GABAergic Interneurons Shape the Functional Maturation of the Cortex

From early embryonic development to adulthood, GABA release participates in the construction of the mammalian cerebral cortex. The maturation of GABAergic neurotransmission is a protracted process which takes place in discrete steps and results from the dynamic interaction between developmentally directed gene expression and brain activity. During the course of development, GABAergic interneurons contribute to key aspects of the functional maturation of the cortex in different ways, from exerting a trophic role to pacing immature neural networks. In this review, we provide an overview of the maturation of GABAergic neurotransmission and discuss the role of GABAergic interneurons in cortical wiring, plasticity, and network activity during pre- and postnatal development. We also discuss psychiatric diseases that may be considered at least in part developmental disorders of the GABAergic system.

[1]  Kristina D. Micheva,et al.  Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry , 1996, The Journal of comparative neurology.

[2]  B. Sakmann,et al.  Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS , 1995, Neuron.

[3]  D. Kullmann,et al.  Roles of distinct glutamate receptors in induction of anti‐Hebbian long‐term potentiation , 2008, The Journal of physiology.

[4]  Michael L. Wallace,et al.  Maternal Loss of Ube3a Produces an Excitatory/Inhibitory Imbalance through Neuron Type-Specific Synaptic Defects , 2012, Neuron.

[5]  S. Anderson,et al.  Mutations of the Homeobox Genes Dlx-1 and Dlx-2 Disrupt the Striatal Subventricular Zone and Differentiation of Late Born Striatal Neurons , 1997, Neuron.

[6]  P. Somogyi,et al.  Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Vladislav Volman,et al.  Downregulation of Parvalbumin at Cortical GABA Synapses Reduces Network Gamma Oscillatory Activity , 2011, The Journal of Neuroscience.

[8]  S. Cheung,et al.  Genetics of Autism Spectrum Disorders: The Opportunity and Challenge in the Genetics Clinic , 2015 .

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

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

[11]  R. Froemke,et al.  Intrinsically determined cell death of developing cortical interneurons , 2012, Nature.

[12]  J. A. Payne,et al.  The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation , 1999, Nature.

[13]  J. Barker,et al.  Differential Response of Cortical Plate and Ventricular Zone Cells to GABA as a Migration Stimulus , 1998, The Journal of Neuroscience.

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

[15]  Zhen Huang.  Molecular regulation of neuronal migration during neocortical development , 2009, Molecular and Cellular Neuroscience.

[16]  B. Moghaddam,et al.  NMDA Receptor Hypofunction Produces Opposite Effects on Prefrontal Cortex Interneurons and Pyramidal Neurons , 2007, The Journal of Neuroscience.

[17]  G. Fishell,et al.  Mechanisms of inhibition within the telencephalon: "where the wild things are". , 2011, Annual review of neuroscience.

[18]  D. L. Martin,et al.  Two isoforms of glutamate decarboxylase: why? , 1998, Trends in pharmacological sciences.

[19]  B. Hutcheon,et al.  Developmental change in GABAA receptor desensitization kinetics and its role in synapse function in rat cortical neurons , 2000, The Journal of physiology.

[20]  Rodney C. Samaco,et al.  GABAergic dysfunction mediates autism-like stereotypies and Rett syndrome phenotypes , 2010, Nature.

[21]  A. Hendrickson,et al.  Coincidental appearance of the α1 subunit of the gaba-a receptor and the type ibenzodiazepine receptor near birth in macaque monkey visual cortex , 1994, International Journal of Developmental Neuroscience.

[22]  I. Katona,et al.  In Vivo Labeling of Parvalbumin-Positive Interneurons and Analysis of Electrical Coupling in Identified Neurons , 2002, The Journal of Neuroscience.

[23]  M. Stryker,et al.  Local GABA circuit control of experience-dependent plasticity in developing visual cortex. , 1998, Science.

[24]  M. Fagiolini,et al.  Autism: A “Critical Period” Disorder? , 2011, Neural plasticity.

[25]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[26]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[27]  T. Südhof,et al.  Common circuit defect of excitatory-inhibitory balance in mouse models of autism , 2009, Journal of Neurodevelopmental Disorders.

