Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context

Frontiers in Behavioral Neuroscience

Volumn 8, Issue JUNE, 2014, Pages

  Bredewold, Remco ^a   Smith, Caroline J W ^a   Dumais, Kelly M ^a   Veenema, Alexa H ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

Female; Juvenile; Lateral septum; Male; Oxytocin receptor; Play fighting; Sex difference; V1a receptor

Indexed keywords

OXYTOCIN; OXYTOCIN RECEPTOR; VASOPRESSIN; VASOPRESSIN V1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; FEMALE; FIGHTING; HORMONAL REGULATION; HORMONE RESPONSE; JUVENILE ANIMAL; LATERAL SEPTUM; MALE; NONHUMAN; PLAY; RAT; SEPTUM PELLUCIDUM; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; SOCIAL PLAY;

EID: 84902594527     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00216     Document Type: Article

References (83)

1. Alessandri, S. M. (1992). Attention, play, and social behavior in ADHD preschoolers. J. Abnorm. Child Psychol. 20, 289-302. doi: 10.1007/BF00916693
2. Bales, K. L., Perkeybile, A. M., Conley, O. G., Lee, M. H., Guoynes, C. D., Downing, G. M., et al. (2013). Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles. Biol. Psychiatry 74, 180-188. doi: 10.1016/j.biopsych.2012.08.025
3. Bales, K. L., Pfeifer, L. A., and Carter, C. S. (2004). Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles. Dev. Psychobiol. 44, 123-131. doi: 10.1002/dev.10165
4. Bartz, J. A., Zaki, J., Bolger, N., and Ochsner, K. N. (2011). Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 15, 301-309. doi: 10.1016/j.tics.2011.05.002
5. Bartz, J. A., Zaki, J., Ochsner, K. N., Bolger, N., Kolevzon, A., Ludwig, N., et al. (2010). Effects of oxytocin on recollections of maternal care and closeness. Proc. Natl. Acad. Sci. U.S.A. 107, 21371-21375. doi: 10.1073/pnas.1012669107
6. Beery, A. K., Lacey, E. A., and Francis, D. D. (2008). Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J. Comp. Neurol. 507, 1847-1859. doi: 10.1002/cne.21638
7. Beery, A. K., and Zucker, I. (2010). Oxytocin and same-sex social behavior in female meadow voles. Neuroscience 169, 665-673. doi: 10.1016/j.neuroscience.2010.05.023
8. Beiderbeck, D. I., Neumann, I. D., and Veenema, A. H. (2007). Differences in intermale aggression are accompanied by opposite vasopressin release patterns within the septum in rats bred for low and high anxiety. Eur. J. Neurosci. 26, 3597-3605. doi: 10.1111/j.1460-9568.2007.05974.x
9. Bekoff, M., and Byers, J. A. (1998). Animal Play: Evolutionary, Comparative, and Ecological Perspectives. Cambridge: Cambridge University Press.
10. Blume, A., Bosch, O. J., Miklos, S., Torner, L., Wales, L., Waldherr, M., et al. (2008). Oxytocin reduces anxiety via ERK1/2 activation: local effect within the rat hypothalamic paraventricular nucleus. Eur. J. Neurosci. 27, 1947-1956. doi: 10.1111/j.1460-9568.2008.06184.x
11. Bluthé, R. M., and Dantzer, R. (1990). Social recognition does not involve vaso-pressinergic neurotransmission in female rats. Brain Res. 535, 301-304. doi: 10.1016/0006-8993(90)91613-L
12. Burghardt, G. M. (2005). The Genesis of Animal Play: Testing the Limits. Cambridge, MA: MIT Press.
13. Carter, C. S. (2007). Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav. Brain Res. 176, 170-186. doi: 10.1016/j.bbr.2006.08.025
14. Chini, B., and Manning, M. (2007). Agonist selectivity in the oxytocin/vasopressin receptor family: new insights and challenges. Biochem. Soc. Trans. 35, 737-741. doi: 10.1042/BST0350737
15. Cho, M. M., DeVries, A. C., Williams, J. R., and Carter, C. S. (1999). The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 113, 1071-1079. doi: 10.1037/0735-7044.113.5.1071
