Control of GABA release at mossy fiber-CA3 connections in the developing hippocampus

Frontiers in Synaptic Neuroscience

Volumn , Issue FEB, 2010, Pages

  Safiulina, Victoria F ^a   Caiati, Maddalena D ^a   Sivakumaran, Sudhir ^a   Bisson, Giacomo ^a   Migliore, Michele ^b   Cherubini, Enrico ^a  

^a SISSA   (Italy)

^b CNR   (Italy)

Author keywords

Activity dependent plasticity; Developing hippocampus; GABA A mediated post synaptic currents; Mossy fibres; Presynaptic GABA B receptors; Presynaptic GluK1 receptors; Quantal analysis; Realistic modelling

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; CALCIUM; GLUTAMIC ACID; KAINIC ACID RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ADULTHOOD; DENTATE GYRUS; DEPOLARIZATION; DOWN REGULATION; ELECTRIC CURRENT; EXTRACELLULAR SPACE; GRANULE CELL; HIPPOCAMPAL CA3 REGION; HUMAN; INTERNEURON; MOSSY FIBER; NERVE EXCITABILITY; NERVE FIBER; PERINATAL PERIOD; PHENOTYPE; PRESYNAPTIC NERVE; PYRAMIDAL NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 80054862125     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/neuro.19.001.2010     Document Type: Review

References (80)

