Central oxytocin, vasopressin, and corticotropin-releasing factor receptor densities in the basal forebrain predict isolation potentiated startle in rats

Journal of Neuroscience

Volumn 25, Issue 49, 2005, Pages 11479-11488

  Nair, Hemanth P ^a   Gutman, Alisa R ^a   Davis, Michael ^a   Young, Larry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anxiety; Corticotropin releasing factor; Oxytocin; Social support; Startle; Vasopressin

Indexed keywords

CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; NEUROPEPTIDE; OXYTOCIN; OXYTOCIN RECEPTOR; VASOPRESSIN; VASOPRESSIN V1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BINDING SITE; CONTROLLED STUDY; CORRELATION ANALYSIS; FOREBRAIN; HORMONAL REGULATION; MALE; MULTIPLE REGRESSION; MULTIVARIATE ANALYSIS; NONHUMAN; NUCLEUS ACCUMBENS; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; RAT; RECEPTOR DENSITY; REGRESSION ANALYSIS; STARTLE REFLEX; STATISTICAL SIGNIFICANCE; STRIA TERMINALIS;

ACOUSTIC STIMULATION; ANIMALS; MALE; PREDICTIVE VALUE OF TESTS; PROSENCEPHALON; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, OXYTOCIN; RECEPTORS, VASOPRESSIN; SOCIAL ISOLATION; STARTLE REACTION;

EID: 30544433895     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2524-05.2005     Document Type: Article

References (74)

