Experience-dependent regulation of presynaptic NMDARs enhances neurotransmitter release at neocortical synapses

Sensory experience can selectively alter excitatory synaptic strength at neocortical synapses. The rapid increase in synaptic strength induced by selective whisker stimulation (single-row experience/SRE, where all but one row of whiskers has been removed from the mouse face) is due, at least in part, to the trafficking of AMPA receptors (AMPARs) to the post-synaptic membrane, and is developmentally regulated. How enhanced sensory experience can alter presynaptic release properties in the developing neocortex has not been investigated. Using paired-pulse stimulation at layer 4-2/3 synapses in acute brain slices, we found that presynaptic release probability progressively increases in the spared-whisker barrel column over the first 24 h of SRE. Enhanced release probability can be at least partly attributed to presynaptic NMDA receptors (NMDARs). We find that the influence of presynaptic NMDARs in enhancing EPSC amplitude markedly increases during SRE. This occurs at the same time when recently potentiated synapses become highly susceptible to a NMDAR-dependent form of synaptic depression, during the labile phase of plasticity. Thus, these data show that augmented sensory stimulation can enhance release probability at layer 4-2/3 synapses and enhance the function of presynaptic NMDARs. Because presynaptic NMDARs have been linked to synaptic depression at layer 4-2/3 synapses, we propose that SRE-dependent up-regulation of presynaptic NMDARs is responsible for enhanced synaptic depression during the labile stage of plasticity.

[1]  R. Nicoll,et al.  Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. , 1989, Science.

[2]  Y. Benjamini,et al.  More powerful procedures for multiple significance testing. , 1990, Statistics in medicine.

[3]  T. Dawson,et al.  Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  B. Sakmann,et al.  Developmental and regional expression in the rat brain and functional properties of four NMDA receptors , 1994, Neuron.

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

[6]  N. Berretta,et al.  Tonic facilitation of glutamate release by presynaptic N-methyl-d-aspartate autoreceptors in the entorhinal cortex , 1996, Neuroscience.

[7]  Daniel E Feldman,et al.  Long-Term Depression at Thalamocortical Synapses in Developing Rat Somatosensory Cortex , 1998, Neuron.

[8]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[9]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[10]  G. Westbrook,et al.  The Incorporation of NMDA Receptors with a Distinct Subunit Composition at Nascent Hippocampal Synapses In Vitro , 1999, The Journal of Neuroscience.

[11]  Mark F. Bear,et al.  Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo , 1999, Nature Neuroscience.

[12]  B. Connors,et al.  Sensory experience modifies the short-term dynamics of neocortical synapses , 1999, Nature.

[13]  H. Schröder,et al.  Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon , 1999, Brain Research.

[14]  S. Hrabetova,et al.  Distinct NMDA Receptor Subpopulations Contribute to Long-Term Potentiation and Long- Term Depression Induction , 2000, The Journal of Neuroscience.

[15]  K. Svoboda,et al.  Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo , 2000, Nature.

[16]  M. Bear,et al.  Visual Experience and Deprivation Bidirectionally Modify the Composition and Function of NMDA Receptors in Visual Cortex , 2001, Neuron.

[17]  Alison L. Barth,et al.  NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses , 2001, Nature Neuroscience.

[18]  T. Schikorski,et al.  Inactivity Produces Increases in Neurotransmitter Release and Synapse Size , 2001, Neuron.

[19]  P. De Camilli,et al.  Chronic Blockade of Glutamate Receptors Enhances Presynaptic Release and Downregulates the Interaction between Synaptophysin-Synaptobrevin–Vesicle-Associated Membrane Protein 2 , 2001, The Journal of Neuroscience.

[20]  B. Sakmann,et al.  Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell‐specific difference in presynaptic calcium dynamics , 2001, The Journal of physiology.

[21]  L. Maffei,et al.  Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex , 2002, Science.

[22]  Niraj S. Desai,et al.  Critical periods for experience-dependent synaptic scaling in visual cortex , 2002, Nature Neuroscience.

[23]  Hiroto Takahashi,et al.  Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits , 2002, Nature.

