Shaping inhibition: activity dependent structural plasticity of GABAergic synapses

Inhibitory transmission through the neurotransmitter γ-aminobutyric acid (GABA) shapes network activity in the mammalian cerebral cortex by filtering synaptic incoming information and dictating the activity of principal cells. The incredibly diverse population of cortical neurons that use GABA as neurotransmitter shows an equally diverse range of mechanisms that regulate changes in the strength of GABAergic synaptic transmission and allow them to dynamically follow and command the activity of neuronal ensembles. Similarly to glutamatergic synaptic transmission, activity-dependent functional changes in inhibitory neurotransmission are accompanied by alterations in GABAergic synapse structure that range from morphological reorganization of postsynaptic density to de novo formation and elimination of inhibitory contacts. Here we review several aspects of structural plasticity of inhibitory synapses, including its induction by different forms of neuronal activity, behavioral and sensory experience and the molecular mechanisms and signaling pathways involved. We discuss the functional consequences of GABAergic synapse structural plasticity for information processing and memory formation in view of the heterogenous nature of the structural plasticity phenomena affecting inhibitory synapses impinging on somatic and dendritic compartments of cortical and hippocampal neurons.

[1]  Vivien Chevaleyre,et al.  Endocannabinoid-mediated synaptic plasticity in the CNS. , 2006, Annual review of neuroscience.

[2]  T. Freund,et al.  Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells , 2001, Neuroscience.

[3]  C. Gilbert,et al.  Axonal Dynamics of Excitatory and Inhibitory Neurons in Somatosensory Cortex , 2010, PLoS biology.

[4]  T. Bonhoeffer,et al.  GABAergic synapses are formed without the involvement of dendritic protrusions , 2008, Nature Neuroscience.

[5]  P. Scheiffele,et al.  Control of Excitatory and Inhibitory Synapse Formation by Neuroligins , 2005, Science.

[6]  Tobias Bonhoeffer,et al.  Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation , 2013, Front. Neural Circuits.

[7]  O. Marín,et al.  Integration of GABAergic Interneurons into Cortical Cell Assemblies: Lessons from Embryos and Adults , 2013, Neuron.

[8]  Y. Ben-Ari,et al.  Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance , 2002, Trends in Neurosciences.

[9]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[10]  G. Knott,et al.  GAD67-Mediated GABA Synthesis and Signaling Regulate Inhibitory Synaptic Innervation in the Visual Cortex , 2007, Neuron.

[11]  R. Carroll,et al.  Selective translocation of Ca2+/calmodulin protein kinase IIα (CaMKIIα) to inhibitory synapses , 2010, Proceedings of the National Academy of Sciences.

[12]  J. Kirsch,et al.  Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin , 2000, Nature Neuroscience.

[13]  Idan Segev,et al.  Principles Governing the Operation of Synaptic Inhibition in Dendrites , 2012, Neuron.

[14]  W. Sieghart,et al.  Gephyrin, the enigmatic organizer at GABAergic synapses , 2012, Front. Cell. Neurosci..

[15]  Jun Noguchi,et al.  GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling , 2013, Nature Neuroscience.

[16]  Matthew E. Larkum,et al.  The GABAB1b Isoform Mediates Long-Lasting Inhibition of Dendritic Ca2+ Spikes in Layer 5 Somatosensory Pyramidal Neurons , 2006, Neuron.

[17]  Z. J. Huang.  Activity‐dependent development of inhibitory synapses and innervation pattern: role of GABA signalling and beyond , 2009, The Journal of physiology.

[18]  J. Sanes,et al.  Dystroglycan Is Selectively Associated with Inhibitory GABAergic Synapses But Is Dispensable for Their Differentiation , 2002, The Journal of Neuroscience.

[19]  T. Bonhoeffer,et al.  Experience leaves a lasting structural trace in cortical circuits , 2008, Nature.

