Brain sexual dimorphism and sex differences in parental and other social behaviors

Annals of the New York Academy of Sciences

Volumn 807, Issue , 1997, Pages 273-286

  De Vries, Geert J ^a   Villalba, Constanza ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; OPIATE; OXYTOCIN; VASOPRESSIN;

ANIMAL EXPERIMENT; CONFERENCE PAPER; CONTROLLED STUDY; FEMALE; MALE; MATERNAL BEHAVIOR; NEUROTRANSMITTER RELEASE; NONHUMAN; PATERNAL BEHAVIOR; RAT; REARING; SEX DIFFERENCE; SOCIAL BEHAVIOR;

ANIMALIA;

EID: 0030956290     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.1997.tb51926.x     Document Type: Conference Paper

References (89)

1. KLEIMAN, D. 1977. Monogamy in mammals. Q. Rev. Biol. 52: 39-69.
2. DUDLEY, D. 1974. Paternal behavior in the California mouse Peromyscus californicus. Behav. Biol. 11: 247-252.
3. ÅRGUN, G. 1976. Social and territorial behaviour in the Mongolian gerbil (Meriones unguiculatus) under seminatural conditions. Biol. Behav. 1: 267-285.
4. ELWOOD, R. W. 1977. Changes in the responses of male and female gerbils (Meriones unguiculatus) towards test pups during the pregnancy of the female. Anim. Behav. 25: 46-51.
5. GUBERNICK, D. J. & J. R. ALBERS. 1987. The biparental care system of the California mouse, Peromyscus californicus. J. Comp. Psychol. 101: 169-177.
6. GETZ, L. L. & J. E. HOFMANN. 1986. Social organization in free-living prairie voles, Microtus ochrogaster. Behav. Ecol. Sociobiol. 18: 275-282.
7. DULCE MADEIRA, M., & A. R. LIEBERMAN. 1995. Sexual dimorphism in the mammalian limbic system. Progr. Neurobiol. 45: 257-333.
8. NUMAN M. 1988. Maternal behavior. In The Physiology of Reproduction. E. Knobil & J. Neill, Eds.: 1569-1645. Raven Press. New York.
9. ROSENBLATT, J. S. & H. I. SIEGEL. 1981. Factors governing the onset and maintenance of maternal behavior among nonprimate mammals. In Parental Care in Mammals. D. J. Gubernick & P. H. Klopfer, Eds.: 13-76. Wiley. New York.
10. BEACH, F. A. & J. JAYENS. 1956. Studies of maternal retrieving in rats: III. Sensory cues involved in the lactating female's response to her young. Behaviour 10: 104-125.
11. BENUCK, I. & F. A. ROWE. 1975. Centrally and peripherally induced anosmia: Influences on maternal behavior in lactating female rats. Physiol. Behav. 14: 439-447.
12. HERRENKOHL, L. R. & P. A. ROSENBERG. 1972. Exteroceptive stimulation of maternal behavior in the naive rat. Physiol. Behav. 8: 595-598.
13. KENYON, P., P. CRONIN & S. KEEBLE. 1981. Disruption of maternal behavior by perioral anesthesia. Physiol. Behav. 27: 313-321.
14. FLEMING, A. S., F. VACCARINO, L. TAMBOSSO & P. CHEE. 1979. Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203: 372-374.
15. FLEMING, A. S., F. VACCARINO & C. LUEBKE. 1980. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 25: 731-743.
16. DEL CERRO, M. C. R., M. A. P. IZQUIERDO, P. COLLADO, S. SEGOVIA & A. GUILLAMON. 1991. Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats. Physiol. Behav. 50: 67-71.
17. SMOTHERMAN, W. P., R. W. BELL, J. STARZEC, J. ELIAS & T. A. ZACHMAN. 1974. Maternal responses to infant vocalizations and olfactory cues in rats and mice. Behav. Biol. 12: 55-66.
18. ROSENBLATT, J. S. & H. I. SIEGEL. 1975. Hysterectomy-induced maternal behavior during pregnancy in the rat. J. Comp. Physiol. Psychol. 89: 685-700.
19. BRIDGES, R. S., H. H. FEDER & J. S. ROSENBLATT. 1977. Induction of maternal behaviors in primigravid rats by ovariectomy, hysterectomy, or ovariectomy, plus hysterectomy: Effect of length of gestation. Horm. Behav. 9: 156-169.
20. MAYER, A. D. & J. S. ROSENBLATT. 1984. Prepartum changes in maternal responsiveness and nest defense in Rattus norwegicus. J. Comp. Psychol. 98: 177-188.
21. ROSENBLATT, J. S., A. D. MAYER & A. L. GIORDANO. 1988. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 13: 29-46.
