Idazoxan blocks the nicotine-induced reversal of the memory impairment caused by the NMDA glutamate receptor antagonist dizocilpine

Pharmacology Biochemistry and Behavior

Volumn 90, Issue 3, 2008, Pages 372-381

  Timofeeva, Olga A ^a   Levin, Edward D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alpha2 adrenoreceptors; Hippocampus; Local inhibition; Nicotinic receptors; Radial maze; Schizophrenia; Seizure; Working memory

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; DIZOCILPINE; IDAZOXAN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE TARTRATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPLEX PARTIAL SEIZURE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFECT; DRUG INHIBITION; FEMALE; MAZE TEST; MEMORY; MEMORY DISORDER; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; SEIZURE; WORKING MEMORY;

ADRENERGIC ALPHA-ANTAGONISTS; ANIMALS; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; IDAZOXAN; MAZE LEARNING; MEMORY; MEMORY DISORDERS; MEMORY, SHORT-TERM; NICOTINE; NICOTINIC AGONISTS; NOREPINEPHRINE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES; SYNAPTIC TRANSMISSION;

RATTUS;

EID: 44549089090     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2008.03.011     Document Type: Article

References (129)

1. Addy N.A., Nakijama A., and Levin E.D. Nicotinic mechanisms of memory: effects of acute local DHbetaE and MLA infusions in the basolateral amygdala. Brain Res Cogn Brain Res 16 (2003) 51-57
2. Alkondon M., and Albuquerque E. Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86 (2001) 3043-3055
3. Alkondon M., Pereira E., Eisenberg H., and Albuquerque E. Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. J Neurosci 19 (1999) 2693-2705
4. Alkondon M., Pereira E., Almeida L., Randall W., and Albuquerque E. Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 39 (2000) 2726-2739
5. Arnsten A.F., and Contant T.A. Alpha-2 adrenergic agonists decrease distractibility in aged monkeys performing the delayed response task. Psychopharmacology (Berl) 108 (1992) 159-169
6. Aston-Jones G., Chiang C., and Alexinsky T. Discharge of noeadrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 88 (1991) 501-520
7. Azam L., and McIntosh J.M. Characterization of nicotinic acetylcholine receptors that modulate nicotine-evoked [3H]norepinephrine release from mouse hippocampal synaptosomes. Mol Pharmacol 70 (2006) 967-976
8. Barnes C.A. Spatial learning and memory: the search for their neurobiological mechanisms in the rat. Trends Neurosci 11 (1988) 163-169
9. Bettany J., and Levin E. Ventral hippocampal alpha 7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze. Pharmacol Biochem Behav 70 (2001) 467-474
10. Birthelmer A., Stemmelin J., Jackisch R., and Cassel J.C. Presynaptic modulation of acetylcholine, noradrenaline, and serotonin release in the hippocampus of aged rats with various levels of memory impairments. Brain Res Bull 60 (2003) 283-296
11. Blackstad T.W., Fuxe K., and Hokfelt T. Noradrenaline nerve terminals in the hippocampal region of the rat and the guinea pig. Z Zellforsch Mikrosk Anat 78 (1967) 463-473
12. Breese C.R., Lee M.J., Adams C.E., Sullivan B., Logel J., Gillen K.M., et al. Abnormal regulation of high affinity nicotinic receptors in subjects with schizophrenia. Neuropsychopharmacology 23 (2000) 351-364
13. Brioni J.D., Decker M.W., Sullivan J.P., and Arneric S.P. The pharmacology of (-)-nicotine and novel cholinergic channel modulators. Adv Pharmacol 37 (1997) 153-214
