Schaffer collateral and perforant path inputs activate different subtypes of NMDA receptors on the same CA1 pyramidal cell

British Journal of Pharmacology

Volumn 142, Issue 2, 2004, Pages 317-322

  Arrigoni, Elda ^a   Greene, Robert W ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

EPSC decay kinetics; Ifenprodil; NMDA receptor mediated EPSC; NR2B subunit; Perforant pathway; Schaffer collateral; Whole cell patch clamp

Indexed keywords

AMPA RECEPTOR; IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STATISTICAL SIGNIFICANCE; STEREOCHEMISTRY; SYNAPSE;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; N-METHYLASPARTATE; PERFORANT PATHWAY; PYRAMIDAL CELLS; QUINOXALINES; RATS; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 2942605738     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705744     Document Type: Article

References (54)

1. AULT, B. & NADLER, J.V. (1982). Baclofen selectively inhibits transmission at synapses made by axons of CA3 pyramidal cells in the hippocampal slice. J. Pharmacol. Exp. Ther., 223, 291-297.
2. BARTH, A.L. & MALENKA, R.C. (2001). NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses. Nat. Neurosci., 4, 235-236.
3. BERGERON, R., MEYER, T.M., COYLE, J.T. & GREENE, R.W. (1998). Modulation of N-methyl-D-aspartate receptor function by glycine transport. Proc. Natl. Acad. Sci. U.S.A., 95, 15730-15734.
4. BICKLER, P.E., FAHLMAN, C.S. & TAYLOR, D.M. (2003). Oxygen sensitivity of NMDA receptors: relationship to NR2 subunit composition and hypoxia tolerance of neonatal neurons. Neuroscience, 118, 25-35.
5. BRANDOLI, C., SANNA, A., DE BERNARDI, M.A., FOLLESA, P., BROOKER, G. & MOCCHETTI, I. (1998). Brain-derived neurotrophic factor and basic fibroblast growth factor downregulate NMDA receptor function in cerebellar granule cells. J. Neurosci., 18, 7953-7961.
6. BRIMECOMBE, J.C., BOECKMAN, F.A. & AIZENMAN, E. (1997). Functional consequences of NR2 subunit composition in single recombinant N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A., 94, 11019-11024.
7. CHAPMAN, D.E., KEEFE, K.A. & WILCOX, K.S. (2003). Evidence for functionally distinct synaptic NMDA receptors in ventromedial versus dorsolateral striatum. J. Neurophysiol., 89, 69-80.
8. CHEN, N., LUO, T. & RAYMOND, L.A. (1999). Subtype-dependence of NMDA receptor channel open probability. J. Neurosci., 19, 6844-6854.
9. COLBERT, C.M. & LEVY, W.B. (1992). Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol., 68, 1-8.
10. CULL-CANDY, S., BRICKLEY, S. & FARRANT, M. (2001). NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol., 11, 327-335.
11. DINGLEDINE, R., BORGES, K., BOWIE, D. & TRAYNELIS, S.F. (1999). The glutamate receptor ion channels. Pharmacol. Rev., 51, 7-61.
12. FLINT, A.C., MAISCH, U.S., WEISHAUPT, J.H., KRIEGSTEIN, A.R. & MONYER, H. (1997). NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci., 17, 2469-2476.
13. FORREST, D., YUZAKI, M., SOARES, H.D., NG, L., LUK, D.C., SHENG, M., STEWART, C.L., MORGAN, J.I., CONNOR, J.A. & CURRAN, T. (1994). Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron, 13, 325-338.
14. HASSELMO, M.E. & SCHNELL, E. (1994). Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J. Neurosci., 14, 3898-3914.
15. HAUSSER, M. & ROTH, A. (1997). Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method. J. Neurosci., 17, 7606-7625.
