Dopamine Regulation of Pair Bonding in Monogamous Prairie Voles

Neurobiology of the Parental Brain

Volumn , Issue , 2008, Pages 347-360

  Gobrogge, Kyle L ^a   Liu, Yan ^a   Wang, Zuoxin ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882875241     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374285-8.00022-6     Document Type: Chapter

References (131)

1. Aragona B.J., Wang Z. Opposing regulation of pair bond formation by cAMP signaling within the nucleus accumbens shell. J. Neurosci. 2007, 27:13352-13356.
2. Aragona B.J., Liu Y., Curtis J.T., Stephan F.K., Wang Z. A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. J. Neurosci. 2003, 23:3483-3490.
3. Aragona B.J., Liu Y., Yu Y.J., Curtis J.T., Detwiler J.M., Insel T.R., Wang Z. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat. Neurosci. 2006, 9:133-139.
4. Aragona B.J., Detwiler J.M., Wang Z. Amphetamine reward in the monogamous prairie vole. Neurosci. Lett. 2007, 418:190-194.
5. Argiolas A., Melis M.R., Gessa G.L. Yawning and penile erection: Central dopamine-oxytocin-adrenocorticotropin connection. Ann. NY Acad. Sci. 1988, 525:330-337.
6. Argiolas A., Collu M., D'Aquila P., Gessa G.L., Melis M.R., Serra G. Apomorphine stimulation of male copulatory behavior is prevented by the oxytocin antagonist d(CH2)5 Tyr(Me)-Orn8-vasotocin in rats. Pharmacol. Biochem. Behav. 1989, 33:81-83.
7. Baler R.D., Volkow N.D. Drug addiction: The neurobiology of disrupted self-control. Trends Mol. Med. 2006, 12:559-566.
8. Bamshad M., Novak M.A., De Vries G.J. Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J. Neuroendocrinol. 1993, 5:247-255.
9. Bartels A., Zeki S. The neural correlates of maternal and romantic love. Neuroimage 2004, 21:1155-1166.
10. Bowler C.M., Cushing B.S., Carter C.S. Social factors regulate female-female aggression and affiliation in prairie voles. Physiol. Behav. 2002, 76:559-566.
11. Boyson S.J., McGonigle P., Molinoff P.B. Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J. Neurosci. 1986, 6:3177-3188.
12. Brackett N.L., Iuvone P.M., Edwards D.A. Midbrain lesions, dopamine and male sexual behavior. Behav. Brain Res. 1986, 20:231-240.
13. Bridges T.E., Hillhouse E.W., Jones M.T. The effect of dopamine on neurohypophysial hormone release in vivo and from the rat neural lobe and hypothalamus in vitro. J. Physiol. 1976, 260:647-666.
14. Buijs R.M., Geffard M., Pool C.W., Hoorneman E.M. The dopaminergic innervation of the supraoptic and paraventricular nucleus. A light and electron microscopical study. Brain Res. 1984, 323:65-72.
15. Callier S., Snapyan M., Le Crom S., Prou D., Vincent J.D., Vernier P. Evolution and cell biology of dopamine receptors in vertebrates. Biol. Cell 2003, 95:489-502.
16. Calon F., Hadj Tahar A., Blanchet P.J., Morissette M., Grondin R., Goulet M., Doucet J.P., Robertson G.S., Nestler E., Di Paolo T., Bedard P.J. Dopamine-receptor stimulation: Biobehavioral and biochemical consequences. Trends Neurosci. 2000, 23:S92-S100.
17. Carr D.B., Sesack S.R. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 2000, 20:3864-3873.
18. Carter C.S., Getz L.L. Monogamy and the prairie vole. Sci. Am. 1993, 268:100-106.
19. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy: The prairie vole model. Neurosci. Biobehav. Rev. 1995, 19:303-314.
20. Chassler L. Understanding anorexia nervosa and bulimia nervosa from an attachment perspective. Clin. Soc. Work J. 1997, 25:407-423.
