Role of glutamate NMDA receptors and nitric oxide located within the periaqueductal gray on defensive behaviors in mice confronted by predator

Psychopharmacology

Volumn 204, Issue 4, 2009, Pages 617-625

  Carvalho Netto, Eduardo F ^a,b   Gomes, Karina S ^a,b   Amaral, Vanessa C S ^b,c   Nunes De Souza, Ricardo L ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

Author keywords

Animal model and mice; Anxiety; Defense; Glutamate; Nitric oxide; Periaqueductal gray

Indexed keywords

GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N(G) PROPYLARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; DEFENSIVE BEHAVIOR; DOSE RESPONSE; DRUG DOSE COMPARISON; FREEZING; MALE; MOUSE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PREDATOR; PRIORITY JOURNAL;

ANIMALS; ARGININE; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEAR; FREEZING REACTION, CATALEPTIC; MALE; MICE; N-METHYLASPARTATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PERIAQUEDUCTAL GRAY; PREDATORY BEHAVIOR; RATS; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 67349235334     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-009-1492-9     Document Type: Article

References (60)

1. DC Aguiar AC De Lucca FS Guimarães 2004 Role of nitric oxide on chemically-induced defensive reactions in the dorsolateral periaqueductal grey Eur Neuropsychopharmacol 14 suppl. 3 S305
2. R Bandler P Carrive 1988 Integrated defense reaction elicited by excitatory amino acid in the midbrain periaqueductal gray region of the unrestrained cat Brain Res 439 95 106 (Pubitemid 18067510)
3. Bandler R, Depaulis A (1991) Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In: Bandler R, Depaulis A (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization. Plenum, New York, pp 175-197
4. R Bandler MT Shipley 1994 Columnar organization in the midbrain periaqueductal gray: modulates for emotional expression? Trends Neurosci 17 379 389 (Pubitemid 24256076)
5. R Bandler P Carrive SP Zhang 1991 Integration of somatic autonomic reactions within the midbrain periaqueductal gray: viscerotopic, somatotopic and functional organization Prog Brain Res 87 269 305
6. MM Behbehani 1995 Functional characteristics of the midbrain periaqueductal gray Progress Neurobiol 46 575 605
7. V Beijamini FS Guimarães 2006 c-Fos expression increase in NADPH-diaphorase positive neurons after exposure to a live cat Behav Brain Res 170 52 61
8. V Bergink HJGM Van Megen HGM Westenberg 2004 Glutamate and anxiety Eur Neuropharmacol 14 175 183 (Pubitemid 38410952)
9. LJ Bertoglio H Zangrossi Jr 2006 Involvement of dorsolateral periaqueductal gray N-methyl-d-aspartic acid glutamate receptors in the regulation of risk assessment and inhibitory avoidance behaviors in the rat elevated T-maze Behav Pharmacol 17 589 596 (Pubitemid 44526735)
10. RJ Blanchard MA Hebert PF Ferrari P Palanza R Figueira DC Blanchard S Parmigiani 1998 Defensive behaviors in wild and laboratory (Swiss) mice: the mouse defense test battery Physiol Behav 65 2 201 209 (Pubitemid 28548639)
11. A Calvo-Torrent PF Brain M Martinez 1999 Effect of predatory stress on sucrose intake and behavior on the plus-maze in male mice Physiol Behav 67 189 196 (Pubitemid 29361419)
12. AP Carobrez KV Teixeira FG Graeff 2001 Modulation of defensive behavior by periaqueductal gray NMDA/glycine-B receptor Neurosci Biobehav Rev 25 697 709 (Pubitemid 34136899)
13. P Carrive 1993 The periaqueductal gray and defensive behavior: functional significance and neuronal organization Behav Brain Res 58 27 47 (Pubitemid 24024043)
14. EF Carvalho-Netto C Markham DC Blanchard RL Nunes-De-Souza RJ Blanchard 2006 Physical environment modulates the behavioral responses induced by chemical stimulation of dorsal periaqueductal gray in mice Pharmacol Biochem Behav 85 140 147 (Pubitemid 44772916)
15. EF Carvalho-Netto Y Litvin RL Nunes-De-Souza DC Blanchard RJ Blanchard 2007 Effects of intra-PAG infusion of ovine CRF on defensive behaviors in Swiss-Webster mice Behav Brain Res 176 222 229 (Pubitemid 44880085)
