Desynchronization of Neocortical Networks by Asynchronous Release of GABA at Autaptic and Synaptic Contacts from Fast-Spiking Interneurons

An activity-dependent long-lasting asynchronous release of GABA from identified fast-spiking inhibitory neurons in the neocortex can impair the reliability and temporal precision of activity in a cortical network.

[1]  Heinke,et al.  Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons , 2022 .

[2]  Massimo Scanziani,et al.  Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells , 2006, Nature Neuroscience.

[3]  Yuri Zilberter,et al.  Endocannabinoid-Independent Retrograde Signaling at Inhibitory Synapses in Layer 2/3 of Neocortex: Involvement of Vesicular Glutamate Transporter 3 , 2004, The Journal of Neuroscience.

[4]  D. Prince,et al.  Functional Autaptic Neurotransmission in Fast-Spiking Interneurons: A Novel Form of Feedback Inhibition in the Neocortex , 2003, The Journal of Neuroscience.

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

[6]  Y. Kubota,et al.  GABAergic cell subtypes and their synaptic connections in rat frontal cortex. , 1997, Cerebral cortex.

[7]  M. C. Angulo,et al.  Molecular and Physiological Diversity of Cortical Nonpyramidal Cells , 1997, The Journal of Neuroscience.

[8]  L. Palmer,et al.  Response to Contrast of Electrophysiologically Defined Cell Classes in Primary Visual Cortex , 2003, The Journal of Neuroscience.

[9]  Wolf Singer,et al.  Distributed processing and temporal codes in neuronal networks , 2009, Cognitive Neurodynamics.

[10]  G Bard Ermentrout,et al.  Optimal time scale for spike-time reliability: theory, simulations, and experiments. , 2008, Journal of neurophysiology.

[11]  M. Dichter,et al.  Calcium-dependent Paired-pulse Facilitation of Miniature Epsc Frequency Accompanies Depression of Epscs at Hippocampal Synapses in Culture , 1996 .

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

[13]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[15]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[16]  M. Sirota,et al.  Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. , 1998, Journal of neurophysiology.

[17]  T. Südhof,et al.  A dual-Ca2+-sensor model for neurotransmitter release in a central synapse , 2007, Nature.

[18]  W. Regehr,et al.  Delayed Release of Neurotransmitter from Cerebellar Granule Cells , 1998, The Journal of Neuroscience.

[19]  B. Connors,et al.  Two dynamically distinct inhibitory networks in layer 4 of the neocortex. , 2003, Journal of neurophysiology.

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

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

[22]  C D Woody,et al.  Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. II. Membrane parameters, action potentials, current-induced voltage responses and electrotonic structures. , 1993, Journal of neurophysiology.

[23]  Miles A Whittington,et al.  Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro , 2003, Trends in Neurosciences.

[24]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[25]  Stefan Hefft,et al.  Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron–principal neuron synapse , 2005, Nature Neuroscience.

[26]  Lu-Yang Wang,et al.  Developmental Transformation of the Release Modality at the Calyx of Held Synapse , 2005, The Journal of Neuroscience.

[27]  M. Steriade,et al.  Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates. , 2003, Journal of neurophysiology.

[28]  M. Ferrari,et al.  Enhanced Excitatory Transmission at Cortical Synapses as the Basis for Facilitated Spreading Depression in CaV2.1 Knockin Migraine Mice , 2009, Neuron.

[29]  T. Sudhof,et al.  The synaptic vesicle cycle. , 2004, Annual review of neuroscience.

[30]  Gabor Szabo,et al.  Asynchronous Transmitter Release from Cholecystokinin-Containing Inhibitory Interneurons Is Widespread and Target-Cell Independent , 2009, The Journal of Neuroscience.

[31]  Ad Aertsen,et al.  Frontiers in Neural Circuits Neural Circuits Precisely Timed Signal Transmission in Neocortical Networks with Reliable Intermediate-range Projections , 2009 .

[32]  T. Sakaba.  Two Ca2+-Dependent Steps Controlling Synaptic Vesicle Fusion and Replenishment at the Cerebellar Basket Cell Terminal , 2008, Neuron.

[33]  A. Bacci,et al.  Enhancement of Spike-Timing Precision by Autaptic Transmission in Neocortical Inhibitory Interneurons , 2006, Neuron.

[34]  Maria V. Sanchez-Vives,et al.  Influence of low and high frequency inputs on spike timing in visual cortical neurons. , 1997, Cerebral cortex.

[35]  S. Royer,et al.  Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. , 2001, Journal of neurophysiology.

[36]  A. Marty,et al.  Developmental Changes in Parvalbumin Regulate Presynaptic Ca2+ Signaling , 2005, The Journal of Neuroscience.

[37]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Ethan M. Goldberg,et al.  Specific Functions of Synaptically Localized Potassium Channels in Synaptic Transmission at the Neocortical GABAergic Fast-Spiking Cell Synapse , 2005, The Journal of Neuroscience.

[39]  W. Regehr,et al.  Contributions of Residual Calcium to Fast Synaptic Transmission , 1999, The Journal of Neuroscience.

[40]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[41]  C. Davies,et al.  Cholinergic modulation of hippocampal cells and circuits , 2005, The Journal of physiology.

