Glutamate-Mediated Synaptic Excitation of Cortical Interneurons

  • J. R. P. Geiger
  • A. Roth
  • B. Taskin
  • P. Jonas
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 141)


Principal neurons and interneurons are the two main classes of cells in cortical neuronal networks. Principal neurons (granule cells or pyramidal neurons) have transregional axonal projections and release glutamate onto their postsynaptic target cells. In contrast, interneurons have local, but often extensive, axonal arborizations and use γ-aminobutyric acid (GABA) as a transmitter. Although interneurons represent only approximately 10% of the neuronal population, they control the electrical activity of the entire network (Freund and Buzsáki 1996). Interneurons forming inhibitory synapses on the somata or axon initial segments of their postsynaptic target cells are thought to set the threshold of action potential initiation (Miles et al. 1996) and can synchronize the collective activities of large principal neuron ensembles (Cobb et al. 1995). In contrast, interneurons establishing inhibitory synapses mainly on dendrites could suppress dendritic Na+ or Ca2+ spikes (Buzsáki et al. 1996; Miles et al. 1996) and, thus, regulate plasticity at glutamatergic synapses in the cortex (Davies et al. 1991).


Metabotropic Glutamate Receptor Basket Cell Principal Neuron Cortical Interneuron Outer Molecular Layer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