[28]  M. Fanselow,et al.  Mice Lacking the β3 Subunit of the GABAA Receptor Have the Epilepsy Phenotype and Many of the Behavioral Characteristics of Angelman Syndrome , 1998, The Journal of Neuroscience.

[29]  I. Ferrer,et al.  Development of GABA‐immunoreactivity in the neocortex of the mouse , 1992, The Journal of comparative neurology.

[30]  R. Schneggenburger,et al.  Parvalbumin Is a Mobile Presynaptic Ca2+ Buffer in the Calyx of Held that Accelerates the Decay of Ca2+ and Short-Term Facilitation , 2007, The Journal of Neuroscience.

[31]  A. Lieberman,et al.  The development of non-pyramidal neurons in the visual cortex of the rat , 2004, Anatomy and Embryology.

[32]  D. Volk,et al.  Increased density of microtubule associated protein 2-immunoreactive neurons in the prefrontal white matter of schizophrenic subjects , 1996, Schizophrenia Research.

[33]  A. Bird,et al.  Reversal of Neurological Defects in a Mouse Model of Rett Syndrome , 2007, Science.

[34]  Rosa Cossart,et al.  Sequential Generation of Two Distinct Synapse-Driven Network Patterns in Developing Neocortex , 2008, The Journal of Neuroscience.

[35]  A. Kirkwood,et al.  Dark Rearing Alters the Development of GABAergic Transmission in Visual Cortex , 2002, The Journal of Neuroscience.

[36]  Chang-Gyu Hahn,et al.  Dysbindin-1 is a synaptic and microtubular protein that binds brain snapin. , 2006, Human molecular genetics.

[37]  Gavin P. Reynolds,et al.  A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia , 2002, Schizophrenia Research.

[38]  L. Bosman,et al.  Neonatal development of the rat visual cortex: synaptic function of GABAA receptor alpha subunits. , 2002, The Journal of physiology.

[39]  Arnold R Kriegstein,et al.  GABA Regulates Excitatory Synapse Formation in the Neocortex via NMDA Receptor Activation , 2008, The Journal of Neuroscience.

[40]  Ken Sugino,et al.  Transcriptional and Electrophysiological Maturation of Neocortical Fast-Spiking GABAergic Interneurons , 2009, The Journal of Neuroscience.

[41]  M. C. Angulo,et al.  Developmental Synaptic Changes Increase the Range of Integrative Capabilities of an Identified Excitatory Neocortical Connection , 1999, The Journal of Neuroscience.

[42]  P. Somogyi,et al.  Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus , 2002, The Journal of Neuroscience.

[43]  Daphne Bavelier,et al.  Removing Brakes on Adult Brain Plasticity: From Molecular to Behavioral Interventions , 2010, The Journal of Neuroscience.

[44]  J. Krystal,et al.  First in vivo evidence of an NMDA receptor deficit in medication-free schizophrenic patients , 2006, Molecular Psychiatry.

[45]  M. Frotscher,et al.  Subcellular Localization of Metabotropic GABAB Receptor Subunits GABAB1a/b and GABAB2 in the Rat Hippocampus , 2003, The Journal of Neuroscience.

[46]  M. Poo,et al.  Excitatory GABA Action Is Essential for Morphological Maturation of Cortical Neurons In Vivo , 2007, The Journal of Neuroscience.

[47]  Raquel E Gur,et al.  Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. , 2004, The Journal of clinical investigation.

[48]  Dante S. Bortone,et al.  KCC2 Expression Promotes the Termination of Cortical Interneuron Migration in a Voltage-Sensitive Calcium-Dependent Manner , 2009, Neuron.

[49]  R. McCarley,et al.  Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia , 2009, BMC Neuroscience.

[50]  Takahisa Taguchi,et al.  Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia. , 2004, Human molecular genetics.

[51]  W. Singer,et al.  Neuronal Dynamics and Neuropsychiatric Disorders: Toward a Translational Paradigm for Dysfunctional Large-Scale Networks , 2012, Neuron.

[52]  Zhong-Wei Zhang,et al.  Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. , 2004, Journal of neurophysiology.

[53]  D. Prince,et al.  Postnatal maturation of the GABAergic system in rat neocortex. , 1991, Journal of neurophysiology.

[54]  O. Marín,et al.  Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling , 2010, Nature.