22. BRIDGES, R. S. 1990. Endocrine regulation of parental behavior in rodents. In Mammalian Parenting. Biochemical Neurobiological, and Behavioral Determinants. N. A. Krasnegor & R. S. Bridges, Eds.: 93-117. Oxford University Press. New York.
23. ROSENBLATT, J. S. 1967. Nonhormonal basis of maternal behavior in the rat. Science 156: 1512-1514.
24. PFAFF, D. W. & M. KEINER. 1973. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 151: 121-158.
25. NUMAN, M., J. S. ROSENBLATT & B. R. KOMISARUK. 1977. Medial preoptic area and onset of maternal behavior in the rat. J. Comp. Physiol. Psychol. 91: 146-164.
26. SLOTNICK, B. M. 1967. Disturbances of maternal behavior in the rat following lesions of the cingulate cortex. Behaviour 29: 204-236.
27. KIMBLE, D. P., L. ROGERS & L. HENDRICKSON. 1967. Hippocampal lesions disrupt maternal, not sexual, behavior in the albino rat. J. Comp. Physiol. Psychol. 63: 401-407.
28. FLEISCHER, S. & B. M. SLOTNICK. 1978. Disruption of maternal behavior in rats with lesions of the septal area. Physiol. Behav. 21: 189-200.
29. CORODIMAS, K. P., J. S. ROSENBLATT, M. E. CANFIELD & J. I. MORRELL. 1993. Neurons in the lateral subdivision of the habenular complex mediate the hormonal onset of maternal behavior in rats. Behav. Neurosci. 107: 827-843.
30. NUMAN, M. & M. NUMAN. 1996. A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev. Psychobiol. 29: 23-51.
31. NUMAN, M. & H. G. SMITH. 1984. Maternal behavior in rats: Evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 98: 712-727.
32. HANSEN, S. & A. FERREIRA. 1986. Food intake, aggression, and fear behavior in the mother rat: Control by neural systems concerned with milk ejection and maternal behavior. Behav. Neurosci. 100: 64-70.
33. MAYER, A. D., N. C. G. FREEMAN & J. S. ROSENBLATT. 1979. Ontogeny of maternal behavior in the laboratory rat: Factors underlying changes in responsiveness from 30 to 90 days. Dev. Psychobiol. 12: 425-439.
34. BROWN, R. E. 1986. Paternal behavior in the male Long-Evans rat (Rattus norvegicus). J. Comp. Psychol. 100: 162-172.
35. SEGOVIA, S. & A. GUILLAMON. 1993. Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res. Rev. 18: 51-74.
36. SEGOVIA, S., L. M. ORENSANZ, A. VALENCIA & A GUILLAMON. 1984. Effects of sex steroids on the development of the accessory olfactory bulb in the rat: A volumetric study. Dev. Brain Res. 16: 312-314.
37. COLLADO, P., A. GUILLAMON, A. VALENCIA & S. SEGOVIA. 1990. Sexual dimorphism in the bed nucleus of the accessory olfactory tract in the rat. Dev. Brain Res. 56: 263-268.
38. MIZUKAMI, S., M. NISHIZYKA & Y. ARAI. 1983. Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp. Neurol. 79: 569-575.
39. HINES, M., L. S. ALLEN & R. A. GORSKI. 1992. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res. 579: 321-326.
40. DEL ABRIL, A., S. SEGOVIA & A. GUILLAMON. 1987. The bed nucleus of the stria terminalis in the rat: Regional sex differences controlled by gonadal steroids early after birth. Dev. Brain Res. 32: 295-300.
41. MENELLA, J. A. & H. MOLTZ. 1988. Infanticide in the male rats: The role of the vomeronasal organ. Physiol. Behav. 42: 303-306.
42. IZQUIERDO, P., P. COLLADO, S. SEGOVIA, A. GUILLAMON & M. A. P. DEL CERRO. 1992. Maternal behavior induced in male rats by bilateral lesions of the bed nucleus of the accessory olfactory tract. Physiol. Behav. 52: 707-712.
43. YAHR, P. 1988. Sexual differentiation of behavior in the context of developmental psychobiology. In Handbook of Behavioral Neurobiology. Vol. 9. E. M. Blass, Ed.: 197-243. Plenum. New York.
44. 3H]-dihydrotestosterone administration. J. Steroid Biochem. 8: 1131-1135.
45. GORSKI, R. A., J. H. GORDAN, J. E. SHRYNE & A. M. SOLTHAM. 1978. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 148: 333-346.
