Pubertal hormones, the adolescent brain, and the maturation of social behaviors: Lessons from the Syrian hamster

Molecular and Cellular Endocrinology

Volumn 254-255, Issue , 2006, Pages 120-126

  Schulz, Kalynn M ^a   Sisk, Cheryl L ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Adolescence; Aggression; Lordosis; Organizational effects; Puberty; Reproductive behavior; Sensitive period; Social behavior; Testosterone

Indexed keywords

SEX HORMONE; TESTIS PEPTIDE HORMONE; TESTOSTERONE;

ADOLESCENT DEVELOPMENT; AGGRESSION; ARTICLE; BRAIN FUNCTION; BRAIN MATURATION; FEMININITY; HUMAN; LORDOSIS; MASCULINITY; NONHUMAN; PREPUBERTY; PRIORITY JOURNAL; PUBERTY; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SYRIAN HAMSTER;

ADOLESCENT; AGONISTIC BEHAVIOR; ANIMALS; CRICETINAE; FEMALE; GONADAL HORMONES; HUMANS; MALE; MESOCRICETUS; OVARY; PUBERTY; REPRODUCTIVE BEHAVIOR; SEXUAL MATURATION; SOCIAL BEHAVIOR; TESTICULAR HORMONES;

EID: 33745910269     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2006.04.025     Document Type: Article

References (52)

