Synaptic plasticity in glutamatergic and GABAergic neurotransmission following chronic memantine treatment in an in vitro model of limbic epileptogenesis

Neuropharmacology

Volumn 77, Issue , 2014, Pages 379-386

  He, Shuijin ^b   Bausch, Suzanne B ^a,b  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

Author keywords

Dentate granule cell; Electrophysiology; Hippocampus; Resting membrane potential; Slice culture

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL GRANULE; CONTROLLED STUDY; EPILEPTOGENESIS; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; GLUTAMATERGIC TRANSMISSION; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; MEMBRANE STEADY POTENTIAL; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACSF; ARTIFICIAL CEREBROSPINAL FLUID; BICUCULLINE METHIODIDE; BMI; CNQX; D(-)-2-AMINO-5-PHOSPHONOPENTANOIC ACID; D-APV; DENTATE GRANULE CELL; ELECTROPHYSIOLOGY; GABA; HIPPOCAMPUS; LARGE AMPLITUDE SPONTANEOUS EXCITATORY POSTSYNAPTIC CURRENT; MEPSC; MINIATURE EXCITATORY POSTSYNAPTIC CURRENT; MINIATURE INHIBITORY POSTSYNAPTIC CURRENT; MIPSC; N-METHYL-D-ASPARTATE RECEPTORS; NMDAR; POSTSYNAPTIC CURRENT; PSC; RESTING MEMBRANE POTENTIAL; RMP; SEM; SEPSC; SEPSC(LARGE); SEPSC(SMALL); SIPSC; SLICE CULTURE; SMALL AMPLITUDE SPONTANEOUS EXCITATORY POSTSYNAPTIC CURRENT; SPONTANEOUS EXCITATORY POSTSYNAPTIC CURRENT; SPONTANEOUS INHIBITORY POSTSYNAPTIC CURRENT; STANDARD ERROR OF THE MEAN; TETRODOTOXIN; TTX; Γ-AMINOBUTYRIC ACID;

ANIMALS; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; MEMANTINE; NEURONAL PLASTICITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84887594198     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.10.016     Document Type: Article

References (41)