[20]  M. Pangalos,et al.  The Clustering of GABAA Receptor Subtypes at Inhibitory Synapses is Facilitated via the Direct Binding of Receptor α2 Subunits to Gephyrin , 2008, The Journal of Neuroscience.

[21]  M. Colonnier.  Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[22]  A. Craig,et al.  Inhibitory Synapse Dynamics: Coordinated Presynaptic and Postsynaptic Mobility and the Major Contribution of Recycled Vesicles to New Synapse Formation , 2011, The Journal of Neuroscience.

[23]  J. Fawcett,et al.  The perineuronal net and the control of CNS plasticity , 2012, Cell and Tissue Research.

[24]  T. Freund,et al.  Perisomatic Inhibition , 2007, Neuron.

[25]  Arianna Maffei,et al.  Inhibitory Plasticity Dictates the Sign of Plasticity at Excitatory Synapses , 2014, The Journal of Neuroscience.

[26]  Susumu Y. Imanishi,et al.  Extracellular Signal-regulated Kinase and Glycogen Synthase Kinase 3β Regulate Gephyrin Postsynaptic Aggregation and GABAergic Synaptic Function in a Calpain-dependent Mechanism* , 2013, The Journal of Biological Chemistry.

[27]  H. Schindelin,et al.  The crystal structure of Escherichia coli MoeA and its relationship to the multifunctional protein gephyrin. , 2001, Structure.

[28]  J. Takagi,et al.  Higher-order architecture of cell adhesion mediated by polymorphic synaptic adhesion molecules neurexin and neuroligin. , 2012, Cell reports.

[29]  N. Brandon,et al.  Receptor for Activated C Kinase-1 Facilitates Protein Kinase C-Dependent Phosphorylation and Functional Modulation of GABAA Receptors with the Activation of G-Protein-Coupled Receptors , 2002, The Journal of Neuroscience.

[30]  Alberto Bacci,et al.  Assortment of GABAergic Plasticity in the Cortical Interneuron Melting Pot , 2011, Neural plasticity.

[31]  Alan R. Mardinly,et al.  Npas4 Regulates Excitatory-Inhibitory Balance within Neural Circuits through Cell-Type-Specific Gene Programs , 2014, Cell.

[32]  M. Kossut,et al.  Rapid, Learning-Induced Inhibitory Synaptogenesis in Murine Barrel Field , 2010, The Journal of Neuroscience.

[33]  Ann Marie Craig,et al.  Neurexins Induce Differentiation of GABA and Glutamate Postsynaptic Specializations via Neuroligins , 2004, Cell.

[34]  T. Südhof.  Neuroligins and neurexins link synaptic function to cognitive disease , 2008, Nature.

[35]  Elly Nedivi,et al.  Clustered Dynamics of Inhibitory Synapses and Dendritic Spines in the Adult Neocortex , 2012, Neuron.

[36]  D. Piomelli.  The molecular logic of endocannabinoid signalling , 2003, Nature Reviews Neuroscience.

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

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

[39]  K. Mikoshiba,et al.  Activity-Dependent Tuning of Inhibitory Neurotransmission Based on GABAAR Diffusion Dynamics , 2009, Neuron.

[40]  S. Moss,et al.  Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition , 2003, Current Opinion in Neurobiology.

[41]  Stephen J. Moss,et al.  Modulation of GABAA receptors by tyrosine phosphorylation , 1995, Nature.

[42]  N. Brose,et al.  Faculty Opinions recommendation of Differential dynamics and activity-dependent regulation of alpha- and beta-neurexins at developing GABAergic synapses. , 2011 .

[43]  D. Muller,et al.  Regulation of GABAergic synapse formation and plasticity by GSK3β-dependent phosphorylation of gephyrin , 2010, Proceedings of the National Academy of Sciences.

[44]  G. Shepherd,et al.  Transient and Persistent Dendritic Spines in the Neocortex In Vivo , 2005, Neuron.

