Corticospinal excitability is dependent on the parameters of peripheral electric stimulation: a preliminary study.

OBJECTIVE To evaluate the effect of 6 electric stimulation paradigms on corticospinal excitability. DESIGN Using a same subject pre-post test design, transcranial magnetic stimulation (TMS) was used to measure the responsiveness of corticomotor pathway to biceps and triceps brachii muscles before and after 30 minutes of electric stimulation over the biceps brachii. Six different electric stimulation paradigms were applied in random order, at least 3 days apart. SETTING Motor control research laboratory. PARTICIPANTS Healthy subjects (N=10; 5 women, 5 men; mean age ± SD, 26 ± 3.6y). INTERVENTIONS Six different electric stimulation paradigms with varied stimulus amplitude, frequency, and ramp settings. MAIN OUTCOME MEASURE Amplitudes of TMS-induced motor evoked potentials at biceps and triceps brachii normalized to maximal M-wave amplitudes. RESULTS Electric stimulation delivered at stimulus amplitude sufficient to evoke a sensory response at both 10 Hz and 100 Hz, and stimulus amplitude to create a noxious response at 10 Hz decreased corticomotor responsiveness (all P<0.01). Stimulation sufficient to induce a motor contraction (30 Hz) applied in a ramped pattern to mimic a voluntary activation increased corticomotor responsiveness (P=0.002), whereas constant low- and high-intensity motor stimulation at 10 Hz did not. Corticomotor excitability changes were similar for both the stimulated muscle and its antagonist. CONCLUSIONS Stimulus amplitude (intensity) and the nature (muscle flicker vs contraction) of motor stimulation have a significant impact on changes in corticospinal excitability induced by electric stimulation. Here, we demonstrate that peripheral electric stimulation at stimulus amplitude to create a sensory response reduces corticomotor responsiveness. Conversely, stimulus amplitude to create a motor response increases corticomotor responsiveness, but only the parameters that create a motor response that mimics a voluntary muscle contraction.

[1]  Domenica Le Pera,et al.  Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain , 2001, Clinical Neurophysiology.

[2]  D N Rushton,et al.  Functional electrical stimulation and rehabilitation--an hypothesis. , 2003, Medical engineering & physics.

[3]  Lorie G. Richards,et al.  Movement-dependent stroke recovery: A systematic review and meta-analysis of TMS and fMRI evidence , 2008, Neuropsychologia.

[4]  C. Price,et al.  Electrical stimulation for preventing and treating post-stroke shoulder pain. , 2000, The Cochrane database of systematic reviews.

[5]  S. Gandevia,et al.  Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation , 2003, The Journal of physiology.

[6]  M. Ridding,et al.  Prolonged peripheral nerve stimulation induces persistent changes in excitability of human motor cortex , 2003, Journal of the Neurological Sciences.

[7]  Christian Hofer,et al.  The Vienna functional electrical stimulation system for restoration of walking functions in spastic paraplegia. , 2002, Artificial organs.

[8]  J. L. Taylor,et al.  Altered responses of human elbow flexors to peripheral-nerve and cortical stimulation during a sustained maximal voluntary contraction , 1999, Experimental Brain Research.

[9]  J. Rothwell,et al.  Driving Plasticity in Human Adult Motor Cortex Is Associated with Improved Motor Function after Brain Injury , 2002, Neuron.

[10]  Evaluations of inhibitory effect on the motor cortex by cutaneous pain via application of capsaicin. , 2003 .

[11]  G. Moretto,et al.  Long-lasting modulation of human motor cortex following prolonged transcutaneous electrical nerve stimulation (TENS) of forearm muscles: evidence of reciprocal inhibition and facilitation , 2005, Experimental Brain Research.

[12]  J. Neilson,et al.  Transcutaneous electrical nerve stimulation (TENS) for pain relief in labour. , 2009, The Cochrane database of systematic reviews.

[13]  M. Hallett,et al.  Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[14]  S. C. Gandevia,et al.  Theta burst stimulation does not reliably depress all regions of the human motor cortex , 2006, Clinical Neurophysiology.

[15]  J. Rothwell,et al.  How repeatable are the physiological effects of TENS? , 2008, Clinical Neurophysiology.

[16]  M. Ridding,et al.  Time course of induction of increased human motor cortex excitability by nerve stimulation , 2002, Neuroreport.

[17]  S. Schabrun,et al.  Peripheral electrical stimulation to induce cortical plasticity: A systematic review of stimulus parameters , 2011, Clinical Neurophysiology.

[18]  Uta Noppeney,et al.  Sustained attention modulates the immediate effect of de-afferentation on the cortical representation of the digits: source localization of somatosensory evoked potentials in humans , 1999, Neuroscience Letters.

