Nitric oxide facilitates active avoidance learning via enhancement of glutamate levels in the hippocampal dentate gyrus

Behavioural Brain Research

Volumn 271, Issue , 2014, Pages 177-183

  Wang, Shi ^a   Pan, De Xi ^a,b   Wang, Dan ^a   Wan, Peng ^a   Qiu, De Lai ^a   Jin, Qing Hua ^a  

^a YANBIAN UNIVERSITY   (China)

^b CHINA JAPAN UNION HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

Active avoidance learning; Glutamate level; Hippocampal dentate gyrus; Nitric oxide; Synaptic efficiency

Indexed keywords

GLUTAMIC ACID; NITRIC OXIDE; ENZYME INHIBITOR; N(G) METHYLARGININE; NITRIC OXIDE DONOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIORAL SCIENCE; BRAIN LEVEL; CONTROLLED STUDY; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; MICRODIALYSIS; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; ANIMAL; DRUG EFFECTS; MEMORY; METABOLISM; MICROINJECTION; PHYSIOLOGY; PROBLEM BASED LEARNING; REINFORCEMENT; WISTAR RAT;

ANIMALS; AVOIDANCE LEARNING; DENTATE GYRUS; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXTINCTION, PSYCHOLOGICAL; GLUTAMIC ACID; MALE; MEMORY; MICROINJECTIONS; NITRIC OXIDE; NITRIC OXIDE DONORS; OMEGA-N-METHYLARGININE; PROBLEM-BASED LEARNING; RATS; RATS, WISTAR;

EID: 84903198322     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.06.011     Document Type: Article

References (68)

