Ionotropic receptors at hippocampal mossy fibres: Roles in axonal excitability, synaptic transmission and plasticity

Frontiers in Neural Circuits

Volumn , Issue DEC, 2012, Pages

  Ruiz, Arnaud ^a   Kullmann, Dimitri ^b  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CALCIUM ION; GLYCINE RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM ION;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; BRAIN REGION; HIPPOCAMPAL MOSSY FIBER; IMMUNOLOCALIZATION; NERVE CELL PLASTICITY; NERVE ENDING; NERVE EXCITABILITY; NERVE FIBER; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC POTENTIAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BLOCKING; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

EID: 84871271243     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2012.00112     Document Type: Review

References (97)

1. Acsady, 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. Akaike, N., and Moorhouse, A.J. (2003). Techniques: applications of the nerve-bouton preparation in neuropharmacology. Trends Pharmacol Sci 24, 44-47.
3. Alle, H., and Geiger, J.R. (2005). NMDA receptors in hippocampal mossy fibers. Acta Physiol 186, supp 650.
4. Alle, H., and Geiger, J.R. (2007). GABAergic spill-over transmission onto hippocampal mossy fiber boutons. J Neurosci 27, 942-950.
5. Amaral, D.G., Ishizuka, N., and Claiborne, B. (1990). Neurons, numbers and the hippocampal network. Prog Brain Res 83, 1-11.
6. Araki, T., Yamano, M., Murakami, T., Wanaka, A., Betz, H., and Tohyama, M. (1988). Localization of glycine receptors in the rat central nervous system: an immunocytochemical analysis using monoclonal antibody. Neuroscience 25, 613-624.
7. Awatramani, G.B., Price, G.D., and Trussell, L.O. (2005). Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 48, 109-121.
8. Bahn, S., Volk, B., and Wisden, W. (1994). Kainate receptor gene expression in the developing rat brain. J Neurosci 14, 5525-5547.
9. Bardoni, R., Torsney, C., Tong, C.K., Prandini, M., and Macdermott, A.B. (2004). Presynaptic NMDA receptors modulate glutamate release from primary sensory neurons in rat spinal cord dorsal horn. J Neurosci 24, 2774-2781.
10. Bischofberger, J., Engel, D., Li, L., Geiger, J.R., and Jonas, P. (2006). Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc 1, 2075-2081.
11. Bortolotto, Z.A., Clarke, V.R., Delany, C.M., Parry, M.C., Smolders, I., Vignes, M., Ho, K.H., Miu, P., Brinton, B.T., Fantaske, R., Ogden, A., Gates, M., Ornstein, P.L., Lodge, D., Bleakman, D., and Collingridge, G.L. (1999). Kainate receptors are involved in synaptic plasticity. Nature 402, 297-301.
12. Brasier, D.J., and Feldman, D.E. (2008). Synapse-specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex. J Neurosci 28, 2199-2211.
13. Breustedt, J., and Schmitz, D. (2004). Assessing the role of GLUK5 and GLUK6 at hippocampal mossy fiber synapses. J Neurosci 24, 10093-10098.
14. Buchanan, K.A., Blackman, A.V., Moreau, A.W., Elgar, D., Costa, R.P., Lalanne, T., Tudor Jones, A.A., Oyrer, J., and Sjostrom, P.J. (2012). Target-Specific Expression of Presynaptic NMDA Receptors in Neocortical Microcircuits. Neuron 75, 451-466.
15. 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.
16. Castillo, P.E., Weisskopf, M.G., and Nicoll, R.A. (1994). The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 12, 261-269.
17. Cattaert, D., and El Manira, A. (1999). Shunting versus inactivation: analysis of presynaptic inhibitory mechanisms in primary afferents of the crayfish. J Neurosci 19, 6079-6089.
18. Chandler, K.E., Princivalle, A.P., Fabian-Fine, R., Bowery, N.G., Kullmann, D.M., and Walker, M.C. (2003). Plasticity of GABA(B) receptor-mediated heterosynaptic interactions at mossy fibers after status epilepticus. J Neurosci 23, 11382-11391.
19. Contractor, A., Mulle, C., and Swanson, G.T. (2012). Kainate receptors coming of age: milestones of two decades of research. Trends Neurosci 34, 154-163.
20. Contractor, A., Swanson, G., and Heinemann, S.F. (2001). Kainate receptors are involved in short- and long- term plasticity at mossy fiber synapses in the hippocampus. Neuron 29, 209-216.
