Calcium dependent plasticity applied to repetitive transcranial magnetic stimulation with a neural field model

The calcium dependent plasticity (CaDP) approach to the modeling of synaptic weight change is applied using a neural field approach to realistic repetitive transcranial magnetic stimulation (rTMS) protocols. A spatially-symmetric nonlinear neural field model consisting of populations of excitatory and inhibitory neurons is used. The plasticity between excitatory cell populations is then evaluated using a CaDP approach that incorporates metaplasticity. The direction and size of the plasticity (potentiation or depression) depends on both the amplitude of stimulation and duration of the protocol. The breaks in the inhibitory theta-burst stimulation protocol are crucial to ensuring that the stimulation bursts are potentiating in nature. Tuning the parameters of a spike-timing dependent plasticity (STDP) window with a Monte Carlo approach to maximize agreement between STDP predictions and the CaDP results reproduces a realistically-shaped window with two regions of depression in agreement with the existing literature. Developing understanding of how TMS interacts with cells at a network level may be important for future investigation.

[1]  K. Svoboda,et al.  The Life Cycle of Ca2+ Ions in Dendritic Spines , 2002, Neuron.

[2]  David W. Nauen,et al.  Coactivation and timing-dependent integration of synaptic potentiation and depression , 2005, Nature Neuroscience.

[3]  P. Robinson,et al.  Multiscale brain modelling , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  James J. Wright,et al.  Propagation and stability of waves of electrical activity in the cerebral cortex , 1997 .

[5]  J. Rothwell,et al.  The role of interneuron networks in driving human motor cortical plasticity. , 2013, Cerebral cortex.

[6]  L. Cooper,et al.  A biophysical model of bidirectional synaptic plasticity: Dependence on AMPA and NMDA receptors , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Marcus T. Wilson,et al.  General Anesthetic-induced Seizures Can Be Explained by a Mean-field Model of Cortical Dynamics , 2006, Anesthesiology.

[8]  Nikos K. Logothetis,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[9]  Tomasz Zyss.  Technique of transcranial magnetic stimulation in therapy of depressions - advantages and disadvantages of computer modeling , 2010, Bio Algorithms Med Syst..

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

[11]  D. Liley,et al.  Modeling the effects of anesthesia on the electroencephalogram. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  Yasuo Terao,et al.  Effects of the motor cortical quadripulse transcranial magnetic stimulation (QPS) on the contralateral motor cortex and interhemispheric interactions. , 2014, Journal of neurophysiology.

[13]  Nicolas Brunel,et al.  STDP in a Bistable Synapse Model Based on CaMKII and Associated Signaling Pathways , 2007, PLoS Comput. Biol..

[14]  Wulfram Gerstner,et al.  Frontiers in Synaptic Neuroscience Synaptic Neuroscience , 2022 .

[15]  Nicolas Brunel,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[16]  P. Robinson.  Propagator theory of brain dynamics. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[17]  James A. Roberts,et al.  Biophysical Mechanisms of Multistability in Resting-State Cortical Rhythms , 2011, The Journal of Neuroscience.

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

[19]  Gastone C. Castellani,et al.  Converging evidence for a simplified biophysical model of synaptic plasticity , 2002, Biological Cybernetics.

[20]  Matthew E. Larkum,et al.  The GABAB1b Isoform Mediates Long-Lasting Inhibition of Dendritic Ca2+ Spikes in Layer 5 Somatosensory Pyramidal Neurons , 2006, Neuron.

[21]  David T. J. Liley,et al.  A continuum theory of electro-cortical activity , 1999, Neurocomputing.

[22]  Eugene M. Izhikevich,et al.  Relating STDP to BCM , 2003, Neural Computation.

[23]  L. Cooper,et al.  A unified model of NMDA receptor-dependent bidirectional synaptic plasticity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Sleigh,et al.  The Sleep Cycle Modelled as a Cortical Phase Transition , 2005, Journal of biological physics.

[25]  Vincenzo Di Lazzaro,et al.  Theta Burst Stimulation in the Rehabilitation of the Upper Limb , 2012, Neurorehabilitation and neural repair.

[26]  P A Robinson,et al.  Neural field theory of calcium dependent plasticity with applications to transcranial magnetic stimulation. , 2013, Journal of theoretical biology.

[27]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[28]  M. Hallett.  Transcranial Magnetic Stimulation: A Primer , 2007, Neuron.

[29]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[30]  D. Liley,et al.  Theoretical electroencephalogram stationary spectrum for a white-noise-driven cortex: evidence for a general anesthetic-induced phase transition. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[31]  H. Haken,et al.  A derivation of a macroscopic field theory of the brain from the quasi-microscopic neural dynamics , 1997 .

[32]  P. Robinson,et al.  Neural field theory of synaptic metaplasticity with applications to theta burst stimulation. , 2014, Journal of theoretical biology.

[33]  Jc Rothwell,et al.  Perspectives - Opinion - Is there a future for therapeutic use of transcranial magnetic stimulation? , 2007 .

