BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses

In the past 15 years numerous reports provided strong evidence that brain-derived neurotrophic factor (BDNF) is one of the most important modulators of glutamatergic and GABAergic synapses. Remarkable progress regarding localization, kinetics, and molecular mechanisms of BDNF secretion has been achieved, and a large number of studies provided evidence that continuous extracellular supply of BDNF is important for the proper formation and functional maturation of glutamatergic and GABAergic synapses. BDNF can play a permissive role in shaping synaptic networks, making them more susceptible for the occurrence of plastic changes. In addition, BDNF appears to be also an instructive factor for activity-dependent long-term synaptic plasticity. BDNF release just in response to synaptic stimulation might be a molecular trigger to convert high-frequency synaptic activity into long-term synaptic memories. This review attempts to summarize the current knowledge in synaptic secretion and synaptic action of BDNF, including both permissive and instructive effects of BDNF in synaptic plasticity.

[1]  L. Reichardt,et al.  TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum , 2002, Nature Neuroscience.

[2]  C. Bramham,et al.  BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis , 2005, Progress in Neurobiology.

[3]  K. Takimoto,et al.  Ca2+-Induced Deprotonation of Peptide Hormones Inside Secretory Vesicles in Preparation for Release , 1999, The Journal of Neuroscience.

[4]  G. Turrigiano,et al.  Postsynaptic Expression of Homeostatic Plasticity at Neocortical Synapses , 2005, The Journal of Neuroscience.

[5]  Ted Abel,et al.  Recombinant BDNF Rescues Deficits in Basal Synaptic Transmission and Hippocampal LTP in BDNF Knockout Mice , 1996, Neuron.

[6]  K. Svoboda,et al.  Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. , 1999, Science.

[7]  J. Lochner,et al.  Activity-dependent release of tissue plasminogen activator from the dendritic spines of hippocampal neurons revealed by live-cell imaging. , 2006, Journal of neurobiology.

[8]  Jun Yao,et al.  Actin-Dependent Activation of Presynaptic Silent Synapses Contributes to Long-Term Synaptic Plasticity in Developing Hippocampal Neurons , 2006, The Journal of Neuroscience.

[9]  Y. Loh,et al.  A bi-directional carboxypeptidase E-driven transport mechanism controls BDNF vesicle homeostasis in hippocampal neurons , 2008, Molecular and Cellular Neuroscience.

[10]  J. Wuu,et al.  Precursor form of brain‐derived neurotrophic factor and mature brain‐derived neurotrophic factor are decreased in the pre‐clinical stages of Alzheimer's disease , 2005, Journal of neurochemistry.

[11]  S. Rumpel,et al.  Insulin promotes functional induction of silent synapses in differentiating rat neocortical neurons , 2001, The European journal of neuroscience.

[12]  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.

[13]  Tobias Bonhoeffer,et al.  Essential Role for TrkB Receptors in Hippocampus-Mediated Learning , 1999, Neuron.

[14]  S. Moss,et al.  Molecular Brain-Derived Neurotrophic Factor Modulates Fast Synaptic Inhibition by Regulating GABAA Receptor Phosphorylation , Activity , and Cell-Surface Stability , 2004 .

[15]  C. Henneberger,et al.  Brain-derived neurotrophic factor modulates GABAergic synaptic transmission by enhancing presynaptic glutamic acid decarboxylase 65 levels, promoting asynchronous release and reducing the number of activated postsynaptic receptors , 2005, Neuroscience.

[16]  B. Lu,et al.  Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus , 1996, Nature.

[17]  S. McMahon,et al.  Brain-Derived Neurotrophic Factor Is Released in the Dorsal Horn by Distinctive Patterns of Afferent Fiber Stimulation , 2001, The Journal of Neuroscience.

[18]  J. Keifer,et al.  Coordinate action of pre- and postsynaptic brain-derived neurotrophic factor is required for AMPAR trafficking and acquisition of in vitro classical conditioning , 2008, Neuroscience.

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

[20]  F. Lee,et al.  Activation of Trk neurotrophin receptors in the absence of neurotrophins , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  S. Nelson,et al.  BDNF Has Opposite Effects on the Quantal Amplitude of Pyramidal Neuron and Interneuron Excitatory Synapses , 1998, Neuron.

[22]  S. Itohara,et al.  Impaired Cerebellar Development and Function in Mice Lacking CAPS2, a Protein Involved in Neurotrophin Release , 2007, The Journal of Neuroscience.

[23]  A. R. Boxall,et al.  GABAergic mIPSCs in rat cerebellar Purkinje cells are modulated by TrkB and mGluR1‐mediated stimulation of Src , 2000, The Journal of physiology.

[24]  T. Tsumoto,et al.  Brain-derived neurotrophic factor-dependent unmasking of “silent” synapses in the developing mouse barrel cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  C. Bramham,et al.  Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. , 1998, Journal of neurophysiology.

[26]  The action of BDNF on GABA(A) currents changes from potentiating to suppressing during maturation of rat hippocampal CA1 pyramidal neurons. , 2003, The Journal of physiology.

[27]  Arthur Konnerth,et al.  Postsynaptic Induction of BDNF-Mediated Long-Term Potentiation , 2002, Science.

[28]  Guosong Liu,et al.  A Developmental Switch in Neurotransmitter Flux Enhances Synaptic Efficacy by Affecting AMPA Receptor Activation , 2001, Neuron.

[29]  T. Tsumoto,et al.  Brain‐derived neurotrophic factor induces long‐lasting potentiation of synaptic transmission in visual cortex in vivo in young rats, but not in the adult , 2001, The European journal of neuroscience.

[30]  D. G. Herrera,et al.  Sortilin Controls Intracellular Sorting of Brain-Derived Neurotrophic Factor to the Regulated Secretory Pathway , 2005, The Journal of Neuroscience.

[31]  D. Lo,et al.  Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth , 2000, Nature Neuroscience.