[19]  Margarita Pérez,et al.  Effects of transcutaneous short-term electrical stimulation on M. vastus lateralis characteristics of healthy young men , 2002, Pflügers Archiv.

[20]  Massimiliano Valeriani,et al.  Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation , 2001, Neuroscience Letters.

[21]  P. Tugwell,et al.  Transcutaneous electrical nerve stimulation (TENS) for the treatment of rheumatoid arthritis in the hand. , 2003, The Cochrane database of systematic reviews.

[22]  Lumy Sawaki,et al.  Modulation of human corticomotor excitability by somatosensory input , 2002, The Journal of physiology.

[23]  T. S. Miles,et al.  Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects , 2000, Experimental Brain Research.

[24]  S C Gandevia,et al.  Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans , 2008, The Journal of physiology.

[25]  A. Berardelli,et al.  Attention influences the excitability of cortical motor areas in healthy humans , 2007, Experimental Brain Research.

[26]  V. Robertson,et al.  Electrotherapy Explained: Principles and Practice , 1990 .

[27]  J. Rothwell,et al.  Short-term high-frequency transcutaneous electrical nerve stimulation decreases human motor cortex excitability , 2004, Neuroscience Letters.

[28]  J. Kaas.  Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[29]  John C. Rothwell,et al.  Long-term reorganization of human motor cortex driven by short-term sensory stimulation , 1998, Nature Neuroscience.

[30]  E. Wassermann,et al.  A safety screening questionnaire for transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[31]  Peter Svensson,et al.  Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation , 2003, European journal of pain.

[32]  P Hunter Peckham,et al.  Wireless wearable controller for upper-limb neuroprosthesis. , 2009, Journal of rehabilitation research and development.

[33]  M. Ridding,et al.  The influence of correlated afferent input on motor cortical representations in humans , 2007, Experimental Brain Research.

[34]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[35]  K. Ragnarsson.  Functional electrical stimulation after spinal cord injury: current use, therapeutic effects and future directions , 2008, Spinal Cord.

[36]  L. G. Cohen,et al.  Nervous system reorganization following injury , 2002, Neuroscience.

[37]  Richard B. Stein,et al.  Electrical stimulation of the human common peroneal nerve elicits lasting facilitation of cortical motor-evoked potentials , 2003, Experimental Brain Research.

[38]  M. Ridding,et al.  Increased cortical excitability induced by transcranial DC and peripheral nerve stimulation , 2003, Journal of Neuroscience Methods.

[39]  T. Sinkjaer,et al.  Increase in tibialis anterior motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve , 2002, Experimental Brain Research.

[40]  Timothy S Miles,et al.  Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans , 2001, Clinical Neurophysiology.

[41]  Alfredo Berardelli,et al.  Effects of attention on inhibitory and facilitatory phenomena elicited by paired-pulse transcranial magnetic stimulation in healthy subjects , 2008, Experimental Brain Research.

[42]  R. Nicoll,et al.  Postsynaptically Silent Synapses in Single Neuron Cultures , 1998, Neuron.

[43]  R. Stein,et al.  Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles , 2004, Experimental Brain Research.

[44]  O. Sujith.  Functional electrical stimulation in neurological disorders. , 2008 .

[45]  M. A. Johnson,et al.  Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 2. Morphological and histochemical properties , 1995, Paraplegia.

[46]  K. Stefan,et al.  Modulation of associative human motor cortical plasticity by attention. , 2004, Journal of neurophysiology.

[47]  KM Jacobs,et al.  Reshaping the cortical motor map by unmasking latent intracortical connections , 1991, Science.

[48]  Richard B. Stein,et al.  Does Functional Electrical Stimulation for Foot Drop Strengthen Corticospinal Connections? , 2010, Neurorehabilitation and neural repair.

[49]  Bernhard Neundörfer,et al.  Effects of long-impulse electrical stimulation on atrophy and fibre type composition of chronically denervated fast rabbit muscle , 1990, Journal of Neurology.

[50]  M. Ridding,et al.  Normalizing motor cortex representations in focal hand dystonia. , 2009, Cerebral cortex.

[51]  P. Rossini,et al.  Neuronal post-stroke plasticity in the adult. , 2004, Restorative neurology and neuroscience.

[52]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[53]  G. Wells,et al.  Transcutaneous electrical nerve stimulation (TENS) versus placebo for chronic low-back pain. , 2008, The Cochrane database of systematic reviews.

[54]  M. Bear,et al.  Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. , 1992, Proceedings of the National Academy of Sciences of the United States of America.