16. HAWKINS, L.M., CHAZOT, P.L. & STEPHENSON, F.A. (1999). Biochemical evidence for the co-association of three N-methyl-D-aspartate (NMDA) R2 subunits in recombinant NMDA receptors. J. Biol. Chem., 274, 27211-27218.
17. HESTRIN, S. (1992). Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature, 357, 686-689.
18. HESTRIN, S., NICOLL, R.A., PERKEL, D.J. & SAH, P. (1990). Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J. Physiol., 422, 203-225.
19. HIROI, N., MAREK, G.J., BROWN, J.R., YE, H., SAUDOU, F., VAIDYA, V.A., DUMAN, R.S., GREENBERG, M.E. & NESTLER, E.J. (1998). Essential role of the fosB gene in molecular, cellular, and behavioral actions of chronic electroconvulsive seizures. J. Neurosci., 18, 6952-6962.
20. ITO, I., KAWAKAMI, R., SAKIMURA, K., MISHINA, M. & SUGIYAMA, H. (2000). Input-specific targeting of NMDA receptor subtypes at mouse hippocampal CA3 pyramidal neuron synapses. Neuropharmacology, 39, 943-951.
21. JAROLIMEK, W., DEMMELHUBER, J., BIJAK, M. & MISGELD, U. (1993). CGP 55845A blocks baclofen, gamma-aminobutyric acid and inhibitory postsynaptic potassium currents in guinea pig CA3 neurons. Neurosci. Lett., 154, 31-34.
22. KAWAKAMI, R., SHINOHARA, Y., KATO, Y., SUGIYAMA, H., SHIGEMOTO, R. & ITO, I. (2003). Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science, 300, 990-994.
23. KEW, J.N., RICHARDS, J.G., MUTEL, V. & KEMP, J.A. (1998). Developmental changes in NMDA receptor glycine affinity and ifenprodil sensitivity reveal three distinct populations of NMDA receptors in individual rat cortical neurons. J. Neurosci., 18, 1935-1943.
24. KEW, J.N., TRUBE, G. & KEMP, J.A. (1996). A novel mechanism of activity-dependent NMDA receptor antagonism describes the effect of ifenprodil in rat cultured cortical neurones. J. Physiol., 497 (Part 3), 761-772.
25. KIRSON, E.D. & YAARI, Y. (1996). Synaptic NMDA receptors in developing mouse hippocampal neurones: functional properties and sensitivity to ifenprodil. J. Physiol., 497 (Part 2), 437-455.
26. KOVALCHUK, Y., EILERS, J., LISMAN, J. & KONNERTH, A. (2000). NMDA receptor-mediated subthreshold Ca(2 +) signals in spines of hippocampal neurons. J. Neurosci., 20, 1791-1799.
27. KRUPP, J.J., VISSEL, B., HEINEMANN, S.F. & WESTBROOK, G.L. (1996). Calcium-dependent inactivation of recombinant N-methyl-D-aspartate receptors is NR2 subunit specific. Mol. Pharmacol., 50, 1680-1688.
28. KUMAR, S.S. & HUGUENARD, J.R. (2003). Pathway-specific differences in subunit composition of synaptic NMDA receptors on pyramidal neurons in neocortex. J. Neurosci., 23, 10074-10083.
29. KUTSUWADA, T., KASHIWABUCHI, N., MORI, H., SAKIMURA, K., KUSHIYA, E., ARAKI, K., MEGURO, H., MASAKI, H., KUMANISHI, T., ARAKAWA, M. & MISHINA, M (1992). Molecular diversity of the NMDA receptor channel. Nature, 358, 36-41.
30. LEI, S. & MCBAIN, C.J. (2002). Distinct NMDA receptors provide differential modes of transmission at mossy fiber-interneuron synapses. Neuron, 33, 921-933.
31. LOFTIS, J.M. & JANOWSKY, A. (2003). The N-methyl-d-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol. Ther., 97, 55-85.
32. LOPEZ DE ARMENTIA, M. & SAH, P. (2003). Development and subunit composition of synaptic NMDA receptors in the amygdala: NR2B synapses in the adult central amygdala. J. Neurosci., 23, 6876-6883.
33. MARKS, J.D., FRIEDMAN, J.E. & HADDAD, G.G. (1996). Vulnerability of CA1 neurons to glutamate is developmentally regulated. Brain Res. Dev. Brain Res., 97, 194-206.
