The prairie vole (Microtus ochrogaster): An animal model for behavioral neuroendocrine research on pair bonding

ILAR Journal

Volumn 45, Issue 1, 2004, Pages 35-45

  Aragona, Brandon J ^a   Wang, Zuoxin ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Corticosterone; Dopamine; Mating; Microtus; Monogamy; Oxytocin; Pair bond; Social attachment; Vasopressin

Indexed keywords

ARGIPRESSIN; ARGIPRESSIN RECEPTOR; CORTICOSTERONE; DOPAMINE; NEUROPEPTIDE; OXYTOCIN; OXYTOCIN RECEPTOR; VASOPRESSIN; GLUCOCORTICOID; VASOPRESSIN DERIVATIVE;

ANIMAL BEHAVIOR; BREEDING; FEMALE; HORMONAL REGULATION; MALE; MOLECULAR MECHANICS; MONOGAMY; NEUROANATOMY; NEUROCHEMISTRY; NEUROENDOCRINE SYSTEM; NONHUMAN; REGULATORY MECHANISM; REVIEW; SEX DIFFERENCE; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL INTERACTION; VOLE; ANIMAL; ANIMAL MODEL; ARVICOLINAE; COMPARATIVE STUDY; NEUROSECRETION; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALIA; MICROTUS; MICROTUS OCHROGASTER; MURIDAE;

ANIMALS; ARVICOLINAE; DOPAMINE; GLUCOCORTICOIDS; MODELS, ANIMAL; NEUROSECRETORY SYSTEMS; PAIR BOND; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; VASOPRESSINS;

EID: 1442287363     PISSN: 10842020     EISSN: None     Source Type: Journal    
DOI: 10.1093/ilar.45.1.35     Document Type: Review

References (128)

