Advertisement

Glutamatergic Neurotransmission in the Hippocampus

  • Katalin Tóth
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI, volume 5)

Abstract

This chapter will summarize key data about glutamatergic transmission in the hippocampus. Glutamate is the major excitatory neurotransmitter similar to other CNS regions. Biophysical properties of various receptors and channels will be described and functional relevance of these parameters discussed.

Keywords

NMDA Receptor Pyramidal Cell AMPA Receptor Metabotropic Glutamate Receptor Kainate Receptor 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Further Reading

  1. Acsády, L., Kamondi, A., Sík, A., Freund, T. and Buzsáki, G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18, 3386–3403 (1998).PubMedGoogle Scholar
  2. Adesnik, H., Nicoll, R. A. and England, P. M. Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 48, 977–985 (2005).PubMedCrossRefGoogle Scholar
  3. Amaral, D. G. and Dent, J. A. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195, 51–86 (1981).PubMedCrossRefGoogle Scholar
  4. Amaral, D. G. and Witter, M. P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571–591 (1989).PubMedCrossRefGoogle Scholar
  5. Amaral, D. G., Ishizuka, N. and Claiborne, B. Neurons, numbers and the hippocampal network. Prog Brain Res 83, 1–11 (1990).PubMedCrossRefGoogle Scholar
  6. Andrasfalvy, B. K. and Magee, J. C. Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J Neurosci 21, 9151–9159 (2001).PubMedGoogle Scholar
  7. Arrigoni, E. and Greene, R. W. Schaffer collateral and perforant path inputs activate different subtypes of NMDA receptors on the same CA1 pyramidal cell. Br J Pharmacol 142, 317–322 (2004).PubMedCrossRefGoogle Scholar
  8. Barberis, A., Sachidhanandam, S. and Mulle, C. GluR6/KA2 kainate receptors mediate slow-deactivating currents. J Neurosci 28, 6402–6406 (2008).PubMedCrossRefGoogle Scholar
  9. Benke, T. A., Lüthi, A., Isaac, J. T. and Collingridge, G. L. Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793–797 (1998).PubMedCrossRefGoogle Scholar
  10. Berzhanskaya, J., Urban, N. N. and Barrionuevo, G. Electrophysiological and pharmacological characterization of the direct perforant path input to hippocampal area CA3. J Neurophysiol 79, 2111–2118 (1998).PubMedGoogle Scholar
  11. Bischofberger, J., Geiger, J. R. and Jonas, P. Timing and efficacy of Ca2+ channel activation in hippocampal mossy fiber boutons. J Neurosci 22, 10593–10602 (2002).PubMedGoogle Scholar
  12. Blaschke, M., Keller, B. U., Rivosecchi, R., Hollmann, M., et al. A single amino acid determines the subunit-specific spider toxin block of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor channels. Proc Natl Acad Sci USA 90, 6528–6532 (1993).PubMedCrossRefGoogle Scholar
  13. Bortolotto, Z. A., Fitzjohn, S. M. and Collingridge, G. L. Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr Opin Neurobiol 9, 299–304 (1999).PubMedCrossRefGoogle Scholar
  14. Bowie, D. and Mayer, M. L. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15, 453–462 (1995).PubMedCrossRefGoogle Scholar
  15. Breustedt, J. and Schmitz, D. Assessing the role of GLUK5 and GLUK6 at hippocampal mossy fiber synapses. J Neurosci 24, 10093–10098 (2004).PubMedCrossRefGoogle Scholar
  16. Calixto, E., Galván, E. J., Card, J. P. and Barrionuevo, G. Coincidence detection of convergent perforant path and mossy fibre inputs by CA3 interneurons. J Physiol 586, 2695–2712 (2008).PubMedCrossRefGoogle Scholar
  17. Capogna, M. Distinct properties of presynaptic group II and III metabotropic glutamate receptor-mediated inhibition of perforant pathway-CA1 EPSCs. Eur J Neurosci 19, 2847–2858 (2004).PubMedCrossRefGoogle Scholar
