How different priming stimulations affect the corticospinal excitability induced by noninvasive brain stimulation techniques: a systematic review and meta-analysis

Abstract Noninvasive brain stimulation (NIBS) techniques could induce changes in corticospinal excitability (CSE) and neuroplasticity. These changes could be affected by different factors, including having a session of stimulation called the ‘priming’ protocol before the main stimulation session called the ‘test’ protocol. Literature indicates that a priming protocol could affect the activity of postsynaptic neurons, form a neuronal history, and then modify the expected effects of the test protocol on CSE indicated by the amplitude of transcranial magnetic stimulation-induced motor-evoked potentials. This prior history affects a threshold to activate the necessary mechanism stabilizing the neuronal activity within a useful dynamic range. For studying the effects of this history and related metaplasticity mechanisms in the human primary motor cortex (M1), priming-test protocols are successfully employed. Thirty-two studies were included in this review to investigate how different priming protocols could affect the induced effects of a test protocol on CSE in healthy individuals. The results showed that if the history of synaptic activity were high or low enough to displace the threshold, the expected effects of the test protocol would be the reverse. This effect reversal is regulated by homeostatic mechanisms. On the contrary, the effects of the test protocol would not be the reverse, and at most we experience a prolongation of the lasting effects if the aforementioned history is not enough to displace the threshold. This effect prolongation is mediated by nonhomeostatic mechanisms. Therefore, based on the characteristics of priming-test protocols and the interval between them, the expected results of priming-test protocols would be different. Moreover, these findings could shed light on the different mechanisms of metaplasticity involved in NIBS. It helps us understand how we can improve the expected outcomes of these techniques in clinical approaches.

[1]  M. Ridding,et al.  Modulating motor cortical neuroplasticity with priming paired associative stimulation in young and old adults , 2017, Clinical Neurophysiology.

[2]  M. Ridding,et al.  Priming theta burst stimulation enhances motor cortex plasticity in young but not old adults , 2017, Brain Stimulation.

[3]  B. Hordacre,et al.  Response variability to non-invasive brain stimulation protocols , 2015, Clinical Neurophysiology.

[4]  M. Ridding,et al.  Spaced Noninvasive Brain Stimulation , 2015, Neurorehabilitation and neural repair.

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

[6]  U. Ziemann,et al.  Augmenting LTP-Like Plasticity in Human Motor Cortex by Spaced Paired Associative Stimulation , 2015, PloS one.

[7]  Ulf Ziemann,et al.  Metaplasticity in Human Cortex , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[8]  Michael C. Ridding,et al.  Inter-subject Variability of LTD-like Plasticity in Human Motor Cortex: A Matter of Preceding Motor Activation , 2014, Brain Stimulation.

[9]  S. Jaberzadeh,et al.  Within-session repeated a-tDCS: The effects of repetition rate and inter-stimulus interval on corticospinal excitability and motor performance , 2014, Clinical Neurophysiology.

[10]  Robert Chen,et al.  Heterosynaptic Modulation of Motor Cortical Plasticity in Human , 2014, The Journal of Neuroscience.

[11]  A. G. Witney,et al.  Pressure Pain Thresholds Increase after Preconditioning 1 Hz Repetitive Transcranial Magnetic Stimulation with Transcranial Direct Current Stimulation , 2014, PloS one.

[12]  M. Ridding,et al.  Neuroplastic Modulation of Inhibitory Motor Cortical Networks by Spaced Theta Burst Stimulation Protocols , 2013, Brain Stimulation.

[13]  Walter Paulus,et al.  Induction of Late LTP-Like Plasticity in the Human Motor Cortex by Repeated Non-Invasive Brain Stimulation , 2013, Brain Stimulation.

[14]  T. Bergmann,et al.  Brain-Derived Neurotrophic Factor – A Major Player in Stimulation-Induced Homeostatic Metaplasticity of Human Motor Cortex? , 2013, PloS one.

[15]  Janet L. Taylor,et al.  Paired associative stimulation increases motor cortex excitability more effectively than theta-burst stimulation , 2012, Clinical Neurophysiology.