[55]  C. Weickert,et al.  Higher Gamma-Aminobutyric Acid Neuron Density in the White Matter of Orbital Frontal Cortex in Schizophrenia , 2012, Biological Psychiatry.

[56]  Philippe Séguéla,et al.  Downregulation of tonic GABAergic inhibition in a mouse model of fragile X syndrome. , 2009, Cerebral cortex.

[57]  Jürgen Bolz,et al.  Disrupted-in-Schizophrenia 1 (DISC1) Is Necessary for the Correct Migration of Cortical Interneurons , 2012, The Journal of Neuroscience.

[58]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[59]  Tobias M. Fischer,et al.  Short- and Long-Range Attraction of Cortical GABAergic Interneurons by Neuregulin-1 , 2004, Neuron.

[60]  Klaartje Heinen,et al.  Mice lacking the major adult GABAA receptor subtype have normal number of synapses, but retain juvenile IPSC kinetics until adulthood. , 2005, Journal of neurophysiology.

[61]  D. Coulter,et al.  Protracted postnatal development of inhibitory synaptic transmission in rat hippocampal area CA1 neurons. , 2000, Journal of neurophysiology.

[62]  Michel A. Picardo,et al.  Pioneer GABA Cells Comprise a Subpopulation of Hub Neurons in the Developing Hippocampus , 2011, Neuron.

[63]  G. Di Cristo,et al.  Neural Activity and Neurotransmission Regulate the Maturation of the Innervation Field of Cortical GABAergic Interneurons in an Age-Dependent Manner , 2012, The Journal of Neuroscience.

[64]  G. Blatt,et al.  Reduced GABAA receptors and benzodiazepine binding sites in the posterior cingulate cortex and fusiform gyrus in autism , 2011, Brain Research.

[65]  T. Hökfelt,et al.  TrkB signaling in parvalbumin-positive interneurons is critical for gamma-band network synchronization in hippocampus , 2011, Proceedings of the National Academy of Sciences.

[66]  Leanne M Williams,et al.  "Gamma (40 Hz) phase synchronicity" and symptom dimensions in schizophrenia , 2003, Cognitive neuropsychiatry.

[67]  Jyh-Jang Sun,et al.  Three Patterns of Oscillatory Activity Differentially Synchronize Developing Neocortical Networks In Vivo , 2009, The Journal of Neuroscience.

[68]  V. Meskenaite,et al.  GABAB‐receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization , 1999, The European journal of neuroscience.

[69]  Pat Levitt,et al.  Molecular Characterization of Schizophrenia Viewed by Microarray Analysis of Gene Expression in Prefrontal Cortex , 2000, Neuron.

[70]  Leyuan Shi,et al.  Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. , 1997, Science.

[71]  Alessandro Sale,et al.  Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition , 2007, Nature Neuroscience.

[72]  A. Kriegstein,et al.  Blocking early GABA depolarization with bumetanide results in permanent alterations in cortical circuits and sensorimotor gating deficits. , 2011, Cerebral cortex.

[73]  Wenjun Gao,et al.  Cell-type Specific Development of NMDA Receptors in the Interneurons of Rat Prefrontal Cortex , 2009, Neuropsychopharmacology.

[74]  Z. J. Huang,et al.  Development of GABA innervation in the cerebral and cerebellar cortices , 2007, Nature Reviews Neuroscience.

[75]  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.

[76]  S. Hirsch,et al.  Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia , 1998, Journal of neurology, neurosurgery, and psychiatry.

[77]  G. Knott,et al.  GABA Signaling Promotes Synapse Elimination and Axon Pruning in Developing Cortical Inhibitory Interneurons , 2012, The Journal of Neuroscience.

[78]  Karel Svoboda,et al.  Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs , 2004, Nature Neuroscience.

[79]  I. Cohen,et al.  The DLX1and DLX2 genes and susceptibility to autism spectrum disorders , 2009, European Journal of Human Genetics.

[80]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[81]  O. Paulsen,et al.  Expression and distribution of metabotropic GABA receptor subtypes GABABR1 and GABABR2 during rat neocortical development , 2002, The European journal of neuroscience.

[82]  D. Lewis,et al.  Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. , 2000, Archives of general psychiatry.

[83]  Edvard I Moser,et al.  Development of the Spatial Representation System in the Rat , 2010, Science.

