Annals of the New York Academy of Sciences Combined Neurostimulation and Neuroimaging in Cognitive Neuroscience: Past, Present, and Future

Modern neurostimulation approaches in humans provide controlled inputs into the operations of cortical regions, with highly specific behavioral consequences. This enables causal structure–function inferences, and in combination with neuroimaging, has provided novel insights into the basic mechanisms of action of neurostimulation on distributed networks. For example, more recent work has established the capacity of transcranial magnetic stimulation (TMS) to probe causal interregional influences, and their interaction with cognitive state changes. Combinations of neurostimulation and neuroimaging now face the challenge of integrating the known physiological effects of neurostimulation with theoretical and biological models of cognition, for example, when theoretical stalemates between opposing cognitive theories need to be resolved. This will be driven by novel developments, including biologically informed computational network analyses for predicting the impact of neurostimulation on brain networks, as well as novel neuroimaging and neurostimulation techniques. Such future developments may offer an expanded set of tools with which to investigate structure–function relationships, and to formulate and reconceptualize testable hypotheses about complex neural network interactions and their causal roles in cognition.

[1]  M. Rushworth,et al.  Functionally Specific Reorganization in Human Premotor Cortex , 2007, Neuron.

[2]  R. Lemon,et al.  State of the art: Physiology of transcranial motor cortex stimulation , 2008, Brain Stimulation.

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

[4]  Sven Bestmann,et al.  Concurrent brain-stimulation and neuroimaging for studies of cognition , 2009, Trends in Cognitive Sciences.

[5]  J. Rothwell,et al.  Speech Facilitation by Left Inferior Frontal Cortex Stimulation , 2011, Current Biology.

[6]  J C Rothwell,et al.  I-Waves in Motor Cortex , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[7]  A. Antal,et al.  Investigating Neuroplastic Changes in the Human Brain Induced by Transcranial Direct (tDCS) and Alternating Current (tACS) Stimulation Methods , 2012, Clinical EEG and neuroscience.

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

[9]  Taraz G. Lee,et al.  The Dynamic Nature of Top-Down Signals Originating from Prefrontal Cortex: A Combined fMRI–TMS Study , 2012, The Journal of Neuroscience.

[10]  Yusuf Tufail,et al.  Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound , 2011, Nature Protocols.

[11]  Karl J. Friston Modalities, Modes, and Models in Functional Neuroimaging , 2009, Science.

[12]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[13]  Karl J. Friston,et al.  Population dynamics under the Laplace assumption , 2009, NeuroImage.

[14]  Heidi Johansen-Berg,et al.  What are we measuring with GABA magnetic resonance spectroscopy? , 2011, Communicative & integrative biology.

[15]  P. Jezzard,et al.  Neurochemical Effects of Theta Burst Stimulation as Assessed by Magnetic Resonance Spectroscopy , 2009, Journal of neurophysiology.

[16]  Mark D'Esposito,et al.  The Prefrontal Cortex Modulates Category Selectivity in Human Extrastriate Cortex , 2011, Journal of Cognitive Neuroscience.

[17]  Kerstin Irlbacher,et al.  Influence of ipsilateral transcranial magnetic stimulation on the triphasic EMG pattern accompanying fast ballistic movements in humans , 2006, The Journal of physiology.

[18]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

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

[20]  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.

[21]  R. Deichmann,et al.  Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. , 2008, Cerebral cortex.

[22]  Karl J. Friston,et al.  Neural Coding of Tactile Decisions in the Human Prefrontal Cortex , 2006, The Journal of Neuroscience.

[23]  E. J. Tehovnik,et al.  Direct and indirect activation of cortical neurons by electrical microstimulation. , 2006, Journal of neurophysiology.

[24]  Gregor Thut,et al.  Alpha-generation as basic response-signature to transcranial magnetic stimulation (TMS) targeting the human resting motor cortex: a TMS/EEG co-registration study. , 2011, Psychophysiology.

[25]  E. J. Tehovnik,et al.  Mapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque , 2005, Neuron.