trans-1-aminocyclopentane-1,3-dicarboxylic acid


α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors




Central nervous system


Diffusion coefficient for glutamate


Excitatory postsynaptic current


Excitatory postsynaptic potential


-aminobutyric acid


Hilar—commissural-association pathway


Hilar—perforant path


Kainate receptors


Long-term depression


Long-term potentiation


Metabotropic glutamate receptors


α-methyl-4-carboxyphenyl glycine


Molecular layer—perforant path


N-methyl-D-aspartate receptors


Oriens-alveus—lacunosum moleculare


Outer molecular layer


Paired-pulse depression


Paired-pulse facilitation


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  1. Acsâdy L, Kamondi A, Szk A, Freund T, Buzsâki G (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18: 3386–3403PubMedGoogle Scholar
  2. Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol (Lond) 507: 185–199CrossRefGoogle Scholar
  3. Ali AB, Deuchars J, Pawelzik H, Thomson AM (1998) CAl pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J Physiol (Lond) 507: 201–217CrossRefGoogle Scholar
  4. Angulo MC, Lambolez B, Audinat E, Hestrin S, Rossier J (1997) Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical non-pyramidal cells. J Neurosci 17: 6685–6696PubMedGoogle Scholar
  5. Bahn S, Volk B, Wisden W (1994) Kainate receptor gene expression in the developing rat brain. J Neurosci 14: 5525–5547PubMedGoogle Scholar
  6. Barbour B, Keller BU, Llano I, Marty A (1994) Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron 12: 1331–1343PubMedCrossRefGoogle Scholar
  7. Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends in Neurosci 20: 377–384CrossRefGoogle Scholar
  8. Bartol TM, Land BR, Salpeter EE, Salpeter MM (1991) Monte Carlo simulation of miniature endplate current generation in the vertebrate neuromuscular junction. Biophys J 59: 1290–1307PubMedCrossRefGoogle Scholar
  9. Baude A, Nusser Z, Roberts JDB, Mulvihill E, McIlhinney RAJ, Somogyi P (1993) The metabotropic glutamate receptor (mGluRl a) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11: 771–787PubMedCrossRefGoogle Scholar
  10. Baude A, Nusser Z, Molnar E, McIlhinney RAJ, Somogyi P (1995) High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69: 1031–1055PubMedCrossRefGoogle Scholar
  11. Blasco-Ibâfiez JM, Freund TF (1995) Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CAl subfield: Structural basis of feed-back activation. Eur J Neurosci 7: 2170–2180Google Scholar
  12. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39PubMedCrossRefGoogle Scholar
  13. Bochet P, Audinat E, Lambolez B, Crépel F, Rossier J, lino M, Tsuzuki K, Ozawa S (1994) Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel. Neuron 12: 383–388PubMedCrossRefGoogle Scholar
  14. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368: 823–828PubMedCrossRefGoogle Scholar
  15. Buhl EH, Tamâs G, Szilâgyi T, Stricker C, Paulsen O, Somogyi P (1997) Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. J Physiol (Lond) 500: 689–713Google Scholar
  16. Buzsâki G, Penttonen M, Nâdasdy Z, Bragin A (1996) Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc Natl Acad Sci USA 93: 9921–9925PubMedCrossRefGoogle Scholar
  17. Ceranik K, Bender R, Geiger JRP, Monyer H, Jonas P, Frotscher M, Lübke J (1997) A novel type of GABAergic interneuron connecting the input and the output regions of the hippocampus. J Neurosci 17: 5380–5394PubMedGoogle Scholar
  18. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75–78PubMedCrossRefGoogle Scholar
  19. Colquhoun D, Jonas P, Sakmann B (1992) Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. J Physiol (Lond) 458: 261–287Google Scholar
  20. Congar P, Khazipov R, Ben-Ari Y (1995) Direct demonstration of functional disconnection by anoxia of inhibitory interneurons from excitatory inputs in rat hippocampus. J Neurophysiol 73: 421–426PubMedGoogle Scholar
  21. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) G1uR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nature Neurosci 1: 470–478PubMedCrossRefGoogle Scholar
  22. Cowan AI, Stricker C, Reece LJ, Redman SJ (1998) Long-term plasticity at excitatory synapses on aspinous interneurons in area CAl lacks synaptic specificity. J Neurophysiol 79: 13–20PubMedGoogle Scholar
  23. Csicsvari J, Hirase H, Czurko A, Buzsâki G (1998) Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21: 179–189PubMedCrossRefGoogle Scholar
  24. Datyner NB, Gage PW (1980) Phasic secretion of acetylcholine at a mammalian neuromuscular junction. J Physiol (Lond) 303: 299–314Google Scholar
  25. Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABAB autoreceptors regulate the induction of LTE Nature 349: 609–611CrossRefGoogle Scholar
  26. Debanne D, Guérineau NC, Gähwiler BH, Thompson SM (1995) Physiology and pharmacology of unitary synaptic connections between pairs of cells in areas CA3 and CAl of rat hippocampal slice cultures. J Neurophysiol 73: 1282–1294PubMedGoogle Scholar
  27. Desai MA, McBain CJ, Kauer JA, Conn PJ (1994) Metabotropic glutamate receptor-induced disinhibition is mediated by reduced transmission at excitatory synapses onto interneurons and inhibitory synapses onto pyramidal cells. Neurosci Lett 181: 78–82PubMedCrossRefGoogle Scholar
