Neuroendocrine and Behavioural Responses to Exposure to an Infant in Male Prairie Voles

Journal of Neuroendocrinology

Volumn 24, Issue 6, 2012, Pages 874-886

  Kenkel, W M ^a   Paredes, J ^a,b   Yee, J R ^a   Pournajafi Nazarloo, H ^a   Bales, K L ^a,c   Carter, C S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alloparental behaviour; Corticotrophin releasing hormone; Oxytocin; Pair bonding; Prairie voles; Vasopressin

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; OXYTOCIN; PROTEIN C FOS; VASOPRESSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; CORTICOSTEROID RELEASE; CORTICOSTERONE BLOOD LEVEL; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; HYPOTHESIS; MALE; NERVE CELL; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PUP (RODENT); REPRODUCTION; VOLE;

AGGRESSION; ANIMALS; ARVICOLINAE; BEHAVIOR, ANIMAL; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; FEMALE; HOUSING, ANIMAL; MALE; OXYTOCIN; PATERNAL BEHAVIOR; RANDOM ALLOCATION; SOCIAL BEHAVIOR; VASOPRESSINS;

EID: 84860904520     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02301.x     Document Type: Article

References (75)

1. Olazabal DE, Young LJ. Oxytocin receptors in the nucleus accumbens facilitate 'spontaneous' maternal behavior in adult female prairie voles. Neuroscience 2006; 141: 559-568.
2. Pedersen CA, Prange AJ Jr. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci USA 1979; 76: 6661-6665.
3. Kleiman DG. Monogamy in mammals. Q Rev Biol 1977; 52: 39-69.
4. Carter CS, Roberts RL. The psychobiological basis of cooperative breeding. In: Solomon NG, French JA, eds. Cooperative Breeding in Mammals. New York, NY: Cambridge Press, 1997: 231-266.
5. Carter CS, DeVries AC, Getz LL. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 1995; 19: 303-314.
6. Aragona BJ, Wang Z. The prairie vole (Microtus ochrogaster): an animal model for behavioral neuroendocrine research on pair bonding. ILAR J 2004; 45: 35-45.
7. Young KA, Liu Y, Wang Z. The neurobiology of social attachment: a comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comp Biochem Physiol C Toxicol Pharmacol 2008; 148: 401-410.
8. Young LJ, Wang Z. The neurobiology of pair bonding. Nat Neurosci 2004; 7: 1048-1054.
9. Lonstein JS, De Vries GJ. Social influences on parental and nonparental responses towards pups in virgin female prairie voles (Microtus ochrogaster). J Comp Psychol 2001; 115: 53-61.
10. Roberts RL, Miller AK, Taymans SE, Carter CS. Role of social and endocrine factors in alloparental behavior of prairie voles (Microtus ochrogaster). Can J Zool 1998; 76: 1862-1868.
11. Lonstein JS, De Vries GJ. Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 2000; 24: 669-686.
12. Roberts RL, Williams JR, Wang AK, Carter CS. Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation. Anim Behav 1998; 55: 1131-1140.
13. Keverne EB, Kendrick KM. Oxytocin facilitation of maternal behavior in sheep. Ann NY Acad Sci 1992; 652: 83-101.
14. Feldman R. Parent-infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. J Child Psychol Psychiatry 2007; 4: 329-354.
15. Feldman R, Gordon I, Schneiderman I, Weisman O, Zagoory-Sharon O. Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 2010; 35: 1133-1141.
16. Saito A, Nakamura K. Oxytocin changes primate paternal tolerance to offspring in food transfer. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2011; 197: 329-337.
17. Lonstein JS, De Vries GJ. Sex differences in the parental behaviour of adult virgin prairie voles: independence from gonadal hormones and vasopressin. J Neuroendocrinol 1999; 11: 441-449.
18. Schradin C. Comments to K.E. Wynne-Edwards and M.E. Timonin 2007. Paternal care in rodents: weakening support of hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care, Horm & Behav 52: 114-121. Horm Behav 2007; 52: 557-559.
19. Wynne-Edwards KE, Timonin ME. Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm Behav 2007; 52: 114-121.
20. Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J Neurosci 2004; 24: 2974-2982.
21. Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J Neuroendocrinol 2000; 12: 235-243.
