Neural field theory of calcium dependent plasticity with applications to transcranial magnetic stimulation.

Calcium dependent plasticity (CaDP), a physiologically realistic plasticity mechanism in the microscopic regime, is incorporated into a neural field theory to explore system-level plasticity. This system-level plasticity model is capable of reproducing the characteristic plasticity window of spike-timing dependent plasticity (STDP) in paired associative stimulation (PAS), where a peripheral electric pulse stimulation is paired to transcranial magnetic stimulation (TMS) in the cortex, and rTMS frequency dependent plasticity, where low and high frequency rTMS trains induce depression and potentiation, respectively. These thus reproduce experimental results for system-level plasticity for the first time. This also bridges the gap between microscopic plasticity theory and system-level plasticity observed experimentally, and addresses long standing problems of stability and adaptability by predicting stable plasticity, a possible seizure state where neurons fire at a high rate, and spike-rate adaptation.

[1]  G. Bi,et al.  Timing in synaptic plasticity: from detection to integration , 2005, Trends in Neurosciences.

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

[3]  Gary W. Thickbroom,et al.  Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models , 2007, Experimental Brain Research.

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

[5]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[6]  Wulfram Gerstner,et al.  A History of Spike-Timing-Dependent Plasticity , 2011, Front. Syn. Neurosci..

[7]  P. Robinson,et al.  Modal analysis of corticothalamic dynamics, electroencephalographic spectra, and evoked potentials. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  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.

[9]  P. J. Basser,et al.  Stimulation of a myelinated nerve axon by electromagnetic induction , 1991, Medical and Biological Engineering and Computing.

[10]  Steven J. Schiff,et al.  Dynamical evolution of spatiotemporal patterns in mammalian middle cortex. , 2007 .

[11]  Wulfram Gerstner,et al.  Phenomenological models of synaptic plasticity based on spike timing , 2008, Biological Cybernetics.

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

[13]  N. Hatsopoulos,et al.  Propagating waves mediate information transfer in the motor cortex , 2006, Nature Neuroscience.

[14]  Jeffrey P. Gavornik,et al.  Effect of stochastic synaptic and dendritic dynamics on synaptic plasticity in visual cortex and hippocampus. , 2007, Journal of neurophysiology.

[15]  Peter A. Robinson,et al.  Spike-rate adaptation and neuronal bursting in a mean-field model of brain activity , 2007, Biological Cybernetics.

[16]  R. L. Beurle Properties of a mass of cells capable of regenerating pulses , 1956, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[17]  Jian-Young Wu,et al.  Compression and Reflection of Visually Evoked Cortical Waves , 2007, Neuron.

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

[19]  P A Robinson,et al.  Estimation of multiscale neurophysiologic parameters by electroencephalographic means , 2004, Human brain mapping.

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

[21]  J L Lancaster,et al.  Detailed 3D models of the induced electric field of transcranial magnetic stimulation coils , 2007, Physics in medicine and biology.

[22]  Nikos K. Logothetis,et al.  Directed Coupling in Local Field Potentials of Macaque V4 During Visual Short-Term Memory Revealed by Multivariate Autoregressive Models , 2010, Front. Comput. Neurosci..

[23]  T. Sejnowski,et al.  The Book of Hebb , 1999, Neuron.

[24]  X J Wang,et al.  Calcium coding and adaptive temporal computation in cortical pyramidal neurons. , 1998, Journal of neurophysiology.

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

[26]  L. Partridge Calcium independence of slow currents underlying spike frequency adaptation. , 1980, Journal of neurobiology.

[27]  Wulfram Gerstner,et al.  Spike-timing dependent plasticity , 2010, Scholarpedia.

[28]  Hauke R. Heekeren,et al.  Linking neuronal variability to perceptual decision making via neuroimaging , 2011 .

[29]  A. Berardelli,et al.  Motor cortex excitability following short trains of repetitive magnetic stimuli , 2001, Experimental Brain Research.

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

[31]  L. Raymond,et al.  Changes in agonist concentration dependence that are a function of duration of exposure suggest N-methyl-D-aspartate receptor nonsaturation during synaptic stimulation. , 2001, Molecular pharmacology.

[32]  Zafiris J Daskalakis,et al.  Transcranial magnetic stimulation: a new investigational and treatment tool in psychiatry. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[33]  Nicolas Brunel,et al.  Mechanisms of Induction and Maintenance of Spike-Timing Dependent Plasticity in Biophysical Synapse Models , 2010, Front. Comput. Neurosci..

[34]  P. Robinson,et al.  Dynamics of large-scale brain activity in normal arousal states and epileptic seizures. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  L. Cohen,et al.  A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. , 2003, Journal of neurophysiology.

[36]  Stephen Coombes,et al.  Waves, bumps, and patterns in neural field theories , 2005, Biological Cybernetics.

[37]  Wulfram Gerstner,et al.  Mathematical formulations of Hebbian learning , 2002, Biological Cybernetics.

[38]  P. Nunez,et al.  Neocortical Dynamics and Human EEG Rhythms , 1995 .

[39]  Y. Sugita Global plasticity in adult visual cortex following reversal of visual input , 1996, Nature.

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

[41]  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.

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

[43]  Ramón Huerta,et al.  Biophysical model of synaptic plasticity dynamics , 2003, Biological Cybernetics.

[44]  J. Classen,et al.  Plasticity Resembling Spike-Timing Dependent Synaptic Plasticity: The Evidence in Human Cortex , 2010, Front. Syn. Neurosci..

[45]  Donald O. Walter,et al.  Mass action in the nervous system , 1975 .

[46]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[47]  Arjen van Ooyen,et al.  Competition in the development of nerve connections: a review of models , 2001 .

[48]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[49]  R. Kempter,et al.  Hebbian learning and spiking neurons , 1999 .

[50]  Gayle M. Wittenberg,et al.  Spike Timing Dependent Plasticity: A Consequence of More Fundamental Learning Rules , 2010, Front. Comput. Neurosci..

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

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

[53]  J. Bell,et al.  Auditory transduction: A model for the role of intracellular calcium in short-term adaptation , 1991 .

[54]  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.

[55]  Refael Hassin,et al.  Minimum cost flow with set-constraints , 1982, Networks.

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

[57]  E. Kunesch,et al.  Timing‐dependent plasticity in human primary somatosensory cortex , 2005, The Journal of physiology.

[58]  O. Krishtal,et al.  Distinct quantal features of AMPA and NMDA synaptic currents in hippocampal neurons: implication of glutamate spillover and receptor saturation. , 2003, Biophysical journal.

[59]  P R Montague,et al.  The resource consumption principle: attention and memory in volumes of neural tissue. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Leon N. Cooper,et al.  Calcium as the associative signal for a model of Hebbian plasticity: application to multi-input environments , 2003, Neurocomputing.

[61]  R. Brownstone,et al.  Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones , 2005, The Journal of physiology.

[62]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[63]  M. Iino,et al.  Visualization of glutamate as a volume transmitter , 2011, The Journal of physiology.

[64]  J. Rothwell,et al.  Consensus: Motor cortex plasticity protocols , 2008, Brain Stimulation.

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

[66]  J. S. McCasland,et al.  Large-scale plasticity in barrel cortex following repeated whisker trimming in young adult hamsters , 2003, Experimental Neurology.

[67]  M. Binder,et al.  Multiple mechanisms of spike-frequency adaptation in motoneurones , 1999, Journal of Physiology-Paris.