46. NOTTEBOHM, F. & A. P. ARNOLD. 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194: 211-213.
47. GUBERNICK, D. J., D. R. SENGELAUB & E. M. KURZ. 1993. A neuroanatomical correlate of paternal and maternal behavior in the biparental California mouse (Peromyscys californicus). Behav. Neurosci. 107: 194-201.
48. SHAPIRO, L. E., C. M. LEONARD, C. E. SESSIONS, D. A. DEWSBURY & T. R. INSEL. 1991. Comparative neuroanatomy of the sexually dimorphic hypothalamus in monogamous and polygamous vole. Brain Res. 541: 232-240.
49. SIMERLY, R. B., R. A. GORSKI & L. W. SWANSON. 1986. Neurotransmitter specificity of cells and fibers in the medial preoptic nucleus: An immunohistochemical study in the rat. J. Comp. Neurol. 246: 343-363.
50. DE VRIES, G. J. 1990. Sex differences in neurotransmitter systems. J. Neuroendocrinol. 2: 1-13.
51. POPPER, P., C. A. PRIEST & P. E. MICEVYCH. 1995. Effects of sex steroids on the cholecystokinin circuit modulating reproductive behavior. In Neurobiological Effects of Sex Steroid Hormones, P. E. Micevych & R. P. Hammer, Jr., Eds.: 160-183. Cambridge University Press. Cambridge.
52. MCCARTHY, M. M., P. J. BROOKS, J. G. PFAUS, H. E. BROWN, L. M. FLANAGAN, S. SCHWARTZ-GIBLIN & D. W. PFAFF. 1993. Antisense oligodeoxynucleotides in behavioral neuroscience. Neuroprotocols 2: 67-74.
53. RUBIN, B. S. & R. S. BRIDGES. 1984. Disruption of ongoing maternal responsiveness in rats by central administration of morphine sulfate. Brain Res. 307: 91-97.
54. SIMERLY, R. B., L. D. MCCALL & S. J. WATSON. 1988. Distribution of opioid peptides in the preoptic region: Immunohistochemical evidence for a steroid-sensitive enkephalin sexual dimorphism. J. Comp. Neurol. 276: 442-459.
55. WATSON, R. E., JR., G. E. HOFFMAN & S. J. WIEGAND. 1986. Sexually dimorphic opioid distribution in the preoptic area: Manipulation by gonadal steroids. Brain Res. 398: 157-163.
56. HAMMER, R. P., JR. 1984. The sexually dimorphic region of the preoptic area in rats contains denser opiate receptor binding sites in females. Brain Res. 308: 172-176.
57. HAMMER, R. P., & R. S. BRIDGES. 1987. Preoptic area opioids and opiate receptors increase during pregnancy and decrease during lactation. Brain Res. 420: 48-56.
58. PEDERSEN, C. A., J. A. ASCHE, Y. L. MONROE & A. J. PRANGE. 1982. Oxytocin induces maternal behavior in virgin female rats. Science 216: 648-649.
59. INSEL, T. R. & L. E. SHAPIRO. 1992. Oxytocin receptors and maternal behavior. Ann. N.Y. Acad. Sci. 652: 122-141.
60. DE VRIES, G. J. & R. M. Buns. 1983. The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res. 273: 307-317.
61. INSEL, T. R. & C. R. HARBAUGH. 1989. Lesions of the hypothalamic paraventriuclar nucleus disrupt the initiation of maternal behavior. Physiol. Behav. 45: 1033-1041.
62. NUMAN, M. & K. P. CORODIMAS. 1985. The effects of paraventricular hypothalamic lesions on maternal behavior in rats. Physiol. Behav. 35: 417-425.
63. WIDEMAN, C. H. & H. M. MURPHY. 1990. Vasopressin, maternal behavior and pup well-being. Curr. Psychol. Res. Rev. 9: 285-295.
64. DE VRIES, G. J., R. M. BUIJS, F. W. VAN LEEUWEN, A. R. CAFFÉ & D. F. SWAAB. 1985. The vasopressinergic innervation of the brain in normal and castrated rats. J. Comp. Neurol. 233: 236-254.
65. MERKER, G. S., S. BLAHSER & E. ZEISBERGER. 1980. Reactivity patterns of vasopressin containing neurons and its relation to the antipyretic reaction in guinea pig. Cell Tiss. Res. 212: 47-61.
66. CALDWELL, J. D., E. R. GREER, M. F. JOHNSON, A. J. PRANGE, JR. & C. A. PEDERSEN. 1987. Oxytocin and vasopressin immunoreactivity in hypothalamic and extrahypothalamic sites in late pregnant and postpartum rats. Neuroendocrinology 46: 39-47.
67. LANDGRAF, R., I. NEUMANN & Q. J. PITTMAN. 1991. Septal and hippocampal release of vasopressin and oxytocin during late pregnancy and parturition in the rat. Neuroendocrinology 54: 378-383.