21. Cheung S., Ballew J.R., Moore K.E., Lookingland K.J. Contribution of dopamine neurons in the medial zona incerta to the innervation of the central nucleus of the amygdala, horizontal diagonal band of Broca and hypothalamic paraventricular nucleus. Brain Res. 1998, 808:174-181.
22. Clifton P.G., Somerville E.M. Disturbance of meal patterning following nucleus accumbens lesions in the rat. Brain Res. 1994, 667:123-128.
23. Curtis J.T., Wang Z. Glucocorticoid receptor involvement in pair bonding in female prairie voles: The effects of acute blockade and interactions with central dopamine reward systems. Neuroscience 2005, 134:369-376.
24. Curtis J.T., Wang Z. Ventral tegmental area involvement in pair bonding in male prairie voles. Physiol. Behav. 2005, 86:338-346.
25. DeVries A.C., DeVries M.B., Taymans S., Carter C.S. Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc. Natl Acad. Sci. USA 1995, 92:7744-7748.
26. Dewsbury D.A. The comparative psychology of monogamy. Nebr. Symp. Motiv. 1987, 35:1-50.
27. Deyo R.A., Straube K.T., Disterhoft J.F. Nimodipine facilitates associative learning in aging rabbits. Science 1989, 243:809-811.
28. Dominguez J.M., Gil M., Hull E.M. Preoptic glutamate facilitates male sexual behavior. J. Neurosci. 2006, 26:1699-1703.
29. Drago F., Caldwell J.D., Pedersen C.A., Continella G., Scapagnini U., Prange A.J. Dopamine neurotransmission in the nucleus accumbens may be involved in oxytocin-enhanced grooming behavior of the rat. Pharmacol. Biochem. Behav. 1986, 24:1185-1188.
30. Duncan, G. J., Wilkerson, B., and England, P. (2003). Cleaning up their act: The impact of marriage and cohabitation on licit and illicit drug use. Northwestern University, WP.
31. Ericsson M., Poston W.S., Foreyt J.P. Common biological pathways in eating disorders and obesity. Addict. Behav. 1996, 21:733-743.
32. Eyny Y.S., Horvitz J.C. Opposing roles of D1 and D2 receptors in appetitive conditioning. J. Neurosci. 2003, 23:1584-1587.
33. Febo M., Ferris C.F. Development of cocaine sensitization before pregnancy affects subsequent maternal retrieval of pups and prefrontal cortical activity during nursing. Neuroscience 2007, 148:400-412.
34. Fisher H., Aron A., Brown L.L. Romantic love: An fMRI study of a neural mechanism for mate choice. J. Comp. Neurol. 2005, 493:58-62.
35. Getz L.L., Hofmann J.E. Social organization in free-living prairie voles, Microtus ochrogaster. Behav. Ecol. Sociobiol. 1986, 18:275-282.
36. Getz L.L., Carter C.S., Gavish L. The mating system of the prairie vole, Microtus ochrogaster. Field and laboratory evidence for pair-bonding. Behav. Ecol. Sociobiol. 1981, 8:189-194.
37. Gingrich B., Liu Y., Cascio C., Wang Z., Insel T.R. Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav. Neurosci. 2000, 114:173-183.
38. Giordano A.L., Johnson A.E., Rosenblatt J.S. Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats. Physiol. Behav. 1990, 48:211-214.
39. Gobrogge K.L., Liu Y., Jia X., Wang Z. Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles. J. Comp. Neurol. 2007, 502:1109-1122.
40. Gonzaga G.C., Turner R.A., Keltner D., Campos B., Altemus M. Romantic love and sexual desire in close relationships. Emotion 2006, 6:163-179.
41. Hammock E.A., Young L.J. Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 2005, 308:1630-1634.
42. Hansen S., Bergvall A.H., Nyiredi S. Interaction with pups enhances dopamine release in the ventral striatum of maternal rats: A microdialysis study. Pharmacol. Biochem. Behav. 1993, 45:673-676.