14. Brown R.A., Walling S.G., Milway J.S., and Harley C.W. Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. J Neurosci 25 (2005) 1985-1991
15. Bunzey M., and Strupp B. Specific effects of idazoxan in a distraction task: evidence that endogenous norepinephrine plays a role in selective attention in rats. Behav Neurosci 109 (1995) 903-911
16. Burchfiel J.L., Duchowny M.S., and Duffy F.H. Neuronal supersensitivity to acetylcholine induced by kindling in the rat hippocampus. Science 204 (1979) 1096-1098
17. Cain D.P. Excitatory neurotransmitters in kindling: excitatory amino acid, cholinergic, and opiate mechanisms. Neurosci Biobehav Rev 13 (1989) 269-276
18. Chambers R., Moore J., McEvoy J., and Levin E. Cognitive effects of neonatal hippocampal lesions in a rat model of schizophrenia. Neuropsychopharmacology 15 (1996) 587-594
19. Chopin P., Colpaert F.C., and Marien M. Effects of acute and subchronic administration of dexefaroxan, an alfa2-adrenoreceptor antagonist, on memory performance in young adult and aged rodents. J Pharmacol Exp Ther 301 (2002) 187-196
20. Clarke R.W., and Harris J. RX 821002 as a tool for physiological investigation of alpha(2)-adrenoceptors. CNS Drug Rev 8 (2002) 177-192
21. Coull J., Jones M., Egan T., Frith C., and Maze M. Attentional effects of noradrenaline vary with arousal level: selective activation of thalamic pulvinar in humans. Neuroimage 22 (2004) 315-322
22. Court J., Spurden D., Lloyd S., McKeith I., Ballard C., Cairns N., et al. Neuronal nicotinic receptors in dementia with Lewy bodies and schizophrenia: alpha-bungarotoxin and nicotine binding in the thalamus. J Neurochem 73 (1999) 1590-1597
23. Dabire H. Idazoxan: a novel pharmacological tool for the study of alpha 2-adrenoceptors. J Pharmacol 17 (1986) 113-118
24. Damaj M.I., Glassco W., Dukat M., and Martin B.R. Pharmacological characterization of nicotine-induced seizures in mice. J Pharmacol Exp Ther 291 (1999) 1284-1291
25. Dasheiff R.M. d-tubocurarine causes neuronal death when injected directly into rat brain. Exp Neurol 89 (1985) 172-188
26. Davis H.P., Tribuna J., Pulsinelli W.A., and Volpe B.T. Reference and working memory of rats following hippocampal damage induced by transient forebrain ischemia. Physiol Behav 37 (1986) 387-392
27. Decker M.W., Brioni J.D., Bannon A.W., and Arneric S.P. Diversity of neuronal nicotinic acetylcholine receptors: lessons from behavior and implications for CNS therapeutics. Life Sci 56 (1995) 545-570
28. Dennis T., L'Heureux R., Carter C., and Scatton B. Presynaptic alpha-2 adrenoceptors play a major role in the effects of idazoxan on cortical noradrenaline release (as measured by in vivo dialysis) in the rat. J Pharmacol Exp Ther 241 (1987) 642-649
29. Devauges V., and Sara S. Memory retrival enhancement by locus coeruleus stimulation: evidence for mediation by beta receptors. Brain Res 43 (1991) 93-97
30. Durany N., Zochling R., Boissl K.W., Paulus W., Ransmayr G., Tatschner T., et al. Human post-mortem striatal alpha4beta2 nicotinic acetylcholine receptor density in schizophrenia and Parkinson's syndrome. Neurosci Lett 287 (2000) 109-112
31. Farber N.B., Foster J., Duhan N.L., and Olney J.W. alpha 2 adrenergic agonists prevent MK-801 neurotoxicity. Neuropsychopharmacology 12 (1995) 347-349
32. Felix R., and Levin E.D. Nicotinic antagonist administration into the ventral hippocampus and spatial working memory in rats. Neuroscience 81 (1997) 1009-1017