16. Cordoni, G., and Palagi, E. (2011). Ontogenetic trajectories of chimpanzee social play: similarities with humans. PLoS ONE 6:e27344. doi: 10.1371/journal.pone.0027344
17. Declerck, C. H., Boone, C., and Kiyonari, T. (2010). Oxytocin and cooperation under conditions of uncertainty: the modulating role of incentives and social information. Horm. Behav. 57, 368-374. doi: 10.1016/j.yhbeh.2010.01.006
18. De Vries, G. J., Buijs, R. M., and Swaab, D. F. (1981). Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain-presence of a sex difference in the lateral septum. Brain Res. 218, 67-78. doi: 10.1016/0006-8993(81)90989-6
19. De Vries, G. J., and Panzica, G. C. (2006). Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138, 947-955. doi: 10.1016/j.neuroscience.2005.07.050
20. Domes, G., Heinrichs, M., Glascher, J., Buchel, C., Braus, D. F., and Herpertz, S. C. (2007). Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol. Psychiatry 62, 1187-1190. doi: 10.1016/j.biopsych.2007.03.025
21. Domes, G., Lischke, A., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., et al. (2010). Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35, 83-93. doi: 10.1016/j.psyneuen.2009.06.016
22. Donaldson, Z. R., and Young, L. J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904. doi: 10.1126/science.1158668
23. Dumais, K. M., Alonso, A. G., Mayer, T. E., Bredewold, R., and Veenema, A. H. (2013b). Sex differences in oxytocin receptor binding in the bed nucleus of the stria terminalis and amygdala: Implications for differential expression and regulation of social behavior. Soc. Neurosci. Abstr. 378.02/III42.
24. Dumais, K. M., Bredewold, R., Mayer, T. E., and Veenema, A. H. (2013a). Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region-and sex-specific ways. Horm. Behav. 64, 693-701. doi: 10.1016/j.yhbeh.2013.08.012
25. Engelmann, M., Ebner, K., Wotjak, C. T., and Landgraf, R. (1998). Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav. Brain Res. 90, 89-94. doi: 10.1016/S0166-4328(97)00084-3
26. Feldman, R. (2012). Oxytocin and social affiliation in humans. Horm. Behav. 61, 380-391. doi: 10.1016/j.yhbeh.2012.01.008
27. Feldman, R., Weller, A., Zagoory-Sharon, O., and Levine, A. (2007). Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol. Sci. 18, 965-970. doi: 10.1111/j.1467-9280.2007.02010.x
28. Ferris, C. F., and Potegal, M. (1988). Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol. Behav. 44, 235-239. doi: 10.1016/0031-9384(88)90144-8
29. Goodson, J. L., Kabelik, D., and Schrock, S. E. (2009). Dynamic neuromodulation of aggression by vasotocin: influence of social context and social phenotype in territorial songbirds. Biol. Lett. 5, 554-556. doi: 10.1098/rsbl. 2009.0316
30. Goodson, J. L., and Thompson, R. R. (2010). Nonapeptide mechanisms of social cognition, behavior and species-specific social systems. Curr. Opin. Neurobiol. 20, 784-794. doi: 10.1016/j.conb.2010.08.020
31. Grillon, C., Krimsky, M., Charney, D. R., Vytal, K., Ernst, M., and Cornwell, B. (2013). Oxytocin increases anxiety to unpredictable threat. Mol. Psychiatry, 18, 958-960. doi: 10.1038/mp.2012.156
32. Guralnick, M. J., Connor, R. T., Neville, B., and Hammond, M. A. (2006). Promoting the peer-related social development of young children with mild developmental delays: effectiveness of a comprehensive intervention. Am. J. Ment. Retard. 111, 336-356. doi: 10.1352/0895-8017(2006)111[336:PTPSDO]2.0.CO;2