[16]  U. Ziemann,et al.  Homeostatic metaplasticity of corticospinal excitatory and intracortical inhibitory neural circuits in human motor cortex , 2012, The Journal of physiology.

[17]  Mark F. Bear,et al.  The BCM theory of synapse modification at 30: interaction of theory with experiment , 2012, Nature Reviews Neuroscience.

[18]  S. Jaberzadeh,et al.  Does the Longer Application of Anodal-transcranial Direct Current Stimulation Increase Corticomotor Excitability Further? A Pilot Study , 2012 .

[19]  G. Cosentino,et al.  Transcranial direct current stimulation preconditioning modulates the effect of high‐frequency repetitive transcranial magnetic stimulation in the human motor cortex , 2012, The European journal of neuroscience.

[20]  M. Ridding,et al.  The application of spaced theta burst protocols induces long‐lasting neuroplastic changes in the human motor cortex , 2012, The European journal of neuroscience.

[21]  M. Ridding,et al.  Modulation of cortical motor networks following primed theta burst transcranial magnetic stimulation , 2011, Experimental Brain Research.

[22]  Walter Paulus,et al.  Impact of repetitive theta burst stimulation on motor cortex excitability , 2011, Brain Stimulation.

[23]  Alfredo Berardelli,et al.  Short‐term and long‐term plasticity interaction in human primary motor cortex , 2011, The European journal of neuroscience.

[24]  J. Rothwell,et al.  Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. , 2011, Journal of neurophysiology.

[25]  J. Rothwell,et al.  Reversal of plasticity‐like effects in the human motor cortex , 2010, The Journal of physiology.

[26]  M. Ridding,et al.  Determinants of the induction of cortical plasticity by non‐invasive brain stimulation in healthy subjects , 2010, The Journal of physiology.

[27]  A. Antal,et al.  Simply longer is not better: reversal of theta burst after-effect with prolonged stimulation , 2010, Experimental Brain Research.

[28]  Walter Paulus,et al.  Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). , 2010, Journal of neurophysiology.

[29]  I. Delvendahl,et al.  Occlusion of bidirectional plasticity by preceding low-frequency stimulation in the human motor cortex , 2010, Clinical Neurophysiology.

[30]  G. Deuschl,et al.  Inducing homeostatic-like plasticity in human motor cortex through converging corticocortical inputs. , 2009, Journal of neurophysiology.

[31]  M. Ridding,et al.  Priming theta-burst repetitive transcranial magnetic stimulation with low- and high-frequency stimulation , 2009, Experimental Brain Research.

[32]  Daniel Zeller,et al.  Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. , 2008, Cerebral cortex.

[33]  R. Hanajima,et al.  Bidirectional long‐term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation , 2008, The Journal of physiology.

[34]  Hartwig R. Siebner,et al.  Modifying motor learning through gating and homeostatic metaplasticity , 2008, Brain Stimulation.

[35]  Ulf Ziemann,et al.  Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation , 2007, The European journal of neuroscience.

[36]  Walter Paulus,et al.  Timing-Dependent Modulation of Associative Plasticity by General Network Excitability in the Human Motor Cortex , 2007, The Journal of Neuroscience.

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

[38]  J. Rothwell,et al.  Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects , 2004, Biological Psychiatry.

[39]  J. Rothwell,et al.  Preconditioning of Low-Frequency Repetitive Transcranial Magnetic Stimulation with Transcranial Direct Current Stimulation: Evidence for Homeostatic Plasticity in the Human Motor Cortex , 2004, The Journal of Neuroscience.

[40]  E. Wassermann,et al.  Priming Stimulation Enhances the Depressant Effect of Low-Frequency Repetitive Transcranial Magnetic Stimulation , 2003, The Journal of Neuroscience.

[41]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[42]  L. Cohen,et al.  Induction of plasticity in the human motor cortex by paired associative stimulation. , 2000, Brain : a journal of neurology.

[43]  N. Black,et al.  The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. , 1998, Journal of epidemiology and community health.

[44]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[45]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.