Lateral septal infusions of the neuropeptide Y Y2 receptor agonist, NPY13-36 differentially affect different defensive behaviors in male, Long Evans rats

Physiology and Behavior

Volumn 110-111, Issue , 2013, Pages 20-29

  Trent, Natalie L ^a   Menard, Janet L ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

Animal models of anxiety; Anxiety; Behavioral defense; Emotion; Fear; Lateral septum; Neuropeptide Y2 receptors

Indexed keywords

N [2 [1,2 DIHYDRO 3,5(4H) DIOXO 1,2 DIPHENYL 1,2,4 TRIAZOL 4 YL]ETHYL] N2 [[1 [2 [4 [5,11 DIHYDRO 6(6H) OXODIBENZ[B,E]AZEPIN 11 YL] 1 PIPERAZINYL] 2 OXOETHYL]CYCLOPENTYL]ACETYL]ARGININAMIDE; NEUROPEPTIDE Y [13-36]; NEUROPEPTIDE Y2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ANXIETY DISORDER; APPETITE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; DRUG INFUSION; EXPLORATORY BEHAVIOR; LATENT PERIOD; LATERAL SEPTUM; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; THREAT; TRANQUILIZING ACTIVITY;

EID: 84872440879     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2012.12.011     Document Type: Article

References (73)