33. Gutzler, S. J., Karom, M., Erwin, W. D., and Albers, H. E. (2010). Arginine-vasopressin and the regulation of aggression in female Syrian hamsters (Mesocricetus auratus). Eur. J. Neurosci. 31, 1655-1663. doi: 10.1111/j.14609568.2010.07190.x
34. Guzman, Y. F., Tronson, N. C., Jovasevic, V., Sato, K., Guedea, A. L., Mizukami, H., et al. (2013). Fear-enhancing effects of septal oxytocin receptors. Nat. Neurosci. 16, 1185-1187. doi: 10.1038/nn.3465
35. Harmon, A. C., Moore, T. O., Huhman, K. L., and Albers, H. E. (2002). Social experience and social context alter the behavioral response to centrally administered oxytocin in female Syrian hamsters. Neuroscience 109, 767-772. doi: 10.1016/S0306-4522(01)00523-1
36. Insel, T. R., and Hulihan, T. J. (1995). A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav. Neurosci. 109, 782-789. doi: 10.1037/0735-7044.109.4.782
37. Jordan, R. (2003). Social play and autistic spectrum disorders: a perspective on theory, implications and educational approaches. Autism 7, 347-360. doi: 10.1177/1362361303007004002
38. Kingsbury, M. A., Miller, K. M., and Goodson, J. L. (2013). VPAC receptor signaling modulates grouping behavior and social responses to contextual novelty in a gregarious finch: a role for a putative prefrontal cortex homologue. Horm. Behav. 64, 511-518. doi: 10.1016/j.yhbeh.2013.07.004
39. Kojima, S., and Alberts, J. R. (2011). Oxytocin mediates the acquisition of filial, odor-guided huddling for maternally-associated odor in preweanling rats. Horm. Behav. 60, 549-558. doi: 10.1016/j.yhbeh.2011.08.003
40. Landgraf, R., Gerstberger, R., Montkowski, A., Probst, J. C., Wotjak, C. T., Holsboer, F., et al. (1995). V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J. Neurosci. 15, 4250-4258.
41. Lischke, A., Gamer, M., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., et al. (2012). Oxytocin increases amygdala reactivity to threatening scenes in females. Psychoneuroendocrinology 37, 1431-1438. doi: 10.1016/j.psyneuen.2012.01.011
42. Lukas, M., Bredewold, R., Landgraf, R., Neumann, I. D., and Veenema, A. H. (2011). Early life stress impairs social recognition due to a blunted response of vasopressin release within the septum of adult male rats. Psychoneuroendocrinology 36, 843-853. doi: 10.1016/j.psyneuen.2010.11.007
43. Lukas, M., Bredewold, R., Neumann, I. D., and Veenema, A. H. (2010). Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 58, 78-87. doi: 10.1016/j.neuropharm.2009.06.020
44. Lukas, M., Toth, I., Veenema, A. H., and Neumann, I. D. (2013). Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 38, 916-926. doi: 10.1016/j.psyneuen.2012.09.018
45. Luo, A. H., Tahsili-Fahadan, P., Wise, R. A., Lupica, C. R., and Aston-Jones, G. (2011). Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333, 353-357. doi: 10.1126/science.1204622
46. MacDonald, K. S. (2013). Sex, receptors, and attachment: a review of individual factors influencing response to oxytocin. Front. Neurosci. 6:194. doi: 10.3389/fnins.2012.00194
47. MacDonald, K., MacDonald, T. M., Brüne, M., Lamb, K., Wilson, M. P., Golshan, S., et al. (2013). Oxytocin and psychotherapy: a pilot study of its physiological, behavioral and subjective effects in males with depression. Psychoneuroendocrinology 38, 2831-2843. doi: 10.1016/j.psyneuen.2013.05.014
48. Manning, M., Stoev, S., Chini, B., Durroux, T., Mouillac, B., and Guillon, G. (2008). Peptide and non-peptide agonists and antagonists for the vasopressin and oxytocin V1a, V1b, V2 and OT receptors: research tools and potential therapeutic agents. Prog. Brain Res. 170, 473-512. doi: 10.1016/S0079-6123(08) 00437-8