[26]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[27]  Gregor Thut,et al.  A new device and protocol for combining TMS and online recordings of EEG and evoked potentials , 2005, Journal of Neuroscience Methods.

[28]  John C. Rothwell,et al.  State of the art: Pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation , 2008, Brain Stimulation.

[29]  J C Rothwell,et al.  Effect of tonic voluntary activity on the excitability of human motor cortex. , 1994, The Journal of physiology.

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

[31]  A. Thielscher,et al.  Determining the cortical target of transcranial magnetic stimulation , 2009, NeuroImage.

[32]  Raymond J. Dolan,et al.  Alterations in Brain Connectivity Underlying Beta Oscillations in Parkinsonism , 2011, PLoS Comput. Biol..

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

[34]  Sven Bestmann,et al.  Rapid Modulation of Distributed Brain Activity by Transcranial Magnetic Stimulation of Human Motor Cortex , 2006, Behavioural neurology.

[35]  Sven Bestmann,et al.  Left Dorsal Premotor Cortex and Supramarginal Gyrus Complement Each Other during Rapid Action Reprogramming , 2012, The Journal of Neuroscience.

[36]  Jeffrey S. Johnson,et al.  Task-dependent changes in cortical excitability and effective connectivity: a combined TMS-EEG study. , 2012, Journal of neurophysiology.

[37]  V. Amassian,et al.  Measurement of information processing delays in human visual cortex with repetitive magnetic coil stimulation , 1993, Brain Research.

[38]  J C Rothwell,et al.  Relationship between physiological measures of excitability and levels of glutamate and GABA in the human motor cortex , 2011, The Journal of physiology.

[39]  Nikolaus Weiskopf,et al.  Causal evidence for frontal involvement in memory target maintenance by posterior brain areas during distracter interference of visual working memory , 2011, Proceedings of the National Academy of Sciences.

[40]  A. Bompas,et al.  More GABA, less distraction: a neurochemical predictor of motor decision speed , 2010, Nature Neuroscience.

[41]  V. Amassian,et al.  Suppression of visual perception by magnetic coil stimulation of human occipital cortex. , 1989, Electroencephalography and clinical neurophysiology.

[42]  M. Nitsche,et al.  The Importance of Timing in Segregated Theta Phase-Coupling for Cognitive Performance , 2012, Current Biology.

[43]  M. Rushworth,et al.  A primer of magnetic stimulation as a tool for neuropsychology. , 1999, Neuropsychologia.

[44]  K. Welch,et al.  Brain excitability in migraine: evidence from transcranial magnetic stimulation studies. , 1998, Current opinion in neurology.

[45]  M. Siegel,et al.  A framework for local cortical oscillation patterns , 2011, Trends in Cognitive Sciences.

[46]  R. Deichmann,et al.  Image Artifacts in Concurrent Transcranial Magnetic Stimulation (TMS) and fMRI Caused by Leakage Currents: Modeling and Compensation , 2009, Journal of magnetic resonance imaging : JMRI.

[47]  John C. Rothwell,et al.  Time Course of Functional Connectivity between Dorsal Premotor and Contralateral Motor Cortex during Movement Selection , 2006, The Journal of Neuroscience.

[48]  Robert E. Lenkinski,et al.  Recent advances in magnetic resonance neurospectroscopy , 2007, Neurotherapeutics.

[49]  Abhishek Datta,et al.  Imaging artifacts induced by electrical stimulation during conventional fMRI of the brain , 2014, NeuroImage.

[50]  Sven Bestmann,et al.  Concurrent TMS and functional magnetic resonance imaging: methods and current advances , 2008 .

[51]  W Paulus,et al.  Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation , 2001, Magnetic resonance in medicine.

[52]  V E Amassian,et al.  Human cerebral cortical responses to contralateral transcranial stimulation. , 1987, Neurosurgery.

[53]  Petroc Sumner,et al.  Individual Differences in Subconscious Motor Control Predicted by GABA Concentration in SMA , 2010, Current Biology.

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

[55]  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.

[56]  Sven Bestmann,et al.  Studying the Role of Human Parietal Cortex in Visuospatial Attention with Concurrent TMS–fMRI , 2010, Cerebral cortex.

