Temporal modulation of spike-timing-dependent plasticity

Spike-timing-dependent plasticity (STDP) has attracted considerable experimental and theoretical attention over the last decade. In the most basic formulation, STDP provides a fundamental unit – a spike pair – for quantifying the induction of long-term changes in synaptic strength. However, many factors, both pre- and postsynaptic, can affect synaptic transmission and integration, especially when multiple spikes are considered. Here we review the experimental evidence for multiple types of nonlinear temporal interactions in STDP, focusing on the contributions of individual spike pairs, overall spike rate, and precise spike timing for modification of cortical and hippocampal excitatory synapses. We discuss the underlying processes that determine the specific learning rules at different synapses, such as postsynaptic excitability and short-term depression. Finally, we describe the success of efforts toward building predictive, quantitative models of how complex and natural spike trains induce long-term synaptic modifications.

[1]  N. RafaelLorenteDe,et al.  SYNAPTIC STIMULATION OF MOTONEURONS AS A LOCAL PROCESS , 1938 .

[2]  L. Bindman,et al.  Long-lasting Changes in the Level of the Electrical Activity of the Cerebral Cortex produced by Polarizing Currents , 1962, Nature.

[3]  E. Fischer Conditioned Reflexes , 1942, American journal of physical medicine.

[4]  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.

[5]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[6]  T. Neild,et al.  Membrane properties. , 1979, British medical bulletin.

[7]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[8]  A. Baranyi,et al.  Synaptic facilitation requires paired activation of convergent pathways in the neocortex , 1981, Nature.

[9]  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.

[10]  W. Levy,et al.  Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus , 1983, Neuroscience.

[11]  H. Scharfman,et al.  Postsynaptic firing during repetitive stimulation is required for long-term potentiation in hippocampus , 1985, Brain Research.

[12]  S. Kelso,et al.  Hebbian synapses in hippocampus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[13]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  T. Sejnowski,et al.  Associative long-term depression in the hippocampus induced by hebbian covariance , 1989, Nature.

[15]  Drew McDermott,et al.  A critique of pure reason 1 , 1987, The Philosophy of Artificial Intelligence.

[16]  T. H. Brown,et al.  Biophysical model of a Hebbian synapse. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[17]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[18]  H. Higashi,et al.  Membrane properties of guinea pig cingulate cortical neurons in vitro. , 1991, Journal of neurophysiology.

[19]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[20]  M. Bear,et al.  Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Bear,et al.  Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. , 1993, Science.

[22]  D. Debanne,et al.  Asynchronous pre- and postsynaptic activity induces associative long-term depression in area CA1 of the rat hippocampus in vitro. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Mark F. Bear,et al.  Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience , 1995, Nature.

[24]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[25]  D. Debanne,et al.  Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[27]  Steven L. Miller,et al.  Temporal Processing Deficits of Language-Learning Impaired Children Ameliorated by Training , 1996, Science.

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

[29]  Steven L. Miller,et al.  Language Comprehension in Language-Learning Impaired Children Improved with Acoustically Modified Speech , 1996, Science.

[30]  S. Cruikshank,et al.  Evidence for the Hebbian hypothesis in experience-dependent physiological plasticity of neocortex: a critical review , 1996, Brain Research Reviews.

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

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

[33]  D. Johnston,et al.  K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons , 1997, Nature.

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

[35]  W. Singer,et al.  Relation Between Dendritic Ca2+ Levels and the Polarity of Synaptic Long‐term Modifications in Rat Visual Cortex Neurons , 1997, The European journal of neuroscience.

[36]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[37]  D. Debanne,et al.  Action-potential propagation gated by an axonal IA-like K+ conductance in hippocampus , 1997, Nature.

[38]  L. Abbott,et al.  A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex , 1997, The Journal of Neuroscience.

[39]  J. Hopfield,et al.  All-or-none potentiation at CA3-CA1 synapses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[41]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  C. Gilbert Adult cortical dynamics. , 1998, Physiological reviews.

[44]  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.

[45]  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.

[46]  D. Buonomano,et al.  Distinct Functional Types of Associative Long-Term Potentiation in Neocortical and Hippocampal Pyramidal Neurons , 1999, The Journal of Neuroscience.

[47]  D. Debanne,et al.  Heterogeneity of Synaptic Plasticity at Unitary CA3–CA1 and CA3–CA3 Connections in Rat Hippocampal Slice Cultures , 1999, The Journal of Neuroscience.

[48]  O. Paulsen,et al.  Rapid report: postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus. , 1999, The Journal of physiology.

[49]  R. Zucker,et al.  Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. , 1999, Journal of neurophysiology.

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

[51]  C. Stevens,et al.  Response of Hippocampal Synapses to Natural Stimulation Patterns , 1999, Neuron.

[52]  R. Zucker Calcium- and activity-dependent synaptic plasticity , 1999, Current Opinion in Neurobiology.

