Glutamate Release Monitored with Astrocyte Transporter Currents during LTP

Long-term potentiation (LTP) of synaptic transmission in the CA1 region of the hippocampus is thought to result from either increased transmitter release, heightened postsynaptic sensitivity, or a combination of the two. We have measured evoked glutamate release from Schaffer collateral/commissural fiber terminals in CA1 by recording synaptically activated glutamate transporter currents in hippocampal astrocytes located in stratum radiatum. Although several manipulations of release probability caused parallel changes in extracellular field potentials and synaptically activated transporter current amplitudes, induction of LTP failed to alter transporter-mediated responses, suggesting that LTP does not alter the amount of glutamate released upon synaptic stimulation.

[1]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[2]  Y. Yaari,et al.  Kinetic properties of NMDA receptor‐mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. , 1993, The Journal of physiology.

[3]  Dimitri M. Kullmann,et al.  The site of expression of NMDA receptor-dependent LTP: New fuel for an old fire , 1995, Neuron.

[4]  B. Clark,et al.  Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices , 1997, The Journal of physiology.

[5]  R. Zucker,et al.  Exocytosis: A Molecular and Physiological Perspective , 1996, Neuron.

[6]  C. Jahr,et al.  Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. , 1997, Science.

[7]  E. Kandel,et al.  Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  K. P. Lehre,et al.  Arachidonic Acid Inhibits a Purified and Reconstituted Glutamate Transporter Directly from the Water Phase and Not via the Phospholipid Membrane (*) , 1995, The Journal of Biological Chemistry.

[9]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[10]  D. Kullmann,et al.  Extrasynaptic Glutamate Spillover in the Hippocampus: Dependence on Temperature and the Role of Active Glutamate Uptake , 1997, Neuron.

[11]  M. Kavanaugh,et al.  Differential Modulation of Human Glutamate Transporter Subtypes by Arachidonic Acid (*) , 1995, The Journal of Biological Chemistry.

[12]  C. Jahr,et al.  Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Garthwaite,et al.  Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain , 1988, Nature.

[14]  L. Voronin,et al.  Long-term potentiation in the hippocampus , 1983, Neuroscience.

[15]  H. Shinozaki,et al.  Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. , 1996, The Journal of physiology.

[16]  Steven Mennerick,et al.  Glial contributions to excitatory neurotransmission in cultured hippocampal cells , 1994, Nature.

[17]  T. Bliss,et al.  An in vitro study of the effect of lipoxygenase and cyclo-oxygenase inhibitors of arachidonic acid on the induction and maintenance of long-term potentiation in the hippocampus , 1989, Neuroscience Letters.

[18]  U. Förstermann,et al.  Mechanisms of action of lipoxygenase and cytochrome P‐450‐mono‐oxygenase inhibitors in blocking endothelium‐dependent vasodilatation , 1988, British journal of pharmacology.

[19]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[20]  M. Kavanaugh,et al.  An excitatory amino-acid transporter with properties of a ligand-gated chloride channel , 1995, Nature.

[21]  Paul Antoine Salin,et al.  Distinct short-term plasticity at two excitatory synapses in the hippocampus. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[22]  A. Konnerth,et al.  Long-term potentiation and functional synapse induction in developing hippocampus , 1996, Nature.

[23]  D. Attwell,et al.  Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells , 1987, Nature.

[24]  CE Jahr,et al.  NMDA channel behavior depends on agonist affinity , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Dimitri M Kullmann,et al.  LTP of AMPA and NMDA Receptor–Mediated Signals: Evidence for Presynaptic Expression and Extrasynaptic Glutamate Spill-Over , 1996, Neuron.

[26]  K. Tóth,et al.  Target-specific expression of presynaptic mossy fiber plasticity. , 1998, Science.

[27]  M. Kavanaugh,et al.  Ion fluxes associated with excitatory amino acid transport , 1995, Neuron.

[28]  C. Jahr,et al.  Synaptic Activation of Glutamate Transporters in Hippocampal Astrocytes , 1997, Neuron.

[29]  R. Nicoll,et al.  Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. , 1993, Journal of neurophysiology.

[30]  J. Storm-Mathisen,et al.  Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  L. W. Leung,et al.  Field Potentials in the Central Nervous System , 1990 .

[32]  K. Harris,et al.  Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. Linden,et al.  Long-Term Potentiation of Glial Synaptic Currents in Cerebellar Culture , 1997, Neuron.

[34]  J. Bockaert,et al.  NMDA receptors activate the arachidonic acid cascade system in striatal neurons , 1988, Nature.

[35]  T. Bliss,et al.  Nordihydroguaiaretic acid blocks the synaptic component of long-term potentiation and the associated increases in release of glutamate and arachidonate: An in vivo study in the dentate gyrus of the rat , 1989, Neuroscience.

[36]  D. Kullmann.  Amplitude fluctuations of , 1994, Neuron.

[37]  C. Zorumski,et al.  Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  R. Nicoll,et al.  Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. , 1994, Science.

[39]  T. Kosaka,et al.  Three‐dimensional structure of astrocytes in the rat dentate gyrus , 1986, The Journal of comparative neurology.

[40]  M. Kuhar,et al.  Nitric oxide inhibits 3H‐glutamate transport in synaptosomes , 1994, Synapse.

[41]  A. Levey,et al.  Localization of neuronal and glial glutamate transporters , 1994, Neuron.

[42]  R. Nicoll,et al.  Contrasting properties of two forms of long-term potentiation in the hippocampus , 1995, Nature.

[43]  M. Hediger,et al.  Knockout of Glutamate Transporters Reveals a Major Role for Astroglial Transport in Excitotoxicity and Clearance of Glutamate , 1996, Neuron.

[44]  Masahiko Watanabe,et al.  Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. , 1997, Science.

[45]  D. Attwell,et al.  Arachidonic acid induces a prolonged inhibition of glutamate uptake into glial cells , 1989, Nature.

[46]  C. Jahr,et al.  Retinal glial cell glutamate transporter is coupled to an anionic conductance. , 1996, Proceedings of the National Academy of Sciences of the United States of America.