[32]  Y. Loh,et al.  Sorting and Activity-Dependent Secretion of BDNF Require Interaction of a Specific Motif with the Sorting Receptor Carboxypeptidase E , 2005, Neuron.

[33]  I. Black,et al.  Blockade of NR2B-containing NMDA receptors prevents BDNF enhancement of glutamatergic transmission in hippocampal neurons. , 1999, Learning & memory.

[34]  A. Leslie Morrow,et al.  GABAA Receptor α1 Subunit Deletion Prevents Developmental Changes of Inhibitory Synaptic Currents in Cerebellar Neurons , 2001, The Journal of Neuroscience.

[35]  I. Black,et al.  Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-D-aspartic acid receptor activity. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Y. Ben-Ari,et al.  ã Federation of European Neuroscience Societies Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus , 2001 .

[37]  Lawrence C. Katz,et al.  Neurotrophins regulate dendritic growth in developing visual cortex , 1995, Neuron.

[38]  H. Atwood,et al.  Silent synapses in neural plasticity: current evidence. , 1999, Learning & memory.

[39]  T. Tsumoto,et al.  Brain-Derived Neurotrophic Factor Enhances Long-Term Potentiation in Rat Visual Cortex , 1997, The Journal of Neuroscience.

[40]  James E. Vaughn,et al.  Review: Fine structure of synaptogenesis in the vertebrate central nervous system , 1989 .

[41]  M. Bear,et al.  Brain-derived neurotrophic factor alters the synaptic modification threshold in visual cortex , 1998, Neuropharmacology.

[42]  V. Staiger,et al.  Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Y. Mizoguchi,et al.  The action of BDNF on GABAA currents changes from potentiating to suppressing during maturation of rat hippocampal CA1 pyramidal neurons , 2003 .

[44]  G. Knott,et al.  Altered Synapse Formation in the Adult Somatosensory Cortex of Brain-Derived Neurotrophic Factor Heterozygote Mice , 2004, The Journal of Neuroscience.

[45]  B. Berninger,et al.  BDNF and NT-3 induce intracellular Ca2+ elevation in hippocampal neurones. , 1993, Neuroreport.

[46]  J. Isaac Postsynaptic silent synapses: evidence and mechanisms , 2003, Neuropharmacology.

[47]  B H Gähwiler,et al.  Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. , 1989, Journal of neurophysiology.

[48]  T. Bonhoeffer,et al.  A caged Ab reveals an immediate/instructive effect of BDNF during hippocampal synaptic potentiation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  C. Henneberger,et al.  Postsynaptic action of BDNF on GABAergic synaptic transmission in the superficial layers of the mouse superior colliculus. , 2002, Journal of neurophysiology.

[50]  L. Maffei,et al.  Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D. Kunze,et al.  Brain-Derived Neurotrophic Factor Acutely Inhibits AMPA-Mediated Currents in Developing Sensory Relay Neurons , 2000, The Journal of Neuroscience.

[52]  E. Schuman,et al.  Neurotrophins and Time: Different Roles for TrkB Signaling in Hippocampal Long-Term Potentiation , 1997, Neuron.

[53]  B. Frey,et al.  Brain-derived neurotrophic factor and neuroplasticity in bipolar disorder , 2008, Expert review of neurotherapeutics.

[54]  D. Smith,et al.  Deficient long-term memory and long-lasting long-term potentiation in mice with a targeted deletion of neurotrophin-4 gene. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[55]  V. Lessmann,et al.  Mechanisms, locations, and kinetics of synaptic BDNF secretion: An update , 2009, Neuroscience Research.

[56]  C. Altar,et al.  Neurotrophin trafficking by anterograde transport , 1998, Trends in Neurosciences.

[57]  Berta Alsina,et al.  Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF , 2001, Nature Neuroscience.

[58]  T. Mittmann,et al.  Reduced presynaptic efficiency of excitatory synaptic transmission impairs LTP in the visual cortex of BDNF‐heterozygous mice , 2006, The European journal of neuroscience.

[59]  W. Tyler,et al.  BDNF Enhances Quantal Neurotransmitter Release and Increases the Number of Docked Vesicles at the Active Zones of Hippocampal Excitatory Synapses , 2001, The Journal of Neuroscience.

[60]  B. Gähwiler,et al.  Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. , 1989, Journal of neurophysiology.

[61]  Steven A. Siegelbaum,et al.  Visualization of changes in presynaptic function during long-term synaptic plasticity , 2001, Nature Neuroscience.

[62]  R. Nicoll,et al.  Expression mechanisms underlying long-term potentiation: a postsynaptic view. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  E. Kandel,et al.  Some Forms of cAMP-Mediated Long-Lasting Potentiation Are Associated with Release of BDNF and Nuclear Translocation of Phospho-MAP Kinase , 2001, Neuron.

[64]  Y. Ishikawa,et al.  Biological characterization and optical imaging of brain‐derived neurotrophic factor‐green fluorescent protein suggest an activity‐dependent local release of brain‐derived neurotrophic factor in neurites of cultured hippocampal neurons , 2001, Journal of neuroscience research.

[65]  T. Bliss,et al.  Brain-Derived Neurotrophic Factor Induces Long-Term Potentiation in Intact Adult Hippocampus: Requirement for ERK Activation Coupled to CREB and Upregulation of Arc Synthesis , 2002, The Journal of Neuroscience.

[66]  M Sur,et al.  Short-term synaptic plasticity in the visual cortex during development. , 1996, Cerebral cortex.

[67]  H. Federoff,et al.  Proteolytic processing of proNGF is necessary for mature NGF regulated secretion from neurons. , 2007, Biochemical and biophysical research communications.

[68]  J. Lisman Long-term potentiation: outstanding questions and attempted synthesis. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[69]  Paresh D Patel,et al.  Variant Brain-Derived Neurotrophic Factor (BDNF) (Met66) Alters the Intracellular Trafficking and Activity-Dependent Secretion of Wild-Type BDNF in Neurosecretory Cells and Cortical Neurons , 2004, The Journal of Neuroscience.