21. Darstein, M., Petralia, R.S., Swanson, G.T., Wenthold, R.J., and Heinemann, S.F. (2003). Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23, 8013-8019.
22. Duguid, I.C., and Smart, T.G. (2004). Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7, 525-533.
23. Edwards, F.R., Harrison, P.J., Jack, J.J., and Kullmann, D.M. (1989). Reduction by baclofen of monosynaptic EPSPs in lumbosacral motoneurones of the anaesthetized cat. J Physiol (Lond) 416, 539-556.
24. Foster, A.C., Mena, E.E., Monaghan, D.T., and Cotman, C.W. (1981). Synaptic localization of kainic acid binding sites. Nature 289, 73-75.
25. Fricker, D., Verheugen, J.A., and Miles, R. (1999). Cell-attached measurements of the firing threshold of rat hippocampal neurones. J Physiol 517 (Pt 3), 791-804.
26. Geiger, J.R., and Jonas, P. (2000). Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. Neuron 28, 927-939.
27. Graham, B., and Redman, S. (1994). A simulation of action potentials in synaptic boutons during presynaptic inhibition. J Neurophysiol 71, 538-549.
28. Gulyas, A.I., Sik, A., Payne, J.A., Kaila, K., and Freund, T.F. (2001). The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13, 2205- 2217.
29. Harvey, R.J., and Rigo, J.M. (2010). Glycinergic transmission: physiological, developmental and pathological implications. Front Mol Neurosci 3.
30. Henze, D.A., Wittner, L., and Buzsaki, G. (2002). Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5, 790-795.
31. Hori, T., and Takahashi, T. (2009). Mechanisms underlying short-term modulation of transmitter release by presynaptic depolarization. J Physiol 587, 2987-3000.
32. Hubner, C.A., Stein, V., Hermans-Borgmeyer, I., Meyer, T., Ballanyi, K., and Jentsch, T.J. (2001). Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30, 515-524.
33. Ishikawa, T., Kaneko, M., Shin, H.S., and Takahashi, T. (2005). Presynaptic N-type and P/Q-type Ca2+ channels mediating synaptic transmission at the calyx of Held of mice. J Physiol 568, 199-209.
34. Jang, I.S., Jeong, H.J., and Akaike, N. (2001). Contribution of the Na-K-Cl cotransporter on GABA(A) receptor-mediated presynaptic depolarization in excitatory nerve terminals. J Neurosci 21, 5962-5972.
35. Jang, I.S., Nakamura, M., Ito, Y., and Akaike, N. (2006). Presynaptic GABAA receptors facilitate spontaneous glutamate release from presynaptic terminals on mechanically dissociated rat CA3 pyramidal neurons. Neuroscience 138, 25-35.
36. Jones, M.V., and Westbrook, G.L. (1995). Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15, 181-191.
37. Jung, M.W., and Mcnaughton, B.L. (1993). Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3, 165-182.
38. Kamiya, H., and Ozawa, S. (2000). Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J Physiol 523 Pt 3, 653-665.
39. Kidd, F.L., Coumis, U., Collingridge, G.L., Crabtree, J.W., and Isaac, J.T. (2002). A presynaptic kainate receptor is involved in regulating the dynamic properties of thalamocortical synapses during development. Neuron 34, 635-646.
40. Kirischuk, S., Clements, J.D., and Grantyn, R. (2002). Presynaptic and postsynaptic mechanisms underlie paired pulse depression at single GABAergic boutons in rat collicular cultures. J Physiol 543, 99-116.
41. Kullmann, D.M. (2001). Presynaptic kainate receptors in the hippocampus: slowly emerging from obscurity. Neuron 32, 561-564.
42. Kullmann, D.M., Ruiz, A., Rusakov, D.M., Scott, R., Semyanov, A., and Walker, M.C. (2005). Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: where and why? Prog Biophys Mol Biol 87, 33-46.
43. Kwon, H.B., and Castillo, P.E. (2008). Role of glutamate autoreceptors at hippocampal mossy fiber synapses. Neuron 60, 1082-1094.
44. Lauri, S.E., Bortolotto, Z.A., Bleakman, D., Ornstein, P.L., Lodge, D., Isaac, J.T., and Collingridge, G.L. (2001). A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 32, 697-709.
