Clinical and Research Methods for Evaluating Cortical Excitability

Summary The evaluation of motor cortical output after transcranial magnetic stimulation (TMS) is a means of investigating how the motor cortex reacts to external stimuli (i.e., a method to assess the excitability of the motor cortex). The recording of the descending volleys at the surface of the spinal cord provides a direct measure of the motor cortical output. However, this approach is highly invasive and can be used only during particular conditions. On the other hand, electromyographic recordings of the motor phenomena induced by TMS provide a completely painless, noninvasive, indirect measure of the cortical output, with these phenomena obviously reflecting the excitability of the spinal motoneurons as well as that of the muscle itself. The authors review how the electromyographic activity induced by TMS can provide valuable information about motor cortical excitability for use in clinical practice and research.

[1]  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.

[2]  J C Rothwell,et al.  Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. , 1998, Electroencephalography and clinical neurophysiology.

[3]  Influence of peripheral nerve stimulation on human motor cortical excitability in patients with ventrolateral thalamic lesion. , 1997, Archives of neurology.

[4]  M. Dimitrijevic,et al.  Facilitation of motor evoked potentials by somatosensory afferent stimulation. , 1992, Electroencephalography and clinical neurophysiology.

[5]  F. Tremblay,et al.  Modulation of corticospinal excitability during imagined knee movements. , 2001, Journal of rehabilitation medicine.

[6]  G. Abbruzzese,et al.  Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. , 2001, Brain : a journal of neurology.

[7]  Babak Boroojerdi,et al.  Transcallosal inhibition in cortical and subcortical cerebral vascular lesions , 1996, Journal of the Neurological Sciences.

[8]  M. Hallett,et al.  Effects of transcranial magnetic stimulation on ipsilateral muscles , 1991, Neurology.

[9]  P. Ashby,et al.  Mechanism of the silent period following transcranial magnetic stimulation Evidence from epidural recordings , 1999, Experimental Brain Research.

[10]  B. Shahani,et al.  Hemispheric threshold differences for motor evoked potentials produced by magnetic coil stimulation , 1991, Neurology.

[11]  K. Mills,et al.  The influence of vibration on the excitability of alpha motoneurones. , 1988, Electroencephalography and clinical neurophysiology.

[12]  J. Rothwell,et al.  Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[13]  L M Harrison,et al.  Task‐dependent changes in the size of response to magnetic brain stimulation in human first dorsal interosseous muscle. , 1989, The Journal of physiology.

[14]  L Kiers,et al.  Facilitatory effect of thinking about movement on magnetic motor-evoked potentials. , 1997, Electroencephalography and clinical neurophysiology.

[15]  Walter Paulus,et al.  Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy , 1999, The Lancet.

[16]  J C Rothwell,et al.  Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man. , 1991, The Journal of physiology.

[17]  W Paulus,et al.  Inhibition of human motor cortex by ethanol. A transcranial magnetic stimulation study. , 1995, Brain : a journal of neurology.

[18]  M. Hallett,et al.  Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior , 2000, Clinical Neurophysiology.

[19]  Roger Q. Cracco,et al.  Cerebral function revealed by transcranial magnetic stimulation , 1999, Journal of Neuroscience Methods.

[20]  A Berardelli,et al.  Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. , 1993, The Journal of physiology.

[21]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[22]  P. Schönle,et al.  Silent period measurement revives as a valuable diagnostic tool with transcranial magnetic stimulation. , 1992, Electroencephalography and clinical neurophysiology.

[23]  J. Rothwell,et al.  Inhibitory action of forearm flexor muscle afferents on corticospinal outputs to antagonist muscles in humans , 1998, The Journal of physiology.

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

[25]  P M Rossini,et al.  Interhemispheric differences of hand muscle representation in human motor cortex , 1997, Muscle & nerve.

[26]  H. Tsuji,et al.  Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation , 1996, Neuroscience Letters.

[27]  M Schieppati,et al.  Selective facilitation of responses to cortical stimulation of proximal and distal arm muscles by precision tasks in man. , 1996, The Journal of physiology.

[28]  P. Pasqualetti,et al.  Effects of motor imagery on motor cortical output topography in Parkinson’s disease , 2001, Neurology.

[29]  J C Rothwell,et al.  Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[30]  Á. Pascual-Leone,et al.  Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression , 1996, The Lancet.

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

[32]  S. Bandinelli,et al.  Effects of coil design on delivery of focal magnetic stimulation. Technical considerations. , 1990, Electroencephalography and clinical neurophysiology.

