Involvement of estrogen receptor α, β and oxytocin in social discrimination: A detailed behavioral analysis with knockout female mice

Genes, Brain and Behavior

Volumn 5, Issue 7, 2006, Pages 528-539

  Choleris, E ^a,b   Ogawa, S ^b   Kavaliers, M ^c   Gustafsson, J A ^d   Korach, K S ^e   Muglia, L J ^f   Pfaff, D W ^b  

^a UNIVERSITY OF GUELPH   (Canada)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d KAROLINSKA INSTITUTE   (Sweden)

^e NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activity; Anxiety; Ethological analysis; Social interactions; Social recognition

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; OXYTOCIN;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIORAL SCIENCE; CONTROLLED STUDY; FEMALE; GROOMING; KNOCKOUT MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; RAT; SOCIAL BEHAVIOR; SOCIAL DISCRIMINATION; STIMULUS RESPONSE; TASK PERFORMANCE; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; DISCRIMINATION (PSYCHOLOGY); ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; EXPLORATORY BEHAVIOR; FEMALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; MULTIVARIATE ANALYSIS; OXYTOCIN; SOCIAL BEHAVIOR;

ANIMALIA;

EID: 33748917601     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2006.00203.x     Document Type: Article

References (60)

1. Bales, K.L. & Carter, C.S. (2003) Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44, 178-184.
2. Baron-Cohen, S. (2002) The extreme male brain theory of autism. Trends Cogn Sci 6, 248-254.
3. Bartel, A. & Zeki, S. (2004) The neural correlates of maternal and Romantic love. Neuroimage 21, 1155-1166.
4. Beauchamp, J.K. & Yamazaki, K. (2003) Chemical signalling in mice. Biochem Soc Trans 31, 147-151.
5. Blanchard, R.J., Yudko, E.B., Rodgers, R.J. & Blanchard, D.C. (1993) Defense systems in psychopharmacology: an ethological approach to the pharmacology of fear and anxiety. Behav Brain Res 58, 155-165.
6. Cho, M.M., De Vries, A.C., Williams, J.R. & Carter, C.S. (1999) The effects of oxytocin and vasopressin on partner preference in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113, 1071-1079.
7. Choleris, E., Thomas, A.W., Ossenkopp, K.-P., Kavaliers, M., Valsecchi, P. & Prato, F.S. (2000) Sex differences in conditioned taste aversion and in the effects of exposure to a pulsed magnetic field in deer mice, Peromyscus maniculatus. Physiol Behav 71, 237-249.
8. Choleris, E., Thomas, A.W., Kavaliers, M. & Prato, F.S. (2001) A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev 25, 235-260.
9. Choleris, E., Gustafsson, J.Å., Korach, K.S., Muglia, L.J., Pfaff, D.W. & Ogawa, S. (2003) An estrogen dependent micronet mediating social recognition: a study with oxytocin- and estrogen receptor α- and β-knockout mice. Proc Natl Acad Sci USA 100, 6192-6197.
10. Couse, J.F. & Korach, K.S. (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20, 358-417.
11. Dulac, C. & Torello, T. (2003) Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4, 551-562.
12. Engelmann, M., Wotjak, C.T. & Landgraf, R. (1995) Social discrimination procedure: an alternative method to investigate juvenile recognition abilities in rats. Physiol Behav 58, 315-321.
13. Ferguson, J.N., Young, L.J., Hearn, E.F., Matzuk, M.M., Insel, T.R. & Winslow, J.T. (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25, 284-288.
14. Ferguson, J.N., Aldag, J.M., Insel, T.R. & Young, L.J. (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21, 8278-8285.
15. Gheusi, G., Blunthé, R.-M., Goodall, G. & Dantzer, R. (1994) Social and individual recognition in rodents: methodological aspects and neurobiological bases. Behav Process 33, 59-88.
16. Giovenardi, M., Padoin, M.J., Cadore, L.P. & Lucion, A.B. (1998) Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol Behav 63, 351-359.