  28. Deuchars J, Thomson AM (1996) CA1 pyramid-pyramid connections in rat hippocampus in vitro: Dual intracellular recordings with biocytin filling. Neuroscience 74: 1009–1018Google Scholar
  29. Diamond JS, Jahr CE (1997) Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17: 4672–4687PubMedGoogle Scholar
  30. Doherty J, Dingledine R (1997) Regulation of excitatory input to inhibitory interneurons of the dentate gyrus during hypoxia. J Neurophysiol 77: 393–404PubMedGoogle Scholar
  31. Doherty J, Dingledine R (1998) Differential regulation of synaptic inputs to dentate hilar border interneurons by metabotropic glutamate receptors. J Neurophysiol 79: 2903–2910PubMedGoogle Scholar
  32. Dudel J, Franke C, Hatt H (1990) Rapid activation, desensitization, and resensitization of synaptic channels of crayfish muscle after glutamate pulses. Biophys J 57: 533–545PubMedCrossRefGoogle Scholar
  33. Faber DS, Young WS, Legendre P, Korn H (1992) Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science 258: 14941498Google Scholar
  34. Fortunato C, Debanne D, Scanziani M, Gähwiler BH, Thompson SM (1996) Functional characterization and modulation of feedback inhibitory circuits in area CA3 of rat hippocampal slice cultures. Eur J Neurosci 8: 1758–1768PubMedCrossRefGoogle Scholar
  35. Franke C, Hatt H, Dudel J (1987) Liquid filament switch for ultra-fast exchanges of solutions at excised patches of synaptic membrane of crayfish muscle. Neurosci Lett 77: 199–204PubMedCrossRefGoogle Scholar
  36. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nature Neurosci 1: 479–486PubMedCrossRefGoogle Scholar
  37. Freund TF, Buzsâki G (1996) Interneurons of the hippocampus. Hippocampus 6: 347–470PubMedCrossRefGoogle Scholar
  38. Geiger JRP, Melcher T, Koh D-S, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995)Google Scholar
  39. Relative abundance of subunit mRNAs determinesatin and Ca’ permeability g P Y of AMPA principal receptors in rind al neurons and interneurons in rat CNS. Neuron P 15:193–204Google Scholar
  40. Geiger JRP, Lübke J, Frotscher M, Jonas P (1996) Rapid kinetics of AMPA receptormediated excitatory synaptic transmission onto GABAergic interneurons. Pflügersg Arch 431: R19Google Scholar
  41. Geiger JRP, Lübke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18: 1009–1023PubMedCrossRefGoogle Scholar
  42. Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366: 683–687PubMedCrossRefGoogle Scholar
  43. Gulyas AI, T6th K, McBain CJ, Freund TF (1997) Anatomical and physiological characterization of stratum radiatum giant cells: a unique type of principal cell in the CA1 area of the rat hippocampus. Society for Neuroscience Abstracts 23: 188. 13Google Scholar
  44. Han Z-S, Buhl EH, Lörinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5: 395410Google Scholar
  45. Haverkampf K, Lübke J, Jonas P (1997) Single-channel properties of native AMPA receptors depend on the putative subunit composition. Society for Neuroscience Abstracts 23: 478. 23Google Scholar
  46. He Y, Janssen WGM, Vissavajjhala P, Morrison JH (1998) Synaptic distribution of GluR2 in hippocampal GABAergic interneurons and pyramidal cells: a double-label immunogold analysis. Exp Neurol 150: 1–13PubMedCrossRefGoogle Scholar
  47. Heckmann M, Bufler J, Franke C, Dudel J (1996) Kinetics of homomeric G1uR6 glutamate receptor channels. Biophys J 71: 1743–1750.PubMedCrossRefGoogle Scholar
  48. Hestrin S, Nicoll RA, Perkel DJ, Sah P (1990) Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol (Lond) 422: 203–225Google Scholar
  49. Hestrin S (1993) Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron 11: 10831091Google Scholar
  50. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9: 1179–1209PubMedCrossRefGoogle Scholar
  51. Ikeda K, Nagasawa M, Mori H, Araki K, Sakimura K, Watanabe M, Inoue Y, Mishina M (1992) Cloning and expression of the s4 subunit of the NMDA receptor channel. FEBS Letters 313: 34–38PubMedCrossRefGoogle Scholar
  52. Isa T, Itazawa S, Iino M, Tsuzuki K, Ozawa S (1996) Distribution of neurones expressing inwardly rectifying and Ca’-permeable AMPA receptors in rat hippocampal slices. J Physiol (Lond) 491: 719–733Google Scholar
  53. Isaacson JS, Walmsley B (1995) Counting quanta: direct measurements of transmitter release at a central synapse. Neuron 15: 875–884PubMedCrossRefGoogle Scholar
  54. Jack JJB, Redman SJ (1971) The propagation of transient potentials in some linear cable structures. J Physiol (Lond) 215: 283–320Google Scholar
  55. Jonas P, Sakmann B (1992) Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J Physiol (Lond) 455: 143–171Google Scholar
  56. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol (Loud) 472: 615–663Google Scholar
  57. Jonas P, Spruston N (1994) Mechanisms shaping glutamate-mediated excitatory post-synaptic currents in the CNS. Curr Opin Neurobiol 4: 366–372PubMedCrossRefGoogle Scholar
  58. Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H (1994) Differences in Ca’ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12: 1281–1289PubMedCrossRefGoogle Scholar
