Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: Current approaches and future perspectives

Non-invasive transcranial brain stimulation (NTBS) techniques such as transcranial magnetic stimulation (TMS) and transcranial current stimulation (TCS) are important tools in human systems and cognitive neuroscience because they are able to reveal the relevance of certain brain structures or neuronal activity patterns for a given brain function. It is nowadays feasible to combine NTBS, either consecutively or concurrently, with a variety of neuroimaging and electrophysiological techniques. Here we discuss what kind of information can be gained from combined approaches, which often are technically demanding. We argue that the benefit from this combination is twofold. Firstly, neuroimaging and electrophysiology can inform subsequent NTBS, providing the required information to optimize where, when, and how to stimulate the brain. Information can be achieved both before and during the NTBS experiment, requiring consecutive and concurrent applications, respectively. Secondly, neuroimaging and electrophysiology can provide the readout for neural changes induced by NTBS. Again, using either concurrent or consecutive applications, both "online" NTBS effects immediately following the stimulation and "offline" NTBS effects outlasting plasticity-inducing NTBS protocols can be assessed. Finally, both strategies can be combined to close the loop between measuring and modulating brain activity by means of closed-loop brain state-dependent NTBS. In this paper, we will provide a conceptual framework, emphasizing principal strategies and highlighting promising future directions to exploit the benefits of combining NTBS with neuroimaging or electrophysiology.

[1]  P. Schyns,et al.  Entrainment of Perceptually Relevant Brain Oscillations by Non-Invasive Rhythmic Stimulation of the Human Brain , 2011, Front. Psychology.

[2]  Y Kamitani,et al.  Effects of single-pulse transcranial magnetic stimulation (TMS) on functional brain activity: a combined event-related TMS and evoked potential study , 2003, Clinical Neurophysiology.

[3]  Christo Pantev,et al.  Magnetoencephalographic evidence for the modulation of cortical swallowing processing by transcranial direct current stimulation , 2013, NeuroImage.

[4]  Alexander Schlaefer,et al.  Towards direct head navigation for robot-guided Transcranial Magnetic Stimulation using 3D laserscans: Idea, setup and feasibility , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[5]  A. Antal,et al.  Transcranial alternating current stimulation (tACS) , 2013, Front. Hum. Neurosci..

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

[7]  Alexander Opitz,et al.  Determinants of the electric field during transcranial direct current stimulation , 2015, NeuroImage.

[8]  C. Gerloff,et al.  Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex , 2009, Neuropsychologia.

[9]  H. Morton,et al.  Stimulation of the cerebral cortex in the intact human subject , 1980, Nature.

[10]  C. Gerloff,et al.  Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency , 2003, The European journal of neuroscience.

[11]  K. Uludağ,et al.  Interleaved TMS/CASL: A motor cortex study , 2008, Brain Stimulation.

[12]  T. Ros,et al.  Tuning pathological brain oscillations with neurofeedback: a systems neuroscience framework , 2014, Front. Hum. Neurosci..

[13]  C. Schönfeldt-Lecuona,et al.  Accuracy of Stereotaxic Positioning of Transcranial Magnetic Stimulation , 2005, Brain Topography.

[14]  Thomas Dierks,et al.  Theta burst TMS increases cerebral blood flow in the primary motor cortex during motor performance as assessed by arterial spin labeling (ASL) , 2012, NeuroImage.

[15]  Abas Sabouni,et al.  BRAIN initiative: Transcranial magnetic stimulation automation and calibration , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[16]  J. Rothwell,et al.  Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study , 2001, Neuropsychologia.

[17]  J. Rothwell,et al.  Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity , 2000, Current Opinion in Neurobiology.

[18]  Hellmuth Obrig,et al.  Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy , 2003, NeuroImage.

[19]  Richard S. J. Frackowiak,et al.  Low-Frequency Transcranial Magnetic Stimulation over Left Dorsal Premotor Cortex Improves the Dynamic Control of Visuospatially Cued Actions , 2010, The Journal of Neuroscience.