22. DeVries AC, DeVries MB, Taymans SE, Carter CS. The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc Natl Acad Sci USA 1996; 93: 11980-11984.
23. Bales KL, Kramer KM, Lewis-Reese AD, Carter CS. Effects of stress on parental care are sexually dimorphic in prairie voles. Physiol Behav 2006; 87: 424-429.
24. DeVries AC, Guptaa T, Cardillo S, Cho M, Carter CS. Corticotropin-releasing factor induces social preferences in male prairie voles. Psychoneuroendocrinology 2002; 27: 705-714.
25. Saltzman W, Boettcher CA, Post JL, Abbott DH. Inhibition of maternal behaviour by central infusion of corticotrophin- releasing hormone in marmoset monkeys. J Neuroendocrinol 2011; 23: 1139-1148.
26. Simmons DM, Swanson LW. Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: toward a global 3D model. J Comp Neurol 2009; 516: 423-441.
27. Jacobson L, Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 1991; 12: 118-134.
28. Liang KC, Lee EH. Intra-amygdala injections of corticotropin releasing factor facilitate inhibitory avoidance learning and reduce exploratory behavior in rats. Psychopharmacology 1988; 96: 232-236.
29. Sahuque LL, Kullberg EF, McGeehan AJ, Kinder JR, Hicks MP, Blanton MG, Janak PH, Olive MF. Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: role of CRF receptor subtypes. Psychopharmacology 2006; 186: 122-132.
30. Kirkpatrick B, Kim JW, Insel TR. Limbic system fos expression associated with paternal behavior. Brain Res 1994; 658: 112-118.
31. Swain JE, Kim P, Shaun HoS. Neuroendocrinology of parental response to baby-cry. J Neuroendocrinol 2011; 23: 1036-1041.
32. Carter CS. Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res 2007; 176: 170-186.
33. Wang Z, Young LJ, De Vries GJ, Insel TR. Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 1998; 119: 483-499.
34. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 1993; 365: 545-548.
35. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B. Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 2010; 31: 307-321.
36. Ferris CF, Singer EA, Meenan DM, Albers HE. Inhibition of vasopressin-stimulated flank marking behavior by V1-receptor antagonists. Eur J Pharmacol 1988; 154: 153-159.
37. Wang Z, Ferris CF, De Vries GJ. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc Natl Acad Sci USA 1994; 91: 400-404.
38. Bester-Meredith JK, Young LJ, Marler CA. Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 1999; 36: 25-38.
39. de Jong TR, Chauke M, Harris BN, Saltzman W. From here to paternity: neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus). Horm Behav 2009; 56: 220-231.
40. Bales KL, Kim AJ, Lewis-Reese AD, Sue Carter C. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav 2004; 45: 354-361.
41. Cho MM, DeVries AC, Williams JR, Carter CS. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 1999; 113: 1071-1079.
42. Liu Y, Curtis JT, Wang Z. Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav Neurosci 2001; 115: 910-919.
43. Williams JR, Insel TR, Harbaugh CR, Carter CS. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 1994; 6: 247-250.
44. Williams JR, Catania KC, Carter CS. Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm Behav 1992; 26: 339-349.
45. Ruscio MG, Sweeny TD, Hazelton JL, Suppatkul P, Boothe E, Carter CS. Pup exposure elicits hippocampal cell proliferation in the prairie vole. Behav Brain Res 2008; 187: 9-16.
46. Cushing BS, Mogekwu N, Le WW, Hoffman GE, Carter CS. Cohabitation induced Fos immunoreactivity in the monogamous prairie vole. Brain Res 2003; 965: 203-211.
47. Bales KL, van Westerhuyzen JA, Lewis-Reese AD, Grotte ND, Lanter JA, Carter CS. Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles. Horm Behav 2007; 52: 274-279.
48. DeVries AC, Carter CS. Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster). Can J Zool 1999; 77: 885-889.
49. Carter CS, Getz LL, Gavish L, McDermott JL, Arnold P. Male-related pheromones and the activation of female reproduction in the prairie vole (Microtus ochrogaster). Biol Reprod 1980; 23: 1038-1045.
50. Carter CS, Witt DM, Schneider J, Harris ZL, Violkening D. Male stimuli are necessary for female sexual behavior and uterine growth in prairie voles (Microtus ochrogaster). Horm Behav 1987; 21: 74-82.