[70]  Teiichi Furuichi,et al.  The Secretory Granule-Associated Protein CAPS2 Regulates Neurotrophin Release and Cell Survival , 2004, The Journal of Neuroscience.

[71]  S. Rumpel,et al.  Silent synapses in the immature visual cortex: layer-specific developmental regulation. , 2004, Journal of neurophysiology.

[72]  M. Lynch,et al.  BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events , 2004, Neurobiology of Aging.

[73]  M. Amaral,et al.  TRPC3 Channels Are Necessary for Brain-Derived Neurotrophic Factor to Activate a Nonselective Cationic Current and to Induce Dendritic Spine Formation , 2007, The Journal of Neuroscience.

[74]  M. Poo,et al.  Spike Timing-Dependent LTP/LTD Mediates Visual Experience-Dependent Plasticity in a Developing Retinotectal System , 2006, Neuron.

[75]  J. Kapur,et al.  Synaptic and extrasynaptic localization of brain‐derived neurotrophic factor and the tyrosine kinase B receptor in cultured hippocampal neurons , 2004, The Journal of comparative neurology.

[76]  T. Tsumoto,et al.  Difference in trafficking of brain-derived neurotrophic factor between axons and dendrites of cortical neurons, revealed by live-cell imaging , 2005, BMC Neuroscience.

[77]  Scooter D. Johnson,et al.  Mechanisms of Transport and Exocytosis of Dense-Core Granules Containing Tissue Plasminogen Activator in Developing Hippocampal Neurons , 2005, The Journal of Neuroscience.

[78]  B. Michalski,et al.  The Precursor Pro-Nerve Growth Factor Is the Predominant Form of Nerve Growth Factor in Brain and Is Increased in Alzheimer's Disease , 2001, Molecular and Cellular Neuroscience.

[79]  P. Greengard,et al.  Synapsins as mediators of BDNF-enhanced neurotransmitter release , 2000, Nature Neuroscience.

[80]  Enrico Cherubini,et al.  ‘Deaf, mute and whispering’ silent synapses: their role in synaptic plasticity , 2004, The Journal of physiology.

[81]  E. Kandel,et al.  Presynaptic BDNF Required for a Presynaptic but Not Postsynaptic Component of LTP at Hippocampal CA1-CA3 Synapses , 2003, Neuron.

[82]  T. Mittmann,et al.  Impaired GABAergic inhibition in the visual cortex of brain‐derived neurotrophic factor heterozygous knockout mice , 2008, The Journal of physiology.

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

[84]  M. Poo,et al.  Brain-Derived Neurotrophic Factor Modulation of GABAergic Synapses by Postsynaptic Regulation of Chloride Transport , 2003, The Journal of Neuroscience.

[85]  V. Murthy,et al.  Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons , 2002, Nature.

[86]  D. Katz,et al.  Activity-Dependent Release of Endogenous Brain-Derived Neurotrophic Factor from Primary Sensory Neurons Detected by ELISAIn Situ , 2000, The Journal of Neuroscience.

[87]  B. Holtmann,et al.  Truncated TrkB receptor-induced outgrowth of dendritic filopodia involves the p75 neurotrophin receptor , 2004, Journal of Cell Science.

[88]  E. Cattaneo,et al.  Brain-derived neurotrophic factor in neurodegenerative diseases , 2009, Nature Reviews Neurology.

[89]  B. Lu,et al.  Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. , 1999, Learning & memory.

[90]  T Bonhoeffer,et al.  Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Sacha B. Nelson,et al.  Postsynaptic Depolarization Scales Quantal Amplitude in Cortical Pyramidal Neurons , 2001, The Journal of Neuroscience.

[92]  Noam E. Ziv,et al.  Synapse development: still looking for the forest, still lost in the trees , 2006, Cell and Tissue Research.

[93]  M. Chao,et al.  A role for Fyn in Trk receptor transactivation by G-protein-coupled receptor signaling , 2006, Molecular and Cellular Neuroscience.

[94]  R. Heumann,et al.  BDNF, and NT‐4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones , 1994, Neuroreport.

[95]  H. Thoenen,et al.  Are there differences between the secretion characteristics of NGF and BDNF? Implications for the modulatory role of neurotrophins in activity‐dependent neuronal plasticity , 1999, Microscopy research and technique.

[96]  Y. Ben-Ari,et al.  Endogenous Neurotrophins Are Required for the Induction of GABAergic Long-Term Potentiation in the Neonatal Rat Hippocampus , 2005, The Journal of Neuroscience.

[97]  P. Rorsman,et al.  Delay between Fusion Pore Opening and Peptide Release from Large Dense-Core Vesicles in Neuroendocrine Cells , 2002, Neuron.

[98]  Y. Barde,et al.  Physiology of the neurotrophins. , 1996, Annual review of neuroscience.

[99]  Hyejin Kang,et al.  A role for BDNF in the late-phase of hippocampal long-term potentiation , 1998, Neuropharmacology.

[100]  T. Bonhoeffer,et al.  Mechanism of TrkB-Mediated Hippocampal Long-Term Potentiation , 2002, Neuron.

[101]  J. McNamara,et al.  Localization of Brain-Derived Neurotrophic Factor to Distinct Terminals of Mossy Fiber Axons Implies Regulation of Both Excitation and Feedforward Inhibition of CA3 Pyramidal Cells , 2004, The Journal of Neuroscience.

[102]  Barbara L. Hempstead,et al.  Regulation of Cell Survival by Secreted Proneurotrophins , 2001, Science.

[103]  Mu-ming Poo,et al.  Postsynaptic Target Specificity of Neurotrophin-Induced Presynaptic Potentiation , 2000, Neuron.

[104]  E. Schuman,et al.  A Requirement for Local Protein Synthesis in Neurotrophin-Induced Hippocampal Synaptic Plasticity , 1996, Science.

[105]  A. Cattaneo,et al.  Trk B signalling controls LTP but not LTD expression in the developing rat visual cortex , 2000, The European journal of neuroscience.