1. Acsády, L., Kamondi, A., Sik, A., Freund, T., and Buzsaki, G. (1998). GABAergic cells are the major postsynaptic targets of mossy FIbers in the rat hippocampus. J. Neurosci. 18, 3386-3403.
2. Alle, H., and Geiger, J. R. (2007). GABAergic spill-over transmission onto hippocampal mossy FIber boutons. J, Neurosci. 27, 942-950.
3. 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.
4. Amaral, D. G., and Dent, J. A. (1981). 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.
5. Bahn, S., Volk, B., and Wisden, W. (1994). Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14, 5525-5547.
6. Bekkers, J. M. (2005). Presynaptically silent GABA synapses in hippocampus. J. Neurosci. 25, 4031-4039.
7. 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.
8. 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.
9. Bergersen, L., Ruiz, A., Bjaalie, J. G, Kullmann, D. M., and Gundersen, V. (2003). GABA and GABAA receptors at hippocampal mossy FIbre synapses. Eur. J. Neurosci. 18, 931-941.
10. Bettler, B., Boulter, J., Hermans-Borgmeyer, I., O'Shea-Greenfield, A., Deneris, E. S., Moll, C., Borgmeyer, U., Hollmann, M., and Heinemann, S. (1990). Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583-595.
11. Bischofberger, J., Engel, D., Frotscher, M., and Jonas, P. (2006). Timing and efFI-cacy of transmitter release at mossy fiber synapses in the hippocampal network. PFlugers Arch. 453, 361-372.
12. Buzsaki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929.
13. Caiati, M. D., Sivakumaran, S., and Cherubini, E. (2010). In the developing rat hippocampus, endogenous activation of presynaptic kainate receptors reduces GABA release from mossy FIber terminals. J. Neurosci. 30, 1750-1759.
14. 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.
15. Danbolt, N. C. (2001). Glutamate uptake. Prog. Neurobiol. 65, 1-105.
16. 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.
17. Durand, G. M., Kovalchuk, Y., and Konnerth, A. (1996). Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381, 71-75.
18. 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.
19. Edwards, F. A., Konnerth, A. and Sakmann, B. (1990). Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J. Physiol. 430, 213-249.
20. 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.
21. Frotscher, M., Jonas, P., and Sloviter, R. S. (2006). Synapses formed by normal and abnormal hippocampal mossy FIbers. Cell Tissue Res. 326, 361-367.
22. Gaarskjaer, F. B. (1985). The development of the dentate area and the hippocampal mossy FIber projection of the rat. J. Comp. Neurol. 241, 154-170.
23. 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.
24. 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.
25. Gillespie, D. C., Kim, G., and Kandler, K. (2005). Inhibitory synapses in the developing auditory system are glutamatergic. Nat. Neurosci. 8, 332-338.
26. Gómez-Lira, G., Lamas, M., Romo-Parra, H., and Gutiérrez, R. (2005). Programmed and induced phenotype of the hippocampal granule cells. J. Neurosci. 25:6939-6946.
27. Gutierrez, R., and Heinemann, U. (2001). Kindling induces transient fast inhibition in the dentate gyrus-CA3 projection. Eur. J. Neurosci. 13, 1371-1379.
28. 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.
29. Hemond, P., Epstein, D., Boley, A., Migliore, M., Ascoli, G. A., and Jaffe, D. B. (2008). Distinct classes of pyramidal cells exhibit mutually exclusive FIring patterns in hippocampal area CA3b. Hippocampus 18, 411-24.
30. Henze, D. A., Urban, N. N., and Barrionuevo, G. (2000). The multifarious hippocampal mossy FIber pathway: a review. Neuroscience 98, 407-427.
31. Jaffe, D. B., and Gutiérrez, R. (2007). Mossy fiber synaptic transmission: communication from the dentate gyrus to area CA3. Prog. Brain. Res. 163, 109-132.
32. Jonas, P., Bischofberger, J., and Sandkuhler, J. (1998). Corelease of two fast neurotransmitters at a central synapse. Science 281, 419-424.
33. 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.
34. 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.
35. Kannenberg, K., Sieghart, W., and Reuter, H. (1999). Clusters of GABAA receptors on cultured hippocampal cells correlate only partially with functional synapses. Eur. J. Neurosci. 11, 1256-1264.
36. Kasyanov, A. M., Safiulina, V. F., Voronin, L. L., and Cherubini, E. (2004). GABAmediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efFIcacy in the developing hippocampus. Proc. Natl. Acad. Sci. U.S.A. 101, 3967-3972.
37. Kerchner, G. A., and Nicoll, R. A. (2008). Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat. Rev. Neurosci. 9, 813-825.
38. 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.
39. Lanthorn, T. H., Ganong, A. H., and Cotman, C. W. (1984). 2-Amino-4-phosphonobutyrate selectively blocks mossy FIber-CA3 responses in guinea pig but not rat hippocampus. Brain Res. 290, 174-178.
40. Lauri, S. E., Segerstråle, M., Vesikansa, A., Maingret, F., Mulle, C., Collingridge, G. L., Isaac, J. T., and Taira, T. (2005). Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus. J. Neurosci. 25, 4473-4484.
41. Lauri, S. E., Vesikansa, A., Segerstråle, M., Collingridge, G. L., Isaac, J. T., and Taira, T. (2006). Functional maturation of CA1 synapses involves activity-dependent loss of tonic kainate receptor-mediated inhibition of glutamate release. Neuron 50, 415-429.
42. 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.
