Tonically active NMDA receptors - a signalling mechanism critical for interneuronal excitability in the CA1 stratum radiatum

European Journal of Neuroscience

Volumn 43, Issue 2, 2016, Pages 169-178

  Culley, Georgia ^a   Dósa, Zita ^b   Radi, Shayma ^a   Strand, Karin ^a   Fröjd, Victoria ^a   Hanse, Eric ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Alzheimer's disease; Disinhibition; Extrasynaptic; Hippocampus; Schizophrenia

Indexed keywords

MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHENCYCLIDINE; 4 AMINOBUTYRIC ACID RECEPTOR; CULTURE MEDIUM; NR2D NMDA RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; HUMAN; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MALE; NERVE CELL EXCITABILITY; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; STRATUM RADIATUM; ANIMAL; CEREBROSPINAL FLUID; CULTURE MEDIUM; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; NERVE CELL INHIBITION; PHARMACOLOGY; PHYSIOLOGY; SYNAPTIC POTENTIAL;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CEREBROSPINAL FLUID; CULTURE MEDIA; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GABAERGIC NEURONS; HUMANS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MALE; MEMANTINE; NEURAL INHIBITION; PHENCYCLIDINE; PYRAMIDAL CELLS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC POTENTIALS;

EID: 84955194959     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.13128     Document Type: Article

References (62)

