Short-Term Synaptic Plasticity in Central Pattern Generators

Short-term synaptic plasticity (STP) is a transient (milliseconds to minutes) activity-dependent change in the amplitude (strength) of the postsynaptic current in response to presynaptic activity. It has clear implications for neural signaling and has been studied for several decades. Much of the modeling work has focused on the events in the presynaptic terminal and primarily on the role of Ca in of neurotransmitters (Zucker & Regehr ; Fioravante and Regehr 2+ synaptic release 2002 ). However, postsynaptic effects such as saturation of can also contribute to STP (Hennig 2011 postsynaptic receptors ; Xu-Friedman and Regehr ). A complete understanding of short-term synaptic plasticity requires knowing how 2013 2004 the preand postsynaptic neurons interact to alter synaptic strength. The contribution of short-term synaptic plasticity to network-level output has probably been best examined in studies of networks. CPG networks produce rhythmic patterned outputs without patterned input and central pattern generator (CPG) are best understood in the analysis of rhythmic motor activities such as locomotion and respiration. For instance, the CPG underlying the inspiratory phase of respiration is located in the found within the ventrolateral pre-Botzinger complex medulla of the mammalian brain (Grillner ). Identified CPG circuits are known to govern locomotion in invertebrates, 2003 including , mollusks, and crustaceans (Arshavsky Yu et al. ; Ayers ; Friesen and Kristan ). leeches 1993 2004 2007 Additionally, locomotion in mammals is believed to be governed by CPG networks in the spinal cord (MacKay-Lyons 2002 ). The understanding of CPGs in producing motor behaviors has been greatly advanced through the use of computational (Butera et al. ; Tabak et al. ; Oh et al. ; Vavoulis et al. ; Sherwood et al. ). models 1999 200

[1]  Thomas C. Südhof,et al.  Multiple Roles for the Active Zone Protein RIM1α in Late Stages of Neurotransmitter Release , 2004, Neuron.

[2]  A. Ijspeert,et al.  From Swimming to Walking with a Salamander Robot Driven by a Spinal Cord Model , 2007, Science.

[3]  J. C. Smith,et al.  Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. , 1991, Science.

[4]  Jeffrey L. Mendenhall,et al.  Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations , 2009, Proceedings of the National Academy of Sciences.

[5]  T. Südhof The Presynaptic Active Zone , 2012, Neuron.

[6]  Jan-Marino Ramirez,et al.  Differential Contribution of Pacemaker Properties to the Generation of Respiratory Rhythms during Normoxia and Hypoxia , 2004, Neuron.

[7]  H. Markram,et al.  Information Processing with Frequency-Dependent Synaptic Connections , 1998, Neurobiology of Learning and Memory.

[8]  A. Roberts,et al.  The neuromuscular basis of rhythmic struggling movements in embryos of Xenopus laevis. , 1982, The Journal of experimental biology.

[9]  W. Stein,et al.  Functional consequences of activity-dependent synaptic enhancement at a crustacean neuromuscular junction , 2006, Journal of Experimental Biology.

[10]  M. Wilson,et al.  SNAP-25 and synaptotagmin involvement in the final Ca(2+)-dependent triggering of neurotransmitter exocytosis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Farzan Nadim,et al.  Peptide Neuromodulation of Synaptic Dynamics in an Oscillatory Network , 2011, The Journal of Neuroscience.

[12]  R. Jahn,et al.  Molecular machines governing exocytosis of synaptic vesicles , 2012, Nature.

[13]  R S Zucker,et al.  Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[14]  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.

[15]  W. Regehr Short-term presynaptic plasticity. , 2012, Cold Spring Harbor perspectives in biology.

[16]  Y. Arshavsky,et al.  Neuronal control of swimming locomotion: analysis of the pteropod mollusc Clione and embryos of the amphibian Xenopus , 1993, Trends in Neurosciences.

[17]  J. Eilers,et al.  Paired‐pulse facilitation at recurrent Purkinje neuron synapses is independent of calbindin and parvalbumin during high‐frequency activation , 2013, The Journal of physiology.

[18]  J. Ayers Underwater walking. , 2004, Arthropod structure & development.

[19]  C. Jahr,et al.  Multivesicular Release at Climbing Fiber-Purkinje Cell Synapses , 2001, Neuron.

