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Testosterone–cortisol dissociation in children exposed to prenatal maternal stress, and relationship with aggression: Project Ice Storm

  • Tuong-Vi Nguyen (a1), Sherri L. Jones (a2) (a3), Guillaume Elgbeili (a2), Patricia Monnier (a1), Chunbo Yu (a4), David P. Laplante (a2) and Suzanne King (a2) (a3)...
  • Please note an addendum has been issued for this article.

Abstract

Prenatal maternal stress (PNMS) has been associated with postnatal behavioral alterations that may be partly explained by interactions between the hypothalamic–pituitary–adrenal (HPA) and hypothalamic–pituitary–gonadal (HPG) axes. Yet it remains unclear whether PNMS leads to enduring HPA–HPG alterations in the offspring, and whether HPA–HPG interactions can impact behavior during development, in particular levels of aggression in childhood. Here we investigated the relationship between a marker for HPG axis function (baseline testosterone) and a marker for HPA axis response (cortisol area under the curve) in 11½-year-olds whose mothers were exposed to the 1998 Quebec ice storm during pregnancy (n = 59 children; 31 boys, 28 girls). We examined (a) whether the degree of objective or subjective PNMS regulates the testosterone–cortisol relationship at age 11½, and (b) whether this testosterone–cortisol relationship is associated with differences in aggressive behavior. We found that, at lower levels of subjective PNMS, baseline testosterone and cortisol reactivity were positively correlated; in contrast, there was no relationship between these hormones at higher levels of subjective PNMS. Cortisol response moderated the relationship between testosterone and aggression. These results support the notion PNMS may explain variance in fetal HPA–HPG interactions, and that these interactions may be associated with aggressive behavior in late childhood.

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Corresponding author

Address correspondence and reprint requests to: Suzanne King, Douglas Mental Health University Institute, 6875 LaSalle Blvd., Verdun, QC, Canada H4H 1R3; E-mail: suzanne.king@mcgill.ca.

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The Montreal General Foundation and the Senator W. David Angus Award for Research in Major Psychiatric Diseases provided a salary award for Tuong-Vi Nguyen. The Integrated Research Network in Perinatology of Quebec and Eastern Ontario provided operating funds for this project. The Canadian Institutes of Health Research provided operating funds for Project Ice Storm (S. King, Principal Investigator). Tuong-Vi Nguyen is a Fonds de Recherche Sante Quebec (FRQS) Clinician Scientist and received funding from MERCK, SHARP and DOHME, the Research Institute of the McGill University Health Center, the Montreal General Hospital and Royal Victoria Hospital Foundations, the Senator W. David Angus Award ,and the Integrated Research Network in Perinatology of Quebec and Eastern Ontario. All other coauthors, as part of Suzanne King's lab, received funding from the Canadian Institutes of Health Research. Sherri Lee Jones is funded by a Postdoctoral Fellowship awarded by FRQS.