[106]  C. Bramham Local protein synthesis, actin dynamics, and LTP consolidation , 2008, Current Opinion in Neurobiology.

[107]  Petti T. Pang,et al.  Cleavage of proBDNF by tPA/Plasmin Is Essential for Long-Term Hippocampal Plasticity , 2004, Science.

[108]  V. Lessmann Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. , 1998, General pharmacology.

[109]  T. Bonhoeffer,et al.  Hippocampal Long-Term Potentiation Is Supported by Presynaptic and Postsynaptic Tyrosine Receptor Kinase B-Mediated Phospholipase Cγ Signaling , 2006, The Journal of Neuroscience.

[110]  Girstaute Dagyte,et al.  Sustained Arc/Arg3.1 Synthesis Controls Long-Term Potentiation Consolidation through Regulation of Local Actin Polymerization in the Dentate Gyrus In Vivo , 2007, The Journal of Neuroscience.

[111]  T. Tsumoto,et al.  Activity-Dependent Transfer of Brain-Derived Neurotrophic Factor to Postsynaptic Neurons , 2001, Science.

[112]  Shigetada Nakanishi,et al.  Membrane potential‐regulated Ca2+ signalling in development and maturation of mammalian cerebellar granule cells , 2006, The Journal of physiology.

[113]  T. Marissal,et al.  Spontaneous glutamatergic activity induces a BDNF‐dependent potentiation of GABAergic synapses in the newborn rat hippocampus , 2008, The Journal of physiology.

[114]  H. G. Kim,et al.  Neurotrophin 3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[115]  Eric C. Griffith,et al.  Brain-Specific Phosphorylation of MeCP2 Regulates Activity-Dependent Bdnf Transcription, Dendritic Growth, and Spine Maturation , 2006, Neuron.

[116]  C. V. von Bartheld Axonal transport and neuronal transcytosis of trophic factors, tracers, and pathogens. , 2004, Journal of neurobiology.

[117]  V. Lessmann,et al.  A common thread for pain and memory synapses? Brain-derived neurotrophic factor and trkB receptors. , 2003, Trends in pharmacological sciences.

[118]  C. Bramham,et al.  Brain-Derived Neurotrophic Factor Triggers Transcription-Dependent, Late Phase Long-Term Potentiation In Vivo , 2002, The Journal of Neuroscience.

[119]  Bai Lu,et al.  Activation of p75NTR by proBDNF facilitates hippocampal long-term depression , 2005, Nature Neuroscience.

[120]  William J Tyler,et al.  Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones , 2003, The Journal of physiology.

[121]  W. Betz,et al.  Monitoring synaptic vesicle recycling in frog motor nerve terminals with FM dyes , 2003, Journal of neurocytology.

[122]  J. Meier,et al.  Altered Balance of Glutamatergic/GABAergic Synaptic Input and Associated Changes in Dendrite Morphology after BDNF Expression in BDNF-Deficient Hippocampal Neurons , 2006, The Journal of Neuroscience.

[123]  M Segal,et al.  Neurotrophins Induce Formation of Functional Excitatory and Inhibitory Synapses between Cultured Hippocampal Neurons , 1998, The Journal of Neuroscience.

[124]  J. McNamara,et al.  Zinc-Mediated Transactivation of TrkB Potentiates the Hippocampal Mossy Fiber-CA3 Pyramid Synapse , 2008, Neuron.

[125]  L. Buée,et al.  Neurotrophic factors in Alzheimer’s disease: role of axonal transport , 2008, Genes, brain, and behavior.

[126]  J. Gaiarsa,et al.  Backpropagating Action Potentials Trigger Dendritic Release of BDNF during Spontaneous Network Activity , 2008, The Journal of Neuroscience.

[127]  Volkmar Lessmann,et al.  Neurotrophin secretion: current facts and future prospects , 2003, Progress in Neurobiology.

[128]  N. Seidah,et al.  Biosynthesis and Post-translational Processing of the Precursor to Brain-derived Neurotrophic Factor* , 2001, The Journal of Biological Chemistry.

[129]  T. Bonhoeffer,et al.  Endogenous Brain-Derived Neurotrophic Factor Triggers Fast Calcium Transients at Synapses in Developing Dendrites , 2007, The Journal of Neuroscience.

[130]  R. Tsien,et al.  Frequency-Dependent Kinetics and Prevalence of Kiss-and-Run and Reuse at Hippocampal Synapses Studied with Novel Quenching Methods , 2006, Neuron.

[131]  R. Mohrmann,et al.  Target-Specific Factors Regulate the Formation of Glutamatergic Transmitter Release Sites in Cultured Neocortical Neurons , 1999, The Journal of Neuroscience.

[132]  K. Gottmann,et al.  NT-3 regulates BDNF-induced modulation of synaptic transmission in cultured hippocampal neurons , 2001, Neuroreport.

[133]  I. Black,et al.  Rab3A Is Required for Brain-Derived Neurotrophic Factor-Induced Synaptic Plasticity: Transcriptional Analysis at the Population and Single-Cell Levels , 2001, The Journal of Neuroscience.

[134]  P. Scheiffele Cell-cell signaling during synapse formation in the CNS. , 2003, Annual review of neuroscience.

[135]  H. Thoenen Neurotrophins and Neuronal Plasticity , 1995, Science.

[136]  M. Vasko,et al.  Mechanisms of the Release of Anterogradely Transported Neurotrophin-3 from Axon Terminals , 2002, The Journal of Neuroscience.

[137]  E. Schuman,et al.  Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus , 1995, Science.

[138]  Michael J Higley,et al.  Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons , 2008, The Journal of physiology.

[139]  J. Lübke,et al.  Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal–Retzius Cells in the Developing Rat Neocortex , 2002, The Journal of Neuroscience.

[140]  L. Maffei,et al.  BDNF Regulates the Maturation of Inhibition and the Critical Period of Plasticity in Mouse Visual Cortex , 1999, Cell.

