Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons

Spontaneous excitatory postsynaptic currents (sEPSCs) and responses to rapid application of glutamate were recorded in excitatory spiny, pyramidal neurons and compared with those recorded in inhibitory aspiny interneurons. The sEPSC decay time constant was faster in aspiny interneurons (2.5 ms) compared with pyramidal neurons (4.6 ms). The decay time constant in response to a brief application (1 ms) of glutamate (10 mM) in patches excised from pyramidal and aspiny interneurons were similar (1.9 and 2.7 ms, respectively). However, the rate of desensitization was faster in patches from interneurons compared with pyramidal neurons (3.4 and 12.0 ms, respectively). In addition, single-channel conductance was larger in aspiny interneurons (27 pS) compared with pyramidal neurons (9 pS). These results indicate that pyramidal neurons and aspiny interneurons express different non-N-methyl-D-aspartate receptors and that selective desensitization of interneuron receptors may contribute to depression of inhibition.

[1]  S. Vicini,et al.  Slower spontaneous excitatory postsynaptic currents in spiny versus aspiny hilar neurons , 1992, Neuron.

[2]  H. Hatt,et al.  Rapid activation, desensitization, and resensitization of synaptic channels of crayfish muscle after glutamate pulses. , 1990, Biophysical journal.

[3]  R. Petralia,et al.  Light and electron immunocytochemical localization of AMPA‐selective glutamate receptors in the rat brain , 1992, The Journal of comparative neurology.

[4]  S. Kelso,et al.  Activity‐induced decreased in early and late inhibitory synaptic conductances in hippocampus , 1991, Synapse.

[5]  D. Clifford,et al.  Wheat germ agglutinin enhances EPSCs in cultured postnatal rat hippocampal neurons by blocking ionotropic quisqualate receptor desensitization. , 1992, Journal of neurophysiology.

[6]  Arnold R. Kriegstein,et al.  Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex , 1989, Journal of Neuroscience Methods.

[7]  L. Trussell,et al.  Desensitization of AMPA receptors upon multiquantal neurotransmitter release , 1993, Neuron.

[8]  E. White.  Cortical Circuits: Synaptic Organization of the Cerebral Cortex , 1989 .

[9]  E. Costa,et al.  Glutamate-activated currents in outside-out patches from spiny versus aspiny hilar neurons of rat hippocampal slices , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  RW Baughman,et al.  The pharmacology of synapses formed by identified corticocollicular neurons in primary cultures of rat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. E. Huettner.  Glutamate receptor channels in rat DRG neurons: Activation by kainate and quisqualate and blockade of desensitization by con A , 1990, Neuron.

[12]  D. Prince,et al.  Frequency‐dependent depression of inhibition in guinea‐pig neocortex in vitro by GABAB receptor feed‐back on GABA release. , 1989, The Journal of physiology.

[13]  R. Dingledine,et al.  Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. , 1993, The Journal of physiology.

[14]  M. Mayer,et al.  Modulation of excitatory synaptic transmission by drugs that reduce desensitization at AMPA/kainate receptors , 1991, Neuron.

[15]  Y. Ben-Ari,et al.  Hippocampal seizures and failure of inhibition , 1979 .

[16]  P. Seeburg,et al.  Mammalian ionotropic glutamate receptors , 1993, Current Opinion in Neurobiology.

[17]  R. Scobey,et al.  Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. , 1991, Science.

[18]  B. Gähwiler,et al.  Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. , 1989, Journal of neurophysiology.

[19]  M. Dichter,et al.  Quisqualate activates a rapidly inactivating high conductance ionic channel in hippocampal neurons. , 1989, Science.

[20]  J. Morrison,et al.  Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  S. Ozawa,et al.  Two types of kainate response in cultured rat hippocampal neurons. , 1991, Journal of neurophysiology.

[22]  K. A. Yamada,et al.  Diazoxide blocks glutamate desensitization and prolongs excitatory postsynaptic currents in rat hippocampal neurons. , 1992, The Journal of physiology.

[23]  G. Lynch,et al.  Modulation of the time course of fast EPSCs and glutamate channel kinetics by aniracetam. , 1991, Science.

[24]  S N Davies,et al.  Paired‐pulse depression of monosynaptic GABA‐mediated inhibitory postsynaptic responses in rat hippocampus. , 1990, The Journal of physiology.

[25]  Y. Kawaguchi,et al.  Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. , 1993, Journal of neurophysiology.

[26]  B. Sakmann,et al.  Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. , 1992, The Journal of physiology.

[27]  B. Sakmann,et al.  Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. , 1992, The Journal of physiology.

[28]  G. Westbrook,et al.  The time course of glutamate in the synaptic cleft. , 1992, Science.

[29]  M. Rogawski,et al.  GYKI 52466, a 2,3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses , 1993, Neuron.

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

[31]  B. Sakmann,et al.  A family of AMPA-selective glutamate receptors. , 1990, Science.

[32]  P. Somogyi,et al.  Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit: Cellular and subcellular distribution in the rat forebrain , 1993, Neuroscience.

[33]  R. Huganir,et al.  AMPA glutamate receptor subunits are differentially distributed in rat brain , 1993, Neuroscience.

[34]  M. Mayer,et al.  Kinetic analysis of interactions between kainate and AMPA: Evidence for activation of a single receptor in mouse hippocampal neurons , 1991, Neuron.

[35]  H. Hatt,et al.  Liquid filament switch for ultra-fast exchanges of solutions at excised patches of synaptic membrane of crayfish muscle , 1987, Neuroscience Letters.

[36]  B. Alger,et al.  Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro. , 1985, Journal of neurophysiology.

[37]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[38]  R. Nicoll,et al.  Aniracetam reduces glutamate receptor desensitization and slows the decay of fast excitatory synaptic currents in the hippocampus. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[39]  D. Wyllie,et al.  Evidence for more than one type of non‐NMDA receptor in outside‐out patches from cerebellar granule cells of the rat. , 1993, The Journal of physiology.

[40]  A. Peters,et al.  The neuronal composition of area 17 of rat visual cortex. I. The pyramidal cells , 1985, The Journal of comparative neurology.

[41]  F. Sigworth.  The variance of sodium current fluctuations at the node of Ranvier , 1980, The Journal of physiology.

[42]  L. Trussell,et al.  Glutamate receptor desensitization and its role in synaptic transmission , 1989, Neuron.

[43]  S. Heinemann,et al.  The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  B Sakmann,et al.  Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. , 1992, The Journal of physiology.

[45]  Shaul Hestrin,et al.  Activation and desensitization of glutamate-activated channels mediating fast excitatory synaptic currents in the visual cortex , 1992, Neuron.