  18. Castillo, P. E., Malenka, R. C. and Nicoll, R. A. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388, 182–186 (1997).PubMedCrossRefGoogle Scholar
  19. Chicurel, M. E. and Harris, K. M. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 325, 169–182 (1992).PubMedCrossRefGoogle Scholar
  20. Chittajallu, R., Vignes, M., Dev, K. K., Barnes, J. M., et al. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379, 78–81 (1996).PubMedCrossRefGoogle Scholar
  21. Chiu, C. Q. and Castillo, P. E. Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus. Neuropharmacology 54, 68–78 (2008).PubMedCrossRefGoogle Scholar
  22. Colbert, C. M. and Levy, W. B. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J Neurophysiol 68, 1–8 (1992).PubMedGoogle Scholar
  23. Contractor, A., Swanson, G. and Heinemann, S. F. Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29, 209–216 (2001).PubMedCrossRefGoogle Scholar
  24. Contractor, A., Sailer, A. W., Darstein, M., Maron, C., et al. Loss of kainate receptor-mediated heterosynaptic facilitation of mossy-fiber synapses in KA2–/– mice. J Neurosci 23, 422–429 (2003).PubMedGoogle Scholar
  25. Cossart, R., Esclapez, M., Hirsch, J. C., Bernard, C. and Ben-Ari, Y. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1, 470–478 (1998).PubMedCrossRefGoogle Scholar
  26. Cossart, R., Tyzio, R., Dinocourt, C., Esclapez, M., et al. Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29, 497–508 (2001).PubMedCrossRefGoogle Scholar
  27. Cossart, R., Epsztein, J., Tyzio, R., Becq, H., et al. Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35, 147–159 (2002).PubMedCrossRefGoogle Scholar
  28. Dahl, D. and Sarvey, J. M. Norepinephrine induces pathway-specific long-lasting potentiation and depression in the hippocampal dentate gyrus. Proc Natl Acad Sci USA 86, 4776–4780 (1989).PubMedCrossRefGoogle Scholar
  29. Darstein, M., Petralia, R. S., Swanson, G. T., Wenthold, R. J. and Heinemann, S. F. Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23, 8013–8019 (2003).PubMedGoogle Scholar
  30. Dingledine, R., Borges, K., Bowie, D. and Traynelis, S. F. The glutamate receptor ion channels. Pharmacol Rev 51, 7–61 (1999).PubMedGoogle Scholar
  31. Donevan, S. D. and Rogawski, M. A. Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Proc Natl Acad Sci USA 92, 9298–9302 (1995).PubMedCrossRefGoogle Scholar
  32. Durand, G. M., Kovalchuk, Y. and Konnerth, A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381, 71–75 (1996).PubMedCrossRefGoogle Scholar
  33. Empson, R. M. and Heinemann, U. Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus 5, 104–107 (1995).PubMedCrossRefGoogle Scholar
  34. Empson, R. M. and Heinemann, U. The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol 484 (Pt 3), 707–720 (1995).PubMedGoogle Scholar
  35. Enoki, R., Hu, Y., Hamilton, D. and Fine, A. Expression of long-term plasticity at individual synapses in the hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62, 242–253 (2009).PubMedCrossRefGoogle Scholar
  36. Frerking, M., Schmitz, D., Zhou, Q., Johansen, J. and Nicoll, R. A. Kainate receptors depress excitatory synaptic transmission at CA3–>CA1 synapses in the hippocampus via a direct presynaptic action. J Neurosci 21, 2958–2966 (2001).PubMedGoogle Scholar
  37. Frerking, M. and Ohliger-Frerking, P. AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22, 7434–7443 (2002).PubMedGoogle Scholar
  38. Geiger, J. R., Melcher, T., Koh, D. S., Sakmann, B., et al. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193–204 (1995).PubMedCrossRefGoogle Scholar