1. Albers HE, Hennessey AC, Whitman, DC. 1992. Vasopressin and the regulation of hamster social behavior. Ann N Y Acad Sci 652:227-242.
2. Aragona BJ, Liu Y, Curtis JT, Stephan FK, Wang ZX. 2003a. A critical role for nucleus accumbens dopamine in partner preference formation of male prairie voles. J Neurosci 23:3483-3490.
3. Aragona BJ, Liu Y, Yu YJ, Damron A, Perlman G, Wang ZX. 2003b. Opposite modulation of social attachment by D1- and D2-type dopamine receptor activation in nucleus accumbens shell (Abstract). Horm Behav 44:37.
4. Argiolas A, Collu M, D'Aquila P, Gessa GL, Melis MR, Serra G. 1989. Apomorphine stimulation of male copulatory behavior is prevented by the oxytocin antagonist d(CH2)5 Tyr(Me)-Orn8-vasotocin in rats. Pharmacol Biochem Behav 33:81-83.
5. Argiolas A, Melis MR, Gessa GL. 1988. Yawning and penile erection: Central dopamine-oxytocin-adrenocorticotropin connection. Ann N Y Acad Sci 525:330-337.
6. Bamshad M, Novak MA, De Vries GJ. 1993. Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster, and meadow voles, Microtus pennsylvanicus. J Neuroendocrinol 5:247-255.
7. Bamshad M, Novak MA, De Vries GJ. 1994. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles ( Microtus ochrogaster). Physiol Behav 56:751-758.
8. Barberis C, Tribollet E. 1996. Vasopressin and oxytocin receptors in the central nervous system. Crit Rev Neurobiol 10:119-154.
9. Bilbo SD, Mein SL, DeVries AC, Nelson RJ. 1999. Lipopolysaccharide facilitates partner preference behaviors in female prairie voles. Physiol Behav 68:151-156.
10. Birney EC, Grant WE, Baird DD. 1976. Importance of vegetative cover to cycles of Microtus populations. Ecology 57:1043-1051.
11. Bluthe RM, Dantzer R. 1990. Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res 535:301-304.
12. Bowler CM, Cushing BS, Carter CS. 2002. Social factors regulate female-female aggression and affiliation in prairie voles. Physiol Behav 76: 559-566.
13. Carter CS. 1992. Oxytocin and sexual behavior. Neurosci Biobehav Rev 16:131-144.
14. Carter CS, DeVries AC, Getz LL. 1995. Physiological substrates of mammalian monogamy: The prairie vole model. Neurosci Biobehav Rev 19:303-314.
15. Carter CS, Getz LL. 1993. Monogamy and the prairie vole. Sci Am 268: 100-106.
16. Carter CS, Witt DM, Manock SR, Adams KA, Bahr JM, Carlstead K. 1989. Hormonal correlates of sexual behavior and ovulation in male-induced and postpartum estrus in female prairie voles. Physiol Behav 46:941-948.
17. Cho MM, DeVries AC, Williams JR, Carter CS. 1999. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113:1071-1079.
18. Compaan JC, Buijs RM, Pool CW, De Ruiter AJ, Koolhaas JM. 1993. Differential lateral septal vasopressin innervation in aggressive and nonaggressive male mice. Brain Res Bull 30:1-6.
19. Crenshaw BJ, De Vries GJ, Yahr P. 1992. Vasopressin innervation of sexually dimorphic structures of the gerbil forebrain under various hormonal conditions. J Comp Neurol 322:589-598.
20. Curtis JT, Stowe JR, Wang ZX. 2003. Differential effects of intraspecific interactions on the striatal dopamine system in social and non-social voles. Neuroscience 118:1165-1173.
21. Curtis JT, Wang, ZX. 2003. Forebrain c-fos expression under conditions conducive to pair bonding in female prairie voles (Microtus ochrogaster). Physiol Behav (In Press).
22. Cushing BS, Martin JO, Young LJ, Carter CS. 2001. The effects of peptides on partner preference formation are predicted by habitat in prairie voles. Horm Behav 39:48-58.
23. Cushing BS, Mogekwu N, Le WW, Hoffman GE, Carter CS. 2003. Cohabitation induced Fos immunoreactivity in the monogamous prairie vole. Brain Res 965:203-211.
24. Dantzer R, Koob GF, Bluthe RM, Le Moal M. 1988. Septal vasopressin modulates social memory in male rats. Brain Res 457:143-147.
25. De Vries GJ, Best W, Sluiter AA. 1983. The influence of androgens on the development of a sex difference in the vasopressinergic innervation of the rat lateral septum. Brain Res 284:377-380.
26. De Vries GJ, Miller MA. 1998. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog Brain Res 119:3-20.
27. DeVries AC, DeVries MB, Taymans S, Carter CS. 1995. Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc Natl Acad Sci U S A 92:7744-7748.
28. DeVries AC, DeVries MB, Taymans SE, Carter CS. 1996. The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc Natl Acad Sci U S A 93:11980-11984.
29. DeVries AC, Guptaa T, Cardillo S, Cho M, Carter CS. 2002. Corticotropin-releasing factor induces social preferences in male prairie voles. Psychoneuroendocrinology 27:705-714.
30. DeVries AC, Johnson CL, Carter CS. 1997. Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster). Can J Zool 75:295-301.