45. Lee, E.A., Cho, J.H., Choi, I.S., Nakamura, M., Park, H.M., Lee, J.J., Lee, M.G., Choi, B.J., and Jang, I.S. (2009). Presynaptic glycine receptors facilitate spontaneous glutamate release onto hilar neurons in the rat hippocampus. J Neurochem 109, 275-286.
46. Liu, H., Mantyh, P.W., and Basbaum, A.I. (1997). NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature 386, 721-724.
47. Liu, H., Wang, H., Sheng, M., Jan, L.Y., Jan, Y.N., and Basbaum, A.I. (1994). Evidence for presynaptic N- methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci U S A 91, 8383-8387.
48. Lukasiewicz, P.D., and Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. J Neurosci 14, 1213-1223.
49. Manabe, T., Wyllie, D.J., Perkel, D.J., and Nicoll, R.A. (1993). Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70, 1451-1459.
50. Monaghan, D.T., and Cotman, C.W. (1982). The distribution of [3H]kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res 252, 91-100.
51. More, J.C., Nistico, R., Dolman, N.P., Clarke, V.R., Alt, A.J., Ogden, A.M., Buelens, F.P., Troop, H.M., Kelland, E.E., Pilato, F., Bleakman, D., Bortolotto, Z.A., Collingridge, G.L., and Jane, D.E. (2004). Characterisation of UBP296: a novel, potent and selective kainate receptor antagonist. Neuropharmacology 47, 46-64.
52. Morkve, S.H., and Hartveit, E. (2009). Properties of glycine receptors underlying synaptic currents in presynaptic axon terminals of rod bipolar cells in the rat retina. J Physiol 587, 3813-3830.
53. Nicoll, R.A., and Schmitz, D. (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6, 863-876.
54. Nistico, R., Dargan, S.L., Amici, M., Collingridge, G.L., and Bortolotto, Z.A. (2012). Synergistic interactions between kainate and mGlu receptors regulate bouton Ca signalling and mossy fibre LTP. Sci Rep 1, 103.
55. Perrais, D., Coussen, F., and Mulle, C. (2009). Atypical functional properties of GluK3-containing kainate receptors. J Neurosci 29, 15499-15510.
56. Perrais, D., Pinheiro, P.S., Jane, D.E., and Mulle, C. (2009). Antagonism of recombinant and native GluK3- containing kainate receptors. Neuropharmacology 56, 131-140.
57. Perrais, D., and Ropert, N. (1999). Effect of zolpidem on miniature IPSCs and occupancy of postsynaptic GABAA receptors in central synapses. J Neurosci 19, 578-588.
58. Petralia, R.S., Wang, Y.X., and Wenthold, R.J. (1994). 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.
59. Pinheiro, P.S., and Mulle, C. (2008). Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9, 423-436.
60. Pinheiro, P.S., Perrais, D., Coussen, F., Barhanin, J., Bettler, B., Mann, J.R., Malva, J.O., Heinemann, S.F., and Mulle, C. (2007). GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci U S A 104, 12181-12186.
61. Price, G.D., and Trussell, L.O. (2006). Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held. J Neurosci 26, 11432-11436.
62. Pugh, J.R., and Jahr, C.E. (2012). NMDA receptor agonists fail to alter release from cerebellar basket cells. J Neurosci 31, 16550-16555.
63. Represa, A., Tremblay, E., and Ben-Ari, Y. (1987). Kainate binding sites in the hippocampal mossy fibers: localization and plasticity. Neuroscience 20, 739-748.
64. Rodriguez-Moreno, A., Kohl, M.M., Reeve, J.E., Eaton, T.R., Collins, H.A., Anderson, H.L., and Paulsen, O. (2012). Presynaptic induction and expression of timing-dependent long-term depression demonstrated by compartment-specific photorelease of a use-dependent NMDA receptor antagonist. J Neurosci 31, 8564-8569.
65. Rodriguez-Moreno, A., and Sihra, T.S. (2007). Metabotropic actions of kainate receptors in the CNS. J Neurochem 103, 2121-2135.
66. Ruiz, A., Campanac, E., Scott, R.S., Rusakov, D.A., and Kullmann, D.M. (2010). Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat Neurosci 13, 431-438.
67. 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.
68. Rusakov, D.A., and Kullmann, D.M. (1998). Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18, 3158-3170.
69. 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.
70. 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.
71. Schmitz, D., Frerking, M., and Nicoll, R.A. (2000). Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27, 327-338.
72. Schmitz, D., Mellor, J., Breustedt, J., and Nicoll, R.A. (2003). Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat Neurosci 6, 1058-1063.