  39. Geiger, J. R., Lübke, J., Roth, A., Frotscher, M. and Jonas, P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009–1023 (1997).PubMedCrossRefGoogle Scholar
  40. Geiger, J. R. and Jonas, P. Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. Neuron 28, 927–939 (2000).PubMedCrossRefGoogle Scholar
  41. Gereau, R. W. and Conn, P. J. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci 15,6879–6889 (1995).PubMedGoogle Scholar
  42. Hallermann, S., Pawlu, C., Jonas, P. and Heckmann, M. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc Natl Acad Sci USA 100, 8975–8980 (2003).PubMedCrossRefGoogle Scholar
  43. Han, Z. S., Buhl, E. H., Lörinczi, Z. and Somogyi, P. 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, 395–410 (1993).PubMedCrossRefGoogle Scholar
  44. Harris, K. M. and Sultan, P. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34, 1387–1395 (1995).PubMedCrossRefGoogle Scholar
  45. Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., et al. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287,2262–2267 (2000).PubMedCrossRefGoogle Scholar
  46. Henze, D. A., Card, J. P., Barrionuevo, G. and Ben-Ari, Y. Large amplitude miniature excitatory postsynaptic currents in hippocampal CA3 pyramidal neurons are of mossy fiber origin. J Neurophysiol 77, 1075–1086 (1997).PubMedGoogle Scholar
  47. Henze, D. A., McMahon, D. B., Harris, K. M. and Barrionuevo, G. Giant miniature EPSCs at the hippocampal mossy fiber to CA3 pyramidal cell synapse are monoquantal. J Neurophysiol 87, 15–29 (2002).PubMedGoogle Scholar
  48. Henze, D. A., Wittner, L. and Buzsáki, G. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5, 790–795 (2002).PubMedGoogle Scholar
  49. Heuss, C., Scanziani, M., Gähwiler, B. H. and Gerber, U. G-protein-independent signaling mediated by metabotropic glutamate receptors. Nat Neurosci 2, 1070–1077 (1999).PubMedCrossRefGoogle Scholar
  50. Ho, M. T., Pelkey, K. A., Topolnik, L., Petralia, R. S., et al. Developmental expression of Ca2+-permeable AMPA receptors underlies depolarization-induced long-term depression at mossy fiber CA3 pyramid synapses. J Neurosci 27, 11651–11662 (2007).PubMedCrossRefGoogle Scholar
  51. Isaac, J. T., Ashby, M. and McBain, C. J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54, 859–871 (2007).PubMedCrossRefGoogle Scholar
  52. Ito, K., Contractor, A. and Swanson, G. T. Attenuated plasticity of postsynaptic kainate receptors in hippocampal CA3 pyramidal neurons. J Neurosci 24, 6228–6236 (2004).PubMedCrossRefGoogle Scholar
  53. Jarsky, T., Roxin, A., Kath, W. L. and Spruston, N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci 8, 1667–1676 (2005).PubMedCrossRefGoogle Scholar
  54. Jonas, P., Major, G. and Sakmann, B. Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol 472, 615–663 (1993).PubMedGoogle Scholar
  55. Jonas, P., Racca, C., Sakmann, B., Seeburg, P. H. and Monyer, H. Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12, 1281–1289 (1994).PubMedCrossRefGoogle Scholar
  56. Kahle, J. S. and Cotman, C. W. Carbachol depresses synaptic responses in the medial but not the lateral perforant path. Brain Res 482, 159–163 (1989).PubMedCrossRefGoogle Scholar
  57. Kamboj, S. K., Swanson, G. T. and Cull-Candy, S. G. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486 (Pt 2),297–303 (1995).PubMedGoogle Scholar
  58. Kamiya, H., Shinozaki, H. and Yamamoto, C. Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J Physiol 493 (Pt 2), 447–455 (1996).PubMedGoogle Scholar
  59. Kamiya, H. and Ozawa, S. Kainate receptor-mediated inhibition of presynaptic Ca2+ influx and EPSP in area CA1 of the rat hippocampus. J Physiol 509 (Pt 3), 833–845 (1998).PubMedCrossRefGoogle Scholar