43. Havassy B.E., Wasserman D.A., Hall S.M. Social relationships and abstinence from cocaine in an American treatment sample. Addiction 1995, 90:699-710.
44. Hernandez L., Hoebel B.G. Food intake and lateral hypothalamic self-stimulation covary after medial hypothalamic lesions or ventral midbrain 6-hydroxydopamine injections that cause obesity. Behav. Neurosci. 1989, 103:412-422.
45. Hull E.M., Dominguez J.M. Getting his act together: Roles of glutamate, nitric oxide, and dopamine in the medial preoptic area. Brain Res. 2006, 1126:66-75.
46. Hull E.M., Dominguez J.M. Sexual behavior in male rodents. Horm. Behav. 2007, 52:45-55.
47. Hull E.M., Eaton R.C., Moses J., Lorrain D. Copulation increases dopamine activity in the medial preoptic area of male rats. Life Sci. 1993, 52:935-940.
48. Hull E.M., Muschamp J.W., Sato S. Dopamine and serotonin: Influences on male sexual behavior. Physiol. Behav. 2004, 83:291-307.
49. Ikemoto S., Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking. Brain Res. Rev. 1999, 31:6-41.
50. Insel T.R. Is social attachment an addictive disorder?. Physiol. Behav. 2003, 79:351-357.
51. Insel T.R., Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl Acad. Sci. USA 1992, 89:5981-5985.
52. Insel T.R., Hulihan T.J. A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles. Behav. Neurosci. 1995, 109:782-789.
53. Insel T.R., Wang Z.X., Ferris C.F. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 1994, 14:5381-5392.
54. Insel T.R., Preston S., Winslow J.T. Mating in the monogamous male: Behavioral consequences. Physiol. Behav. 1995, 57:615-627.
55. Insel T.R., Winslow J.T., Wang Z., Young L.J. Oxytocin, vasopressin, and the neuroendocrine basis of pair bond formation. Adv. Exp. Med. Biol. 1998, 449:215-224.
56. Jannett F. Nesting patterns of adult voles, Microtus montanus, in field populations. J. Mammal. 1982, 63:495-498.
57. Kaestner, R. (1995). The effects of cocaine and marijuana use on marriage and marital stability. National Bureau of Economic Research Working Paper No. 5038.
58. Kandel D.B., Rosenbaum E., Chen K. Impact of maternal drug-use and life experiences on preadolescent children born to teenage mothers. J. Marriage Fam. 1994, 56:325-340.
59. Keer S.E., Stern J.M. Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol. Behav. 1999, 67:659-669.
60. Kendrick K.M. The neurobiology of social bonds. J. Neuroendocrinol. 2004, 16:1007-1008.
61. Koob G.F. Neurobiology of addiction. Toward the development of new therapies. Ann. NY Acad. Sci. 2000, 909:170-185.
62. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharm. 2001, 24:97-129.
63. Kovacs G.L., Sarnyai Z., Barbarczi E., Szabo G., Telegdy G. The role of oxytocin-dopamine interactions in cocaine-induced locomotor hyperactivity. Neuropharm. 1990, 29:365-368.
64. Lansing S.W., Lonstein J.S. Tyrosine hydroxylase-synthesizing cells in the hypothalamus of prairie voles (Microtus ochrogaster): Sex differences in the anteroventral periventricular preoptic area and effects of adult gonadectomy or neonatal gonadal hormones. J. Neurobiol. 2006, 66:197-204.
65. Lavi-Avnon Y., Weller A., Finberg J.P., Gispan-Herman I., Kinor N., Stern Y., et al. The reward system and maternal behavior in an animal model of depression: A microdialysis study. Psychopharmacology (Berl.) 2007.