[20]  M. Nitsche,et al.  Physiological Basis of Transcranial Direct Current Stimulation , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[21]  P. Brown,et al.  Phase dependent modulation of tremor amplitude in essential tremor through thalamic stimulation , 2013, Brain : a journal of neurology.

[22]  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.

[23]  J. Born,et al.  EEG-Guided Transcranial Magnetic Stimulation Reveals Rapid Shifts in Motor Cortical Excitability during the Human Sleep Slow Oscillation , 2012, The Journal of Neuroscience.

[24]  Abhishek Datta,et al.  Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: A basis for high-definition tDCS , 2013, NeuroImage.

[25]  Alan C. Evans,et al.  Transcranial Magnetic Stimulation during Positron Emission Tomography: A New Method for Studying Connectivity of the Human Cerebral Cortex , 1997, The Journal of Neuroscience.

[26]  U. Ziemann,et al.  A practical guide to diagnostic transcranial magnetic stimulation: Report of an IFCN committee , 2012, Clinical Neurophysiology.

[27]  Peter G. Morris,et al.  tDCS-induced alterations in GABA concentration within primary motor cortex predict motor learning and motor memory: A 7 T magnetic resonance spectroscopy study , 2014, NeuroImage.

[28]  Ulf Ziemann,et al.  TMS-EEG Signatures of GABAergic Neurotransmission in the Human Cortex , 2014, The Journal of Neuroscience.

[29]  H. Topka,et al.  Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types , 2001, Clinical Neurophysiology.

[30]  J. Schoenen,et al.  Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. , 2002, Brain : a journal of neurology.

[31]  V. Walsh,et al.  State-dependency in brain stimulation studies of perception and cognition , 2008, Trends in Cognitive Sciences.

[32]  L. Parra,et al.  Effects of weak transcranial alternating current stimulation on brain activity—a review of known mechanisms from animal studies , 2013, Front. Hum. Neurosci..

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

[34]  G. Rees,et al.  Individual Differences in Alpha Frequency Drive Crossmodal Illusory Perception , 2015, Current Biology.

[35]  Arno M. Janssen,et al.  The effect of local anatomy on the electric field induced by TMS: evaluation at 14 different target sites , 2014, Medical & Biological Engineering & Computing.

[36]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[37]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[38]  J. Born,et al.  Auditory Closed-Loop Stimulation of the Sleep Slow Oscillation Enhances Memory , 2013, Neuron.

[39]  S. Haber,et al.  Closed-Loop Deep Brain Stimulation Is Superior in Ameliorating Parkinsonism , 2011, Neuron.

[40]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[41]  L. Bindman,et al.  The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long‐lasting after‐effects , 1964, The Journal of physiology.

[42]  Thomas Kammer,et al.  Anisotropy in the visual cortex investigated by neuronavigated transcranial magnetic stimulation , 2007, NeuroImage.

[43]  Á. Pascual-Leone,et al.  A Review of Combined TMS-EEG Studies to Characterize Lasting Effects of Repetitive TMS and Assess Their Usefulness in Cognitive and Clinical Neuroscience , 2009, Brain Topography.

[44]  M. Hallett,et al.  Modeling the current distribution during transcranial direct current stimulation , 2006, Clinical Neurophysiology.

[45]  Walter Paulus,et al.  No correlation between moving phosphene and motor thresholds: a transcranial magnetic stimulation study. , 2004, Neuroreport.

[46]  Axel Thielscher,et al.  On the importance of electrode parameters for shaping electric field patterns generated by tDCS , 2015, NeuroImage.

[47]  Alexander Opitz,et al.  Electric field calculations in brain stimulation: The importance of geometrically accurate head models , 2012 .

[48]  Bernhard Strasser,et al.  A novel coil array for combined TMS/fMRI experiments at 3 T , 2014, Magnetic resonance in medicine.