33. Fernandez-Pastor B., and Meana J.J. In vivo tonic modulation of the noradrenaline release in the rat cortex by locus coeruleus somatodendritic alpha(2)-adrenoceptors. Eur J Pharmacol 442 (2002) 225-229
34. Fisher J.L., and Dani J.A. Nicotinic receptors on hippocampal cultures can increase synaptic glutamate currents while decreasing the NMDA-receptor component. Neuropharmacology 39 (2000) 2756-2769
35. Frazier C., Buchler A., Weiner J., and Dunwiddie T. Synaptic potentials mediated via alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18 (1998) 8228-8235
36. Frazier C., Rollins Y., Breese C., Leonard S., Freedman R., and Dunwiddie T. Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 18 (1998) 1187-1195
37. Frazier C., Strowbridge B., and Papke R. Nicotinic receptors on local circuit neurons in dentate gyrus: a potential role in regulation of granule cell excitability. J Neurophysiol 89 (2003) 3018-3028
38. Freedman R., Hall M., Adler L.E., and Leonard S. Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia. Biol Psychiatry 38 (1995) 22-33
39. Fu Y., Matta S.G., James T.J., and Sharp B.M. Nicotine-induced norepinephrine release in the rat amygdala and hippocampus is mediated through brainstem nicotinic cholinergic receptors. J Pharmacol Exp Ther 284 (1998) 1188-1196
40. Gellman R.L., Kallianos J.A., and McNamara J.O. Alpha-2 receptors mediate an endogenous noradrenergic suppression of kindling development. J Pharmacol Exp Ther 241 (1987) 891-898
41. Giorgi F.S., Pizzanelli C., Biagioni F., Murri L., and Fornai F. The role of norepinephrine in epilepsy: from the bench to the bedside. Neurosci Biobehav Rev 28 (2004) 507-524
42. Giovannini M.G., Mutolo D., Bianchi L., Michelassi A., and Pereu G. NMDA receptor antagonists decrease GABA outflow from the septum and increase acetylcholine outflow from the hippocampus: a microdialysis study. J Neurosci 14 (1994) 1358-1365
43. Grigoryan G.A., Mitchell S.N., Hodges H., Sinden J.D., and Gray J.A. Are the cognitive-enhancing effects of nicotine in the rat with lesions to the forebrain cholinergic projection system mediated by an interaction with the noradrenergic system?. Pharmacol Biochem Behav 49 (1994) 511-521
44. Grunze H.C.R., Rainnie D.G., Hasselmo M.E., Barkai E., and Hearn E.F. NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16 (1996) 2034-2043
45. Guan Z.Z., Zhang X., Blennow K., and Nordberg A. Decreased protein level of nicotinic receptor alpha7 subunit in the frontal cortex from schizophrenic brain. Neuroreport 10 (1999) 1779-1782
46. Haapalinna A., Sirvio J., MacDonald E., Virtanen R., and Heinonen E. The effects of a specific alpha(2)-adrenoceptor antagonist, atipamezole, on cognitive performance and brain neurochemistry in aged Fisher 344 rats. Eur J Pharmacol 387 (2000) 141-150
47. Handa F., Tanaka M., Nishikawa T., and Toyooka H. Effects of oral clonidine premedication on side effects of intravenous ketamine anesthesia: a randomized, double-blind, placebo-controlled study. J Clin Anesth 12 (2000) 19-24
48. Hasegawa M., Kinoshita H., Amano M., Hasegawa T., Kameyama T., and Nabeshima T. MK-801 increases endogenous acetylcholine release in the rat parietal cortex: a study using brain microdialysis. Neurosci Lett 150 (1993) 53-56
49. Hiraga Y., and Iwasaki T. Effects of cholinergic and monoaminergic antagonists and tranquilizers upon spatial memory in rats. Pharmacol Biochem Behav 20 (1984) 205-207
50. Hlinak Z., and Krejci I. Spontaneous alternation behaviour in rats: kynurenic acid attenuated deficits induced by MK-801. Behav Brain Res 168 (2006) 144-149