1. Arnth-Jensen, N., Jabaudon, D. & Scanziani, M. (2002) Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat. Neurosci., 5, 325-331.
2. Björefeldt, A., Andreasson, U., Daborg, J., Riebe, I., Wasling, P., Zetterberg, H. & Hanse, E. (2015) Human cerebrospinal fluid increases the excitability of pyramidal neurons in the in vitro brain slice. J. Physiol., 593, 231-243.
3. Brickley, S.G., Misra, C., Mok, M.H., Mishina, M. & Cull-Candy, S.G. (2003) NR2B and NR2D subunits coassemble in cerebellar Golgi cells to form a distinct NMDA receptor subtype restricted to extrasynaptic sites. J. Neurosci., 23, 4958-4966.
4. Browne, C.A. & Lucki, I. (2013) Antidepressive effects of ketamine: mechanisms underlying fast-acting novel antidepressants. Front. Pharmacol., 4, 1-18.
5. Cavelier, P. & Attwell, D. (2005) Tonic release of glutamate by a DIDS-sensitive mechanism in rat hippocampal slices. J. Physiol., 564, 397-410.
6. Chen, H.S., Pellegrini, J.W., Aggarwal, S.K., Lei, S.Z., Warach, S., Jensen, F.E. & Lipton, S.A. (1992) Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity. J. Neurosci., 12, 4427-4436.
7. Chen, P.E., Geballe, M.T., Stansfeld, P.J., Johnston, A.R., Yuan, H., Jacob, A.L., Snyder, J.P., Traynelis, S.F. & Wyllie, D.J.A. (2005) Structural features of the glutamate binding site in recombinant NR1/NR2A N-Methyl-D-aspartate receptors determined by site-directed mutagenesis and molecular modeling. Mol. Pharmacol., 67, 1470-1484.
8. Chitwood, R.A., Hubbard, A. & Jaffe, D.B. (1999) Passive electrotonic properties of rat hippocampal CA3 interneurones. J. Physiol., 515, 743-756.
9. Cull-Candy, S., Brickley, S. & Farrant, M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol., 11, 327-335.
10. Daniels, B.A. & Baldridge, W.H. (2010) D-Serine enhancement of NMDA receptor-mediated calcium increases in rat retinal ganglion cells. J. Neurochem., 112, 1180-1189.
11. Davies, C.H., Davies, S.N. & Collingridge, G.L. (1990) Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol., 424, 513-531.
12. Dimpfel, W. (1995) Effects of memantine on synaptic transmission in the hippocampus in vitro. Arzneimittelforsch., 45, 1-5.
13. von Engelhardt, J., Bocklisch, C., Tönges, L., Herb, A., Mishina, M. & Monyer, H. (2015) GluN2D-containing NMDA receptors-mediate synaptic currents in hippocampal interneurons and pyramidal cells in juvenile mice. Front. Cell. Neurosci., 9, 95.
14. Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G. & Carmignoto, G. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron, 43, 729-743.
15. Gilling, K.E., Jatzke, C., Hechenberger, M. & Parsons, C.G. (2009) Potency, voltage-dependency, agonist concentration-dependency, blocking kinetics and partial untrapping of the uncompetitive N-methyl-D-aspartate (NMDA) channel blocker memantine at human NMDA (GluN1/GluN2A) receptors. Neuropharmacology, 56, 866-875.
16. Greene, R. (2001) Circuit analysis of NMDAR hypofunction in the hippocampus, in vitro, and psychosis of schizophrenia. Hippocampus, 11, 569-577.
17. Groc, L., Bard, L. & Choquet, D. (2009) Surface trafficking of N-methyl-D-aspartate receptors: physiological and pathological perspectives. Neuroscience, 158, 4-18.
18. Grunze, H.C., Rainnie, D.G., Hasselmo, M.E., Barkai, E., Hearn, E.F., McCarley, R.W. & Greene, R.W. (1996) NMDA-dependent modulation of CA1 local circuit inhibition. J. Neurosci., 16, 2034-2043.
19. Hardingham, G.E. & Bading, H. (2003) The Yin and Yang of NMDA receptor signalling. Trends Neurosci., 26, 81-89.
20. Herman, M.A. & Jahr, C.E. (2007) Extracellular glutamate concentration in hippocampal slice. J. Neurosci., 27, 9736-9741.
21. Herman, M.A., Nahir, B. & Jahr, C.E. (2011) Distribution of extracellular glutamate in the neuropil of hippocampus. PLoS One, 6, 1-5.
22. Homayoun, H. & Moghaddam, B. (2007) NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J. Neurosci., 27, 11496-11500.
23. Javitt, D.C. (2007) Glutamate and schizophrenia: phencyclidine, N-methyl-D-aspartate receptors, and dopamine-glutamate interactions. Int. Rev. Neurobiol., 78, 69-108.
24. Javitt, D.C. & Zukin, S.R. (1991) Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychat., 148, 1301-1308.
25. Javitt, D.C., Zukin, S.R., Heresco-Levy, U. & Umbricht, D. (2012) Has an angel shown the way? Etiological and therapeutic implications of the PCP/NMDA model of schizophrenia. Schizophr. Bull., 38, 958-966.
26. Kalia, L.V., Kalia, S.K. & Salter, M.W. (2008) NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol., 7, 742-755.
27. Kaufman, A.M., Milnerwood, A.J., Sepers, M.D., Coquinco, A., She, K., Wang, L., Lee, H., Craig, A.M., Cynader, M. & Raymond, L.A. (2012) Opposing roles of synaptic and extrasynaptic NMDA receptor signalling in cocultured striatal and cortical neurons. J. Neurosci., 32, 3992-4003.
28. Kirson, E.D., Schirram, C., Konnerth, A. & Yaari, Y. (1999) Early postnatal switch in magnesium sensitivity of NMDA receptors in rat CA1 pyramidal cells. J. Physiol., 521, 99-111.
29. 2+ imparts NMDA receptor subtype selectivity to the Alzheimer's drug memantine. J. Neurosci., 29, 2774-2779.
30. Lamsa, K., Heeroma, J.H., Rusakov, D.A. & Kullmann, D.M. (2005) Constitutive Src-family kinase activity is required for NMDA receptor dependent LTP in inhibitory interneurons. Soc. Neurosci. Abstr., 496, 3.
31. Lamsa, K., Irvine, E.E., Giese, K.P. & Kullmann, D.M. (2007) NMDA receptor-dependent long-term potentiation in mouse hippocampal interneurons shows a unique dependence on Ca(2+)/calmodulin-dependent kinases. J. Physiol., 584, 885-894.
32. Lau, C.G. & Zukin, R.S. (2007) NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci., 8, 413-426.