[49]  Toralf Neuling,et al.  Friends, not foes: Magnetoencephalography as a tool to uncover brain dynamics during transcranial alternating current stimulation , 2015, NeuroImage.

[50]  M. Nicolelis,et al.  Global Forebrain Dynamics Predict Rat Behavioral States and Their Transitions , 2004, The Journal of Neuroscience.

[51]  Tracy R. Henderson,et al.  Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. , 2005, Journal of neurophysiology.

[52]  Á. Pascual-Leone,et al.  Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. , 2008, Cerebral cortex.

[53]  A. Chesson,et al.  The American Academy of Sleep Medicine (AASM) Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications , 2007 .

[54]  Rainer Goebel,et al.  Optimizing Functional Accuracy of TMS in Cognitive Studies: A Comparison of Methods , 2009, Journal of Cognitive Neuroscience.

[55]  P. Brown,et al.  Tremor Suppression by Rhythmic Transcranial Current Stimulation , 2013, Current Biology.

[56]  Tomás Paus,et al.  Combining Functional Neuroimaging with Off-line Brain Stimulation: Modulation of Task-related Activity in Language Areas , 2011, Journal of Cognitive Neuroscience.

[57]  R. Hanajima,et al.  Quadro-pulse stimulation is more effective than paired-pulse stimulation for plasticity induction of the human motor cortex , 2007, Clinical Neurophysiology.

[58]  Richard S. J. Frackowiak,et al.  Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. , 2003, Brain : a journal of neurology.

[59]  P. Matthews,et al.  Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation , 2009, The Journal of Neuroscience.

[60]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[61]  J. Rothwell,et al.  Consensus Paper: Probing Homeostatic Plasticity of Human Cortex With Non-invasive Transcranial Brain Stimulation , 2015, Brain Stimulation.

[62]  Guglielmo Foffani,et al.  Prefrontal hemodynamic changes produced by anodal direct current stimulation , 2010, NeuroImage.

[63]  L. Parra,et al.  Inter-Individual Variation during Transcranial Direct Current Stimulation and Normalization of Dose Using MRI-Derived Computational Models , 2012, Front. Psychiatry.

[64]  J. Lisman,et al.  Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer , 2005, Trends in Neurosciences.

[65]  Jörn M. Horschig,et al.  Hypothesis-driven methods to augment human cognition by optimizing cortical oscillations , 2014, Front. Syst. Neurosci..

[66]  Hartwig R. Siebner,et al.  BOLD MRI responses to repetitive TMS over human dorsal premotor cortex , 2005, NeuroImage.

[67]  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.

[68]  Kuniyoshi L. Sakai,et al.  An event-related optical topography study of cortical activation induced by single-pulse transcranial magnetic stimulation , 2003, NeuroImage.

[69]  Walter Paulus,et al.  Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study , 2011, NeuroImage.

[70]  P. Fitzgerald,et al.  A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition , 2006, Clinical Neurophysiology.

[71]  S. Jaberzadeh,et al.  Differential Modulation of Corticospinal Excitability by Different Current Densities of Anodal Transcranial Direct Current Stimulation , 2013, PloS one.

[72]  Karl J. Friston Functional integration and inference in the brain , 2002, Progress in Neurobiology.

[73]  Thomas Kammer,et al.  Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship , 1998, Neuropsychologia.

[74]  M. Nitsche,et al.  Shaping the effects of transcranial direct current stimulation of the human motor cortex. , 2007, Journal of neurophysiology.

[75]  G. Tononi,et al.  Triggering sleep slow waves by transcranial magnetic stimulation , 2007, Proceedings of the National Academy of Sciences.

[76]  Ole Jensen,et al.  Frontal Eye Fields Control Attentional Modulation of Alpha and Gamma Oscillations in Contralateral Occipitoparietal Cortex , 2015, The Journal of Neuroscience.