1. Albers H.E., Huhman K.L., and Meisel R.L. Hormonal basis of social conflict and communication. In: Pfaff D. (Ed). Hormones, Brain and Behavior (2002), Academic Press 393-433
2. Albert D.J., and Walsh M.L. Neural systems and the inhibitory modulation of agonistic behavior: a comparison of mammalian species. Neurosci. Biobehav. Rev. 8 (1984) 5-24
3. Andersen S.L., Thompson A.T., Rutstein M., Hostetter J.C., and Teicher M.H. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37 (2000) 167-169
4. Arnold A.P., and Breedlove S.M. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm. Behav. 19 (1985) 469-498
5. Baum M.J. Precocious mating in male rats following treatment with androgen or estrogen. J. Comp. Physiol. Psychol. 78 (1972) 356-367
6. Beach F.A., Stern B., Carmichael M., and Ranson E. Comparisons of sexual receptivity and proceptivity in female hamsters. Behav. Biol. 18 (1976) 473-487
7. Bloch G.J., Mills R., and Gale S. Prepubertal testosterone treatment of female rats: defeminization of behavioral and endocrine function in adulthood. Neurosci. Biobehav. Rev. 19 (1995) 177-186
8. Carter C.S., Clemens L.G., and Hoekema D.J. Neonatal androgen and adult sexual behavior in the golden hamster. Physiol. Behav. 9 (1972) 89-95
9. Chung W.C., De Vries G.J., and Swaab D.F. Sexual differentiation of the bed nucleus of the stria terminalis in humans may extend into adulthood. J. Neurosci. 22 (2002) 1027-1033
10. Davis E.C., Shryne J.E., and Gorski R.A. A revised critical period for the sexual differentiation of the sexually dimorphic nucleus of the preoptic area in the rat. Neuroendocrinology 62 (1995) 579-585
11. Davis E.C., Shryne J.E., and Gorski R.A. Structural sexual dimorphisms in the anteroventral periventricular nucleus of the rat hypothalamus are sensitive to gonadal steroids perinatally, but develop peripubertally. Neuroendocrinology 63 (1996) 142-148
12. de Jonge F.H., Muntjewerff J.W., Louwerse A.L., and van de Poll N.E. Sexual behavior and sexual orientation of the female rat after hormonal treatment during various stages of development. Horm. Behav. 22 (1988) 100-115
13. Dominguez J.M., and Hull E.M. Dopamine, the medial preoptic area, and male sexual behavior. Physiol. Behav. 86 (2005) 356-368
14. Eaton G. Effect of a single prepubertal injection of testosterone propionate on adult bisexual behavior of male hamsters castrated at birth. Endocrinology 87 (1970) 934-940
15. Eichmann F., and Holst D.V. Organization of territorial marking behavior by testosterone during puberty in male tree shrews. Physiol. Behav. 65 (1999) 785-791
16. Ferris C.F., Axelson J.F., Shinto L.H., and Albers H.E. Scent marking and the maintenance of dominant/subordinate status in male golden hamsters. Physiol. Behav. 40 (1987) 661-664
17. Ferris C.F., Gold L., De Vries G.J., and Potegal M. Evidence for a functional and anatomical relationship between the lateral septum and the hypothalamus in the control of flank marking behavior in Golden hamsters. J. Comp. Neurol. 293 (1990) 476-485
18. Ferris C.F., Delville Y., Irvin R.W., and Potegal M. Septo-hypothalamic organization of a stereotyped behavior controlled by vasopressin in golden hamsters. Physiol. Behav. 55 (1994) 755-759
19. Fitch R.H., and Denenberg V.H. A role for ovarian hormones in sexual differentiation of the brain. Behav. Brain Sci. 21 (1998) 311-327 discussion 327-352
20. Ford J.J. Testicular control of defeminization in male pigs. Biol. Reprod. 27 (1982) 425-430
21. Ford J.J. Postnatal differentiation of sexual preference in male pigs. Horm. Behav. 17 (1983) 152-162
22. Ford J.J., and Christenson R.K. Influences of pre- and postnatal testosterone treatment on defeminization of sexual receptivity in pigs. Biol. Reprod. 36 (1987) 581-587
23. Ge X., Conger R.D., and Elder Jr. G.H. Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms. Dev. Psychol. 37 (2001) 404-417
24. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., and Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2 (1999) 861-863
25. Hull E.M., Du J., Lorrain D.S., and Matuszewich L. Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J. Neurosci. 15 (1995) 7465-7471
26. Irvin R.W., Szot P., Dorsa D.M., Potegal M., and Ferris C.F. Vasopressin in the septal area of the golden hamster controls scent marking and grooming. Physiol. Behav. 48 (1990) 693-699
27. Johnston R.E. Scent marking by male golden hamsters (Mesocricetus auratus). II. The role of the flank gland scent in the causation of marking. Z. Tierpsychol. 37 (1975) 138-144