[141]  J. E. Vaughn,et al.  Fine structure of synaptogenesis in the vertebrate central nervous system. , 1989, Synapse.

[142]  P. Pavlidis,et al.  Pair Recordings Reveal All-Silent Synaptic Connections and the Postsynaptic Expression of Long-Term Potentiation , 2001, Neuron.

[143]  K. Gottmann,et al.  Presynaptic plasticity in an immature neocortical network requires NMDA receptor activation and BDNF release. , 2006, Journal of neurophysiology.

[144]  R. Teasdale,et al.  Intracellular sorting and transport of proteins. , 2003, Progress in biophysics and molecular biology.

[145]  E. Shooter,et al.  The Regulated Secretion and Vectorial Targeting of Neurotrophins in Neuroendocrine and Epithelial Cells* , 1996, The Journal of Biological Chemistry.

[146]  K. Gottmann,et al.  Activity- and BDNF-induced plasticity of miniature synaptic currents in ES cell-derived neurons integrated in a neocortical network. , 2005, Journal of neurophysiology.

[147]  Yildirim Sara,et al.  Development of Vesicle Pools during Maturation of Hippocampal Synapses , 2002, The Journal of Neuroscience.

[148]  B. Luikart,et al.  TrkB Has a Cell-Autonomous Role in the Establishment of Hippocampal Schaffer Collateral Synapses , 2005, The Journal of Neuroscience.

[149]  W. Huttner,et al.  Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network , 1991, The Journal of cell biology.

[150]  Rafael Yuste,et al.  BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2 , 2003, Development.

[151]  R. Heumann,et al.  Modulation of unitary glutamatergic synapses by neurotrophin-4/5 or brain-derived neurotrophic factor in hippocampal microcultures: presynaptic enhancement depends on pre-established paired-pulse facilitation , 1998, Neuroscience.

[152]  M. Poo,et al.  Retrograde signaling at central synapses , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[153]  A. Konnerth,et al.  Neurotrophin-evoked rapid excitation through TrkB receptors , 1999, Nature.

[154]  T. Tsumoto,et al.  Long-Term Depression Is Not Induced by Low-Frequency Stimulation in Rat Visual Cortex In Vivo: A Possible Preventing Role of Endogenous Brain-Derived Neurotrophic Factor , 2003, The Journal of Neuroscience.

[155]  R. Jaenisch,et al.  Knocking the NT4 gene into the BDNF locus rescues BDNF deficient mice and reveals distinct NT4 and BDNF activities , 2000, Nature Neuroscience.

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

[157]  C. Montell,et al.  Activation of a TRPC3-Dependent Cation Current through the Neurotrophin BDNF , 1999, Neuron.

[158]  Laurent Groc,et al.  AMPA signalling in nascent glutamatergic synapses: there and not there! , 2006, Trends in Neurosciences.

[159]  Y. Ben-Ari Excitatory actions of gaba during development: the nature of the nurture , 2002, Nature Reviews Neuroscience.

[160]  Barbara L. Hempstead,et al.  Sortilin is essential for proNGF-induced neuronal cell death , 2004, Nature.

[161]  Michael C. Crair,et al.  Silent Synapses during Development of Thalamocortical Inputs , 1997, Neuron.

[162]  M. Yamada,et al.  Brain-Derived Neurotrophic Factor Promotes the Maturation of GABAergic Mechanisms in Cultured Hippocampal Neurons , 2002, The Journal of Neuroscience.

[163]  F. Lee,et al.  Distinctive features of Trk neurotrophin receptor transactivation by G protein-coupled receptors. , 2002, Cytokine & growth factor reviews.

[164]  T Bonhoeffer,et al.  Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[165]  A. Konnerth,et al.  Neurotrophin-evoked depolarization requires the sodium channel NaV1.9 , 2002, Nature.

[166]  R. Heumann,et al.  Synaptic secretion of BDNF after high‐frequency stimulation of glutamatergic synapses , 2001, The EMBO journal.

[167]  S. Gasparini,et al.  Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[168]  Y. Umezawa,et al.  Cell-based fluorescent indicator to visualize brain-derived neurotrophic factor secreted from living neurons. , 2008, ACS chemical biology.

[169]  P. Stanton,et al.  BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses , 2006, The Journal of physiology.

[170]  T. Tsumoto,et al.  Brain-derived neurotrophic factor increases inhibitory synapses, revealed in solitary neurons cultured from rat visual cortex , 2004, Neuroscience.

[171]  C. Gravel,et al.  BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain , 2005, Nature.

[172]  J. Benson,et al.  BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABAA receptor surface expression , 2001, The European journal of neuroscience.

[173]  N. Woo,et al.  Distinct Role of Long 3′ UTR BDNF mRNA in Spine Morphology and Synaptic Plasticity in Hippocampal Neurons , 2008, Cell.

[174]  Ana Luísa Carvalho,et al.  BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons , 2007, Molecular and Cellular Neuroscience.

[175]  M. Silhol,et al.  New insights into brain BDNF function in normal aging and Alzheimer disease , 2008, Brain Research Reviews.

[176]  O. Lindvall,et al.  Increased synaptic inhibition in dentate gyrus of mice with reduced levels of endogenous brain-derived neurotrophic factor , 2000, Neuroscience.

[177]  M. Sanderson,et al.  Inhibition of regulated catecholamine secretion from PC12 cells by the Ca2+/calmodulin kinase II inhibitor KN-62. , 1995, Journal of cell science.

[178]  D. Katz,et al.  Cellular Mechanisms Regulating Activity-Dependent Release of Native Brain-Derived Neurotrophic Factor from Hippocampal Neurons , 2002, The Journal of Neuroscience.

[179]  J. Meier,et al.  GluR‐ and TrkB‐mediated maturation of GABAA receptor function during the period of eye opening , 2005, The European journal of neuroscience.