  59. Jones EG, Huntley GW, Benson DL (1994) Alpha calcium/calmodulin-dependent protein kinase II selectively expressed in a subpopulation of excitatory neurons in monkey sensory-motor cortex: comparison with GAD-67 expression. J Neurosci 14: 611–629PubMedGoogle Scholar
  60. Keller BU, Konnerth A, Yaari Y (1991) Patch clamp analysis of excitatory synaptic currents in granule cells of rat hippocampus. J Physiol (Lond) 435: 275–293Google Scholar
  61. Khazipov R, Congar P, Ben-Ari Y (1995) Hippocampal CA1 lacunosum-moleculare interneurons: comparison of effects of anoxia on excitatory and inhibitory post-synaptic currents. J Neurophysiol 74: 2138–2149PubMedGoogle Scholar
  62. Koh D-S, Geiger JRP, Jonas P, Sakmann B (1995a) Cat’-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol (Lond) 485: 383–402Google Scholar
  63. Koh D-S, Burnashev N, Jonas P (1995b) Block of native Ca’-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol (Lond) 486: 305–312Google Scholar
  64. Kullmann DM, Asztely F (1998) Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends in Neurosci 21: 8–14CrossRefGoogle Scholar
  65. Livsey CT, Vicini S (1992) Slower spontaneous excitatory postsynaptic currents in spiny versus aspiny hilar neurons. Neuron 8: 745–755PubMedCrossRefGoogle Scholar
  66. Livsey CT, Costa E, Vicini S (1993) Glutamate-activated currents in outside-out patches from spiny versus aspiny hilar neurons of rat hippocampal slices. J Neurosci 13: 5324–5333PubMedGoogle Scholar
  67. Longsworth LG (1953) Diffusion measurements, at 25°, of aqueous solutions of amino acids, peptides and sugars. J Am Chem Soc 75: 5705–5709CrossRefGoogle Scholar
  68. Maccaferri G, McBain CJ (1995) Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CAl region. Neuron 15: 137–145PubMedCrossRefGoogle Scholar
  69. Maccaferri G, McBain CJ (1996) Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16: 5334–5343PubMedGoogle Scholar
  70. Maccaferri G, T6th K, McBain CJ (1998) Target-specific expression of presynaptic mossy fiber plasticity. Science 279: 1368–1370PubMedCrossRefGoogle Scholar
  71. Mahanty NK, Sah P (1998) Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394: 683–687PubMedCrossRefGoogle Scholar
  72. Major G, Larkman AU, Jonas P, Sakmann B, Jack JJB (1994) Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J Neurosci 14: 4613–4638PubMedGoogle Scholar
  73. Malinow R, Tsien RW (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346: 177–180PubMedCrossRefGoogle Scholar
  74. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurons in the developing rat neocortex. J Physiol (Lond) 500: 409–440Google Scholar
  75. Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323–5328PubMedCrossRefGoogle Scholar
  76. McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol (Lond) 462: 373–392Google Scholar
  77. McBain CJ, DiChiara TJ, Kauer JA (1994) Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14: 4433–4445PubMedGoogle Scholar
  78. McMahon LL, Kauer JA (1997) Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18: 295–305PubMedCrossRefGoogle Scholar
  79. McNaughton BL, Barnes CA (1990) From cooperative synaptic enhancement to asso-Google Scholar
  80. ciative memory: bridging the abyss. Seminars in Neurosci 2:403–416Google Scholar
  81. Miles R, Wong RKS (1986) Excitatory synaptic interactions between CA3 neurons inGoogle Scholar
  82. the guinea-pig hippocampus. J Physiol (Lond) 373:397–418Google Scholar
  83. Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol (Lond) 428: 61–77Google Scholar
  84. Miles R, Poncer J-C (1993) Metabotropic glutamate receptors mediate a post-tetanic excitation of guinea-pig hippocampal inhibitory neurones. J Physiol (Lond) 463: 461–473Google Scholar
  85. Miles R, Toth K, Gulyas AI, Hâjos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815–823PubMedCrossRefGoogle Scholar
  86. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529–540PubMedCrossRefGoogle Scholar
  87. Nusser Z, Lujan R, Laube G, Roberts JDB, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21: 545–559PubMedCrossRefGoogle Scholar
  88. Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993a) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53: 1009–1018PubMedCrossRefGoogle Scholar
  89. Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993b) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J Comp Neurol 335: 252–266PubMedCrossRefGoogle Scholar
  90. Ohishi H, Akazawa C, Shigemoto R, Nakanishi S, Mizuno N (1995) Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol 360: 555570Google Scholar
  91. Otis TS, Jahr CE (1998) Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci 18: 7099–7110PubMedGoogle Scholar
  92. Ouardouz M, Lacaille J-C (1995) Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. J Neurophysiol 73: 810–819PubMedGoogle Scholar
  93. Perouansky M, Yaari Y (1993) Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurons. J Physiol (Lond) 465: 223–244Google Scholar
  94. Pin J-P, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1–26PubMedCrossRefGoogle Scholar
  95. Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30: 1138–1168PubMedGoogle Scholar