34. MCBAIN, C.J. & MAYER, M.L. (1994). N-methyl-D-aspartic acid receptor structure and function. Physiol. Rev., 74, 723-760.
35. MOMIYAMA, A. (2000). Distinct synaptic and extrasynaptic NMDA receptors identified in dorsal horn neurones of the adult rat spinal cord. J. Physiol., 523 (Part 3), 621-628.
36. MONYER, H., BURNASHEV, N., LAURIE, D.J., SAKMANN, B. & SEEBURG, P.H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529-540.
37. MONYER, H., SPRENGEL, R., SCHOEPFER, R., HERB, A., HIGUCHI, M., LOMELI, H., BURNASHEV, N., SAKMANN, B. & SEEBURG, P.H. (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science, 256, 1217-1221.
38. MOTT, D.D., DOHERTY, J.J., ZHANG, S., WASHBURN, M.S., FENDLEY, M.J., LYUBOSLAVSKY, P., TRAYNELIS, S.F. & DINGLEDINE, R. (1998). Phenylethanolamines inhibit NMDA receptors by enhancing proton inhibition. Nat. Neurosci., 1, 659-667.
39. NEJTEK, V. & DAHL, D. (1997). Pathway specificity of 1-isoproterenol indicates beta-adrenergic modulation of the Schaffer collateral pathway in field CA1 in the rat hippocampal slice. Neuroreport, 8, 745-749.
40. OTMAKHOVA, N.A. & LISMAN, J.E. (1999). Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J. Neurosci., 19, 1437-1445.
41. OTMAKHOVA, N.A. & LISMAN, J.E. (2000). Dopamine, serotonin, and noradrenaline strongly inhibit the direct perforant path-CA1 synaptic input, but have little effect on the Schaffer collateral input. Ann. N.Y. Acad. Sci., 911, 462-464.
42. OTMAKHOVA, N.A., OTMAKHOV, N. & LISMAN, J.E. (2002). Pathway-specific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells. J. Neurosci., 22, 1199-1207.
43. PHILPOT, B.D., SEKHAR, A.K., SHOUVAL, H.Z. & BEAR, M.F. (2001). Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron, 29, 157-169.
44. QUINLAN, E.M., PHILPOT, B.D., HUGANIR, R.L. & BEAR, M.F. (1999). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci., 2, 352-357.
45. RUMBAUGH, G. & VICINI, S. (1999). Distinct synaptic and extra-synaptic NMDA receptors in developing cerebellar granule neurons. J. Neurosci., 19, 10603-10610.
46. SHI, J., AAMODT, S.M. & CONSTANTINE-PATON, M. (1997). Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. J. Neurosci., 17, 6264-6276.
47. STEWARD, O. (1976). Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comput. Neurol., 167, 285-314.
48. STOCCA, G. & VICINI, S. (1998). Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J. Physiol., 507 (Part 1), 13-24.
49. TANG, Y.P., SHIMIZU, E., DUBE, G.R., RAMPON, C., KERCHNER, G.A., ZHUO, M., LIU, G. & TSIEN, J.Z. (1999). Genetic enhancement of learning and memory in mice. Nature, 401, 63-69.
50. TOVAR, K.R. & WESTBROOK, G.L. (1999). The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci., 19, 4180-4188.
51. VICINI, S., WANG, J.F., LI, J.H., ZHU, W.J., WANG, Y.H., LUO, J.H., WOLFE, B.B. & GRAYSON, D.R. (1998). Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J. Neurophysiol., 79, 555-566.
52. WATKINS, C.J., PEI, Q. & NEWBERRY, N.R. (1998). Differential effects of electroconvulsive shock on the glutamate receptor mRNAs for NR2A, NR2B and mGluR5b. Brain. Res. Mol. Brain. Res., 61, 108-113.
53. WILLIAMS, K. (1993). Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol. Pharmacol., 44, 851-859.
54. WILLIAMS, K. (1995). Pharmacological properties of recombinant N-methyl-D-aspartate (NMDA) receptors containing the epsilon 4 (NR2D) subunit. Neurosci. Lett., 184, 181-184.