Cell-type specific GABA synaptic transmission and activity-dependent plasticity in rat hippocampal stratum radiatum interneurons

European Journal of Neuroscience

Volumn 22, Issue 1, 2005, Pages 179-188

  Patenaude, Christian ^a   Massicotte, Guy ^b   Lacaille, Jean Claude ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

Author keywords

GABAergic synapses; Hippocampus; IPSCs; Sprague Dawley rat; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR ANTAGONIST;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; ELECTRIC CURRENT; ELECTRIC POTENTIAL; ELECTROSTIMULATION; GABAERGIC TRANSMISSION; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; KINETICS; LONG TERM POTENTIATION; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RAT STRAIN; SYNAPSE; SYNAPTIC TRANSMISSION; THETA BURST STIMULATION; VOLTAGE CLAMP;

ANIMALS; CELL SHAPE; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; MALE; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-B; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 23044458148     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04207.x     Document Type: Article

References (67)

1. Aaron, G.B. & Dichter, M.A. (2001) Excitatory synapses from CA3 pyramidal cells onto neighboring pyramidal cells differ from those onto inhibitory interneurons. Synapse, 42, 199-202.
2. Acsády, L., Göres, T.J. & Freund, T.F. (1996) Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience, 73, 317-334.
3. Atzori, M. (1996) Pyramidal cells and stratum lacunosum-moleculare interneurons in the CA1 hippocampal region share a GABAergic spontaneous input. Hippocampus, 6, 72-78.
4. Bacci, A., Huguenard, J.R. & Prince, D.A. (2002) Differential modulation of synaptic transmission by neuropeptide Y in rat neocortical neurons. Proc. Natl Acad. Sci. USA, 99, 17125-17130.
5. Bacci, A., Rudolph, U., Huguenard, J.R. & Prince, D.A. (2003) Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J. Neurosci., 23, 9664-9674.
6. Bartos, M., Vida, I., Frotscher, M., Geiger, J.R. & Jonas, P. (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J. Neurosci., 21, 2687-2698.
7. Bartos, M., Vida, I., Frotscher, M., Meyer, A., Monyer, H., Geiger, J.R. & Jonas, P. (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl Acad. Sci. USA, 99, 13222-13227.
8. Beierlein, M., Gibson, J.R. & Connors, B.W. (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol., 90, 2987-3000.
9. Bibbig, A., Traub, R.D. & Whittington, M.A. (2002) Long-range synchronization of γ and β oscillations and the plasticity of excitatory and inhibitory synapses: a network model. J. Neurophysiol., 88, 1634-1654.
10. Bischofberger, J. & Jonas, P. (2002) TwoB or not twoB: differential transmission at glutamatergic mossy fiber-interneuron synapses in the hippocampus. TINS, 25, 600-603.
11. Chapman, C.A. & Lacaille, J.C. (1999a) Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J. Neurosci., 19, 8637-8645.
12. Chapman, C.A. & Lacaille, J.C. (1999b) Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J. Neurophysiol., 81, 1296-1307.
13. Chevaleyre, V. & Castillo, P.E. (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron, 38, 461-472.
14. Christie, B.R., Franks, K.M., Seamans, J.K., Saga, K. & Sejnowski, T.J. (2000) Synaptic plasticity in morphologically identified CA1 stratum radiatum interneurons and giant projection cells. Hippocampus, 10, 673-683.
15. Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O. & Somogyi, P. (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature, 378, 75-78.
16. Cowan, A.I., Stricker, C., Reece, L.J. & Redman, S.J. (1998) Long-term plasticity at excitatory synapses on aspinous interneurons in area CA1 lacks synaptic specificity. J. Neurophysiol., 79, 13-20.
