: a re-evaluation.  Electroencephalogr Clin Neurophysiol. 1994;  93 358-371
    PubMedGoogle Scholar
  • 50 Sack A T, Hubl D, Prvulovic D, Formisano E, Jandl M, Zanella F E, Maurer K, Goebel R, Dierks T, Linden D E. The experimental combination of rTMS and fMRI reveals the functional relevance of parietal cortex for visuospatial functions.  Brain Res Cogn Brain Res. 2002;  13 85-93
    CrossrefPubMedGoogle Scholar
  • 51 Sack A T, Sperling J M, Prvulovic D, Formisano E, Goebel R, Salle F Di, Dierks T, Linden D E. Tracking the mind's image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery.  Neuron. 2002;  35 195-204
    CrossrefPubMedGoogle Scholar
  • 52 Saypol J M, Roth B J, Cohen L G, Hallett M. A theoretical comparison of electric and magnetic stimulation of the brain.  Ann Biomed Eng. 1991;  19 317-328
    PubMedGoogle Scholar
  • 53 Schnitzler A, Benecke R. The silent period after transcranial magnetic stimulation is of exclusive cortical origin: evidence from isolated cortical ischemic lesions in man.  Neurosci Lett. 1994;  180 41-45
    CrossrefPubMedGoogle Scholar
  • 54 Shajahan P M, Glabus M F, Steele J D, Doris A B, Anderson K, Jenkins J A, Gooding P A, Ebmeier K P. Left dorso-lateral repetitive transcranial magnetic stimulation affects cortical excitability and functional connectivity, but does not impair cognition in major depression.  Prog Neuropsychopharmacol Biol Psychiatry. 2002;  26 945-954
    CrossrefPubMedGoogle Scholar
  • 55 Shastri A, George M S, Bohning D E. Performance of a system for interleaving transcranial magnetic stimulation with steady-state magnetic resonance imaging.  Electroencephalogr Clin Neurophysiol. 1999;  51, Suppl 55-64
    PubMedGoogle Scholar
  • 56 Siebner H R, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity.  Exp Brain Res. 2003;  148 1-16
    CrossrefPubMedGoogle Scholar
  • 57 Singh K D, Hamdy S, Aziz Q, Thompson D G. Topographic mapping of trans-cranial magnetic stimulation data on surface rendered MR images of the brain.  Electroencephalogr Clin Neurophysiol. 1997;  105 345-351
    CrossrefPubMedGoogle Scholar
  • 58 Singh K D, Holliday I E, Furlong P L, Harding G F. Evaluation of MRI-MEG/EEG co-registration strategies using Monte Carlo simulation.  Electroencephalogr Clin Neurophysiol. 1997;  102 81-85
    PubMedGoogle Scholar
  • 59 Strafella A P, 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
    PubMedGoogle Scholar
  • 60 Strens L H, Oliviero A, Bloem B R, Gerschlager W, Rothwell J C, Brown P. The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence.  Clin Neurophysiol. 2002;  113 1279-1285
    CrossrefPubMedGoogle Scholar
  • 61 Teneback C C, Nahas Z, Speer A M, Molloy M, Stallings L E, Spicer K M, Risch S C, George M S. Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS.  J Neuropsychiatry Clin Neurosci. 1999;  11 426-435
    PubMedGoogle Scholar
  • 62 Triggs W J, McCoy K J, Greer R, Rossi F, Bowers D, Kortenkamp S, Nadeau S E, Heilman K M, Goodman W K. Effects of left frontal transcranial magnetic stimulation on depressed mood, cognition, and corticomotor threshold.  Biol Psychiatry. 1999;  45 1440-1446
    CrossrefPubMedGoogle Scholar
  • 63 Vickery R M, Bindman L J. Long-lasting decreases of AMPA responses following postsynaptic activity in single hippocampal neurons.  Synapse. 1997;  25 103-106
    CrossrefPubMedGoogle Scholar
  • 64 Weiss S R, Li X L, Rosen J B, Li H, Heynen T, Post R M. Quenching: inhibition of development and expression of amygdala kindled seizures with low frequency stimulation.  Neuroreport. 1995;  6 2171-2176
    PubMedGoogle Scholar

Agnes Flöel

Klinik und Poliklinik für Neurologie

Albert-Schweitzer-Straße 33

48129 Münster

Phone: 0251/8349970

Fax: 0251/8348181

Email: floeel@uni-muenster.de

      >