51. Kramer K, Cushing B, Carter CS, Wu J, Ottinger M. Sex and species differences in plasma oxytocin using an enzyme immunoassay. Can J Zool 2004; 82: 1194-1200.
52. DeVries AC, DeVries MB, Taymans S, Carter CS. Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc Natl Acad Sci USA 1995; 92: 7744-7748.
53. Cushing BS, Klein D, Hoffman GE, Carter CS, Le WW, de Vries GJ. Comparison of fixation techniques: immersion versus perfusion. Horm Behav 2001; 39: 329.
54. Watson RE Jr, Wiegand SJ, Clough RW, Hoffman GE. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 1986; 7: 155-159.
55. Grippo AJ, Cushing BS, Carter CS. Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 2007; 32: 966-980.
56. Grippo AJ, Cushing BS, Carter CS. Depression-like behavior and stressor-induced neuroendocrine activation in female prairie voles exposed to chronic social isolation. Psychosom Med 2007; 69: 149-157.
57. Lonstein JS, De Vries GJ. Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster). Physiol Behav 1999; 66: 33-40.
58. Legros JJ, Chiodera P, Geenen V. Inhibitory action of exogenous oxytocin on plasma cortisol in normal human subjects: evidence of action at the adrenal level. Neuroendocrinology 1988; 48: 204-206.
59. Legros JJ, Chiodera P, Geenen V, von Frenckell R. Confirmation of the inhibitory influence of exogenous oxytocin on cortisol and ACTH in man: evidence of reproducibility. Acta Endocrinol 1987; 114: 345-349.
60. Stachowiak A, Macchi C, Nussdorfer GG, Malendowicz LK. Effects of oxytocin on the function and morphology of the rat adrenal cortex: in vitro and in vivo investigations. Res Exp Med 1995; 195: 265-274.
61. Banks WA, Kastin AJ. Permeability of the blood-brain barrier to neuropeptides: the case for penetration. Psychoneuroendocrinology 1985; 10: 385-399.
62. Parker KJ, Lee TM. Central vasopressin administration regulates the onset of facultative paternal behavior in Microtus pennsylvanicus (meadow voles). Horm Behav 2001; 39: 285-294.
63. Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M. Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience 1998; 85: 1209-1222.
64. Kovacs KJ. c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 1998; 33: 287-297.
65. Bosch OJ, Neumann ID. Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm Behav 2011; 61: 293-303.
66. Kiyama H, Emson PC. Evidence for the co-expression of oxytocin and vasopressin messenger ribonucleic acids in magnocellular neurosecretory cells: simultaneous demonstration of two neurohypophysin messenger ribonucleic acids by hybridization histochemistry. J Neuroendocrinol 1990; 2: 257-259.
67. Francis DD, Champagne FC, Meaney MJ. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 2000; 12: 1145-1148.
68. Olazábal DE, Young LJ. Variability in 'spontaneous' maternal behavior is associated with anxiety-like behavior and affiliation in naïve juvenile and adult female prairie voles (Microtus ochrogaster). Dev Psychobiol 2005; 47: 166-178.
69. Olazábal DE, Young LJ. Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm Behav 2006; 49: 681-687.
70. Stock S, Uvnas-Moberg K. Increased plasma levels of oxytocin in response to afferent electrical stimulation of the sciatic and vagal nerves and in response to touch and pinch in anaesthetized rats. Acta Physiol Scand 1988; 132: 29-34.
71. Uvnas-Moberg K, Bruzelius G, Alster P, Lundeberg T. The antinociceptive effect on non-noxious sensory stimulation is mediated partly through oxytocinergic mechanisms. Acta Physiol Scand 1993; 149: 199-204.
72. Engelmann M, Landgraf R, Wotjak CT. The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited. Front Neuroendocrinol 2004; 4: 132-149.
73. Windle RJ, Shanks N, Lightman SL, Ingram CD. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 1997; 138: 2829-2834.
74. Carter CS, DeVries AC, Taymans SE, Roberts RL, Williams JR, Chrousos GP. Adrenocorticoid hormones and the development and expression of mammalian monogamy. Ann NY Acad Sci 1995; 771: 82-91.
75. Bales KL, Carter CS. Developmental exposure to oxytocin facilitates partner preference in male prairie voles (Microtus ochrogaster). Behav Neurosci 2003; 117: 854-859.