Effect of Inhibitory Spike-Timing-Dependent Plasticity on Fast Sparsely Synchronized Rhythms in A Small-World Neuronal Network

We consider the Watts-Strogatz small-world network (SWN) consisting of inhibitory fast spiking Izhikevich interneurons. This inhibitory neuronal population has adaptive dynamic synaptic strengths governed by the inhibitory spike-timing-dependent plasticity (iSTDP). In previous works without iSTDP, fast sparsely synchronized rhythms, associated with diverse cognitive functions, were found to appear in a range of large noise intensities for fixed strong synaptic inhibition strengths. Here, we investigate the effect of iSTDP on fast sparse synchronization (FSS) by varying the noise intensity D. We employ an asymmetric anti-Hebbian time window for the iSTDP update rule [which is in contrast to the Hebbian time window for the excitatory STDP (eSTDP)]. Depending on values of D, population-averaged values of saturated synaptic inhibition strengths are potentiated [long-term potentiation (LTP)] or depressed [long-term depression (LTD)] in comparison with the initial mean value, and dispersions from the mean values of LTP/LTD are much increased when compared with the initial dispersion, independently of D. In most cases of LTD where the effect of mean LTD is dominant in comparison with the effect of dispersion, good synchronization (with higher spiking measure) is found to get better via LTD, while bad synchronization (with lower spiking measure) is found to get worse via LTP. This kind of Matthew effect in inhibitory synaptic plasticity is in contrast to that in excitatory synaptic plasticity where good (bad) synchronization gets better (worse) via LTP (LTD). Emergences of LTD and LTP of synaptic inhibition strengths are intensively investigated via a microscopic method based on the distributions of time delays between the pre- and the post-synaptic spike times. Furthermore, we also investigate the effects of network architecture on FSS by changing the rewiring probability p of the SWN in the presence of iSTDP.

[1]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[2]  Henning Sprekeler,et al.  Inhibitory synaptic plasticity: spike timing-dependence and putative network function , 2013, Front. Neural Circuits.

[3]  Maxi San Miguel,et al.  STOCHASTIC EFFECTS IN PHYSICAL SYSTEMS , 2000 .

[4]  Markus Diesmann,et al.  Spike-Timing-Dependent Plasticity in Balanced Random Networks , 2007, Neural Computation.

[5]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[6]  Y. Dan,et al.  Spike Timing-Dependent Plasticity of Neural Circuits , 2004, Neuron.

[7]  Thomas J. Palmeri,et al.  ENCYCLOPEDIA OF COGNITIVE SCIENCE , 2001 .

[8]  Shan Yu,et al.  A Small World of Neuronal Synchrony , 2008, Cerebral cortex.

[9]  S. Solla,et al.  Multiple attractors, long chaotic transients, and failure in small-world networks of excitable neurons. , 2007, Chaos.

[10]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[11]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[12]  Nicolas Brunel,et al.  Sparsely synchronized neuronal oscillations. , 2008, Chaos.

[13]  D. Watts,et al.  Small Worlds: The Dynamics of Networks between Order and Randomness , 2001 .

[14]  Woochang Lim,et al.  Burst synchronization in a scale-free neuronal network with inhibitory spike-timing-dependent plasticity , 2018, Cognitive Neurodynamics.

[15]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[16]  Guanrong Chen,et al.  Impact of delays and rewiring on the dynamics of small-world neuronal networks with two types of coupling , 2010 .

[17]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[18]  M. Woodin,et al.  Spike-Timing Dependent Plasticity in Inhibitory Circuits , 2010, Front. Syn. Neurosci..

[19]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[22]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[23]  Peter A. Tass,et al.  Self-organized noise resistance of oscillatory neural networks with spike timing-dependent plasticity , 2013, Scientific Reports.

[24]  Danielle M. Santarelli.  The developing brain. , 1969, Nature.

[25]  Nicolas Brunel,et al.  Fast Global Oscillations in Networks of Integrate-and-Fire Neurons with Low Firing Rates , 1999, Neural Computation.

[26]  Shigeru Shinomoto,et al.  Kernel bandwidth optimization in spike rate estimation , 2009, Journal of Computational Neuroscience.

[27]  John Guare,et al.  Six Degrees of Separation: A Play , 1990 .

[28]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[29]  R. Traub,et al.  Inhibition-based rhythms: experimental and mathematical observations on network dynamics. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[30]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[31]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

[32]  Eugene M. Izhikevich,et al.  Neural excitability, Spiking and bursting , 2000, Int. J. Bifurc. Chaos.