[34]  R. Hanajima,et al.  Quadro-pulse stimulation is more effective than paired-pulse stimulation for plasticity induction of the human motor cortex , 2007, Clinical Neurophysiology.

[35]  P. Mitchell,et al.  A review of the efficacy of transcranial magnetic stimulation (TMS) treatment for depression, and current and future strategies to optimize efficacy. , 2005, Journal of affective disorders.

[36]  J. Rothwell,et al.  Is there a future for therapeutic use of transcranial magnetic stimulation? , 2007, Nature Reviews Neuroscience.

[37]  D. Alistair Steyn-Ross,et al.  Modeling brain activation patterns for the default and cognitive states , 2009, NeuroImage.

[38]  D. Alistair Steyn-Ross,et al.  Complementarity of Spike- and Rate-Based Dynamics of Neural Systems , 2012, PLoS Comput. Biol..

[39]  Á. Pascual-Leone,et al.  A Review of Combined TMS-EEG Studies to Characterize Lasting Effects of Repetitive TMS and Assess Their Usefulness in Cognitive and Clinical Neuroscience , 2009, Brain Topography.

[40]  Daniel Lehmann,et al.  Regulated Criticality in the Brain? , 1998, Adv. Complex Syst..

[41]  P A Robinson,et al.  Neural field theory of plasticity in the cerebral cortex. , 2013, Journal of theoretical biology.

[42]  Á. Pascual-Leone,et al.  Non-invasive brain stimulation for Parkinson’s disease: a systematic review and meta-analysis of the literature , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[43]  S. Wang,et al.  Malleability of Spike-Timing-Dependent Plasticity at the CA3–CA1 Synapse , 2006, The Journal of Neuroscience.

[44]  P. Basser,et al.  A model of the stimulation of a nerve fiber by electromagnetic induction , 1990, IEEE Transactions on Biomedical Engineering.

[45]  C. Civardi,et al.  Applications of transcranial magnetic stimulation in sleep medicine. , 2009, Sleep medicine reviews.

[46]  John N. J. Reynolds,et al.  Numerical modelling of plasticity induced by transcranial magnetic stimulation , 2014, Journal of Computational Neuroscience.

[47]  Leon N. Cooper,et al.  A Biophysical Basis for the Inter-spike Interaction of Spike-timing-dependent Plasticity , 2006, Biological Cybernetics.

[48]  W. Paulus,et al.  Breaks during 5Hz rTMS are essential for facilitatory after effects , 2010, Clinical Neurophysiology.

[49]  Ingo Bojak,et al.  Axonal Velocity Distributions in Neural Field Equations , 2010, PLoS Comput. Biol..

[50]  H. Haken,et al.  Field Theory of Electromagnetic Brain Activity. , 1996, Physical review letters.

[51]  P. Robinson,et al.  Prediction of electroencephalographic spectra from neurophysiology. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  Shinsuke Shimojo,et al.  A model of magnetic stimulation of neocortical neurons , 2001, Neurocomputing.

[53]  Carson C. Chow,et al.  Calcium time course as a signal for spike-timing-dependent plasticity. , 2005, Journal of neurophysiology.

[54]  Á. Pascual-Leone,et al.  Safety of Theta Burst Transcranial Magnetic Stimulation: A Systematic Review of the Literature , 2011, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[56]  Diane Ruge,et al.  Short‐interval paired‐pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity , 2002, The Journal of physiology.

[57]  Gaby S. Pell,et al.  Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: Influence of timing and geometrical parameters and underlying mechanisms , 2011, Progress in Neurobiology.

[58]  P. Basser,et al.  Elucidating the mechanisms and loci of neuronal excitation by transcranial magnetic stimulation using a finite element model of a cortical sulcus , 2008, Clinical Neurophysiology.

[59]  W. Gerstner,et al.  Triplets of Spikes in a Model of Spike Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[60]  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.

[61]  H. Shouval,et al.  Stochastic properties of synaptic transmission affect the shape of spike time-dependent plasticity curves. , 2005, Journal of neurophysiology.

[62]  William W. McDonald,et al.  Efficacy and Safety of Transcranial Magnetic Stimulation in the Acute Treatment of Major Depression: A Multisite Randomized Controlled Trial , 2007, Biological Psychiatry.

[63]  Klaus Funke,et al.  Cortical cellular actions of transcranial magnetic stimulation. , 2010, Restorative neurology and neuroscience.

[64]  M. Poo,et al.  Calcium stores regulate the polarity and input specificity of synaptic modification , 2000, Nature.

[65]  Abraham Zangen,et al.  Translational Neuromodulation: Approximating Human Transcranial Magnetic Stimulation Protocols in Rats , 2012, Neuromodulation : journal of the International Neuromodulation Society.

[66]  P A Robinson,et al.  Neural field theory of synaptic plasticity. , 2011, Journal of theoretical biology.

[67]  John C. Rothwell,et al.  Plasticity in the Human Nervous System: Techniques of transcranial magnetic stimulation , 2003 .