17. Gonzalez, L.E., Andrews, N. & File, S. (1996) 5-HT1A and benzodiazepine receptors in the basolateral amygdala modulate anxiety in the social interaction test, but not in the elevated plus-maze. Brain Res 732, 145-153.
18. Green, L.A., Fein, D., Modhal, C., Feinstein, C., Waterhouse, L. & Morris, M. (2001) Oxytocin and autistic disorder: alteration in peptide forms. Biol Psychiatry 50, 609-613.
19. Gross, G., Imamura, T., Luedke, C., Vogt, S.K., Olson, L.M., Nelson, D.M., Sadovksy, Y. & Muglia, L.J. (1998) Opposing actions of prostaglandins and oxytocin determine the onset of murine labor. Proc Natl Acad Sci USA 95, 11875-11879.
20. Harmon, A.C., Huhman, K.L., Moore, T.O. & Albers, H.E. (2002) Oxytocin inhibits aggression in female Syrian hamsters. J Neuroendocrinol 12, 963-969.
21. Hliňák, Z. (1993) Social recognition in ovariectomized and estradiol-treated female rats. Horm Behav 27, 159-166.
22. Hollander, E., Novotny, S., Hanratty, M., Yaffe, R., DeCaria, C.M., Aronwitz, B.R. & Mosovich, S. (2003) Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology 28, 191-198.
23. Imwalle, D.B., Scordakales, E.M. & Rissman, E.F. (2002) Estrogen receptor α influences socially motivated behaviors. Horm Behav 42, 484-491.
24. Insel, T.R. & Fernald, R.D. (2004) How the brain processes social information: searching the social brain. Annu Rev Neurosci 27, 697-722.
25. Insel, T.R. & Hulihan, T.J. (1995) A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109, 782-789.
26. Insel, T.R., O'Brien, D.J. & Leckman, J.F. (1999) Oxytocin, vasopressin and autism: is there a connection? Biol Psychiatry 45, 145-157.
27. Kavaliers, M., Colwell, D.D., Choleris, E., Ågmo, A., Muglia, L.J., Ogawa, S. & Pfaff, D.W. (2003) Impaired discrimination of and aversion to parasitized male odors by female oxytocin knockout mice. Genes Brain Behav 2, 220-230.
28. Kavaliers, M., Choleris, E., Ågmo, A. & Pfaff, D.W. (2004) Olfactory mediated parasite recognition and avoidance: linking genes to behavior. Horm Behav 46, 272-283.
29. Kavaliers, M., Choleris, E. & Pfaff, D.W. (2005a) Recognition and avoidance of the odors of parasitized conspecifics and predators: differential genomic correlates. Neurosci Biobehav Rev 29, 1347-1359.
30. Kavaliers, M., Choleris, E., Ågmo, A., Muglia, L.J., Ogawa, S. & Pfaff, D.W. (2005b) Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice. Anim Behav 70, 693-702.
31. Kendrick, K.M. (2000) Oxytocin, motherhood and bonding. Exp Physiol 85, 111S-124S.
32. deKloet, E.R., Voorhuis, A.M., Boxhma, Y. & Elands J. (1986) Estradiol modulates density of putative 'oxytocin receptors' in discrete brain regions. Neuroendocrinology 44, 415-421.
33. Krege, J.H., Hodgin, J.B., Couse, J.F., Enmark, E., Warner, M., Mahler, J.F., Sar, M., Korach, K.S., Gustafsson, J.A. & Smithies, O. (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci USA 95, 15677-15682.
34. Kudryavtseva, N.N., Bondar, N.P. & Avgustinovich, D.F. (2002) Association between experience of aggression and anxiety in male mice. Behav Brain Res 133, 83-93.
35. Lister, R.G. (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46, 321-340.
36. Loup, F., Tribollet, E., Dubois-Dauphin, M. & Dreifuss, J.J. (1991) Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res 555, 220-232.
37. Lubahn, D.B., Moyer, J.S., Golding, T.S., Couse, J.F., Korach, K.S. & Smithies, O. (1993) Alteration of reproductive function but not prenatal sexual development after insertion disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90, 1165-11166.
38. Lubin, D.A., Elliott, J.C., Black, M.C. & Johns, J.M. (2003) An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav Neurosci 117, 195-201.
39. McCarthy, M.M. (1990) Oxytocin inhibits infanticide in female house mice (Mus domesticus). Horm Behav 24, 365-375.
40. McCarthy, M.M., McDonald, C.H., Brooks, P.J. & Goldman, D. (1996) An anxiolytic action of oxytocin is enhanced by estrogen in the mouse. Physiol Behav 60, 1209-1215.