[42]  William M. Connelly,et al.  Modulation and function of the autaptic connections of layer V fast spiking interneurons in the rat neocortex , 2010, The Journal of physiology.

[43]  G. Ermentrout,et al.  Reliability, synchrony and noise , 2008, Trends in Neurosciences.

[44]  I. Módy,et al.  Activation of GABAA Receptors: Views from Outside the Synaptic Cleft , 2007, Neuron.

[45]  Peter Somogyi,et al.  Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro , 2000, The Journal of physiology.

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

[47]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[48]  Suk-Ho Lee,et al.  Kinetics of Ca2+ binding to parvalbumin in bovine chromaffin cells: implications for [Ca2+] transients of neuronal dendrites , 2000, The Journal of physiology.

[49]  Arnd Roth,et al.  Submillisecond AMPA Receptor-Mediated Signaling at a Principal Neuron–Interneuron Synapse , 1997, Neuron.

[50]  L. Trussell,et al.  Inhibitory Transmission Mediated by Asynchronous Transmitter Release , 2000, Neuron.

[51]  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.

[52]  C. Pouzat,et al.  Somatic Recording of GABAergic Autoreceptor Current in Cerebellar Stellate and Basket Cells , 1999, The Journal of Neuroscience.

[53]  Takeshi Sakaba,et al.  Roles of the Fast-Releasing and the Slowly Releasing Vesicles in Synaptic Transmission at the Calyx of Held , 2006, The Journal of Neuroscience.

[54]  Ian Duguid,et al.  Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron–Purkinje cell synapses , 2004, Nature Neuroscience.

[55]  C D Woody,et al.  Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. I. Patterns of firing activity and synaptic responses. , 1993, Journal of neurophysiology.

[56]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[57]  D. Prince,et al.  Major Differences in Inhibitory Synaptic Transmission onto Two Neocortical Interneuron Subclasses , 2003, The Journal of Neuroscience.

[58]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[59]  Pankaj Sah,et al.  Ca2+-activated K+ currents in neurones: types, physiological roles and modulation , 1996, Trends in Neurosciences.

[60]  J R Huguenard,et al.  GABAB receptor‐mediated responses in GABAergic projection neurones of rat nucleus reticularis thalami in vitro. , 1996, The Journal of physiology.

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

[62]  Gábor Szabó,et al.  Cannabinoid sensitivity and synaptic properties of 2 GABAergic networks in the neocortex. , 2008, Cerebral cortex.

[63]  H. Markram,et al.  Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. , 2002, Cerebral cortex.

[64]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[65]  E. Neher,et al.  Kinetics of both synchronous and asynchronous quantal release during trains of action potential‐evoked EPSCs at the rat calyx of Held , 2007, The Journal of physiology.

[66]  P. Somogyi,et al.  Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus , 1997, Neuroscience.

[67]  O. Caillard,et al.  Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[68]  G. Vrbóva,et al.  Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. , 1999, American journal of physiology. Cell physiology.

[69]  M. Frotscher,et al.  Nanodomain Coupling between Ca2+ Channels and Ca2+ Sensors Promotes Fast and Efficient Transmitter Release at a Cortical GABAergic Synapse , 2008, Neuron.

[70]  P. Somogyi,et al.  Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex , 1997, The Journal of Neuroscience.

[71]  D. Hagler,et al.  Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. , 2001, Journal of neurophysiology.

[72]  P. Jonas,et al.  Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates , 2006, Neuron.

[73]  Xiaoqin Wang,et al.  Temporal and rate representations of time-varying signals in the auditory cortex of awake primates , 2001, Nature Neuroscience.

[74]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[75]  M. Steriade,et al.  The role of chloride-dependent inhibition and the activity of fast-spiking neurons during cortical spike–wave electrographic seizures , 2002, Neuroscience.

[76]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

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

[78]  M. Stocker.  Ca2+-activated K+ channels: molecular determinants and function of the SK family , 2004, Nature Reviews Neuroscience.

[79]  J. Huguenard,et al.  Inhibitory Interconnections Control Burst Pattern and Emergent Network Synchrony in Reticular Thalamus , 2003, The Journal of Neuroscience.

[80]  Richard Miles,et al.  EPSP Amplification and the Precision of Spike Timing in Hippocampal Neurons , 2000, Neuron.

[81]  S. Kirischuk,et al.  Intraterminal Ca2+ concentration and asynchronous transmitter release at single GABAergic boutons in rat collicular cultures , 2003, The Journal of physiology.

[82]  Tamás F Freund,et al.  Interneuron Diversity series: Rhythm and mood in perisomatic inhibition , 2003, Trends in Neurosciences.

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

[84]  Jiandie D. Lin,et al.  Parvalbumin Deficiency and GABAergic Dysfunction in Mice Lacking PGC-1α , 2010, The Journal of Neuroscience.

[85]  R. Miles,et al.  Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea‐pig in vitro. , 1990, The Journal of physiology.

[86]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[87]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[88]  F. Dudek,et al.  Intracellular correlates of fast (>200 Hz) electrical oscillations in rat somatosensory cortex. , 2000, Journal of neurophysiology.

[89]  J. Bains,et al.  Integration of Asynchronously Released Quanta Prolongs the Postsynaptic Spike Window , 2007, The Journal of Neuroscience.