Peripheral electrical stimulation to induce cortical plasticity: A systematic review of stimulus parameters

Peripheral electrical stimulation (ES) is commonly used as an intervention to facilitate movement and relieve pain in a variety of conditions. It is widely accepted that ES induces rapid plastic change in the motor cortex. This leads to the exciting possibility that ES could be used to drive cortical plasticity in movement disorders, such as stroke, and conditions where pain affects motor control. This paper aimed to critically review the literature to determine which parameters induced cortical plasticity in healthy individuals using ES. A literature search located papers that assessed plasticity in the primary motor cortex of adult humans. Studies that evaluated plasticity using change in the amplitude of potentials evoked by transcranial magnetic stimulation of the motor cortex were included. Details from each study including sample size, ES parameters and reported findings were extracted and compared. Where data were available, Cohen's standardised mean differences (SMD) were calculated. Nineteen studies were located. Of the parameters evaluated, variation of the intensity of peripheral ES appeared to have the most consistent effect on modulation of excitability of corticomotor pathway to stimulated muscles. There was a trend for stimulation above motor threshold to increase excitability (SMD 0.79 mV, CI -0.10 to 1.64). Stimulation below motor threshold, but sufficient to induce sensory perception, produced conflicting results. Further studies with consistent methodology and larger subject numbers are needed before definitive conclusions can be drawn. There also appeared to be a time effect. That is, longer periods of ES induced more sustained changes in cortical excitability. There is insufficient evidence to determine the effect of other stimulation parameters such as frequency and waveform. Further research is needed to confirm whether modulation of these parameters affects plastic change.

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

[2]  Ji-Sheng Han,et al.  Acupuncture: neuropeptide release produced by electrical stimulation of different frequencies , 2003, Trends in Neurosciences.

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

[4]  John E Misiaszek,et al.  The H‐reflex as a tool in neurophysiology: Its limitations and uses in understanding nervous system function , 2003, Muscle & nerve.

[5]  M. Ridding,et al.  Modification of the human motor cortex by associative stimulation , 2004, Experimental Brain Research.

[6]  Thomas Sinkjær,et al.  Cortical excitability changes following grasping exercise augmented with electrical stimulation , 2008, Experimental Brain Research.

[7]  K. Nakashima,et al.  Short-interval intracortical inhibition is modulated by high-frequency peripheral mixed nerve stimulation , 2007, Neuroscience Letters.

[8]  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.

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

[10]  Gereon R. Fink,et al.  Interhemispheric Competition After Stroke: Brain Stimulation to Enhance Recovery of Function of the Affected Hand , 2009, Neurorehabilitation and neural repair.

[11]  M. Ridding,et al.  Afferent stimulation facilitates performance on a novel motor task , 2006, Experimental Brain Research.

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

[13]  Richard L. Huganir,et al.  Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons , 1999, Nature Neuroscience.

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

[15]  L. Ada,et al.  Efficacy of electrical stimulation in preventing or reducing subluxation of the shoulder after stroke: a meta-analysis. , 2002, The Australian journal of physiotherapy.

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

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

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

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

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

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

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

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

[24]  D. O. Hebb,et al.  The organization of behavior , 1988 .

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

[26]  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.

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

[28]  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.

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

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

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

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

[33]  B. Godde,et al.  Tactile Coactivation-Induced Changes in Spatial Discrimination Performance , 2000, The Journal of Neuroscience.

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

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

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

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

[38]  M. Merzenich,et al.  Cortical plasticity and memory , 1993, Current Opinion in Neurobiology.

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

[40]  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.

[41]  Thomas Sinkjaer,et al.  Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive , 2005, Experimental Brain Research.

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

[43]  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.

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

[45]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

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

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

[48]  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.

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