51. Honack D., and Loscher W. Sex differences in NMDA receptor mediated responses in rats. Brain Res 620 (1993) 167-170
52. Huerta P., Sun L., Wilson M., and Tonegawa S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25 (2000) 473-480
53. Jarrard L.E. Selective hippocampal lesions: differential effects on performance by rats of spatial task with preoperative versus postoperative training. J Comp Physiol Psychol 92 (1978) 1119-1127
54. Jarrard L.E. Selective hippocampal lesions and behavior: implications for current research and theorizing. In: Isaacson R.L., and Pribram K.H. (Eds). The hippocampus (1986), Plenum, New York 93-126
55. Jentsch J.D., and Anzivino L.A. A low dose of the alpha2 agonist clonidine ameliorates the visual attention and spatial working memory deficits produced by phencyclidine administration to rats. Psychopharmacology (Berl) 175 (2004) 76-83
56. Ji D., and Dani J. Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83 (2000) 2682-2690
57. Jones S., and Yakel J.L. Fuctional nicotinic ACh receptors on interneurons in the rat hippocampus. J Physiol 504 (1997) 603-610
58. Kamisaki Y., Hamahashi T., Okada C.M., and Itoh T. Clonidine inhibition of potassium-evoked release of glutamate and aspartate from rat cortical synaptosomes. Brain Res 568 (1991) 193-198
59. Kamisaki Y., Hamahashi T., Hamada T., Maeda K., and Itoh T. Presynaptic inhibition by clonidine of neurotransmitter amino acid release in various brain regions. Eur J Pharmacol 217 (1992) 57-63
60. Kawai H., Zago W., and Berg D. Nicotinic alpha7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophines. J Neurosci 22 (2002) 7903-7912
61. Kim S.H., Price M.T., Olney J.W., and Farber N.B. Excessive cerebrocortical release of acetylcholine induced by NMDA antagonists is reduced by GABAergic and alpha2-adrenergic agonists. Mol Psychiatry 4 (1999) 344-352
62. Kitajima I., Yamamoto T., Ohno M., and Ueki S. Working and reference memory in rats in the three-panel runway task following dorsal hippocampal lesions. Jpn J Pharmacol 58 (1992) 175-183
63. Kitchigina V., Vankov A., Harley C., and Sara S. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur J Neurosci 9 (1997) 41-47
64. Knight J., and Harley C.W. Idazoxan increases perforant path-evoked EPSP slope paired pulse inhibition and reduces perforant path-evoked population spike paired pulse facilitation in rat dentate gyrus. Brain Res 1072 (2006) 36-45
65. Kobayashi M., Ohno M., Yamamoto T., and Watanabe S. Concurrent blockade of beta-adrenergic and muscarinic receptors disrupts working memory but not reference memory in rats. Physiol Behav 58 (1995) 307-314
66. Kohl B.K., and Dannhardt G. The NMDA receptor complex: a promising target for novel antiepileptic strategies. Curr Med Chem 8 (2001) 1275-1289
67. Kullmann D.M., and Lamsa K.P. Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8 (2007) 687-699
68. Kunchandy J., and Kulkarni S.K. Modulatory effect of alpha 2 adrenoceptor agonists on Ro 5-4864-induced convulsions in rats and mice. Psychopharmacology (Berl) 93 (1987) 113-117
69. Lapiz M.D.S., and Morilak D.A. Noradrenergic modulation of the cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Nueroscience 137 (2006) 10-39-1049
70. Lazarova M., Bendotti C., and Samanin R. The role of different types of adrenergic receptors in pentylenetetrazol-induced seizures and the effect of di-n-propylacetate in the rat. Psychopharmacology (Berl) 81 (1983) 177-182
