Horizontal spread of activity in neocortical inhibitory networks.

In the presence of 4-aminopyridine (4-AP) and excitatory amino acid receptor blockers, GABAergic networks in the neocortex give rise to large spontaneous GABA-mediated depolarizations. We used voltage-sensitive dye techniques to explore the network properties of depolarizing GABA responses. Voltage-sensitive dye signals demonstrated that the superficial layers support the propagation of depolarizing GABA responses, with only minimal signals detected in deeper cortical layers. GABA responses propagated at a speed of 2.7 +/- 0.2 mm/s, a rate intermediate to fast synaptic transmission and spreading depression. Changes in the extracellular potassium concentration altered the propagation speed of the depolarizing GABA response. Taken together, these data support a role for both direct synaptic action of GABA at GABA(A) receptors and nonsynaptic mechanisms in the generation and propagation of depolarizing GABA responses.

[1]  R. Traub,et al.  Synaptic and nonsynaptic contributions to giant ipsps and ectopic spikes induced by 4-aminopyridine in the hippocampus in vitro. , 2001, Journal of neurophysiology.

[2]  U. Eysel,et al.  Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition , 1993, The Journal of comparative neurology.

[3]  M. Gutnick,et al.  Non-uniform propagation of epileptiform discharge in brain slices of rat neocortex , 1993, Neuroscience.

[4]  B H Gähwiler,et al.  Activity-dependent disinhibition. III. Desensitization and GABAB receptor-mediated presynaptic inhibition in the hippocampus in vitro. , 1989, Journal of neurophysiology.

[5]  K. Staley,et al.  Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors , 1995, Science.

[6]  R. Frostig,et al.  Optical imaging of neuronal activity. , 1988, Physiological reviews.

[7]  Christoph Baumgartner,et al.  Laminar interactions in rat motor cortex during cyclical excitability changes of the penicillin focus , 1990, Brain Research.

[8]  M. Avoli,et al.  4-aminopyridine-induced epileptiform activity and a GABA-mediated long- lasting depolarization in the rat hippocampus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  B. Connors,et al.  Laminar origins of inhibitory synaptic inputs to pyramidal neurons of the rat neocortex. , 1996, The Journal of physiology.

[10]  F. Zhou,et al.  Morphological properties of intracellularly labeled layer I neurons in rat neocortex , 1996, The Journal of comparative neurology.

[11]  J. Hablitz,et al.  Spread of epileptiform activity in the immature rat neocortex studied with voltage-sensitive dyes and laser scanning microscopy. , 1994, Journal of neurophysiology.

[12]  D. Mattia,et al.  Pharmacology and electrophysiology of a synchronous gaba-mediated potential in the human neocortex , 1994, Neuroscience.

[13]  K. Staley,et al.  Modulation of mammalian dendritic GABAA receptor function by the kinetics of Cl− and HCO3− transport , 1999, The Journal of physiology.

[14]  L. Benardo,et al.  Laminar properties of 4-aminopyridine-induced synchronous network activities in rat neocortex , 2002, Neuroscience.

[15]  J. Hablitz,et al.  Potassium-Coupled Chloride Cotransport Controls Intracellular Chloride in Rat Neocortical Pyramidal Neurons , 2000, The Journal of Neuroscience.

[16]  P. Saggau,et al.  Imaging of 4-AP-induced, GABA(A)-dependent spontaneous synchronized activity mediated by the hippocampal interneuron network. , 2001, Journal of neurophysiology.

[17]  S. Hestrin,et al.  Synaptic Interactions of Late-Spiking Neocortical Neurons in Layer 1 , 2003, The Journal of Neuroscience.

[18]  Y. Kubota,et al.  Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex , 1998, Neuroscience.

[19]  Y. Kawaguchi.  Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Huguenard,et al.  Whole-cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons. , 1986, Journal of neurophysiology.

[21]  W. Chen,et al.  Different mechanisms underlying the repolarization of narrow and wide action potentials in pyramidal cells and interneurons of cat motor cortex , 1996, Neuroscience.

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

[23]  R. Llinás,et al.  Synaptic transmission in squid giant synapse after potassium conductance blockage with external 3- and 4-aminopyridine. , 1976, Biophysical journal.

[24]  Lie Yang,et al.  Removal of superficial inhibition releases hyperexcitability in middle and deep horizontal slices from rat somatosensory neocortex , 1998, Neuroscience Letters.

