Localized GABAergic inhibition of dendritic Ca2+ signalling

Neuronal circuits are defined by synaptic connections between their cellular constituents. In this article, I highlight several recent studies emphasizing the surprising level of precision exhibited by inhibitory GABAergic synapses within the neocortex and hippocampus. Specifically, GABAergic inputs to dendritic shafts and spines of pyramidal cells have a key role in the localized regulation of neuronal Ca2+ signalling. These findings provide important new insights into the cellular mechanisms underlying the contributions of inhibitory transmission to both normal and abnormal brain activity.

[1]  C. Aoki,et al.  Knockout of the γ-aminobutyric acid receptor subunit α4 reduces functional δ-containing extrasynaptic receptors in hippocampal pyramidal cells at the onset of puberty , 2012, Brain Research.

[2]  M. Larkum,et al.  NMDA spikes enhance action potential generation during sensory input , 2014, Nature Neuroscience.

[3]  J. Ruppersberg.  Ion Channels in Excitable Membranes , 1996 .

[4]  A. Losonczy,et al.  Regulation of neuronal input transformations by tunable dendritic inhibition , 2012, Nature Neuroscience.

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

[6]  W. Denk,et al.  Two types of calcium response limited to single spines in cerebellar Purkinje cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Massimo Scanziani,et al.  Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex , 2007, Nature Neuroscience.

[8]  Adam G. Carter,et al.  GABAB receptor modulation of synaptic function , 2011, Current Opinion in Neurobiology.

[9]  Lewis D. Griffin,et al.  NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the γ2 subunit , 2010, Proceedings of the National Academy of Sciences.

[10]  P. Somogyi,et al.  Salient features of synaptic organisation in the cerebral cortex 1 Published on the World Wide Web on 3 March 1998. 1 , 1998, Brain Research Reviews.

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

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

[13]  J. Magee,et al.  Integrative Properties of Radial Oblique Dendrites in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[14]  H. Markram,et al.  Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells , 2007, Neuron.

[15]  W. N. Ross,et al.  IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons. , 1996, Journal of neurophysiology.

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

[17]  Hans R. Gelderblom,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001 .

[18]  W. Senn,et al.  Dendritic encoding of sensory stimuli controlled by deep cortical interneurons , 2009, Nature.

[19]  Edward O. Mann,et al.  Role of GABAergic inhibition in hippocampal network oscillations , 2007, Trends in Neurosciences.

[20]  T J Sejnowski,et al.  When is an inhibitory synapse effective? , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[21]  C. Hölscher.  Synaptic plasticity and learning and memory: LTP and beyond , 1999, Journal of neuroscience research.

[22]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[23]  J. Schiller,et al.  Active properties of neocortical pyramidal neuron dendrites. , 2013, Annual review of neuroscience.

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

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

[26]  Bernardo L. Sabatini,et al.  Competitive regulation of synaptic Ca influx by D2 dopamine and A2A adenosine receptors , 2010, Nature Neuroscience.

[27]  Jun Noguchi,et al.  Spatial Distributions of GABA Receptors and Local Inhibition of Ca2+ Transients Studied with GABA Uncaging in the Dendrites of CA1 Pyramidal Neurons , 2011, PloS one.

[28]  P. Somogyi,et al.  Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. , 1997, The Journal of physiology.

[29]  Antonius M. J. VanDongen,et al.  Biology of the NMDA receptor , 2008 .

[30]  M. Scanziani,et al.  How Inhibition Shapes Cortical Activity , 2011, Neuron.

[31]  Adam G. Carter,et al.  GABAB Receptors Modulate NMDA Receptor Calcium Signals in Dendritic Spines , 2010, Neuron.

[32]  Satoru Kondo,et al.  Neocortical Inhibitory Terminals Innervate Dendritic Spines Targeted by Thalamocortical Afferents , 2007, The Journal of Neuroscience.

[33]  P. Slesinger,et al.  GABAB receptor coupling to G-proteins and ion channels. , 2010, Advances in pharmacology.

[34]  Mark T. Harnett,et al.  Nonlinear dendritic integration of sensory and motor input during an active sensing task , 2012, Nature.

[35]  Meng Zhang,et al.  ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation , 2010, Proceedings of the National Academy of Sciences.

[36]  H. Taniguchi,et al.  The Spatial and Temporal Origin of Chandelier Cells in Mouse Neocortex , 2013, Science.

[37]  G. Fishell,et al.  Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons , 2011, Developmental neurobiology.

[38]  D. Contreras,et al.  Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation , 2006, The Journal of Neuroscience.

[39]  H. Markram,et al.  Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat , 2004, The Journal of physiology.

[40]  A. D. De Blas,et al.  Synaptic and nonsynaptic localization of GABAA receptors containing the α5 subunit in the rat brain , 2006 .

[41]  Rafael Yuste,et al.  Protein kinase A regulates calcium permeability of NMDA receptors , 2006, Nature Neuroscience.

[42]  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.

[43]  Rafael Yuste,et al.  Electrical compartmentalization in dendritic spines. , 2013, Annual review of neuroscience.

[44]  Mark Farrant,et al.  Regulation of Ca2+-permeable AMPA receptors: synaptic plasticity and beyond , 2006, Current Opinion in Neurobiology.

[45]  Bernardo L Sabatini,et al.  Anatomical and physiological plasticity of dendritic spines. , 2007, Annual review of neuroscience.

[46]  E. Callaway,et al.  Immunochemical characterization of inhibitory mouse cortical neurons: Three chemically distinct classes of inhibitory cells , 2010, The Journal of comparative neurology.

[47]  Bernardo L Sabatini,et al.  Phosphorylation of Ser1166 on GluN2B by PKA Is Critical to Synaptic NMDA Receptor Function and Ca2+ Signaling in Spines , 2014, The Journal of Neuroscience.

[48]  T. Bonhoeffer,et al.  Molecular and Electrophysiological Characterization of GFP-Expressing CA1 Interneurons in GAD65-GFP Mice , 2010, PloS one.

[49]  O. Paulsen,et al.  Maturation of Long-Term Potentiation Induction Rules in Rodent Hippocampus: Role of GABAergic Inhibition , 2003, The Journal of Neuroscience.

[50]  A. Fairén,et al.  Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development , 2004, Hippocampus.

[51]  Adriano B. L. Tort,et al.  OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons , 2012, Nature Neuroscience.

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

[53]  Z. J. Huang,et al.  Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules , 2006, Nature Neuroscience.

[54]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[55]  Rafael Yuste,et al.  Nanotools for neuroscience and brain activity mapping. , 2013, ACS nano.

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

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

[58]  B. Rudy,et al.  Perisomatic GABA Release and Thalamocortical Integration onto Neocortical Excitatory Cells Are Regulated by Neuromodulators , 2008, Neuron.

[59]  L. Sivilotti,et al.  GABA receptor mechanisms in the central nervous system , 1991, Progress in Neurobiology.

[60]  Jackie Schiller,et al.  Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo , 2012, Nature.

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

[62]  B. Sabatini,et al.  Calcium Signaling in Dendrites and Spines: Practical and Functional Considerations , 2008, Neuron.

[63]  T. Hashimoto,et al.  Deciphering the disease process of schizophrenia: the contribution of cortical GABA neurons. , 2007, International review of neurobiology.

[64]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[65]  Adam G. Carter,et al.  GABAB Receptor Modulation of Voltage-Sensitive Calcium Channels in Spines and Dendrites , 2011, The Journal of Neuroscience.