Developmental effects of oxytocin on neural activation and neuropeptide release in response to social stimuli

Hormones and Behavior

Volumn 49, Issue 2, 2006, Pages 206-214

  Kramer, Kristin M ^a,b   Choe, Christina ^a   Carter, C Sue ^a   Cushing, Bruce S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF MEMPHIS   (United States)

Author keywords

c Fos; Central amygdala; Development; Microtus; Monogamy; Neural activation; Oxytocin; Social bonds; Vasopressin; Vole

Indexed keywords

ARGIPRESTOCIN; ESTROGEN RECEPTOR ALPHA; NEUROPEPTIDE; OXYTOCIN; PROTEIN C FOS; VASOPRESSIN RECEPTOR;

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BLOOD ANALYSIS; COITUS; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HETEROSEXUALITY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MONOGAMY; NERVE CELL; NERVE CONDUCTION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; STIMULUS RESPONSE; VOLE;

AMYGDALA; ANIMALS; ANIMALS, NEWBORN; ARGININE VASOPRESSIN; ARVICOLINAE; BRAIN CHEMISTRY; FEMALE; GENE EXPRESSION; GENES, FOS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; NEUROPEPTIDES; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; SEX CHARACTERISTICS; SOCIAL ENVIRONMENT; SUPRAOPTIC NUCLEUS;

EID: 31444443543     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2005.07.001     Document Type: Article

References (53)