[53]  B. Sakmann,et al.  Developmental Switch in the Short-Term Modification of Unitary EPSPs Evoked in Layer 2/3 and Layer 5 Pyramidal Neurons of Rat Neocortex , 1999, The Journal of Neuroscience.

[54]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

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

[56]  Y. Frégnac,et al.  Activity-dependent regulation of receptive field properties of cat area 17 by supervised Hebbian learning. , 1999, Journal of neurobiology.

[57]  D. Debanne,et al.  The role of dendritic filtering in associative long-term synaptic plasticity. , 1999, Learning & memory.

[58]  Mark C. W. van Rossum,et al.  Stable Hebbian Learning from Spike Timing-Dependent Plasticity , 2000, The Journal of Neuroscience.

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

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

[61]  S. Nelson,et al.  Hebb and homeostasis in neuronal plasticity , 2000, Current Opinion in Neurobiology.

[62]  S. Wang,et al.  Coincidence detection in single dendritic spines mediated by calcium release , 2000, Nature Neuroscience.

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

[64]  T. Sejnowski,et al.  Natural patterns of activity and long-term synaptic plasticity , 2000, Current Opinion in Neurobiology.

[65]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[66]  M. Bear,et al.  Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity , 2000, Nature.

[67]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

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

[69]  Henry Markram,et al.  An Algorithm for Modifying Neurotransmitter Release Probability Based on Pre- and Postsynaptic Spike Timing , 2001, Neural Computation.

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

[71]  Joseph E LeDoux,et al.  Fear conditioning and LTP in the lateral amygdala are sensitive to the same stimulus contingencies , 2001, Nature Neuroscience.

[72]  Rajesh P. N. Rao,et al.  Spike-Timing-Dependent Hebbian Plasticity as Temporal Difference Learning , 2001, Neural Computation.

[73]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[74]  R. Malinow,et al.  Postsynaptic conversion of silent synapses during LTP affects synaptic gain and transmission dynamics , 2001, Nature Neuroscience.

[75]  Charlotte A. Boettiger,et al.  Developmentally Restricted Synaptic Plasticity in a Songbird Nucleus Required for Song Learning , 2001, Neuron.

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

[77]  Karim Nader,et al.  Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective , 2001, Trends in Neurosciences.

[78]  Shigeo Watanabe,et al.  Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[79]  G. Bi,et al.  Temporal asymmetry in spike timing-dependent synaptic plasticity , 2002, Physiology & Behavior.

[80]  Guo-Qiang Bi,et al.  Synaptic modification in neural circuits: a timely action. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[81]  Dean V. Buonomano,et al.  Mechanisms and significance of spike-timing dependent plasticity , 2002, Biological Cybernetics.

[82]  Terrence J Sejnowski,et al.  Complexity of calcium signaling in synaptic spines. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[83]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[84]  B. Sakmann,et al.  Molecular dissection of hippocampal theta-burst pairing potentiation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[85]  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.

[86]  Y. Dan,et al.  Spike-timing-dependent synaptic modification induced by natural spike trains , 2002, Nature.

[87]  U. Karmarkar,et al.  A model of spike-timing dependent plasticity: one or two coincidence detectors? , 2002, Journal of neurophysiology.

[88]  Navzer D. Engineer,et al.  Cortical network reorganization guided by sensory input features , 2002, Biological Cybernetics.

[89]  H. Abarbanel,et al.  Dynamical model of long-term synaptic plasticity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[90]  M. Min,et al.  Enhancement of Associative Long-Term Potentiation by Activation of β-Adrenergic Receptors at CA1 Synapses in Rat Hippocampal Slices , 2003, The Journal of Neuroscience.

[91]  P. J. Sjöström,et al.  Neocortical LTD via Coincident Activation of Presynaptic NMDA and Cannabinoid Receptors , 2003, Neuron.

[92]  J J Hopfield,et al.  Learning rules and network repair in spike-timing-based computation networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Andreas Knoblauch,et al.  Synaptic plasticity, conduction delays, and inter-areal phase relations of spike activity in a model of reciprocally connected areas , 2003, Neurocomputing.

[94]  O. Paulsen,et al.  Maturation of Long-Term Potentiation Induction Rules in Rodent Hippocampus: Role of GABAergic Inhibition , 2003, The Journal of Neuroscience.

[95]  D. Johnston,et al.  Active dendrites, potassium channels and synaptic plasticity. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[96]  Shigeo Watanabe,et al.  Synaptically Activated Ca2+ Waves in Layer 2/3 and Layer 5 Rat Neocortical Pyramidal Neurons , 2003, The Journal of physiology.

[97]  R. Lorente,et al.  SYNAPTIC STIMULATION OF MOTONEURONS AS A LOCAL PROCESS , 2004 .