[180]  Y. Mizoguchi,et al.  A Rapid Increase in the Total Number of Cell Surface Functional GABAA Receptors Induced by Brain-derived Neurotrophic Factor in Rat Visual Cortex* , 2003, Journal of Biological Chemistry.

[181]  W. Betz,et al.  Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytic events , 1999, Nature Neuroscience.

[182]  T. Tsumoto,et al.  Brain-derived neurotrophic factor blocks long-term depression in rat visual cortex. , 1996, Journal of neurophysiology.

[183]  T. Tsumoto,et al.  A Local Reduction in Cortical GABAergic Synapses after a Loss of Endogenous Brain-Derived Neurotrophic Factor, as Revealed by Single-Cell Gene Knock-Out Method , 2007, The Journal of Neuroscience.

[184]  M. Poo,et al.  Synaptic reliability correlates with reduced susceptibility to synaptic potentiation by brain-derived neurotrophic factor. , 1999, Learning & memory.

[185]  S. Rumpel,et al.  Silent Synapses in the Developing Rat Visual Cortex: Evidence for Postsynaptic Expression of Synaptic Plasticity , 1998, The Journal of Neuroscience.

[186]  F. Lee,et al.  Single-Cell Characterization of Retrograde Signaling by Brain-Derived Neurotrophic Factor , 2006, The Journal of Neuroscience.

[187]  Y. Ben-Ari,et al.  Long‐term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus , 1999, The Journal of physiology.

[188]  P. Worley,et al.  The Immediate Early Gene Arc/Arg3.1: Regulation, Mechanisms, and Function , 2008, The Journal of Neuroscience.

[189]  A. Nikolakopoulou,et al.  BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo , 2005, Development.

[190]  T. Tsumoto,et al.  Brain‐derived neurotrophic factor blocks long‐term depression in solitary neurones cultured from rat visual cortex , 2000, Journal of Physiology.

[191]  Ning Li,et al.  Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor , 2005, Nature.

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

[193]  D. Lo,et al.  Brain-Derived Neurotrophic Factor Differentially Regulates Excitatory and Inhibitory Synaptic Transmission in Hippocampal Cultures , 2000, The Journal of Neuroscience.

[194]  A. Konnerth,et al.  Long-term potentiation and functional synapse induction in developing hippocampus , 1996, Nature.

[195]  Tobias Bonhoeffer,et al.  A Role for Local Calcium Signaling in Rapid Synaptic Partner Selection by Dendritic Filopodia , 2008, Neuron.

[196]  Mu-ming Poo,et al.  Neurotrophins as synaptic modulators , 2001, Nature Reviews Neuroscience.

[197]  Eric C. Griffith,et al.  Derepression of BDNF Transcription Involves Calcium-Dependent Phosphorylation of MeCP2 , 2003, Science.

[198]  C. Duarte,et al.  Role of the brain‐derived neurotrophic factor at glutamatergic synapses , 2008, British journal of pharmacology.

[199]  M. Constantine‐Paton,et al.  BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation , 2007, Nature Neuroscience.

[200]  B. Smith,et al.  Activity‐Dependent Recruitment of Silent Synapses a , 1991, Annals of the New York Academy of Sciences.

[201]  J. Conner,et al.  Distribution of Brain-Derived Neurotrophic Factor (BDNF) Protein and mRNA in the Normal Adult Rat CNS: Evidence for Anterograde Axonal Transport , 1997, The Journal of Neuroscience.

[202]  G. Carmignoto,et al.  Brain‐derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex. , 1997, The Journal of physiology.

[203]  J. Pavelić,et al.  Rett Syndrome: From the Gene to the Disease , 2008, European Neurology.

[204]  Yves-Alain Barde,et al.  Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF , 2008, Nature Neuroscience.

[205]  T. Bonhoeffer,et al.  Relative Contribution of Endogenous Neurotrophins in Hippocampal Long-Term Potentiation , 1999, The Journal of Neuroscience.

[206]  Josep M. Canals,et al.  Mutant huntingtin Impairs the Post-Golgi Trafficking of Brain-Derived Neurotrophic Factor But Not Its Val66Met Polymorphism , 2006, The Journal of Neuroscience.

[207]  E. Carbone,et al.  Brain-Derived Neurotrophic Factor Enhances GABA Release Probability and Nonuniform Distribution of N- and P/Q-Type Channels on Release Sites of Hippocampal Inhibitory Synapses , 2005, The Journal of Neuroscience.

[208]  S. Barati,et al.  Distribution and localization of pro‐brain‐derived neurotrophic factor‐like immunoreactivity in the peripheral and central nervous system of the adult rat , 2004, Journal of neurochemistry.

[209]  Alan Morgan,et al.  Secretory granule exocytosis. , 2003, Physiological reviews.

[210]  Tanja Brigadski,et al.  Postsynaptic Secretion of BDNF and NT-3 from Hippocampal Neurons Depends on Calcium–Calmodulin Kinase II Signaling and Proceeds via Delayed Fusion Pore Opening , 2007, The Journal of Neuroscience.

[211]  D. Katz,et al.  Breathing dysfunction in Rett syndrome: Understanding epigenetic regulation of the respiratory network , 2008, Respiratory Physiology & Neurobiology.

[212]  Barbara L. Hempstead,et al.  ProBDNF Induces Neuronal Apoptosis via Activation of a Receptor Complex of p75NTR and Sortilin , 2005, The Journal of Neuroscience.

[213]  N. Matsuki,et al.  Inhibition of GABAA Synaptic Responses by Brain-Derived Neurotrophic Factor (BDNF) in Rat Hippocampus , 1997, The Journal of Neuroscience.

[214]  S. Furukawa,et al.  Pro-region of neurotrophins determines the processing efficiency. , 2007, Biochemical and biophysical research communications.

[215]  R. Heumann,et al.  BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. , 1998, Journal of cell science.

[216]  R. Mohrmann,et al.  Developmental maturation of synaptic vesicle cycling as a distinctive feature of central glutamatergic synapses , 2003, Neuroscience.