[45]  Jun Noguchi,et al.  The Subspine Organization of Actin Fibers Regulates the Structure and Plasticity of Dendritic Spines , 2008, Neuron.

[46]  Kristina D. Micheva,et al.  An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[47]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[48]  M. Scanziani,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001, Science.

[49]  P. Caroni,et al.  Structural plasticity upon learning: regulation and functions , 2012, Nature Reviews Neuroscience.

[50]  Norio Matsuki,et al.  Locally Synchronized Synaptic Inputs , 2012, Science.

[51]  D. Kullmann,et al.  Plasticity of Inhibition , 2012, Neuron.

[52]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[53]  G. Knott,et al.  Experience and Activity-Dependent Maturation of Perisomatic GABAergic Innervation in Primary Visual Cortex during a Postnatal Critical Period , 2004, The Journal of Neuroscience.

[54]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[55]  K. Svoboda,et al.  Spine growth precedes synapse formation in the adult neocortex in vivo , 2006, Nature Neuroscience.

[56]  W. Gan,et al.  Stably maintained dendritic spines are associated with lifelong memories , 2009, Nature.

[57]  Gord Fishell,et al.  The genetics of early telencephalon patterning: some assembly required , 2008, Nature Reviews Neuroscience.

[58]  Massimo Scanziani,et al.  Routing of spike series by dynamic circuits in the hippocampus , 2004, Nature.

[59]  Kristen M Harris,et al.  Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP , 2011, Hippocampus.

[60]  J. Fritschy,et al.  Gephyrin: a master regulator of neuronal function? , 2014, Nature Reviews Neuroscience.

[61]  J. Fritschy,et al.  Molecular and functional heterogeneity of GABAergic synapses , 2012, Cellular and Molecular Life Sciences.

[62]  Seung-Hye Lee,et al.  Synaptic adhesion molecules , 2006 .

[63]  J. Brontë Gatenby,et al.  MATURATION OF RAT MAST CELLS , 1966, The Journal of Cell Biology.

[64]  S. Nelson,et al.  Potentiation of cortical inhibition by visual deprivation , 2006, Nature.

[65]  Robert J. Harvey,et al.  Gephyrin: where do we stand, where do we go? , 2008, Trends in Neurosciences.

[66]  R. Carroll,et al.  NMDA Receptor Activation Potentiates Inhibitory Transmission through GABA Receptor-Associated Protein-Dependent Exocytosis of GABAA Receptors , 2007, The Journal of Neuroscience.

[67]  J. Fawcett,et al.  Extracellular matrix and perineuronal nets in CNS repair , 2011, Developmental neurobiology.

[68]  Tobias Bonhoeffer,et al.  Loss of Sensory Input Causes Rapid Structural Changes of Inhibitory Neurons in Adult Mouse Visual Cortex , 2011, Neuron.

[69]  K. Svoboda,et al.  Structure and function of dendritic spines. , 2002, Annual review of physiology.

[70]  A. Matus,et al.  Actin-based plasticity in dendritic spines. , 2000, Science.

[71]  G. Schulte,et al.  Brain‐derived neurotrophic factor controls functional differentiation and microcircuit formation of selectively isolated fast‐spiking GABAergic interneurons , 2004, The European journal of neuroscience.

[72]  E. Cherubini,et al.  Gephyrin phosphorylation in the functional organization and plasticity of GABAergic synapses , 2014, Front. Cell. Neurosci..

[73]  Thomas M. Morse,et al.  Compartmentalization of GABAergic Inhibition by Dendritic Spines , 2013, Science.

[74]  H. Betz,et al.  Homeostatic regulation of gephyrin scaffolds and synaptic strength at mature hippocampal GABAergic postsynapses. , 2013, Cerebral cortex.

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

[76]  M. Greenberg,et al.  The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition , 2013, Nature.

[77]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[78]  Kirsten Harvey,et al.  Collybistin splice variants differentially interact with gephyrin and Cdc42 to regulate gephyrin clustering at GABAergic synapses , 2011, Journal of Cell Science.