1. Andrade CS, Guimaraes FS (2003) Anxiolytic-like effect of group housing on stress-induced behavior in rats. Depress Anxiety 18:149-152.
2. Barberis C, Tribollet E (1996) Vasopressin and oxytocin receptors in the central nervous system. Crit Rev Neurobiol 10:119-154.
3. Barberis C, Balestre M-N, Jard S, Tribollet E, Arsenijevic Y, Dreifuss JJ, Bankowski K, Manning M, Chan WY, Schlosser SS, Holsboer F, Elands J (1995) Characterization of a novel, linear radioiodinated vasopressin antagonist: an excellent radioligand for vasopressin V1a receptors. Neuroendocrinology 62:135-146.
4. Berkman LF (1995) The role of social relations in health promotion. Psychosom Med 57:245-254.
5. Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29:483-493.
6. Cassella JV, DavisM (1986) The design and calibration of a startle measurement system. Physiol Behav 36:377-383.
7. Champagne F, Diorio J, Sharma S, Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98:12736-12741.
8. De Boer SF, Koolhaas JM (2003) Defensive burying in rodents: ethology, neurobiology and psychopharmacology. Eur J Pharmacol 463:145-161.
9. de Olmos JS, Heimer L (1999) The concepts of the ventral striatopallidal system and extended amygdala. New York: The New York Academy of Sciences.
10. Dunn AJ, Berridge CW (1990) Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses? Brain Res Brain Res Rev 15:71-100.
11. Everts HG, Koolhaas JM (1999) Differential modulation of lateral septal vasopressin receptor blockade in spatial learning, social recognition, and anxiety-related behaviors in rats. Behav Brain Res 99:7-16.
12. Everts HG, De Ruiter AJ, Koolhaas JM (1997) Differential lateral septal vasopressin in wild-type rats: correlation with aggression. Horm Behav 31:136-144.
13. Francis DD, Young LJ, Meaney MJ, Insel TR (2002) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349-353.
14. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB (1997) Hypothalamic paraventricular nucleus, oxytocin, and maternal aggression in rats. Ann NY Acad Sci 807:606-609.
15. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB (1998) Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol Behav 63:351-359.
16. Goodson JL, Bass AH (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Brain Res Rev 35:246-265.
17. 125I-Tyro-sauvagine: a novel high affinity radioligand for the pharmacological and biochemical study of human corticotropinreleasing factor 2 alpha receptors. Mol Pharmacol 50:679-686.
18. Haller J, Halasz J (1999) Mild social stress abolishes the effects of isolation on anxiety and chlordiazepoxide reactivity. Psychopharmacology (Berl) 144:311-315.
19. Haller J, Leveleki C, Baranyi J, Mikics E, Bakos N (2003) Stress, social avoidance and anxiolytics: a potential model of stress-induced anxiety. Behav Pharmacol 14:439-446.
20. 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.
21. Hammock EA, Young LJ (2004) Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol Biol Evol 21:1057-1063.
22. Hammock EA, Young LJ (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630-1634.
23. Harmon AC, Huhman KL, Moore TO, Albers HE (2002) Oxytocin inhibits aggression in female Syrian hamsters. J Neuroendocrinol 14:963-969.
24. Hatch AM, Wiberg GS, Grice HC (1963) Long-term isolation stress in rats. Science 142:507.
25. Horwitz B, Soncrant TT, Haxby JV (1992) Covariance analysis of functional interactions in the brain using metabolic and blood flow data. In: Advances in metabolic mapping techniques for brain imaging of behavioral and learning functions (Gonzalez-Lima F, Finkenstadt T, Sheich H, eds). Boston: Kluwer Academic.
26. Insel TR (1992) Oxytocin - a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 17:3-35.
27. Insel TR, Shapiro LE (1992) Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci USA 89:5981-5985.
28. Insel TR, Gelhard R, Shapiro LE (1991) The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience 43:623-630.
29. Koolhaas JM, Everts H, de Ruiter AJ, de Boer SF, Bohus B (1998) Coping with stress in rats and mice: differential peptidergic modulation of the amygdala-lateral septum complex. Prog Brain Res 119:437-448.
30. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673-676.
31. Lee Y, DavisM (1997) Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropinreleasing hormone on the acoustic startle reflex. J Neurosci 17:6434-6446.
32. Liang KC, Melia KR, Miserendino MJ, Falls WA, Campeau S, Davis M (1992) Corticotropin-releasing factor: long-lasting facilitation of the acoustic startle reflex. J Neurosci 12:2303-2312.
33. Liebsch G, Wotjak CT, Landgraf R, Engelmann M (1996) Septal vasopressin modulates anxiety-related behaviour in rats. Neurosci Lett 217:101-104.
34. Lim MM, Nair HP, Young LJ (2005) Species and sex differences in brain distribution of CRF receptor subtypes 1 and 2 in monogamous and promiscuous voles species. J Comp Neurol 487:75-92.
35. Lubin DA, Elliott JC, Black MC, Johns JM (2003) An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav Neurosci 117:195-201.
36. McIntosh AR, Lobaugh NJ (2004) Partial least squares analysis of neuroimaging data: applications and advances. NeuroImage 23 [Suppl 1]:S250-S263.
37. McIntosh AR, Rajah MN, Lobaugh NJ (1999) Interactions of prefrontal cortex in relation to awareness in sensory learning. Science 284:1531-1533.