[25]  S. Hestrin,et al.  Morphology and Physiology of Cortical Neurons in Layer I , 1996, The Journal of Neuroscience.

[26]  B. Connors,et al.  Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. , 1989, Journal of neurophysiology.

[27]  A Lücke,et al.  Synchronous GABA-Mediated Potentials and Epileptiform Discharges in the Rat Limbic System In Vitro , 1996, The Journal of Neuroscience.

[28]  M. Avoli,et al.  GABA-mediated synchronization in the human neocortex: elevations in extracellular potassium and presynaptic mechanisms , 2001, Neuroscience.

[29]  Synchronized GABAergic IPSPs recorded in the neocortex after blockade of synaptic transmission mediated by excitatory amino acids. , 1991, Journal of neurophysiology.

[30]  K. L. Perkins.  Cl- accumulation does not account for the depolarizing phase of the synaptic GABA response in hippocampal pyramidal cells. , 1999, Journal of neurophysiology.

[31]  Serge Charpak,et al.  Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. , 2002, Journal of neurophysiology.

[32]  M. Avoli,et al.  Reverberation of chloride-dependent synaptic potentials in the rat entorhinal cortex in vitro , 1996, Neuroscience Letters.

[33]  H. Michelson,et al.  Gap junctions synchronize the firing of inhibitory interneurons in guinea pig hippocampus , 2001, Brain Research.

[34]  A. Konnerth,et al.  Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity , 1998, Progress in Neurobiology.

[35]  J. van Brederode,et al.  Differences in inhibitory synaptic input between layer II-III and layer V neurons of the cat neocortex. , 1995, Journal of neurophysiology.

[36]  B. Connors,et al.  A network of electrically coupled interneurons drives synchronized inhibition in neocortex , 2000, Nature Neuroscience.

[37]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[38]  U. Kuhnt,et al.  Optical recording of epileptiform voltage changes in the neocortical slice , 2004, Experimental Brain Research.

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

[40]  B. Sakmann,et al.  Mechanism of anion permeation through channels gated by glycine and gamma‐aminobutyric acid in mouse cultured spinal neurones. , 1987, The Journal of physiology.

[41]  J. Hablitz,et al.  Ectopic action potential generation in cortical interneurons during synchronized GABA responses , 2005, Neuroscience.

[42]  B. Connors.  Initiation of synchronized neuronal bursting in neocortex , 1984, Nature.

[43]  M. Avoli,et al.  GABA‐dependent generation of ectopic action potentials in the rat hippocampus , 1998, The European journal of neuroscience.

[44]  M. Gutnick,et al.  Laminar pattern of synaptic inhibition during convulsive activity induced by 4-aminopyridine in neocortical slices. , 1995, Journal of neurophysiology.

[45]  J. Hablitz,et al.  Excitability changes in freeze-induced neocortical microgyria , 1998, Epilepsy Research.

[46]  D. Nicholls,et al.  Repetitive Action Potentials in Isolated Nerve Terminals in the Presence of 4‐Aminopyridine: Effects on Cytosolic Free Ca2+ and Glutamate Release , 1989, Journal of neurochemistry.

[47]  J. Voipio,et al.  Long-Lasting GABA-Mediated Depolarization Evoked by High-Frequency Stimulation in Pyramidal Neurons of Rat Hippocampal Slice Is Attributable to a Network-Driven, Bicarbonate-Dependent K+ Transient , 1997, The Journal of Neuroscience.

[48]  P. Somogyi,et al.  Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat , 1998, The Journal of Neuroscience.

[49]  S. Peterson,et al.  Muscarinic Receptors Mediate Carbachol‐Induced Inhibition of Maximal Electroshock Seizures in the Nucleus Reticularis Pontis Oralis , 1999, Epilepsia.

[50]  R. Traub,et al.  Neuronal networks for induced ‘40 Hz’ rhythms , 1996, Trends in Neurosciences.

[51]  L. Benardo,et al.  Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. , 1997, Journal of neurophysiology.

[52]  K. Kaila,et al.  Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. , 1997, Journal of neurophysiology.

[53]  Y. Kubota,et al.  Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex , 1994, Brain Research.

[54]  B. Connors,et al.  Periodicity and directionality in the propagation of epileptiform discharges across neocortex. , 1988, Journal of neurophysiology.

[55]  R. Wong,et al.  Ionic basis of the postsynaptic depolarizing GABA response in hippocampal pyramidal cells. , 1996, Journal of neurophysiology.