Oxytocin microinjected into the central amygdaloid nuclei exerts anti-aggressive effects in male rats

Neuropharmacology

Volumn 90, Issue , 2015, Pages 74-81

  Calcagnoli, Federica ^a   Stubbendorff, Christine ^b   Meyer, Neele ^c   De Boer, Sietse F ^a   Althaus, Monika ^d   Koolhaas, Jaap M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Central amygdala; Dorsal raphe; Intermale offensive behavior; Oxytocin; Social exploration

Indexed keywords

L 368899; OXYTOCIN; OXYTOCIN ANTAGONIST; OXYTOCIN RECEPTOR; SEROTONIN 1A AGONIST; UNCLASSIFIED DRUG; BORNANE DERIVATIVE; CENTRAL NERVOUS SYSTEM AGENTS; PIPERAZINE DERIVATIVE;

ADULT; AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CONNECTOME; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; EXPLORATORY BEHAVIOR; FEMALE; MALE; MICROINJECTION; NONHUMAN; RAT; SOCIAL BEHAVIOR; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; INDWELLING CATHETER; METABOLISM; PHYSIOLOGY; RANDOMIZATION;

AGGRESSION; ANIMALS; BORNANES; CATHETERS, INDWELLING; CENTRAL AMYGDALOID NUCLEUS; CENTRAL NERVOUS SYSTEM AGENTS; DORSAL RAPHE NUCLEUS; MALE; MICROINJECTIONS; OXYTOCIN; PIPERAZINES; RANDOM ALLOCATION; RATS; RECEPTORS, OXYTOCIN;

EID: 84917706077     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.11.012     Document Type: Article

References (77)