71. Levanen J., Makela M.L., and Scheinin H. Dexmedetomidine premedication attenuates ketamine-induced cardiostimulatory effects and postanesthetic delirium. Anesthesiology 82 (1995) 1117-1125
72. Levin E.D. Nicotinic receptor subtypes and cognitive function. J Neurobiol 53 (2002) 633-640
73. Levin E.D., Bettegowda C., Weawer T., and Christopher N. Nicotin-dizocilpine interactions and working and reference memory performance of rats in the radial-arm maze. Pharmacol Biochem Behav 61 (1998) 335-340
74. Levin E.D., Bradley A., and Addy N. N S. Hippocampal alpha7 and alpha4beta2 nicotinic receptors and working memory. Neuroscience 109 (2002) 757-765
75. Levin E.D., McClernon F.J., and Rezvani A.H. Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomical localization. Psychopharmacology 184 (2006) 523-539
76. Loscher W., Potschka H., Wlaz P., Danysz W., and Parsons C.G. Are neuronal nicotinic receptors a target for antiepileptic drug development? Studies in different seizure models in mice and rats. Eur J Pharmacol 466 (2003) 99-111
77. Loy R., Koziell D.A., Lindsey J.D., and Moore R.Y. Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189 (1980) 699-710
78. M'Harzi M., Willig F., Bardelay C., and Palou A.M. C. O. Effects of RU 52583, an alpha 2-antagonist, on memory in rats with excitotoxic damage to the septal area. Pharmacol Biochem Behav 56 (1997) 649-655
79. Mansvelder H.D., van Aerde K.I., Couey J.J., and Brussaard A.B. Nicotinic modulation of neuronal networks: from receptors to cognition. Psychopharmacology (Berl) 184 (2006) 292-305
80. Marrs W., Kuperman J., Avedian T., Roth R., and Jentsch J. Alpha-2 adrenoceptor activation inhibits phencyclidine-induced deficits of spatial working memory in rats. Neuropsychopharmacology 30 (2005) 1500-1510
81. Martin L.F., Kem W.R., and Freedman R. Alpha-7 nicotinic receptor agonists: potential new candidates for the treatment of schizophrenia. Psychopharmacology (Berl) 174 (2004) 54-64
82. McIntyre D.C., and Giugno L. Effect of clonidine on amygdala kindling in normal and 6-hydroxydopamine-pretreated rats. Exp Neurol 99 (1988) 96-106
83. McQuiston A.R., and Madison D.V. Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19 (1998) 2887-2896
84. Meyerhoff J.L., and Bates V.E. Combined treatment with muscarinic and nicotinic cholinergic antagonists slows development of kindled seizures. Brain Res 339 (1985) 386-389
85. Michel M.C., Brodde O.E., Schnepel B., Behrendt J., Tschada R., Motulsky H.J., et al. [3H]idazoxan and some other alpha 2-adrenergic drugs also bind with high affinity to a nonadrenergic site. Mol Pharmacol 35 (1989) 324-330
86. Moghaddam B., Adams B., Verma A., and Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 17 (1997) 2921-2927
87. Newcomer J.W., and Krystal J.H. NMDA receptor regulation of memory and behavior. Hippocampus 11 (2001) 529-542
88. Newcomer J.W., Farber N.B., Selke G., Melson A.K., Jevtovic-Todorovic V., and Olney J.W. Guanabenz effects on NMDA antagonist-induced mental symptoms in humans. Soc Neurosci Abstr 24 (1998) 525
89. Nott A., and Levin E.D. Dorsal hippocampal alpha7 and alpha4beta2 nicotinic receptors and memory. Brain Res 1081 (2006) 72-78
90. Ohno M., Yamamoto T., and Watanabe S. Effects of intrahippocampal injections of N-methyl-d-aspartate receptor antagonists and scopolamine on working and reference memory assessed in rats by a three-panel runway task. J Pharmacol Exp Ther 263 (1992) 943-950