38. Nair HP, Gonzalez-Lima F (2003) Large-scale networks in learning analyzed with partial least squares. In: Exploratory analysis and data modeling in functional neuroimaging (Sommer FT, Wichert A, eds). Cambridge, MA: MIT.
39. Nair HP, Berndt JD, Barrett D, Gonzalez-Lima F (2001) Maturation of extinction behavior in infant rats: large-scale regional interactions with medial prefrontal cortex, orbitofrontal cortex, and anterior cingulate cortex. J Neurosci 21:4400-4407.
40. Nemeroff CB (1988) The role of corticotropin-releasing factor in the pathogenesis of major depression. Pharmacopsychiatry 21:76-82.
41. Neumann ID, Torner L, Wigger A (2000) Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience 95:567-575.
42. Odendaal JS, Meintjes RA (2003) Neurophysiological correlates of affiliative behaviour between humans and dogs. Vet J 165:296-301.
43. Petersson KM, Nichols TE, Poline JB, Holmes AP (1999) Statistical limitations in functional neuroimaging. I. Non-inferential methods and statistical models. Philos Trans R Soc Lond B Biol Sci 354:1239-1260.
44. Phelps SM, Young LJ (2003) Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. J Comp Neurol 466:564-576.
45. Phelps SM, Sharer CA, Young LJ (2002) Individual differences in vasopressin V1a receptors, promoter structure, and social behavior. Soc Neurosci Abstr 28:89.1.
46. 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.
47. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME, Kim JY, Goumnerova LC, Black PM, Lau C, Allen JC, Zagzag D, Olson JM, Curran T, Wetmore C, Biegel JA, Poggio T, Mukherjee S, Rifkin R, Califano A, et al. (2002) Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415:436-442.
48. Primus RJ, Yevich E, Baltazar C, Gallager DW (1997) Autoradiographic localization of CRF1 and CRF2 binding sites in adult rat brain. Neuropsychopharmacology 17:308-316.
49. Ragnauth AK, Devidze N, Moy V, Finley K, Goodwillie A, Kow LM, Muglia LJ, Pfaff DW (2005) Female oxytocin gene-knockout mice, in a seminatural environment, display exaggerated aggressive behavior. Genes Brain Behav 4:229-239.
50. Rosner B (2006) Fundamentals of biostatistics, Ed 6. Belmont, CA: Thomson.
51. Ruis MA, te Brake JH, Buwalda B, De Boer SF, Meerlo P, Korte SM, Blokhuis HJ, Koolhaas JM (1999) Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 24:285-300.
52. Sanchez MM, Young LJ, Plotsky PM, Insel TR (1999) Autoradiographic and in situ hybridization localization of corticotropin-releasing factor 1 and 2 receptors in nonhuman primate brain. J Comp Neurol 408:365-377.
53. Schulz DW, Mansbach RS, Sprouse J, Braselton JP, Collins J, Corman M, Dunaiskis A, Faraci S, Schmidt AW, Seeger T, Seymour P, Tingley III FD, Winston EN, Chen YL, Heym J (1996) CP-154,526: a potent and selective nonpeptide antagonist of corticotropin releasing factor receptors. Proc Natl Acad Sci USA 93:10477-10482.
54. Sharp JL, Zammit TG, Azar TA, Lawson DM (2002) Stress-like responses to common procedures in male rats housed alone or with other rats. Contemp Top Lab Anim Sci 41:8-14.
55. Sommer FT, Wichert A, eds (2003) Large-scale networks in learning analyzed with partial least squares. Cambridge, MA: MIT.
56. Staiger JF, Nurnberger F (1989) Pattern of afferents to the lateral septum in the guinea pig. Cell Tissue Res 257:471-490.
57. Stern JA, Winokur G, Eisenstein A, Taylor R, Sly M (1960) The effect of group vs. individual housing on behaviour and physiological responses to stress in the ablino rat. J Psychosom Res 4:185-190.
58. Stevens J (1996) Applied multivariate statistics for the social sciences, Ed 3. Mahwah, NJ: Erlbaum.
59. Swerdlow NR, Geyer MA, Vale WW, Koob GF (1986) Corticotropinreleasing factor potentiates acoustic startle in rats: blockade by chlordiazepoxide. Psychopharmacology (Berl) 88:147-152.
60. Uchino BN, Garvey TS (1997) The availability of social support reduces cardiovascular reactivity to acute psychological stress. J Behav Med 20:15-27.
61. Walker DL, Davis M (1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17:9375-9383.
62. Wang Z, Young LJ (1997) Ontogeny of oxytocin and vasopressin receptor binding in the lateral septum in prairie and montane voles. Brain Res Dev Brain Res 104:191-195.
63. Wang Z, 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.
64. Wang Z, Young LJ, Liu Y, Insel TR (1997) 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.
65. Watanabe M, Irie M, Kobayashi F (2004) Relationship between effortreward imbalance, low social support and depressive state among Japanese male workers. J Occup Health 46:78-81.
66. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302:296-299.
67. Wigger A, Sanchez MM, Mathys KC, Ebner K, Frank E, Liu D, Kresse A, Neumann ID, Holsboer F, Plotsky PM, Landgraf R (2004) Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29:1-14.
68. Windle RJ, Shanks N, Lightman SL, Ingram CD (1997) Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 138:2829-2834.
69. 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.
70. Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048-1054.
71. 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.
72. Young LJ, Wang Z, Insel TR (1998a) Neuroendocrine bases of monogamy. Trends Neurosci 21:71-75.
73. Young III WS, Shepard E, DeVries AC, Zimmer A, LaMarca ME, Ginns EI, Amico J, Nelson RJ, Hennighausen L, Wagner KU (1998b) Targeted reduction of oxytocin expression provides insights into its physiological roles. Adv Exp Med Biol 449:231-240.
74. 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.