41. Mikics, É., Barsy, B., Barsvári, B. & Haller, J. (2005) Behavioral specificity of non-genomic glucocorticoid effects in rats: effects on risk assessment in the elevated plus-maze and the open-field. Horm Behav 48, 152-162.
42. Mikulka, P.J. & Klein, S.B. (1997) The effects of CS familiarization and extinction procedure on the resistance to extinction of a conditioned taste aversion. Behav Biol 19, 518-522.
43. Mitra, S.W., Hoskin, E., Yudkovitz, J., Pear, L., Wilkinson, H.A., Hayashi, S., Pfaff, D.W., Ogawa, S., Rohrer, S.P., Schaeffer, J.M., McEwen, B.S. & Alves, S.E. (2003) Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor α. Endocrinology 144, 2055-2067.
44. Modhal, C.M., Green, L.A., Fein, D., Morris, M., Waterhouse, L., Feinstein, C. & Levin, H. (1998) Plasma oxytocin levels in autistic children. Biol Psychiatry 43, 270-277.
45. Nomura, M., McKenna, E., Korach, K.S., Pfaff, D.W. & Ogawa, S. (2002) Estrogen receptor β regulates the gene expression of oxytocin and arginine vasopressin in the hypothalamic paraventricular nucleus of male mice. Brain Res Mol Brain Res 109, 84-94.
46. Ogawa, S., Krebs, C.J., Zhu, Y.S. & Pfaff, D.W. (2000) Genes participating in reproductive behaviors. In: Pfaff, D.W., Berrettini, W.H., Joh, T.H. & Maxon, S.C. (eds), Genetic Influences on Neural and Behavioral Functions. CRC Press, New York, pp. 417-430.
47. Ogawa, S., Chan, J., Gustafsson, J.-Å., Korach, K.S. & Pfaff, D.W. (2003) Estrogen increases locomotor activity in mice through estrogen receptor a: specificity for the type of activity. Endocrinology 144, 230-239.
48. Ogawa, S., Choleris, E. & Pfaff, D.W. (2004) Genetic influences on aggressive behavior and arousability in animals. Ann N Y Acad Sci 1036, 257-266.
49. Pedersen, C.A. (2004) Biological aspects of social bonding and the roots of human violence. Ann N Y Acad Sci 1036, 106-127.
50. Pedersen, C.A., Caldwell, J.D., Walker, C., Ayers, G. & Mason, G.A. (1994) oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108, 1163-1171.
51. Popik, P. & van Ree, J.M. (1998) Neurohypophyseal peptides and social recognition in rats. Prog Brain Res 119, 415-436.
52. Ragnauth, A.K., Devidze, N., Moy, V., Finley, K., Goodwillie, A., Kow, L.-M., Muglia, L.J. & Pfaff, D.W. (2005) Female oxytocin gene-knockout mice, in a seminatural environment, display exaggerated aggressive behavior. Genes Brain Behav 4, 229-239.
53. Razzoli, M., Cushing, B.S., Carter, C.S. & Valsecchi, P. (2003) Hormonal regulation of agonistic and affiliative behavior in female Mongolian gerbils (Meriones unguiculatus). Horm Behav 43, 549-553.
54. Rodgers, R.J. & Dalvi, A. (1997) Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 21, 801-810.
55. Rodgers, R.J. & Waters, A.J. (1985) Benzodiazepines and their antagonists: a pharmacoethological analysis with particular reference to effects on 'aggression'. Neurosci Biobehav Rev 9, 21-35.
56. Roy, V. & Chapillon, P. (2004) Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents. Behav Brain Res 154, 439-448.
57. Taylor, S.E., Cousino Klein, L., Lewis, B.P., Gruenewald, T.L., Gurung, R.A.R. & Updegraff, J.A. (2000) Biobehavioral responses to stress in females tend-and-be-friend, not fight-or-flight. Psychol Rev 107, 411-429.
58. Young, L.J., Winslow, J.T., Wang, Z., Gingrich, B., Guo, Q., Matzuk, M.M. & Insel, T.R. (1997) Gene targeting approaches to neuroendocrinology: oxytocin, maternal behavior and affiliation. Horm Behav 31, 221-231.
59. Young, L.J., Wang, Z., Donaldson, R. & Rissman, E.F. (1998) Estrogen receptor α is essential for induction of oxytocin receptor by estrogen. Neuroreport 9, 933-936.
60. Young, L.J., Pitkow, L.J. & Fergurson, J.N. (2002) Neuropeptides and social behavior: animal models relevant to autism. Mol Psychiatry 7, S38-S39.