[77]  A. Chesson,et al.  The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Techinical Specifications , 2007 .

[78]  Kristoffer Hougaard Madsen,et al.  Monocular visual deprivation suppresses excitability in adult human visual cortex. , 2011, Cerebral cortex.

[79]  Sergiu Groppa,et al.  A novel dual-site transcranial magnetic stimulation paradigm to probe fast facilitatory inputs from ipsilateral dorsal premotor cortex to primary motor cortex , 2012, NeuroImage.

[80]  Marcello Massimini,et al.  General indices to characterize the electrical response of the cerebral cortex to TMS , 2010, NeuroImage.

[81]  G. Tononi,et al.  TMS-Induced Cortical Potentiation during Wakefulness Locally Increases Slow Wave Activity during Sleep , 2007, PloS one.

[82]  Wolfgang Rosenstiel,et al.  Coupling BCI and cortical stimulation for brain-state-dependent stimulation: methods for spectral estimation in the presence of stimulation after-effects , 2012, Front. Neural Circuits.

[83]  Alexander Opitz,et al.  Electric field calculations in brain stimulation based on finite elements: An optimized processing pipeline for the generation and usage of accurate individual head models , 2013, Human brain mapping.

[84]  J. Rothwell,et al.  Mapping causal interregional influences with concurrent TMS–fMRI , 2008, Experimental Brain Research.

[85]  Patrick Ragert,et al.  Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control , 2008, The Journal of physiology.

[86]  T. Paus,et al.  Repetitive Transcranial Magnetic Stimulation of the Human Prefrontal Cortex Induces Dopamine Release in the Caudate Nucleus , 2001, The Journal of Neuroscience.

[87]  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.

[88]  Walter Paulus,et al.  Transcranial direct current stimulation over the primary motor cortex during fMRI , 2011, NeuroImage.

[89]  Rolf Verleger,et al.  On how the motor cortices resolve an inter‐hemispheric response conflict: an event‐related EEG potential‐guided TMS study of the flankers task , 2009, The European journal of neuroscience.

[90]  J. Born,et al.  A local signature of LTP‐ and LTD‐like plasticity in human NREM sleep , 2008, The European journal of neuroscience.

[91]  Christoph Braun,et al.  Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS) , 2016, NeuroImage.

[92]  P. Miranda,et al.  Physics of effects of transcranial brain stimulation. , 2013, Handbook of clinical neurology.

[93]  Hartwig R. Siebner,et al.  Inter-subject and Inter-session Variability of Plasticity Induction by Non-invasive Brain Stimulation: Boon or Bane? , 2015, Brain Stimulation.

[94]  L. Marshall,et al.  Acute changes in motor cortical excitability during slow oscillatory and constant anodal transcranial direct current stimulation. , 2009, Journal of neurophysiology.

[95]  J. Rothwell,et al.  How does transcranial magnetic stimulation modify neuronal activity in the brain? Implications for studies of cognition , 2009, Cortex.

[96]  Risto J. Ilmoniemi,et al.  Projecting out muscle artifacts from TMS-evoked EEG , 2011, NeuroImage.

[97]  P. Schyns,et al.  Rhythmic TMS Causes Local Entrainment of Natural Oscillatory Signatures , 2011, Current Biology.

[98]  Rolf Pohmann,et al.  Uncovering a Context-Specific Connectional Fingerprint of Human Dorsal Premotor Cortex , 2012, The Journal of Neuroscience.

[99]  P. Rossini,et al.  Consensus paper: Combining transcranial stimulation with neuroimaging , 2009, Brain Stimulation.

[100]  Frank Padberg,et al.  Skin lesions after treatment with transcranial direct current stimulation (tDCS) , 2008, Brain Stimulation.

[101]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[102]  K. Harris,et al.  Cortical state and attention , 2011, Nature Reviews Neuroscience.

