Bisphenol S (BPS) alters maternal behavior and brain in mice exposed during pregnancy/lactation and their daughters

Endocrinology

Volumn 158, Issue 3, 2017, Pages 516-530

  Catanese, Mary C ^a   Vandenberg, Laura N ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISPHENOL S; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; BIS(4-HYDROXYPHENYL)SULFONE; PHENOL DERIVATIVE; SULFONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH; BRAIN REGION; CHILD NEGLECT; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; INFANTICIDE; LACTATION; LATENT PERIOD; MATERNAL BEHAVIOR; MATERNAL CARE; MEDIAL PREOPTIC AREA; MOUSE; NESTING; NONHUMAN; PERINATAL DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; PROGENY; PUERPERIUM; QUANTITATIVE ANALYSIS; VENTRAL TEGMENTUM; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; PRENATAL EXPOSURE; PREOPTIC AREA;

ANIMALS; BRAIN; ENDOCRINE DISRUPTORS; ESTROGEN RECEPTOR ALPHA; FEMALE; LACTATION; MATERNAL BEHAVIOR; MICE; NESTING BEHAVIOR; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PREOPTIC AREA; SULFONES; TYROSINE 3-MONOOXYGENASE;

EID: 85014422940     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1723     Document Type: Article

References (109)

1. Fahrbach SE, Pfaff DW. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm Behav. 1986;20(3):354-363.
2. Numan M, Rosenblatt JS, Komisaruk BR. Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol. 1977;91(1):146-164.
3. Wagner CK, Morrell JI. In situ analysis of estrogen receptor mRNA expression in the brain of female rats during pregnancy. Brain Res Mol Brain Res. 1995;33(1):127-135.
4. Giordano AL, Ahdieh HB, Mayer AD, Siegel HI, Rosenblatt JS. Cytosol and nuclear estrogen receptor binding in the preoptic area and hypothalamus of female rats during pregnancy and ovariectomized, nulliparous rats after steroid priming: correlation with maternal behavior. Horm Behav. 1990;24(2):232-255.
5. Giordano AL, Siegel HI, Rosenblatt JS. Nuclear estrogen receptor binding in the preoptic area and hypothalamus of pregnancyterminated rats: correlation with the onset of maternal behavior. Neuroendocrinology. 2008;50(3):248-258.
6. Giordano AL, Siegel HI, Rosenblatt JS. Nuclear estrogen receptor binding in microdissected brain regions of female rats during pregnancy: implications for maternal and sexual behavior. Physiol Behav. 1991;50(6):1263-1267.
7. Numan M, Insel T. The Neurobiology of Parental Behavior. New York, NY: Springer Verlag; 2003.
8. Jacobson CD, Terkel J, Gorski RA, Sawyer CH. Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res. 1980;194(2):471-478.
9. Numan M. Long-term effects of preoptic area knife cuts on the maternal behavior of postpartum rats. Behav Neural Biol. 1990; 53(2):284-290.
10. Wiesner BP, Sheard NM. Maternal Behaviour in the Rat. Oxford, UK: Oliver and Boyd; 1933.
11. Leblond C. Extrahormonal factors in maternal behavior. Proc Soc Exp Biol Med. 1938;38:66-70.
12. Leblond C. Nervous and hormonal factors in the maternal behavior of the mouse. J Genet Psychol. 1940;57:327-344.
13. Rosenblatt JS. Nonhormonal basis of maternal behavior in the rat. Science. 1967;156(3781):1512-1513.
14. Stolzenberg DS, Rissman EF. Oestrogen-independent, experienceinduced maternal behaviour in female mice. J Neuroendocrinol. 2011;23(4):345-354.
15. Gandelman R. Maternal behavior in the mouse: effect of estrogen and progesterone. Physiol Behav. 1973;10(1):153-155.
16. Hauser H, Gandelman R. Lever pressing for pups: evidence for hormonal influence upon maternal behavior of mice. Horm Behav. 1985;19(4):454-468.
17. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW. Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in femalemice. Endocrinology. 1998;139(12):5070-5081.
18. Ribeiro AC, Musatov S, Shteyler A, Simanduyev S, Arrieta-Cruz I, Ogawa S, Pfaff DW. siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice. Proc Natl Acad Sci USA. 2012; 109(40):16324-16329.