  60. Kilbride, J., Rush, A. M., Rowan, M. J. and Anwyl, R. Presynaptic group II mGluR inhibition of short-term depression in the medial perforant path of the dentate gyrus in vitro. J Neurophysiol 85, 2509–2515 (2001).PubMedGoogle Scholar
  61. Koh, D. S., Burnashev, N. and Jonas, P. Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486 (Pt 2), 305–312 (1995).PubMedGoogle Scholar
  62. Kullmann, D. M. Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12, 1111–1120 (1994).PubMedCrossRefGoogle Scholar
  63. Kwon, H. B. and Castillo, P. E. Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses. Neuron 57, 108–120 (2008).PubMedCrossRefGoogle Scholar
  64. Kwon, H. B. and Castillo, P. E. Role of glutamate autoreceptors at hippocampal mossy fiber synapses. Neuron 60, 1082–1094 (2008).PubMedCrossRefGoogle Scholar
  65. Lambert, J. D. and Jones, R. S. Activation of N-methyl-D-aspartate receptors contributes to the EPSP at perforant path synapses in the rat dentate gyrus in vitro. Neurosci Lett 97, 323–328 (1989).PubMedCrossRefGoogle Scholar
  66. Lambert, J. D. and Jones, R. S. A reevaluation of excitatory amino acid-mediated synaptic transmission in rat dentate gyrus. J Neurophysiol 64, 119–132 (1990).PubMedGoogle Scholar
  67. Larkman, A. U., Jack, J. J. and Stratford, K. J. Quantal analysis of excitatory synapses in rat hippocampal CA1 in vitro during low-frequency depression. J Physiol 505 (Pt 2), 457–471 (1997).PubMedCrossRefGoogle Scholar
  68. Lauri, S. E., Bortolotto, Z. A., Bleakman, D., Ornstein, P. L., et al. A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 32, 697–709 (2001).PubMedCrossRefGoogle Scholar
  69. Lawrence, J. J., Grinspan, Z. M. and McBain, C. J. Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus. J Physiol 554, 175–193 (2004).PubMedCrossRefGoogle Scholar
  70. Le Vasseur, M., Ran, I. and Lacaille, J. C. Selective induction of metabotropic glutamate receptor 1- and metabotropic glutamate receptor 5-dependent chemical long-term potentiation at oriens/alveus interneuron synapses of mouse hippocampus. J Neurosci 151, 28–42 (2008).CrossRefGoogle Scholar
  71. Lei, S. and McBain, C. J. Distinct NMDA receptors provide differential modes of transmission at mossy fiber-interneuron synapses. Neuron 33, 921–933 (2002).PubMedCrossRefGoogle Scholar
  72. Li, X. G., Somogyi, P., Ylinen, A. and Buzsáki, G. The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339, 181–208 (1994).PubMedCrossRefGoogle Scholar
  73. Liao, D., Hessler, N. A. and Malinow, R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400–404 (1995).PubMedCrossRefGoogle Scholar
  74. Macek, T. A., Winder, D. G., Gereau, R. W., Ladd, C. O. and Conn, P. J. Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol 76, 3798–3806 (1996).PubMedGoogle Scholar
  75. Magee, J. C. and Cook, E. P. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3, 895–903 (2000).PubMedCrossRefGoogle Scholar
  76. McBain, C. J. and Dingledine, R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462, 373–392 (1993).PubMedGoogle Scholar
  77. McBain, C. J., DiChiara, T. J. and Kauer, J. A. Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14, 4433–4445 (1994).PubMedGoogle Scholar
  78. McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., et al. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94–99 (2007).PubMedCrossRefGoogle Scholar
  79. McNaughton, B. L. Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res 199, 1–19 (1980).PubMedCrossRefGoogle Scholar