[103]  M. Ridding,et al.  Transcranial electric and magnetic stimulation: technique and paradigms. , 2013, Handbook of clinical neurology.

[104]  M. Nitsche,et al.  Transcranial direct current stimulation (tDCS) – Application in neuropsychology , 2015, Neuropsychologia.

[105]  S. Jaberzadeh,et al.  Does anodal transcranial direct current stimulation enhance excitability of the motor cortex and motor function in healthy individuals and subjects with stroke: A systematic review and meta-analysis , 2012, Clinical Neurophysiology.

[106]  Pascal Fries,et al.  Visual stimulus eccentricity affects human gamma peak frequency , 2013, NeuroImage.

[107]  Carlo Miniussi,et al.  What do you feel if I apply transcranial electric stimulation? Safety, sensations and secondary induced effects , 2015, Clinical Neurophysiology.

[108]  R. Töpper,et al.  Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging , 1999, Clinical Neurophysiology.

[109]  Romain Quentin,et al.  Corrigendum: Frontal eye field, where art thou? Anatomy, function, and non-invasive manipulation of frontal regions involved in eye movements and associated cognitive operations , 2014, Front. Integr. Neurosci..

[110]  Kristoffer Hougaard Madsen,et al.  Motivational Tuning of Fronto-Subthalamic Connectivity Facilitates Control of Action Impulses , 2014, The Journal of Neuroscience.

[111]  Christoph S. Herrmann,et al.  BOLD signal effects of transcranial alternating current stimulation (tACS) in the alpha range: A concurrent tACS–fMRI study , 2016, NeuroImage.

[112]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[113]  C. Herrmann,et al.  Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG , 2010, PloS one.

[114]  D. McCormick,et al.  Neural control of brain state , 2014, Current Opinion in Neurobiology.

[115]  M. Nitsche,et al.  Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence. , 2004, Investigative ophthalmology & visual science.

[116]  Tharshan Vaithianathan,et al.  Elevated haemoglobin levels in the motor cortex following 1 Hz transcranial magnetic stimulation: a preliminary study , 2007, Experimental Brain Research.

[117]  Sergiu Groppa,et al.  The human dorsal premotor cortex facilitates the excitability of ipsilateral primary motor cortex via a short latency cortico‐cortical route , 2012, Human brain mapping.

[118]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[119]  Sergiu Groppa,et al.  Manual activity shapes structure and function in contralateral human motor hand area , 2011, NeuroImage.

[120]  G. Tononi,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Repetitive Transcranial Magnetic Stimulation Affects Behavior by Biasing Endogenous Cortical Oscillations , 2022 .

[121]  Walter Paulus,et al.  Combining functional magnetic resonance imaging with transcranial electrical stimulation , 2013, Front. Hum. Neurosci..

[122]  Stefan Klöppel,et al.  The cortical motor threshold reflects microstructural properties of cerebral white matter , 2008, NeuroImage.

[123]  A. Antal,et al.  Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans , 2008, Brain Stimulation.

[124]  A. Drzezga,et al.  Continuous Transcranial Magnetic Stimulation during Positron Emission Tomography: A Suitable Tool for Imaging Regional Excitability of the Human Cortex , 2001, NeuroImage.

[125]  Jyrki P. Mäkelä,et al.  Reproducibility of TMS—Evoked EEG responses , 2009, Human brain mapping.

[126]  Rüdiger Hilker,et al.  The relationship between TMS measures of functional properties and DTI measures of microstructure of the corticospinal tract , 2012, Brain Stimulation.

[127]  Richard S. J. Frackowiak,et al.  How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? , 2005, The European journal of neuroscience.

[128]  O. Jensen,et al.  University of Birmingham Attention Modulates TMS-Locked Alpha Oscillations in the Visual Cortex , 2015 .

[129]  David Poeppel,et al.  Systematic latency variation of the auditory evoked M100: from average to single-trial data , 2004, NeuroImage.

