At immature mossy fibers-CA3 connections, activation of presynaptic GABAB receptors by endogenously released GABA contributes to synapses silencing

Frontiers in Cellular Neuroscience

Volumn 3, Issue FEB, 2009, Pages

  Safiulina, Victoria F ^a   Cherubini, Enrico ^a  

^a SISSA   (Italy)

Author keywords

Frequency dependent synaptic depression; GABA transporters; GABAA mediated synaptic currents; GABAB autoreceptors; Immature hippocampus; Mossy fiber CA3 synapses; Probability of GABA release

Indexed keywords

EID: 67649947125     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.03.001.2009     Document Type: Article

References (65)

1. Alle, H., and Geiger, J. R. (2007). GABAergic spill-over transmission onto hippocampal mossy fiber boutons. J. Neurosci. 27, 942-950.
2. Allen, C., and Stevens, C. F. (1994). An evaluation of causes for unreliability of synaptic transmission. Proc. Natl. Acad. Sci. U.S.A. 91, 10380-10383.
3. Ben-Ari, Y., Cherubini, E., Corradetti, R., and Gaiarsa, J. L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416, 303-325.
4. Ben-Ari, Y., Gaiarsa, J. L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284.
5. Bettler, B., Kaupmann, K., Mosbacher, J., and Gassmann, M. (2004). Molecular structure and physiological functions of GABA(B) receptors. Physiol. Rev. 84, 835-867.
6. Binda, F., Bossi, E., Giovannardi, S., Forlani, G., and Peres, A. (2002). Temperature effects on the presteadystate and transport-associated currents of GABA cotransporter rGAT1. FEBS Lett. 512, 303-307.
7. Bischofberger, J., Engel, D., Frotscher, M., and Jonas, P. (2006). Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network. Pflugers Arch. 453, 361-372.
8. Borden, L. A. (1996). GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem. Int. 29, 335-356.
9. Caillard, O., McLean, H. A., Ben-Ari, Y., and Gaïarsa, J. L. (1998). Ontogenesis of presynaptic GABAB receptormediated inhibition in the CA3 region of the rat hippocampus. J. Neurophysiol. 79, 1341-1348.
10. Castillo, P. E., Malenka, R. C., and Nicoll, R. A. (1997). Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388, 182-186.
11. Cherubini, E., Martina, M., Sciancalepore, M., and Strata, F. (1998). GABA excites immature CA3 pyramidal cells through bicucullinesensitive and-insensitive chloridedependent receptors. Perspect. Dev. Neurobiol. 5, 289-304.
12. Dupuy, S. T., and Houser, C. R. (1997). Developmental changes in GABA neurons of the rat dentate gyrus: an in situ hybridization and birthdating study. J. Comp. Neurol. 389, 402-418.
13. Dzhala, V. I., Talos, D. M., Sdrulla, D. A., Brumback, A. C., Mathews, G. C., Benke, T. A., Delpire, E., Jensen, F. E., and Staley, K. J. (2005). NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11, 1205-1213.
14. Frahm, C., and Draguhn, A. (2001). GAD and GABA transporter (GAT-1) mRNA expression in the developing rat hippocampus. Brain Res. Dev. Brain Res. 132, 1-13.
15. Gaiarsa, J. L., Tseeb, V., and Ben-Ari, Y. (1995). Postnatal development of preand postsynaptic GABAB-mediated inhibitions in the CA3 hippocampal region of the rat. J. Neurophysiol. 73, 246-255.
16. Gasparini, S., Saviane, C., Voronin, L. L., and Cherubini, E. (2000). Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc. Natl. Acad. Sci. U.S.A. 97, 9741-9746.
17. Gutierrez, R. (2005). The dual glutamatergic-GABAergic phenotype of hippocampal granule cells. Trends Neurosci. 28, 297-303.
18. Gutierrez, R., Romo-Parra, H., Maqueda, J., Vivar, C., Ramirez, M., Morales, M. A., and Lamas, M. (2003). Plasticity of the GABAergic phenotype of the "glutamatergic" granule cells of the rat dentate gyrus. J. Neurosci. 23, 5594-5598.