  80. Megías, M., Emri, Z., Freund, T. F. and Gulyás, A. I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527–540 (2001).PubMedCrossRefGoogle Scholar
  81. Min, M. Y., Asztely, F., Kokaia, M. and Kullmann, D. M. Long-term potentiation and dual-component quantal signaling in the dentate gyrus. Proc Natl Acad Sci USA 95, 4702–4707 (1998).PubMedCrossRefGoogle Scholar
  82. Mulle, C., Sailer, A., Pérez-Otaño, I., Dickinson-Anson, H., et al. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601–605 (1998).PubMedCrossRefGoogle Scholar
  83. Neu, A., Földy, C. and Soltesz, I. Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J Physiol 578, 233–247 (2007).PubMedCrossRefGoogle Scholar
  84. Nimchinsky, E. A., Yasuda, R., Oertner, T. G. and Svoboda, K. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J Neurosci 24, 2054–2064 (2004).PubMedCrossRefGoogle Scholar
  85. O’Connor, V., El Far, O., Bofill-Cardona, E., Nanoff, C., et al. Calmodulin dependence of presynaptic metabotropic glutamate receptor signaling. Science 286, 1180–1184 (1999).PubMedCrossRefGoogle Scholar
  86. Oertner, T. G., Sabatini, B. L., Nimchinsky, E. A. and Svoboda, K. Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5, 657–664 (2002).PubMedGoogle Scholar
  87. Otmakhova, N. A., Otmakhov, N. and Lisman, J. E. Pathway-specific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells. J Neurosci 22, 1199–1207 (2002).PubMedGoogle Scholar
  88. Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A. and Ehlers, M. D. Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972–1975 (2004).PubMedCrossRefGoogle Scholar
  89. Pelkey, K. A., Lavezzari, G., Racca, C., Roche, K. W. and McBain, C. J. mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 46, 89–102(2005).PubMedCrossRefGoogle Scholar
  90. Pelkey, K. A., Yuan, X., Lavezzari, G., Roche, K. W. and McBain, C. J. mGluR7 undergoes rapid internalization in response to activation by the allosteric agonist AMN082. Neuropharmacology 52, 108–117 (2007).PubMedCrossRefGoogle Scholar
  91. Pelletier, M. R., Kirkby, R. D., Jones, S. J. and Corcoran, M. E. Pathway specificity of noradrenergic plasticity in the dentate gyrus. Hippocampus 4, 181–188 (1994).PubMedCrossRefGoogle Scholar
  92. Perouansky, M. and Yaari, Y. Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. J Physiol 465, 223–244 (1993).PubMedGoogle Scholar
  93. Petralia, R. S., Wang, Y. X. and Wenthold, R. J. Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J Comp Neurol 349, 85–110 (1994).PubMedCrossRefGoogle Scholar
  94. Petralia, R. S., Yokotani, N. and Wenthold, R. J. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 14, 667–696 (1994).PubMedGoogle Scholar
  95. Petralia, R. S., Wang, Y. X. and Wenthold, R. J. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14, 6102–6120 (1994).PubMedGoogle Scholar
  96. Pinheiro, P. S., Perrais, D., Coussen, F., Barhanin, J., et al. GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 104, 12181–12186 (2007).PubMedCrossRefGoogle Scholar
  97. Price, C. J., Karayannis, T., Pál, B. Z. and Capogna, M. Group II and III mGluRs-mediated presynaptic inhibition of EPSCs recorded from hippocampal interneurons of CA1 stratum lacunosum moleculare. Neuropharmacology 49 (Suppl 1), 45–56 (2005).PubMedCrossRefGoogle Scholar
  98. Raastad, M. and Lipowski, R. Diversity of postsynaptic amplitude and failure probability of unitary excitatory synapses between CA3 and CA1 cells in the rat hippocampus. Eur J Neurosci 8, 1265–1274 (1996).PubMedCrossRefGoogle Scholar
  99. Racca, C., Stephenson, F. A., Streit, P., Roberts, J. D. and Somogyi, P. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20, 2512–2522(2000).PubMedGoogle Scholar