[33]  Arjen van Ooyen,et al.  Dynamic Hebbian Cross-Correlation Learning Resolves the Spike Timing Dependent Plasticity Conundrum , 2018, Front. Comput. Neurosci..

[34]  Jean-Michel Deniau,et al.  Cell‐specific spike‐timing‐dependent plasticity in GABAergic and cholinergic interneurons in corticostriatal rat brain slices , 2008, The Journal of physiology.

[35]  A. Pérez-Villalba.  Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[36]  L. Trussell,et al.  Cell-specific, spike timing–dependent plasticities in the dorsal cochlear nucleus , 2004, Nature Neuroscience.

[37]  Xiao-Jing Wang.  Neural Oscillations , 2002 .

[38]  O. Kwon,et al.  Coherence resonance in small-world networks of excitable cells , 2002 .

[39]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[40]  Alexander L. Green.  Cortical Oscillations in Health and Disease. Oxford Univ. Press, New York (2010), June, Color plates, Hard cover, 448 pp, $74.95., ISBN: 978-0-19-534279-6 , 2010 .

[41]  S. Solla,et al.  Self-sustained activity in a small-world network of excitable neurons. , 2003, Physical review letters.

[42]  Christof Koch,et al.  Local Field Potentials Encode Place Cell Ensemble Activation during Hippocampal Sharp Wave Ripples , 2015, Neuron.

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

[44]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[45]  Woochang Lim,et al.  Realistic thermodynamic and statistical-mechanical measures for neural synchronization , 2014, Journal of Neuroscience Methods.

[46]  Daniel D. Lee,et al.  Equilibrium properties of temporally asymmetric Hebbian plasticity. , 2000, Physical review letters.

[47]  Eran Stark,et al.  Sharp wave ripples during learning stabilize hippocampal spatial map , 2017, Nature Neuroscience.

[48]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[49]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

[50]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[51]  Eugene M Izhikevich,et al.  Hybrid spiking models , 2010, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[52]  Y. Dan,et al.  Spike timing-dependent plasticity: from synapse to perception. , 2006, Physiological reviews.

[53]  Nicolas Brunel,et al.  Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges. , 2005, Journal of neurophysiology.

[54]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[55]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[56]  Olaf Sporns,et al.  Small worlds inside big brains , 2006, Proceedings of the National Academy of Sciences.

[57]  Duncan J. Watts,et al.  Book Review: Small Worlds. The Dynamics of Networks Between Order and Randomness , 2000 .

[58]  E. Marder,et al.  Activity-dependent modification of inhibitory synapses in models of rhythmic neural networks , 2001, Nature Neuroscience.

[59]  D. Kullmann,et al.  Plasticity of Inhibition , 2012, Neuron.

[60]  J. Glowinski,et al.  Bidirectional Activity-Dependent Plasticity at Corticostriatal Synapses , 2005, The Journal of Neuroscience.

[61]  G Tononi,et al.  Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. , 2000, Cerebral cortex.

[62]  B. Sakmann,et al.  Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex , 1999, Nature Neuroscience.

[63]  Marcus Kaiser,et al.  Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems , 2006, PLoS Comput. Biol..

[64]  S. Strogatz.  Exploring complex networks , 2001, Nature.

[65]  Mikhail Prokopenko,et al.  Information Dynamics in Small-World Boolean Networks , 2011, Artificial Life.

[66]  Kamran Diba,et al.  Regulation of Hippocampal Firing by Network Oscillations during Sleep , 2016, Current Biology.

[67]  A. Hodgkin.  The local electric changes associated with repetitive action in a non‐medullated axon , 1948, The Journal of physiology.

[68]  Li I. Zhang,et al.  A critical window for cooperation and competition among developing retinotectal synapses , 1998, Nature.

[69]  T. Sejnowski,et al.  Storing covariance with nonlinearly interacting neurons , 1977, Journal of mathematical biology.

[70]  L F Lago-Fernández,et al.  Fast response and temporal coherent oscillations in small-world networks. , 1999, Physical review letters.

[71]  J. Gross,et al.  Brain Rhythms of Pain , 2017, Trends in Cognitive Sciences.

[72]  Nicolas Brunel,et al.  How Noise Affects the Synchronization Properties of Recurrent Networks of Inhibitory Neurons , 2006, Neural Computation.

[73]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

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

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

[76]  Henning Sprekeler,et al.  Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks , 2011, Science.

[77]  G. Buzsáki.  Hippocampal sharp waves: Their origin and significance , 1986, Brain Research.

