Skip to main content

Glutamate-Mediated Synaptic Excitation of Cortical Interneurons

  • Chapter

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 141))

Abstract

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).

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   429.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   549.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

ACPD:

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

AMPARs:

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

ATPA:

2-Amino-3-(3-hydroxy-5-tert-butylisoxazole-4-yl)propanoate

CNS:

Central nervous system

D:

Diffusion coefficient for glutamate

EPSC:

Excitatory postsynaptic current

EPSP:

Excitatory postsynaptic potential

GABA:

-aminobutyric acid

HICAP:

Hilar—commissural-association pathway

HIPP:

Hilar—perforant path

KARs:

Kainate receptors

LTD:

Long-term depression

LTP:

Long-term potentiation

mGluRs:

Metabotropic glutamate receptors

MCPG:

α-methyl-4-carboxyphenyl glycine

MOPP:

Molecular layer—perforant path

NMDARs:

N-methyl-D-aspartate receptors

OALM:

Oriens-alveus—lacunosum moleculare

OML:

Outer molecular layer

PPD:

Paired-pulse depression

PPF:

Paired-pulse facilitation

References

  • 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: 3386–3403

    PubMed  Google Scholar 

  • 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: 185–199

    Article  CAS  Google Scholar 

  • 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: 201–217

    Article  CAS  Google Scholar 

  • 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: 6685–6696

    PubMed  CAS  Google Scholar 

  • Bahn S, Volk B, Wisden W (1994) Kainate receptor gene expression in the developing rat brain. J Neurosci 14: 5525–5547

    PubMed  CAS  Google Scholar 

  • Barbour B, Keller BU, Llano I, Marty A (1994) Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron 12: 1331–1343

    Article  PubMed  CAS  Google Scholar 

  • Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends in Neurosci 20: 377–384

    Article  CAS  Google Scholar 

  • 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: 1290–1307

    Article  PubMed  CAS  Google Scholar 

  • 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: 771–787

    Article  PubMed  CAS  Google Scholar 

  • 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: 1031–1055

    Article  PubMed  CAS  Google Scholar 

  • 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: 2170–2180

    Google Scholar 

  • Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39

    Article  PubMed  CAS  Google Scholar 

  • 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: 383–388

    Article  PubMed  CAS  Google Scholar 

  • Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368: 823–828

    Article  PubMed  CAS  Google Scholar 

  • 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: 689–713

    CAS  Google Scholar 

  • 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: 9921–9925

    Article  PubMed  Google Scholar 

  • 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: 5380–5394

    PubMed  CAS  Google Scholar 

  • Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75–78

    Article  PubMed  CAS  Google Scholar 

  • 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: 261–287

    CAS  Google Scholar 

  • 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: 421–426

    PubMed  CAS  Google Scholar 

  • 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: 470–478

    Article  PubMed  CAS  Google Scholar 

  • 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: 13–20

    PubMed  CAS  Google Scholar 

  • 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: 179–189

    Article  PubMed  CAS  Google Scholar 

  • Datyner NB, Gage PW (1980) Phasic secretion of acetylcholine at a mammalian neuromuscular junction. J Physiol (Lond) 303: 299–314

    CAS  Google Scholar 

  • Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABAB autoreceptors regulate the induction of LTE Nature 349: 609–611

    Article  CAS  Google Scholar 

  • 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: 1282–1294

    PubMed  CAS  Google Scholar 

  • 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: 78–82

    Article  PubMed  CAS  Google Scholar 

  • Deuchars J, Thomson AM (1996) CA1 pyramid-pyramid connections in rat hippocampus in vitro: Dual intracellular recordings with biocytin filling. Neuroscience 74: 1009–1018

    Google Scholar 

  • Diamond JS, Jahr CE (1997) Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17: 4672–4687

    PubMed  CAS  Google Scholar 

  • Doherty J, Dingledine R (1997) Regulation of excitatory input to inhibitory interneurons of the dentate gyrus during hypoxia. J Neurophysiol 77: 393–404

    PubMed  CAS  Google Scholar 

  • Doherty J, Dingledine R (1998) Differential regulation of synaptic inputs to dentate hilar border interneurons by metabotropic glutamate receptors. J Neurophysiol 79: 2903–2910

    PubMed  CAS  Google Scholar 

  • Dudel J, Franke C, Hatt H (1990) Rapid activation, desensitization, and resensitization of synaptic channels of crayfish muscle after glutamate pulses. Biophys J 57: 533–545

    Article  PubMed  CAS  Google Scholar 

  • Faber DS, Young WS, Legendre P, Korn H (1992) Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science 258: 14941498

    Google Scholar 

  • 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: 1758–1768

    Article  PubMed  CAS  Google Scholar 

  • 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: 199–204

    Article  PubMed  CAS  Google Scholar 

  • Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nature Neurosci 1: 479–486

    Article  PubMed  CAS  Google Scholar 

  • Freund TF, Buzsâki G (1996) Interneurons of the hippocampus. Hippocampus 6: 347–470