  100. Rebola, N., Sachidhanandam, S., Perrais, D., Cunha, R. A. and Mulle, C. Short-term plasticity of kainate receptor-mediated EPSCs induced by NMDA receptors at hippocampal mossy fiber synapses. J Neurosci 27, 3987–3993 (2007).PubMedCrossRefGoogle Scholar
  101. Rebola, N., Lujan, R., Cunha, R. A. and Mulle, C. Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron 57, 121–134 (2008).PubMedCrossRefGoogle Scholar
  102. Remondes, M. and Schuman, E. M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 416, 736–740 (2002).PubMedCrossRefGoogle Scholar
  103. Rollenhagen, A., Sätzler, K., Rodríguez, E. P., Jonas, P., et al. Structural determinants of transmission at large hippocampal mossy fiber synapses. J Neurosci 27, 10434–10444 (2007).PubMedCrossRefGoogle Scholar
  104. Rosenmund, C., Clements, J. D. and Westbrook, G. L. Nonuniform probability of glutamate release at a hippocampal synapse. Science 262, 754–757 (1993).PubMedCrossRefGoogle Scholar
  105. Rush, A. M., Kilbride, J., Rowan, M. J. and Anwyl, R. Presynaptic group III mGluR modulation of short-term plasticity in the lateral perforant path of the dentate gyrus in vitro. Brain Res 952, 38–43 (2002).PubMedCrossRefGoogle Scholar
  106. Salin, P. A., Scanziani, M., Malenka, R. C. and Nicoll, R. A. Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci USA 93, 13304–13309 (1996).PubMedCrossRefGoogle Scholar
  107. Sambandan, S. and Bartos, M. Unpublished Observation (2009).Google Scholar
  108. Scanziani, M., Salin, P. A., Vogt, K. E., Malenka, R. C. and Nicoll, R. A. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385, 630–634 (1997).PubMedCrossRefGoogle Scholar
  109. Schikorski, T. and Stevens, C. F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17, 5858–5867 (1997).PubMedGoogle Scholar
  110. Schmitz, D., Frerking, M. and Nicoll, R. A. Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27, 327–338 (2000).PubMedCrossRefGoogle Scholar
  111. Schmitz, D., Mellor, J. and Nicoll, R. A. Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291, 1972–1976 (2001).PubMedCrossRefGoogle Scholar
  112. Schmitz, D., Mellor, J., Breustedt, J. and Nicoll, R. A. Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat Neurosci 6,1058–1063 (2003).PubMedCrossRefGoogle Scholar
  113. Semyanov, A. and Kullmann, D. M. Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25, 663–672 (2000).PubMedCrossRefGoogle Scholar
  114. Shi, S. H., Hayashi, Y., Petralia, R. S., Zaman, S. H., et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811–1816 (1999).PubMedCrossRefGoogle Scholar
  115. Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., et al. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17, 7503–7522 (1997).PubMedGoogle Scholar
  116. Smith, M. A., Ellis-Davies, G. C. and Magee, J. C. Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons. J Physiol 548, 245–258 (2003).PubMedCrossRefGoogle Scholar
  117. Spruston, N., Jonas, P. and Sakmann, B. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J Physiol 482 (Pt 2), 325–352 (1995).PubMedGoogle Scholar
  118. Sun, H. Y. and Dobrunz, L. E. Presynaptic kainate receptor activation is a novel mechanism for target cell-specific short-term facilitation at Schaffer collateral synapses. J Neurosci 26,10796–10807 (2006).PubMedCrossRefGoogle Scholar
  119. Sun, H. Y., Bartley, A. F. and Dobrunz, L. E. Calcium-permeable presynaptic kainate receptors involved in excitatory short-term facilitation onto somatostatin interneurons during natural stimulus patterns. J Neurophysiol 99 (2), 799–813.(2008).CrossRefGoogle Scholar