[98]  P. Jonas,et al.  Kinetics of Mg2+ unblock of NMDA receptors: implications for spike‐timing dependent synaptic plasticity , 2004, The Journal of physiology.

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

[100]  D. Ulrich,et al.  Firing Mode-Dependent Synaptic Plasticity in Rat Neocortical Pyramidal Neurons , 2004, The Journal of Neuroscience.

[101]  P. J. Sjöström,et al.  Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. , 2004, Journal of neurophysiology.

[102]  Takeshi Aihara,et al.  Spatial analysis of spike‐timing‐dependent LTP and LTD in the CA1 area of hippocampal slices using optical imaging , 2005, Hippocampus.

[103]  Y. Dan,et al.  Spike-timing-dependent synaptic plasticity depends on dendritic location , 2005, Nature.

[104]  S. Wang,et al.  Graded bidirectional synaptic plasticity is composed of switch-like unitary events. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[107]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

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

[109]  L. Abbott,et al.  Cascade Models of Synaptically Stored Memories , 2005, Neuron.

[110]  Tobias M. Rasse,et al.  Glutamate receptor dynamics organizing synapse formation in vivo , 2005, Nature Neuroscience.

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

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

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

[114]  Daniel Johnston,et al.  Deletion of Kv4.2 Gene Eliminates Dendritic A-Type K+ Current and Enhances Induction of Long-Term Potentiation in Hippocampal CA1 Pyramidal Neurons , 2006, The Journal of Neuroscience.

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

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

[117]  Vanessa A. Bender,et al.  Two Coincidence Detectors for Spike Timing-Dependent Plasticity in Somatosensory Cortex , 2006, The Journal of Neuroscience.

[118]  H. Sompolinsky,et al.  The tempotron: a neuron that learns spike timing–based decisions , 2006, Nature Neuroscience.

[119]  B. Sakmann,et al.  Spine Ca2+ Signaling in Spike-Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

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

[121]  H. Markram The Blue Brain Project , 2006, Nature Reviews Neuroscience.

[122]  Karel Svoboda,et al.  Locally dynamic synaptic learning rules in pyramidal neuron dendrites , 2007, Nature.

[123]  C. Shatz,et al.  A Burst-Based “Hebbian” Learning Rule at Retinogeniculate Synapses Links Retinal Waves to Activity-Dependent Refinement , 2007, PLoS biology.

[124]  C. Schreiner,et al.  A synaptic memory trace for cortical receptive field plasticity , 2007, Nature.

[125]  Yun Wang,et al.  Developmental Switch in the Contribution of Presynaptic and Postsynaptic NMDA Receptors to Long-Term Depression , 2007, The Journal of Neuroscience.

[126]  A. Kirkwood,et al.  Neuromodulators Control the Polarity of Spike-Timing-Dependent Synaptic Plasticity , 2007, Neuron.

[127]  J. Mellor,et al.  The development of synaptic plasticity induction rules and the requirement for postsynaptic spikes in rat hippocampal CA1 pyramidal neurones , 2007, The Journal of physiology.

[128]  L. Trussell,et al.  Coactivation of Pre- and Postsynaptic Signaling Mechanisms Determines Cell-Specific Spike-Timing-Dependent Plasticity , 2007, Neuron.

[129]  Masahiko Watanabe,et al.  SK2 channel plasticity contributes to LTP at Schaffer collateral–CA1 synapses , 2008, Nature Neuroscience.

[130]  Haruo Kasai,et al.  Protein Synthesis and Neurotrophin-Dependent Structural Plasticity of Single Dendritic Spines , 2008, Science.

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

[132]  H. Urakubo,et al.  Requirement of an Allosteric Kinetics of NMDA Receptors for Spike Timing-Dependent Plasticity , 2008, The Journal of Neuroscience.

[133]  P. Greengard,et al.  Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity , 2008, Science.

[134]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[135]  J. Kerr,et al.  Dopamine Receptor Activation Is Required for Corticostriatal Spike-Timing-Dependent Plasticity , 2008, The Journal of Neuroscience.

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

[137]  Emilie Campanac,et al.  Spike timing‐dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons , 2008, The Journal of physiology.

[138]  D. Feldman Synaptic mechanisms for plasticity in neocortex. , 2009, Annual review of neuroscience.

[139]  Sten Grillner,et al.  Input specificity and dependence of spike timing-dependent plasticity on preceding postsynaptic activity at unitary connections between neocortical layer 2/3 pyramidal cells. , 2009, Cerebral cortex.

[140]  G. Bi,et al.  Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses , 2009, Proceedings of the National Academy of Sciences.

[141]  Alan Fine,et al.  Expression of Long-Term Plasticity at Individual Synapses in Hippocampus Is Graded, Bidirectional, and Mainly Presynaptic: Optical Quantal Analysis , 2009, Neuron.

[142]  Bruce D. Gelb,et al.  The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction , 2009, Cell.