Theoretical models of synaptic short term plasticity

Short term plasticity is a highly abundant form of rapid, activity-dependent modulation of synaptic efficacy. A shared set of mechanisms can cause both depression and enhancement of the postsynaptic response at different synapses, with important consequences for information processing. Mathematical models have been extensively used to study the mechanisms and roles of short term plasticity. This review provides an overview of existing models and their biological basis, and of their main properties. Special attention will be given to slow processes such as calcium channel inactivation and the effect of activation of presynaptic autoreceptors.

[1]  I. Forsythe,et al.  Facilitation of the presynaptic calcium current at an auditory synapse in rat brainstem , 1998, The Journal of physiology.

[2]  T. Abe.  [Calcium channels]. , 1997, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[3]  Adrian Y. C. Wong,et al.  Unmasking group III metabotropic glutamate autoreceptor function at excitatory synapses in the rat CNS , 2005, The Journal of physiology.

[4]  L. Trussell,et al.  Rapid desensitization of glutamate receptors in vertebrate central neurons. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[5]  D. Brody,et al.  Preferential Closed-State Inactivation of Neuronal Calcium Channels , 1998, Neuron.

[6]  Idan Segev,et al.  Multiple mechanisms govern the dynamics of depression at neocortical synapses of young rats , 2004, The Journal of physiology.

[7]  Patrick J Drew,et al.  Models and properties of power-law adaptation in neural systems. , 2006, Journal of neurophysiology.

[8]  Wade G. Regehr,et al.  Associative Short-Term Synaptic Plasticity Mediated by Endocannabinoids , 2005, Neuron.

[9]  E. Neher,et al.  Combining Deconvolution and Noise Analysis for the Estimation of Transmitter Release Rates at the Calyx of Held , 2001, The Journal of Neuroscience.

[10]  B. Doiron,et al.  Short-term synaptic depression and stochastic vesicle dynamics reduce and shape neuronal correlations. , 2013, Journal of neurophysiology.

[11]  V. Klyachko,et al.  Short-Term Plasticity Optimizes Synaptic Information Transmission , 2011, The Journal of Neuroscience.

[12]  T. Sejnowski,et al.  Independent Sources of Quantal Variability at Single Glutamatergic Synapses , 2003, The Journal of Neuroscience.

[13]  Jason S. Rothman,et al.  Modeling Synapses , 2014, Encyclopedia of Computational Neuroscience.

[14]  D. Quastel,et al.  The binomial model in fluctuation analysis of quantal neurotransmitter release. , 1997, Biophysical journal.

[15]  W. Catterall,et al.  Regulation of Presynaptic CaV2.1 Channels by Ca2+ Sensor Proteins Mediates Short-Term Synaptic Plasticity , 2008, Neuron.

[16]  Ian D Forsythe,et al.  Interactions between multiple sources of short‐term plasticity during evoked and spontaneous activity at the rat calyx of Held , 2008, The Journal of physiology.

[17]  A. Zippelius,et al.  Heterogeneous presynaptic release probabilities: functional relevance for short-term plasticity. , 2003, Biophysical journal.

[18]  Matthias H Hennig,et al.  Acceleration of AMPA receptor kinetics underlies temperature‐dependent changes in synaptic strength at the rat calyx of Held , 2007, The Journal of physiology.

[19]  W. Betz,et al.  Synaptic vesicle pools , 2005, Nature Reviews Neuroscience.

[20]  W. Regehr,et al.  Determinants of the Time Course of Facilitation at the Granule Cell to Purkinje Cell Synapse , 1996, The Journal of Neuroscience.

[21]  Brent Doiron,et al.  Short Term Synaptic Depression Imposes a Frequency Dependent Filter on Synaptic Information Transfer , 2012, PLoS Comput. Biol..

[22]  Terrence J. Sejnowski,et al.  An Efficient Method for Computing Synaptic Conductances Based on a Kinetic Model of Receptor Binding , 1994, Neural Computation.

[23]  B. Katz,et al.  Quantal components of the end‐plate potential , 1954, The Journal of physiology.

[24]  Maria Blatow,et al.  Ca2+ Buffer Saturation Underlies Paired Pulse Facilitation in Calbindin-D28k-Containing Terminals , 2003, Neuron.

[25]  L. Trussell,et al.  Desensitization of AMPA receptors upon multiquantal neurotransmitter release , 1993, Neuron.

[26]  A. W. Liley,et al.  An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. , 1953, Journal of neurophysiology.

[27]  J. C. Nelson,et al.  Quantal Analysis Reveals a Functional Correlation between Presynaptic and Postsynaptic Efficacy in Excitatory Connections from Rat Neocortex , 2010, The Journal of Neuroscience.