[33]  G. Abbruzzese,et al.  Intracortical inhibition after paired transcranial magnetic stimulation depends on the current flow direction , 1999, Clinical Neurophysiology.

[34]  H. Steinmetz,et al.  Coil placement in magnetic brain stimulation related to skull and brain anatomy. , 1991, Electroencephalography and clinical neurophysiology.

[35]  M. Hallett,et al.  Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles , 1996, Experimental Brain Research.

[36]  R. Mutani,et al.  Parkinson's disease rigidity , 1991, Neurology.

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

[38]  Franca Tecchio,et al.  Corticospinal excitability modulation during mental simulation of wrist movements in human subjects , 1998, Neuroscience Letters.

[39]  M. Hallett,et al.  Human motor evoked responses to paired transcranial magnetic stimuli. , 1992, Electroencephalography and clinical neurophysiology.

[40]  T. Kasai,et al.  Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery , 1997, Brain Research.

[41]  V. Kostic,et al.  Impairment of cortical inhibition in writer's cramp as revealed by changes in electromyographic silent period after transcranial magnetic stimulation , 1997, Neuroscience Letters.

[42]  M. Hallett,et al.  Spinal motor neuron excitability during the silent period after cortical stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[43]  M. Hallett,et al.  Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. , 1994, Brain : a journal of neurology.

[44]  J. Rothwell,et al.  Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? , 2001, Clinical Neurophysiology.

[45]  M. Schieppati,et al.  Comparison of intracortical inhibition and facilitation in distal and proximal arm muscles in humans , 1999, The Journal of physiology.

[46]  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.

[47]  J C Rothwell,et al.  Transcranial electric and magnetic stimulation of the leg area of the human motor cortex: single motor unit and surface EMG responses in the tibialis anterior muscle. , 1993, Electroencephalography and clinical neurophysiology.

[48]  D. C. Weaver.  The effects of diazepam. , 1969, Anesthesiology.

[49]  Brian L. Day,et al.  Different sites of action of electrical and magnetic stimulation of the human brain , 1987, Neuroscience Letters.

[50]  K. Mills,et al.  Responses in small hand muscles from magnetic stimulation of the human brain. , 1987, The Journal of physiology.

[51]  B. Day,et al.  Modulation of motor cortical excitability by electrical stimulation over the cerebellum in man. , 1991, The Journal of physiology.

[52]  W Paulus,et al.  Transcranial magnetic stimulation: its current role in epilepsy research , 1998, Epilepsy Research.

[53]  M. Cosottini,et al.  Motor imagery in a locked-in patient: evidence from transcranial magnetic stimulation , 1999, The Italian Journal of Neurological Sciences.

[54]  J C Rothwell,et al.  Abnormalities of the balance between inhibition and excitation in the motor cortex of patients with cortical myoclonus. , 1996, Brain : a journal of neurology.

[55]  U. Ziemann,et al.  Spinal and supraspinal mechanisms contribute to the silent period in the contracting soleus muscle after transcranial magnetic stimulation of human motor cortex , 1993, Neuroscience Letters.

[56]  L. Larsson,et al.  Late muscular responses to transcranial cortical stimulation in man. , 1990, Electroencephalography and clinical neurophysiology.

[57]  Walter Paulus,et al.  Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation , 1999, Experimental Brain Research.

[58]  A. Eisen,et al.  Reliability of transcranial magnetic stimulation for mapping the human motor cortex. , 1994, Electroencephalography and clinical neurophysiology.

[59]  K. Sakai,et al.  Paired‐pulse magnetic stimulation of the human motor cortex: differences among I waves , 1998, The Journal of physiology.

[60]  V E Amassian,et al.  An analysis of the activation of motor cortical neurons by surface stimulation. , 1967, Journal of neurophysiology.

[61]  R. Benecke,et al.  On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects , 2004, Experimental Brain Research.

[62]  M. Hallett,et al.  Modulation of cortical motor output maps during development of implicit and explicit knowledge. , 1994, Science.

[63]  C. Marsden,et al.  The effect of percutaneous motor cortex stimulation on H reflexes in muscles of the arm and leg in intact man. , 1986, The Journal of physiology.

[64]  Walter Paulus,et al.  The effect of lorazepam on the motor cortical excitability in man , 1996, Experimental Brain Research.

[65]  P M Rossini,et al.  Post-stroke reorganization of brain motor output to the hand: a 2-4 month follow-up with focal magnetic transcranial stimulation. , 1997, Electroencephalography and clinical neurophysiology.

