Neural activity related to volitional regulation of cortical excitability

To date there exists no reliable method to non-invasively upregulate or downregulate the state of the resting human motor system over a large dynamic range. Here we show that an operant conditioning paradigm which provides neurofeedback of the size of motor evoked potentials (MEPs) in response to transcranial magnetic stimulation (TMS), enables participants to self-modulate their own brain state. Following training, participants were able to robustly increase (by 83.8%) and decrease (by 30.6%) their MEP amplitudes. This volitional up-versus down-regulation of corticomotor excitability caused an increase of late-cortical disinhibition (LCD), a TMS derived read-out of presynaptic GABAB disinhibition, which was accompanied by an increase of gamma and a decrease of alpha oscillations in the trained hemisphere. This approach paves the way for future investigations into how altered brain state influences motor neurophysiology and recovery of function in a neurorehabilitation context.

[1]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

[2]  M. Ridding,et al.  Task-related changes in intracortical inhibition assessed with paired- and triple-pulse transcranial magnetic stimulation. , 2015, Journal of neurophysiology.

[3]  H. Bostock,et al.  Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking , 2002, Experimental Brain Research.

[4]  P. Derambure,et al.  Late cortical disinhibition in relaxed versus active hand muscles , 2015, Neuroscience.

[5]  E. Olivier,et al.  Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation , 1997, The Journal of physiology.

[6]  D. Lewis,et al.  Facilitation of the induction of long-term potentiation by GABAB receptors , 1991, Science.

[7]  R. Carson,et al.  Characterizing Changes in the Excitability of Corticospinal Projections to Proximal Muscles of the Upper Limb , 2013, Brain Stimulation.

[8]  Wolfgang Rosenstiel,et al.  An MEG-based brain–computer interface (BCI) , 2007, NeuroImage.

[9]  C. Gerloff,et al.  Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex , 2009, Neuropsychologia.

[10]  S. Swinnen,et al.  Kinesthetic, but not visual, motor imagery modulates corticomotor excitability , 2005, Experimental Brain Research.

[11]  G W Thickbroom,et al.  Inhibitory and disinhibitory effects on I-wave facilitation in motor cortex. , 2011, Journal of neurophysiology.

[12]  G. Hammond,et al.  Modulation of long-interval intracortical inhibition and the silent period by voluntary contraction , 2007, Brain Research.

[13]  Bernhard Schölkopf,et al.  Causal influence of gamma oscillations on the sensorimotor rhythm , 2011, NeuroImage.

[14]  Niels Birbaumer,et al.  Enhancing Hebbian Learning to Control Brain Oscillatory Activity. , 2015, Cerebral cortex.

[15]  Ethan R. Buch,et al.  Think to Move: a Neuromagnetic Brain-Computer Interface (BCI) System for Chronic Stroke , 2008, Stroke.

[16]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[17]  Susan D Horn,et al.  Timing of initiation of rehabilitation after stroke. , 2005, Archives of physical medicine and rehabilitation.

[18]  Ulf Ziemann,et al.  Interference of short-interval intracortical inhibition (SICI) and short-interval intracortical facilitation (SICF) , 2008, Clinical Neurophysiology.

[19]  B. Shen,et al.  GABAB receptor blockade enhances theta and gamma rhythms in the hippocampus of behaving rats , 2007, Hippocampus.

[20]  L. Craighero,et al.  Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study , 1998, Neuropsychologia.

[21]  C. Stinear,et al.  Modulation of motor cortex inhibition during motor imagery. , 2017, Journal of neurophysiology.

[22]  Robert Oostenveld,et al.  Using Brain–Computer Interfaces and Brain-State Dependent Stimulation as Tools in Cognitive Neuroscience , 2011, Front. Psychology.

[23]  C. Braun,et al.  Chronic stroke recovery after combined BCI training and physiotherapy: a case report. , 2011, Psychophysiology.

[24]  D. Avery,et al.  EEG and the Variance of Motor Evoked Potential Amplitude , 2006, Clinical EEG and neuroscience.

[25]  Xiang Yang Chen,et al.  Acquisition of a Simple Motor Skill: Task-Dependent Adaptation Plus Long-Term Change in the Human Soleus H-Reflex , 2009, The Journal of Neuroscience.

[26]  J. Krystal,et al.  Move over ANOVA: progress in analyzing repeated-measures data and its reflection in papers published in the Archives of General Psychiatry. , 2004, Archives of general psychiatry.

[27]  Rajesh P. N. Rao,et al.  Cortical activity during motor execution, motor imagery, and imagery-based online feedback , 2010, Proceedings of the National Academy of Sciences.

[28]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[29]  Alexander Leemans,et al.  Structural and Functional Cortical Connectivity Mediating Cross Education of Motor Function , 2017, The Journal of Neuroscience.

[30]  Jarrod A. Lewis-Peacock,et al.  Closed-loop brain training: the science of neurofeedback , 2017, Nature Reviews Neuroscience.