[78]  Matthew A. Wilson,et al.  From hippocampus to V1: Effect of LTP on spatio-temporal dynamics of receptive fields , 2000, Neurocomputing.

[79]  R. Froemke.  Plasticity of cortical excitatory-inhibitory balance. , 2015, Annual review of neuroscience.

[80]  Chiayu Q. Chiu,et al.  Long-term plasticity at inhibitory synapses , 2011, Current Opinion in Neurobiology.

[81]  K. I. Blum,et al.  Functional significance of long-term potentiation for sequence learning and prediction. , 1996, Cerebral cortex.

[82]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[83]  G. Feng,et al.  Next-Generation Optical Technologies for Illuminating Genetically Targeted Brain Circuits , 2006, The Journal of Neuroscience.

[84]  Erik De Schutter,et al.  Dynamic synchronization of Purkinje cell simple spikes. , 2006, Journal of neurophysiology.

[85]  Peter A. Tass,et al.  Desynchronizing electrical and sensory coordinated reset neuromodulation , 2012, Front. Hum. Neurosci..

[86]  M. Shanahan.  Dynamical complexity in small-world networks of spiking neurons. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[87]  Johannes J. Letzkus,et al.  Learning Rules for Spike Timing-Dependent Plasticity Depend on Dendritic Synapse Location , 2006, The Journal of Neuroscience.

[88]  V. Han,et al.  Synaptic plasticity in a cerebellum-like structure depends on temporal order , 1997, Nature.

[89]  Guanrong Chen,et al.  Synchronization transitions on small-world neuronal networks: Effects of information transmission delay and rewiring probability , 2008 .

[90]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[91]  J. Knott.  The organization of behavior: A neuropsychological theory , 1951 .

[92]  C. Malsburg.  Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[93]  Eugene M. Izhikevich,et al.  Which model to use for cortical spiking neurons? , 2004, IEEE Transactions on Neural Networks.

[94]  M. Ozer,et al.  Stochastic resonance on Newman–Watts networks of Hodgkin–Huxley neurons with local periodic driving , 2009 .

[95]  Woochang Lim,et al.  Stochastic spike synchronization in a small-world neural network with spike-timing-dependent plasticity , 2017, Neural Networks.

[96]  M. Carandini,et al.  Subcortical Source and Modulation of the Narrowband Gamma Oscillation in Mouse Visual Cortex , 2016, Neuron.

[97]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[98]  Jasmine A. Nirody,et al.  Exploiting pallidal plasticity for stimulation in Parkinson’s disease , 2015, Journal of neural engineering.

[99]  Nicole C. Swann,et al.  Gamma Oscillations in the Hyperkinetic State Detected with Chronic Human Brain Recordings in Parkinson's Disease , 2016, Journal of Neuroscience.

[100]  G. Stent.  A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[101]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[102]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

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

[104]  L. Abbott,et al.  Cortical Development and Remapping through Spike Timing-Dependent Plasticity , 2001, Neuron.

[105]  Xiao-Jing Wang.  Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[106]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Dgpartement de Physique.  Synchronization of the Stochastic Fitzhugh-Nagumo Equations to Periodic Forcing ( * ) . , 1995 .

[108]  Y. Dan,et al.  Contribution of individual spikes in burst-induced long-term synaptic modification. , 2006, Journal of neurophysiology.

[109]  T. Sejnowski,et al.  Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5–2 Hz), theta (5–12 Hz), and gamma (35–70 Hz) bands , 2000, Hippocampus.

[110]  D. Long.  Networks of the Brain , 2011 .

[111]  Tsuyoshi Murata,et al.  {m , 1934, ACML.

[112]  D. Feldman.  The Spike-Timing Dependence of Plasticity , 2012, Neuron.

[113]  Péter P. Ujma,et al.  Nap sleep spindle correlates of intelligence , 2015, Scientific Reports.

[114]  Woochang Lim,et al.  Statistical-mechanical measure of stochastic spiking coherence in a population of inhibitory subthreshold neurons , 2011, Journal of Computational Neuroscience.

[115]  Chris G. Antonopoulos,et al.  Spike timing-dependent plasticity induces non-trivial topology in the brain , 2016, Neural Networks.

[116]  Phillip Larimer,et al.  Nonrandom Local Circuits in the Dentate Gyrus , 2008, The Journal of Neuroscience.

[117]  André Longtin.  Stochastic aspects of neural phase locking to periodic signals , 2000 .