1. Heilig M. The NPY, system in stress, anxiety and depression. Neuropeptides 2004, 38:213-224.
2. Kask A., Harro J., von Horsten S., Redrobe J.P., Dumont Y., Quirion R. The neurocircuitry and receptor subtypes mediating the anxiolytic-like effects of neuropeptide Y. Neurosci Biobehav Rev 2002, 26:259-283.
3. Wu G., Feder A., Wegener G., Bailey C., Saxena S., Charney D., et al. Central functions of neuropeptide Y in mood and anxiety disorders. Expert Opin Ther Targets 2011, 15:1317-1331.
4. Domschke K., Hohoff C., Jacob C., Maier W., Fritze J., Bandelow B., et al. Chromosome 4q31-34 panic disorder risk locus: association of neuropeptide Y Y5 receptor variants. Am J Med Genet B Neuropsychiatr Genet 2008, 147B:510-516.
5. Nikisch G., Baumann P., Liu T., Mathe A.A. Quetiapine affects neuropeptide Y and corticotropin-releasing hormone in cerebrospinal fluid from schizophrenia patients: relationship to depression and anxiety symptoms and to treatment response. Int J Neuropsychopharmacol 2011, 15:1051-1061.
6. Sah R., Ekhator N.N., Strawn J.R., Sallee F.R., Baker D.G., Horn P.S., et al. Low cerebrospinal fluid neuropeptide Y concentrations in posttraumatic stress disorder. Biol Psychiatry 2009, 66:705-707.
7. Bannon A.W., Seda J., Carmouche M., Francis J.M., Norman M.H., Karbon B., et al. Behavioral characterization of neuropeptide Y knockout mice. Brain Res 2000, 868:79-87.
8. Karl T., Duffy L., Herzog H. Behavioural profile of a new mouse model for NPY deficiency. Eur J Neurosci 2008, 28:173-180.
9. Carvajal C.C., Vercauteren F., Dumont Y., Michalkiewicz M., Quirion R. Aged neuropeptide Y transgenic rats are resistant to acute stress but maintain spatial and non-spatial learning. Behav Brain Res 2004, 153:471-480.
10. Thorsell A., Michalkiewicz M., Dumont Y., Quirion R., Caberlotto L., Rimondini R., et al. Behavioral insensitivity to restraint stress, absent fear suppression of behavior and impaired spatial learning in transgenic rats with hippocampal neuropeptide Y overexpression. Proc Natl Acad Sci U S A 2000, 97:12852-12857.
11. Cohen H., Liu T., Kozlovsky N., Kaplan Z., Zohar J., Mathe A.A. The neuropeptide Y (NPY)-ergic system is associated with behavioral resilience to stress exposure in an animal model of post-traumatic stress disorder. Neuropsychopharmacology 2012, 37:350-363.
12. Heilig M., Murison R. Intracerebroventricular neuropeptide Y suppresses open field and home cage activity in the rat. Regul Pept 1987, 19:221-231.
13. Heilig M., Soderpalm B., Engel J.A., Widerlov E. Centrally administered neuropeptide Y (NPY) produces anxiolytic-like effects in animal anxiety models. Psychopharmacology 1989, 98:524-529.
14. Karlsson R., Holmes A., Heilig M., Crawley J.N. Anxiolytic-like actions of centrally-administered neuropeptide Y, but not galanin, in C57BL/6J mice. Pharmacol Biochem Behav 2005, 80:427-436.
15. Heilig M., McLeod S., Menzaghi F., Heinrichs S.C., Brot M., Koob G.F., et al. Anxiolytic-like action of neuropeptide Y: mediation by Y1 receptors in amygdala, and dissociation from food intake effects. Neuropsychopharmacology 1993, 8:357-363.
16. Sajdyk T.J., Vandergriff M.G., Gehlert D.R. Amygdalar neuropeptide Y Y1 receptors mediate the anxiolytic-like actions of neuropeptide Y in the social interaction test. Eur J Pharmacol 1999, 368:143-147.
17. Kask A., Nguyen H.P., Pabst R., von Horsten S., Neuropeptide Y. Y1 receptor-mediated anxiolysis in the dorsocaudal lateral septum: functional antagonism of corticotrophin releasing hormone-induced anxiety. Neuroscience 2001, 104:259-283.
18. Smialowska M.S., Wieronska J.M., Domin H., Zieba B. The effect of intrahippocampal injection of group II and III metabotropic glutamate receptor agonists on anxiety; the role of neuropeptide Y. Neuropsychopharmacology 2007, 32:1242-1250.
19. Harro J. CCK and NPY as anti-anxiety treatment targets: promises, pitfalls, and strategies. Amino Acids 2006, 31:215-230.
20. Bleakman D., Harrison N.L., Colmers W.F., Miller R.J. Investigations into neuropeptide Y-mediated presynaptic inhibition in cultured hippocampal neurones of the rat. Br J Pharmacol 1992, 107:334-340.
21. Greber S., Schwarzer C., Sperk G. Neuropeptide Y inhibits potassium-stimulated glutamate release through Y2 receptors in rat hippocampal slices in vitro. Br J Pharmacol 1994, 113:737-740.
22. Silva A.P., Carvalho A.P., Carvalho C.M., Malva J.O. Modulation of intracellular calcium changes and glutamate release by neuropeptide Y1 and Y2 receptors in the rat hippocampus: differential effects in CA1, CA3 and dentate gyrus. J Neurochem 2001, 79:286-296.
