Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds

Nature Neuroscience

Volumn 9, Issue 1, 2006, Pages 133-139

  Aragona, Brandon J ^a   Liu, Yan ^a   Yu, Y Joy ^a   Curtis, J Thomas ^a   Detwiler, Jacqueline M ^a   Insel, Thomas R ^b   Wang, Zuoxin ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DOPAMINE RECEPTOR BLOCKING; DOPAMINERGIC SYSTEM; DOPAMINERGIC TRANSMISSION; FEMALE; MALE; MONOGAMY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SOCIAL INTERACTION; SOCIAL STRUCTURE; VOLE;

(R)-2,3,4,5-TETRAHYDRO-8-CHLORO-3-METHYL-5-PHENYL-1H-3-BENZAZEPIN-7-OL; 2,3,4,5-TETRAHYDRO-7,8-DIHYDROXY-1-PHENYL-1H-3-BENZAZEPINE; ANIMALS; ARVICOLINAE; AUTORADIOGRAPHY; DOPAMINE; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; FEMALE; MALE; NUCLEUS ACCUMBENS; PAIR BOND; QUINPIROLE; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; SALICYLAMIDES; SEXUAL BEHAVIOR, ANIMAL;

EID: 29444436968     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1613     Document Type: Article

References (50)

1. 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. 8, 189-194 (1981).
2. Getz, L.L., McGuire, B., Pizzuto, T., Hofmann, J. & Frase, B. Social organization of the prairie vole, Microtus ochrogaster. J. Mammal. 74, 44-58 (1993).
3. Carter, C.S., DeVries, A.C. & Getz, L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 19, 303-314 (1995).
4. Insel, T.R. & Young, L.J. The neurobiology of attachment. Nat. Rev. Neurosci. 2, 129-136 (2001).
5. Young, L.J. & Wang, Z. The neurobiology of pair bonding. Nat. Neurosci. 7, 1048-1054 (2004).
6. 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 365, 545-548 (1993).
7. Wang, Z. et al. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): a mechanism for pair bonding? Behav. Neurosci. 113, 602-611 (1999).
8. 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. 114, 173-183 (2000).
9. 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. 23, 3483-3490 (2003).
10. Liu, Y. & Wang, Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121, 537-544 (2003).
11. Lim, M.M. & Young, L.J. Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125, 35-45 (2004).
12. Lim, M.M. et al. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754-757 (2004).
13. 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. 767, 321-332 (1997).
14. Ikemoto, S. & Panksepp, J. 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 (1999).
15. Horvitz, J.C. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96, 651-656 (2000).
16. Salamone, J.D. & Correa, M. Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav. Brain Res. 137, 3-25 (2002).
17. Di Chiara, G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res. 137, 75-114 (2002).
18. Berridge, K.C. & Robinson, T.E. Parsing reward. Trends Neurosci. 26, 507-513 (2003).
19. Nestler, E.J. Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol. Sci. 25, 210-218 (2004).
20. Kelley, A.E. Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44, 161-179 (2004).
21. Wise, R.A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494 (2004).
22. Carelli, R.M. & Wightman, R.M. Functional microcircuitry in the accumbens underlying drug addiction: insights from real-time signaling during behavior. Curr. Opin. Neurobiol. 14, 763-768 (2004).
23. Williams, J.R., Catania, K.C. & Carter, C.S. Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm. Behav. 26, 339-349 (1992).
24. Zahm, D.S. An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci. Biobehav. Rev. 24, 85-105 (2000).
25. Kalivas, P.W. & McFarland, K. Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl.) 168, 44-56 (2003).
26. Roitman, M.F., Stuber, G.D., Phillips, P.E., Wightman, R.M. & Carelli, R.M. Dopamine operates as a subsecond modulator of food seeking. J. Neurosci. 24, 1265-1271 (2004).
27. Phillips, P.E., Stuber, G.D., Heien, M.L., Wightman, R.M. & Carelli, R.M. Subsecond dopamine release promotes cocaine seeking. Nature 422, 614-618 (2003).
28. Cardinal, R.N. & Everitt, B.J. Neural and psychological mechanisms underlying appetitive learning: links to drug addiction. Curr. Opin. Neurobiol. 14, 156-162 (2004).
29. Reynolds, S.M. & Berridge, K.C. Glutamate motivational ensembles in nucleus accumbens: rostrocaudal shell gradients of fear and feeding. Eur. J. Neurosci. 17, 2187-2200 (2003).
30. Pizzuto, T. & Getz, L.L. Female prairie voles (Microtus ochrogaster) fail to form a new pair after loss of mate. Behav. Processes 43, 79-86 (1998).
31. Dewsbury, D.A. The comparative psychology of monogamy. Nebr. Symp. Motiv. 35, 1-50 (1987).
32. Everitt, B.J. Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci. Biobehav. Rev. 14, 217-232 (1990).
33. Schultz, W. Multiple reward signals in the brain. Nat. Rev. Neurosci. 1, 199-207 (2000).
34. 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 97, 459-469 (2002).
35. 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 271, 1586-1589 (1996).
36. Ikemoto, S., Glazier, B.S., Murphy, J.M. & McBride, W.J. Role of dopamine D1 and D2 receptors in the nucleus accumbens in mediating reward. J. Neurosci. 17, 8580-8587 (1997).
37. Missale, C., Nash, S.R., Robinson, S.W., Jaber, M. & Caron, M.G. Dopamine receptors: from structure to function. Physiol. Rev. 78, 189-225 (1998).
38. Eyny, Y.S. & Horvitz, J.C. Opposing roles of D1 and D2 receptors in appetitive conditioning. J. Neurosci. 23, 1584-1587 (2003).
39. Kebabian, J.W. & Calne, D.B. Multiple receptors for dopamine. Nature 277, 93-96 (1979).
40. Kelley, A.E. & Berridge, K.C. The neuroscience of natural rewards: relevance to addictive drugs. J. Neurosci. 22, 3306-3311 (2002).
41. Ungless, M.A. Dopamine: the salient issue. Trends Neurosci. 27, 702-706 (2004).
42. Insel, T.R. Is social attachment an addictive disorder? Physiol. Behav. 79, 351-357 (2003).
43. Champagne, F.A. et al. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J. Neurosci. 24, 4113-4123 (2004).
44. Robinson, D.L., Heien, M.L. & Wightman, R.M. Frequency of dopamine concentration transients increases in dorsal and ventral striatum of male rats during introduction of conspecifics. J. Neurosci. 22, 10477-10486 (2002).
45. Berke, J.D. & Hyman, S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25, 515-532 (2000).
46. Schuiling, G.A. The benefit and the doubt: why monogamy? J. Psychosom. Obstet. Gynaecol. 24, 55-61 (2003).
47. Insel, T.R. & Shapiro, L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. USA 89, 5981-5985 (1992).
48. Insel, T.R., Wang, Z.X. & Ferris, C.F. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14, 5381-5392 (1994).
49. Wang, Z., Young, L.J., Liu, Y. & Insel, T.R. 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 (1997).
50. Cho, M.M., DeVries, A.C., Williams, J.R. & Carter, C.S. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 113, 1071-1079 (1999).