17. Duguid, I.C. & Smart, T.G. (2004) Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nature Neurosci., 7, 525-533.
18. Ferraguti, F., Cobden, P., Pollard, M., Cope, D., Shigemoto, R., Watanabe, M. & Somogyi, P. (2004) Immunolocalization of metabotropic glutamate receptor 1α (mGluR1α) in distinct classes of interneuron in the CA1 region of the rat hippocampus. Hippocampus, 14, 193-215.
19. Freund, T.F. & Antal, M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336, 170-173.
20. Fritschy, J.M. & Möhler, H. (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neurol., 359, 154-194.
21. Gaiarsa, J.L., Caillard, O. & Ben-Ari, Y. (2002) Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. TINS, 25, 564-570.
22. Gao, B. & Fritschy, J.M. (1994) Selective allocation of GABAA receptors containing the alpha 1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons. Ew. J. Neurosci., 6, 837-853.
23. Geiger, J.R., Lubke, J., Roth, A., Frotscher, M. & Jonas. P. (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron, 18, 1009-1023.
24. Gulyás, A.I., Hájos, N. & Freund, T.F. (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci., 16, 3397-3411.
25. Gulyás, A.I., Megias, M., Emri, Z. & Freund, T.F. (1999) Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci., 19, 10082-10097.
26. Gupta, A., Wang, Y. & Markram, H. (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science, 287, 273-278.
27. Hájos, N. & Mody, I. (1997) Synaptic communication among hippocampal interneurons: Properties of spontaneous IPSCs in morphologically identified cells. J. Neurosci., 17, 8427-8442.
28. Hoffman, A.F., Riegel, A.C. & Lupica, C.R. (2003) Functional localization of cannabinoid receptors and endogenous cannabinoid production in distinct neuron populations of the hippocampus. Eur. J. Neurosci., 18, 524-534.
29. van Hooft, J.A., Giuffrida, R., Blatow, M. & Monyer, H. (2000) Differential expression of group 1 metabotropic glutamate receptors in functionally distinct hippocampal interneurons. J. Neurosci., 20, 3544-3551.
30. Jones, M.V. & Westbrook, G.L. (1997) Shaping of IPSCs by endogenous calcineurin activity. J. Neurosci., 17, 7626-7633.
31. 2+/calmodulin-dependent kinase II. Proc. Natl Acad. Sci. USA, 93, 13351-13356.
32. Katona, I., Sperlágh, B., Sik, A., Käfalvi, A., Vizi, E.S., Mackie, K. & Freund, T.F. (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci., 19, 4544-4558.
33. Khazipov, R., Congar, P. & Ben-Ari, Y. (1995) Hippocampal CA1 lacunosum-moleculare interneurons: modulation of monosynaptic GABAergic IPSCs by presynaptic GABAB receptors. J. Neurophysiol., 74, 2126-2137.
34. 2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses. J. Neurosci., 16, 6342-6352.
35. B2 in the rat hippocampus. J. Neurosci., 23, 11026-11035.
36. Lacaille, J.C. (1991) Postsynaptic potentials mediated by excitatory and inhibitory amino acids in interneurons of stratum pyramidale of the CA1 region of rat hippocampal slices in vitro. J. Neurophysiol., 66, 1441-1454.
37. Lapointe, V., Morin, F., Ratte, S., Croce, A., Conquet, F. & Lacaille, J.C. (2004) Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition. J. Physiol. (Lond.), 555, 125-135.
38. Lei, S. & McBain, C.J. (2002) Distinct NMDA receptors provide differential modes of transmission at mossy fiber-interneuron synapses. Neuron, 33, 921-933.
39. Llano, I., Leresche, N. & Marty, A. (1991) Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron, 6, 565-574.
40. Lu, Y.M., Mansuy, I.M., Kandel, E.R. & Roder, J. (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron, 26, 197-205.
41. Maccaferri, G. & McBain, C.J. (1996) Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J. Neurosci., 16, 5334-5343.
42. Malenka, R.C. & Nicoll, R.A. (1999) Long-term potentiation - a decade of progress? Science, 285, 1870-1874.