[84]  Mark F Bear,et al.  The pathophysiology of fragile X (and what it teaches us about synapses). , 2012, Annual review of neuroscience.

[85]  Yehezkel Ben-Ari,et al.  Retinal Waves Trigger Spindle Bursts in the Neonatal Rat Visual Cortex , 2006, The Journal of Neuroscience.

[86]  S. Schulz,et al.  Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices , 2002, Biological Psychiatry.

[87]  L. Bosman,et al.  Neonatal development of the rat visual cortex: synaptic function of GABAa receptor α subunits , 2002 .

[88]  J. Coyle,et al.  NMDA receptor function, neuroplasticity, and the pathophysiology of schizophrenia. , 2004, International review of neurobiology.

[89]  Daniel R Weinberger,et al.  Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. , 2004, Archives of general psychiatry.

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

[91]  I. Soltesz,et al.  GABAA Receptor–Mediated Miniature Postsynaptic Currents and α-Subunit Expression in Developing Cortical Neurons , 1999 .

[92]  J DeFelipe,et al.  Postnatal development of the vesicular gaba transporter in rat cerebral cortex , 2003, Neuroscience.

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

[94]  Jan-Fang Cheng,et al.  Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome , 2005, Nature Genetics.

[95]  A. Prochiantz,et al.  Experience-Dependent Transfer of Otx2 Homeoprotein into the Visual Cortex Activates Postnatal Plasticity , 2008, Cell.

[96]  Konstantin Khodosevich,et al.  “Small Axonless Neurons”: Postnatally Generated Neocortical Interneurons with Delayed Functional Maturation , 2011, The Journal of Neuroscience.

[97]  E R Martin,et al.  Association Analysis of Chromosome 15 GABAA Receptor Subunit Genes in Autistic Disorder , 2001, Journal of neurogenetics.

[98]  Rodney C Samaco,et al.  Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. , 2005, Human molecular genetics.

[99]  David A. Lewis,et al.  Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia , 2012, Trends in Neurosciences.

[100]  J. Coyle,et al.  Neurochemical aspects of the ontogenesis of gabanergic neurons in the rat brain , 1976, Brain Research.

[101]  Y. Ben-Ari,et al.  Giant synaptic potentials in immature rat CA3 hippocampal neurones. , 1989, The Journal of physiology.

[102]  P. Bregestovski,et al.  Excitatory GABA: How a Correct Observation May Turn Out to be an Experimental Artifact , 2012, Front. Pharmacol..

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

[104]  Ravinesh A. Kumar,et al.  Genetics of autism spectrum disorders , 2009, Current neurology and neuroscience reports.

[105]  Fiona E. N. LeBeau,et al.  Recruitment of Parvalbumin-Positive Interneurons Determines Hippocampal Function and Associated Behavior , 2007, Neuron.

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

[107]  J. Isaac,et al.  Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex , 2007, Nature Neuroscience.

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

[109]  A. Kriegstein,et al.  GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis , 1995, Neuron.

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

[111]  Chun Li,et al.  Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder , 2008, Autism research : official journal of the International Society for Autism Research.

[112]  Michael P Stryker,et al.  Cortical Plasticity Induced by Inhibitory Neuron Transplantation , 2010, Science.

[113]  F. Conti,et al.  GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications , 2004, Brain Research Reviews.

[114]  T. Mitsuhashi,et al.  Genetic regulation of proliferation/differentiation characteristics of neural progenitor cells in the developing neocortex , 2009, Brain and Development.

[115]  Thomas J. Wills,et al.  Development of the Hippocampal Cognitive Map in Preweanling Rats , 2010, Science.

[116]  P. Thuras,et al.  mRNA and Protein Levels for GABAAα4, α5, β1 and GABABR1 Receptors are Altered in Brains from Subjects with Autism , 2010, Journal of autism and developmental disorders.

[117]  Kevin M. Spencer,et al.  Baseline gamma power during auditory steady-state stimulation in schizophrenia , 2012, Front. Hum. Neurosci..

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

[119]  C. Gillberg and,et al.  Autism and Asperger syndrome: coexistence with other clinical disorders , 2000, Acta psychiatrica Scandinavica.