1. Grecksch G., Bernstein H.G., Becker A., Höllt V., Bogerts B. Disruption of latent inhibition in rats with postnatal hippocampal lesions. Neuropsychopharmacology 1999, 20:525-532.
2. Lehmann H., Lacanilao S., Sutherland R.J. Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories. Eur J Neurosci 2007, 25(5):1278-1286.
3. Harooni H.E., Naghdi N., Sepehri H., Rohani A.H. The role of hippocampal nitric oxide (NO) on learning and immediate, short- and long-term memory retrieval in inhibitory avoidance task in male adult rats. Behav Brain Res 2009, 201(1):166-172.
4. Manabe T. Molecular mechanism of hippocampal synaptic transmission, plasticity and memory. Mol Med 2004, 14(9):1095-1101.
5. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
6. Fedulov V., Rex C.S., Simmons D.A., Palmer L., Gall C.M., Lynch G. Evidence that long-term potentiation occurs within individual hippocampal synapses during learning. J Neurosci 2007, 27(30):8031-8039.
7. Bliss T.V.P., Collingridye G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
8. Bashir Z.I., Alford S., Davies S.N., Randall A.D., Collingridge G.L. Long-term potentiation of NMDA receptor-mediated synaptic transmission in the hippocampus. Nature 1991, 349:156-158.
9. Malenka R.C., Kauer J.A., Perkel D.J., Mauk M.D., Kelly P.T., Nicoll R.A., Waxham M.N. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 1989, 340(6234):554-557.
10. O'dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc Nat Acad Sci 1991, 88:11285-11289.
11. Bekkers J.M., Stevens C.F. Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 1990, 346(6286):724-729.
12. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., Snyder S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 1991, 7(4):615-624.
13. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991, 43(2):109-142.
14. Arancio O., Lev-Ram V., Tsien R.Y., Kandel E.R., Hawkins R.D. Nitric oxide acts as a retrograde messenger during long-term potentiation in cultured hippocampal neurons. J Physiol (Paris) 1996, 90:321-322.
15. Bon C.L.M., Garthwaite J. On the role of nitric oxide in hippocampal long-term potentiation. J. Neurosci 2003, 23:1941-1948.
16. Regehr W.G., Carey M.R., Best A.R. Activity-dependent regulation of synapses by retrograde messengers. Neuron 2009, 63:154-170.
17. Qiang M., Chen Y.C., Wang R., Wu F.M., Qiao J.T. Nitric oxide is involved in the formation of learning and memory in rats: studies using passive avoidance response and Morris water maze task. Behav Pharmacol 1997, 8:183-187.
18. Yildirim M., Marangoz C. Effects of nitric oxide on passive avoidance learning in rats. Int J Neurosci 2004, 114:597-606.
19. Zarrindast M.R., Shendy M.M., Ahmadi S. Nitric oxide modulates state dependency induced by lithium in an inhibitory avoidance task in mice. Behav Pharmacol 2007, 18:289-295.
20. Fin C., da Cunha C., Bromberg E., Schmitz P.K., Bianchin M., Medina J.H., Izquierdo I. Experiments suggesting a role for nitric oxide in the hippocampus in memory processes. Neurobiol Learn Mem 1995, 63:113-115.
21. Majlessi N., Choopani S., Bozorgmehr T., Azizi Z. Involvement of hippocampal nitric oxide in spatial learning in the rat. Neurobiol Learn Mem 2008, 90:413-419.
22. McClelland J.L., Goddard N.H. Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus 1996, 6:654-665.
23. Redish A.D., Touretzky D.S. Cognitive maps beyond the hippocampus. Hippocampus 1997, 7:15-35.
24. Kesner R.P., Lee I., Gilbert P. A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 2004, 15:333-351.
25. Rolls E.T., Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 2006, 79:1-48.
26. Austin K.B., Bronzino J.D., Morgane P.J. Paired-pulse facilitation and inhibition in the dentate gyrus is dependent on behavioral state. Exp Brain Res 1989, 77:1594-1604.
27. Bramham C.R., Srebro B. Synaptic plasticity in the hippocampus is modulated by behavioral state. Brain Res 1989, 493:74-86.
28. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic press, New York, NY. 2nd ed.
29. Jin Q.H., Yeda Y., Ishizuka Y., Kunitake T., Kannan H. Cardiovascular changes induced by central hypertonic saline are accompanied by glutamate release in awake rats. Am J Physiol Regul Integr Comp Physiol 2001, 281:R1224-R1231.
30. Garthwaite J., Boulton C.L. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 1995, 57:683-706.
31. Antonov I., Ha T., Antonova I., Moroz L.L., Hawkins R.D. Role of nitric oxide in classical conditioning of siphon withdrawal in aplysia. J Neurosci 2007, 27:10993-11002.
32. Edwards T.M., Rickard N.S. New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes. Neurosci Biobehav Rev 2007, 31:413-425.
33. Sadeghian R., Fereidoni M., Soukhtanloo M., Azizi-Malekabadi H., Hosseini M. Decreased nitric oxide levels in the hippocampus may play a role in learning and memory deficits in ovariectomized rats treated by a high dose of estradiol. Arq Neuropsiquiatr 2012, 70(11):874-879.
34. Prendergast M.A., Buccafusco J.J., Terry A.V. Nitric oxide synthase inhibition impairs spatial navigation learning and induces conditioned taste aversion. Pharmacol Biochem Behav. 1997, 57:347-352.
35. Zou L.B., Yamada K., Tanaka T., Kameyama T., Nabeshima T. Nitric oxide synthase inhibitors impair reference memory formation in a radial arm maze task in rats. Neuropharmacology 1998, 37:323-330.
36. Koylu E.O., Kanit L., Taskiran D., Dagci T., Balkan B., Pogun S. Effects of nitric oxide synthase inhibition on spatial discrimination learning and central DA2 and mACh receptors. Pharmacol Biochem Behav 2005, 81:32-40.
