Oxytocin and vasopressin modulate the social response to threat: A preclinical study

International Journal of Neuropsychopharmacology

Volumn 17, Issue 10, 2014, Pages 1621-1633

  Bowen, Michael T ^a   McGregor, Iain S ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Anxiety; Defensive behaviour; Oxytocin; Social behaviour; Vasopressin

Indexed keywords

1-(5-CHLORO-1-((2,4-DIMETHOXYPHENYL)SULFONYL)-3-(2-METHOXYPHENYL)-2-OXO-2,3-DIHYDRO-1H-INDOL-3-YL)-4-HYDROXY-N,N-DIMETHYL-2-PYRROLIDINECARBOXAMIDE; HORMONE ANTAGONIST; INDOLE DERIVATIVE; OXYTOCIN; PYRROLIDINE DERIVATIVE; RELCOVAPTAN; VASOPRESSIN DERIVATIVE;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMAL; CAT; DISEASE MODEL; DRUG EFFECTS; DRUG INTERACTION; DRUG THERAPY; MALE; MENTAL STRESS; ODOR; PSYCHOLOGY; RAT; WISTAR RAT;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; CATS; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; HORMONE ANTAGONISTS; INDOLES; MALE; ODORS; OXYTOCIN; PYRROLIDINES; RATS; RATS, WISTAR; STRESS, PSYCHOLOGICAL; VASOPRESSINS;

EID: 84930243696     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145714000388     Document Type: Article

References (64)