1. Amat, J., Baratta, M.V., Paul, E., Bland, S.T., Watkins, L.R., Maier, S.F., 2005. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat. Neurosci. 8, 365-371.
2. Arango, V., Underwood, M.D., Mann, J.J., 2002. Serotonin brain circuits involved in major depression and suicide. Prog. Brain Res. 136, 443-453.
3. Bannai, M., Fish, E.W., Faccidomo, S., Miczek, K.A., 2007. Anti-aggressive effects of agonists at 5-HT1B receptors in the dorsal raphe nucleus of mice. Psychopharmacology 193, 295-304.
4. Barberis, C., Audigier, S., Durroux, T., Elands, J., Schmidt, A., Jard, S., 1992. Pharmacology of oxytocin and vasopressin receptors in the central and peripheral nervous system. Ann. N. Y. Acad. Sci. 652, 39-45.
5. Barberis, C., Tribollet, E., 1996. Vasopressin and oxytocin receptors in the central nervous system. Crit. Rev. Neurobiol. 10, 119-154.
6. Baskerville, T.A., Douglas, A.J., 2008. Interactions between dopamine and oxytocin in the control of sexual behaviour. Prog. Brain Res. 170, 277-290.
7. Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., Fehr, E., 2008. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58, 639-650.
8. Bertsch, K., Gamer, M., Schmidt, B., Schmidinger, I., Walther, S., Kastel, T., Schnell, K., Buchel, C., Domes, G., Herpertz, S.C., 2013. Oxytocin and reduction of social threat hypersensitivity in women with borderline personality disorder. Am. J. Psychiatry 170, 1169-1177.
9. Bosch, O.J., Meddle, S.L., Beiderbeck, D.I., Douglas, A.J., Neumann, I.D., 2005. Brain oxytocin correlates with maternal aggression: link to anxiety. J. Neurosci. 25, 6807-6815.
10. Bosch, O.J., Sartori, S.B., Singewald, N., Neumann, I.D., 2007. Extracellular amino acid levels in the paraventricular nucleus and the central amygdala in high- and low-anxiety dams rats during maternal aggression: regulation by oxytocin. Stress 10, 261-270.
11. Calcagnoli, F., de Boer, S.F., Althaus, M., den Boer, J.A., Koolhaas, J.M., 2013. Anti-aggressive activity of central oxytocin in male rats. Psychopharmacology 229, 639-651.
12. Calcagnoli, F., Kreutzmann, J.C., de Boer, S.F., Althaus, M., Koolhaas, J.M., 2014a. Acute and repeated intranasal oxytocin administration exerts anti-aggressive and pro-affiliative effects in male rats. Psychoneuroendocrinology 51, 112-121.
13. Calcagnoli, F., Meyer, N., de Boer, S.F., Althaus, M., Koolhaas, J.M., 2014b. Chronic enhancement of brain oxytocin levels causes enduring anti-aggressive and prosocial explorative behavioral effects in male rats. Horm. Behav. 65, 427-433.
14. Chiavegatto, S., Nelson, R.J., 2003. Interaction of nitric oxide and serotonin in aggressive behavior. Hormones Behav. 44, 233-241.
15. Choleris, E., Clipperton-Allen, A.E., Phan, A., Kavaliers, M., 2009. Neuroendocrinology of social information processing in rats and mice. Front. Neuroendocrinol. 30, 442-459.
16. Coccaro, E.F., McCloskey, M.S., Fitzgerald, D.A., Phan, K.L., 2007. Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol. Psychiatry 62, 168-178.
17. Consiglio, A.R., Borsoi, A., Pereira, G.A.M., Lucion, A.B., 2005. Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol. Behav. 85, 354-362.
18. de Almeida, R.M., Ferrari, P.F., Parmigiani, S., Miczek, K.A., 2005. Escalated aggressive behavior: dopamine, serotonin and GABA. Eur. J. Pharmacol. 526, 51-64.
19. de Almeida, R.M., Rowlett, J.K., Cook, J.M., Yin, W., Miczek, K.A., 2004. GABAA/alpha1 receptor agonists and antagonists: effects on species-typical and heightened aggressive behavior after alcohol self-administration in mice. Psychopharmacology 172, 255-263.
20. de Boer, S.F., Caramaschi, D., Natarajan, D., Koolhaas, J.M., 2009. The vicious cycle towards violence: focus on the negative feedback mechanisms of brain serotonin neurotransmission. Front. Behav. Neurosci. 3, 1-6.
21. de Boer, S.F., Koolhaas, J.M., 2005. 5-HT1A and 5-HT1B receptor agonists and aggression: a pharmacological challenge of the serotonin deficiency hypothesis. Eur. J. Pharmacol. 526, 125-139.
22. de Boer, S.F., van der Vegt, B.J., Koolhaas, J.M., 2003. Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav. Genet. 33, 485-501.
23. Devarajan, K., Marchant, E.G., Rusak, B., 2005. Circadian and light regulation of oxytocin and parvalbumin protein levels in the ciliated ependymal layer of the third ventricle in the C57 mouse. Neuroscience 134, 539-547.
24. Dolen, G., Darvishzadeh, A., Huang, K.W., Malenka, R.C., 2013. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501, 179-184.
25. Domes, G., Lischke, A., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., Herpertz, S.C., 2010. Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35, 83-93.
26. Donegan, N.H., Sanislow, C.A., Blumberg, H.P., Fulbright, R.K., Lacadie, C., Skudlarski, P., Gore, J.C., Olson, I.R., McGlashan, T.H., Wexler, B.E., 2003. Amygdala hyperreactivity in borderline personality disorder: implications for emotional dysregulation. Biol. Psychiatry 54, 1284-1293.