[79]  M. Korte,et al.  Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin‐deficient mice , 2007, The EMBO journal.

[80]  M. Hoon,et al.  Neuroligin 2 Drives Postsynaptic Assembly at Perisomatic Inhibitory Synapses through Gephyrin and Collybistin , 2009, Neuron.

[81]  P. Castillo,et al.  Heterosynaptic LTD of Hippocampal GABAergic Synapses A Novel Role of Endocannabinoids in Regulating Excitability , 2003, Neuron.

[82]  Y. Komatsu,et al.  GABAB Receptors, Monoamine Receptors, and Postsynaptic Inositol Trisphosphate-Induced Ca2+ Release Are Involved in the Induction of Long-Term Potentiation at Visual Cortical Inhibitory Synapses , 1996, The Journal of Neuroscience.

[83]  Z. Henderson,et al.  Perineuronal nets ensheath fast spiking, parvalbumin‐immunoreactive neurons in the medial septum/diagonal band complex , 2000, The European journal of neuroscience.

[84]  Athar N. Malik,et al.  Activity-dependent regulation of inhibitory synapse development by Npas4 , 2008, Nature.

[85]  C. Holmgren,et al.  Coincident Spiking Activity Induces Long-Term Changes in Inhibition of Neocortical Pyramidal Cells , 2001, The Journal of Neuroscience.

[86]  M. Ahmadian,et al.  Collybistin activation by GTP-TC10 enhances postsynaptic gephyrin clustering and hippocampal GABAergic neurotransmission , 2013, Proceedings of the National Academy of Sciences.

[87]  Nicoletta Berardi,et al.  Critical periods during sensory development , 2000, Current Opinion in Neurobiology.

[88]  R. Yasuda,et al.  AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK–dependent manner during long-term potentiation , 2010, Proceedings of the National Academy of Sciences.

[89]  S. Goldman,et al.  Astrocyte-mediated potentiation of inhibitory synaptic transmission , 1998, Nature Neuroscience.

[90]  Chiayu Q. Chiu,et al.  Long-term plasticity at inhibitory synapses , 2011, Current Opinion in Neurobiology.

[91]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[92]  M. Sheng,et al.  Phosphorylation of Threonine-19 of PSD-95 by GSK-3β is Required for PSD-95 Mobilization and Long-Term Depression , 2013, The Journal of Neuroscience.

[93]  E. Gray,et al.  Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. , 1959, Journal of anatomy.

[94]  Roberto Malinow,et al.  Compartmentalized versus Global Synaptic Plasticity on Dendrites Controlled by Experience , 2011, Neuron.

[95]  S. Jamain,et al.  Neuroligin 2 is exclusively localized to inhibitory synapses. , 2004, European journal of cell biology.

[96]  J. Connelly,et al.  The crystal structure of Cdc42 in complex with collybistin II, a gephyrin-interacting guanine nucleotide exchange factor. , 2006, Journal of molecular biology.

[97]  J. Scott,et al.  A-kinase anchoring proteins: protein kinase A and beyond. , 2000, Current opinion in cell biology.

[98]  Chris J. McBain,et al.  Interneurons unbound , 2001, Nature Reviews Neuroscience.

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

[100]  E. M. Petrini,et al.  Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP , 2014, Nature Communications.

[101]  K. Svoboda,et al.  Experience-dependent structural synaptic plasticity in the mammalian brain , 2009, Nature Reviews Neuroscience.

[102]  C. Houston,et al.  CaMKII phosphorylation of the GABAA receptor: receptor subtype‐ and synapse‐specific modulation , 2009, The Journal of physiology.

[103]  Alcino J. Silva,et al.  Neurofibromin Regulation of ERK Signaling Modulates GABA Release and Learning , 2008, Cell.

[104]  F. Saraga,et al.  Inhibitory synaptic plasticity regulates pyramidal neuron spiking in the rodent hippocampus , 2008, Neuroscience.