[217]  E. Shooter,et al.  Nerve growth factor, brain‐derived neurotrophic factor, and neurotrophin‐3 are sorted to dense‐core vesicles and released via the regulated pathway in primary rat cortical neurons , 2004, Journal of neuroscience research.

[218]  H. Thoenen,et al.  Characterization of Nerve Growth Factor (NGF) Release from Hippocampal Neurons: Evidence for a Constitutive and an Unconventional Sodium‐dependent Regulated Pathway , 1995, The European journal of neuroscience.

[219]  K. Kaila,et al.  Ionic basis of GABAA receptor channel function in the nervous system , 1994, Progress in Neurobiology.

[220]  E. Castrén,et al.  Targeting TrkB neurotrophin receptor to treat depression. , 2008, Expert opinion on therapeutic targets.

[221]  A. Draguhn,et al.  Different mechanisms regulate IPSC kinetics in early postnatal and juvenile hippocampal granule cells. , 1996, Journal of neurophysiology.

[222]  Michael E. Greenberg,et al.  A brain-specific microRNA regulates dendritic spine development , 2006, Nature.

[223]  C. A. Frank,et al.  Mechanisms Underlying the Rapid Induction and Sustained Expression of Synaptic Homeostasis , 2006, Neuron.

[224]  N. Seidah,et al.  Neurotrophin-3 Sorts to the Constitutive Secretory Pathway of Hippocampal Neurons and Is Diverted to the Regulated Secretory Pathway by Coexpression with Brain-Derived Neurotrophic Factor , 2000, The Journal of Neuroscience.

[225]  C. Sotelo,et al.  Neuronal Activity and Brain-Derived Neurotrophic Factor Regulate the Density of Inhibitory Synapses in Organotypic Slice Cultures of Postnatal Hippocampus , 2000, The Journal of Neuroscience.

[226]  P. Halban,et al.  Sorting and processing of secretory proteins. , 1994, The Biochemical journal.

[227]  T. Bonhoeffer,et al.  The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[228]  D. Faber,et al.  Silent Synaptic Connections and Their Modifiability a , 1991, Annals of the New York Academy of Sciences.

[229]  H. Scharfman Hyperexcitability in combined entorhinal/hippocampal slices of adult rat after exposure to brain-derived neurotrophic factor. , 1997, Journal of neurophysiology.

[230]  Naiphinich Kotchabhakdi,et al.  Developmental Changes of Inhibitory Synaptic Currents in Cerebellar Granule Neurons: Role of GABAA Receptor α6 Subunit , 1996, The Journal of Neuroscience.

[231]  R. Wenthold,et al.  Neurotrophins act at presynaptic terminals to activate synapses among cultured hippocampal neurons , 2001, The European journal of neuroscience.

[232]  M. Amaral,et al.  BDNF induces calcium elevations associated with IBDNF, a nonselective cationic current mediated by TRPC channels. , 2007, Journal of neurophysiology.

[233]  W Wisden,et al.  The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[234]  T. Tsumoto,et al.  Brain‐derived neurotrophic factor acutely depresses excitatory synaptic transmission to GABAergic neurons in visual cortical slices , 2004, European Journal of Neuroscience.

[235]  Smith Ma,et al.  Anterograde transport of endogenous brain-derived neurotrophic factor in hippocampal mossy fibers. , 1997 .

[236]  H. Lester,et al.  Enhancement of Neurotransmitter Release Induced by Brain-Derived Neurotrophic Factor in Cultured Hippocampal Neurons , 1998, The Journal of Neuroscience.

[237]  R. Nicoll,et al.  The Role of Brain-Derived Neurotrophic Factor Receptors in the Mature Hippocampus: Modulation of Long-Term Potentiation through a Presynaptic Mechanism involving TrkB , 2000, The Journal of Neuroscience.

[238]  Menahem Segal,et al.  Role of neurotrophins in central synapse formation and stabilization , 2002, Nature Reviews Neuroscience.

[239]  Haruo Kasai,et al.  Comparative biology of Ca2+-dependent exocytosis: implications of kinetic diversity for secretory function , 1999, Trends in Neurosciences.

[240]  J. Barker,et al.  Differential and transient expression of GABAA receptor alpha-subunit mRNAs in the developing rat CNS , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[241]  W. Ren,et al.  BDNF induces late-phase LTP of C-fiber evoked field potentials in rat spinal dorsal horn , 2008, Experimental Neurology.

[242]  E. Cherubini,et al.  Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3–CA1 connections in the hippocampus , 2007, Proceedings of the National Academy of Sciences.

[243]  K. Christian,et al.  BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? , 2008, Neurobiology of Learning and Memory.

[244]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[245]  J. Voipio,et al.  BDNF-induced TrkB activation down-regulates the K+–Cl− cotransporter KCC2 and impairs neuronal Cl− extrusion , 2002, The Journal of cell biology.

[246]  M. Bergami,et al.  Hippocampal neurons recycle BDNF for activity‐dependent secretion and LTP maintenance , 2006, The EMBO journal.

[247]  E. Carbone,et al.  BDNF up‐regulates evoked GABAergic transmission in developing hippocampus by potentiating presynaptic N‐ and P/Q‐type Ca2+ channels signalling , 2002, The European journal of neuroscience.

[248]  V. Lessmann,et al.  Imaging of evoked dense-core-vesicle exocytosis in hippocampal neurons reveals long latencies and kiss-and-run fusion events , 2009, Journal of Cell Science.

[249]  Rafal Butowt,et al.  Anterograde axonal transport, transcytosis, and recycling of neurotrophic factors , 2001, Molecular Neurobiology.

[250]  L. Zhang,et al.  Impairments in High-Frequency Transmission, Synaptic Vesicle Docking, and Synaptic Protein Distribution in the Hippocampus of BDNF Knockout Mice , 1999, The Journal of Neuroscience.

[251]  Lawrence C. Katz,et al.  Opposing Roles for Endogenous BDNF and NT-3 in Regulating Cortical Dendritic Growth , 1997, Neuron.