[118]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

[119]  William L. Ditto,et al.  Spike timing dependent plasticity promotes synchrony of inhibitory networks in the presence of heterogeneity , 2008, Journal of Computational Neuroscience.

[120]  Woochang Lim,et al.  Effect of spike-timing-dependent plasticity on stochastic burst synchronization in a scale-free neuronal network , 2017, Cognitive Neurodynamics.

[121]  Jesper Tegnér,et al.  Spike-timing-dependent plasticity: common themes and divergent vistas , 2002, Biological Cybernetics.

[122]  Woochang Lim,et al.  Effect of Small-World Connectivity on Fast Sparsely Synchronized Cortical Rhythms , 2014, 1403.1034.

[123]  Y. Ben-Ari,et al.  Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance , 2002, Trends in Neurosciences.

[124]  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.

[125]  M. Poo,et al.  Coincident Pre- and Postsynaptic Activity Modifies GABAergic Synapses by Postsynaptic Changes in Cl− Transporter Activity , 2003, Neuron.

[126]  J. Rinzel,et al.  Clustering in globally coupled inhibitory neurons , 1994 .

[127]  Raoul Borges,et al.  Effects of the spike timing-dependent plasticity on the synchronisation in a random Hodgkin-Huxley neuronal network , 2015, Commun. Nonlinear Sci. Numer. Simul..

[128]  Sharon L. Milgram,et al.  The Small World Problem , 1967 .

[129]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[130]  L. F. Abbott,et al.  A Model of Spatial Map Formation in the Hippocampus of the Rat , 1999, Neural Computation.

[131]  D. Kullmann,et al.  Long-term synaptic plasticity in hippocampal interneurons , 2007, Nature Reviews Neuroscience.

[132]  Bartlett W. Mel,et al.  Cortical rewiring and information storage , 2004, Nature.

[133]  P. Brown,et al.  EEG–EMG, MEG–EMG and EMG–EMG frequency analysis: physiological principles and clinical applications , 2002, Clinical Neurophysiology.

[134]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

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

[136]  Front , 2020, 2020 Fourth World Conference on Smart Trends in Systems, Security and Sustainability (WorldS4).

[137]  Jessica A. Cardin,et al.  Dissecting local circuits in vivo: Integrated optogenetic and electrophysiology approaches for exploring inhibitory regulation of cortical activity , 2012, Journal of Physiology-Paris.

[138]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[139]  P. Steerenberg,et al.  Targeting pathophysiological rhythms: prednisone chronotherapy shows sustained efficacy in rheumatoid arthritis. , 2010, Annals of the rheumatic diseases.

[140]  T. Sejnowski,et al.  Cortical gamma band synchronization through somatostatin interneurons , 2017, Nature Neuroscience.

[141]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[142]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.

[143]  Jie Wu,et al.  Small Worlds: The Dynamics of Networks between Order and Randomness , 2003 .

[144]  Celso Grebogi,et al.  Synaptic Plasticity and Spike Synchronisation in Neuronal Networks , 2017, 1709.00455.

[145]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[146]  W. Gerstner,et al.  Spike-Timing-Dependent Plasticity: A Comprehensive Overview , 2012, Front. Syn. Neurosci..

[147]  G. Tamás,et al.  Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro , 1998, The Journal of physiology.

[148]  Woochang Lim,et al.  Sparsely-synchronized brain rhythm in a small-world neural network , 2013, Journal of the Korean Physical Society.

[149]  H. Abarbanel,et al.  Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. , 2006, Journal of neurophysiology.

[150]  N. Spruston,et al.  Questions about STDP as a General Model of Synaptic Plasticity , 2010, Front. Syn. Neurosci..

[151]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[152]  Woochang Lim,et al.  Effect of Sparse Random Connectivity on the Stochastic Spiking Coherence of Inhibitory Subthreshold Neurons , 2011 .

[153]  Charles M. Gray,et al.  Synchronous oscillations in neuronal systems: Mechanisms and functions , 1994, Journal of Computational Neuroscience.

[154]  Woochang Lim,et al.  Fast sparsely synchronized brain rhythms in a scale-free neural network. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[155]  G. Buzsáki,et al.  Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus , 2017, Science.

[156]  Antal Berényi,et al.  Role of Hippocampal CA2 Region in Triggering Sharp-Wave Ripples , 2016, Neuron.

[157]  I. Freiman.  Conditioned Reflexes and Neuron Organization , 1950 .

[158]  G. Buzsáki,et al.  Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons , 2004, Trends in Neurosciences.

[159]  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.

[160]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.