Neuroscience
Frontiers in Evolutionary Neuroscience ·
Volume 3 - 2011 | https://doi.org/10.3389/fnevo.2011.00010
Maternal Programming of Reproductive Function and Behavior in the Female Rat
- Nicole M. Cameron1*corresponding author
- 1 Center for Development and Behavioral Neuroscience, Psychology and Biology Departments, Binghamton University – State University of New York Binghamton, NY, USA
Abstract
Parental investment can be used as a forecast for the environmental conditions in which offspring will develop to adulthood. In the rat, maternal behavior is transmitted to the next generation through epigenetic modifications such as methylation and histone acetylation, resulting in variations in estrogen receptor alpha expression. Natural variations in maternal care also influence the sexual strategy adult females will adopt later in life. Lower levels of maternal care are associated with early onset of puberty as well as increased motivation to mate and greater receptivity toward males during mating. Lower levels of maternal care are also correlated with greater activity of the hypothalamus–pituitary–gonadal axis, responsible for the expression of these behaviors. Contrary to the transition of maternal care, sexual behavior cannot simply be explained by maternal attention, since adoption studies changed the sexual phenotypes of offspring born to low caring mothers but not those from high caring dams. Indeed, mothers showing higher levels of licking/grooming have embryos that are exposed to high testosterone levels during development, and adoption studies suggest that this androgen exposure may protect their offspring from lower levels of maternal care. We propose that in the rat, maternal care and the in utero environment interact to influence the reproductive strategy female offspring display in adulthood and that this favors the species by allowing it to thrive under different environmental conditions.
Keywords
References
- Belsky J., Steinberg L., Houts R., Halpern-Felsher B., Network N. E. C. C. R. (2010). The development of reproductive strategy in females: early maternal harshness –> earlier menarche –> increased sexual risk takingThe development of reproductive strategy in females: early maternal harshness –> earlier menarche –> increased sexual risk taking. Dev. Psychol. 46, 120 – 128. doi:10.1037/a0015549
- Bifulco A., Moran P. M., Ball C., Jacobs C., Baines R., Bunn A., Cavagin J. (2002). Childhood adversity, parental vulnerability and disorder: examining inter-generational transmission of risk. J. Child Psychol. Psychiatry 43, 1075 – 1086. doi:10.1111/1469-7610.00234
- Bird A. P. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6 – 21. doi:10.1101/gad.947102
- Bjornstrom L., Sjoberg M. (2005). Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol. 19, 833 – 842. doi:10.1210/me.2004-0486
- Bredy T. W., Humpartzoomian R. A., Cain D. P., Meaney M. J. (2003). Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience 118, 571 – 576. doi:10.1016/S0306-4522(02)00918-1
- Brouette-Lahlou I., Godinot F., Vernet-Maury E. (1999). The mother rat’s vomeronasal organ is involved in detection of dodecyl propionate, the pup’s preputial gland pheromone. Physiol. Behav. 66, 427 – 436. doi:10.1016/S0031-9384(98)00334-5
- Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P. M., Meaney M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U.S.A. 95, 5335 – 5340. doi:10.1073/pnas.95.9.5335
- Cameron N. M., Del Corpo A., Diorio J., McAllister K., Sharma S., Meaney M. J. (2008a). Maternal programming of sexual behavior and hypothalamic-pituitary-gonadal function in the female rat. PLoS ONE 3, e2210. doi:10.1371/journal.pone.0002210
- Cameron N. M., Fish E. W., Meaney M. J. (2008b). Maternal influences on the sexual behavior and reproductive success of the female rat. Horm. Behav. 54, 178 – 184. doi:10.1016/j.yhbeh.2008.02.013
- Cameron N. M., Shahrokh D., Del Corpo A., Dhir S. K., Szyf M., Champagne F. A., Meaney M. J. (2008c). Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J. Neuroendocrinol. 20, 795 – 801. doi:10.1111/j.1365-2826.2008.01725.x
- Cameron N. M., Soehngen E., Meaney M. J. (2011). Variation in maternal care influences ventromedial hypothalamus activation in the rat. J. Neuroendocrinol. 23, 393 – 400. doi:10.1111/j.1365-2826.2011.02124.x
- Champagne F. A., Francis D. D., Mar A., Meaney M. J. (2003a). Variation in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 79, 359 – 371. doi:10.1016/S0031-9384(03)00149-5
- Champagne F. A., Weaver I. C. G., Diorio J., Sharma S., Meaney M. J. (2003b). Natural variations in maternal care are associated with estrogen receptor α expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144, 4720 – 4724. doi:10.1210/en.2003-0564
- Champagne F. A., Meaney M. J. (2006). Stress During gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol. Psychiatry 59, 1227 – 1235. doi:10.1016/j.biopsych.2005.10.016
- Champagne F. A., Weaver I. C. G., Diorio J., Dymov S., Szyf M., Meaney M. J. (2006). Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147, 2909 – 2915. doi:10.1210/en.2005-1119
- Chapillon P., Patin V., Roy V., Vicent A., Caston J. (2002). Prenatal stress does not alter innate novelty-seeking behavioral traits, but differentially affects individual differences in neuroendocrine stress responsivity. Dev. Psychobiol. 33, 162 – 177.