1. Alberts JR (2007) Huddling by rat pups: ontogeny of individual and group behavior. Dev Psychobiol 49:22-32.
2. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123-1144.
3. Bales KL, Perkeybile AM, Conley OG, Lee MH, Guoynes CD, Downing GM, Yun CR, Solomon M, Jacob S, Mendoza SP (2013) Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles. Biol Psychiatry 74:180-188.
4. Beels CC (1981) Social support and schizophrenia. Schizophr Bull 7:58.
5. Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ (2004a) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29:483-493.
6. Bielsky IF, Hu S-B, Szegda KL, Westphal H, Young LJ (2004b) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29:483-493.
7. Blanchard RJ, Griebel G, Farrokhi C, Markham C, Yang M, Blanchard DC (2005) AVP V1b selective antagonist SSR149415 blocks aggressive behaviors in hamsters. Pharmacol Biochem Behav 80:189-194.
8. Bleickardt CJ, Mullins DE, MacSweeney CP, Werner BJ, Pond AJ, Guzzi MF, Martin FDC, Varty GB, Hodgson RA (2009) Characterization of the V1a antagonist, JNJ-17308616, in rodent models of anxiety-like behavior. Psychopharmacology (Berl) 202:711-718.
9. Boakes R, Boot B, Clarke J, Carver A (2000) Comparing albino and hooded Wistar rats of both sexes on a range of behavioral and learning tasks. Psychobiology 28:339-359.
10. Bosch OJ, Neumann ID (2012) Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm Behav 61:293-303.
11. Bowen MT, Carson DS, Spiro A, Arnold JC, McGregor IS (2011) Adolescent oxytocin exposure causes persistent reductions in anxiety and alcohol consumption and enhances sociability in rats. PLoS ONE 6:e27237.
12. Bowen MT, Keats K, Kendig MD, Cakic V, Callaghan PD, McGregor IS (2012) Aggregation in quads but not pairs of rats exposed to cat odor or bright light. Behav Processes 90:331-336.
13. Bowen MT, Kevin RC, May M, Staples LG, Hunt GE, McGregor IS (2013) Defensive aggregation (huddling) in Rattus Norvegicus toward predator odor: individual differences, social buffering effects and neural correlates. PLoS ONE 8:e68483.
14. Braida D, Donzelli A, Martucci R, Capurro V, Busnelli M, Chini B, Sala M (2012) Neurohypophyseal hormones manipulation modulate social and anxiety-related behavior in zebrafish. Psychopharmacology (Berl) 220:319-330.
15. Caraco T, Martindale S, Pulliam HR (1980) Avian flocking in the presence of a predator. Nature 285:400-401.
16. Chini B, Manning M (2007) Agonist selectivity in the oxytocin/vasopressin receptor family: new insights and challenges. Biochem Soc Trans 35:737-741.
17. Dielenberg RA, McGregor IS (2001) Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 25:597-609.
18. Dielenberg RA, Carrive P, McGregor I (2001) The cardiovascular and behavioral response to cat odor in rats: unconditioned and conditioned effects1. Brain Res 897:228-237.
19. Dielenberg RA, Leman S, Carrive P (2004) Effect of dorsal periaqueductal gray lesions on cardiovascular and behavioral responses to cat odor exposure in rats. Behav Brain Res 153:487-496.
20. Feifel D, MacDonald K, Cobb P, Minassian A (2012) Adjunctive intranasal oxytocin improves verbal memory in people with schizophrenia. Schizophr Res 139:207-210.
21. Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466-467.
22. Goodson JL, Schrock SE, Klatt JD, Kabelik D, Kingsbury MA (2009) Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science 325:862-866.
23. Griebel G, Simiand J, Serradeil-Le Gal C, Wagnon J, Pascal M, Scatton B, Maffrand JP, Soubrie P (2002) Anxiolytic- and antidepressant-like effects of the non-peptide vasopressin V1b receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders. Proc Natl Acad Sci U S A 99:6370-6375.
24. Griebel G, Stemmelin J, Gal CS, Soubrie P (2005) Non-peptide vasopressin V1b receptor antagonists as potential drugs for the treatment of stress-related disorders. Curr Pharm Des 11:1549-1559.
25. Gump BB, Kulik JA (1997) Stress, affiliation, and emotional contagion. J Pers Soc Psychol 72:305-319.
26. Hamilton W (1971) Geometry for the selfish herd. J Theor Biol 31:295-311.
27. Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U (2003) Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 54:1389-1398.
28. Hollander E, Novotny S, Hanratty M, Yaffe R, DeCaria CM, Aronowitz BR, Mosovich S (2003) Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology 28:193-198.
29. Hollander E, Bartz J, Chaplin W, Phillips A, Sumner J, Soorya L, Anagnostou E, Wasserman S (2007) Oxytocin increases retention of social cognition in autism. Biol Psychiatry 61:498-503.
30. Johnson AE, Audigier S, Rossi F, Jard S, Tribollet E, Barberis C (1993) Localization and characterization of vasopressin binding sites in the rat brain using an iodinated linear AVP antagonist. Brain Res 622:9-16.
31. Kelly AM, Kingsbury MA, Hoffbuhr K, Schrock SE, Waxman B, Kabelik D, Thompson RR, Goodson JL (2011) Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty. Horm Behav 60:12-21.
32. Kendig MD, Bowen MT, Kemp AH, McGregor IS (2011) Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience. Behav Brain Res 225:405-414.
33. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc B Biol Sci 361:2215-2228.