[31]  Robert Chen,et al.  Interactions between two different inhibitory systems in the human motor cortex , 2001, The Journal of physiology.

[32]  N. Chino,et al.  Facilitatory effect of thinking about movement on motor-evoked potentials to transcranial magnetic stimulation of the brain , 1995 .

[33]  G W Thickbroom,et al.  Late cortical disinhibition in human motor cortex: a triple-pulse transcranial magnetic stimulation study. , 2010, Journal of neurophysiology.

[34]  Robert Chen,et al.  Short interval intracortical inhibition and facilitation during the silent period in human , 2007, The Journal of physiology.

[35]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[36]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[37]  EEG-triggered TMS reveals stronger brain state-dependent modulation of motor evoked potentials at weaker stimulation intensities , 2019, Brain Stimulation.

[38]  Christiane,et al.  World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. , 2013, JAMA.

[39]  T. Ichida World Medical Association declaration of Helsinki , 1991, Gastroenterologia Japonica.

[40]  G. Buzsáki Rhythms of the brain , 2006 .

[41]  R. Magill Motor learning and control : concepts and applications , 2004 .

[42]  Christoph Zrenner,et al.  Real-time EEG-defined excitability states determine efficacy of TMS-induced plasticity in human motor cortex , 2017, Brain Stimulation.

[43]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

[44]  A. Labarga,et al.  Alpha and beta oscillatory activity during a sequence of two movements , 2004, Clinical Neurophysiology.

[45]  L. Cohen,et al.  Brain–machine interfaces in neurorehabilitation of stroke , 2015, Neurobiology of Disease.

[46]  Ulf Ziemann,et al.  The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. , 2006, Experimental brain research.

[47]  E. Fetz Volitional Control of Cortical Oscillations and Synchrony , 2013, Neuron.

[48]  D. Mantini,et al.  Improving the quality of combined EEG-TMS neural recordings: Introducing the coil spacer , 2017, Journal of Neuroscience Methods.

[49]  G. Pfurtscheller,et al.  Patterns of cortical activation during planning of voluntary movement. , 1989, Electroencephalography and clinical neurophysiology.

[50]  O. Jensen,et al.  Prestimulus alpha and mu activity predicts failure to inhibit motor responses , 2009, Human brain mapping.

[51]  John J. Foxe,et al.  The strength of anticipatory spatial biasing predicts target discrimination at attended locations: a high‐density EEG study , 2009, The European journal of neuroscience.

[52]  C. W. Hess,et al.  Magnetic stimulation of the human brain: Facilitation of motor responses by voluntary contraction of ipsilateral and contralateral muscles with additional observations on an amputee , 1986, Neuroscience Letters.

[53]  Ulf Ziemann,et al.  Augmenting Plasticity Induction in Human Motor Cortex by Disinhibition Stimulation. , 2016, Cerebral cortex.

[54]  Risto J. Ilmoniemi,et al.  EEG oscillations and magnetically evoked motor potentials reflect motor system excitability in overlapping neuronal populations , 2010, Clinical Neurophysiology.

[55]  I. Toni,et al.  Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions. , 2014, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  U. Ziemann,et al.  The role of GABAB receptors in intracortical inhibition in the human motor cortex , 2006, Experimental Brain Research.

[57]  Niels Birbaumer,et al.  Brain oscillatory signatures of motor tasks. , 2015, Journal of neurophysiology.

[58]  A. Aron,et al.  Training voluntary motor suppression with real-time feedback of motor evoked potentials. , 2015, Journal of neurophysiology.

[59]  K. Ruddy Directionality of interhemispheric communication , 2017, Brain Structure and Function.

[60]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[61]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[62]  WestonJason,et al.  Gene Selection for Cancer Classification using Support Vector Machines , 2002 .

[63]  Salvatore Maria Aglioti,et al.  Error, rather than its probability, elicits specific electrocortical signatures: a combined EEG-immersive virtual reality study of action observation. , 2018, Journal of neurophysiology.

[64]  Steven Lemm,et al.  Now you feel it--now you don't: ERP correlates of somatosensory awareness. , 2006, Psychophysiology.

[65]  Stuart D. Greenhill,et al.  Phase-amplitude coupled persistent theta and gamma oscillations in rat primary motor cortex in vitro , 2017, Neuropharmacology.

[66]  P. Derambure,et al.  Task‐dependent changes in late inhibitory and disinhibitory actions within the primary motor cortex in humans , 2014, The European journal of neuroscience.

[67]  C. Capaday,et al.  Input-output properties and gain changes in the human corticospinal pathway , 1997, Experimental Brain Research.

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

[69]  Jason Weston,et al.  Gene Selection for Cancer Classification using Support Vector Machines , 2002, Machine Learning.

[70]  Alexander Leemans,et al.  Transcallosal connectivity of the human cortical motor network , 2016, Brain Structure and Function.

[71]  Hagai Bergman,et al.  Inducing Gamma Oscillations and Precise Spike Synchrony by Operant Conditioning via Brain-Machine Interface , 2013, Neuron.