[130]  L. Cohen,et al.  In vivo assessment of human brain oscillations during application of transcranial electric currents , 2013, Nature Communications.

[131]  Giulio Ruffini,et al.  Optimization of multifocal transcranial current stimulation for weighted cortical pattern targeting from realistic modeling of electric fields , 2014, NeuroImage.

[132]  S. Rossi,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee , 2015, Clinical Neurophysiology.

[133]  Walter Paulus,et al.  Functional Neuroimaging and Transcranial Electrical Stimulation , 2012, Clinical EEG and neuroscience.

[134]  C. Herrmann,et al.  Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes , 2013, Front. Hum. Neurosci..

[135]  C. Price,et al.  Perturbation of the left inferior frontal gyrus triggers adaptive plasticity in the right homologous area during speech production , 2013, Proceedings of the National Academy of Sciences.

[136]  Risto J. Ilmoniemi,et al.  Methodology for Combined TMS and EEG , 2009, Brain Topography.

[137]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

[138]  Á. Pascual-Leone,et al.  Microstates in resting-state EEG: Current status and future directions , 2015, Neuroscience & Biobehavioral Reviews.

[139]  A. Destexhe,et al.  Are corticothalamic ‘up’ states fragments of wakefulness? , 2007, Trends in Neurosciences.

[140]  Matti Stenroos,et al.  Uncovering neural independent components from highly artifactual TMS-evoked EEG data , 2012, Journal of Neuroscience Methods.

[141]  G. Tononi,et al.  Sleep function and synaptic homeostasis. , 2006, Sleep medicine reviews.

[142]  Axel Thielscher,et al.  Modeling the effects of noninvasive transcranial brain stimulation at the biophysical, network, and cognitive level. , 2015, Progress in brain research.

[143]  Nathan Weisz,et al.  Probing of Brain States in Real-Time: Introducing the ConSole Environment , 2011, Front. Psychology.

[144]  Gregor Thut,et al.  Alpha Power Increase After Transcranial Alternating Current Stimulation at Alpha Frequency (α-tACS) Reflects Plastic Changes Rather Than Entrainment , 2015, Brain Stimulation.

[145]  Robert J. Zatorre,et al.  Mapping interhemispheric connectivity using functional MRI after transcranial magnetic stimulation on the human auditory cortex , 2013, NeuroImage.

[146]  C. Price,et al.  Phonological decisions require both the left and right supramarginal gyri , 2010, Proceedings of the National Academy of Sciences.

[147]  Kenneth D. Harris,et al.  Top-Down Control of Cortical State , 2013, Neuron.

[148]  Rainer Goebel,et al.  On the feasibility of concurrent human TMS-EEG-fMRI measurements. , 2013, Journal of neurophysiology.

[149]  N. Parks Concurrent application of TMS and near-infrared optical imaging: methodological considerations and potential artifacts , 2013, Front. Hum. Neurosci..

[150]  T. Paus,et al.  Transcranial magnetic stimulation and the challenge of coil placement: A comparison of conventional and stereotaxic neuronavigational strategies , 2008, Human brain mapping.

[151]  M. Iacoboni,et al.  Correlation between motor and phosphene thresholds: A transcranial magnetic stimulation study , 2008, Human brain mapping.

[152]  Alexander Opitz,et al.  How the brain tissue shapes the electric field induced by transcranial magnetic stimulation , 2011, NeuroImage.

[153]  M. Belluscio,et al.  Closed-Loop Control of Epilepsy by Transcranial Electrical Stimulation , 2012, Science.

[154]  Thomas Martinetz,et al.  Driving Sleep Slow Oscillations by Auditory Closed-Loop Stimulation—A Self-Limiting Process , 2015, The Journal of Neuroscience.

[155]  P. Bandettini,et al.  What's New in Neuroimaging Methods? , 2009, Annals of the New York Academy of Sciences.