19. Welshons WV, Nagel SC, vom Saal FS. Large effects from small exposures: III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology. 2006; 147(6, Suppl):S56-S69.
20. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev. 2009;30(1):75-95.
21. Colborn T, vom Saal FS, Soto AM. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993;101(5):378-384.
22. Watson CS, Pappas TC, Gametchu B. The other estrogen receptor in the plasma membrane: implications for the actions of environmental estrogens. Environ Health Perspect. 1995;103(Suppl 7):41-50.
23. Vandenberg LN, Ehrlich S, Belcher SM, Ben-Jonathan N, Dolinoy DC, Hugo ER, Hunt PA, Newbold RR, Rubin BS, Saili KS, Soto AM, Wang HS, Vom Saal FS. Low dose effects of bisphenol A: an integrated review of in vitro, laboratory animal and epidemiology studies. Endocr Disruptors (Austin). 2013;1(1):e25078.
24. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007; 24(2):139-177.
25. vom Saal FS, Akingbemi BT, Belcher SM, Birnbaum LS, Crain DA, Eriksen M, Farabollini F, Guillette LJ Jr, Hauser R, Heindel JJ, Ho SM, Hunt PA, Iguchi T, Jobling S, Kanno J, Keri RA, Knudsen KE, Laufer H, LeBlanc GA, Marcus M, McLachlan JA, Myers JP, Nadal A, Newbold RR, Olea N, Prins GS, Richter CA, Rubin BS, Sonnenschein C, Soto AM, Talsness CE, Vandenbergh JG, Vandenberg LN, Walser-Kuntz DR, Watson CS, Welshons WV, Wetherill Y, Zoeller RT. Chapel Hill bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol. 2007;24(2):131-138.
26. Wolstenholme JT, Rissman EF, Connelly JJ. The role of bisphenol A in shaping the brain, epigenome and behavior. Horm Behav. 2011;59(3):296-305.
27. Della Seta D, Minder I, Dessí-Fulgheri F, Farabollini F. Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Res Bull. 2005;65(3):255-260.
28. Palanza PL, Howdeshell KL, Parmigiani S, vom Saal FS. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ Health Perspect. 2002; 110(Suppl 3):415-422.
29. Cox KH, Gatewood JD, Howeth C, Rissman EF. Gestational exposure to bisphenol A and cross-fostering affect behaviors in juvenile mice. Horm Behav. 2010;58(5):754-761.
30. Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller RL, Perera FP, Champagne FA. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci USA. 2013;110(24):9956-9961.
31. Johnson SA, Javurek AB, Painter MS, Peritore MP, Ellersieck MR, Roberts RM, Rosenfeld CS. Disruption of parenting behaviors in California mice, a monogamous rodent species, by endocrine disrupting chemicals. PLoS One. 2015;10(6):e0126284.
32. Boudalia S, Berges R, Chabanet C, Folia M, Decocq L, Pasquis B, Abdennebi-Najar L, Canivenc-Lavier MC. A multi-generational study on low-dose BPA exposure in Wistar rats: effects on maternal behavior, flavor intake and development. Neurotoxicol Teratol. 2014;41:16-26.
33. Liao C, Liu F, Kannan K. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and itsassociationwithbisphenol a residues. Environ Sci Technol. 2012;46(12):6515-6522.
34. Liao C, Kannan K. Concentrations and profiles of bisphenolA and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure. J Agric Food Chem. 2013; 61(19):4655-4662.
35. Liao C, Kannan K. A survey of alkylphenols, bisphenols, and triclosan in personal care products from China and the United States. Arch Environ Contam Toxicol. 2014;67(1):50-59.
36. Simoneau C, Valzacchi S, Morkunas V, Van den Eede L. Comparison of migration from polyethersulphone and polycarbonate baby bottles. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2011;28(12):1763-1768.
37. Liao C, Liu F, Alomirah H, Loi VD, Mohd MA, Moon HB, Nakata H, Kannan K. Bisphenol S in urine from the United States and seven Asian countries: occurrence and human exposures. Environ Sci Technol. 2012;46(12):6860-6866.
38. Ye X, Wong LY, Kramer J, Zhou X, Jia T, Calafat AM. Urinary concentrations of bisphenol A and three other bisphenols in convenience samples of U.S. adults during 2000-2014. Environ Sci Technol. 2015;49(19):11834-11839.