[120]  M. Vreugdenhil,et al.  Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. , 2003, Journal of neurophysiology.

[121]  K. Nakazawa,et al.  Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes , 2010, Nature Neuroscience.

[122]  A. Sampson,et al.  Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. , 2000, Archives of general psychiatry.

[123]  P. Ernfors,et al.  Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells , 2011, Proceedings of the National Academy of Sciences.

[124]  D. Ulrich,et al.  GABAB receptors: synaptic functions and mechanisms of diversity , 2007, Current Opinion in Neurobiology.

[125]  Wenjun Gao,et al.  Development of calcium‐permeable AMPA receptors and their correlation with NMDA receptors in fast‐spiking interneurons of rat prefrontal cortex , 2010, The Journal of physiology.

[126]  Nathan R. Wilson,et al.  Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice , 2009, Proceedings of the National Academy of Sciences.

[127]  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.

[128]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[129]  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.

[130]  M. Stryker,et al.  Genomic imprinting of experience-dependent cortical plasticity by the ubiquitin ligase gene Ube3a , 2010, Proceedings of the National Academy of Sciences.

[131]  Court Hull,et al.  Postsynaptic Mechanisms Govern the Differential Excitation of Cortical Neurons by Thalamic Inputs , 2009, The Journal of Neuroscience.

[132]  A. Prochiantz,et al.  Otx2 Binding to Perineuronal Nets Persistently Regulates Plasticity in the Mature Visual Cortex , 2012, The Journal of Neuroscience.

[133]  David A Lewis,et al.  Glutamate Receptor Subtypes Mediating Synaptic Activation of Prefrontal Cortex Neurons: Relevance for Schizophrenia , 2011, The Journal of Neuroscience.

[134]  M. Stryker,et al.  Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[135]  A. Kriegstein,et al.  Excitatory GABA Responses in Embryonic and Neonatal Cortical Slices Demonstrated by Gramicidin Perforated-Patch Recordings and Calcium Imaging , 1996, The Journal of Neuroscience.

[136]  Bassem A. Hassan,et al.  Decreased expression of the GABAA receptor in fragile X syndrome , 2006, Brain Research.

[137]  L. Benevento,et al.  The effects of dark-rearing on the electrophysiology of the rat visual cortex , 1992, Brain Research.

[138]  D. Weinberger,et al.  Role of dysbindin in dopamine receptor trafficking and cortical GABA function , 2009, Proceedings of the National Academy of Sciences.

[139]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[140]  G. Miyoshi,et al.  Physiologically Distinct Temporal Cohorts of Cortical Interneurons Arise from Telencephalic Olig2-Expressing Precursors , 2007, The Journal of Neuroscience.

[141]  Mark F Bear,et al.  Toward fulfilling the promise of molecular medicine in fragile X syndrome. , 2011, Annual review of medicine.

[142]  Caleb F. Davis,et al.  Genetic Disruption of Cortical Interneuron Development Causes Region- and GABA Cell Type-Specific Deficits, Epilepsy, and Behavioral Dysfunction , 2003, The Journal of Neuroscience.

[143]  A. Addington,et al.  GAD1 (2q31.1), which encodes glutamic acid decarboxylase (GAD67), is associated with childhood-onset schizophrenia and cortical gray matter volume loss , 2005, Molecular Psychiatry.

[144]  A. Malhotra,et al.  Association of ketamine-induced psychosis with focal activation of the prefrontal cortex in healthy volunteers. , 1997, The American journal of psychiatry.

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

[146]  C. Lois,et al.  Transplanted neurons form both normal and ectopic projections in the adult brain , 2008, Developmental neurobiology.

[147]  L. Maffei,et al.  The Antidepressant Fluoxetine Restores Plasticity in the Adult Visual Cortex , 2008, Science.

[148]  Daniel L. Schacter,et al.  Spatial Representation in the Entorhinal Cortex , 2004 .

[149]  J. Glausier,et al.  Selective Pyramidal Cell Reduction of GABAA Receptor α1 Subunit Messenger RNA Expression in Schizophrenia , 2011, Neuropsychopharmacology.

[150]  A. Sampson,et al.  Gene Expression Deficits in a Subclass of GABA Neurons in the Prefrontal Cortex of Subjects with Schizophrenia , 2003, The Journal of Neuroscience.

