Insights on the neural basis of motor plasticity induced by theta burst stimulation from TMS–EEG

Transcranial magnetic stimulation (TMS) is a useful tool to induce and measure plasticity in the human brain. However, the cortical effects are generally indirectly evaluated with motor‐evoked potentials (MEPs) reflective of modulation of cortico‐spinal excitability. In this study, we aim to provide direct measures of cortical plasticity by combining TMS with electroencephalography (EEG). Continuous theta‐burst stimulation (cTBS) was applied over the primary motor cortex (M1) of young healthy adults, and we measured modulation of (i) MEPs, (ii) TMS‐induced EEG evoked potentials (TEPs), (iii) TMS‐induced EEG synchronization and (iv) eyes‐closed resting EEG. Our results show the expected cTBS‐induced decrease in MEP size, which we found to be paralleled by a modulation of a combination of TEPs. Furthermore, we found that cTBS increased the power in the theta band of eyes‐closed resting EEG, whereas it decreased single‐pulse TMS‐induced power in the theta and alpha bands. In addition, cTBS decreased the power in the beta band of eyes‐closed resting EEG, whereas it increased single‐pulse TMS‐induced power in the beta band. We suggest that cTBS acts by modulating the phase alignment between already active oscillators; it synchronizes low‐frequency (theta and/or alpha) oscillators and desynchronizes high‐frequency (beta) oscillators. These results provide novel insight into the cortical effects of cTBS and could be useful for exploring cTBS‐induced plasticity outside of the motor cortex.

[1]  Thomas Kammer,et al.  Electroencephalographic response to transcranial magnetic stimulation in children: Evidence for giant inhibitory potentials , 2005, Annals of neurology.

[2]  Abbas F. Sadikot,et al.  The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions , 2006, Experimental Brain Research.

[3]  Robert Chen,et al.  The clinical diagnostic utility of transcranial magnetic stimulation: Report of an IFCN committee , 2008, Clinical Neurophysiology.

[4]  Seppo Kähkönen,et al.  The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation , 2004, Human brain mapping.

[5]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[6]  T. Paus,et al.  Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. , 2001, Journal of neurophysiology.

[7]  Á. Pascual-Leone,et al.  Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability , 2000, Experimental Brain Research.

[8]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[9]  Daniel Zeller,et al.  Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. , 2008, Cerebral cortex.

[10]  Y. Z. Huang,et al.  Theta‐burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex , 2005, The Journal of physiology.

[11]  P. Manganotti,et al.  Long Lasting Modulation of Cortical Oscillations after Continuous Theta Burst Transcranial Magnetic Stimulation , 2012, PloS one.

[12]  Risto J. Ilmoniemi,et al.  The relationship between peripheral and early cortical activation induced by transcranial magnetic stimulation , 2010, Neuroscience Letters.

[13]  V. Nikouline,et al.  The role of the coil click in TMS assessed with simultaneous EEG , 1999, Clinical Neurophysiology.

[14]  M. Bonnard,et al.  Prior intention can locally tune inhibitory processes in the primary motor cortex: direct evidence from combined TMS‐EEG , 2009, The European journal of neuroscience.

[15]  J. Rothwell,et al.  Theta Burst Stimulation of the Human Motor Cortex , 2005, Neuron.

[16]  P. Fitzgerald TMS–EEG: A technique that has come of age? , 2010, Clinical Neurophysiology.

[17]  Á. Pascual-Leone,et al.  Characterizing Brain Cortical Plasticity and Network Dynamics Across the Age-Span in Health and Disease with TMS-EEG and TMS-fMRI , 2011, Brain Topography.

[18]  Seppo Kähkönen,et al.  The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research , 2006, Brain Research Reviews.

[19]  Giulio Tononi,et al.  Human brain connectivity during single and paired pulse transcranial magnetic stimulation , 2011, NeuroImage.

[20]  G. Tononi,et al.  Measures of Cortical Plasticity after Transcranial Paired Associative Stimulation Predict Changes in Electroencephalogram Slow-Wave Activity during Subsequent Sleep , 2008, The Journal of Neuroscience.

[21]  Giorgio Fuggetta,et al.  Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: A combined EEG and TMS study , 2005, NeuroImage.

[22]  Thomas Kammer,et al.  Mechanisms and Applications of Theta-burst rTMS on the Human Motor Cortex , 2009, Brain Topography.

[23]  C. Miniussi,et al.  Combining TMS and EEG Offers New Prospects in Cognitive Neuroscience , 2009, Brain Topography.

[24]  M. Ridding,et al.  Determinants of the induction of cortical plasticity by non‐invasive brain stimulation in healthy subjects , 2010, The Journal of physiology.

[25]  Debora Brignani,et al.  Modulation of cortical oscillatory activity during transcranial magnetic stimulation , 2008, Human brain mapping.

[26]  Steven K. Esser,et al.  A direct demonstration of cortical LTP in humans: A combined TMS/EEG study , 2006, Brain Research Bulletin.

[27]  M. Massimini,et al.  Natural Frequencies of Human Corticothalamic Circuits , 2009, The Journal of Neuroscience.

[28]  John C Rothwell,et al.  Cortical oscillatory activity and the induction of plasticity in the human motor cortex , 2011, The European journal of neuroscience.

[29]  M. Bonnard,et al.  Cortical mechanisms underlying stretch reflex adaptation to intention: A combined EEG–TMS study , 2010, NeuroImage.

[30]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[31]  C. Miniussi,et al.  Transcranial magnetic stimulation and cortical evoked potentials: A TMS/EEG co-registration study , 2006, Clinical Neurophysiology.

[32]  Klaus Funke,et al.  Theta-Burst Transcranial Magnetic Stimulation Alters Cortical Inhibition , 2011, The Journal of Neuroscience.

[33]  J. Rothwell,et al.  The after-effect of human theta burst stimulation is NMDA receptor dependent , 2007, Clinical Neurophysiology.

[34]  J. Rothwell,et al.  Selective modulation of intracortical inhibition by low-intensity Theta Burst Stimulation , 2008, Clinical Neurophysiology.

[35]  Tomáš Paus,et al.  The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions , 2006, Experimental Brain Research.

[36]  Michael C. Ridding,et al.  A comparison of two different continuous theta burst stimulation paradigms applied to the human primary motor cortex , 2011, Clinical Neurophysiology.

[37]  R. J. Ilmoniemi,et al.  Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation , 1999, Medical & Biological Engineering & Computing.

[38]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.