1. Y. Aracava, E.F. Pereira, A. Maelicke, and E.X. Albuquerque Memantine blocks alpha7* nicotinic acetylcholine receptors more potently than n-methyl-D-aspartate receptors in rat hippocampal neurons J. Pharmacol. Exp. Ther. 312 2005 1195 1205
2. M. Avoli, and M. de Curtis GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity Prog. Neurobiol. 95 2011 104 132
3. S.B. Bausch Organotypic hippocampal slice cultures as a model of limbic epileptogenesis S.C. Baraban, Neuromethods: Innovations in Epilepsy Research Neuromethods vol. 40 2009 Humana Press New York 183 201
4. S.B. Bausch, and J.O. McNamara Synaptic connections from multiple subfields contribute to granule cell hyperexcitability in hippocampal slice cultures J. Neurophysiol. 84 2000 2918 2932
5. S.B. Bausch, and J.O. McNamara Contributions of mossy fiber and CA1 pyramidal cell sprouting to dentate granule cell hyperexcitability in kainic acid-treated hippocampal slice cultures J. Neurophysiol. 92 2004 3582 3595
6. S.B. Bausch, S. He, Y. Petrova, X.M. Wang, and J.O. McNamara Plasticity of both excitatory and inhibitory synapses is associated with seizures induced by removal of chronic blockade of activity in cultured hippocampus J. Neurophysiol. 96 2006 2151 2167
7. M.F. Bear, A. Kleinschmidt, Q.A. Gu, and W. Singer Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist J. Neurosci. 10 1990 909 925
8. 2+ induced epileptiform activity from the rat entorhinal cortex to the hippocampus after kindling studied in vitro Neurosci. Lett. 216 1996 41 44
9. J. Behr, K.J. Lyson, and I. Mody Enhanced propagation of epileptiform activity through the kindled dentate gyrus J. Neurophysiol. 79 1998 1726 1732
10. I. Bresink, W. Danysz, C.G. Parsons, P. Tiedtke, and E. Mutschler Chronic treatment with the uncompetitive NMDA receptor antagonist memantine influences the polyamine and glycine binding sites of the NMDA receptor complex in aged rats J. Neural Transm. 10 1995 11 26
11. H.S. Chen, J.W. Pellegrini, S.K. Aggarwal, S.Z. Lei, S. Warach, F.E. Jensen, and S.E. Lipton Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity J. Neurosci. 12 1992 4427 4436
12. H.T. Cline, E.A. Debski, and M. Constantine-Paton N-methyl-D-aspartate receptor antagonist desegregates eye-specific stripes Proc. Natl. Acad. Sci. U. S. A. 84 1987 4342 4345
13. R.C. Collins, R.G. Tearse, and E.W. Lothman Functional anatomy of limbic seizures: focal discharges from medial entorhinal cortex in rat Brain Res. 280 1983 25 40
14. R. Dingledine, C.J. McBain, and J.O. McNamara Excitatory amino acid receptors in epilepsy Trends Pharmacol. Sci. 11 1990 334 338
15. N.B. Fredj, and J. Burrone A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse Nat. Neurosci. 12 2009 751 758
16. B. Gafurov, and S.B. Bausch GABAergic transmission facilitates ictogenesis and synchrony between CA3, hilus, and dentate gyrus in slices from epileptic rats J. Neurophysiol. 110 2013 441 455
17. S. He, L.R. Shao, W.B. Rittase, and S.B. Bausch Increased Kv1 channel expression may contribute to decreased sIPSC frequency following chronic inhibition of NR2B-containing NMDAR Neuropsychopharmacology 37 2012 1338 1356
18. S. He, L.-R. Shao, Y. Wang, and S.B. Bausch Synaptic and extrasynaptic plasticity in glutamatergic circuits involving dentate granule cells following chronic N-methyl-D-aspartate receptor inhibition J. Neurophysiol. 109 2013 1535 1547
19. J.W. Johnson, and S.E. Kotermanski Mechanism of action of memantine Curr. Opin. Pharmacol. 6 2006 61 67
20. J. Kornhuber, and G. Quack Cerebrospinal fluid and serum concentrations of the N-methyl-D-aspartate (NMDA) receptor antagonist memantine in man Neurosci. Lett. 195 1995 137 139
21. S.Y. Lin, and M. Constantine-Paton Suppression of sprouting: an early function of NMDA receptors in the absence of AMPA/kainate receptor activity J. Neurosci. 18 1998 3725 3737
22. S.E. Lipton Neuroprotective effects of memantine Reply Neurol. 43 1993 1054 1055
23. S.A. Lipton Pathologically activated therapeutics for neuroprotection Nat. Rev. Neurosci. 8 2007 803 808
24. W. Loscher Pharmacology of glutamate receptor antagonists in the kindling model of epilepsy Prog. Neurobiol. 54 1998 721 741
25. P. Mareš, and A. Mikulecká Different effects of two N-methyl-D-aspartate receptor antagonists on seizures, spontaneous behavior, and motor performance in immature rats Epilepsy Behav. 14 2009 32 39
26. R.A. McKinney, A. Luthi, C.E. Bandtlow, B.H. Gahwiler, and S.M. Thompson Selective glutamate receptor antagonists can induce or prevent axonal sprouting in rat hippocampal slice cultures Proc. Natl. Acad. Sci. U. S. A. 96 1999 11631 11636
27. B.S. Meldrum, L. Turski, M. Schwarz, S.J. Czuczwar, and K.H. Sontag Anticonvulsant action of 1,3-dimethyl-5-aminoadamantane. Pharmacological studies in rodents and baboon, Papio papio Naunyn Schmiedebergs Arch. Pharmacol. 332 1986 93 97
28. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540
29. K. Moriyoshi, M. Masu, T. Ishii, R. Shigemoto, N. Mizuno, and S. Nakanishi Molecular cloning and characterization of the rat NMDA receptor Nature 354 1991 31 37
30. K.W. Muir, and K.R. Lees Clinical experience with excitatory amino acid antagonist drugs Stroke 26 1995 503 513
31. R.J. O'Brien, S. Kamboj, M.D. Ehlers, K.R. Rosen, G.D. Fischbach, and R.L. Huganir Activity-dependent modulation of synaptic AMPA receptor accumulation Neuron 21 1998 1067 1078
32. C.G. Parsons, G. Quack, I. Bresink, L. Baran, E. Przegalinski, W. Kostowski, P. Krzascik, S. Hartmann, and W. Danysz Comparison of the potency, kinetics and voltage-dependency of open channel blockade for a series of uncompetitive NMDA antagonists in vitro with anticonvulsive and motor impairment activity in vivo Neuropharmacology 34 1995 1239 1258
33. C.G. Parsons, W. Danysz, and G. Quack Memantine is a clinically well tolerated N-methyl-D-aspartate (NMDA) receptor antagonist-a review of preclinical data Neuropharmacology 38 1999 735 767
34. C.G. Parsons, A. Stöffler, and W. Danysz 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 2007 699 723
35. G. Rammes, R. Rupprecht, U. Ferrari, W. Zieglgänsberger, and C.G. Parsons The N-methyl-D-aspartate receptor channel blockers memantine, MRZ 2/579 and other amino-alkyl-cyclohexanes antagonise 5-HT(3) receptor currents in cultured HEK-293 and N1E-115 cell systems in a non-competitive manner Neurosci. Lett. 306 2001 81 84
36. A. Rao, and A.M. Craig Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons Neuron 19 1997 801 812
37. M.A. Rogawski Therapeutic potential of excitatory amino acid antagonists: channel blockers and 2,3-benzodiazepines Trends Pharmacol. Sci. 14 1993 325 331
38. L. Stoppini, P.A. Buchs, and D. Muller A simple method for organotypic cultures of nervous tissue J. Neurosci. Methods 37 1991 173 182
39. S. Sveinbjornsdottir, J.W.A.S. Sander, D. Upton, P.J. Thompson, P.N. Patsalos, D. Hirt, M. Emre, D. Lowe, and J.S. Duncan The excitatory amino acid antagonist D-CPP-ene (SDZ EAA-494) in patients with epilepsy Epilepsy Res. 16 1993 165 174
40. X.M. Wang, and S.B. Bausch Effects of distinct classes of N-methyl-D-aspartate receptor antagonists on seizures, axonal sprouting and neuronal loss in vitro: suppression by NR2B-selective antagonists Neuropharmacology 47 2004 1008 1020
41. P. Xia, H.S. Chenm, D. Zhang, and S.A. Lipton Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses J. Neurosci. 30 2010 11246 11250