19. Henze, D. A., Urban, N. N., and Barrionuevo, G. (2000). The multifarious hippocampal mossy fiber pathway: a review. Neuroscience 98, 407-427.
20. Jonas, P., Major, G., and Sakmann, B. (1993). Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. 472, 615-663.
21. Kamiya, H., Shinozaki, H., and Yamamoto, C. (1996). Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J. Physiol. 493, 447-455.
22. Kasyanov, A. M., Safiulina, V. F., Voronin, L. L., and Cherubini, E. (2004). GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc. Natl. Acad. Sci. U.S.A. 101, 3967-3972.
23. Khirug, S., Yamada, J., Afzalov, R., Voipio, J., Khiroug, L., and Kaila, K. (2008). GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J. Neurosci. 28, 4635-4639.
24. Kukley, M., Schwan, M., Fredholm, B. B., and Dietrich, D. (2005). The role of extracellular adenosine in regulating mossy fiber synaptic plasticity. J. Neurosci. 25, 2832-2837.
25. Lamas, M., Gomez-Lira, G., and Gutierrez, R. (2001). Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes. Brain Res. Mol. Brain Res. 93, 209-214.
26. Lei, S., and McBain, C. J. (2003). GABA B receptor modulation of excitatory and inhibitory synaptic transmission onto rat CA3 hippocampal interneurons. J. Physiol. 546, 439-453.
27. Lerma, J. (2003). Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4, 481-495.
28. Lerma, J. (2006). Kainate receptor physiology. Curr. Opin. Pharmacol. 6, 89-97.
29. López-Bendito, G., Shigemoto, R., Kulik, A., Vida, I., Fairén, A., and Luján, R. (2004). Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14, 836-848.
30. + channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19, 687-695.
31. Malinow, R., and Tsien, R. W. (1990). Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177-180.
32. Marchal, C., and Mulle, C. (2004). Postnatal maturation of mossy fibre excitatory transmission in mouse CA3 pyramidal cells: a potential role for kainate receptors. J. Physiol. 561, 27-37.
33. Marchionni, I., Omrani, A., and Cherubini, E. (2007). In the developing rat hippocampus a tonic GABAAmediated conductance selectively enhances the glutamatergic drive of principal cells. J. Physiol. 581, 515-528.
34. McAllister, A. K., and Stevens, C. F. (2000). Nonsaturation of AMPA and NMDA receptors at hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 97, 6173-6178.
35. McBain, C. J. (2008). Differential mechanisms of transmission and plasticity at mossy fiber synapses. Prog. Brain Res. 169, 225-240.
36. McLean, H. A., Caillard, O., Khazipov, R., Ben-Ari, Y., and Gaiarsa, J. L. (1996). Spontaneous release of GABA activates GABAB receptors and controls network activity in the neonatal rat hippocampus. J. Neurophysiol. 76, 1036-1046.
37. Min, M. Y., Rusakov, D. A., and Kullmann, D. M. (1998). Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion. Neuron 21, 561-570.
38. Misgeld, U., Bijak, M., and Jarolimek, W. (1995). A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog. Neurobiol. 46, 423-462.
39. Moore, K. A., Nicoll, R. A., and Schmitz, D. (2003). Adenosine gates synaptic plasticity at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. U.S.A. 100, 14397-14402.
40. Nakamura, M., Sekino, Y., and Manabe, T. (2007). GABAergic interneurons facilitate mossy fiber excitability in the developing hippocampus. J. Neurosci. 27, 1365-1373.
41. Nicholls, J., and Wallace, B. G. (1978). Quantal analysis of transmitter release at an inhibitory synapse in the central nervous system of the leech. J. Physiol. 281, 171-185.
42. Nicoll, R. A., and Schmitz, D. (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6, 863-876.
43. Nurse, S., and Lacaille, J. C. (1999). Late maturation of GABA(B) synaptic transmission in area CA1 of the rat hippocampus. Neuropharmacology 38, 1733-1742.