[20]  Consuelo Morgado-Valle,et al.  Respiratory Rhythm An Emergent Network Property? , 2002, Neuron.

[21]  Christian Rosenmund,et al.  Definition of the Readily Releasable Pool of Vesicles at Hippocampal Synapses , 1996, Neuron.

[22]  John Guckenheimer,et al.  Synaptic patterning of left-right alternation in a computational model of the rodent hindlimb central pattern generator , 2011, Journal of Computational Neuroscience.

[23]  J. Birns,et al.  Phenytoin toxicity: an easily missed cause of cerebellar syndrome , 2008, Journal of clinical pharmacy and therapeutics.

[24]  Susan M. Wagner,et al.  Explaining Math: Gesturing Lightens the Load , 2001, Psychological science.

[25]  Xiao-Jing Wang,et al.  Alternating and Synchronous Rhythms in Reciprocally Inhibitory Model Neurons , 1992, Neural Computation.

[26]  W. O. Friesen,et al.  Leech locomotion: swimming, crawling, and decisions , 2007, Current Opinion in Neurobiology.

[27]  Anatol C. Kreitzer,et al.  Interaction of Postsynaptic Receptor Saturation with Presynaptic Mechanisms Produces a Reliable Synapse , 2002, Neuron.

[28]  L. Lagnado,et al.  Endogenous Calcium Buffers Regulate Fast Exocytosis in the Synaptic Terminal of Retinal Bipolar Cells , 2002, Neuron.

[29]  A. Roberts,et al.  Reconfiguration of a Vertebrate Motor Network: Specific Neuron Recruitment and Context-Dependent Synaptic Plasticity , 2007, The Journal of Neuroscience.

[30]  Joël Tabak,et al.  Parameter Estimation Methods for Single Neuron Models , 2000, Journal of Computational Neuroscience.

[31]  Anders Lansner,et al.  Modeling of Substance P and 5-HT Induced Synaptic Plasticity in the Lamprey Spinal CPG: Consequences for Network Pattern Generation , 2001, Journal of Computational Neuroscience.

[32]  R. Llinás,et al.  Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. , 1985, Biophysical journal.

[33]  Geometrical analysis of bursting pacemaker neurons generated by computational models: comparison to in vitro pre-Bötzinger complex bursting neurons. , 2010, Advances in experimental medicine and biology.

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

[35]  E. Neher Vesicle Pools and Ca2+ Microdomains: New Tools for Understanding Their Roles in Neurotransmitter Release , 1998, Neuron.

[36]  W. Betz,et al.  Active Zones and the Readily Releasable Pool of Synaptic Vesicles at the Neuromuscular Junction of the Mouse , 2011, The Journal of Neuroscience.

[37]  R. Zucker,et al.  A General Model of Synaptic Transmission and Short-Term Plasticity , 2009, Neuron.

[38]  Jianfeng Feng,et al.  Dynamic control of a central pattern generator circuit: a computational model of the snail feeding network , 2007, The European journal of neuroscience.

[39]  Eve Marder,et al.  Mechanisms for oscillation and frequency control in reciprocally inhibitory model neural networks , 1994, Journal of Computational Neuroscience.

[40]  J. Eilers,et al.  Bassoon Speeds Vesicle Reloading at a Central Excitatory Synapse , 2010, Neuron.

[41]  Farzan Nadim,et al.  Short-Term Dynamics of a Mixed Chemical and Electrical Synapse in a Rhythmic Network , 2003, The Journal of Neuroscience.

[42]  Pan-Yue Deng,et al.  The diverse functions of short-term plasticity components in synaptic computations , 2011 .

[43]  Short‐term synaptic plasticity and the ‘active calcium’ hypothesis at a central synapse , 2013, The Journal of physiology.

[44]  Thomas C. Südhof,et al.  RIM Proteins Tether Ca2+ Channels to Presynaptic Active Zones via a Direct PDZ-Domain Interaction , 2011, Cell.

[45]  Farzan Nadim,et al.  Neuromodulatory changes in short-term synaptic dynamics may be mediated by two distinct mechanisms of presynaptic calcium entry , 2012, Journal of Computational Neuroscience.

[46]  E. Marder,et al.  Principles of rhythmic motor pattern generation. , 1996, Physiological reviews.

[47]  R. Bertram,et al.  Modeling study of the effects of overlapping Ca2+ microdomains on neurotransmitter release. , 1999, Biophysical journal.