[66]  R. J. Lockwood,et al.  The muscle silent period following transcranial magnetic cortical stimulation , 1993, Journal of the Neurological Sciences.

[67]  K. Chiappa,et al.  Cortical and spinal motor excitability during the transcranial magnetic stimulation silent period in humans , 1993, Brain Research.

[68]  M Hallett,et al.  Physiological analysis of motor reorganization following lower limb amputation. , 1992, Electroencephalography and clinical neurophysiology.

[69]  M Hallett,et al.  Dextromethorphan decreases the excitability of the human motor cortex , 1998, Neurology.

[70]  B. Shahani,et al.  Motor inhibition and excitation are independent effects of magnetic cortical stimulation , 1992, Annals of neurology.

[71]  M. Hallett,et al.  Task-dependent changes of intracortical inhibition , 1997, Experimental Brain Research.

[72]  Walter Paulus,et al.  Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation , 1998, The Journal of physiology.

[73]  B. Steinhoff,et al.  Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study , 1996, Annals of neurology.

[74]  J. Rothwell,et al.  Short latency inhibition of human hand motor cortex by somatosensory input from the hand , 2000, The Journal of physiology.

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

[76]  V E Amassian,et al.  Mapping of motor cortex gyral sites non-invasively by transcranial magnetic stimulation in normal subjects and patients. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[77]  A. Berardelli,et al.  Effects of diazepam, baclofen and thiopental on the silent period evoked by transcranial magnetic stimulation in humans , 1996, Experimental Brain Research.

[78]  V. Amassian,et al.  Some positive effects of transcranial magnetic stimulation. , 1995, Advances in neurology.

[79]  N Accornero,et al.  Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism. , 1994, Brain : a journal of neurology.

[80]  Á. Pascual-Leone,et al.  Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex , 2002, Clinical Neurophysiology.

[81]  V. Amassian,et al.  Focal stimulation of human cerebral cortex with the magnetic coil: a comparison with electrical stimulation. , 1989, Electroencephalography and clinical neurophysiology.

[82]  J. Rothwell,et al.  Intracortical inhibition and facilitation in different representations of the human motor cortex. , 1998, Journal of neurophysiology.

[83]  Á. Pascual-Leone,et al.  Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp , 1999, Neurology.

[84]  V. Amassian,et al.  Single and multiple-unit analysis of cortical stage of pyramidal tract activation. , 1954, Journal of neurophysiology.

[85]  T. Sawaguchi,et al.  GABAergic inhibition of neuronal activity in the primate motor and premotor cortex during voluntary movement. , 1992, Journal of neurophysiology.

[86]  S. Röricht,et al.  Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices , 1998, Annals of neurology.

[87]  A Berardelli,et al.  Electromyographic silent period after transcranial brain stimulation in huntington's disease , 2004, Movement disorders : official journal of the Movement Disorder Society.

[88]  Mark Hallett,et al.  Modulation of motor cortex excitability by median nerve and digit stimulation , 1999, Experimental Brain Research.

[89]  K. Mills,et al.  Facilitation of muscle responses to magnetic brain stimulation by mechanical stimuli in man , 2004, Experimental Brain Research.

[90]  H. Tsuji,et al.  Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. , 1997, The Journal of physiology.

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

[92]  J. Rothwell,et al.  Facilitation of muscle evoked responses after repetitive cortical stimulation in man , 1998, Experimental Brain Research.

[93]  B. Day,et al.  Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. , 1989, The Journal of physiology.

[94]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[95]  M. Ridding,et al.  Stimulus/response curves as a method of measuring motor cortical excitability in man. , 1997, Electroencephalography and clinical neurophysiology.

[96]  P M Rossini,et al.  Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. , 1997, Stroke.

[97]  Detlef Claus,et al.  Corticospinal conduction studied with magnetic double stimulation in the intact human , 1992, Journal of the Neurological Sciences.

[98]  J Valls-Solé,et al.  Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. , 1993, Electroencephalography and clinical neurophysiology.

[99]  P M Rossini,et al.  Brain excitability and long latency muscular arm responses: non-invasive evaluation in healthy and parkinsonian subjects. , 1991, Electroencephalography and clinical neurophysiology.

[100]  M Hallett,et al.  Topographic maps of human motor cortex in normal and pathological conditions: mirror movements, amputations and spinal cord injuries. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[101]  J. Rothwell,et al.  Techniques and mechanisms of action of transcranial stimulation of the human motor cortex , 1997, Journal of Neuroscience Methods.