16. RW De Oliveira FS Guimarães 1999 Anxiolytic effect of methylene blue microinjected into the dorsal periaqueductal gray Braz J Med Biol Res 32 1529 1532 (Pubitemid 30053339)
17. RW De Oliveira EA Del Bel FS Guimarães 2001 Effects of excitatory amino acids and nitric oxide on flight behavior elicited from the dorsolateral periaqueductal gray Neurosci Biobehav Rev 25 679 685 (Pubitemid 34136897)
18. J Esplugues 2002 NO as a signalling molecule in the nervous system Br J Pharmacol. 135 1079 1095 (Pubitemid 34259107)
19. MS Faria MN Muscara H Moreno Jr SA Dias B Oliveira FG Graeff G De Nucci 1997 Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test Eur J Pharmacol 323 37 343
20. D Forestiero CM Manfrim FS Guimarães RM De Oliveira 2006 Anxiolytic-like effects induced by nitric oxide synthase inhibitors microinjected into the medial amygdala of rats Psychopharmacology (Berl) 184 166 172 (Pubitemid 43083653)
21. J Garthwaite 1991 Glutamate, nitric oxide and cell-cell signalling in the nervous system Trends Neurosci 14 60 67
22. J Garthwaite G Garthwaite RM Palmer S Moncada 1989 NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices Eur J Pharmacol 172 413 416 (Pubitemid 19258411)
23. FG Graeff 1981 Minor tranquilizers and brain defense system Braz J Med Biol Res 14 239 265
24. FG Graeff 1994 Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals Braz J Med Biol Res 27 4 811 829
25. FG Graeff 2004 Serotonin, the periaqueductal gray and panic Neurosci Biobehav Rev 28 239 259 (Pubitemid 38844374)
26. FS Guimarães AP Carobrez JC De Aguiar FG Graeff 1991 Anxiolytic effect in the elevated plus maze of NMDA receptor antagonist AP 7 microinjected into the dorsal periaqueductal gray Psychopharmacology (Berl) 103 91 94
27. FS Guimarães JC De Aguiar EA Del-Bel G Ballejo 1994 Anxiolytic effect of NO synthase inhibitors microinjected into the dorsal central grey Neuro Report 5 123 126
28. FS Guimarães V Beijamini FA Moreira DC Aguiar ACB De Luca 2005 Role of nitric oxide on brain regions related to defensive reactions Neurosci Biobehav Rev 29 1313 1322 (Pubitemid 41446902)
29. HC Lin BH Kang FJ Wan ST Huang CJ Tseng 2000 Reciprocal regulation of nitric oxide and glutamate in the nucleus tractus solitarii of rats Eur J Pharmacol 407 83 89
30. Y Litvin NS Pentkowski DC Blanchard RJ Blanchard 2007 CRF type 1 receptors in the dorsal periaqueductal gray modulate anxiety-induced defensive behaviors Horm Behav 52 244 251 (Pubitemid 47088452)
31. Litvin Y, Pentkowski NS, Pobbe RL, Blanchard DC, Blanchard RJ (2008) Unconditioned models of fear and anxiety. In: Blanchard DC, Blanchard RJ, Griebel G, Nutt D (eds) Handbook of anxiety and fear. Academic Press, Amsterdam, pp 82-99
32. MJ Lohse U Forstermann HHHW Schmidt 1998 Pharmacology of NO: cGMP signal transduction Naunyn-Schmiedeberg's Arch Pharmacol 358 111 112
33. TA Lovick DM Parry VV Stezhka BM Lumb 2000 Serotonergic transmission in the periaqueductal gray matter in relation to aversive behaviour: morphological evidence for direct modulatory effects on identified output neurons Neurosci 95 763 772
34. CM Markham DC Blanchard NS Canteras CD Cuyno RJ Blanchard 2004 Modulation of predatory odor processing following lesions to the dorsal premammillary nucleus Neurosci Lett. 372 22 26 (Pubitemid 39505221)
35. RC Martinez A Ribeiro De Oliveira ML Brandão 2007 Serotonergic mechanisms in the basolateral amygdala differentially regulate the conditioned and unconditioned fear organized in the periaqueductal gray Eur Neuropychopharmacol 17 717 724 (Pubitemid 47419292)
36. RC Martinez EF Carvalho-Netto VC Amaral RL Nunes-de-Souza NS Canteras 2008 Investigation of the hypothalamic defensive system in the mouse Behav Brain Res 192 2 185 190
37. MG Matheus RL Nogueira AP Carobrez FG Graeff FS Guimarães 1994 Anxiolytic effect of glycine antagonists microinjected into the dorsal periaqueductal grey Psychopharmacology (Berl) 113 565 569 (Pubitemid 24150512)
38. N McNaughton PJ Corr 2004 A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance Neurosci Biobehav Rev 28 285 305 (Pubitemid 38844377)