49. Meyer-Lindenberg, A., Domes, G., Kirsch, P., and Heinrichs, M. (2011). Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 12, 524-538. doi: 10.1038/nrn3044
50. Modi, M. E., and Young, L. J. (2012). The oxytocin system in drug discovery for autism: animal models and novel therapeutic strategies. Horm. Behav. 61, 340-350. doi: 10.1016/j.yhbeh.2011.12.010
51. Moller, P., and Husby, R. (2000). The initial prodrome in schizophrenia: searching for naturalistic core dimensions of experience and behavior. Schizophr. Bull. 26, 217-232. doi: 10.1093/oxfordjournals.schbul.a033442
52. Olazábal, D. E., and Young, L. J. (2006). Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm. Behav. 49, 681-687. doi: 10.1016/j.yhbeh.2005.12.010
53. Olff, M., Frijling, J. L., Kubzansky, L. D., Bradley, B., Ellenbogen, M. A., Cardoso, C., et al. (2013). The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38, 1883-1894. doi: 10.1016/j.psyneuen.2013.06.019
54. Panksepp, J. (1981). The ontogeny of play in rats. Dev. Psychobiol. 14, 327-332. doi: 10.1002/dev.420140405
55. Panksepp, J., and Beatty, W. W. (1980). Social deprivation and play in rats. Behav. Neural Biol. 30, 197-206. doi: 10.1016/S0163-1047(80)91077-8
56. Paul, M. J., Terranova, J. I., Probst, C. K., Murray, E. K., Ismail, N. I., and de Vries, G. J. (2014). Sexually dimorphic role for vasopressin in the development of social play. Front. Behav. Neurosci. 8:58. doi: 10.3389/fnbeh.2014.00058
57. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
58. Pellis, S. M., and Iwaniuk, A. N. (2000). Comparative analyses of the role of postnatal development on the expression of play fighting. Dev. Psychobiol. 36, 136-147. doi: 10.1002/(SICI)1098-2302(200003)36:2%3C136::AID-DEV5% 3E3.3.CO;2-M
59. Pellow, S., Chopin, P., File, S. E., and Briley, M. (1985). Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149-167. doi: 10.1016/0165-0270(85)90031-7
60. Rilling, J. K., Demarco, A. C., Hackett, P. D., Chen, X., Gautam, P., Stair, S., et al. (2014). Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction. Psychoneuroendocrinology 39, 237-248. doi: 10.1016/j.psyneuen.2013.09.022
61. Rilling, J. K., DeMarco, A. C., Hackett, P. D., Thompson, R., Ditzen, B., Patel, R., et al. (2012). Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology 37, 447-461. doi: 10.1016/j.psyneuen.2011.07.013
62. Ring, R. H., Malberg, J. E., Potestio, L., Ping, J., Boikess, S., Luo, B., et al. (2006). Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology 185, 218-225. doi: 10.1007/s00213-005-0293-z
63. Rutter, M., Caspi, A., and Moffitt, T. E. (2003). Using sex differences in psychopathology to study causal mechanisms: unifying issues and research strategies. J. Child. Psychol. Psychiatry 44, 1092-1115. doi: 10.1111/1469-7610. 00194
64. Sartor, G. C., and Aston-Jones, G. S. (2012). A septal-hypothalamic pathway drives orexin neurons, which is necessary for conditioned cocaine preference. J. Neurosci. 32, 4623-4631. doi: 10.1523/JNEUROSCI.4561-11.2012
65. Schorscher-Petcu, A., Sotocinal, S., Ciura, S., Dupré, A., Ritchie, J., Sorge, R. E., et al. (2010). Oxytocin-induced analgesia and scratching are mediated by the vasopressin-1A receptor in the mouse. J. Neurosci. 30, 8274-8284. doi: 10.1523/JNEUROSCI.1594-10.2010
66. Sheehan, T. P., Chambers, R. A., and Russell, D. S. (2004). Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res. Rev. 46, 71-117. doi: 10.1016/j.brainresrev.2004.04.009