[102]  R. Benecke,et al.  Inhibitory actions of motor cortex following unilateral brain lesions as studied by magnetic brain stimulation , 2004, Experimental Brain Research.

[103]  P H Ellaway,et al.  Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. , 1994, The Journal of physiology.

[104]  A Berardelli,et al.  Alterations of motor cortical inhibition in patients with dystonia , 1998, Movement disorders : official journal of the Movement Disorder Society.

[105]  J Valls-Solé,et al.  Rapid modulation of human cortical motor outputs following ischaemic nerve block. , 1993, Brain : a journal of neurology.

[106]  P. Mazzone,et al.  Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans , 1998, The Journal of physiology.

[107]  P Ashby,et al.  Corticospinal projections to upper and lower limb spinal motoneurons in man. , 1990, Electroencephalography and clinical neurophysiology.

[108]  V. Amassian,et al.  Physiological basis of motor effects of a transient stimulus to cerebral cortex. , 1987, Neurosurgery.

[109]  B. Kukowski,et al.  Quantitative evaluation of the silent period, evoked by transcranial magnetic stimulation during sustained muscle contraction, in normal man and in patients with stroke. , 1992, Electromyography and clinical neurophysiology.

[110]  T. Yamamoto,et al.  Corticospinal direct response in humans: identification of the motor cortex during intracranial surgery under general anaesthesia. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[111]  D. McCormick,et al.  GABA as an inhibitory neurotransmitter in human cerebral cortex. , 1989, Journal of neurophysiology.

[112]  M. Schieppati,et al.  The excitability of the human motor cortex increases during execution and mental imagination of sequential but not repetitive finger movements , 1996, Experimental Brain Research.

[113]  F L Mastaglia,et al.  Comparison of the magnetically mapped corticomotor representation of a muscle at rest and during low-level voluntary contraction. , 1995, Electroencephalography and clinical neurophysiology.

[114]  K. Krnjević,et al.  Nature of a cortical inhibitory process , 1966, The Journal of physiology.

[115]  H. Siebner,et al.  Abnormal increase in the corticomotor output to the affected hand during repetitive transcranial magnetic stimulation of the primary motor cortex in patients with writer's cramp , 1999, Neuroscience Letters.

[116]  G. Abbruzzese,et al.  Intracortical inhibitory circuits and sensory input: a study with transcranial magnetic stimulation in humans , 2001, Neuroscience Letters.

[117]  G. Deuschl,et al.  Effects of electric and magnetic transcranial stimulation on long latency reflexes , 2004, Experimental Brain Research.

[118]  A. Berardelli,et al.  Cortical inhibition in Parkinson's disease. A study with paired magnetic stimulation. , 1996, Brain : a journal of neurology.

[119]  C W Hess,et al.  Dependence of the transcranially induced silent period on the 'instruction set' and the individual reaction time. , 1998, Electroencephalography and clinical neurophysiology.

[120]  D. Kernell,et al.  Responses of the pyramidal tract to stimulation of the baboon's motor cortex , 1967, The Journal of physiology.

[121]  A. Eisen,et al.  Facilitation of Cortical Motor Evoked Potentials: Evidence for Spinal Contributions. A. S , 1988 .

[122]  Á. Pascual-Leone,et al.  Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation , 2000, Clinical Neurophysiology.

[123]  R. Mutani,et al.  Magnetic brain stimulation: the silent period after the motor evoked potential. , 1992, Neurology.

[124]  R. Lemon,et al.  Organisation of Cortico-motoneuronal Projections from the Primary Motor Cortex: Evidence for Task-Related Function in Monkey and in Man , 1993 .

[125]  M. Ridding,et al.  Afferent input and cortical organisation: a study with magnetic stimulation , 1999, Experimental Brain Research.

[126]  K Kaneko,et al.  The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. , 1996, Electroencephalography and clinical neurophysiology.

[127]  M Hallett,et al.  Transcranial magnetic stimulation. Negative effects. , 1995, Advances in neurology.

[128]  N. Davey,et al.  Facilitation of human first dorsal interosseous muscle responses to transcranial magnetic stimulation during voluntary contraction of the contralateral homonymous muscle , 1998, Muscle & nerve.

[129]  R N Lemon,et al.  Task dependence of responses in first dorsal interosseous muscle to magnetic brain stimulation in man. , 1993, The Journal of physiology.