[57]  R J Ilmoniemi,et al.  Transcranial magnetic stimulation--a new tool for functional imaging of the brain. , 1999, Critical reviews in biomedical engineering.

[58]  Z. Cattaneo,et al.  Investigating visual motion perception using the transcranial magnetic stimulation-adaptation paradigm , 2008, Neuroreport.

[59]  Ziad Nahas,et al.  A combined TMS/fMRI study of intensity-dependent TMS over motor cortex , 1999, Biological Psychiatry.

[60]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[61]  Ulf Ziemann,et al.  TMS and drugs , 2004, Clinical Neurophysiology.

[62]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[63]  Rolf Pohmann,et al.  Effects of parietal TMS on visual and auditory processing at the primary cortical level -- a concurrent TMS-fMRI study. , 2013, Cerebral cortex.

[64]  C. Marsden,et al.  Corticocortical inhibition in human motor cortex. , 1993, The Journal of physiology.

[65]  S. Treue,et al.  Transcranial alternating stimulation in a high gamma frequency range applied over V1 improves contrast perception but does not modulate spatial attention , 2012, Brain Stimulation.

[66]  H. Johansen-Berg,et al.  The Role of GABA in Human Motor Learning , 2011, Current Biology.

[67]  C. Epstein,et al.  Mapping transcranial magnetic stimulation (TMS) fields in vivo with MRI , 1997, Neuroreport.

[68]  Tomás Paus,et al.  Inferring causality in brain images: a perturbation approach , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses: The role of intrinsic connections , 2007, NeuroImage.

[70]  Anna C Nobre,et al.  Subsecond Changes in Top–Down Control Exerted by Human Medial Frontal Cortex during Conflict and Action Selection: A Combined Transcranial Magnetic Stimulation–Electroencephalography Study , 2007, The Journal of Neuroscience.

[71]  J. Lorberbaum,et al.  BOLD‐fMRI response vs. transcranial magnetic stimulation (TMS) pulse‐train length: Testing for linearity , 2003, Journal of magnetic resonance imaging : JMRI.

[72]  R. Goebel,et al.  Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. , 2007, Cerebral cortex.

[73]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[74]  Ethan R. Buch,et al.  Distributed and causal influence of frontal operculum in task control , 2011, Proceedings of the National Academy of Sciences.

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

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

[77]  R. J. Ilmoniemi,et al.  Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans , 2005, NeuroImage.

[78]  A. Karim,et al.  Brain Oscillatory Substrates of Visual Short-Term Memory Capacity , 2009, Current Biology.

[79]  Jacob G. Bernstein,et al.  Optogenetic tools for analyzing the neural circuits of behavior , 2011, Trends in Cognitive Sciences.

[80]  Raymond J. Dolan,et al.  Consistent spectral predictors for dynamic causal models of steady-state responses , 2011, NeuroImage.

[82]  S. Tillery,et al.  Transcranial Pulsed Ultrasound Stimulates Intact Brain Circuits , 2010, Neuron.

[83]  M. Bikson,et al.  Computational Models of Transcranial Direct Current Stimulation , 2012, Clinical EEG and neuroscience.

[84]  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.

[85]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[86]  P. Matthews,et al.  Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning , 2011, Neuropsychologia.

[87]  Tirin Moore,et al.  Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field , 2007, Proceedings of the National Academy of Sciences.

[88]  T. Paus,et al.  Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. , 2003, Brain : a journal of neurology.

[89]  Abhishek Datta,et al.  High‐Resolution Modeling Assisted Design of Customized and Individualized Transcranial Direct Current Stimulation Protocols , 2012, Neuromodulation : journal of the International Neuromodulation Society.

[90]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[91]  M. Bikson,et al.  Electrodes for high-definition transcutaneous DC stimulation for applications in drug delivery and electrotherapy, including tDCS , 2010, Journal of Neuroscience Methods.

[92]  Christopher D. Chambers,et al.  Reducing image artefacts in concurrent TMS/fMRI by passive shimming , 2012, NeuroImage.