[156]  F. Tecchio,et al.  Personalizing the Electrode to Neuromodulate an Extended Cortical Region , 2015, Brain Stimulation.

[157]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[158]  D. Frey,et al.  A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values , 2012, NeuroImage.

[159]  Tipu Z. Aziz,et al.  Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance , 2012, Current Biology.

[160]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

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

[162]  Walter Paulus,et al.  Transcranial direct current stimulation and the visual cortex , 2006, Brain Research Bulletin.

[163]  J. Rothwell,et al.  Consensus: Motor cortex plasticity protocols , 2008, Brain Stimulation.

[164]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[165]  P. Haggard,et al.  Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. , 2008, Cerebral cortex.

[166]  Risto J. Ilmoniemi,et al.  The Effect of Stimulus Parameters on TMS–EEG Muscle Artifacts , 2013, Brain Stimulation.

[167]  Gesa Hartwigsen,et al.  The neurophysiology of language: Insights from non-invasive brain stimulation in the healthy human brain , 2015, Brain and Language.

[168]  Angelo Cappello,et al.  Transcranial direct current stimulation and power spectral parameters: a tDCS/EEG co-registration study , 2014, Front. Hum. Neurosci..

[169]  Vedran Deletis,et al.  Inducing transient language disruptions by mapping of Broca's area with modified patterned repetitive transcranial magnetic stimulation protocol. , 2014, Journal of neurosurgery.

[170]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[171]  Á. Pascual-Leone,et al.  Transcranial Magnetic Stimulation , 2014, Neuromethods.

[172]  Jukka Sarvas,et al.  Removal of large muscle artifacts from transcranial magnetic stimulation-evoked EEG by independent component analysis , 2011, Medical & Biological Engineering & Computing.

[173]  Robert Oostenveld,et al.  Using Brain–Computer Interfaces and Brain-State Dependent Stimulation as Tools in Cognitive Neuroscience , 2011, Front. Psychology.

[174]  Paul B. Fitzgerald,et al.  Removing artefacts from TMS-EEG recordings using independent component analysis: Importance for assessing prefrontal and motor cortex network properties , 2014, NeuroImage.

[175]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[176]  C. Herrmann,et al.  Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states , 2013, Front. Hum. Neurosci..

[177]  R. VanRullen,et al.  The Phase of Ongoing Oscillations Mediates the Causal Relation between Brain Excitation and Visual Perception , 2011, The Journal of Neuroscience.

[178]  Babak Boroojerdi,et al.  Pharmacologic Influences on TMS Effects , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[179]  Ryota Kanai,et al.  Transcranial alternating current stimulation (tACS) modulates cortical excitability as assessed by TMS-induced phosphene thresholds , 2010, Clinical Neurophysiology.

[180]  Jing Fang,et al.  Direct current stimulation over the human sensorimotor cortex modulates the brain's hemodynamic response to tactile stimulation , 2015, The European journal of neuroscience.

[181]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[182]  R. Verleger,et al.  Responsiveness to distracting stimuli, though increased in Parkinson's disease, is decreased in asymptomatic PINK1 and Parkin mutation carriers , 2010, Neuropsychologia.

[183]  Paolo Belardinelli,et al.  Characterization of GABAB-receptor mediated neurotransmission in the human cortex by paired-pulse TMS–EEG , 2014, NeuroImage.

[184]  M. Nitsche,et al.  Partially non‐linear stimulation intensity‐dependent effects of direct current stimulation on motor cortex excitability in humans , 2013, The Journal of physiology.

[185]  Alexander Opitz,et al.  Impact of the gyral geometry on the electric field induced by transcranial magnetic stimulation , 2011, NeuroImage.

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

[187]  Romain Quentin,et al.  Frontal eye field, where art thou? Anatomy, function, and non-invasive manipulation of frontal regions involved in eye movements and associated cognitive operations , 2014, Front. Integr. Neurosci..