91. Ohno M., Yamamoto T., and Watanabe S. Intrahippocampal injections of benzodiazepine and muscimol impair working memory but not reference memory of rats in the three-panel runway task. Eur J Pharmacol 219 (1992) 245-251
92. Ohno M., Yamamoto T., and Watanabe S. Blockade of hippocampal nicotinic receptors impairs working memory but not reference memory in rats. Pharmacol Biochem Behav 45 (1993) 89-93
93. Ohno M., Yamamoto T., and Watanabe S. Deficits in working memory following inhibition of hippocampal nitric oxide synthesis in the rat. Brain Res 632 (1993) 36-40
94. Oleskevich S., Descarries L., and Lacaille J.C. Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J Neurosci 9 (1989) 3803-3815
95. Olney J.W., Labruyere J., Wang G., Wozniak D.F., Price M.T., and Sesma M.A. NMDA antagonist neurotoxicity: mechanism and prevention. Science 254 (1991) 1515-1518
96. Olton D.S., and Papas B.C. Spatial memory and hippocampal function. Neuropsychologia 17 (1979) 669-682
97. Papanicolaou J., Summers R.J., Vajda F.J., and Louis W.J. Anticonvulsant effects of clonidine mediated through central alpha2-adrenoceptors. Eur J Pharmacol 77 (1982) 163-166
98. Papanicolaou J., Summers R.J., Vajda F.J., and Louis W.J. The relationship between alpha 2-adrenoceptor selectivity and anticonvulsant effect in a series of clonidine-like drugs. Brain Res 241 (1982) 393-397
99. Psarropoulou C., Boivin M., and Laudadio M.A. Nicotinic effects on excitatory field potentials recorded from the immature CA3 area of rat hippocampal slices. Exp Brain Res 152 (2003) 353-360
100. Pudovkina O.L., and Westerink B.H. Functional role of alpha1-adrenoceptors in the locus coeruleus: a microdialysis study. Brain Res 1061 (2005) 50-56
101. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32 (1972) 281-294
102. Radcliffe K.A., and Dani J.A. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18 (1998) 7075-7083
103. Radcliffe K.A., Fisher J.L., Gray R., and Dani J.A. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 868 (1999) 591-610
104. Rampon C., and Tsien J. Genetic analysis of learning behavior-induced structural plasticity. Hippocampus 10 (2000) 605-609
105. Rao T.S., Correa L.D., Adams P., Santori E.M., and Sacaan A.I. Pharmacological characterization of dopamine, norepinephrine and serotonin release in the rat prefrontal cortex by neuronal nicotinic acetylcholine receptor agonists. Brain Res 990 (2003) 203-208
106. Sara S., and Devauges V. Idazoxan, an alpha-2 antagonist, facilitates memory retrival in the rat. Behav Neural Biol 51 (1989) 401-411
107. Sara S.J., Vankov A., and Herve A. Locus coeruleus-evoked responses in behaving rats: a clue to the role of noradrenaline in memory. Brain Res Bull 35 (1994) 457-465
108. Sharp B.M., Yatsula M., and Fu Y. Effects of galantamine, a nicotinic allosteric potentiating ligand, on nicotine-induced catecholamine release in hippocampus and nucleus accumbens of rats. J Pharmacol Exp Ther 309 (2004) 1116-1123
109. Shimizu E., Tang Y., Rampon C., and Tsien J. NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science 290 (2000) 1170-1174
110. Shouse M.N., Langer J., Bier M., Farber P.R., Alcalde O., Moghimi R., et al. The alpha 2 adrenoreceptor agonist clonidine suppresses seizures, whereas the alpha 2 adrenoreceptor antagonist idazoxan promotes seizures: pontine microinfusion studies of amygdala-kindled kittens. Brain Res 731 (1996) 203-207