31. Dewsbury DA. 1987. The comparative psychology of monogamy. Nebr Symp Motiv 35:1-50.
32. Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215-223.
33. Engelmann M, Wotjak CT, Neumann I, Ludwig M, Landgraf R. 1996. Behavioral consequences of intracerebral vasopressin and oxytocin: Focus on learning and memory. Neurosci Biobehav Rev 20:341-358.
34. Ferguson JN, Young LJ, Insel TR. 2002. The neuroendocrine basis of social recognition. Front Neuroendocrinol 23:200-224.
35. Ferris CF, Delville Y. 1994. Vasopressin and serotonin interactions in the control of agonistic behavior. Psychoneuroendocrinology 19:593-601.
36. Ferris CF, Melloni RH, Jr., Koppel G, Perry KW, Fuller RW, Delville Y. 1997. Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J Neurosci 17:4331-4340.
37. Fowler CD, Liu Y, Ouimet C, Wang ZX. 2002. The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115-128.
38. Galea LA, McEwen BS. 1999. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89:955-964.
39. Gerkema MP, van der Leest F. 1991. Ongoing ultradian activity rhythms in the common vole, Microtus arvalis, during deprivations of food, water and rest. J Comp Physiol [A] 168:591-597.
40. Getz LL. 1978. Speculation on social structure and population cycles of microtine rodents. Biologist 60:134-147.
41. Getz LL, Carter CS. 1996. Prairie-vole partnerships. Am Sci 84:56-62.
42. Getz LL, Carter CS, Gavish L. 1981. The mating system of the prairie vole Microtus achrogaster: Field and laboratory evidence for pair-bonding. Behav Ecol Sociobiol 8:189-194.
43. Getz LL, Hofmann JE. 1986. Social organization in free-living prairie voles, Microtus ochrogaster. Behav Ecol Sociobiol 18:275-282.
44. Getz LL, McGuire B, Pizzuto T, Hofmann JE, Frase B. 1993. Social organization of the prairie vole (Micratus ochrogaster). J Mamm 74: 44-58.
45. Gingrich B, Liu Y, Cascio C, Wang ZX, Insel TR. 2000. Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav Neurosci 114: 173-183.
46. Goeders NE. 2002. The HPA axis and cocaine reinforcement. Psychoneuroendocrinology 27:13-33.
47. Gruder-Adams S, Getz LL. 1985. Comparisons of the mating system and parental behavior in Microtus ochrogaster and M. Pennsylvanicus. J Mamm 66:165-167.
48. Hall ER. 1981. The Mammals of North America. 2nd ed. New York: John Wiley.
49. Hammock EA, Young LJ. 2002. Variation in the vasopressin V1a receptor promoter and expression: Implications for inter- and intraspecific variation in social behaviour. Eur J Neurosci 16:399-402.
50. Hastings NB, Orchinik M, Aubourg MV, McEwen BS. 1999. Pharmacological characterization of central and peripheral type I and type II adrenal steroid receptors in the prairie vole, a glucocorticoid-resistant rodent. Endocrinology 140:4459-4469.
51. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. 1991. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125.
52. Ikemoto S, Panksepp J. 1999. The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31:6-41.
53. Insel TR. 1992. Oxytocin - a neuropeptide for affiliation: Evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneunoendocrinology 17:3-35.
54. Insel TR, Harbaugh CR. 1989. Central administration of corticotropin releasing factor alters rat pup isolation calls. Pharmacol Biochem Behav 32:197:201.
55. Insel TR, Hulihan TJ. 1995. A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109:782-789.
56. Insel TR, Shapiro LE. 1992. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci U S A 89:5981-5985.
57. Insel TR, Wang ZX, Ferris CF. 1994. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14:5381-5392.
58. Insel TR, Young LJ. 2001. The neurobiology of attachment. Nat Rev Neurosci 2:129-136.
59. Jannett FJ. 1982. Nesting patterns of adult voles, Microtus montanus, in field populations. J Mamm 63:495-498.
60. Jirikowski GF. 1992. Oxytocinergic neuronal systems during mating, pregnancy, parturition, and lactation. Ann N Y Acad Sci 652:253-270.
61. Kendrick KM, Keverne EB, Baldwin BA. 1987. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology 46:56-61.
62. Kim JW, Kirkpatrick B. 1996. Social isolation in animal models of relevance to neuropsychiatric disorders. Biol Psychiatry 40:918-922.
63. Kirkpatrick B, Carter CS, Newman SW, Insel TR. 1994. Axon-sparing lesions of the medial nucleus of the amygdala decrease affiliate behaviors in the prairie vole (Microtus ochrogaster): Behavior and anatomical specificity. Behav Neurosci 108:501-513.
64. Koob GF, Nestler EJ. 1997. The neurobiology of drug addiction. J Neuropsychiatry Clin Neurosci 9:482-497.