[93]  Alan P. Rudell,et al.  Unmasking human visual perception with the magnetic coil and its relationship to hemispheric asymmetry , 1993, Brain Research.

[94]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[95]  M. Nitsche,et al.  Comparing Cortical Plasticity Induced by Conventional and High-Definition 4 × 1 Ring tDCS: A Neurophysiological Study , 2013, Brain Stimulation.

[96]  Sven Bestmann,et al.  Concurrent TMS–fMRI reveals dynamic interhemispheric influences of the right parietal cortex during exogenously cued visuospatial attention , 2011, The European journal of neuroscience.

[97]  Giulio Tononi,et al.  Evaluating the role of prefrontal and parietal cortices in memory-guided response with repetitive transcranial magnetic stimulation , 2009, Neuropsychologia.

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

[99]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[100]  P. Matthews,et al.  Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. , 2006, Journal of neurophysiology.

[101]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

[102]  Karl J. Friston,et al.  Dynamic causal modelling of induced responses , 2008, NeuroImage.

[103]  Takashi Hanakawa,et al.  Time course and spatial distribution of fMRI signal changes during single-pulse transcranial magnetic stimulation to the primary motor cortex , 2011, NeuroImage.

[104]  R. Ricci,et al.  Using interleaved transcranial magnetic stimulation/functional magnetic resonance imaging (fMRI) and dynamic causal modeling to understand the discrete circuit specific changes of medications: Lamotrigine and valproic acid changes in motor or prefrontal effective connectivity , 2011, Psychiatry Research: Neuroimaging.

[105]  P. Thompson,et al.  Motor cortex stimulation in intact man. 2. Multiple descending volleys. , 1987, Brain : a journal of neurology.

[106]  Dae-Shik Kim,et al.  Global and local fMRI signals driven by neurons defined optogenetically by type and wiring , 2010, Nature.

[107]  Stephen M. Smith,et al.  The future of FMRI connectivity , 2012, NeuroImage.

[108]  Risto J. Ilmoniemi,et al.  TMS and electroencephalography: methods and current advances , 2008 .

[109]  Brian N. Pasley,et al.  Transcranial Magnetic Stimulation Elicits Coupled Neural and Hemodynamic Consequences , 2007, Science.

[110]  John C. Rothwell,et al.  Transcranial Magnetic Stimulation Can Be Used to Test Connections to Primary Motor Areas from Frontal and Medial Cortex in Humans , 2001, NeuroImage.

[111]  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.

[112]  J. Rothwell,et al.  The physiological basis of transcranial motor cortex stimulation in conscious humans , 2004, Clinical Neurophysiology.

[113]  Nikolaus Kriegeskorte,et al.  Relating Population-Code Representations between Man, Monkey, and Computational Models , 2009, Front. Neurosci..

[114]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

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

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

[117]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

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

[119]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[120]  S. Bestmann,et al.  Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS) , 2001, Neuroreport.

[121]  Sauli Savolainen,et al.  Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation , 2002, Clinical Neurophysiology.

[122]  M. Corbetta,et al.  Differential contribution of right and left parietal cortex to the control of spatial attention: a simultaneous EEG-rTMS study. , 2012, Cerebral cortex.

[123]  M. Bikson,et al.  Electrode montages for tDCS and weak transcranial electrical stimulation: Role of “return” electrode’s position and size , 2010, Clinical Neurophysiology.

[124]  J. Driver,et al.  Combining TMS and fMRI: From ‘virtual lesions’ to functional-network accounts of cognition , 2009, Cortex.

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

[126]  A. Nobre,et al.  Effects of Decision Variables and Intraparietal Stimulation on Sensorimotor Oscillatory Activity in the Human Brain , 2012, The Journal of Neuroscience.

[127]  L. Hunt,et al.  A mechanism for value-guided choice based on the excitation-inhibition balance in prefrontal cortex , 2012, Nature Neuroscience.

[128]  Rolf Pohmann,et al.  Interleaved TMS/CASL: Comparison of different rTMS protocols , 2009, NeuroImage.