23. Silva A.P., Carvalho A.P., Carvalho C.M., Malva J.O. Functional interaction between neuropeptide Y receptors and modulation of calcium channels in the rat hippocampus. Neuropharmacology 2003, 44:282-292.
24. Bacci A., Huguenard J.R., Prince D.A. Differential modulation of synaptic transmission by neuropeptide Y in rat neocortical neurons. Proc Natl Acad Sci U S A 2002, 99:17125-17130.
25. Silva A.P., Xapelli S., Grouzmann E., Cavadas C. The putative neuroprotective role of neuropeptide Y in the central nervous system. Curr Drug Targets CNS Neurol Disord 2005, 4:331-347.
26. Chen G., van den Pol A.N. Multiple NPY receptors coexist in pre and postsynaptic sites: inhibition of GABA release in isolated self-innervated SCN neurons. J Neurosci 1996, 16:7711-7724.
27. Allen Y.S., Adrian T.E., Allen J.M., Tatemoto K., Crow T.J., Bloom S.R., et al. Neuropeptide Y distribution in rat brain. Science 1983, 221:877-879.
28. Martel J.C., St-Pierre J.A., Quirion R. Neuropeptide Y receptors in rat brain: autoradiographic localization. Peptides 1986, 7:55-60.
29. Larsen P.J., Sheikh S.P., Jakobsen C.R., Schwa T.W., Mikkelsen J.D. Regional distribution of putative NPY Y, receptors and neurons expressing Y, mRNA in forebrain areas of the rat central nervous system. Eur J Neurosci 1993, 5:1622-1637.
30. 13-36 microinjected into vicinity of locus coeruleus in rats. Brain Res 1998, 788:345-348.
31. Trent N.L., Menard J.L. Infusions of NPY into the lateral septum reduce anxiety-related behaviors in the rat. Pharmacol Biochem Behav 2011, 99:580-590.
32. Redrobe J.P., Dumont Y., Herzog H., Quirion R. Neuropeptide Y (NPY) Y2 receptors mediate behaviour in two animal models of anxiety: evidence from Y2 receptor knockout mice. Behav Brain Res 2003, 141:251-255.
33. Tschenett A., Singewald N., Carli M., Balducci C., Salchner P., Vezzani A., et al. Reduced anxiety and improved stress coping ability in mice lacking NPY-Y2 receptors. Eur J Neurosci 2003, 18:143-148.
34. Nakajima M., Inui A., Asakawa A., Momose K., Ueno N., Teranishi A., et al. Neuropeptide Y produces anxiety via Y2-type receptors. Peptides 1998, 19:359-363.
35. Broqua P., Wettstein J.G., Rocher M.N., Gauthier-Martin B., Junien J.L. Behavioral effects of neuropeptide Y receptor agonists on the elevated plus-maze and fear-potentiated startle procedures. Behav Pharmacol 1995, 6:215-222.
36. Britton K.T., Southerland S., Van Uden E., Kirby D., Rivier J., Koob G. Anxiolytic activity of NPY receptor agonists in the conflict test. Psychopharmacology 1997, 132:6-13.
37. Sorensen G., Lindberg C., Wortwein G., Bolwig T.G., Woldbye D.P. Differential roles for neuropeptide Y Y1 and Y5 receptors in anxiety and sedation. J Neurosci Res 2004, 77:723-729.
38. Sajdyk T.J., Schoberb D.A., Smiley D.L., Gehlert D.R. Neuropeptide Y-Y2 receptors mediate anxiety in the amygdala. Pharmacol Biochem Behav 2002, 71:419-423.
39. Dumont Y., Cadieux A., Doods H., Fournier A., Quirion R. Potent and selective tools to investigate neuropeptide Y receptors in the central and peripheral nervous systems: BIBO 3304 (Y1) and CGP71683A (Y5). Can J Physiol Pharmacol 2000, 78:116-125.
40. Drugan R.C., Skolnick P., Paul S.M., Crawley J.N. Low doses of muscimol produce anticonflict actions in the lateral septum of the rat. Neuropharmacology 1986, 25:203-205.
41. Pesold C., Treit D. Excitotoxic lesions of the septum produce anxiolytic effects in the elevated plus-maze and the shock-probe burying tests. Physiol Behav 1992, 52:37-47.
42. Pesold C., Treit D. The neuroanatomical specificity of the anxiolytic effects of intra-septal infusions of midazolam. Brain Res 1996, 710:161-168.
43. Menard J., Treit D. Lateral and medial septal lesions reduce anxiety in the plus-maze and probe-burying tests. Physiol Behav 1996, 60:845-853.
44. Molina M., Tellez-Alcantara P., Perez J., Olivera J., Jaramillo T. Anti-conflict-like actions of intra-lateral septal infusions of allopregnanolone in Wistar rats. Pharmacol Biochem Behav 2003, 75:397-404.
45. Trent N.L., Menard J.L. The ventral hippocampus and the lateral septum work in tandem to regulate rats' open-arm exploration in the elevated plus-maze. Physiol Behav 2010, 101:141-152.
46. Molina-Hernandez M., Tellez-Alcantara N.P., Olivera-Lopez J.I., Jaramillob M.T. Antidepressant- like or anxiolytic-like actions of topiramate alone or co-administered with intra-lateral septal infusions of neuropeptide Y in male Wistar rats. Peptides 2010, 31:1184-1189.