68. DE VRIES, G. J., R. M. BUIJS & A. A. SLUITER. 1984. Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Res. 298: 141-145.
69. VAN LEEUWEN, F. W., A. R. CAFFÉ & G. J. DE VRIES. 1985. Vasopressin cells in the bed nucleus of the stria terminalis of the rat: Sex differences and the influence of androgens. Brain Res. 325: 391-394.
70. MILLER, M. A., G. J. DE VRIES, H. A. AL-SHAMMA & D. M. DORSA. 1992. Rate of decline of vasopressin immunoreactivity and messenger RNA levels in the bed nucleus of the stria terminalis. J. Neurosci. 12: 2881-2887.
71. DE VRIES, G. J., R. M. BUIJS & D. F. SWAAB. 1981. Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain: Presence of a sex difference in the lateral septum. Brain Res. 218: 67-78.
72. MILLER, M. A., L. VICIAN, D. K. CLIFTON & D. M. DORSA. 1989. Sex differences in vasopressin neurons in the bed nucleus of the stria terminalis by in situ hybridization. Peptides 10: 615-619.
73. AL-SHAMMA, H. A. & G. J. DE VRIES. 1996. Neurogenesis of the sexually dimorphic vasopressin cells of the bed nucleus of the stria terminalis and amygdala of rats. J. Neurobiol. 29: 91-98.
74. MCGUIRE, B. & M. NOVAK. 1984. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim. Behav. 32: 1132-1141.
75. OLIVERAS, D. & M. NOVAK. 1986. A comparison of paternal behaviour in the meadow vole, Microtus pennsylvanicus, the pine vole, M. pinetorum and the prairie vole, M. ochrogaster. Anim Behav. 34: 519-526.
76. BAMSHAD, M., M. A. NOVAK & G. J. DE VRIES. 1993. Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J. Neuroendocrinol. 5: 247-255.
77. BAMSHAD, M., M. A. NOVAK & G. J. DE VRIES. 1994. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles, Microtus ochrogaster. Physiol. Behav. 56: 751-758.
78. WANG, Z. X., W. SMITH, D. E. MAJOR & G. J. DE VRIES. 1994. Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain Res. 650: 212-218.
79. GETZ, L. L., C. S. CARTER & L. GAVISH. 1981. The mating system of prairie vole, Microtus ochrogaster: Field and laboratory evidence for pair-bonding. Behav. Ecol. Sociobiol. 8: 189-194.
80. WANG, Z. X., C. F. FERRIS & G. J. DE VRIES. 1994. The role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc. Natl. Acad. Sci. USA 91: 400-404.
81. WINSLOW, J. T., N. HASTINGS, C. S. CARTER, C. R. HARBAUGH & T. R. INSEL. 1993. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365: 545-547.
82. KOOLHAAS, J. M., E. MOOR, Y. HIEMSTRA & B. BOHUS. 1991. The testosterone-dependent vasopressinergic neurons in the medial amygdala and lateral septum: Involvement in social behaviour of male rats. In Vasopressin Colloque INSERM. Vol. 208. S. Jard & R. Jamison, Eds.: 213-219. John Libbey Eurotext Ltd. London.
83. WILLIAMS, J. R., T. R. INSEL, C. R. HARBAUGH & C. S. CARTER. 1994. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Mocrotus ochrogaster). J. Neuroendocrinol. 6: 247-250.
84. INSEL, T. R., C. F. FERRIS & Z. X. WANG. 1994. Pattern of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14: 5381-5392.
85. BLUTHE, R.-M. & R. DANTZER. 1992. Role of the vomeronasal system in the vasopressinergic modulation of social recognition in rats. Brain Res. 604: 205-210.
86. JAKAB, R. L. & C. LERANTH. 1991. Convergent vasopressinergic and hippocampal input onto somatospiny neurons of the rat lateral septal area. Neuroscience 2: 413-421.
87. DANTZER, R., G. F. KOOB, R. M. BLUTHÉ & M. LE MOAL. 1988. Septal vasopressin modulates social memory in male rats. Brain Res. 457: 143-147.
88. BLUTHE, R. M. & R. DANTZER. 1990. Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res. 535: 301-304.
89. IACONO, W. G. & M. BEISER. 1992. Are males more likely than females to develop schizophrenia? Am. J. Psychiatry 149: 1070-1074.