[129]  Rolf Pohmann,et al.  New coil positioning method for interleaved transcranial magnetic stimulation (TMS)/functional MRI (fMRI) and its validation in a motor cortex study , 2009, Journal of magnetic resonance imaging : JMRI.

[130]  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.

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

[132]  S. Lipton,et al.  High-Frequency Hippocampal Oscillations Activated by Optogenetic Stimulation of Transplanted Human ESC-Derived Neurons , 2012, The Journal of Neuroscience.

[133]  Takashi Hanakawa,et al.  Stimulus-response profile during single-pulse transcranial magnetic stimulation to the primary motor cortex. , 2009, Cerebral cortex.

[134]  J. Rothwell,et al.  Interaction between intracortical inhibition and facilitation in human motor cortex. , 1996, The Journal of physiology.

[135]  Karl J. Friston,et al.  Dynamic Causal Models for phase coupling , 2009, Journal of Neuroscience Methods.

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

[137]  H. Johansen-Berg,et al.  Imaging the effects of rTMS-induced cortical plasticity. , 2010, Restorative neurology and neuroscience.

[138]  Marco Davare,et al.  Ventral premotor to primary motor cortical interactions during object-driven grasp in humans , 2009, Cortex.

[139]  Daryl E Bohning,et al.  A TMS coil positioning/holding system for MR image-guided TMS interleaved with fMRI , 2003, Clinical Neurophysiology.

[140]  V E Amassian,et al.  Comparison of human transcallosal responses evoked by magnetic coil and electrical stimulation. , 1989, Electroencephalography and clinical neurophysiology.

[141]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

[142]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

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

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

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

[146]  Steven Lemm,et al.  A novel mechanism for evoked responses in the human brain , 2007, The European journal of neuroscience.

[147]  Walter Paulus,et al.  Transcranial alternating current stimulation in the low kHz range increases motor cortex excitability. , 2011, Restorative neurology and neuroscience.

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

[149]  J. Rothwell,et al.  Effects of paired pulse TMS of primary somatosensory cortex on perception of a peripheral electrical stimulus , 2006, Experimental Brain Research.

[150]  Gregor Thut,et al.  Preperceptual and Stimulus-Selective Enhancement of Low-Level Human Visual Cortex Excitability by Sounds , 2009, Current Biology.

[151]  John C. Rothwell,et al.  Behavioral/systems/cognitive Functional Interplay between Posterior Parietal and Ipsilateral Motor Cortex Revealed by Twin-coil Transcranial Magnetic Stimulation during Reach Planning toward Contralateral Space , 2022 .

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

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

[154]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

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

[156]  Amit P. Mulgaonkar,et al.  A review of low-intensity focused ultrasound pulsation , 2011, Brain Stimulation.

[157]  K. Iramina,et al.  Differences in evoked EEG by transcranial magnetic stimulation at various stimulus points on the head , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[158]  Colin Blakemore,et al.  Spatial Attention Changes Excitability of Human Visual Cortex to Direct Stimulation , 2007, Current Biology.

[159]  J. Rothwell,et al.  Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex , 2004, The Journal of physiology.

[160]  I. Yaar EEG power spectral changes secondary to L-DOPA treatment in parkinsonian patients: a pilot study. , 1977, Electroencephalography and clinical neurophysiology.

[161]  A. T. Sack,et al.  Multimodal transcranial magnetic stimulation: Using concurrent neuroimaging to reveal the neural network dynamics of noninvasive brain stimulation , 2011, Progress in Neurobiology.

[162]  Vladimir Litvak,et al.  Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex , 2007, NeuroImage.

[163]  Nikolaus Weiskopf,et al.  Hemispheric Differences in Frontal and Parietal Influences on Human Occipital Cortex: Direct Confirmation with Concurrent TMS–fMRI , 2009, Journal of Cognitive Neuroscience.

[164]  P. Thompson,et al.  Motor cortex stimulation in intact man. 1. General characteristics of EMG responses in different muscles. , 1987, Brain : a journal of neurology.

[165]  C. Epstein,et al.  The Oxford handbook of transcranial stimulation , 2012 .