65. Kovacs GL, Sarnyai Z, Szabo G. 1998. Oxytocin and addiction: A review. Psychoneuroendocrinology 23:945-962.
66. Kretschmer BD. 2000. Functional aspects of the ventral pallidum. Amino Acids 19:201-210.
67. Lim MM, Young LJ. 2002. Blockade of vasopressin V1a receptors in the ventral pallidum prevents partner preference formation in monogamous male prairie voles (Abstract). Soc Neurosci 89.2.
68. Liu Y, Curtis JT, Fowler CD, Spencer C, Houpt T, Wang ZX. 2001a. Differential expression of vasopressin, oxytocin and corticotrophin-releasing hormone messenger RNA in the paraventricular nucleus of the prairie vole brain following stress. J Neuroendocrinol 13:1059-1065.
69. Liu Y, Curtis JT, Wang ZX. 2001b. Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav Neurosci 115:910-919.
70. Liu Y, Wang ZX. 2003. Nucleus accumbens dopamine and oxytocin interact to regulate pair bond formation in female prairie voles. Neuroscience (In Press).
71. Lonstein JS, De Vries GJ. 2000. Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24:669-686.
72. Mahata SK, Mahata M, Hortnag H, Fischer-Colbrie R, Steiner HJ, Dietze O, Winkler H. 1993. Concomitant changes of messenger ribonucleic acid levels of secretogranin II, VGF, vasopressin and oxytocin in the paraventricular nucleus of rats after adrenalectomy and during lactation. J Neuroendocrinol 5:323-330.
73. Mas M, Fumero B, Gonzalez-Mora JL. 1995. Voltammetric and microdialysis monitoring of brain monoamine neurotransmitter release during sociosexual interactions. Behav Brain Res 71:69-79.
74. McGuire B, Getz LL, Hofmann JE, Pizzuto T, Frase B. 1993. Natal dispersal and philopatry in prairie voles (Microtus ochrogaster in relation to population density, season, and natal social environment. Behav Ecol Sociobiol 32:293-302.
75. McGuire B, Novak M. 1984. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim Behav 32:1132-1141.
76. Mermelstein PG, Becker JB. 1995. Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior. Behav Neurosci 109:354-365.
77. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG. 1998. Dopamine receptors: From structure to function. Physiol Rev 78:189-225.
78. Nelson RJ, Chiavegatto S. 2001. Molecular basis of aggression. Trends Neurosci 24:713-719.
79. Newman SW. 1999. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 29:242-257.
80. Oliveras D, Novak M. 1986. A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster. Anim Behav 34:519-526.
81. Ormerod BK, Galea LA. 2001. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: A possible regulatory role for estradiol. Neuroscience 102:369-379.
82. Pedersen CA, Ascher JA, Monroe YL, Prange AJ, Jr. 1982. Oxytocin induces maternal behavior in virgin female rats. Science 216:648-650.
83. Pedersen CA, Prange AJ, Jr. 1979. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 76:6661-6665.
84. Pfaus JG, Damsma G, Nomikos GG, Wenkstern DG, Blaha CD, Phillips AG, Fibiger HC. 1990. Sexual behavior enhances central dopamine transmission in the male rat. Brain Res 530:345-348.
85. Pfaus JG, Damsma G, Wenkstern D, Fibiger HC. 1995. Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats. Brain Res 693:21-30.
86. Pfaus JG, Kippin TE, Centeno S. 2001. Conditioning and sexual behavior: A review. Horm Behav 40:291-321.
87. Pitkow LJ, Sharer CA, Ren X, Insel TR, Terwilliger EF, Young LJ. 2001. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J Neurosci 21:7392-7396.
88. Ranson RM. 2003. The field vole (Microtus) as a laboratory animal. J Anim Ecol 3:70-76.
89. Richmond ME, Conaway CH. 1969. Induced ovulation and oestrus in Microtus orchrogaster. J Reprod Fertil Suppl 6:357-376.
90. Rissman EF, Wersinger SR, Fugger HN, Foster TC. 1999. Sex with knockout models: Behavioral studies of estrogen receptor alpha. Brain Res 835:80-90.
91. Roberts RL, Cushing BS, Carter CS. 1998a. Intraspecific variation in the induction of female sexual receptivity in prairie voles. Physiol Behav 64:209-212.
92. Roberts RL, Williams JR, Wang AK, Carter CS. 1998b. Cooperative breeding and monogamy in prairie voles: Influence of sire and geographical variation. Anim Behav 55:1131-1140.
93. Robinson DL, Phillips PE, Budygin EA, Trafton BJ, Garris PA, Wightman RM. 2001. Sub-second changes in accumbal dopamine during sexual behavior in male rats. Neuroreport 12:2549-2552.
94. Schultz W. 1997. Dopamine neurons and their role in reward mechanisms. Curr Opin Neurobiol 7:191-197.
95. Self DW, Nestler EJ. 1998. Relapse to drug-seeking: Neural and molecular mechanisms. Drug Alcohol Depend 51:49-60.
96. Shapiro LE, Insel TR. 1990. Infant's response to social separation reflects adult differences in affiliative behavior: A comparative developmental study in prairie and montane voles. Dev Psychobiol 23:375-393.