  120. Szabadics, J. and Soltesz, I. Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J Neurosci 29, 4239–4251 (2009).PubMedCrossRefGoogle Scholar
  121. Takumi, Y., Ramírez-León, V., Laake, P., Rinvik, E. and Ottersen, O. P. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2, 618–624 (1999).PubMedCrossRefGoogle Scholar
  122. Tanabe, Y., Masu, M., Ishii, T., Shigemoto, R. and Nakanishi, S. A family of metabotropic glutamate receptors. Neuron 8, 169–179 (1992).PubMedCrossRefGoogle Scholar
  123. Tanabe, Y., Nomura, A., Masu, M., Shigemoto, R., et al. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 13, 1372–1378 (1993).PubMedGoogle Scholar
  124. Topolnik, L., Azzi, M., Morin, F., Kougioumoutzakis, A. and Lacaille, J. C. mGluR1/5 subtype-specific calcium signalling and induction of long-term potentiation in rat hippocampal oriens/alveus interneurones. J Physiol 575, 115–131 (2006).PubMedCrossRefGoogle Scholar
  125. Toth, K., Suares, G., Lawrence, J. J., Philips-Tansey, E. and McBain, C. J. Differential mechanisms of transmission at three types of mossy fiber synapse. J Neurosci 20, 8279–8289 (2000).PubMedGoogle Scholar
  126. Tóth, K. and McBain, C. J. Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1, 572–578 (1998).PubMedCrossRefGoogle Scholar
  127. Tóth, K. and McBain, C. J. Target-specific expression of pre- and postsynaptic mechanisms. J Physiol 525 (Pt 1), 41–51 (2000).PubMedCrossRefGoogle Scholar
  128. Tyler, W. J., Zhang, X. L., Hartman, K., Winterer, J., et al. BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. J Physiol 574, 787–803 (2006).PubMedCrossRefGoogle Scholar
  129. Valenzuela-Harrington, M., Gruart, A. and Delgado-García, J. M. Contribution of NMDA receptor NR2B subunit to synaptic plasticity during associative learning in behaving rats. Eur J Neurosci 25, 830–836 (2007).PubMedCrossRefGoogle Scholar
  130. Vignes, M. and Collingridge, G. L. The synaptic activation of kainate receptors. Nature 388,179–182 (1997).PubMedCrossRefGoogle Scholar
  131. Vignes, M., Clarke, V. R., Parry, M. J., Bleakman, D., et al. The GluR5 subtype of kainate receptor regulates excitatory synaptic transmission in areas CA1 and CA3 of the rat hippocampus. Neuropharmacology 37, 1269–1277 (1998).PubMedCrossRefGoogle Scholar
  132. von Kitzing, E., Jonas, P. and Sakmann, B. Quantal analysis of excitatory postsynaptic currents at the hippocampal mossy fiber-CA3 pyramidal cell synapse. Adv Second Messenger Phosphoprotein Res 29, 235–260 (1994).Google Scholar
  133. Walker, H. C., Lawrence, J. J. and McBain, C. J. Activation of kinetically distinct synaptic conductances on inhibitory interneurons by electrotonically overlapping afferents. Neuron 35, 161–171 (2002).PubMedCrossRefGoogle Scholar
  134. Washburn, M. S. and Dingledine, R. Block of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J Pharmacol Exp Ther 278, 669–678 (1996).PubMedGoogle Scholar
  135. Watanabe, M., Fukaya, M., Sakimura, K., Manabe, T., et al. Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10, 478–487 (1998).PubMedCrossRefGoogle Scholar
  136. Winder, D. G., Ritch, P. S., Gereau, R. W. and Conn, P. J. Novel glial-neuronal signalling by coactivation of metabotropic glutamate and beta-adrenergic receptors in rat hippocampus. J Physiol 494 (Pt 3), 743–755 (1996).PubMedGoogle Scholar
  137. Witter, M. P. Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3 Spec No, 33–44 (1993).PubMedGoogle Scholar
  138. Yeckel, M. F., Kapur, A. and Johnston, D. Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2, 625–633 (1999).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Centre de recherche Université Laval Robert GiffardQuebecCanada

Personalised recommendations