27. Earley, C.J., Leonard, B.E., 1977. The effect of testosterone and cyproterone acetate on the concentration of gamma-aminobutyric acid in brain areas of aggressive and non-aggressive mice. Pharmacol. Biochem. Behav. 6, 409-413.
28. Ebner, K., Bosch, O.J., Kromer, S.A., Singewald, N., Neumann, I.D., 2005. Release of oxytocin in the rat central amygdala modulates stress-coping behavior and the release of excitatory amino acids. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 30, 223-230.
29. Ferris, C.F., Foote, K.B., Meltser, H.M., Plenby, M.G., Smith, K.L., Insel, T.R., 1992. Oxytocin in the amygdala facilitates maternal aggression. Ann. N. Y. Acad. Sci. 652, 456-457.
30. Freund-Mercier, M.J., Stoeckel, M.E., Palacios, J.M., Pazos, A., Reichhart, J.M., Porte, A., Richard, P., 1987. Pharmacological characteristics and anatomical distribution of [3H]oxytocin-binding sites in the Wistar rat brain studied by autoradiography. Neuroscience 20, 599-614.
31. Gamer, M., Zurowski, B., Buchel, C., 2010. Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc. Natl. Acad. Sci. U. S. A. 107, 9400-9405.
32. Goodson, J.L., 2005. The vertebrate social behavior network: evolutionary themes and variations. Horm. Behav. 48, 11-22.
33. Gould, B.R., Zingg, H.H., 2003. Mapping oxytocin receptor gene expression in the mouse brain and mammary gland using an oxytocin receptor-LacZ reporter mouse. Neuroscience 122, 155-167.
34. Haller, J., Toth, M., Halasz, J., De Boer, S.F., 2006. Patterns of violent aggression-induced brain c-fos expression in male mice selected for aggressiveness. Physiol. Behav. 88, 173-182.
35. Hammock, E.A., Young, L.J., 2006. Oxytocin, vasopressin and pair bonding: implications for autism. Phil. Trans. R. Soc. Lond. Ser. B Biol. Sci. 361, 2187-2198.
36. Heinrichs, M., Domes, G., 2008. Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans. Prog. Brain Res. 170, 337-350.
37. Heinrichs, M., von Dawans, B., Domes, G., 2009. Oxytocin, vasopressin, and human social behavior. Front. Neuroendocrinol. 30, 548-557.
38. Herpertz, S.C., Dietrich, T.M., Wenning, B., Krings, T., Erberich, S.G., Willmes, K., Thron, A., Sass, H., 2001. Evidence of abnormal amygdala functioning in borderline personality disorder: a functional MRI study. Biol. Psychiatry 50, 292-298.
39. Huber, D., Veinante, P., Stoop, R., 2005. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308, 245-248.
40. Insel, T.R., Young, L.J., 2001. The neurobiology of attachment. Nat. Rev. Neurosci. 2, 129-136.
41. Jacobs, B.L., Azmitia, E.C., 1992. Structure and function of the brain serotonin system. Physiol. Rev. 72, 165-229.
42. Jones, P.M., Robinson, I.C., 1982. Differential clearance of neurophysin and neurohypophysial peptides from the cerebrospinal fluid in conscious guinea pigs. Neuroendocrinology 34, 297-302.
43. Kirsch, P., Esslinger, C., Chen, Q., Mier, D., Lis, S., Siddhanti, S., Gruppe, H., Mattay, V.S., Gallhofer, B., Meyer-Lindenberg, A., 2005. Oxytocin modulates neural circuitry for social cognition and fear in humans. J. Neurosci. 25, 11489-11493.
44. Knobloch, S.H., Charlet, A., Hoffmann, Lena C., Eliava, M., Khrulev, S., Cetin, Ali H., Osten, P., Schwarz, Martin K., Seeburg, Peter H., Stoop, R., Grinevich, V., 2012. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73, 553-566.
45. Koolhaas, J.M., Coppens, C.M., de Boer, S.F., Buwalda, B., Meerlo, P., Timmermans, P.J., 2013. The resident-intruder paradigm: a standardized test for aggression, violence and social stress. J. Vis. Exp. 4, 4367.
46. Koolhaas, J.M., Schuurman, T., Wiepkema, P.R., 1980. The organization of intraspecific agonistic behaviour in the rat. Prog. Neurobiol. 15, 247-268.
47. Kosfeld, M., Heinrichs, M., Zak, P.J., Fischbacher, U., Fehr, E., 2005. Oxytocin increases trust in humans. Nature 435, 673-676.
48. LeDoux, J.E., Iwata, J., Cicchetti, P., Reis, D.J., 1988. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci. Off. J. Soc. Neurosci. 8, 2517-2529.
49. Lee, P.R., Brady, D.L., Shapiro, R.A., Dorsa, D.M., Koenig, J.I., 2005. Social interaction deficits caused by chronic phencyclidine administration are reversed by oxytocin. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 30, 1883-1894.
50. Lischke, A., Gamer, M., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., Herpertz, S.C., Domes, G., 2012. Oxytocin increases amygdala reactivity to threatening scenes in females. Psychoneuroendocrinology 37, 1431-1438.
51. Liu, Y., Wang, Z.X., 2003. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121, 537-544.
52. Lubin, D.A., Elliott, J.C., Black, M.C., Johns, J.M., 2003. An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav. Neurosci. 117, 195-201.