39. Kuruto-Niwa R, Nozawa R, Miyakoshi T, Shiozawa T, Terao Y. Estrogenic activity of alkylphenols, bisphenol S, and their chlorinated derivatives using a GFP expression system. Environ Toxicol Pharmacol. 2005;19(1):121-130.
40. Molina-Molina JM, Amaya E, Grimaldi M, Sáenz JM, Real M, Fernández MF, Balaguer P, Olea N. In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-A congeners and derivatives via nuclear receptors. Toxicol Appl Pharmacol. 2013;272(1):127-136.
41. Viñas R, Watson CS. Bisphenol S disrupts estradiol-induced nongenomic signaling in a rat pituitary cell line: effects on cell functions. Environ Health Perspect. 2013;121(3):352-358.
42. Kim B, Colon E, Chawla S, Vandenberg LN, Suvorov A. Endocrine disruptors alter social behaviors and indirectly influence social hierarchies via changes in body weight. Environ Health. 2015;14:64.
43. Castro B, Sánchez P, Torres JM, Ortega E. Bisphenol A, bisphenol F and bisphenol S affect differently 5α-reductase expression and dopamine-serotonin systems in the prefrontal cortex of juvenile female rats. Environ Res. 2015;142:281-287.
44. Numan M, Stolzenberg DS. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol. 2009;30(1):46-64.
45. Pereira M, Morrell JI. Functional mapping of the neural circuitry of rat maternal motivation: effects of site-specific transient neural inactivation. J Neuroendocrinol. 2011;23(11):1020-1035.
46. Morrell JI, Schwanzel-Fukuda M, Fahrbach SE, Pfaff DW. Axonal projections and peptide content of steroid hormone concentrating neurons. Peptides. 1984;5(Suppl 1):227-239.
47. Fahrbach SE, Morrell JI, Pfaff DW. Identification of medial preoptic neurons that concentrate estradiol and project to the midbrain in the rat. J Comp Neurol. 1986;247(3):364-382.
48. Shahrokh DK, Zhang TY, Diorio J, Gratton A, Meaney MJ. Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology. 2010;151(5):2276-2286.
49. Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, Rubin BS, Soto AM. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol. 2008;26(3-4):210-219.
50. Gauger KJ, Giera S, Sharlin DS, Bansal R, Iannacone E, Zoeller RT. Polychlorinated biphenyls 105 and 118 form thyroid hormone receptor agonists after cytochrome P4501A1 activation in rat pituitary GH3 cells. Environ Health Perspect. 2007;115(11):1623-1630.
51. US EPA. BisphenolA Alternatives in Thermal Paper, Final Report. Available at: https://www.epa.gov/sites/production/files/2015-08/documents/bpa-final.pdf. Accessed 14 November 2016.
52. Vandenberg LN. Low-dose effects of hormones and endocrine disruptors. Vitam Horm. 2014;94:129-165.
53. Holmes A, le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev. 2005; 29(8):1335-1346.
54. Suvorov A, Vandenberg LN. To cull or not to cull? Considerations for studies of endocrine-disrupting chemicals. Endocrinology. 2016;157(7):2586-2594.
55. Catanese MC, Suvorov A, Vandenberg LN. Beyond a means of exposure: a new view of the mother in toxicology research. Toxicol Res. 2015;4(3):592-612.
56. Hess SE, Rohr S, Dufour BD, Gaskill BN, Pajor EA, Garner JP. Home improvement: C57BL/6J mice given more naturalistic nesting materials build better nests. J Am Assoc Lab Anim Sci. 2008;47(6):25-31.
57. Franklin K, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press; 1997.
58. Franklin K, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 4th ed. San Diego, CA: Academic Press; 2012.
59. van der Loos CM. Multiple immunoenzyme staining: methods and visualizations for the observation with spectral imaging. J Histochem Cytochem. 2007;56(4):313-328.
60. Rudbeck L. Adding quality to your qualitative IHC. MLO Med Lab Obs. 2015;47(12):18-19, 21.
61. Tsuneoka Y, Maruyama T, Yoshida S, Nishimori K, Kato T, Numan M, Kuroda KO. Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J Comp Neurol. 2013;521(7):1633-1663.