[48]  S Grillner,et al.  Long‐lasting substance‐P‐mediated modulation of NMDA‐induced rhythmic activity in the lamprey locomotor network involves separate RNA‐ and protein‐synthesis‐dependent stages , 1999, The European journal of neuroscience.

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

[50]  E. Marder,et al.  Invertebrate Central Pattern Generation Moves along , 2005, Current Biology.

[51]  A. Marty,et al.  Readily releasable pool of synaptic vesicles measured at single synaptic contacts , 2012, Proceedings of the National Academy of Sciences.

[52]  R. Bertram,et al.  Buffers on Synaptic Facilitation 2 + Ca Can Account for the Effects of 2 + Residual Bound Ca , 2006 .

[53]  E. Neher,et al.  Vesicle pools and short-term synaptic depression: lessons from a large synapse , 2002, Trends in Neurosciences.

[54]  S. Grillner The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[55]  R. Bertram,et al.  A minimal model for G protein-mediated synaptic facilitation and depression. , 2003, Journal of neurophysiology.

[56]  Andrei Rozov,et al.  Presynaptic Ca2+ dynamics, Ca2+ buffers and synaptic efficacy. , 2005, Cell calcium.

[57]  Arthur Sherman,et al.  New and corrected simulations of synaptic facilitation. , 2002, Biophysical journal.

[58]  J. C. Smith,et al.  Models of respiratory rhythm generation in the pre-Bötzinger complex. II. Populations Of coupled pacemaker neurons. , 1999, Journal of neurophysiology.

[59]  T. Carew,et al.  Contirbution of Postsynaptic Ca2+ to the Induction of Posttetanic Potentiation in the Neural Circuit for Siphon Withdrawal inAplysia , 2001, The Journal of Neuroscience.

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

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

[62]  E. F. Stanley The calcium channel and the organization of the presynaptic transmitter release face , 1997, Trends in Neurosciences.

[63]  Farzan Nadim,et al.  Modeling the leech heartbeat elemental oscillator I. Interactions of intrinsic and synaptic currents , 1995, Journal of Computational Neuroscience.

[64]  Dmitri A Rusakov,et al.  Main Determinants of Presynaptic Ca2+ Dynamics at Individual Mossy Fiber–CA3 Pyramidal Cell Synapses , 2006, The Journal of Neuroscience.

[65]  R. Bertram,et al.  Residual bound Ca2+ can account for the effects of Ca2+ buffers on synaptic facilitation. , 2006, Journal of neurophysiology.

[66]  M. MacKay-Lyons Central pattern generation of locomotion: a review of the evidence. , 2002, Physical therapy.

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

[68]  W. Regehr,et al.  Structural contributions to short-term synaptic plasticity. , 2004, Physiological reviews.

[69]  H. Ohmori,et al.  Inhibition of presynaptic Na+/K+-ATPase reduces readily releasable pool size at the avian end-bulb of Held synapse , 2012, Neuroscience Research.

[70]  R. Zucker,et al.  Facilitation through buffer saturation: constraints on endogenous buffering properties. , 2004, Biophysical journal.

[71]  R. Jahn,et al.  Munc18-Bound Syntaxin Readily Forms SNARE Complexes with Synaptobrevin in Native Plasma Membranes , 2006, PLoS biology.

[72]  Farzan Nadim,et al.  Contribution of synaptic depression to phase maintenance in a model rhythmic network. , 2003, Journal of neurophysiology.

[73]  M A Xu-Friedman,et al.  Three-Dimensional Comparison of Ultrastructural Characteristics at Depressing and Facilitating Synapses onto Cerebellar Purkinje Cells , 2001, The Journal of Neuroscience.

[74]  Robert J Butera,et al.  Persistent sodium current, membrane properties and bursting behavior of pre-bötzinger complex inspiratory neurons in vitro. , 2002, Journal of neurophysiology.

[75]  P. Kaeser Pushing synaptic vesicles over the RIM , 2011, Cellular logistics.

[76]  Michael J. O'Donovan,et al.  The Role of Activity-Dependent Network Depression in the Expression and Self-Regulation of Spontaneous Activity in the Developing Spinal Cord , 2001, The Journal of Neuroscience.

[77]  Matthias H. Hennig,et al.  Theoretical models of synaptic short term plasticity , 2013, Front. Comput. Neurosci..