[105]  Andreas Lüthi,et al.  Perineuronal Nets Protect Fear Memories from Erasure , 2009, Science.

[106]  Tobias Bonhoeffer,et al.  Activity-Dependent Clustering of Functional Synaptic Inputs on Developing Hippocampal Dendrites , 2011, Neuron.

[107]  Y. Zilberter,et al.  Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex , 2000, The Journal of physiology.

[108]  Gong Chen,et al.  Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABAA receptors , 2007, Molecular and Cellular Neuroscience.

[109]  A. El-Husseini,et al.  Cell adhesion molecules at the synapse. , 2006, Frontiers in bioscience : a journal and virtual library.

[110]  Yu Fu,et al.  Differential dynamics and activity-dependent regulation of α- and β-neurexins at developing GABAergic synapses , 2010, Proceedings of the National Academy of Sciences.

[111]  M. Sassoè-Pognetto,et al.  Understanding the Molecular Diversity of GABAergic Synapses , 2011, Front. Cell. Neurosci..

[112]  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.

[113]  G. Maccaferri,et al.  Stratum oriens horizontal interneurone diversity and hippocampal network dynamics , 2005, The Journal of physiology.

[114]  Chris I. De Zeeuw,et al.  Elimination of Inhibitory Synapses Is a Major Component of Adult Ocular Dominance Plasticity , 2012, Neuron.

[115]  R. Nicoll,et al.  Synaptic plasticity and dynamic modulation of the postsynaptic membrane , 2000, Nature Neuroscience.

[116]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[117]  J. Bourne,et al.  Balancing structure and function at hippocampal dendritic spines. , 2008, Annual review of neuroscience.

[118]  H. Abarbanel,et al.  Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. , 2006, Journal of neurophysiology.

[119]  O. Pascual,et al.  Homeostatic Regulation of Synaptic GlyR Numbers Driven by Lateral Diffusion , 2008, Neuron.

[120]  M. Dahan,et al.  Quantitative Nanoscopy of Inhibitory Synapses: Counting Gephyrin Molecules and Receptor Binding Sites , 2013, Neuron.

[121]  M. Pangalos,et al.  Activity-Dependent Ubiquitination of GABAA Receptors Regulates Their Accumulation at Synaptic Sites , 2007, The Journal of Neuroscience.

[122]  Y. Bae,et al.  The adhesion protein IgSF9b is coupled to neuroligin 2 via S-SCAM to promote inhibitory synapse development , 2013, The Journal of cell biology.

[123]  Eric R Kandel,et al.  Calcineurin-Mediated LTD of GABAergic Inhibition Underlies the Increased Excitability of CA1 Neurons Associated with LTP , 2000, Neuron.

[124]  S. Moss,et al.  The dynamic modulation of GABA(A) receptor trafficking and its role in regulating the plasticity of inhibitory synapses. , 2011, Physiological reviews.

[125]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

[126]  C. Chapman,et al.  GABAB Receptor‐ and Metabotropic Glutamate Receptor‐Dependent Cooperative Long‐Term Potentiation of Rat Hippocampal GABAA Synaptic Transmission , 2003, The Journal of physiology.

[127]  Nicoletta Berardi,et al.  Extracellular Matrix and Visual Cortical Plasticity Freeing the Synapse , 2004, Neuron.

[128]  J. Meier,et al.  Palmitoylation of Gephyrin Controls Receptor Clustering and Plasticity of GABAergic Synapses , 2014, PLoS biology.

[129]  M. Owen,et al.  The GDP-GTP Exchange Factor Collybistin: An Essential Determinant of Neuronal Gephyrin Clustering , 2004, The Journal of Neuroscience.

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

[131]  R. Yuste,et al.  Morphological changes in dendritic spines associated with long-term synaptic plasticity. , 2001, Annual review of neuroscience.

[132]  G. Turrigiano,et al.  Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period , 2013, Proceedings of the National Academy of Sciences.