  96. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B (1998) Target-cellspecific facilitation and depression in neocortical circuits. Nature Neurosci 1: 279–285PubMedCrossRefGoogle Scholar
  97. Riveros N, Fiedler J, Lagos N, Mufioz C, Orrego F (1986) Glutamate in rat brain cortex synaptic vesicles: influence of the vesicle isolation procedure. Brain Res 386: 405–408PubMedCrossRefGoogle Scholar
  98. Romano C, Sesma MA, McDonald CT, O’Malley K, van den Pol AN, Olney JW (1995) Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J Comp Neurol 355: 455–469PubMedCrossRefGoogle Scholar
  99. Rozov A, Zilberter Y, Wollmuth LP, Burnashev N (1998) Facilitation of currents through rat Ca’-permeable AMPA receptor channels by activity-dependent relief from polyamine block. J Physiol (Lond) 511: 361–377CrossRefGoogle Scholar
  100. Rusakov DA, Kullmann DM (1998a) Geometric and viscous components of the tortuosity of the extracellular space in the brain. Proc Natl Acad Sci USA 95: 8975–8980PubMedCrossRefGoogle Scholar
  101. Rusakov DA, Kullmann DM (1998b) Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18: 3158–3170PubMedGoogle Scholar
  102. Scharfman HE, Kunkel DD, Schwartzkroin PA (1990) Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37: 693–707PubMedCrossRefGoogle Scholar
  103. Shigemoto R, Kulik A, Roberts JDB, Ohishi H, Nusser Z, Kaneko T, Somogyi P (1996) Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381: 523–525PubMedCrossRefGoogle Scholar
  104. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17: 7503–7522PubMedGoogle Scholar
  105. Sik A, Penttonen M, Ylinen A, Buzsâki G (1995) Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J Neurosci 15: 6651–6665PubMedGoogle Scholar
  106. SIk A, Hâjos N, Gulâcsi A, Mody I, Freund TF (1998) The absence of a major Ca’ signaling pathway in GABAergic neurons of the hippocampus. Proc Natl Acad Sci USA 95: 3245–3250PubMedCrossRefGoogle Scholar
  107. Sloviter RS (1991) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1: 41–66PubMedCrossRefGoogle Scholar
  108. Sorra KE, Harris KM (1993) Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J Neurosci 13: 3736–3748PubMedGoogle Scholar
  109. Spruston N, Johnston D (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67: 508–529PubMedGoogle Scholar
  110. Spruston N, Jonas P, Sakmann B (1995) Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J Physiol (Lond) 482: 325–352Google Scholar
  111. Standaert DG, Landwehrmeyer GB, Kerner JA, Penney JB, Young AB (1996) Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Mol Brain Res 42: 89–102PubMedCrossRefGoogle Scholar
  112. Stern P, Edwards FA, Sakmann B (1992) Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. J Physiol (Lond) 449: 247–278Google Scholar
  113. Stiles JR, Bartol TM, Salpeter EE, Salpeter MM (1998) Monte Carlo simulation of neurotransmitter release using MCell, a general simulator of cellular physiological processes. In: Bower J (ed) Computational Neuroscience. Plenum press, New York, pp. 279–284CrossRefGoogle Scholar
  114. Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15: 1065–1076PubMedCrossRefGoogle Scholar
  115. Stuart G, Spruston N (1998) Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18: 3501–3510PubMedGoogle Scholar
  116. Thomson AM (1997) Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiol (Lond) 502: 131–147CrossRefGoogle Scholar
  117. Tong G, Jahr CE (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13: 1195–1203PubMedCrossRefGoogle Scholar
  118. Traub RD, Miles R (1995) Pyramidal cell-to-inhibitory cell spike transduction explicable by active dendritic conductances in inhibitory cell. J Comput Neurosci 2: 291–298PubMedCrossRefGoogle Scholar
  119. Trussell LO (1997) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7: 487–492PubMedCrossRefGoogle Scholar
  120. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR (1998) Functional and pharmacological differences between recombinant N-methyl-Daspartate receptors. J Neurophysiol 79: 555–566PubMedGoogle Scholar
  121. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at the stratum radiatum—stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol (Lond) 506: 755–773CrossRefGoogle Scholar
  122. Wahl LM, Pouzat C, Stratford KJ (1996) Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J Neurophysiol 75: 597–608PubMedGoogle Scholar
  123. Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612–615PubMedCrossRefGoogle Scholar
  124. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER (1998) Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92: 25–37PubMedCrossRefGoogle Scholar
  125. Wyllie DJA, Béhé P, Colquhoun D (1998) Single-channel activations and concentration jumps: comparison of recombinant NR1a/NR2A and NR1a/NR2D NMDA receptors. J Physiol (Lond) 510: 1–18CrossRefGoogle Scholar
  126. Zhang S, Trussell LO (1994) A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705–718PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 1999

Authors and Affiliations

  • J. R. P. Geiger
  • A. Roth
  • B. Taskin
  • P. Jonas

There are no affiliations available

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