43. Leinekugel, X., Khazipov, R., Cannon, R., Hirase, H., Ben-Ari, Y., and Buzsaki, G (2002). Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296, 2049-2052.
44. Malenka, R. C., and Nicoll, R. A. (1997). Silent synapses speak up. Neuron 19, 473-476.
45. Malinow, R., Mainen, Z. F., and Hayashi, Y. (2000). LTP mechanisms: from silence to four-lane trafFIc. Curr. Opin. Neurobiol. 10, 352-357.
46. Marchionni, I., Omrani, A., and Cherubini, E. (2007). In the developing rat hippocampus a tonic GABAA-mediated conductance selectively enhances the glutamatergic drive of principal cells. J. Physiol. 581, 515-528.
47. McBain, C. J. (2008). Differential mechanisms of transmission and plasticity at mossy FIber synapses. Prog. Brain Res. 169, 225-240.
48. 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.
49. Mohajerani, M. H., Sivakumaran, S., Zacchi, P., Aguilera, P., and Cherubini, E. (2007). Correlated network activity enhances synaptic efFIcacy via BDNF and the ERK pathway at immature CA3-CA1 connections in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 104, 13176-13181.
50. Montgomery, J. M., Pavlidis, P., and Madison, D. V. (2001). Pair recordings reveal all-silent synaptic connections and the postsynaptic expression of long-term potentiation. Neuron 29, 691-701.
51. Nakamura, M., Sekino, Y., and Manabe, T. (2007). GABAergic interneurons facilitate mossy FIber excitability in the developing hippocampus. J. Neurosci. 27, 1365-1373.
52. Nicoll, R. A., and Schmitz, D. (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6, 863-876.
53. O'Malley, D. M., and Masland, R. H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proc. Natl. Acad. Sci. U.S.A. 86, 3414-3418.
54. Ottersen, O. P., and Storm-Mathisen, J. (1984). Neurons containing or accumulating transmitter amino acids. In Handbook of Chemical Neuroanatomy, A. Bjorklund, T. Hokfelt and M. J. Kuhar, eds (Amsterdam, Elsevier). pp. 141-246.
55. Overstreet, L. S., Pasternak, J. F., Colley, P. A., Slater, N. T., and Trommer, B.L. (1997). Metabotropic glutamate receptor mediated long-term depression in developing hippocampus. Neuropharmacology 36, 831-844.
56. Rao, A., Cha, E. M., and Craig, A. M. (2000). Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J. Neurosci. 20, 8344-8353.
57. Ramon y Cajal, S. R. (1911). Histologie du Système Nerveux de l'Homme et des Vertébrés, Vol. II. Maloine, Paris
58. Redman, S. (1990). Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev. 70, 165-198.
59. Ritter, L. M., Vazquez, D. M., and Meador-Woodruff, J. H. (2002). Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res. Dev. Brain Res. 139, 227-236.
60. Romo-Parra, H., Vivar, C., Maqueda, J., Morales, M. A., and Gutierrez, R. (2003). Activity-dependent induction of multitransmitter signaling onto pyramidal cells and interneurons of hippocampal area CA3. J. Neurophysiol. 89, 3155-3167.
61. Ruiz, A., Fabian-Fine, R., Scott, R., Walker, M. C., Rusakov, D. A., and Kullmann, D. M. (2003). GABAA receptors at hippocampal mossy fibers. Neuron 39, 961-973.
62. Safiulina, V. F., and Cherubini, E. (2009). At immature mossy FIbers-CA3 connections, activation of presynaptic GABA(B) receptors by endogenously released GABA contributes to synapses silencing. Front. Cell. Neurosci. 3, 1-11. doi: 10.3389/neuro.03.001.2009.
63. 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.
64. Salin, P. A., Scanziani, M., Malenka, R. C., and Nicoll, R. A. (1996). Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 93, 13304-13309.
65. Schwarzer, C., and Sperk, G. (1995). Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69, 705-709.
66. Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P. J., Neki, A., Abe, T., Nakanishi, S., and Mizuno, N. (1997). Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17, 7503-7522.
67. 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.
68. Sivakumaran, S., Mohajerani, M. H., and Cherubini, E. (2009). At immature mossy-fiber-CA3 synapses, correlated presynaptic and postsynaptic activity persistently enhances GABA release and network excitability via BDNF and cAMP-dependent PKA. J. Neurosci. 29, 2637-2647.
69. 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.
70. Stirling, R. V., and Bliss, T. V. (1978). Hippocampal mossy FIber development at the ultrastructural level. Prog. Brain Res. 48, 191-198.
71. 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.
72. Trigo, F. F., Marty, A., and Stell, B. M. (2008). Axonal GABAA receptors. Eur. J. Neurosci. 28:841-848.
73. Tyzio, R., Holmes, G. L., Ben-Ari, Y., and Khazipov, R. (2007). Timing of the developmental switch in GABA(A) mediated signaling from excitation to inhibition in CA3 rat hippocampus using gramicidin perforated patch and extracellular recordings. Epilepsia 48, 96-105.
74. 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.
75. Urban, N. N., Henze, D. A. and Barrionuevo, G. (2001). Revisiting the role of the hippocampal mossy fiber synapse. Hippocampus 11, 408-417.
76. Vignes, M., and Collingridge, G. L. (1997). The synaptic activation of kainate receptors. Nature 388, 179-182.
77. 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.
78. Voronin, L. L., and Cherubini, E. (2004). 'Deaf, mute and whispering' silent synapses: their role in synaptic plasticity. J. Physiol. 557, 3-12.
79. 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.
80. 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.