[151]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[152]  H. Adesnik,et al.  Input normalization by global feedforward inhibition expands cortical dynamic range , 2009, Nature Neuroscience.

[153]  Y. Ben-Ari,et al.  Early sequential formation of functional GABAA and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus , 2002, The European journal of neuroscience.

[154]  Mark F. Bear,et al.  Correction of Fragile X Syndrome in Mice , 2007, Neuron.

[155]  Mriganka Sur,et al.  Dendritic Spine Dynamics Are Regulated by Monocular Deprivation and Extracellular Matrix Degradation , 2004, Neuron.

[156]  T. Südhof,et al.  Synaptic assembly of the brain in the absence of neurotransmitter secretion. , 2000, Science.

[157]  E. Mcgeer,et al.  Postnatal changes of GABAergic and glutamatergic parameters. , 1981, Brain research.

[158]  R. Straub,et al.  Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. , 2002, American journal of human genetics.

[159]  G. Roch,et al.  The onset of synaptogenesis in rat temporal cortex , 1975, Anatomy and Embryology.

[160]  J. Kleinman,et al.  Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia , 2003, Molecular Psychiatry.

[161]  Arianna Maffei,et al.  The age of plasticity: developmental regulation of synaptic plasticity in neocortical microcircuits. , 2008, Progress in brain research.

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

[163]  G. Miyoshi,et al.  GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development. , 2011, Cerebral cortex.

[164]  S. Nelson,et al.  Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation , 2004, Nature Neuroscience.

[165]  M. Valdeolmillos,et al.  Receptor-activated calcium signals in tangentially migrating cortical cells. , 2002, Cerebral cortex.

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

[167]  H. Stefánsson,et al.  Neuregulin 1 and susceptibility to schizophrenia. , 2002, American journal of human genetics.

[168]  Y. Ben-Ari,et al.  Glutamate Acting on AMPA But Not NMDA Receptors Modulates the Migration of Hippocampal Interneurons , 2006, The Journal of Neuroscience.

[169]  C. Métin,et al.  Intermediate Zone Cells Express Calcium-Permeable AMPA Receptors and Establish Close Contact with Growing Axons , 2000, The Journal of Neuroscience.

[170]  G. Buzsáki,et al.  Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups , 2005, Neuroscience.

[171]  A. Kirkwood,et al.  A Refractory Period for Rejuvenating GABAergic Synaptic Transmission and Ocular Dominance Plasticity with Dark Exposure , 2010, The Journal of Neuroscience.

[172]  H. Monyer,et al.  Diazepam binding inhibitor promotes progenitor proliferation in the postnatal SVZ by reducing GABA signaling. , 2012, Cell stem cell.

[173]  E. G. Jones,et al.  Stimulus-dependent, reciprocal up- and downregulation of glutamic acid decarboxylase and Ca2+/calmodulin-dependent protein kinase II gene expression in rat cerebral cortex , 1996, Experimental Brain Research.

[174]  Jacqueline Blundell,et al.  A Neuroligin-3 Mutation Implicated in Autism Increases Inhibitory Synaptic Transmission in Mice , 2007, Science.

[175]  P. Jonas,et al.  How the 'slow' Ca2+ buffer parvalbumin affects transmitter release in nanodomain-coupling regimes , 2011, Nature Neuroscience.

[176]  L. Benevento,et al.  Gamma-aminobutyric acid and somatostatin immunoreactivity in the visual cortex of normal and dark-reared rats , 1995, Brain Research.

[177]  Theofanis Karayannis,et al.  Neuronal activity is required for the development of specific cortical interneuron subtypes , 2011, Nature.

[178]  G. Buzsáki,et al.  Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. , 1996, The Journal of physiology.

[179]  O. Marín,et al.  Cell migration in the forebrain. , 2003, Annual review of neuroscience.

[180]  T. Woo,et al.  A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[181]  Kristopher T Kahle,et al.  The GABA Excitatory/Inhibitory Shift in Brain Maturation and Neurological Disorders , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[182]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[183]  D. Hubel,et al.  EFFECTS OF VISUAL DEPRIVATION ON MORPHOLOGY AND PHYSIOLOGY OF CELLS IN THE CATS LATERAL GENICULATE BODY. , 1963, Journal of neurophysiology.