39. J Mendes-Gomes RL Nunes-De-Souza 2005 Concurrent nociceptive stimulation impairs the anxiolytic effect of midazolam injected into the periaqueductal gray in mice Brain Res 1047 97 104 (Pubitemid 40805034)
40. TT Miguel RL Nunes-De-Souza 2006 Defensive-like behaviors and antinociception induced by NMDA injection into the periaqueductal gray of mice depend on nitric oxide synthesis Brain Res 1076 42 48 (Pubitemid 43379171)
41. TT Miguel RL Nunes-De-Souza 2008 Anxiogenic-like effects induced by NMDA receptor activation are prevented by inhibition of neuronal nitric oxide synthase in the periaqueductal gray in mice Brain Res 1240 39 46
42. ML Molchanov FS Guimarães 2002 Anxiolytic-like effects of AP7 injected into the dorsolateral or ventrolateral columns of the periaqueductal gray of rats Psychopharmacology (Berl) 160 30 38 (Pubitemid 34169823)
43. FA Moreira FS Guimarães 2004 Benzodiazepine receptor and serotonin 2A receptor modulate the aversive-like effects of nitric oxide in the dorsolateral periaqueductal gray of rats Psychopharmacology (Berl) 176 362 368 (Pubitemid 40012743)
44. M O'Boyle 1974 Rats and mice together: the predatory nature of the rat's mouse-killing response Psychol Bull 81 4 261 269
45. M O'Boyle 1975 The rat as a predator Psychol Bull 82 460 462
46. D Okada 1992 Two pathways of cyclic GMP production through glutamate receptor-mediated nitric oxide synthesis J Neurochem 59 1203 1210
47. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press, California
48. G Reiser 1990 Mechanism of stimulation of cyclic-GMP level in a neuronal cell line mediated by serotonin (5-HT3) receptors. Involvement of nitric oxide, arachidonic-acid metabolism and cytosolic Ca2+ Eur J Biochem 189 547 552 (Pubitemid 20180427)
49. 2+ ionophore raise cyclic GMP levels in a neuronal cell line via formation of nitric oxide Br J Pharmacol 101 722 726 (Pubitemid 20357202)
50. P Santos AS Bittencourt LC Schenberg AP Carobrez 2006 Elevated T-maze evaluation of anxiety and memory effects of NMDA/glycine-B site ligands injected into the dorsal periaqueductal gray matter and the superior colliculus of rats Neuropharmacol 51 203 212 (Pubitemid 44061884)
51. LC Schenberg AS Bittencourt ECM Sudré LC Vargas 2001 Modeling panic attacks Neurosci Behav Rev 25 647 659 (Pubitemid 34136894)
52. ML Schmitt W Coelho AS Lopes-De-Souza FS Guimarães AP Carobrez 1995 Anxiogenic-like effect of glycine and D-serine microinjected into dorsal periaqueductal gray matter of rats Neurosci Lett 189 93 96
53. E Southam SJ East J Garthwaite 1991 Excitatory amino acid receptors coupled to the nitric oxide/cyclic GMP pathway in rat cerebellum during development J Neurochem 56 2072 2081
54. PC Spolidório MB Echeverry M Iyomasa FS Guimarães EA Del Bel 2007 Anxiolytic effects induced by inhibition of the nitric oxide-cGMP pathway in the rat dorsal hippocampus Psychopharmacoly (Berl) 195 183 192 (Pubitemid 350045842)
55. KV Teixeira AP Carobrez 1999 Effects of glycine or (+/-)-3-amino-1- hydroxy-2-pyrrolidone microinjections along the rostrocaudal axis of the dorsal periaqueductal gray matter on rats' performance in the elevated plus-maze task Behav Neurosci 113 196 203 (Pubitemid 29138460)
56. V Volke A Soosaar S Koks M Bourin PT Mannisto 1995 Inhibition of nitric oxide synthase causes anxiolytic-like behavior in an elevated plus-maze NeuroReport 6 1413 1416
57. V Volke G Wegener M Bourin E Vasar 2003 Antidepressant- and anxiolytic-like effects of selective neuronal NOS inhibitor 1-(2- trifluoromethylphenyl)-imidazole in mice Behav Brain Res 140 141 147 (Pubitemid 36313249)
58. G Wegener V Volke R Rosenberg 2000 Endogenous nitric oxide decreases hippocampal levels of serotonin and dopamine in vivo Br J Pharmacol 130 575 580 (Pubitemid 30332975)
59. PS Whitton DA Richards CS Biggs LJ Fowler 1994 N-methyl-d-aspartate receptors modulate extracellular 5-hydroxytryptamine concentration in rat hippocampus and striatum in vivo Neurosci Lett 169 215 218
60. M Yang H Augustsson C Markham DT Hubbard D Webster PM Wall RJ Blanchard DC Blanchard 2004 The rat exposure test: a model of mouse defensive behaviors Physiol Behav 81 465 473 (Pubitemid 38591535)