[24]  G. Knott,et al.  Formation of Dendritic Spines with GABAergic Synapses Induced by Whisker Stimulation in Adult Mice , 2002, Neuron.

[25]  John R Huguenard,et al.  Pathway-Specific Differences in Subunit Composition of Synaptic NMDA Receptors on Pyramidal Neurons in Neocortex , 2003, The Journal of Neuroscience.

[26]  Y. Yoshimura,et al.  Two Forms of Synaptic Plasticity with Distinct Dependence on Age, Experience, and NMDA Receptor Subtype in Rat Visual Cortex , 2003, The Journal of Neuroscience.

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

[28]  G. Collingridge,et al.  Differential Roles of NR2A and NR2B-Containing NMDA Receptors in Cortical Long-Term Potentiation and Long-Term Depression , 2004, The Journal of Neuroscience.

[29]  M. Sheng,et al.  Role of NMDA Receptor Subtypes in Governing the Direction of Hippocampal Synaptic Plasticity , 2004, Science.

[30]  Richard C Gerkin,et al.  Alteration of Neuronal Firing Properties after In Vivo Experience in a FosGFP Transgenic Mouse , 2004, The Journal of Neuroscience.

[31]  T. Hensch.  Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

[32]  M. Salter,et al.  NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury , 2005, Nature.

[33]  G. Woodhall,et al.  Tonic Facilitation of Glutamate Release by Presynaptic NR2B-Containing NMDA Receptors Is Increased in the Entorhinal Cortex of Chronically Epileptic Rats , 2006, The Journal of Neuroscience.

[34]  Y. Yanagawa,et al.  Major Effects of Sensory Experiences on the Neocortical Inhibitory Circuits , 2006, The Journal of Neuroscience.

[35]  Daniel E. Feldman,et al.  Synaptic Basis for Whisker Deprivation-Induced Synaptic Depression in Rat Somatosensory Cortex , 2006, The Journal of Neuroscience.

[36]  D. Kullmann,et al.  Epileptogenesis is associated with enhanced glutamatergic transmission in the perforant path. , 2006, Journal of neurophysiology.

[37]  Alison L. Barth,et al.  Pathway-Specific Trafficking of Native AMPARs by In Vivo Experience , 2006, Neuron.

[38]  Michael J. Gutnick,et al.  NMDA Receptors in Layer 4 Spiny Stellate Cells of the Mouse Barrel Cortex Contain the NR2C Subunit , 2006, The Journal of Neuroscience.

[39]  D. McCormick,et al.  Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential , 2006, Nature.

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

[41]  Claire E. J. Cheetham,et al.  Sensory Experience Alters Cortical Connectivity and Synaptic Function Site Specifically , 2007, The Journal of Neuroscience.

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

[43]  L. Maffei,et al.  Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity , 2007, Nature Neuroscience.

[44]  S. Roper,et al.  Impaired Developmental Switch of Short‐term Plasticity in Pyramidal Cells of Dysplastic Cortex , 2007, Epilepsia.

[45]  D. Feldman,et al.  Presynaptic NMDA Receptors: Newly Appreciated Roles in Cortical Synaptic Function and Plasticity , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[46]  Benjamin D. Philpot,et al.  Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity , 2008, Neuropharmacology.

[47]  Alison L. Barth,et al.  Ongoing in Vivo Experience Triggers Synaptic Metaplasticity in the Neocortex , 2008, Science.

[48]  Ole Paulsen,et al.  Spike timing–dependent long-term depression requires presynaptic NMDA receptors , 2008, Nature Neuroscience.

[49]  D. Feldman,et al.  Synapse-Specific Expression of Functional Presynaptic NMDA Receptors in Rat Somatosensory Cortex , 2008, The Journal of Neuroscience.

[50]  O. Paulsen,et al.  Double Dissociation of Spike Timing–Dependent Potentiation and Depression by Subunit-Preferring NMDA Receptor Antagonists in Mouse Barrel Cortex , 2009, Cerebral cortex.