[133]  Jun Noguchi,et al.  Structural dynamics of dendritic spines in memory and cognition , 2010, Trends in Neurosciences.

[134]  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.

[135]  Eric R Kandel,et al.  Synapses and memory storage. , 2012, Cold Spring Harbor perspectives in biology.

[136]  S. Moss,et al.  The role of GABAAR phosphorylation in the construction of inhibitory synapses and the efficacy of neuronal inhibition. , 2009, Biochemical Society transactions.

[137]  S. Moss,et al.  Conserved phosphorylation of the intracellular domains of GABAA receptorβ2 and β3 subunits by cAMP-dependent protein kinase, cGMP-dependent protein kinase, protein kinase C and Ca2+/calmodulin type II-dependent protein kinase , 1997, Neuropharmacology.

[138]  Juan Burrone,et al.  Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons , 2006, Nature Neuroscience.

[139]  R. Delorenzo,et al.  Calcium/calmodulin‐dependent kinase II phosphorylation of the GABAA receptor α1 subunit modulates benzodiazepine binding , 2002, Journal of neurochemistry.

[140]  Masahiko Watanabe,et al.  Endocannabinoid-mediated control of synaptic transmission. , 2009, Physiological reviews.

[141]  D. Muller,et al.  Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells , 2011, Neuropharmacology.

[142]  Gray Eg.  Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

[143]  T. Hensch.  Critical period regulation. , 2004, Annual review of neuroscience.

[144]  Y. Ben-Ari,et al.  GABA: an excitatory transmitter in early postnatal life , 1991, Trends in Neurosciences.

[145]  D. Linden.  The Return of the Spike Postsynaptic Action Potentials and the Induction of LTP and LTD , 1999, Neuron.

[146]  Y. Yoshimura,et al.  Activity-Dependent Maintenance of Long-Term Potentiation at Visual Cortical Inhibitory Synapses , 2000, The Journal of Neuroscience.

[147]  T. Südhof,et al.  Activity-Dependent Validation of Excitatory versus Inhibitory Synapses by Neuroligin-1 versus Neuroligin-2 , 2007, Neuron.

[148]  Ann Marie Craig,et al.  Neurexin–neuroligin signaling in synapse development , 2007, Current Opinion in Neurobiology.

[149]  M. Poo,et al.  Coincident Pre- and Postsynaptic Activity Modifies GABAergic Synapses by Postsynaptic Changes in Cl− Transporter Activity , 2003, Neuron.

[150]  R. Malinow,et al.  Ras and Rap Control AMPA Receptor Trafficking during Synaptic Plasticity , 2002, Cell.

[151]  P. Jonas,et al.  Postnatal Differentiation of Basket Cells from Slow to Fast Signaling Devices , 2008, The Journal of Neuroscience.

[152]  T. Südhof,et al.  Neurexins Physically and Functionally Interact with GABAA Receptors , 2010, Neuron.

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

[154]  N. Brandon,et al.  A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABAA receptors by cAMP-dependent protein kinase via selective interaction with receptor β subunits , 2003, Molecular and Cellular Neuroscience.

[155]  D. Stellwagen,et al.  Dystroglycan mediates homeostatic synaptic plasticity at GABAergic synapses , 2014, Proceedings of the National Academy of Sciences.

[156]  Peter Somogyi,et al.  Increased number of synaptic GABAA receptors underlies potentiation at hippocampal inhibitory synapses , 1998, Nature.

[157]  G. Schwarz,et al.  Neuronal Nitric Oxide Synthase-Dependent S-Nitrosylation of Gephyrin Regulates Gephyrin Clustering at GABAergic Synapses , 2014, The Journal of Neuroscience.

[158]  Gabriel M. Belfort,et al.  Npas4 Regulates a Transcriptional Program in CA3 Required for Contextual Memory Formation , 2011, Science.

[159]  Steven W. Flavell,et al.  Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. , 2008, Annual review of neuroscience.