Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole

Neuroscience

Volumn 125, Issue 1, 2004, Pages 35-45

  Lim, M M ^a   Young, L J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AAV; AAV lacZ; AAV V1a; Adeno associated viral vector containing lacZ gene; Adeno associated viral vector containing V1a gene; Adeno associated virus; Affiliation; AVP; Medial amygdala; Mediodorsal thalamus; Reward; V1a receptor; Ventral pallidum

Indexed keywords

ARGIPRESSIN; PROTEIN FOS; VASOPRESSIN ANTAGONIST; VASOPRESSIN V1 RECEPTOR; VIRUS VECTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TRANSFER; GLOBUS PALLIDUS; LIMBIC CORTEX; MALE; MATING; MONOGAMY; NERVE CELL NETWORK; NERVE TRACT; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; PRAIRIE; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; REWARD; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; STRIATE CORTEX; THALAMUS DORSOMEDIAL NUCLEUS; VOLE;

ANIMALS; ARVICOLINAE; BRAIN; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NEURAL PATHWAYS; PAIR BOND; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, VASOPRESSIN; SYNAPTIC TRANSMISSION; VASOPRESSINS;

EID: 1642421279     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.12.008     Document Type: Article

References (47)

1. 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. 23:2003;3483-3490.
2. Baum M.J., Everitt B.J. Increased expression of c-fos in the medial preoptic area after mating in male rats Role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience. 50:1992;627-646.
3. Bester-Meredith J.K., Young L.J., Marler C.A. Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav. 36:1999;25-38.
4. Bielajew C., Fouriezos G. Post-stimulation excitability of mediodorsal thalamic self-stimulation. Behav Brain Res. 17:1985;97-101.
5. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy The prairie vole model. Neurosci Biobehav Rev. 19:1995;303-314.
6. 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. 113:1999;1071-1079.
7. Clayton D.F. The genomic action potential. Neurobiol Learn Mem. 74:2000;185-216.
8. Coolen L.M., Peters H.J., Veening J.G. Distribution of Fos immunoreactivity following mating versus anogenital investigation in the male rat brain. Neuroscience. 77:1997;1151-1161.
9. Curtis J.T., Wang Z. Forebrain c-fos expression under conditions conducive to pair bonding in female prairie voles (Microtus ochrogaster). Physiol Behav. 80:2003;95-101.
10. Cushing B.S., Mogekwu N., Le W.W., Hoffman G.E., Carter C.S. Cohabitation induced Fos immunoreactivity in the monogamous prairie vole. Brain Res. 965:2003;203-211.
11. De Vries G.J., Buijs R.M. The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res. 273:1983;307-317.
12. DeVries A.C., DeVries M.B., Taymans S.E., Carter C.S. The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc Natl Acad Sci USA. 93:1996;11980-11984.
13. Engelmann M., Wotjak C.T., Neumann I., Ludwig M., Landgraf R. Behavioral consequences of intracerebral vasopressin and oxytocin Focus on learning and memory. Neurosci Biobehav Rev. 20:1996;341-358.
14. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci. 21:2001;8278-8285.
15. Fernandez-Fewell G.D., Meredith M. c-fos expression in vomeronasal pathways of mated or pheromone-stimulated male golden hamsters Contributions from vomeronasal sensory input and expression related to mating performance. J Neurosci. 14:1994;3643-3654.
16. Gill C.J., Wersinger S.R., Veney S.L., Rissman E.F. Induction of fos-like immunoreactivity in musk shrews after mating. Brain Res. 811:1998;21-28.
17. 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. 114:2000;173-183.
18. Gong W., Neill D., Justice J.B. Jr. Conditioned place preference and locomotor activation produced by injection of psychostimulants into ventral pallidum. Brain Res. 707:1996;64-74.
19. Gong W., Neill D., Justice J.B. Jr. 6-Hydroxydopamine lesion of ventral pallidum blocks acquisition of place preference conditioning to cocaine. Brain Res. 754:1997;103-112.