97. Smith MT, Pencea V, Wang ZX, Luskin MB, Insel TR. 2001. Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 39:11-21.
98. Stern JM, Lonstein JS. 2001. Neural mediation of nursing and related maternal behaviors. Prog Brain Res 133:263-278.
99. Tamarin R, ed. 1985. Biology of New World Microtus. Am Soc Mamm Spec Pub 8.
100. Taymans SE, DeVries AC, DeVries MB, Nelson RJ, Friedman TC, Castro M, Detera-Wadleigh S, Carter CS, Chrousos GP. 1997. The hypothalamic-pituitary-adrenal axis of prairie voles (Microtus ochrogaster): Evidence for target tissue glucocorticoid resistance. Gen Comp Endocrinol 106:48-61.
101. Thomas JA, Birney EC. 1979. Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav Ecol Sociobiol 5:171-186.
102. van Leeuwen FW, Caffe AR, De Vries GJ. 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.
103. Volkmar FR. 2001. Pharmacological interventions in autism: Theoretical and practical issues. J Clin Child Psychol 30:80-87.
104. Wang ZX. 1995. Species differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Behav Neurosci 109:305-311.
105. Wang ZX, De Vries GJ. 1993. Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles ( Microtus ochrogaster). Brain Res 631:156-160.
106. Wang ZX, Ferris CF, De Vries GJ. 1994a. Role of septal vasopressin innervation in paternal behavior in prairie voles ( Microtus ochrogaster). Proc Natl Acad Sci U S A 91:400-404.
107. Wang ZX, Hulihan TJ, Insel TR. 1997a. Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Res 767:321-332.
108. Wang ZX, Liu Y, Young LJ, Insel TR. 2000. Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent. J Neuroendocrinol 12:111-120.
109. Wang ZX, Novak M. 1992. Influence of the social environment on parental behavior and pup development of meadow voles (Microtus pennsylvanicus) and prairie voles (M. ochrogaster). J Comp Psychol 106:163-171.
110. Wang ZX, Smith W, Major DE, De Vries GJ. 1994b. 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 650:212-218.
111. Wang ZX, Young LJ. 1997. Ontogeny of oxytocin and vasopressin receptor binding in the lateral septum in prairie ad montane voles, Brain Res Dev Brain Res 104:191-195.
112. Wang ZX, Young LJ, De Vries GJ, Insel TR. 1998. Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 119:483-499.
113. Wang ZX, Young LJ, Liu Y, Insel TR. 1997b. Species differences in vasopressin receptor binding are evident early in development: Comparative anatomic studies in prairie and montane voles. J Comp Neurol 378:535-546.
114. Wang ZX, Yu G, Cascio C, Liu Y, Gingrich B, Insel TR. 1999. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): A mechanism for pair bonding? Behav Neurosci 113:602-611.
115. Wang ZX, Zhou L, Hulihan TJ, Insel TR. 1996. Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: A quantitative comparative study. J Comp Neurol 366:726-737.
116. Whitnall MH. 1993. Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog Neurobiol 40:573-629.
117. Williams JR, Catania KC, Carter CS. 1992. Development of partner preferences in female prairie voles (Microtus ochrogaster : The role of social and sexual experience. Horm Behav 26:339-349.
118. Williams JR, Insel TR, Harbaugh CR, Carter CS. 1994. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6:247-250.
119. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR. 1993. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545-548.
120. Winslow JT, Insel TR. 1991. The infant rat separation paradigm: A novel test for novel anxiolytics. Trends Pharmacol Sci 12:402-404.
121. Wise RA. 1996. Neurobiology of addiction. Curr Opin Neurobiol 6:243-251.
122. Wise RA, Rompre PP. 1989. Brain dopamine and reward. Annu Rev Psych 40:191-225.
123. Witt DM, Carter CS, Insel TR. 1991. Oxytocin receptor binding in female prairie voles: Endogenous and exogenous oestradiol stimulation. J Neuroendocrinol 3:155-161.
124. Young LJ, Huot B, Nilsen R, Wang ZX, Insel TR. 1996. Species differences in central oxytocin receptor gene expression: Comparative analysis of promoter sequences. J Neuroendocrinol 8:777-783.
125. Young LJ, Lim MM, Gingrich B, Insel TR. 2001. Cellular mechanisms of social attachment. Horm Behav 40:133-138.
126. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR. 1999. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400:766-768.
127. Young LJ, Wang ZX, Insel TR. 1998. Neuroendocrine bases of monogamy. Trends Neurosci 21:71-75.
128. Young LJ, Winslow JT, Nilsen R, Insel TR. 1997. Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: Behavioral consequences. Behav Neurosci 111:599-605.