[28]  E. Neher,et al.  Quantitative Relationship between Transmitter Release and Calcium Current at the Calyx of Held Synapse , 2001, The Journal of Neuroscience.

[29]  Andrei Rozov,et al.  Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression , 1999, Nature.

[30]  Scott T. Wong,et al.  Ca2+/calmodulin binds to and modulates P/Q-type calcium channels , 1999, Nature.

[31]  Misha Tsodyks,et al.  Persistent Activity in Neural Networks with Dynamic Synapses , 2007, PLoS Comput. Biol..

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

[33]  R. Zucker,et al.  Post-tetanic decay of evoked and spontaneous transmitter release and a residual-calcium model of synaptic facilitation at crayfish neuromuscular junctions , 1983, The Journal of general physiology.

[34]  Wade G Regehr,et al.  Short-term forms of presynaptic plasticity , 2011, Current Opinion in Neurobiology.

[35]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[36]  T. Sakaba,et al.  Activity-dependent modulation of endocytosis by calmodulin at a large central synapse , 2011, Proceedings of the National Academy of Sciences.

[37]  T. Teyler.  Long-term potentiation and memory. , 1987, International journal of neurology.

[38]  Maryann E Martone,et al.  Evidence for Ectopic Neurotransmission at a Neuronal Synapse , 2005, Science.

[39]  Alex M Thomson,et al.  Binomial parameters differ across neocortical layers and with different classes of connections in adult rat and cat neocortex , 2007, Proceedings of the National Academy of Sciences.

[40]  W G Regehr,et al.  Calcium Dependence and Recovery Kinetics of Presynaptic Depression at the Climbing Fiber to Purkinje Cell Synapse , 1998, The Journal of Neuroscience.

[41]  W. Betz,et al.  Depression of transmitter release at the neuromuscular junction of the frog , 1970, The Journal of physiology.

[42]  E. Neher,et al.  Estimating synaptic parameters from mean, variance, and covariance in trains of synaptic responses. , 2001, Biophysical journal.

[43]  Scott T. Wong,et al.  Ca 2 + / calmodulin binds to andmodulates P / Q-typecalciumchannels , 2022 .

[44]  Charles F Stevens,et al.  Activity-Dependent Modulation of the Rate at which Synaptic Vesicles Become Available to Undergo Exocytosis , 1998, Neuron.

[45]  Ralf Schneggenburger,et al.  Intracellular calcium dependence of transmitter release rates at a fast central synapse , 2000, Nature.

[46]  Henry Markram,et al.  Coding of temporal information by activity-dependent synapses. , 2002, Journal of neurophysiology.

[47]  Thomas K. Berger,et al.  Heterogeneity in the pyramidal network of the medial prefrontal cortex , 2006, Nature Neuroscience.

[48]  Takeshi Nakamura,et al.  Developmental changes in calcium/calmodulin‐dependent inactivation of calcium currents at the rat calyx of Held , 2008, The Journal of physiology.

[49]  R. Duvoisin,et al.  Glutamate Transporter Studies Reveal the Pruning of Metabotropic Glutamate Receptors and Absence of AMPA Receptor Desensitization at Mature Calyx of Held Synapses , 2005, The Journal of Neuroscience.

[50]  B Sakmann,et al.  Calcium sensitivity of glutamate release in a calyx-type terminal. , 2000, Science.

[51]  T. Sudhof,et al.  The synaptic vesicle cycle. , 2004, Annual review of neuroscience.

[52]  Terrence J. Sejnowski,et al.  Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism , 1994, Journal of Computational Neuroscience.

[53]  Anatol C. Kreitzer,et al.  Interplay between Facilitation, Depression, and Residual Calcium at Three Presynaptic Terminals , 2000, The Journal of Neuroscience.

[54]  R. Schneggenburger,et al.  A Mechanism Intrinsic to the Vesicle Fusion Machinery Determines Fast and Slow Transmitter Release at a Large CNS Synapse , 2007, The Journal of Neuroscience.

[55]  Thomas J. Carew,et al.  Multiple overlapping processes underlying short-term synaptic enhancement , 1997, Trends in Neurosciences.

[56]  E. Neher,et al.  Quantitative Analysis of Calcium-Dependent Vesicle Recruitment and Its Functional Role at the Calyx of Held Synapse , 2007, The Journal of Neuroscience.

[57]  B Sakmann,et al.  Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem , 1998, The Journal of physiology.