[188]  Ned T. Sahin,et al.  Dynamic circuit motifs underlying rhythmic gain control, gating and integration , 2014, Nature Neuroscience.

[189]  Niels Birbaumer,et al.  Enhancing Hebbian Learning to Control Brain Oscillatory Activity. , 2015, Cerebral cortex.

[190]  J. Gross,et al.  On the Role of Prestimulus Alpha Rhythms over Occipito-Parietal Areas in Visual Input Regulation: Correlation or Causation? , 2010, The Journal of Neuroscience.

[191]  Laurent Goffin,et al.  A custom robot for Transcranial Magnetic Stimulation: First assessment on healthy subjects , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[192]  B. Meyer,et al.  Evaluation of cortical excitability by motor and phosphene thresholds in transcranial magnetic stimulation , 2003, Journal of the Neurological Sciences.

[193]  A. Schnitzler,et al.  The effect of 10 Hz transcranial alternating current stimulation (tACS) on corticomuscular coherence , 2013, Front. Hum. Neurosci..

[194]  A. Antal,et al.  Close to threshold transcranial electrical stimulation preferentially activates inhibitory networks before switching to excitation with higher intensities , 2012, Brain Stimulation.

[195]  O. Carter,et al.  Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: A systematic review , 2015, Neuropsychologia.

[196]  Ole Jensen,et al.  On the relationship between cortical excitability and visual oscillatory responses — A concurrent tDCS–MEG study , 2016, NeuroImage.

[197]  Y. Dan,et al.  Neuromodulation of Brain States , 2012, Neuron.

[198]  Felice T. Sun,et al.  Closed-loop Neurostimulation: The Clinical Experience , 2014, Neurotherapeutics.

[199]  M. Nitsche,et al.  Modulating cortico‐striatal and thalamo‐cortical functional connectivity with transcranial direct current stimulation , 2012, Human brain mapping.

[200]  B. Meyer,et al.  nTMS-based DTI fiber tracking for language pathways correlates with language function and aphasia – A case report , 2015, Clinical Neurology and Neurosurgery.

[201]  Tony Ro,et al.  Locating the Human Frontal Eye Fields With Transcranial Magnetic Stimulation , 2002, Journal of clinical and experimental neuropsychology.

[202]  Maarten De Vos,et al.  Let's face it, from trial to trial: Comparing procedures for N170 single-trial estimation , 2012, NeuroImage.

[203]  M. Erb,et al.  The influence of current direction on phosphene thresholds evoked by transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

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

[205]  I. Toni,et al.  Anterior Prefrontal Cortex Inhibition Impairs Control over Social Emotional Actions , 2011, Current Biology.

[206]  A. Barker,et al.  NON-INVASIVE MAGNETIC STIMULATION OF HUMAN MOTOR CORTEX , 1985, The Lancet.

[207]  R. Cohen Kadosh,et al.  Long-Term Enhancement of Brain Function and Cognition Using Cognitive Training and Brain Stimulation , 2013, Current Biology.

[208]  R. Ilmoniemi,et al.  Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity , 1997, Neuroreport.

[209]  A. Thiel,et al.  Bilateral Transcranial Direct Current Stimulation Modulates Activation-Induced Regional Blood Flow Changes during Voluntary Movement , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[210]  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.

[211]  C. Kennard,et al.  Current orientation induced by magnetic stimulation influences a cognitive task , 2000, Neuroreport.

[212]  Jens Frahm,et al.  Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS , 2003, NeuroImage.

[213]  O. Carter,et al.  Quantitative Review Finds No Evidence of Cognitive Effects in Healthy Populations From Single-session Transcranial Direct Current Stimulation (tDCS) , 2015, Brain Stimulation.

[214]  Lucia M. Li,et al.  The contribution of interindividual factors to variability of response in transcranial direct current stimulation studies , 2015, Front. Cell. Neurosci..