43. Malinow, R. & Tsien, R.W. (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature, 346, 177-180.
44. Marsicano, G. & Lutz, B. (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci., 11, 4213-4225.
45. McLean, H.A., Caillard, O., Ben-Ari, Y. & Gaiarsa, J.L. (1996) Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus. J. Physiol. (Lond.), 496, 471-477.
46. McMahon, L.L. & Kauer, J.A. (1997) Hippocampal interneurons express a novel form of synaptic plasticity. Neuron, 18, 295-305.
47. Nunzi, M.G., Gorio, A., Milan, F., Freund, T.F., Somogyi, P. & Smith, A.D. (1985) Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus. J. Comp. Neurol., 237, 485-505.
48. Nusser, Z., Sieghart, W., Benke, D., Fritschy, J.M. & Somogyi, P. (1996) Differential synaptic localization of two major gamma-aminobutyric acid type A receptor α subunits on hippocampal pyramidal cells. Proc. Natl Acad. Sci. USA, 93, 11939-11944.
49. A receptors by cAMP-dependent protein kinase in mouse cerebellar and olfactory bulb neurones. J. Physiol. (Lond.), 521, 421-435.
50. Ohno-Shosaku, T., Maejima, T. & Kano, M. (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron, 29, 729-738.
51. A receptor α subunits expression with the properties of IPSCs in the developing thalamus. J. Neurosci., 20, 2202-2208.
52. A synaptic transmission. J. Physiol. (Lond.), 553, 155-167.
53. Perez, Y., Chapman, C.A., Woodhall, G.R.R., Robitaille, R. & Lacaille, J.C. (1999) Differential induction of long lasting potentiation of IPSPs by theta patterned stimulation versus 100 HZ. tetanization in hippocampal pyramidal cells in vitro. Neuroscience, 90, 747-757.
54. Perez, Y., Morin, F. & Lacaille, J.C. (2001) A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc. Natl Acad. Sci. USA, 98, 9401-9406.
55. Pitler, T.A. & Alger, B.E. (1992) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J. Neurosci., 12, 4122-4132.
56. A receptor function by PKA and PKC in adult hippocampal neurons. J. Neurosci., 19, 674-683.
57. Saitow, F., Murakoshi, T., Suzuki, H. & Konishi, S. (2005) Metabotropic P2Y purinoceptor-mediated presynaptic and postsynaptic enhancement of cerebellar GABAergic transmission. J. Neurosci., 25, 2108-2116.
58. Semyanov, A. & Kullmann, D.M. (2002) Relative picrotoxin insensitivity distinguishes ionotropic GABA receptor-mediated IPSCs in hippocampal interneurons. Neuropharmacology, 43, 726-736.
59. Shew, T., Yip, S. & Sastry, B.R. (2000) Mechanisms involved in tetanus-induced potentiation of fast IPSCs in rat hippocampal CA1 neurons. J. Neurophysiol., 83, 3388-3401.
60. Thompson, S.M. (1994) Modulation of inhibitory synaptic transmission in the hippocampus. Prog. Neurobiol., 42, 575-609.
61. Tsou, K., Mackie, K., Sañudo-Peña, M.C. & Walker, J.M. (1999) Cannabinoid CB1 receptors are localized primarily on cholecystokinin- containing GABAergic interneurons in the rat hippocampal formation. Neuroscience, 93, 969-975.
62. A receptor α1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J. Neurosci., 21, 3009-3016.
63. Vida, I., Halasy, K., Szinyei, K., Somogyi, P. & Buhl, E.H. (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.
64. Walker, H.C., Lawrence, J.J. & McBain, C.J. (2002) Activation of kinetically distinct synaptic conductances on inhibitory interneurons by electrotonically overlapping afferents. Neuron, 35, 161-171.
65. Wang, X.J. & Buzsaki, G. (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci., 16, 6402-6413.
66. Wilson, R.I. & Nicoll, R.A. (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature, 410, 588-592.
67. Woodin, M.A., Ganguly, K. & Poo, M.M. (2003) Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in C1 transporter activity. Neuron, 39, 807-820.