33. Laube, B., Hirai, H., Sturgess, M., Betz, H. & Kuhse, J. (1997) Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron, 18, 493-503.
34. Le Meur, K., Galante, M., Angulo, M.C. & Audinat, E. (2007) Tonic activation of NMDA receptors by ambient glutamate of non-synaptic origin in the rat hippocampus. J. Physiol., 580, 373-383.
35. Li, Q., Clark, S., Lewis, D.V. & Wilson, W.A. (2002) NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: a potential mechanism of neurotoxicity. J. Neurosci., 22, 3070-3080.
36. Li, S., Hong, S., Shepardson, N.E., Walsh, D.M., Shankar, G.M. & Selkoe, D. (2009) Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron, 62, 788-801.
37. Lipton, S.A. (2004) Failures and successes of NMDA receptor antagonists: molecular basis for the use of open-channel blockers like memantine in the treatment of acute and chronic neurologic insults. NeuroRx, 1, 101-110.
38. Lisman, J.E., Coyle, J.T., Green, R.W., Javitt, D.C., Benes, F.M., Heckers, S. & Grace, A.A. (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci., 31, 234-242.
39. Lozovaya, N.A., Grebenyuk, S.E., Tsintsadze, T., Feng, B., Monaghan, D.T. & Krishtal, O.A. (2004) Extrasynaptic NR2B and NR2D subunits of NMDA receptors shape 'superslow' afterburst EPSC in rat hippocampus. J. Physiol., 558, 451-463.
40. Maccaferri, G. & Dingledine, R. (2002) Control of feedforward dendritic inhibition by NMDA receptor-dependent spike timing in hippocampal interneurons. J. Neurosci., 22, 5462-5472.
41. Mann, E.O. & Mody, I. (2010) Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat. Neurosci., 13, 205-212.
42. Martin, S.J., Grimwood, P.D. & Morris, R.G. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci., 23, 649-711.
43. Matos, M., Augusto, E., Oliveira, C.R. & Agostinho, P. (2008) Amyloid-beta peptide decreases glutamate uptake in cultured astrocytes: involvement of oxidative stress and mitogen-activated protein kinase cascades. Neuroscience, 156, 898-910.
44. Milnerwood, A.J., Gladding, C.M., Pouladi, M.A., Kaufman, A.M., Hines, R.M., Boyd, J.D., Ko, R.W., Vasuta, O.C., Graham, R.K., Hayden, M.R., Murphy, T.H. & Raymond, L.A. (2010) Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron, 65, 178-190.
45. 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.
46. Nanxin, L., Boyoung, L., Rong-Jian, L., Mounira, B., Jason, M.D., Masaaki, I., Xiao-Yuan, L., George, A. & Ronald, S.D. (2010) mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science, 329, 959-964.
47. Paoletti, P. & Neyton, J. (2007) NMDA receptor subunits: function and pharmacology. Curr. Opin. Pharmacol., 7, 39-47.
48. Papouin, T. & Oliet, S.H. (2014) Organization, control and function of extrasynaptic NMDA receptors. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 369, doi:10.1098/rstb.2013.0601.
49. Parsons, C.G., Stoffler, A. & Danysz, W. (2007) Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse. Neuropharmacology, 53, 699-723.
50. Povysheva, N.V. & Johnson, J.W. (2012) Tonic NMDA receptor-mediated current in prefrontal cortical pyramidal cells and fast-spiking interneurons. J. Neurophysiol., 107, 2232-2243.
51. Ramoa, A.S. & Albuquerque, E.X. (1988) Phencyclidine and some of its analogues have distinct effects on NMDA receptors of rat hippocampal neurons. FEBS Lett., 235, 156-162.
52. Riebe, I., Gustafsson, B. & Hanse, E. (2009) Silent synapses onto interneurons in the rat CA1 stratum radiatum. Eur. J. Neurosci., 29, 1870-1882.
53. Rosenmund, C. & Westbrook, G.L. (1993) Rundown of N-methyl-D-aspartate channels during whole-cell recording in rat hippocampal neurons: role of Ca2+ and ATP. J. Physiol., 470, 705-729.
54. Sah, P., Hestrin, S. & Nicoll, R.A. (1989) Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science, 246, 815-818.
55. Scimemi, A., Fine, A., Kullmann, D.M. & Rusakov, D.A. (2004) NR2B-containing receptors mediate cross talk among hippocampal synapses. J. Neurosci., 24, 4767-4777.
56. Standaert, D.G., Landwehrmeyer, G.B., Kerner, J.A., Penney, J.B. & Young, A.B. (1996) Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Brain Res. Mol. Brain Res., 42, 89-102.
57. Stevens, E.R., Gustafson, E.C. & Miller, R.F. (2010) Glycine transport accounts for the differential role of glycine vs. D-serine at NMDA receptor coagonist sites in the salamander retina. Eur. J. Neurosci., 31, 808-816.
58. Sun, W., Shchepakin, D., Kalachev, L.V. & Kavanaugh, M.P. (2014) Glutamate transporter control of ambient glutamate levels. Neurochem. Int., 73, 146-151.
59. Talantova, M., Sanz-Blasco, S., Zhang, X., Xia, P., Akhtar, M.W., Okamoto, S., Dziewczapolski, G., Nakamura, T., Cao, G., Pratt, A.E., Kang, Y.J., Tu, S., Molokanova, E., McKercher, S.R., Hires, S.A., Sason, H., Stouffer, D.G., Buczynski, M.W., Solomon, J.P., Michael, S., Powers, E.T., Kelly, J.W., Roberts, A., Tong, G., Fang-Newmeyer, T., Parker, J., Holland, E.A., Zhang, D., Nakanishi, N., Chen, H.S., Wolosker, H., Wang, Y., Parsons, L.H., Ambasudhan, R., Masliah, E., Heinemann, S.F., Piña-Crespo, J.C. & Lipton, S.A. (2013) Aβ induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. PNAS, 110, 2518-2527.
60. Wrighton, D.C., Baker, E.J., Chen, P.E. & Wyllie, D.J. (2008) Mg2+ and memantine block of rat recombinant NMDA receptors containing chimeric NR2A/2D subunits expressed in Xenopus laevis oocytes. J. Physiol., 586, 211-225.
61. Xia, P., Chen, P.S., Zhang, D. & Lipton, S.A. (2010) Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses. J. Neurosci., 30, 246-250.
62. Yoshiike, Y., Kimura, T., Yamashita, S., Furudate, H., Mizoroki, T., Murayama, M. & Takashima, A. (2008) GABA(A) receptor-mediated acceleration of aging-associated memory decline in APP/PS1 mice and its pharmacological treatment by picrotoxin. PLoS One, 3, 1-12.