66. Lim M.M., Young L.J. Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 2004, 125:35-45.
67. Lim M.M., Wang Z., Olazabal D.E., Ren X., Terwilliger E.F., Young L.J. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 2004, 429:754-757.
68. Lindvall O., Stenevi U. Dopamine and noradrenaline neurons projecting to the septal area in the rat. Cell. Tissue Res. 1978, 190:383-407.
69. Lindvall O., Bjorklund A., Skagerberg G. Selective histochemical demonstration of dopamine terminal systems in rat di- and telencephalon: New evidence for dopaminergic innervation of hypothalamic neurosecretory nuclei. Brain Res. 1984, 306:19-30.
70. Liu Y., Wang Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 2003, 121:537-544.
71. Liu Y., Curtis J.T., Wang Z. Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav. Neurosci. 2001, 115:910-919.
72. Lonstein J.S. Effects of dopamine receptor antagonism with haloperidol on nurturing behavior in the biparental prairie vole. Pharmacol. Biochem. Behav. 2002, 74:11-19.
73. Lonstein J.S., De Vries G.J. Sex differences in the parental behaviour of adult virgin prairie voles: Independence from gonadal hormones and vasopressin. J. Neuroendocrinol. 1999, 11:441-449.
74. Maeda H., Mogenson G.J. An electrophysiological study of inputs to neurons of the ventral tegmental area from the nucleus accumbens and medial preoptic-anterior hypothalamic areas. Brain Res. 1980, 197:365-377.
75. Maldonado R. The neurobiology of addiction. J. Neural Transm. Suppl. 2003, 1-14.
76. Marazziti D., Dell'Osso B., Baroni S., Mungai F., Catena M., Rucci P., Albanese F., Giannaccini G., Betti L., Fabbrini L., Italiani P., Del Debbio A., Lucacchini A., Dell'Osso L. A relationship between oxytocin and anxiety of romantic attachment. Clin. Pract. Epidemol. Ment. Health 2006, 2:28.
77. Marsden C.A. Dopamine: The rewarding years. Br. J. Pharmacol. 2006, 147(Suppl 1):S136-S144.
78. Martel P., Fantino M. Influence of the amount of food ingested on mesolimbic dopaminergic system activity: A microdialysis study. Pharmacol. Biochem. Behav. 1996, 55:297-302.
79. Mas M., Fumero B., Gonzalez-Mora J.L. Voltammetric and microdialysis monitoring of brain monoamine neurotransmitter release during sociosexual interactions. Behav. Brain Res. 1995, 71:69-79.
80. McGuire B., Novak M. A comparison of maternal behavior in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim. Behav. 1984, 32:1132-1141.
81. McGuire B., Novak M. Parental care and its relation to social organization in the montane vole. J. Mammal. 1986, 67:305-311.
82. Meisel R.L., Camp D.M., Robinson T.E. A microdialysis study of ventral striatal dopamine during sexual behavior in female Syrian hamsters. Behav. Brain Res. 1993, 55:151-157.
83. Miller S.M., Lonstein J.S. Dopamine d1 and d2 receptor antagonism in the preoptic area produces different effects on maternal behavior in lactating rats. Behav. Neurosci. 2005, 119:1072-1083.
84. Moos F., Richard P. Excitatory effect of dopamine on oxytocin and vasopressin reflex releases in the rat. Brain Res. 1982, 241:249-260.
85. Moos R.H., Nichol A.C., Moos B.S. Risk factors for symptom exacerbation among treated patients with substance use disorders. Addiction 2002, 97:75-85.
86. Moses J., Loucks J.A., Watson H.L., Matuszewich L., Hull E.M. Dopaminergic drugs in the medial preoptic area and nucleus accumbens: Effects on motor activity, sexual motivation, and sexual performance. Pharmacol. Biochem. Behav. 1995, 51:681-686.