28. Kow L.M., Malsbury C.W., and Pfaff D.W. Lordosis in the male golden hamster elicited by manual stimulation: characteristics and hormonal sensitivity. J. Comp. Physiol. Psychol. 90 (1976) 26-40
29. Lumia A.R., Raskin L.A., and Eckhert S. Effects of androgen on marking and aggressive behavior of neonatally and prepubertally bulbectomized and castrated male gerbils. J. Comp. Physiol. Psychol. 91 (1977) 1377-1389
30. Meek L.R., Romeo R.D., Novak C.M., and Sisk C.L. Actions of testosterone in prepubertal and postpubertal male hamsters: dissociation of effects on reproductive behavior and brain androgen receptor immunoreactivity. Horm. Behav. 31 (1997) 75-88
31. Menard T.A., Schulz K.M., Romeo R.D., and Sisk C.L. Testosterone increases flank marking behavior in adult but not prepubertal male hamsters. Horm. Behav. 44 (2003) 63
32. Payne A.P. Changes in aggressive and sexual responsiveness of male golden hamsters after neonatal androgen administration. J. Endocrinol. 73 (1977) 331-337
33. Romeo R.D., and Sisk C.L. Pubertal and seasonal plasticity in the amygdala. Brain Res. 889 (2001) 71-77
34. Romeo R.D., Cook-Wiens E., Richardson H.N., and Sisk C.L. Dihydrotestosterone activates sexual behavior in adult male hamsters but not in juveniles. Physiol. Behav. 73 (2001) 579-584
35. Romeo R.D., Wagner C.K., Jansen H.T., Diedrich S.L., and Sisk C.L. Estradiol induces hypothalamic progesterone receptors but does not activate mating behavior in male hamsters (Mesocricetus auratus) before puberty. Behav. Neurosci. 116 (2002) 198-205
36. Romeo R.D., Schulz K.M., Nelson A.L., Menard T.A., and Sisk C.L. Testosterone, puberty, and the pattern of male aggression in Syrian hamsters. Dev. Psychobiol. 43 (2003) 102-108
37. Salas-Ramirez K., and Sisk C.L. Centrally administered apomorphine partially reverses detrimental effects on male reproductive behavior resulting from the absence of gonadal hormones during adolescence. Horm. Behav. 48 (2005) 124
38. Schulz K.M., Richardson H.N., Romeo R.D., Morris J.A., Lookingland K.J., and Sisk C.L. Medial preoptic area dopaminergic responses to female pheromones develop during puberty in the male Syrian hamster. Brain Res. 988 (2003) 139-145
39. Schulz K.M., Richardson H.N., Zehr J.L., Osetek A.J., Menard T.A., and Sisk C.L. Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster. Horm. Behav. 45 (2004) 242-249
40. Schulz, K.M., Zehr, J.L., Hingst, E.S., Montalto, P.R., Poole, A.D., Sisk, C.L., 2004b. Ovarian hormones partially defeminize female lordosis behavior during puberty. In: Society for Neuroscience, Abstract Viewer/Itinerary Planner, San Diego, CA [online].
41. Schulz, K.M., Zehr, J.L., Osetek, A.J., Sisk, C.L., 2005. Exposure to gonadal hormones during puberty influences the cross-sectional area of the adult male ventromedial hypothalamus in response to estradiol and progesterone. In: Society for Neuroscience, Abstract Viewer/Itinerary Planner, Washington, DC [online].
42. Schulz, K.M., Menard, T.A., Smith, D.A., Albers, H.E., Sisk, C.L., 2006. Testicular hormone exposure during adolescence organizes flank marking behavior and vasopressin receptor binding in the lateral septum, submitted for publication.
43. Schulz-Wilson K.M., Menard T.A., and Sisk C.L. Gonadal hormones during puberty influence the social, submissive, and aggressive behavior of adult male Syrian hamsters. Horm. Behav. 41 (2002) 488
44. Scott J.P., Stewart J.M., and De Ghett V.J. Critical periods in the organization of systems. Developmental Psychobiology (1974), John Wiley and Sons
45. Seidenfeld M.E., Sosin E., and Rickert V.I. Nutrition and eating disorders in adolescents. Mt. Sinai. J. Med. 71 (2004) 155-161
46. Shrenker P., Maxson S.C., and Ginsburg B.E. The role of postnatal testosterone in the development of sexually dimorphic behaviors in DBA/1Bg mice. Physiol. Behav. 35 (1985) 757-762
47. Sisk C.L., Berglund L.A., Tang Y.P., and Venier J.E. Photoperiod modulates pubertal shifts in behavioral responsiveness to testosterone. J. Biol. Rhythms 7 (1992) 329-339
48. Sisk C.L., Schulz K.M., and Zehr J.L. Puberty: a finishing school for male social behavior. Ann. NY Acad. Sci. 1007 (2003) 189-198
49. Sodersten P., Damassa D.A., and Smith E.R. Sexual behavior in developing male rats. Horm. Behav. 8 (1977) 320-341
50. Tiefer L. Gonadal hormones and mating behavior in the adult golden hamster. Horm. Behav. (1970) 189-202
51. Tiefer L., and Johnson W.A. Female sexual behaviour in male golden hamsters. J. Endocrinol. 51 (1971) 615-620
52. Zehr J.L., Todd B.J., Schulz K.M., McCarthy M.M., and Sisk C.L. Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J. Neurobiol. 66 (2006) 578-590