67. Sigman, M., and Ruskin, E. (1999). Continuity and change in the social competence of children with autism, Down syndrome, and developmental delays. Monogr. Soc. Res. Child. Dev. 64, 1-114. doi: 10.1111/1540-5834.00002
68. Siviy, S. M., and Panksepp, J. (2011). In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci. Biobehav. Rev. 35, 1821-1830. doi: 10.1016/j.neubiorev.2011.03.006
69. Striepens, N., Scheele, D., Kendrick, K. M., Becker, B., Schäfer, L., Schwalba, K., et al. (2012). Oxytocin facilitates protective responses to aversive social stimuli in males. Proc. Natl. Acad. Sci. U.S.A. 109, 18144-18149. doi: 10.1073/pnas.1208852109
70. Szot, P., and Dorsa, D. M. (1993). Differential timing and sexual dimorphism in the expression of the vasopressin gene in the developing rat brain. Dev. Brain Res. 73, 177-183. doi: 10.1016/0165-3806(93)90136-X
71. Taylor, P. V., Veenema, A. H., Paul, M. J., Bredewold, R., Isaacs, S., and de Vries, G. J. (2012). Sexually dimorphic effects of a prenatal immune challenge on social play and vasopressin expression in juvenile rats. Biol. Sex Differ. 3:15. doi: 10.1186/2042-6410-3-15
72. Thompson, R. R., George, K., Walton, J. C., Orr, S. P., and Benson, J. (2006). Sex-specific influences of vasopressin on human social communication. Proc. Natl. Acad. Sci. U.S.A. 103, 7889-7894. doi: 10.1073/pnas.0600406103
73. Thor, D. H., and Holloway, W. R. Jr. (1986). Social play soliciting by male and female juvenile rats: effects of neonatal androgenization and sex of cagemates. Behav. Neurosci. 100, 275-279. doi: 10.1037/0735-7044.100.2.275
74. Trezza, V., Baarendse, P. J., and Vanderschuren, L. J. (2010). The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol. Sci. 31, 463-469. doi: 10.1016/j.tips.2010.06.008
75. Vanderschuren, L. J., Niesink, R. J., and Van Ree, J. M. (1997). The neurobiology of social play behavior in rats. Neurosci. Biobehav. Rev. 21, 309-326. doi: 10.1016/S0149-7634(96)00020-6
76. Van Leeuwen, F. W., Caffe, A. R., and De Vries, G. J. (1985). Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens. Brain Res. 325, 391-394. doi: 10.1016/0006-8993(85)90348-8
77. Veenema, A. H., Beiderbeck, D. I., Lukas, M., and Neumann, I. D. (2010). Distinct correlations of vasopressin release within the lateral septum and the bed nucleus of the stria terminalis with the display of intermale aggression. Horm. Behav. 58, 273-281. doi: 10.1016/j.yhbeh.2010.03.006
78. Veenema, A. H., Bredewold, R., and De Vries, G. J. (2012). Vasopressin regulates social recognition in juvenile and adult rats of both sexes, but in sex-and age-specific ways. Horm. Behav. 61, 50-56. doi: 10.1016/j.yhbeh.2011.10.002
79. Veenema, A. H., Bredewold, R., and De Vries, G. J. (2013). Sex-specific modulation of juvenile social play by vasopressin. Psychoneuroendocrinology 38, 2554-2561. doi: 10.1016/j.psyneuen.2013.06.002
80. Veenema, A. H., and Neumann, I. D. (2008). Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog. Brain Res. 170, 261-276. doi: 10.1016/S0079-6123(08)00422-6
81. Veenema, A. H., and Neumann, I. D. (2009). Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34, 463-467. doi: 10.1016/j.psyneuen.2008.10.017
82. Williams, J. R., Carter, C. S., and Insel, T. (1992). Partner preference development in female prairie voles is facilitated by mating or the central infusion of oxytocin. Ann. N.Y. Acad. Sci. 652, 487-489. doi: 10.1111/j.1749-6632.1992.tb34393.x
83. Windle, R. J., Shanks, N., Lightman, S. L., and Ingram, C. D. (1997). Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 138, 2829-2834. doi: 10.1210/en.138.7.2829