37. Prickaerts J., Steinbusch H.W., Smits J.F., de Vente J. Possible role of nitric oxidecyclic GMP pathway in object recognition memory: effects of 7-nitroindazole and zaprinast. Eur J Pharmacol 1997, 337:125-136.
38. Tashiro A., Makinott Gage F.H. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 2007, 27:3252-3259.
39. Martin S., Grimwood P., Morris R. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000, 23:649-711.
40. Matthies H., Ruethrich H., Ott T., Matthies H.K., Mathies R. Low frequency perforant path stimulation as a conditioned stimulus demonstrates correlations between long-term synaptic potentiation and learning. Physiol Behav 1986, 36:811-821.
41. Li C.H., Wang S.Z., Cai Z.L., Liu W.X., Xu S.T., Xiao P. Effects of intrahippocampal l-NAME treatment on the behavioral long-term potentiation in dentate gyrus. Neurosci Lett 2012, 528(2):201-204.
42. Bliss T., Collingridge G., Morris R. Introduction long-term potentiation and structure of the issue. Philos Trans R Soc Lond B Biol Sci 2003, 358:607-611.
43. Lisman J., Raghavachari S. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 2006, 2006(356):re11.
44. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001, 24:1071-1089.
45. Derkach V.A., Oh M.C., Guire E.S., Soderling T.R. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 2007, 8:101-113.
46. Bohme G.A., Bon C., Stutzmann J.M., Doble A., Blanchard J.C. Possible involvement of nitric oxide in long-term potentiation. Eur J Pharmacol 1991, 199:379-381.
47. Arancio O., Kiebler M., Lee C.J., Lev-Ram V., Tsien R.Y., Kandel E.R., Hawkins R.D. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 1996, 87:1025-1035.
48. Riedel G., Platt B., Micheau J. Glutamate receptor function in learning and memory. Behav Brain Res 2003, 140:1-47.
49. Collingridge G.L., Kehl S.J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 1983, 334:33-46.
50. Kirkwood A., Dudek S.M., Gold J.T., Aizenman C.D., Bear M.F. Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science 1993, 260:1518-1521.
51. Lumme A., Soinila S., Sadeniemi M., Halonen T., Vanhatalo S. Nitric oxide synthase immunoreactivity in the rat hippocampus after status epilepticus induced by perforant pathway stimulation. Brain Res 2000, 871:303-310.
52. Wang H.G., Lu F.M., Jin I., Udo H., Kandel E.R., de Vente J., Walter U., Lohmann S.M., Hawkins R.D., Antonova I. Presynaptic and postsynaptic roles of NO cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 2005, 45:389-403.
53. Schuman E.M., Madison D.V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 1991, 254:1503-1506.
54. Johnstone V.P., Raymond C.R. A protein synthesis and nitric oxide-dependent presynaptic enhancement in persistent forms of long-term potentiation. Learn Mem 2011, 18(10):625-633.
55. Blaise J.H., Bronzino J.D. Effects of stimulus frequency and age on bidirectional synaptic plasticity in the dentate gyrus of freely moving rats. Exp Neurol 2003, 182(2):497-506.
56. Carlini V.P., Perez M.F., Salde E., Schiöth H.B., Ramirez O.A., de Barioglio S.R. Ghrelin induced memory facilitation implicates nitric oxide synthase activation and decrease in the threshold to promote LTP in hippocampal dentate gyrus. Physiol Behav 2010, 101(1):117-123.
57. Christopherson K.S., Hillier B.J., Lim W.A., Bredt D.S. PSD-95 assembles a ternary complex with the N-methyl-d-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 1999, 274:27467-27473.
58. Piedrafita B., Cauli O., Montoliu C., Felipo V. The function of the glutamate-nitric oxide-cGMP pathway in brain in vivo and learning ability decrease in parallel in mature compared with young rats. Learn Mem 2007, 14:248-254.
59. Feil R., Kleppisch T. NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 2008, 184:529-560.
60. Llansola M., Hernandez-Viadel M., Erceg S., Montoliu C., Felipo V. Increasing the function of the glutamate-nitric oxide-cyclic guanosine monophosphate pathway increases the ability to learn a Y-maze task. J Neurosci Res 2009, 87:2351-2355.
61. Jiang Y., Liu Q.F., Bing Y.H., Pan D.X., Jin Y.Z., Jin Q.H. Effect of MK-801 on extracellular levels of glutamate in the hippocampal dentate gyrus during learning-dependent LTP in free-moving conscious rats. China J Mod Med 2009, 19(4):521-526.
62. Sun Z.G., Jiang Y., Bao J.S., Jin X.J., Jin Y.Z., Jin Q.H. Effect of AMPA receptors on learning and memory of the hippocampal dentate gyrus in free-moving conscious rats. Chin J Neurosurg 2009, 25(2):182-184.
63. Kopf S.R., Baratti C.M. Enhancement of the post-training cholinergic tone antagonizes the impairment of retention induced by a nitric oxide synthase inhibitor in mice. Neurobiol Learn Mem 1996, 65:207-212.
64. Majlessi N., Kadkhodaee M., Parviz M., Naghdi N. Serotonin depletion in rat hippocampus attenuates l-NAME-induced spatial learning deficits. Brain Res 2003, 963:244-251.
65. Getting S.J., Segieth J., Ahmad S., Biggs C.S., Whitton P.S. Biphasic modulation of GABA release by nitric oxide in the hippocampus of freely moving rats in vivo. Brain Res 1996, 717:196-199.
66. Prast H., Tran M.H., Fischer H., Philippu A. Nitric oxide-induced release of acetylcholine in the nucleus accumbens: role of cyclic GMP, glutamate, and GABA. J Neurochem 1998, 71:266-273.
67. Wegener G., Volke V., Rosenberg R. Endogenous nitric oxide decreases hippocampal levels of serotonin and dopamine in vivo. Br J Pharmacol 2000, 130:575-580.
68. Kleppisch T. Feil R. cGMP signalling in the mammalian brain: role in synaptic plasticity and behaviour. Handb Exp Pharmacol 2009, 191:549-579.