[51]  B. Brew,et al.  Characterisation of the Expression of NMDA Receptors in Human Astrocytes , 2010, PloS one.

[52]  R. Huganir,et al.  PICK1 Regulates Incorporation of Calcium-Permeable AMPA Receptors during Cortical Synaptic Strengthening , 2010, The Journal of Neuroscience.

[53]  Hui Li Li,et al.  Astrocytes Express N-Methyl-D-Aspartate Receptor Subunits in Development, Ischemia and Post-Ischemia , 2010, Neurochemical Research.

[54]  Takao K. Hensch,et al.  Lynx1, a Cholinergic Brake, Limits Plasticity in Adult Visual Cortex , 2010, Science.

[55]  Hazel A. Collins,et al.  Presynaptic Induction and Expression of Timing-Dependent Long-Term Depression Demonstrated by Compartment-Specific Photorelease of a Use-Dependent NMDA Receptor Antagonist , 2011, The Journal of Neuroscience.

[56]  S. Lipton,et al.  NR3A-containing NMDARs promote neurotransmitter release and spike timing–dependent plasticity , 2011, Nature Neuroscience.

[57]  Alison L. Barth,et al.  Input-Specific Critical Periods for Experience-Dependent Plasticity in Layer 2/3 Pyramidal Neurons , 2011, The Journal of Neuroscience.

[58]  F. Kimura,et al.  Developmental Switch in Spike Timing-Dependent Plasticity at Layers 4–2/3 in the Rodent Barrel Cortex , 2012, The Journal of Neuroscience.

[59]  Alison L. Barth,et al.  Synaptic lability after experience-dependent plasticity is not mediated by calcium-permeable AMPARs , 2012, Front. Mol. Neurosci..

[60]  T. Jones,et al.  Altered neurotransmitter release, vesicle recycling and presynaptic structure in the pilocarpine model of temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

[61]  Karel Svoboda,et al.  Regular Spiking and Intrinsic Bursting Pyramidal Cells Show Orthogonal Forms of Experience-Dependent Plasticity in Layer V of Barrel Cortex , 2012, Neuron.

[62]  H. Beck,et al.  The Presynaptic Active Zone Protein RIM1α Controls Epileptogenesis following Status Epilepticus , 2012, The Journal of Neuroscience.

[63]  Arne V. Blackman,et al.  Target-Specific Expression of Presynaptic NMDA Receptors in Neocortical Microcircuits , 2012, Neuron.

[64]  Sandra J. Kuhlman,et al.  A disinhibitory microcircuit initiates critical period plasticity in visual cortex , 2013, Nature.

[65]  Maria Andres-Alonso,et al.  Molecular mechanisms driving homeostatic plasticity of neurotransmitter release , 2013, Front. Cell. Neurosci..

[66]  P. Honsa,et al.  Send Orders of Reprints at Reprints@benthamscience.net Nmda Receptors in Glial Cells: Pending Questions , 2022 .

[67]  B. Philpot,et al.  Presynaptic NMDA Receptor Mechanisms for Enhancing Spontaneous Neurotransmitter Release , 2013, The Journal of Neuroscience.

[68]  D. Muller,et al.  GluN3A: An NMDA Receptor Subunit with Exquisite Properties and Functions , 2013, Neural plasticity.

[69]  O. Paulsen,et al.  Presynaptic Self-Depression at Developing Neocortical Synapses , 2013, Neuron.

[70]  Alison L. Barth,et al.  Initiation, Labile, and Stabilization Phases of Experience-Dependent Plasticity at Neocortical Synapses , 2013, The Journal of Neuroscience.

[71]  A. Kirkwood,et al.  Obligatory Role for the Immediate Early Gene NARP in Critical Period Plasticity , 2013, Neuron.

[72]  Spencer L. Smith,et al.  Synapse-Specific Control of Experience-Dependent Plasticity by Presynaptic NMDA Receptors , 2014, Neuron.

[73]  Benjamin D. Philpot,et al.  Synapse-Specific Control of Experience-Dependent Plasticity by Presynaptic NMDA Receptors , 2014, Neuron.