73. Schmitz, D., Mellor, J., and Nicoll, R.A. (2001). Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291, 1972-1976.
74. Scott, R., Lalic, T., Kullmann, D.M., Capogna, M., and Rusakov, D.A. (2008). Target-cell specificity of kainate autoreceptor and Ca2+-store-dependent short-term plasticity at hippocampal mossy fiber synapses. J Neurosci 28, 13139-13149.
75. Scott, R., and Rusakov, D.A. (2006). Main determinants of presynaptic Ca2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. J Neurosci 26, 7071-7081.
76. Segev, I. (1990). Computer study of presynaptic inhibition controlling the spread of action potentials into axonal terminals. J Neurophysiol 63, 987-998.
77. Sherwood, J.L., Amici, M., Dargan, S.L., Culley, G.R., Fitzjohn, S.M., Jane, D.E., Collingridge, G.L., Lodge, D., and Bortolotto, Z.A. (2012). Differences in kainate receptor involvement in hippocampal mossy fibre long-term potentiation depending on slice orientation. Neurochem Int 61, 482-489.
78. Siegel, S.J., Brose, N., Janssen, W.G., Gasic, G.P., Jahn, R., Heinemann, S.F., and Morrison, J.H. (1994). Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc Natl Acad Sci U S A 91, 564-568.
79. Singer, J.H., and Berger, A.J. (1999). Contribution of single-channel properties to the time course and amplitude variance of quantal glycine currents recorded in rat motoneurons. J Neurophysiol 81, 1608-1616.
80. Sjostrom, P.J., Turrigiano, G.G., and Nelson, S.B. (2003). Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641-654.
81. Stell, B.M., Brickley, S.G., Tang, C.Y., Farrant, M., and Mody, I. (2003). Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc Natl Acad Sci U S A 100, 14439-14444.
82. Tachibana, M., and Kaneko, A. (1984). gamma-Aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types. Proc Natl Acad Sci U S A 81, 7961-7964.
83. Takahashi, T., and Momiyama, A. (1991). Single-channel currents underlying glycinergic inhibitory postsynaptic responses in spinal neurons. Neuron 7, 965-969.
84. Trigo, F.F., Chat, M., and Marty, A. (2007). Enhancement of GABA release through endogenous activation of axonal GABA(A) receptors in juvenile cerebellum. J Neurosci 27, 12452-12463.
85. Turecek, R., and Trussell, L.O. (2001). Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature 411, 587-590.
86. Turecek, R., and Trussell, L.O. (2002). Reciprocal developmental regulation of presynaptic ionotropic receptors. Proc Natl Acad Sci U S A 99, 13884-13889.
87. Tyzio, R., Ivanov, A., Bernard, C., Holmes, G.L., Ben-Ari, Y., and Khazipov, R. (2003). Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90, 2964-2972.
88. Verdier, D., Lund, J.P., and Kolta, A. (2003). GABAergic control of action potential propagation along axonal branches of mammalian sensory neurons. J Neurosci 23, 2002-2007.
89. Verheugen, J.A., Fricker, D., and Miles, R. (1999). Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J Neurosci 19, 2546-2555.
90. Vignes, M., and Collingridge, G.L. (1997). The synaptic activation of kainate receptors. Nature 388, 179-182.
91. 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.
92. Wachowiak, M., and Cohen, L.B. (1999). Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle. J Neurosci 19, 8808-8817.
93. Wall, P.D. (1958). Excitability changes in afferent fibre terminations and their relation to slow potentials. J Physiol 142, 1-21.
94. Wiebe, S.P., and Staubli, U.V. (1999). Dynamic filtering of recognition memory codes in the hippocampus. J Neurosci 19, 10562-10574.
95. Ye, J.H., Wang, F., Krnjevic, K., Wang, W., Xiong, Z.G., and Zhang, J. (2004). Presynaptic glycine receptors on GABAergic terminals facilitate discharge of dopaminergic neurons in ventral tegmental area. J Neurosci 24, 8961-8974.
96. Zhang, S.J., and Jackson, M.B. (1993). GABA-activated chloride channels in secretory nerve endings. Science 259, 531-534.
97. Zucker, R.S., Kullmann, D.M., and Bennett, M. (1998). Release of neurotransmitters, in Fundamental Neuroscience, eds. M.J. Zigmond, F.E. Bloom, S.C. Landis, J.L. Roberts & L.R. Squire. (London: Academic Press), 155-192.