- Clarkson J., D’Anglemont de Tassigny X., Colledge W. H., Caraty A., Herbison A. E. (2009). Distribution of kisspeptin neurones in the adult female mouse brain. J. Neuroendocrinol. 21, 673 – 682.
- Clinton S., Miller S., Watson S. J., Akil H. (2008). Prenatal stress does not alter innate novelty-seeking behavioral traits, but differentially affects individual differences in neuroendocrine stress responsivity. Psychoneuroendocrinology 33, 162 – 177. doi:10.1016/j.psyneuen.2007.10.012
- Coall D. A., Chisholm J. S. (2003). Evolutionary perspectives on pregnancy: maternal age at menarche and infant birth weight. Soc. Sci. Med. 57, 1771 – 1781. doi:10.1016/S0277-9536(03)00022-4
- Cooper K. J., Fawcett C. P., McCann S. M. (1974). Inhibitory and facilitatory effects of estradiol 17beta on pituitary responsiveness to a luteinizing hormone-follicle stimulating hormone releasing factor (LH-RF–FSH RF) preparation in the ovariectomized rat. Proc. Soc. Exp. Biol. Med. 145, 1422 – 1426.
- De Bellis M. D. (2002). Developmental traumatology: a contributory mechanism for alcohol and substance use disorders. Psychoneuroendocrinology 27, 155 – 170. doi:10.1016/S0306-4530(01)00042-7
- DeFries J. C., Weir M. W., Hegmann J. P. (1967). Differential effects of prenatal maternal stress on offspring behavior in mice as a function of genotype and stress. J. Comp. Physiol. Psychol. 63, 332 – 334. doi:10.1037/h0020842
- Edmonds S., Zoloth S. R., Adler N. T. (1972). Storage of copulatory stimulation in the female rat. Physiol. Behav. 8, 161 – 164. doi:10.1016/0031-9384(72)90354-X
- Erskine M. (1985). Effects of paced coital stimulation on estrus duration in intact cycling rats and ovariectomized and ovariectomized-adrenalectomized hormone-primed rats. Behav. Neurosci. 99, 151 – 161. doi:10.1037/0735-7044.99.1.151
- Erskine M. S. (1989). Solicitation behavior in the estrous female rat: a review. Horm. Behav. 23, 473 – 502. doi:10.1016/0018-506X(89)90037-8
- Erskine M. S., Lehmann M. L., Cameron N. M., Polston E. K. (2004). Co-regulation of female sexual behavior and pregnancy induction: an exploratory synthesis. Behav. Brain Res. 153, 295 – 315. doi:10.1016/j.bbr.2004.01.026
- Fish E., Shahrokh D., Bagot R., Caldji C., Bredy T., Szyf M., Meaney M. (2004). Epigenetic programming of stress responses through variations in maternal care. Ann. N. Y. Acad. Sci. 1036, 167 – 180. doi:10.1196/annals.1330.011
- Fleming A. S., Corter C. (1988). Factors influencing maternal responsiveness in humans: usefulness of an animal model. Psychoneuroendocrinology 13, 189 – 212. doi:10.1016/0306-4530(88)90014-5
- Fleming A. S., O’Day D. H., Kraemer G. W. (1999). Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci. Biobehav. Rev. 23, 673 – 685. doi:10.1016/S0149-7634(99)00011-1
- Francis D., Diorio J., Lui D., Meaney M. J. (1999a). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155 – 1158. doi:10.1126/science.286.5442.1155
- Francis D. D., Caldji C., Champagne F., Plotsky P. M., Meaney M. J. (1999b). The role of corticotropin-releasing factor–norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biol. Psychiatry 46, 1153 – 1166. doi:10.1016/S0006-3223(99)00237-1
- Francis D. D., Diorio J., Plotsky P. M., Meaney M. J. (2002a). Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 22, 7840 – 7843.