87. Murphy T.H., Worley P.F., Baraban J.M. L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron 1991, 7:625-635.
88. Neill D.B., Fenton H., Justice J.B. Increase in accumbal dopaminergic transmission correlates with response cost not reward of hypothalamic stimulation. Behav. Brain Res. 2002, 137:129-138.
89. Nestler E.J., Malenka R.C. The addicted brain. Sci. Am. 2004, 290:78-85.
90. Neve K.A., Seamans J.K., Trantham-Davidson H. Dopamine receptor signaling. J. Recept. Signal Transduct. Res. 2004, 24:165-205.
91. Newman S.W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. NY Acad. Sci. 1999, 877:242-257.
92. Northcutt K.V., Wang Z., Lonstein J.S. Sex and species differences in tyrosine hydroxylase-synthesizing cells of the rodent olfactory extended amygdala. J. Comp. Neurol. 2007, 500:103-115.
93. Numan M. Motivational systems and the neural circuitry of maternal behavior in the rat. Dev. Psychobiol. 2007, 49:12-21.
94. Numan M., Numan M.J., Pliakou N., Stolzenberg D.S., Mullins O.J., Murphy J.M., Smith C.D. The effects of D1 or D2 dopamine receptor antagonism in the medial preoptic area, ventral pallidum, or nucleus accumbens on the maternal retrieval response and other aspects of maternal behavior in rats. Behav. Neurosci. 2005, 119:1588-1604.
95. Oliveras D., Novak M. A comparison of paternal behavior in the meadow vole, Microtus pennsylvanicus, the pine vole, Microtus pinetorum, and prairie vole, Microtus ochrogaster. Anim. Behav. 1986, 34:519-526.
96. Panksepp J., Knutson B., Burgdorf J. The role of brain emotional systems in addictions: A neuro-evolutionary perspective and new 'self-report' animal model. Addiction 2002, 97:459-469.
97. Pecina S., Cagniard B., Berridge K.C., Aldridge J.W., Zhuang X. Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards. J. Neurosci. 2003, 23:9395-9402.
98. Pedersen C.A. Biological aspects of social bonding and the roots of human violence. Ann. NY Acad. Sci. 2004, 1036:106-127.
99. Pfaus J.G., Damsma G., Nomikos G.G., Wenkstern D.G., Blaha C.D., Phillips A.G., Fibiger H.C. Sexual behavior enhances central dopamine transmission in the male rat. Brain Res. 1990, 530:345-348.
100. Pitkow L.J., Sharer C.A., Ren X., Insel T.R., Terwilliger E.F., Young L.J. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J. Neurosci. 2001, 21:7392-7396.
101. Pollack A. Coactivation of D1 and D2 dopamine receptors: In marriage, a case of his, hers, and theirs. Sci. STKE 2004, pe50.
102. Self D.W., Barnhart W.J., Lehman D.A., Nestler E.J. Opposite modulation of cocaine-seeking behavior by D1- and D2-like dopamine receptor agonists. Science 1996, 271:1586-1589.
103. Self D.W., Genova L.M., Hope B.T., Barnhart W.J., Spencer J.J., Nestler E.J. Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J. Neurosci. 1998, 18:1848-1859.
104. Smeltzer M.D., Curtis J.T., Aragona B.J., Wang Z. Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci. Lett. 2006, 394:146-151.
105. Stolzenberg D.S., McKenna J.B., Keough S., Hancock R., Numan M.J., Numan M. Dopamine D1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav. Neurosci. 2007, 121:907-919.
106. Surmeier D.J., Ding J., Day M., Wang Z., Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 2007, 30:228-235.
107. Swain J.E., Lorberbaum J.P., Kose S., Strathearn L. Brain basis of early parent-infant interactions: Psychology, physiology, and in vivo functional neuroimaging studies. J. Child Psychol. Psychiatr. 2007, 48:262-287.
108. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
109. Tamarin R. Biology of new world Microtus. Am. Soc. Mamm. Spec. 1985, Pub 8.
110. Triemstra J.L., Nagatani S., Wood R.I. Chemosensory cues are essential for mating-induced dopamine release in MPOA of male Syrian hamsters. Neuropsychopharm. 2005, 30:1436-1442.
111. Tyagi M.G., Handa R.K., Stephen P.M., Bapna J.S. Vasopressin induces dopamine release and cyclic AMP efflux from the brain of water-deprived rats: Inhibitory effect of vasopressin V2 receptor-mediated phosphorylation. Biol. Signals Recept. 1998, 7:328-336.
112. Volkow N.D., Wang G.J., Fowler J.S., Logan J., Jayne M., Franceschi D., Wong C., Gatley S.J., Gifford A.N., Ding Y.S., Pappas N. "Nonhedonic" food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect. Synapse 2002, 44:175-180.
113. Wang G.J., Volkow N.D., Fowler J.S. The role of dopamine in motivation for food in humans: Implications for obesity. Expert Opin. Ther. Targets 2002, 6:601-609.
114. Wang Z., Aragona B.J. Neurochemical regulation of pair bonding in male prairie voles. Physiol. Behav. 2004, 83:319-328.
115. Wang Z., Smith W., Major D.E., De Vries G.J. Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain Res. 1994, 650:212-218.
116. Wang Z., Hulihan T.J., Insel T.R. Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Res. 1997, 767:321-332.
117. Wang Z., Young L.J., De Vries G.J., Insel T.R. Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog. Brain Res. 1998, 119:483-499.
118. Wang Z., Yu G., Cascio C., Liu Y., Gingrich B., Insel T.R. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): A mechanism for pair bonding?. Behav. Neurosci. 1999, 113:602-611.
119. Wersinger S.R., Rissman E.F. Dopamine activates masculine sexual behavior independent of the estrogen receptor alpha. J. Neurosci. 2000, 20:4248-4254.
120. 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. Ann. NY Acad. Sci. 1992, 652:487-489.
121. 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). J. Neuroendocrinol. 1994, 6:247-250.
122. Winn P., Robbins T.W. Comparative effects of infusions of 6-hydroxydopamine into nucleus accumbens and anterolateral hypothalamus induced by 6-hydroxydopamine on the response to dopamine agonists, body weight, locomotor activity and measures of exploration in the rat. Neuropharm. 1985, 24:25-31.
123. Winslow J.T., Hastings N., Carter C.S., Harbaugh C.R., Insel T.R. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 1993, 365:545-548.
124. Wommack, J. C., and Wang, Z. (2007). Dopamine in the prefrontal cortex regulates partner preference formation in female prairie voles, Poster P1.28, Presented at the Society for Behavioral Neuroendocrinology, Pacific Grove, CA.
125. Yamada S., Uchida S., Ohkura T., Kimura R., Yamaguchi M., Suzuki M., Yamamoto M. Alterations in calcium antagonist receptors and calcium content in senescent brain and attenuation by nimodipine and nicardipine. J. Pharmacol. Exp. Ther. 1996, 277:721-727.
126. Yamaguchi K., Kandel D.B. On the resolution of role incompatibility-A life event history analysis of family roles and marijuana use. Am. J. Sociol. 1985, 90:1284-1325.
127. Young L.J., Wang Z. The neurobiology of pair bonding. Nat. Neurosci. 2004, 7:1048-1054.
128. Young L.J., Winslow J.T., Nilsen R., Insel T.R. Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: Behavioral consequences. Behav. Neurosci. 1997, 111:599-605.
129. Young L.J., Wang Z., Insel T.R. Neuroendocrine bases of monogamy. Trends Neurosci. 1998, 21:71-75.
130. Yun I.A., Wakabayashi K.T., Fields H.L., Nicola S.M. The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J. Neurosci. 2004, 24:2923-2933.
131. Zeiss C.J. Neuroanatomical phenotyping in the mouse: The dopaminergic system. Vet. Pathol. 2005, 42:753-773.