34. Kojima S, Alberts JR (2011) Oxytocin mediates the acquisition of filial, odor-guided huddling for maternally-associated odor in preweanling rats. Horm Behav 60:549-558.
35. Lukas M, Toth I, Reber SO, Slattery DA, Veenema AH, Neumann ID (2011) The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacology 36:2159-2168.
36. Mak P, Broussard C, Vacy K, Broadbear JH (2012) Modulation of anxiety behavior in the elevated plus maze using peptidic oxytocin and vasopressin receptor ligands in the rat. J Psychopharmacol (Oxf) 26:532-542.
37. Manaenko A, Fathali N, Khatibi NH, Lekic T, Shum KJ, Martin R, Zhang JH, Tang J (2011) Post-treatment with SR49059 improves outcomes following an intracerebral hemorrhagic stroke in mice. In: Intracerebral Hemorrhage Research (Zhang JH, Colohan A, eds), pp191-196. Springer.
38. Manning M, Misicka A, Olma A, Bankowski K, Stoev S, Chini B, Durroux T, Mouillac B, Corbani M, Guillon G (2012) Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol 24:609-628.
39. May MD, Bowen MT, McGregor IS, Timberlake W (2012) Rubbings deposited by cats elicit defensive behavior in rats. Physiol Behav 107:711-718.
40. Meyer-Lindenberg A, Tost H (2012) Neural mechanisms of social risk for psychiatric disorders. Nat Neurosci 15:663-668.
41. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12:524-538.
42. Miller N (1966) Motives for fear-induced affiliation: emotional comparison or interpersonal similarity? J Pers 34:481-503.
43. Neumann ID (2008) Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 20:858-865.
44. Neumann ID (2009) The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood. Front Neuroendocrinol 30:483-496.
45. Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35:649-659.
46. Neumann ID, Maloumby R, Beiderbeck DI, Lukas M, Landgraf R (2013) Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology 38:1985-1993.
47. Norman RMG, Malla AK, Manchanda R, Harricharan R, Takhar J, Northcott S (2005) Social support and three-year symptom and admission outcomes for first episode psychosis. Schizophr Res 80:227-234.
48. Odya EC, Sokoloff G, Alberts JR (2002) The effects of oxytocin on the aggregations of infant rats. Society for Neuroscience Abstracts 878.2.
49. Pedersen CA, Gibson CM, Rau SW, Salimi K, Smedley KL, Casey RL, Leserman J, Jarskog LF, Penn DL (2011) Intranasal oxytocin reduces psychotic symptoms and improves Theory of Mind and social perception in schizophrenia. Schizophr Res 132:50-53.
50. Ramos L, Hicks C, Kevin R, Caminer A, Narlawar R, Kassiou M, McGregor IS (2013) Acute prosocial effects of oxytocin and vasopressin when given alone or in combination with 3,4-Methylenedioxymethamphetamine in rats: involvement of the V1A receptor. Neuropsychopharmacology 38:2249-2259.
51. Sala M, Braida D, Lentini D, Busnelli M, Bulgheroni E, Capurro V, Finardi A, Donzelli A, Pattini L, Rubino T, Parolaro D, Nishimori K, Parenti M, Chini B (2011) Pharmacologic rescue of impaired cognitive flexibility, social deficits, increased aggression, and seizure susceptibility in oxytocin receptor null mice: a neurobehavioral model of autism. Biol Psychiatry 69:875-882.
52. Seppälä O, Karvonen A, Valtonen ET (2008) Shoaling behaviour of fish under parasitism and predation risk. Anim Behav 75:145-150.
53. Sergi M, Green M, Widmark C, Reist C, Erhart S, Braff D, Kee K, Marder S, Mintz J (2007) Social cognition and neurocognition: effects of risperidone, olanzapine, and haloperidol. Am J Psychiatry 164:1585-1592.
54. Serradeil-Le Gal C, Wagnon J, Garcia C, Lacour C, Guiraudou P, Christophe B, Villanova G, Nisato D, Maffrand J, Le Fur G (1993) Biochemical and pharmacological properties of SR 49059, a new, potent, nonpeptide antagonist of rat and human vasopressin V1a receptors. J Clin Invest 92:224.
55. Siviy SM (2008) Effects of pre-pubertal social experiences on the responsiveness of juvenile rats to predator odors. Neurosci Biobehav Rev 32:1249-1258.
56. Siviy SM (2010) Play and adversity: how the playful mammalian brain withstands threats and anxieties. Am J Play 2:297-314.
57. Slattery DA, Neumann ID (2008) No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 586:377-385.
58. Thibonnier M, Auzan C, Madhun Z, Wilkins P, Berti-Mattera L, Clauser E (1994) Molecular cloning, sequencing, and functional expression of a cDNA encoding the human V1a vasopressin receptor. J Biol Chem 269:3304-3310.
59. Tribollet E, Barberis C, Jard S, Dubois-Dauphin M, Dreifuss J (1988) Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography. Brain Res 442:105-118.
60. Tsukada J, Tahara A, Tomura Y, Kusayama T, Wada K-i, Ishii N, Taniguchi N, Suzuki T, Yatsu T, Uchida W, Shibasaki M (2005) Pharmacologic properties of YM218, a novel, potent, nonpeptide vasopressin V1A receptor-selective antagonist. Vascul Pharmacol 42:47-55.
61. Wersinger SR, Caldwell HK, Martinez L, Gold P, Hu SB, Young WS (2007) Vasopressin 1a receptor knockout mice have a subtle olfactory deficit but normal aggression. Genes Brain Behav 6:540-551.
62. Witt DM, Winslow JT, Insel TR (1992) Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol Biochem Behav 43:855-861.
63. Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048-1054.
64. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR (1999) Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400:766-768.