- Francis D. D., Young L. J., Meaney M. J., Insel T. R. (2002b). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J. Neuroendocrinol. 14, 349 – 353. doi:10.1046/j.0007-1331.2002.00776.x
- Frasor J., Gibori G. (2003). Prolactin regulation of estrogen receptor expression. Trends Endocrinol. Metab. 14, 118 – 123. doi:10.1016/S1043-2760(03)00030-4
- Gao C., Abou-Nasr R., Norgren R. B. Jr. (1996). Subpopulations of migrating neurons express different levels of LHRH in quail and chick embryos. Brain Res. Dev. Brain Res. 91, 237 – 244. doi:10.1016/0165-3806(95)00189-1
- Georgescu M., Sabongui C., Del Corpo A., Marsan L., Pfaus J. G. (2009). Vaginocervical stimulation induces Fos in glutamate neurons in the ventromedial hypothalamus: attenuation by estrogen and progesterone. Horm. Behav. 56, 450 – 456. doi:10.1016/j.yhbeh.2009.07.014
- Gonzales A., Lovic V., Ward G. R., Wainwright P. E., Fleming A. S. (2001). Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev. Psychol. 38, 11 – 32.
- Hardy D. F., DeBold J. F. (1972). Effects of coital stimulation upon behavior of the female rat. J. Comp. Physiol. Psychol. 78, 449 – 458. doi:10.1037/h0032536
- Heim C., Newport D. J., Heit S., Graham Y. P., Wilcox M., Bonsall R., Miller A. H., Nemeroff C. B. (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284, 592 – 597. doi:10.1001/jama.284.5.592
- Herbison A. E., Theodosis D. T. (1992). Localization of oestrogen receptors in preoptic neurons containing neurotensin but not tyrosine hydroxylase, cholecystokinin or luteinizing hormone-releasing hormone in the male and female rat. Neuroscience 50, 283 – 298. doi:10.1016/0306-4522(92)90423-Y
- Hinde R. A. (1986). “Some implications of evolutionary theory and comparative data for the study of human prosocial and aggressive behaviour,” in Development of Anti-Social and Prosocial Behaviour, eds Olweus D., Block J., Radke-Yarrow M. (Orlando: Academic Press), 13 – 32.
- Huebner A. J., Howell L. W. (2003). Examining the relationship between adolescent sexual risk-taking and perceptions of monitoring, communication, and parenting styles. J. Adolesc. Health 33, 71 – 78. doi:10.1016/S1054-139X(03)00141-1
- Lehmann M. L., Erskine M. S. (2004). Induction of pseudopregnancy using artificial VCS: importance of lordosis intensity and prestimulus estrous cycle length. Horm. Behav. 45, 75 – 83. doi:10.1016/j.yhbeh.2003.09.011
- Levine S. (1967). Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 156, 258 – 260. doi:10.1126/science.156.3783.1744
- Liu D., Diorio J., Day J. C., Francis D. D., Meaney M. J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3, 799 – 806. doi:10.1038/77702
- Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P., Meaney M. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1620 – 1621. doi:10.1126/science.277.5329.1106
- Masur J., Struffaldi G. (1974). Division of labor between rats: influence of differential social rearing conditions. Behav. Biol. 12, 233 – 241. doi:10.1016/S0091-6773(74)91240-1
- McClintock M., Adler N. (1978). The role of the female during copulation in wild and domestic Norway rats (Rattus norvegicus). Behaviour 67, 67 – 96. doi:10.1163/156853978X00260
- McClintock M., Anisko J. (1982). Group mating among Norway rats: sex differences in the pattern and neuroendocrine consequences of copulation. Anim. Behav. 30, 398 – 409. doi:10.1016/S0003-3472(82)80052-3
- McCormack K., Sanchez M., Bardi M., Maestripieri D. (2006). Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev. Psychol. 48, 537 – 550.
- McLoyd V., Wilson L. (1990). Maternal behavior, social support, and economic conditions as predictors of distress in children. New Dir. Child Dev. 46, 49 – 69. doi:10.1002/cd.23219904605
- McLoyd V. C. (1990). The impact of economic hardship on black families and children: psychological distress, parenting, and socioemotional development. Child Dev. 61, 311 – 346. doi:10.1111/j.1467-8624.1990.tb02777.x
- Meschke L. L., Silbereisen R. K. (1997). The influence of puberty, family processes, and leisure activities on the timing of first sexual experience. J. Adolesc. 20, 403 – 418. doi:10.1006/jado.1997.0096
- Moore C. L., Power K. L. (1992). Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring. Dev. Psychol. 25, 165 – 182.