47. Doods H., Gaida W., Wieland H.A., Dollinger H., Schnorrenberg G., Esser F., et al. BIIE0246: A selective and high affinity neuropeptide Y Y receptor 2 antagonist. Eur J Pharmacol 1999, 384:R3-R5.
48. 3-36 binding sites in the rat brain evaluated with two newly developed Y1 and Y2 receptor radioligands. Synapse 1996, 22:139-158.
49. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, New York.
50. Abbott C.R., Small C.J., Kennedy A.R., Neary N.M., Sajedi A., Ghatei M.A., et al. Blockade of the neuropeptide Y Y2 receptor with the specific antagonist BIIE0246 attenuates the effect of endogenous and exogenous peptide YY(3-36) on food intake. Brain Res 2005, 1043:139-144.
51. Blanchard D.C., Griebel G., Pobbe R., Blanchard R.J. Risk assessment as an evolved threat detection and analysis process. Neurosci Biobehav Rev 2011, 35:991-998.
52. Rodgers R.J., Dalvi A. Anxiety, defense, and the elevated plus-maze. Neurosci Biobehav Rev 1997, 21:801-810.
53. Rodgers R.J., Johnson N.J. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol Biochem Behav 1995, 52:297-303.
54. Pellow S., Chopin P., File S.E., Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167.
55. Lever C., Burton S., O'Keefe J. Rearing on hind legs, environmental novelty, and the hippocampal formation. Rev Neurosci 2006, 17:111-133.
56. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
57. Merali Z., Levac C., Anisman H. Validation of a simple, ethologically relevant paradigm for assessing anxiety in mice. Biol Psychiatry 2003, 54:552-565.
58. Treit D., Pinel J.P.J., Fibiger H.C. Conditioned defensive burying: a new paradigm for the study of anxiolytic agents. Pharmacol Biochem Behav 1981, 15:619-626.
59. De Boer S.F., Koolhaas J.M. Defensive burying in rodents: ethology, neurobiology and psychopharmacology. Eur J Pharmacol 2003, 463:145-161.
60. Pich E.M., Solfrini V., Marrama P., Tiengo M., Agnati L.F., Carani C. Centrally administered neuropeptide Y fails to increase food intake but enhances hypoalgesia in spontaneously hypertensive rats. Neurosci Lett 1993, 149:209-212.
61. Broqua P., Wettstein J.G., Rocher M.N., Gauthier-Martin B., Riviere P.J.M., Junien J.L. Antinociceptive effects of neuropeptide Y and related peptides in mice. Brain Res 1996, 724:25-32.
62. Martin J.H. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci Lett 1991, 127:160-164.
63. Olivera-Lopez J.I., Molina-Hernandez M., Tellez-Alcantara N.P., Jaramillo M.T. Estradiol and neuropeptide Y (intra-lateral septal) reduce anxiety-like behavior in two animal models of anxiety. Peptides 2008, 29:1396-1403.
64. Gerald C., Walker M.W., Criscione L., Gustafson E.L., Batzl-Hartmann C., Smith K.E., et al. A receptor subtype involved in neuropeptide-Y-induced food intake. Nature 1996, 382:168-171.
65. Bacchi F., Mathe A.A., Jimenez P., Stasi L., Arban R., Gerrard P., et al. Anxiolytic-like effect of the selective neuropeptide Y Y2 receptor antagonist BIIE0246 in the elevated plus-maze. Peptides 2006, 27:3203-3207.
66. Morales-Medina J.C., Dumont Y., Benoit C.E., Bastianetto S., Flores G., Fournier A., et al. Role of neuropeptide Y Y1 and Y2 receptors on behavioral despair in a rat model of depression with co-morbid anxiety. Neuropharmacology 2012, 62:200-208.
67. King P.J., Williams G., Doods H., Widdowson P.S. Effect of a selective neuropeptide Y Y(2) receptor antagonist, BIIE0246 on neuropeptide Y release. Eur J Pharmacol 2000, 396:R1-R3.
68. Chee S.A., Menard J.L. Lesions of the dorsal lateral septum do not affect neophagia in the novelty induced suppression of feeding paradigm but reduce defensive behaviours in the elevated plus maze and shock probe burying tests. Behav Brain Res 2011, 220:362-366.
69. Molina-Hernandez M., Olivera-Lopez J.I., Tellez-Alcantara N.P., Perez-Garcia J., Jaramillo M.T. Estrus variation in anxiolytic-like effects of intra-lateral septal infusions of the neuropeptide Y in Wistar rats in two animal models of anxiety-like behavior. Peptides 2006, 27:2722-2730.
70. Rodi D., Mazzuferi M., Bregola G., Dumont Y., Fournier A., Quirion R., et al. Changes in NPY-mediated modulation of hippocampal [3H]d-aspartate outflow in the kindling model of epilepsy. Synapse 2003, 49:116-124.
71. Risold P.Y., Swanson L.W. Connections of the rat lateral septal complex. Brain Res Rev 1997, 24:115-195.
72. Menard J., Treit D. Intra-septal infusions of excitatory amino acid receptor antagonists have differential effects in two animal models of anxiety. Behav Pharmacol 2000, 11:99-108.
73. Morin S.M., Gehlert D.R. Distribution of NPY Y5-like immunoreactivity in the rat brain. J Mol Neurosci 2006, 29:109-114.