53. Lukas, M., Toth, I., Reber, S.O., Slattery, D.A., Veenema, A.H., Neumann, I.D., 2011. The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 36, 2159-2168.
54. Melis, M.R., Succu, S., Sanna, F., Boi, A., Argiolas, A., 2009. Oxytocin injected into the ventral subiculum or the posteromedial cortical nucleus of the amygdala induces penile erection and increases extracellular dopamine levels in the nucleus accumbens of male rats. Eur. J. Neurosci. 30, 1349-1357.
55. Mens, W.B., Witter, A., van Wimersma Greidanus, T.B., 1983. Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): halftimes of disappearance of these neuropeptides from CSF. Brain Res. 262, 143-149.
56. Miczek, K.A., Fish, E.W., De Bold, J.F., De Almeida, R.M., 2002. Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and gamma-aminobutyric acid systems. Psychopharmacology 163, 434-458.
57. Millan, M.J., Rivet, J.-M., Canton, H., Lejeune, F.O., Gobert, A., Widdowson, P., Bervoets, K., Brocco, M., Peglion, J.-L., 1993. S 15535: a highly selective benzodioxopiperazine 5-HT1A receptor ligand which acts as an agonist and an antagonist at presynaptic and postsynaptic sites respectively. Eur. J. Pharmacol. 230, 99-102.
58. Nakamura, K., Matsumoto, M., Hikosaka, O., 2008. Reward-dependent modulation of neuronal activity in the primate dorsal raphe nucleus. J. Neurosci. Off. J. Soc. Neurosci. 28, 5331-5343.
59. Neumann, I.D., 2008. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J. Neuroendocrinol. 20, 858-865.
60. Olivier, B., Mos, J., van Oorschot, R., Hen, R., 1995. Serotonin receptors and animal models of aggressive behavior. Pharmacopsychiatry 28, 80-90.
61. Pan, Y., Xu, L., Young, K.A., Wang, Z., Zhang, Z., 2010. Agonistic encounters and brain activation in dominant and subordinate male greater long-tailed hamsters. Horm. Behav. 58, 478-484.
62. Resstel, L.B., Joca, S.R., Guimaraes, F.G., Correa, F.M., 2006. Involvement of medial prefrontal cortex neurons in behavioral and cardiovascular responses to contextual fear conditioning. Neuroscience 143, 377-385.
63. Robinson, I.C., Jones, P.M., 1982. Oxytocin and neurophysin in plasma and CSF during suckling in the guinea-pig. Neuroendocrinology 34, 59-63.
64. Sauer, C., Montag, C., Reuter, M., Kirsch, P., 2013. Imaging oxytocin x dopamine interactions: an epistasis effect of CD38 and COMT gene variants influences the impact of oxytocin on amygdala activation to social stimuli. Front. Neurosci. 7.
65. Seo, D., Patrick, C.J., Kennealy, P.J., 2008. Role of serotonin and dopamine system interactions in the neurobiology of impulsive aggression and its comorbidity with other clinical disorders. Aggress. Violent Behav. 13, 383-395.
66. Sofroniew, M.V., Cross, B.A., Leng, G., 1983. Morphology of Vasopressin and Oxytocin Neurones and Their Central and Vascular Projections, Progress in Brain Research. Elsevier, pp. 101-114.
67. Spaethling, J.M., Piel, D., Dueck, H., Buckley, P.T., Morris, J.F., Fisher, S.A., Lee, J., Sul, J.Y., Kim, J., Bartfai, T., Beck, S.G., Eberwine, J.H., 2014. Serotonergic neuron regulation informed by in vivo single-cell transcriptomics. Faseb J. 28, 771-780.
68. Stockmeier, C.A., 1997. Neurobiology of serotonin in depression and Suicidea. Ann. N. Y. Acad. Sci. 836, 220-232.
69. Takahashi, A., Miczek, K.A., 2013. Neurogenetics of aggressive behavior: studies in rodents. Curr. Top. Behav. Neurosci. 7.
70. Takahashi, A., Shimamoto, A., Boyson, C.O., DeBold, J.F., Miczek, K.A., 2010. GABA(B) receptor modulation of serotonin neurons in the dorsal raphe nucleus and escalation of aggression in mice. J. Neurosci. Off. J. Soc. Neurosci. 30, 11771-11780.
71. Terenzi, M.G., Ingram, C.D., 2005. Oxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei. Neuroscience 134, 345-354.
72. van der Vegt, B.J., Lieuwes, N., van de Wall, E.H., Kato, K., Moya-Albiol, L., Martinez-Sanchis, S., de Boer, S.F., Koolhaas, J.M., 2003. Activation of serotonergic neurotransmission during the performance of aggressive behavior in rats. Behav. Neurosci. 117, 667-674.
73. Veinante, P., Freund-Mercier, M.-J., 1997. Distribution of oxytocin- and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study. J. Comp. Neurol. 383, 305-325.
74. Viviani, D., Terrettaz, T., Magara, F., Stoop, R., 2010. Oxytocin enhances the inhibitory effects of diazepam in the rat central medial amygdala. Neuropharmacology 58, 62-68.
75. Wacker, D.W., Ludwig, M., 2012. Vasopressin, oxytocin, and social odor recognition. Hormones Behav. 61, 259-265.
76. Winslow, J.T., Shapiro, L., Carter, C.S., Insel, T.R., 1993. Oxytocin and complex social behavior: species comparisons. Psychopharmacol. Bull. 29, 409-414.
77. Yoshida, M., Takayanagi, Y., Inoue, K., Kimura, T., Young, L.J., Onaka, T., Nishimori, K., 2009. Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J. Neurosci. 29, 2259-2271.