    Article  PubMed  CAS  Google Scholar 

  • Geiger JRP, Melcher T, Koh D-S, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995)

    Google Scholar 

  • 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 15:193–204

    Google Scholar 

  • Geiger JRP, Lübke J, Frotscher M, Jonas P (1996) Rapid kinetics of AMPA receptormediated excitatory synaptic transmission onto GABAergic interneurons. Pflügersg Arch 431: R19

    Google Scholar 

  • Geiger JRP, Lübke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18: 1009–1023

    Article  PubMed  CAS  Google Scholar 

  • 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: 683–687

    Article  PubMed  CAS  Google Scholar 

  • 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. 13

    Google Scholar 

  • 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: 395410

    Google Scholar 

  • 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. 23

    Google Scholar 

  • 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: 1–13

    Article  PubMed  CAS  Google Scholar 

  • Heckmann M, Bufler J, Franke C, Dudel J (1996) Kinetics of homomeric G1uR6 glutamate receptor channels. Biophys J 71: 1743–1750.

    Article  PubMed  CAS  Google Scholar 

  • 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: 203–225

    CAS  Google Scholar 

  • Hestrin S (1993) Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron 11: 10831091

    Google Scholar 

  • Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9: 1179–1209

    Article  PubMed  CAS  Google Scholar 

  • 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: 34–38

    Article  PubMed  CAS  Google Scholar 

  • 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: 719–733

    CAS  Google Scholar 

  • Isaacson JS, Walmsley B (1995) Counting quanta: direct measurements of transmitter release at a central synapse. Neuron 15: 875–884

    Article  PubMed  CAS  Google Scholar 

  • Jack JJB, Redman SJ (1971) The propagation of transient potentials in some linear cable structures. J Physiol (Lond) 215: 283–320

    CAS  Google Scholar 

  • 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: 143–171

    CAS  Google Scholar 

  • 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: 615–663

    CAS  Google Scholar 

  • Jonas P, Spruston N (1994) Mechanisms shaping glutamate-mediated excitatory post-synaptic currents in the CNS. Curr Opin Neurobiol 4: 366–372

    Article  PubMed  CAS  Google Scholar 

  • 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: 1281–1289

    Article  PubMed  CAS  Google Scholar 

  • 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: 611–629

    PubMed  CAS  Google Scholar 

  • Keller BU, Konnerth A, Yaari Y (1991) Patch clamp analysis of excitatory synaptic currents in granule cells of rat hippocampus. J Physiol (Lond) 435: 275–293

    CAS  Google Scholar 

  • 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: 2138–2149

    PubMed  CAS  Google Scholar 

  • 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: 383–402

    CAS  Google Scholar 

  • 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: 305–312

    CAS  Google Scholar 

  • Kullmann DM, Asztely F (1998) Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends in Neurosci 21: 8–14

    Article  CAS  Google Scholar 

  • Livsey CT, Vicini S (1992) Slower spontaneous excitatory postsynaptic currents in spiny versus aspiny hilar neurons. Neuron 8: 745–755

    Article  PubMed  CAS  Google Scholar 

  • 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: 5324–5333

    PubMed  CAS  Google Scholar 

  • Longsworth LG (1953) Diffusion measurements, at 25°, of aqueous solutions of amino acids, peptides and sugars. J Am Chem Soc 75: 5705–5709

    Article  CAS  Google Scholar 

  • 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: 137–145

    Article  PubMed  CAS  Google Scholar 

  • Maccaferri G, McBain CJ (1996) Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16: 5334–5343

    PubMed  CAS  Google Scholar 

  • Maccaferri G, T6th K, McBain CJ (1998) Target-specific expression of presynaptic mossy fiber plasticity. Science 279: 1368–1370

    Article  PubMed  CAS  Google Scholar 

  • Mahanty NK, Sah P (1998) Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394: 683–687

    Article  PubMed  CAS  Google Scholar 

  • 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: 4613–4638

    PubMed  CAS  Google Scholar 

  • Malinow R, Tsien RW (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346: 177–180

    Article  PubMed  CAS  Google Scholar 

  • 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: 409–440

    CAS  Google Scholar 

  • Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323–5328

    Article  PubMed  CAS  Google Scholar 

  • McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol (Lond) 462: 373–392

    CAS  Google Scholar 

  • 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: 4433–4445

    PubMed  CAS  Google Scholar 

  • McMahon LL, Kauer JA (1997) Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18: 295–305

    Article  PubMed  CAS  Google Scholar 

  • McNaughton BL, Barnes CA (1990) From cooperative synaptic enhancement to asso-

    Google Scholar 

  • ciative memory: bridging the abyss. Seminars in Neurosci 2:403–416

    Google Scholar 

  • Miles R, Wong RKS (1986) Excitatory synaptic interactions between CA3 neurons in