[58]  Adrian Y. C. Wong,et al.  Distinguishing between Presynaptic and Postsynaptic Mechanisms of Short-Term Depression during Action Potential Trains , 2003, Journal of Neuroscience.

[59]  Henry Markram,et al.  Neural Networks with Dynamic Synapses , 1998, Neural Computation.

[60]  B. Lindner,et al.  Synaptic filtering of rate-coded information. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[61]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[62]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[63]  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.

[64]  T. Branco,et al.  The probability of neurotransmitter release: variability and feedback control at single synapses , 2009, Nature Reviews Neuroscience.

[65]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[66]  Jianhua Xu,et al.  The Decrease in the Presynaptic Calcium Current Is a Major Cause of Short-Term Depression at a Calyx-Type Synapse , 2005, Neuron.

[67]  G. Westbrook,et al.  The impact of receptor desensitization on fast synaptic transmission , 1996, Trends in Neurosciences.

[68]  I. Forsythe,et al.  Presynaptic Calcium Current Modulation by a Metabotropic Glutamate Receptor , 1996, Science.

[69]  B. Katz,et al.  The role of calcium in neuromuscular facilitation , 1968, The Journal of physiology.

[70]  Zhijun Yang,et al.  Wide-Band Information Transmission at the Calyx of Held , 2009, Neural Computation.

[71]  Margaret Barnes-Davies,et al.  Inactivation of Presynaptic Calcium Current Contributes to Synaptic Depression at a Fast Central Synapse , 1998, Neuron.

[72]  Felix Felmy,et al.  Probing the Intracellular Calcium Sensitivity of Transmitter Release during Synaptic Facilitation , 2003, Neuron.

[73]  B. Grothe,et al.  Modeling short-term synaptic plasticity at the calyx of Held using in vivo-like stimulation patterns. , 2009, Journal of neurophysiology.

[74]  J. Borst,et al.  Dynamics of the readily releasable pool during post‐tetanic potentiation in the rat calyx of Held synapse , 2007, The Journal of physiology.

[75]  T. Bartol,et al.  Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[76]  R. Schneggenburger,et al.  Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion , 2005, Nature.

[77]  J. Gouaux,et al.  AMPA Receptor Binding Cleft Mutations That Alter Affinity, Efficacy, and Recovery from Desensitization , 2005, The Journal of Neuroscience.

[78]  M. Ghirardi,et al.  Phosphorylation of synapsin domain A is required for post-tetanic potentiation , 2007, Journal of Cell Science.

[79]  Leonard K. Kaczmarek,et al.  High-frequency firing helps replenish the readily releasable pool of synaptic vesicles , 1998, Nature.

[80]  P. Dayan,et al.  Synapses with short-term plasticity are optimal estimators of presynaptic membrane potentials , 2010, Nature Neuroscience.

[81]  Ian Duguid,et al.  Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron–Purkinje cell synapses , 2004, Nature Neuroscience.

[82]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

[83]  P. Jonas,et al.  Efficacy and Stability of Quantal GABA Release at a Hippocampal Interneuron–Principal Neuron Synapse , 2000, The Journal of Neuroscience.

[84]  L. Abbott,et al.  Synaptic computation , 2004, Nature.

[85]  Yukihiro Nakamura,et al.  G protein-dependent presynaptic inhibition mediated by AMPA receptors at the calyx of Held. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[86]  I. Forsythe,et al.  The calyx of Held , 2006, Cell and Tissue Research.

[87]  Matthias H. Hennig,et al.  A biophysical model of short-term plasticity at the calyx of Held , 2007, Neurocomputing.

[88]  Henry Markram,et al.  Multiquantal release underlies the distribution of synaptic effi cacies in the neocortex , 2022 .

[89]  N. Parga,et al.  Short-term Synaptic Depression Causes a Non-monotonic Response to Correlated Stimuli , 2022 .

[90]  Takeshi Sakaba,et al.  The Coupling between Synaptic Vesicles and Ca2+ Channels Determines Fast Neurotransmitter Release , 2007, Neuron.

[91]  E. De robertis,et al.  SOME FEATURES OF THE SUBMICROSCOPIC MORPHOLOGY OF SYNAPSES IN FROG AND EARTHWORM , 1955, The Journal of biophysical and biochemical cytology.

[92]  R. Schneggenburger,et al.  Posttetanic potentiation critically depends on an enhanced Ca2+ sensitivity of vesicle fusion mediated by presynaptic PKC , 2007, Proceedings of the National Academy of Sciences.

[93]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[94]  K. Magleby,et al.  Augmentation and facilitation of transmitter release. A quantitative description at the frog neuromuscular junction , 1982, The Journal of general physiology.