[252]  O. Garaschuk,et al.  Large-scale oscillatory calcium waves in the immature cortex , 2000, Nature Neuroscience.

[253]  V. Lessmann,et al.  Differential Vesicular Targeting and Time Course of Synaptic Secretion of the Mammalian Neurotrophins , 2005, The Journal of Neuroscience.

[254]  M. Yamada,et al.  BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. , 2004, Cerebral cortex.

[255]  I. Black,et al.  Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[256]  C. V. Melo,et al.  Brain-derived Neurotrophic Factor Regulates the Expression and Synaptic Delivery ofα-Amino-3-hydroxy-5-methyl-4-isoxazole Propionic Acid Receptor Subunits in Hippocampal Neurons* , 2007, Journal of Biological Chemistry.

[257]  L. Maffei,et al.  Heterozygous Knock-Out Mice for Brain-Derived Neurotrophic Factor Show a Pathway-Specific Impairment of Long-Term Potentiation But Normal Critical Period for Monocular Deprivation , 2002, The Journal of Neuroscience.

[258]  Hiroki Toyoda,et al.  Cl− uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1 , 2004, The Journal of physiology.

[259]  L. Olson,et al.  Brain-derived neurotrophic factor: subcellular compartmentalization and interneuronal transfer as visualized with anti-peptide antibodies. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[260]  B. Gustafsson,et al.  Creation of AMPA-silent synapses in the neonatal hippocampus , 2004, Nature Neuroscience.

[261]  Daisuke Hattori,et al.  DNA Methylation-Related Chromatin Remodeling in Activity-Dependent Bdnf Gene Regulation , 2003, Science.

[262]  R. Balice-Gordon,et al.  Postsynaptic TrkB-Mediated Signaling Modulates Excitatory and Inhibitory Neurotransmitter Receptor Clustering at Hippocampal Synapses , 2004, The Journal of Neuroscience.

[263]  G. Martens,et al.  Cell-Autonomous TrkB Signaling in Presynaptic Retinal Ganglion Cells Mediates Axon Arbor Growth and Synapse Maturation during the Establishment of Retinotectal Synaptic Connectivity , 2007, The Journal of Neuroscience.

[264]  M. Klau,et al.  Reduced number of functional glutamatergic synapses in hippocampal neurons overexpressing full‐length TrkB receptors , 2001, Journal of neuroscience research.

[265]  Nancy Y. Ip,et al.  Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF , 1993, Nature.

[266]  G. Westbrook,et al.  Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse , 2001, Nature.

[267]  M. Egan,et al.  The BDNF val66met Polymorphism Affects Activity-Dependent Secretion of BDNF and Human Memory and Hippocampal Function , 2003, Cell.

[268]  R. Nicoll,et al.  Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. , 1998, Journal of neurophysiology.

[269]  K. Gottmann Transsynaptic modulation of the synaptic vesicle cycle by cell‐adhesion molecules , 2008, Journal of neuroscience research.

[270]  Q. Yan,et al.  Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system , 1997, Neuroscience.

[271]  G G Turrigiano,et al.  Brain-Derived Neurotrophic Factor Mediates the Activity-Dependent Regulation of Inhibition in Neocortical Cultures , 1997, The Journal of Neuroscience.

[272]  S. Duan,et al.  Activity-Induced Rapid Synaptic Maturation Mediated by Presynaptic Cdc42 Signaling , 2006, Neuron.

[273]  Jian Zhou,et al.  TRPC channels promote cerebellar granule neuron survival , 2007, Nature Neuroscience.

[274]  Wade Morishita,et al.  Generation of Silent Synapses by Acute In Vivo Expression of CaMKIV and CREB , 2005, Neuron.

[275]  E. Cattaneo,et al.  Role of brain-derived neurotrophic factor in Huntington's disease , 2007, Progress in Neurobiology.

[276]  J. Keifer,et al.  BDNF-induced synaptic delivery of AMPAR subunits is differentially dependent on NMDA receptors and requires ERK , 2009, Neurobiology of Learning and Memory.

[277]  J. Weis,et al.  The secreted brain‐derived neurotrophic factor precursor pro‐BDNF binds to TrkB and p75NTR but not to TrkA or TrkC , 2005, Journal of neuroscience research.

[278]  Spartaco Santi,et al.  Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[279]  E. Tongiorgi Activity-dependent expression of brain-derived neurotrophic factor in dendrites: Facts and open questions , 2008, Neuroscience Research.

[280]  B. Lu,et al.  Presynaptic Modulation of Synaptic Transmission and Plasticity by Brain-Derived Neurotrophic Factor in the Developing Hippocampus , 1998, The Journal of Neuroscience.

[281]  T. Voigt,et al.  Activation of Early Silent Synapses by Spontaneous Synchronous Network Activity Limits the Range of Neocortical Connections , 2005, The Journal of Neuroscience.

[282]  L. Olson,et al.  Regulation of brain-derived neurotrophic factor (BDNF) expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[283]  C. Siao,et al.  Neuronal release of proBDNF , 2009, Nature Neuroscience.

[284]  J. A. Payne,et al.  Mechanism of Activity-Dependent Downregulation of the Neuron-Specific K-Cl Cotransporter KCC2 , 2004, The Journal of Neuroscience.

[285]  Jyh-Jang Sun,et al.  Activity-dependent regulation of neuronal apoptosis in neonatal mouse cerebral cortex. , 2008, Cerebral cortex.

[286]  L. C. Katz,et al.  BDNF release from single cells elicits local dendritic growth in nearby neurons , 2002, Nature Neuroscience.

[287]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[288]  O. Arancio,et al.  BDNF-mediated neurotransmission relies upon a myosin VI motor complex , 2006, Nature Neuroscience.

[289]  Fabrice P Cordelières,et al.  Huntingtin Controls Neurotrophic Support and Survival of Neurons by Enhancing BDNF Vesicular Transport along Microtubules , 2004, Cell.