1. J.A. Amico, R.C. Mantella, R.R. Vollmer, and X. Li Anxiety and stress responses in female oxytocin deficient mice J. Neurosci. 16 2004 319 324
2. T.L. Bale, A.M. Davis, A.P. Auger, D.M. Dorsa, and M.M. McCarthy CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior J. Neurosci. 21 2001 2546 2552
3. K.L. Bales, and C.S. Carter Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster) Horm. Behav. 44 2003 178 184
4. K.L. Bales, L.A. Pfeifer, and C.S. Carter Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles Dev. Psychobiol. 44 2004 123 131
5. W.A. Banks, and A.J. Kastin Permeability and vascularity of the blood-brain barrier to neuropeptides: the case for penetration Psychoneuroendocrinology 10 1985 385 399
6. P.C. Barber, and G. Raisman An autoradiographic investigation of the projection of the vomeronasal organ to the accessory olfactory bulb in the mouse Brain Res. 81 1974 21 30
7. S.C. Bressler, and M.J. Baum Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation Neuroscience 71 1996 1063 1072
8. C.S. Carter Developmental consequences of oxytocin Physiol. Behav. 79 2003 383 397
9. C.S. Carter, D.M. Witt, J. Schneider, Z.L. Harris, and D. Volkening Male stimuli are necessary for female sexual behavior and uterine growth in prairie voles (Microtus ochrogaster) Horm. Behav. 21 1987 74 82
10. J.T. Curtis, and Z. Wang Forebrain c-fos expression under conditions conducive to pair bonding in female prairie voles (Microtus ochrogaster) Physiol. Behav. 80 2003 95 101
11. B.S. Cushing, and C.S. Carter Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles Horm. Behav. 37 2000 49 56
12. B.S. Cushing, D. Klein, G.E. Hoffman, C.S. Carter, W.W. Le, and G.J. De Vries Comparison of fixation techniques: immersion versus perfusion Horm. Behav. 39 2001 329
13. B.S. Cushing, N. Mogekwu, W.W. Le, G.E. Hoffman, and C.S. Carter Cohabitation induced Fos immunoreactivity in the monogamous prairie vole Brain Res. 965 2003 203 211
14. B.S. Cushing, Y. Yamamoto, G.E. Hoffman, and C.S. Carter Central expression of c-Fos in neonatal male and female prairie voles in response to treatment with oxytocin Dev. Brain Res. 143 2003 129 136
15. B.S. Cushing, K. Levine, and N.L. Cushing Neonatal manipulations of oxytocin affect reproductive behavior and reproductive success of adult female prairie voles (Microtus ochrogaster) Horm. Behav. 47 2005 22 28
16. A.C. DeVries, and C.S. Carter Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster) Can. J. Zool. 77 1999 885 889
17. D.A. Dewsbury Role of male proximity in pregnancy maintenance in prairie voles, Microtus ochrogaster Physiol. Behav. 57 1995 827 829
18. D.E. Dluzen, V.D. Ramirez, C.S. Carter, and L.L. Getz Male vole urine changes luteinizing hormone-releasing hormone and norepinephrine in female olfactory bulb Science 212 1981 573 575
19. C.A. Dudley, G. Rajendren, and R.L. Moss Induction of fos immunoreactivity in central accessory olfactory structures of the female rat following exposure to conspecific males Mol. Cell Neurosci. 3 1992 360 369
20. G.D. Fernandez-Fewell, and M. Meredith c-fos expression in vomeronasal pathways of mated and pheromone-stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance J. Neurosci. 14 1994 3643 3654
21. J.M. Fiber, P. Adames, and J.M. Swann Pheromones induce c-fos in limbic areas regulating male hamster mating behavior NeuroReport 4 1993 871 874
22. D.D. Francis, L.J. Young, M.J. Meaney, and T.R. Insel Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences J. Neuroendocrinol. 14 2002 349 353
23. L.L. Getz, C.S. Carter, and L. Gavish The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding Behav. Ecol. Sociobiol. 8 1981 189 194
24. G. Gimpl, and F. Fahrenholz The oxytocin receptor system: structure, function, and regulation Physiol. Rev. 81 2001 629 683
25. T.S. Gray, and E.W. Bingaman The amygdala: corticotropin-releasing factor, steroids, and stress Crit. Rev. Neurobiol. 10 1996 155 168
26. H.A. Halern, J.A. Cherry, and M.J. Baum Vomeronasal neuroepithelium and forebrain Fos responses to male pheromones in male and female mice J. Neurobiol. 39 1998 249 263
27. J.L. Hazelton, B.S. Cushing, C.S. Carter, G.E. Hoffman, and M.A. Ottinger Expression of cFos following cohabitation in the prairie vole (Microtus ochrogaster) Horm. Behav. 44 2003 53
28. M.M. Heeb, and P. Yahr c-fos immunoreactivity in the sexually dimorphic area of the hypothalamus and related brain regions of the male gerbils after exposure to sex-related stimuli or performance of specific sexual behaviors Neuroscience 72 1996 1049 1071
29. D. Huber, P. Veinante, and R. Stoop Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala Science 308 2005 245 248
30. T.R. Insel, and J.T. Winslow Central administration of oxytocin modulates the infant rat's response to social isolation Eur. J. Pharmacol. 203 1991 149 152
31. T.R. Insel, J.T. Winslow, Z. Wang, and L.J. Young Oxytocin, vasopressin, and the neuroendocrine basis of pair bond formation Adv. Exp. Med. Biol. 449 1998 215 224
32. C.E. Johanson Permeability and vascularity of the developing brain: cerebellum vs cerebral cortex Brain Res. 190 1980 3 16
33. G.A. Kevetter, and S.S. Winans Efferents of the corticomedial amygdala in the golden hamster: I. Efferents of the 'vomeronasal amygdala' J. Comp. Neurol. 197 1981 81 98
34. K.M. Kramer, B.S. Cushing, and C.S. Carter Developmental effects of oxytocin on stress response: single versus repeated exposure Physiol. Behav. 79 2003 775 782
35. K.M. Kramer, B.S. Cushing, C.S. Carter, J. Wu, and M.A. Ottinger Sex and species differences in plasma oxytocin using an enzyme immunoassay Can. J. Zool. 82 2004 1194 1200
36. M.M. Lim, and L.J. Young Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole Neuroscience 125 2004 35 45
37. R.C. Mantella, R.R. Vollmer, X. Li, and J.A. Amico Female oxytocin-deficient mice display enhanced anxiety-related behavior Endocrinology 144 2003 2291 2296
38. M.M. McCarthy, C.H. McDonald, P.J. Brooks, and D. Goldman An anxiolytic action of oxytocin is enhanced by estrogen in the mouse Physiol. Behav. 60 1996 1209 1215
39. B. McGuire, K.D. Russell, T. Mahoney, and M. Novak The effects of mate removal on pregnancy success in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) Biol. Reprod. 47 1992 37 42
40. S.W. Newman The medial extended amygdala in male reproductive behavior: a node in the mammalian social behavior network Ann. N. Y. Acad. Sci. 877 1999 242 257
41. I.D. Neumann, A. Wigger, L. Torner, F. Holsboer, and R. Landgraf Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo- pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus J. Neuroendocrinol. 12 2000 235 243
42. C.A. Pedersen, and M.L. Boccia Oxytocin links mothering received, mothering bestowed and adult stress responses Stress 5 2002 259 267
43. J.G. Pfaus, and M.M. Heeb Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents Brain Res. Bull. 44 1997 397 407
44. R.L. Roberts, B.S. Cushing, and C.S. Carter Intraspecific variation in the induction of female sexual receptivity in prairie voles Physiol. Behav. 64 1998 209 212
45. H.M. Schellinck, C. Smyth, R. Brown, and M. Wilkinson Odor-induced sexual maturation and expression of c-fos in the olfactory system of juvenile female mice Brain Res. Dev. Brain Res. 74 1993 138 141
46. T.M. Schwab, N.G. Solomon, L.G. Isaacson, and P. Callahan Reproductive activation of pine voles (Microtus pinetorum): examination of physiological markers Brain Res. 1021 2004 256 263
47. L.E. Shapiro, and T.R. Insel Ontogeny of oxytocin receptors in rat forebrain: a quantitative study Synapse 4 1989 259 266
48. L.E. Shapiro, and T.R. Insel Infant's response to social separation reflects adult differences in affiliative behavior: a comparative developmental study in prairie and montane voles Dev. Psychobiol. 23 1990 375 393
49. J.A. Thomas, and E.C. Birney Parental care and mating system of the prairie vole, Microtus ochrogaster Behav. Ecol. Sociobiol. 5 1979 171 186
50. R.E. Watson, S.J. Wiegand, R.W. Clough, and G.E. Hoffman Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology Peptides 7 1986 155 159
51. R.J. Windle, N. Shanks, S.L. Lightman, and C.D. Ingram Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats Endocrinology 138 1997 2829 2834
52. Y. Yamamoto, B.S. Cushing, K.M. Kramer, P.D. Epperson, G.E. Hoffman, and C.S. Carter Neonatal manipulations of oxytocin alter expression of oxytocin and vasopressin immunoreactive cells in the paraventricular nucleus of the hypothalamus in a gender-specific manner Neuroscience 125 2004 947 955
53. Yamamoto, Y., Carter, C.S., Cushing, B.S., in press. Neonatal manipulation of oxytocin affects the expression of estrogen receptor alpha.