111. Shouse M.N., Scordato J.C., Farber P.R., and de Lanerolle N. The alpha2 adrenoreceptor agonist clonidine suppresses evoked and spontaneous seizures, whereas the alpha2 adrenoreceptor antagonist idazoxan promotes seizures in amygdala-kindled kittens. Brain Res 1137 (2007) 58-68
112. Singer S., Rossi S., Verzosa S., Hashim A., Lonow R., Cooper T., et al. Nicotine-induced changes in neurotransmitter levels in brain areas associated with cognitive function. Neurochem Res 29 (2004) 1779-1792
113. Sirvio J., Riekkinen Jr. P., MacDonald E., Airaksinen M., Lammintausta R., and Riekkinen P.J. The effects of alpha-2 adrenoceptor antagonist, atipamezole, on spatial learning in scopolamine-treated and aged rats. J Neural Transm Park Dis Dement Sect 4 (1992) 99-106
114. Sirvio J., Jakala P., Mazurkiewicz M., Haapalinna A., Riekkinen P., and Riekkinen P. Dose- and parameter-dependent effects of atipamezole, and alpha2-antagonists, on the performance of rats in a five choice serial reaction time task. Pharmacol Biochem Behav 45 (1993) 123-129
115. Smith A., and Nutt D. Noradrenaline and attention lapses. Nature 380 (1996) 281
116. Stelzer A., Simon G., Kovacs G., and Rai R. Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield. Proc Natl Acad Sci U S A 91 (1994) 3058-3062
117. Stringer J.L., and Lothman E.W. Cholinergic and adrenergic agents modify the initiation and termination of epileptic discharges in the dentate gyrus. Neuropharmacology 30 (1991) 59-65
118. Sudweeks S., and Yakel J. Functional and molecular characterization of neuronal nicorinic ACh receptors in rat CA1 hippocampal neurons. J Physiol 527 (2000) 515-528
119. Tellez S., Colpaert F.C., and Marien M. Acetylcholine release in the rat prefrontal cortex in vivo: modulation by alpha2-adrenoreceptor agonists and antagonists. J Neurochem 68 (1997) 778-785
120. Tellez S., Colpaert F.C., and Marien M. alpha2-adrenoreceptor modulation of cortical acetylcholine release in vivo. Neuroscience 89 4 (1999) 1041-1050
121. Timofeeva O.A., and Peterson G.M. Dissociation of mossy fiber sprouting and electrically-induced seizure sensitivity: rapid kindling versus adaptation. Epilepsy Res 33 (1999) 99-115
122. Tsai G., and Coyle J. Glutamatergic mechanisms of schizophrenia. Annu Rev Pharmacol Toxicol 42 (2002) 165-179
123. Tsien J., Huerta P., and Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87 (1996) 1327-1338
124. Vankov A., Herve-Minvielle A., and Sara S.J. Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. Eur J Neurosci 7 (1995) 1180-1187
125. Warburton D.M. Nicotine as a cognitive enhancer. Prog Neuropsychopharmacol Biol Psychiatry 16 (1992) 181-191
126. Weiss S., Nosten-Bertrand M., McIntosh J.M., Giros B., and Martres M.P. Nicotine improves cognitive deficits of dopamine transporter knockout mice without long-term tolerance. Neuropsychopharmacology (2007)
127. Witkin J.M., Gasior M., Heifets B., and Tortella F.C. Anticonvulsant efficacy of N-methyl-d-aspartate antagonists against convulsions induced by cocaine. J Pharmacol Exp Ther 289 (1999) 703-711
128. Yamamoto S., Kanno T., Nagata T., Yaguchi T., Tanaka A., and Nishizaki T. The linoleic acid derivative FR236924 facilitates hippocampal synaptic transmission by enhancing activity of presynaptic alpha7 acetylcholine receptors on the glutamatergic terminals. Neuroscience 130 (2005) 207-213
129. Yavich L., Jakala P., and Tanila H. Noradrenaline overflow in mouse dentate gyrus following locus coeruleus and natural stimulation: real-time monitoring by in vivo voltammetry. J Neurochem 95 (2005) 641-650