[184]  Yehezkel Ben-Ari,et al.  The Establishment of GABAergic and Glutamatergic Synapses on CA1 Pyramidal Neurons is Sequential and Correlates with the Development of the Apical Dendrite , 1999, The Journal of Neuroscience.

[185]  P. Wahle,et al.  Neuronal activity and neurotrophic factors regulate GAD‐65/67 mRNA and protein expression in organotypic cultures of rat visual cortex , 2003, The European journal of neuroscience.

[186]  M C O'Donovan,et al.  Support for genetic variation in neuregulin 1 and susceptibility to schizophrenia , 2003, Molecular Psychiatry.

[187]  Nicoletta Berardi,et al.  Reducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity , 2010, The Journal of Neuroscience.

[188]  Paul J. Harrison,et al.  Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis , 2003, Molecular Psychiatry.

[189]  David A Lewis,et al.  The role of glutamatergic inputs onto parvalbumin-positive interneurons: relevance for schizophrenia , 2012, Reviews in the neurosciences.

[190]  A. Sampson,et al.  Relationship of Brain-Derived Neurotrophic Factor and Its Receptor TrkB to Altered Inhibitory Prefrontal Circuitry in Schizophrenia , 2005, The Journal of Neuroscience.

[191]  J. Clayton-Smith,et al.  Angelman syndrome: a review of the clinical and genetic aspects , 2003, Journal of medical genetics.

[192]  Y. Ben-Ari,et al.  A Noncanonical Release of GABA and Glutamate Modulates Neuronal Migration , 2005, The Journal of Neuroscience.

[193]  M. Kossut,et al.  Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning. , 2001, Cerebral cortex.

[194]  O. Paulsen,et al.  Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. , 2003, Cerebral cortex.

[195]  K. Deisseroth,et al.  Dlx5 and Dlx6 Regulate the Development of Parvalbumin-Expressing Cortical Interneurons , 2010, The Journal of Neuroscience.

[196]  J. Rossier,et al.  Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel , 1994, Neuron.

[197]  Hannah Monyer,et al.  NMDA Receptor Ablation on Parvalbumin-Positive Interneurons Impairs Hippocampal Synchrony, Spatial Representations, and Working Memory , 2010, Neuron.

[198]  A. Sampson,et al.  Reciprocal alterations in pre- and postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. , 2002, Cerebral cortex.

[199]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis , 1983, Journal of neurocytology.

[200]  Kevin L Quick,et al.  Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase , 2007, Science.

[201]  David G. Jones,et al.  Frontiers in Cellular Neuroscience Cellular Neuroscience , 2022 .

[202]  L. Benardo,et al.  Recruitment of GABAA inhibition in rat neocortex is limited and not NMDA dependent. , 1995, Journal of neurophysiology.

[203]  M. Fagiolini,et al.  Specific GABAA Circuits for Visual Cortical Plasticity , 2004, Science.

[204]  E. G. Jones,et al.  Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. , 1995, Archives of general psychiatry.

[205]  A. Manira,et al.  Histone H2AX-dependent GABAA receptor regulation of stem cell proliferation , 2008, Nature.

[206]  Shaul Hestrin,et al.  Synaptogenesis of Electrical and GABAergic Synapses of Fast-Spiking Inhibitory Neurons in the Neocortex , 2011, The Journal of Neuroscience.

[207]  Marc G Caron,et al.  Mice with Reduced NMDA Receptor Expression Display Behaviors Related to Schizophrenia , 1999, Cell.

[208]  T. Bártfai,et al.  A Specific Role for NR2A-Containing NMDA Receptors in the Maintenance of Parvalbumin and GAD67 Immunoreactivity in Cultured Interneurons , 2006, The Journal of Neuroscience.

[209]  J. Palva,et al.  Postnatal development of rat hippocampal gamma rhythm in vivo. , 2002, Journal of neurophysiology.

[210]  Jessica A. Cardin,et al.  A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior , 2011, Molecular Psychiatry.

[211]  H. Luhmann,et al.  Thalamic network oscillations synchronize ontogenetic columns in the newborn rat barrel cortex. , 2013, Cerebral cortex.