62. Yamaguchi T, Qi J, Wang HL, Zhang S, Morales M. Glutamatergic and dopaminergic neurons in the mouse ventral tegmental area. Eur J Neurosci. 2015;41(6):760-772.
63. Kelly DA, Varnum MM, Krentzel AA, Krug S, Forger NG. Differential control of sex differences in estrogen receptor α in the bed nucleus of the stria terminalis and anteroventral periventricular nucleus. Endocrinology. 2013;154(10):3836-3846.
64. Hall C. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J Comp Psychol. 1934;18:385-403.
65. Hall C. Emotional behavior in the rat: II. The relationship between need and emotionality. J Comp Psychol. 1936;22:61-68.
66. Archer J. Tests for emotionality in rats and mice: a review. Anim Behav. 1973;21(2):205-235.
67. Belzung C, Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res. 2001; 125(1-2):141-149.
68. Prut L, Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol. 2003;463(1-3):3-33.
69. Spruijt BM, Peters SM, de Heer RC, Pothuizen HH, van der Harst JE. Reproducibility and relevance of future behavioral sciences should benefit from a cross fertilization of past recommendations and today's technology: "back to the future". J Neurosci Methods. 2014;234:2-12.
70. Shoji H, Kato K. Maternal behavior of primiparous females in inbred strains of mice: a detailed descriptive analysis. Physiol Behav. 2006;89(3):320-328.
71. Pereira M, Ferreira A. Neuroanatomical and neurochemical basis of parenting: dynamic coordination of motivational, affective and cognitive processes. Horm Behav. 2016;77:72-85.
72. Lonstein JS, Morrell JI. Neuropharmacology and neuroendocrinology ofmaternal motivation and behavior. In: Blaustein JD, ed. Handbook of Neurochemistry and Molecular Biology: Vol 18-Behavioral Neurobiology. New York, NY: Springer; 2007:195-245.
73. Korff S, Harvey BH. Animal models of obsessive-compulsive disorder: rationale to understanding psychobiology and pharmacology. Psychiatr Clin North Am. 2006;29(2):371-390.
74. Albelda N, Joel D. Current animal models of obsessive compulsive disorder: an update. Neuroscience. 2012;211:83-106.
75. Greene-Schloesser DM, Van der Zee EA, Sheppard DK, Castillo MR, Gregg KA, Burrow T, Foltz H, Slater M, Bult-Ito A. Predictive validity of a non-induced mouse model of compulsive-like behavior. Behav Brain Res. 2011;221(1):55-62.
76. Alonso P, López-Solà C, Real E, Segalàs C, Menchón JM. Animal models of obsessive-compulsive disorder: utility and limitations. Neuropsychiatr Dis Treat. 2015;11:1939-1955.
77. Tomic D, Frech MS, Babus JK, Symonds D, Furth PA, Koos RD, Flaws JA. Effects of ERalpha overexpression on female reproduction in mice. Reprod Toxicol. 2007;23(3):317-325.
78. Witty CF, Foster TC, Semple-Rowland SL, Daniel JM. Increasing hippocampal estrogen receptor alpha levels via viral vectors increases MAP kinase activation and enhances memory in aging rats in the absence of ovarian estrogens. PLoS One. 2012;7(12):e51385.
79. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS, Wise PM. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci USA. 2001;98(4):1952-1957.
80. Shughrue PJ, Bushnell CD, Dorsa DM. Estrogen receptor messenger ribonucleic acid in female rat brain during the estrous cycle: a comparison with ovariectomized females and intact males. Endocrinology. 1992;131(1):381-388.
81. Zhou Y, Shughrue PJ, Dorsa DM. Estrogen receptor protein is differentially regulated in the preoptic area of the brain and in the uterus during the rat estrous cycle. Neuroendocrinology. 2008; 61(3):276-283.
82. Rosenblatt JS, Wagner CK, Morrell JI. Hormonal priming and triggering of maternal behavior in the rat with special reference to the relations between estrogen receptor binding and ER mRNA in specific brain regions. Psychoneuroendocrinology. 1994;19(5-7): 543-552.
83. Wagner CK, Morrell JI. Levels of estrogen receptor immunoreactivity are altered in behaviorally-relevant brain regions in female rats during pregnancy. Brain Res Mol Brain Res. 1996;42(2):328-336.
84. Koch M, Ehret G. Immunocytochemical localization and quantitation of estrogen-binding cells in the male and female (virgin, pregnant, lactating) mouse brain. Brain Res. 1989;489(1):101-112.
85. Murakami G. Distinct effects of estrogen on mouse maternal behavior: the contribution of estrogen synthesis in the brain. PLoS One. 2016;11(3):e0150728.
86. Aloisi AM, Della Seta D, Ceccarelli I, Farabollini F. Bisphenol-A differently affects estrogen receptors-alpha in estrous-cycling and lactating female rats. Neurosci Lett. 2001;310(1):49-52.
87. Phoenix CH, Goy RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology. 1959;65:369-382.
88. Arnold AP, Gorski RA. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci. 1984;7:413-442.
89. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, vom Saal FS. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007;24(2):199-224.
90. Monje L, Varayoud J, Luque EH, Ramos JG. Neonatal exposure to bisphenol A modifies the abundance of estrogen receptor alpha transcripts with alternative 5′-untranslated regions in the female rat preoptic area. J Endocrinol. 2007;194(1):201-212.
91. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. 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. 2006;147(6):2909-2915.
92. Champagne FA, Curley JP. Maternal regulation of estrogen receptor alpha methylation. Curr Opin Pharmacol. 2008;8(6):735-739.
93. Cummings JA, Clemens LG, Nunez AA. Mother counts: how effects of environmental contaminants on maternal care could affect the offspring and future generations. Front Neuroendocrinol. 2010;31(4):440-451.
94. Palanza P, Nagel SC, Parmigiani S, Vom Saal FS. Perinatal exposure to endocrine disruptors: sex, timing and behavioral endpoints. Curr Opin Behav Sci. 2016;7:69-75.
95. Alonso-Magdalena P, Vieira E, Soriano S, Menes L, Burks D, Quesada I, Nadal A. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010;118(9):1243-1250.
96. Alonso-Magdalena P, García-Arévalo M, Quesada I, Nadal Á. Bisphenol-A treatment during pregnancy in mice: a new window of susceptibility for the development of diabetes in mothers later in life. Endocrinology. 2015;156(5):1659-1670.
97. Walker DM, Gore AC. Transgenerational neuroendocrine disruption of reproduction. Nat Rev Endocrinol. 2011;7(4):197-207.
98. Cummings JA, Nunez AA, Clemens LG. A cross-fostering analysis of the effects of PCB 77 on the maternal behavior of rats. Physiol Behav. 2005;85(2):83-91.
99. Gioiosa L, Parmigiani S, Vom Saal FS, Palanza P. The effects of bisphenol A on emotional behavior depend upon the timing of exposure, age and gender in mice. Horm Behav. 2013;63(4):598-605.
100. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci. 1995; 15(1 Pt 1):110-116.
101. Curley JP, Rock V, Moynihan AM, Bateson P, Keverne EB, Champagne FA. Developmental shifts in the behavioral phenotypes of inbred mice: the role of postnatal and juvenile social experiences. Behav Genet. 2010;40(2):220-232.
102. Cox KH, So NL, Rissman EF. Foster dams rear fighters: strainspecific effects of within-strain fostering on aggressive behavior in male mice. PLoS One. 2013;8(9):e75037.
103. Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, Nemeroff CB, Reyes TM, Simerly RB, Susser ES, Nestler EJ. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010;68(4):314-319.
104. Barrett J, Fleming AS. Annual research review: all mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. J Child Psychol Psychiatry. 2010;52(4):368-397.
105. Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry. 2001;49(12):1023-1039.
106. Nemeroff CB. Neurobiological consequences of childhood trauma. J Clin Psychiatry. 2004;65(Suppl 1):18-28.
107. Reisbick S, Rosenblatt JS, Mayer AD. Decline of maternal behavior in the virgin and lactating rat. J Comp Physiol Psychol. 1975;89(7):722-732.
108. Uriarte N, Ferreira A, Rosa XF, Sebben V, Lucion AB. Overlapping litters in rats: effects on maternal behavior and offspring emotionality. Physiol Behav. 2008;93(4-5):1061-1070.
109. Bridges RS. Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol. 2015;36:178-196.