- Ojeda S. R., McCann S. M. (1978). Control of LH and FSH release by LHRH: influence of putative neurotransmitters. Clin. Obstet. Gynaecol. 5, 283 – 303.
- Österlund M. K., Hurd Y. L. (2001). Estrogen receptors in the human forebrain and the relation to neuropsychiatric disorders. Prog. Neurobiol. 64, 251 – 267. doi:10.1016/S0301-0082(00)00059-9
- Phoenix C. H., Goy R. W., Gerall A. A., Young W. C. (1959). Organization action of prenatally administered testosterone propionate on the tissues madiating mating behavior in the female guinea pig. Endocrinology 65, 369 – 382. doi:10.1210/endo-65-3-369
- Rhen T., Crews D. (2002). Variation in reproductive behaviour within a sex: neural systems and endocrine activation. J. Neuroendocrinol. 14, 517 – 531. doi:10.1046/j.1365-2826.2002.00820.x
- Schibler U., Sierra F. (1987). Alternative promoters in developmental gene expression. Annu. Rev. Genet. 21, 237 – 257. doi:10.1146/annurev.ge.21.120187.001321
- Seymour L. (2005). Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30, 939 – 946. doi:10.1016/j.psyneuen.2005.03.013
- Shughrue P. J., Lane M. V., Merchenthaler I. (1997). Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388, 507 – 525. doi:10.1002/(SICI)1096-9861(19971201)388:4<507::AID-CNE1>3.0.CO;2-6
- Suomi S. (1978). Maternal behavior by socially incompetent monkeys: neglect and abuse of offspring. J. Pediatr. Psychol. 3, 28 – 34. doi:10.1093/jpepsy/3.1.28
- Terasawa E., Kurian J. R., Guerriero K. A., Kenealy B. P., Hutz E. D., Keen K. L. (2010). Recent discoveries on the control of gonadotrophin-releasing hormone neurones in nonhuman primates. J. Neuroendocrinol. 22, 630 – 638.
- Tu M. T., Lupien S. J., Walker C.-D. (2005). Measuring stress responses in postpartum mothers: perspectives from studies in human and animal populations. Stress 8, 19 – 34. doi:10.1080/10253890500103806
- van Hasselt F. N., Cornelisse S., Yuan Zhang T., Meaney M. J., Velzing E. H., Krugers H. J., Joëls M. (2011). Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus. [Epub ahead of print]. doi:10.1002/hipo.20892
- Waddington C. H. (1942). The epigenotype. Endeavour 1, 18 – 20.
- Walf A. A., Ciriza I., Garcia-Segura L. M., Frye C. A. (2007). Antisense oligodeoxynucleotides for estrogen receptor-[beta] and [alpha] attenuate estradiol’s modulation of affective and sexual behavior, respectively. Neuropsychopharmacology 33, 431 – 440. doi:10.1038/sj.npp.1301416
- Weaver I. C., Diorio J., Seckl J. R., Szyf M., Meaney M. J. (2004a). Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Ann. N. Y. Acad. Sci. 1024, 182 – 212. doi:10.1196/annals.1321.099
- Weaver I. C. G., Cervoni N., Champagne F. A., D’Alessio A. C., Sharma S., Seckl J. R., Dymov S., Szyf M., Meaney M. J. (2004b). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847 – 854. doi:10.1038/nn1276
- Weaver I. C. G., Champagne F. A., Brown S. E., Dymov S., Sharma S., Meaney M. J., Szyf M. (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 25, 11045 – 11054. doi:10.1523/JNEUROSCI.3652-05.2005
- Widom C. S., Maxfield M. G. (1996). A prospective examination of risk for violence among abused and neglected childrena. Ann. N. Y. Acad. Sci. 794, 224 – 237. doi:10.1111/j.1749-6632.1996.tb32523.x
- Wray S., Hoffman G. E. (1986). A developmental study of the quantitative distribution of LHRH neurons within the central nervous system of postnatal male and female rats. J. Comp. Neurol. 252, 522 – 531. doi:10.1002/cne.902520408
- Yeo S.-H., Herbison A. E. (2011). Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology 152, 2387 – 2399. doi:10.1210/en.2011-0164
Citation
Cameron, N. M. (2011). Maternal Programming of Reproductive Function and Behavior in the Female Rat. Frontiers in Evolutionary Neuroscience, Volume 3. https://doi.org/
- Received
- Accepted
- Published
- Volume
- 3 - 2011
Copyright
Copyright © 2011 Cameron.
License: http://www.frontiersin.org/licenseagreement
*Correspondence: Nicole M. Cameron
Article metrics
- Views
- 0
- Downloads
- 0
- Citations
- 0
- Shares
- 0