44. Overstreet, L. S., Jones, M. V., and Westbrook, G. L. (2000). Slow desensitization regulates the availability of synaptic GABA(A) receptors. J. Neurosci. 20, 7914-7921.
45. Owens, D. F., and Kriegstein, A. R. (2002). Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727.
46. Poncer, J. C., McKinney, R. A., Gähwiler, B. H., and Thompson, S. M. (1997). Either N-or P-type calcium channels mediate GABA release at distinct hippocampal inhibitory synapses. Neuron 18, 463-472.
47. Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., Pirvola, U., Saarma, M., and Kaila, K. (1999). The K+/Cl+cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255.
48. Safiulina, V. F., Fattorini, G., Conti, F., and Cherubini, E. (2006). GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus. J. Neurosci. 26, 597-608.
49. Safiulina, V. F., Kasyanov, A. M., Giniatullin, R., and Cherubini, E. (2005). Adenosine down-regulates giant depolarizing potentials in the developing rat hippocampus by exerting a negative control on glutamatergic inputs. J. Neurophysiol. 94, 2797-2804.
50. Safiulina, V. F., Zacchi, P., Yaari, Y., Taglialatela, M., and Cherubini, E. (2008). Low expression of Kv7/M channels facilitates intrinsic and network bursting in the developing rat hippocampus. J. Physiol. 586, 5437-5453.
51. Salin, P. A., Scanziani, M., Malenka, R. C., and Nicoll, R. A. (1996). Distinct shortterm plasticity at two excitatory synapses in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 93, 13304-13309.
52. Schwarzer, C., and Sperk, G. (1995). Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69, 705-709.
53. Sipilä, S. T., Schuchmann, S., Voipio, J., Yamada, J., and Kaila, K. (2006). The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J. Physiol. 573, 765-773.
54. Sivakumaran, S., Mohajerani, M. H., and Cherubini, E. (2009). At immature mossy fiber-CA3 synapses correlated pre and postsynaptic activity persistently enhances GABA release and network excitability via BDNF and cAMP-dependent PKA. J. Neurosci. 29, 2637-2647.
55. Sloviter, R. S., Dichter, M. A., Rachinsky, T. L., Dean, E., Goodman. J. H., Sollas, A. L., and Martin, D. L. (1996). Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J. Comp. Neurol. 373, 593-618.
56. Thompson, S. M., Haas, H. L., and Gähwiler, B. H. (1992). Comparison of the actions of adenosine at preand postsynaptic receptors in the rat hippocampus in vitro. J. Physiol. 451, 347-363.
57. Toth, K., Suares, G., Lawrence, J. J., Philips-Tansey, E., and McBain, C. J. (2000). Differential mechanisms of transmission at three types of mossy fiber synapse. J. Neurosci. 20, 8279-8289.
58. Tyzio, R., Represa, A., Jorquera, I., Ben-Ari, Y., Gozlan, H., and Aniksztejn, L. (1999). The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci. 19, 10372-10382.
59. Uchigashima, M., Fukaya, M., Watanabe, M., and Kamiya, H. (2007). Evidence against GABA release from glutamatergic mossy fiber terminals in the developing hippocampus. J. Neurosci. 27, 8088-8100.
60. Vignes, M., and Collingridge, G. L. (1997). The synaptic activation of kainate receptors. Nature 388, 179-182.
61. Vogt, K. E., and Nicoll, R. A. (1999). Glutamate and gamma-aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 96, 1118-1122.
62. Walker, M. C., Ruiz, A., and Kullmann, D. M. (2001). Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses. Neuron 29, 703-715.
63. Weisskopf, M. G., Zalutsky, R. A., and Nicoll, R. A. (1993). The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 362, 423-427.
64. Zucker, R. S. (1989). Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31.
65. Zucker, R. S., and Regehr, W. G. (2002). Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405.