    Google Scholar 

  • the guinea-pig hippocampus. J Physiol (Lond) 373:397–418

    Google Scholar 

  • Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol (Lond) 428: 61–77

    CAS  Google Scholar 

  • Miles R, Poncer J-C (1993) Metabotropic glutamate receptors mediate a post-tetanic excitation of guinea-pig hippocampal inhibitory neurones. J Physiol (Lond) 463: 461–473

    CAS  Google Scholar 

  • Miles R, Toth K, Gulyas AI, Hâjos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815–823

    Article  PubMed  CAS  Google Scholar 

  • 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: 529–540

    Article  PubMed  CAS  Google Scholar 

  • 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: 545–559

    Article  PubMed  CAS  Google Scholar 

  • 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: 1009–1018

    Article  PubMed  CAS  Google Scholar 

  • 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: 252–266

    Article  PubMed  CAS  Google Scholar 

  • 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: 555570

    Google Scholar 

  • Otis TS, Jahr CE (1998) Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci 18: 7099–7110

    PubMed  CAS  Google Scholar 

  • 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: 810–819

    PubMed  CAS  Google Scholar 

  • Perouansky M, Yaari Y (1993) Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurons. J Physiol (Lond) 465: 223–244

    CAS  Google Scholar 

  • Pin J-P, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1–26

    Article  PubMed  CAS  Google Scholar 

  • Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30: 1138–1168

    PubMed  CAS  Google Scholar 

  • Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B (1998) Target-cellspecific facilitation and depression in neocortical circuits. Nature Neurosci 1: 279–285

    Article  PubMed  CAS  Google Scholar 

  • 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: 405–408

    Article  PubMed  CAS  Google Scholar 

  • 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: 455–469

    Article  PubMed  CAS  Google Scholar 

  • 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: 361–377

    Article  CAS  Google Scholar 

  • 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: 8975–8980

    Article  PubMed  CAS  Google Scholar 

  • Rusakov DA, Kullmann DM (1998b) Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18: 3158–3170

    PubMed  CAS  Google Scholar 

  • 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: 693–707

    Article  PubMed  CAS  Google Scholar 

  • 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: 523–525

    Article  PubMed  CAS  Google Scholar 

  • 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: 7503–7522

    PubMed  CAS  Google Scholar 

  • Sik A, Penttonen M, Ylinen A, Buzsâki G (1995) Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J Neurosci 15: 6651–6665

    PubMed  CAS  Google Scholar 

  • 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: 3245–3250

    Article  PubMed  CAS  Google Scholar 

  • 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: 41–66

    Article  PubMed  CAS  Google Scholar 

  • 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: 3736–3748

    PubMed  CAS  Google Scholar 

  • Spruston N, Johnston D (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67: 508–529

    PubMed  CAS  Google Scholar 

  • Spruston N, Jonas P, Sakmann B (1995) Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J Physiol (Lond) 482: 325–352

    CAS  Google Scholar 

  • 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: 89–102

    Article  PubMed  CAS  Google Scholar 

  • 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: 247–278

    CAS  Google Scholar 

  • 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. 279–284

    Chapter  Google Scholar 

  • Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15: 1065–1076

    Article  PubMed  CAS  Google Scholar 

  • Stuart G, Spruston N (1998) Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18: 3501–3510

    PubMed  CAS  Google Scholar 

  • 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: 131–147

    Article  CAS  Google Scholar 

  • Tong G, Jahr CE (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13: 1195–1203

    Article  PubMed  CAS  Google Scholar 

  • Traub RD, Miles R (1995) Pyramidal cell-to-inhibitory cell spike transduction explicable by active dendritic conductances in inhibitory cell. J Comput Neurosci 2: 291–298

    Article  PubMed  CAS  Google Scholar 

  • Trussell LO (1997) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7: 487–492

    Article  PubMed  CAS  Google Scholar 

  • 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: 555–566

    PubMed  CAS  Google Scholar 

  • 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: 755–773

    Article  CAS  Google Scholar 

  • Wahl LM, Pouzat C, Stratford KJ (1996) Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J Neurophysiol 75: 597–608

    PubMed  CAS  Google Scholar 

  • Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612–615

    Article  PubMed  CAS  Google Scholar 

  • 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: 25–37

    Article  PubMed  CAS  Google Scholar 

  • 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: 1–18

    Article  CAS  Google Scholar 

  • Zhang S, Trussell LO (1994) A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705–718

    PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Geiger, J.R.P., Roth, A., Taskin, B., Jonas, P. (1999). Glutamate-Mediated Synaptic Excitation of Cortical Interneurons. In: Jonas, P., Monyer, H. (eds) Ionotropic Glutamate Receptors in the CNS. Handbook of Experimental Pharmacology, vol 141. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-08022-1_11

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-08022-1_11

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-08539-0

  • Online ISBN: 978-3-662-08022-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics