Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults

Hormones and Behavior

Volumn 60, Issue 5, 2011, Pages 498-504

  Keebaugh, Alaine C ^a   Young, Larry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alloparenting; Development; Monogamy; Oxytocin receptor; Pair bonding

Indexed keywords

OXYTOCIN; OXYTOCIN RECEPTOR;

ADULT ANIMAL; ALLOPARENTAL BEHAVIOR; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENT; FEMALE; HORMONE ACTION; MALE; MATE CHOICE; NONHUMAN; NUCLEUS ACCUMBENS; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRAL GENE DELIVERY SYSTEM; VOLE;

ANIMALS; ARVICOLINAE; FEMALE; NUCLEUS ACCUMBENS; PAIR BOND; RECEPTORS, OXYTOCIN;

EID: 80555123024     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.07.018     Document Type: Article

References (47)

1. Ahern T.H., Young L.J. The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster). Frontiers in Behavioral Neuroscience 2009, 3:17.
2. Ahern T.H., Modi M.E., Burkett J.P., Young L.J. Evaluation of two automated metrics for analyzing partner preference tests. Journal of Neuroscience Methods 2009, 182:180-188.
3. Ahern T.H., Hammock E.A., Young L.J. Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster). Developmental Psychobiology 2011, 53:118-131.
4. Andari E., Duhamel J.R., Zalla T., Herbrecht E., Leboyer M., Sirigu A. Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:4389-4394.
5. Bales K.L., Carter C.S. Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behavioral Neuroscience 2003, 117:854-859.
6. Bales K.L., Carter C.S. Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Hormones and Behavior 2003, 44:178-184.
7. Bales K.L., Kim A.J., Lewis-Reese A.D., Sue Carter C. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Hormones and Behavior 2004, 45:354-361.
8. Bales K.L., Pfeifer L.A., Carter C.S. Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles. Developmental Psychobiology 2004, 44:123-131.
9. Bales K.L., Plotsky P.M., Young L.J., Lim M.M., Grotte N., Ferrer E., Carter C.S. Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors. Neuroscience 2007, 144:38-45.
10. Carter C.S. Developmental consequences of oxytocin. Physiology & Behavior 2003, 79:383-397.
11. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neuroscience and Biobehavioral Reviews 1995, 19:303-314.
12. Ditzen B., Schaer M., Gabriel B., Bodenmann G., Ehlert U., Heinrichs M. Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biological Psychiatry 2009, 65:728-731.
13. Domes G., Heinrichs M., Michel A., Berger C., Herpertz S.C. Oxytocin improves "mind-reading" in humans. Biological Psychiatry 2007, 61:731-733.
14. Eaton J.L., Roache L., Nguyen K.N., Cushing B.S., Troyer E., Papademetriou E., Raghanti M.A. Organizational effects of oxytocin on serotonin innervation. Developmental Psychobiology 2011, doi:10.1002/dev.20566.
15. Field E.F., Whishaw I.Q., Forgie M.L., Pellis S.M. Neonatal and pubertal, but not adult, ovarian steroids are necessary for the development of female-typical patterns of dodging to protect a food item. Behavioral Neuroscience 2004, 118:1293-1304.
16. Getz L.L., Carter C.S. Prairie-vole partnerships. American Scientist 1996, 84:56-62.
17. Gregory S.G., Connelly J.J., Towers A.J., Johnson J., Biscocho D., Markunas C.A., Lintas C., Abramson R.K., Wright H.H., Ellis P., Langford C.F., Worley G., Delong G.R., Murphy S.K., Cuccaro M.L., Persico A., Pericak-Vance M.A. Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Medicine 2009, 7:62.
18. Guastella A.J., Mitchell P.B., Dadds M.R. Oxytocin increases gaze to the eye region of human faces. Biological Psychiatry 2008, 63:3-5.
19. Guastella A.J., Einfeld S.L., Gray K.M., Rinehart N.J., Tonge B.J., Lambert T.J., Hickie I.B. Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biological Psychiatry 2010, 67:692-694.
20. Hollander E., Bartz J., Chaplin W., Phillips A., Sumner J., Soorya L., Anagnostou E., Wasserman S. Oxytocin increases retention of social cognition in autism. Biological Psychiatry 2007, 61:498-503.
21. Insel T.R., Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:5981-5985.
22. Insel T.R., Shapiro L.E. Oxytocin receptors and maternal behavior. Annals of the New York Academy of Sciences 1992, 652:122-141.
23. Kendrick K.M., Keverne E.B., Baldwin B.A. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 1987, 46:56-61.
24. Kendrick K.M., Da Costa A.P., Broad K.D., Ohkura S., Guevara R., Levy F., Keverne E.B. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Research Bulletin 1997, 44:383-395.
25. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
26. Kramer K.M., Cushing B.S., Carter C.S. Developmental effects of oxytocin on stress response: single versus repeated exposure. Physiology & Behavior 2003, 79:775-782.
27. Kramer K.M., Yoshida S., Papademetriou E., Cushing B.S. The organizational effects of oxytocin on the central expression of estrogen receptor alpha and oxytocin in adulthood. BMC Neuroscience 2007, 8:71.
28. Lipschitz D.L., Crowley W.R., Bealer S.L. Central blockade of oxytocin receptors during late gestation disrupts systemic release of oxytocin during suckling in rats. Journal of Neuroendocrinology 2003, 15:743-748.
29. Lonstein J.S., De Vries G.J. Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster). Physiology & Behavior 1999, 66:33-40.
30. Lonstein J.S., De Vries G.J. Influence of gonadal hormones on the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster). Behavioural Brain Research 2000, 114:79-87.
31. Lonstein J.S., De Vries G.J. Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster). Journal of Comparative Psychology 2001, 115:53-61.
32. Olazabal D.E., Young L.J. Variability in "spontaneous" maternal behavior is associated with anxiety-like behavior and affiliation in naive juvenile and adult female prairie voles (Microtus ochrogaster). Developmental Psychobiology 2005, 47:166-178.
33. Olazabal D.E., Young L.J. Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 2006, 141:559-568.
34. Olazabal D.E., Young L.J. Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Hormones and Behavior 2006, 49:681-687.
35. Pedersen C.A., Prange A.J. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proceedings of the National Academy of Sciences of the United States of America 1979, 76:6661-6665.
36. Perry A.N., Paramadilok A., Cushing B.S. Neonatal oxytocin alters subsequent estrogen receptor alpha protein expression and estrogen sensitivity in the female rat. Behavioural Brain Research 2009, 205:154-161.
37. Phoenix C.H., Goy R.W., Gerall A.A., Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959, 65:369-382.
38. Ross H.E., Cole C.D., Smith Y., Neumann I.D., Landgraf R., Murphy A.Z., Young L.J. Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 2009, 162:892-903.
39. Ross H.E., Freeman S.M., Spiegel L.L., Ren X., Terwilliger E.F., Young L.J. Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. The Journal of Neuroscience 2009, 29:1312-1318.
40. Schulz K.M., Molenda-Figueira H.A., Sisk C.L. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Hormones and Behavior 2009, 55:597-604.
41. Swithers S.E., McCurley M., Hamilton E., Doerflinger A. Influence of ovarian hormones on development of ingestive responding to alterations in fatty acid oxidation in female rats. Hormones and Behavior 2008, 54:471-477.
42. Wang Z.X., Novak M.A. Influence of the social-environment on parental behavior and pup develoment of meadow voles (Microtus pennsylvanicus) and prairie voles (Microtus ochrogaster). Journal of Comparative Psychology 1992, 106:163-171.
43. Williams J.R., Carter C.S., Insel T. Partner preference development in female prairie voles is facilitated by mating or the central infusion of oxytocin. Annals of the New York Academy of Sciences 1992, 652:487-489.
44. Williams J.R., Insel T.R., Harbaugh C.R., Carter C.S. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). Journal of Neuroendocrinology 1994, 6:247-250.
45. Yamamoto Y., Carter C.S., Cushing B.S. Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience 2006, 137:157-164.
46. Young L.J., Wang Z. The neurobiology of the pair bond. Nature Neuroscience 2004, 7:1048-1054.
47. Young L.J., Lim M.M., Gingrich B., Insel T.R. Cellular mechanisms of social attachment. Hormones and Behavior 2001, 40:133-138.