[212]  T. Tsumoto,et al.  Metabotropic Glutamate Receptor Type 5-Dependent Long-Term Potentiation of Excitatory Synapses on Fast-Spiking GABAergic Neurons in Mouse Visual Cortex , 2008, The Journal of Neuroscience.

[213]  J. Barker,et al.  GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. , 2000, Cerebral cortex.

[214]  Ethan M. Goldberg,et al.  Rapid developmental maturation of neocortical FS cell intrinsic excitability. , 2011, Cerebral cortex.

[215]  R. Yuste,et al.  The Enigmatic Function of Chandelier Cells , 2010, Front. Neurosci..

[216]  G. Miyoshi,et al.  Genetic Fate Mapping Reveals That the Caudal Ganglionic Eminence Produces a Large and Diverse Population of Superficial Cortical Interneurons , 2010, The Journal of Neuroscience.

[217]  W. Brown,et al.  Decreased GABAA receptor expression in the seizure-prone fragile X mouse , 2005, Neuroscience Letters.

[218]  J. Poncer,et al.  Role of the neuronal K-Cl co-transporter KCC2 in inhibitory and excitatory neurotransmission , 2012, Front. Cell. Neurosci..

[219]  Z Josh Huang,et al.  Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance plasticity. , 2011, Journal of neurophysiology.

[220]  Ileana L. Hanganu-Opatz,et al.  Coupled Oscillations Mediate Directed Interactions between Prefrontal Cortex and Hippocampus of the Neonatal Rat , 2011, Neuron.

[221]  Qian-Quan Sun,et al.  Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein , 2007, Neuroscience Letters.

[222]  J. Wolff,et al.  Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity , 1984, Neuroscience Letters.

[223]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis , 1983, Journal of neurocytology.

[224]  R. Shigemoto,et al.  GABAB-receptor subtypes assemble into functional heteromeric complexes , 1998, Nature.

[225]  J. Pierri,et al.  Alterations in chandelier neuron axon terminals in the prefrontal cortex of schizophrenic subjects. , 1999, The American journal of psychiatry.

[226]  古塚 大介,et al.  ペンチレンテトラゾール誘発痙攣によるマウス脳Ca^ /calmodulin dependent protein kinase II活性の変化 , 1996 .

[227]  R. Olsen,et al.  Angelman syndrome: Correlations between epilepsy phenotypes and genotypes , 1998, Annals of neurology.

[228]  M. Stryker,et al.  Columnar Architecture Sculpted by GABA Circuits in Developing Cat Visual Cortex , 2004, Science.

[229]  R. Prakash,et al.  Ube3a is required for experience-dependent maturation of the neocortex , 2009, Nature Neuroscience.

[230]  T. Tsumoto,et al.  The Maturation of GABAergic Transmission in Visual Cortex Requires Endocannabinoid-Mediated LTD of Inhibitory Inputs during a Critical Period , 2010, Neuron.

[231]  M. Stewart,et al.  Quantitative morphological effects of dark-rearing and light exposure on the synaptic connectivity of layer 4 in the rat visual cortex (area 17) , 2004, Experimental Brain Research.

[232]  G. Buzsáki,et al.  Early motor activity drives spindle bursts in the developing somatosensory cortex , 2004, Nature.

[233]  G. Blatt,et al.  Decreased GAD67 mRNA levels in cerebellar Purkinje cells in autism: pathophysiological implications , 2007, Acta Neuropathologica.

[234]  A. Sirota,et al.  Early Gamma Oscillations Synchronize Developing Thalamus and Cortex , 2011, Science.

[235]  Nobuko Mataga,et al.  Experience-Dependent Pruning of Dendritic Spines in Visual Cortex by Tissue Plasminogen Activator , 2004, Neuron.

[236]  Michael P. Stryker,et al.  Reversing Neurodevelopmental Disorders in Adults , 2008, Neuron.

[237]  Kari Stefansson,et al.  Association of neuregulin 1 with schizophrenia confirmed in a Scottish population. , 2003, American journal of human genetics.

[238]  A. Kriegstein,et al.  Connexin 43 Mediates the Tangential to Radial Migratory Switch in Ventrally Derived Cortical Interneurons , 2010, The Journal of Neuroscience.

[239]  M. Fagiolini,et al.  Inhibitory threshold for critical-period activation in primary visual cortex , 2000, Nature.