[166]  Walter Paulus,et al.  Transcranial direct current stimulation--update 2011. , 2011, Restorative neurology and neuroscience.

[167]  Sean L. Hill,et al.  Modeling the effects of transcranial magnetic stimulation on cortical circuits. , 2005, Journal of neurophysiology.

[168]  J. Rothwell,et al.  The after effects of motor cortex rTMS depend on the state of contraction when rTMS is applied , 2004, Clinical Neurophysiology.

[169]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[170]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[171]  Nikolaus Weiskopf,et al.  Interhemispheric Effect of Parietal TMS on Somatosensory Response Confirmed Directly with Concurrent TMS–fMRI , 2008, The Journal of Neuroscience.

[172]  S. Bestmann,et al.  On the synchronization of transcranial magnetic stimulation and functional echo‐planar imaging , 2003, Journal of magnetic resonance imaging : JMRI.

[173]  J. Karhu,et al.  EEG responses evoked by transcranial magnetic stimulation. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[174]  J. Rothwell,et al.  Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits , 2004, The European journal of neuroscience.

[175]  D. Bohning,et al.  Cortical and subcortical brain effects of Transcranial Magnetic Stimulation (TMS)-induced movement: An interleaved TMS/functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[176]  B L Day,et al.  Some experiences of techniques for stimulation of the human cerebral motor cortex through the scalp. , 1987, Neurosurgery.

[177]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[178]  M. Nitsche,et al.  Dopaminergic Impact on Cortical Excitability in Humans , 2010, Reviews in the neurosciences.

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

[180]  Sven Bestmann,et al.  Muscle and Timing-specific Functional Connectivity between the Dorsolateral Prefrontal Cortex and the Primary Motor Cortex , 2013, Journal of Cognitive Neuroscience.

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

[182]  Walter Paulus,et al.  Boosting brain excitability by transcranial high frequency stimulation in the ripple range , 2010, The Journal of physiology.

[183]  P. Dechent,et al.  Cortical correlates of TMS-induced phantom hand movements revealed with concurrent TMS-fMRI , 2006, Neuropsychologia.

[184]  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.

[185]  N. Logothetis,et al.  The effects of electrical microstimulation on cortical signal propagation , 2010, Nature Neuroscience.

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

[187]  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.

[188]  Juha Silvanto,et al.  Neural adaptation reveals state‐dependent effects of transcranial magnetic stimulation , 2007, The European journal of neuroscience.

[189]  G. Thut,et al.  Noninvasive Brain Stimulation and Neuroimaging: Novel Ways of Assessing Causal Relationships in Brain Networks , 2012 .

[190]  Bruce T Volpe,et al.  Transcranial magnetic stimulation, synaptic plasticity and network oscillations , 2009, Journal of NeuroEngineering and Rehabilitation.

[191]  K. Mills,et al.  Magnetic and electrical transcranial brain stimulation: physiological mechanisms and clinical applications. , 1987, Neurosurgery.

[192]  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.

[193]  J. L. Taylor,et al.  The effect of voluntary contraction on cortico‐cortical inhibition in human motor cortex. , 1995, The Journal of physiology.

[194]  Karl J. Friston,et al.  Repetitive Transcranial Magnetic Stimulation-Induced Changes in Sensorimotor Coupling Parallel Improvements of Somatosensation in Humans , 2006, The Journal of Neuroscience.

[195]  Seung Woo Lee,et al.  Microscopic magnetic stimulation of neural tissue , 2012, Nature Communications.

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

[197]  V Zemon,et al.  Magnetic coil stimulation of human visual cortex: studies of perception. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[198]  Juha Silvanto,et al.  The role of the human extrastriate visual cortex in mirror symmetry discrimination: A TMS-adaptation study , 2011, Brain and Cognition.

[199]  Mauro Ursino,et al.  A neural mass model of interconnected regions simulates rhythm propagation observed via TMS-EEG , 2011, NeuroImage.

[200]  Sven Bestmann,et al.  Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury , 2011, The European journal of neuroscience.

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