20. Groenewegen H.J., Berendse H.W., Haber S.N. Organization of the output of the ventral striatopallidal system in the rat Ventral pallidal efferents. Neuroscience. 57:1993;113-142.
21. Insel T.R., Hulihan T.J. A gender-specific mechanism for pair bonding Oxytocin and partner preference formation in monogamous voles. Behav Neurosci. 109:1995;782-789.
22. Insel T.R., Young L.J. The neurobiology of attachment. Nat Rev Neurosci. 2:2001;129-136.
23. Insel T.R., Wang Z.X., Ferris C.F. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci. 14:1994;5381-5392.
24. Insel T.R., Preston S., Winslow J.T. Mating in the monogamous male Behavioral consequences. Physiol Behav. 57:1995;615-627.
25. Kalivas P.W., Churchill L., Romanides A. Involvement of the pallidal-thalamocortical circuit in adaptive behavior. Ann NY Acad Sci. 877:1999;64-70.
26. Landgraf R., Frank E., Aldag J.M., Neumann I.D., Sharer C.A., Ren X., Terwilliger E.F., Niwa M., Wigger A., Young L.J. Viral vector-mediated gene transfer of the vole V1a vasopressin receptor in the rat septum Improved social discrimination and active social behaviour. Eur J Neurosci. 18:2003;403-411.
27. Lim MM, Murphy AZ, Young LJ (2004a) Ventral striato-pallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster). J Comp Neurol 468:555-570.
28. Lim MM, Hammock EAD, Young LJ (2004b) A method for acetylcholinesterase staining of brain sections previously processed for receptor autoradiography. Biotechnic and Histochemistry, in press.
29. Liu Y., Curtis J.T., Wang Z. Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav Neurosci. 115:2001;910-919.
30. Meisel R.L., Sachs B.D. The physiology of male sexual behavior. Knobil E., Neill J.D. The physiology of reproduction. 2nd ed. 1994;Raven Press, New York.
31. Michael R.P., Clancy A.N., Zumpe D. Effects of mating on c-fos expression in the brains of male macaques. Physiol Behav. 66:1999;591-597.
32. Mogenson G.J., Ciriello J., Garland J., Wu M. Ventral pallidum projections to mediodorsal nucleus of the thalamus An anatomical and electrophysiological investigation in the rat. Brain Res. 404:1987;221-230.
33. Newman S.W., Parfitt D.B., Kollack-Walker S. Mating-induced c-fos expression patterns complement and supplement observations after lesions in the male Syrian hamster brain. Ann NY Acad Sci. 807:1997;239-259.
34. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 4th ed :1998;Academic Press, San Diego, CA.
35. Phelps SM, Young LJ (2003) Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochragaster): patterns of variation and covariation. J Comp Neurol 466(4):564-576.
36. 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. 21:2001;7392-7396.
37. Reyna-Neyra A., Camacho-Arroyo I., Cerbon M.A., Gonzalez-Mariscal G. Mating modifies c-fos expression in the brain of male and female rabbits. Neurosci Lett. 284:2000;1-4.
38. Sagar S.M., Sharp F.R., Curran T. Expression of c-fos protein in brain Metabolic mapping at the cellular level. Science. 240:1988;1328-1331.
39. 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. 378:1997;535-546.
40. Wang Z., Toloczko D., Young L.J., Moody K., Newman J.D., Insel T.R. Vasopressin in the forebrain of common marmosets (Callithrix jacchus) Studies with in situ hybridization, immunocytochemistry and receptor autoradiography. Brain Res. 768:1997;147-156.
41. 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. 26:1992;339-349.
42. 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. 365:1993;545-548.
43. Young L.J., Frank A. Beach Award Oxytocin and vasopressin receptors and species-typical social behaviors. Horm Behav. 36:1999;212-221.
44. Young L.J., Toloczko D., Insel T.R. Localization of vasopressin (V1a) receptor binding and mRNA in the rhesus monkey brain. J Neuroendocrinol. 11:1999;291-297.
45. 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. 111:1997;599-605.
46. Young L.J., Lim M.M., Gingrich B., Insel T.R. Cellular mechanisms of social attachment. Horm Behav. 40:2001;133-138.
47. Zahm D.S., Heimer L. Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol. 302:1990;437-446.