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References

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Adler, G., & Achenbach, C. (2001). Verbal perseveration after right-unilateral ECT. European Psychiatry, 16, 7578.
Anderson, R. H., Fleming, D. E., Rhees, R. W., & Kinghorn, E. (1986). Relationships between sexual-activity, plasma testosterone, and the volume of the sexually dimorphic nucleus of the preoptic area in prenatally stressed and nonstressed rats. Brain Research, 370, 110.
Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319345. doi:10.1016/j.neubiorev.2004.12.007
August, G. P., Tkachuk, M., & Grumbach, M. M. (1969). Plasma testosterone-binding affinity and testosterone in umbilical cord plasma, late pregnancy, prepubertal children, and adults. Journal of Clinical Endocrinology and Metabolism, 29, 891899. doi:10.1210/jcem-29-7-891
Bale, T. L. (2011). Sex differences in prenatal epigenetic programing of stress pathways. Stress, 14, 348356. doi:10.3109/10253890.2011.586447
Barrett, E. S., Parlett, L. E., Sathyanarayana, S., Liu, F., Redmon, J. B., Wang, C., & Swan, S. H. (2013). Prenatal exposure to stressful life events is associated with masculinized anogenital distance (AGD) in female infants. Physiology & Behavior, 114, 1420. doi:10.1016/j.physbeh.2013.03.004
Beck, J. G., Grant, D. M., Read, J. P., Clapp, J. D., Coffey, S. F., Miller, L. M., & Palyo, S. A. (2008). The impact of event scale-revised: Psychometric properties in a sample of motor vehicle accident survivors. Journal of Anxiety Disorders, 22, 187198. doi:10.1016/j.janxdis.2007.02.007
Bergman, K., Glover, V., Sarkar, P., Abbott, D. H., & O'Connor, T. G. (2010). In utero cortisol and testosterone exposure and fear reactivity in infancy. Hormones and Behavior, 57, 306312. doi:10.1016/j.yhbeh.2009.12.012
Bordin, I. A., Rocha, M. M., Paula, C. S., Teixeira, M. C. T. V., Achenbach, T. M., Rescorla, L. A., & Silvares, E. F. M. (2013). Child Behavior Checklist (CBCL), Youth Self-Report (YSR) and Teacher's Report Form (TRF): An overview of the development of the original and Brazilian versions. Cadernos De Saude Publica, 29, 1328.
Brambilla, D. J., Matsumoto, A. M., Araujo, A. B., & McKinlay, J. B. (2009). The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in men. Journal of Clinical Endocrinology and Metabolism, 94, 907913. doi:10.1210/jc.2008-1902
Brennan, P. A., Pargas, R., Walker, E. F., Green, P., Newport, D. J., & Stowe, Z. (2008). Maternal depression and infant cortisol: Influences of timing, comorbidity and treatment. Journal of Child Psychology and Psychiatry, 49, 10991107. doi:10.1111/j.1469-7610.2008.01914
Brunet, A., St.-Hilaire, A., Jehel, L., & King, S. (2003). Validation of a French version of the Impact of Event Scale—Revised. Canadian Journal of Psychiatry, 48, 5661. doi:10.1177/070674370304800111
Buss, C., Davis, E. P., Shahbaba, B., Pruessner, J. C., Head, K., & Sandman, C. A. (2012). Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences of the United States of America, 109, E1312E1319. doi:10.1073/pnas.1201295109
Buss, C., Entringer, S., Reyes, J. F., Chicz-DeMet, A., Sandman, C. A., Waffarn, F., & Wadhwa, P. D. (2009). The maternal cortisol awakening response in human pregnancy is associated with the length of gestation. American Journal of Obstetrics and Gynecology, 201, 398 e1e8. doi:10.1016/j.ajog.2009.06.063
Canton, R. F., Scholten, D. E., Marsh, G., de Jong, P. C., & Van den Berg, M. (2008). Inhibition of human placental aromatase activity by hydroxylated polybrominated diphenyl ethers (OH-PBDEs). Toxicology and Applied Pharmacology, 227, 6875. doi:10.1016/j.taap.2007.09.025
Cao, X. J., Laplante, D. P., Brunet, A., Ciampi, A., & King, S. (2014). Prenatal maternal stress affects motor function in 5 1/2-year-old children: Project Ice Storm. Developmental Psychobiology, 56, 117125. doi:10.1002/dev.21085
Cao-Lei, L., Dancause, K. N., Elgbeili, G., Massart, R., Szyf, M., Liu, A. H., … King, S. (2015). DNA methylation mediates the impact of exposure to prenatal maternal stress on BMI and central adiposity in children at age 13 1/2 years: Project Ice Storm. Epigenetics, 10, 749761. doi:10.1080/15592294.2015.1063771
Cao-Lei, L., Massart, R., Suderman, M. J., Machnes, Z., Elgbeili, G., Laplante, D. P., … King, S. (2014). DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: Project Ice Storm. PLOS ONE, 9. doi:10.1371/journal.pone.0107653
Chamoux, E., Otis, M., & Gallo-Payet, N. (2005). A connection between extracellular matrix and hormonal signals during the development of the human fetal adrenal gland. Brazilian Journal of Medical and Biological Research, 38, 14951503. doi:10.1590/S0100-879X2005001000006
Choi, J. C., Lee, J. H., Choi, E., Chung, M. I., Seo, S. M., & Lim, H. K. (2014). Effects of seasonal differences in testosterone and cortisol levels on pain responses under resting and anxiety conditions. Yonsei Medical Journal, 55, 216223. doi:10.3349/ymj.2014.55.1.216
Crofton, P. M., Evans, A. E., Groome, N. P., Taylor, M. R., Holland, C. V., & Kelnar, C. J. (2002). Dimeric inhibins in girls from birth to adulthood: Relationship with age, pubertal stage, FSH and oestradiol. Clinical Endocrinology, 56, 223230. doi:10.1046/j.0300-0664.2001.01449.x
Dabbs, J. M. (1991). Salivary testosterone measurements—Collecting, storing, and mailing saliva samples. Physiology & Behavior, 49, 815817. doi:10.1016/0031-9384(91)90323-G
Dabbs, J. M., Jurkovic, G. J., & Frady, R. L. (1991). Salivary testosterone and cortisol among late adolescent male-offenders. Journal of Abnormal Child Psychology, 19, 469478.
Dancause, K. N., Laplante, D. P., Fraser, S., Brunet, A., Ciampi, A., Schmitz, N., & King, S. (2012). Prenatal exposure to a natural disaster increases risk for obesity in 5(1/2)-year-old children. Pediatric Research, 71, 126131. doi:10.1038/pr.2011.18
Dancause, K. N., Laplante, D. P., Oremus, C., Fraser, S., Brunet, A., & King, S. (2011). Disaster-related prenatal maternal stress influences birth outcomes: Project Ice Storm. Early Human Development, 87, 813820. doi:10.1016/j.earlhumdev.2011.06.007
Dancause, K. N., Veru, F., Andersen, R. E., Laplante, D. P., & King, S. (2013). Prenatal stress due to a natural disaster predicts insulin secretion in adolescence. Early Human Development, 89, 773776. doi:10.1016/j.earlhumdev.2013.06.006
de Almeida, R. M., Cabral, J. C., & Narvaes, R. (2015). Behavioural, hormonal and neurobiological mechanisms of aggressive behaviour in human and nonhuman primates. Physiology & Behavior, 143, 121135. doi:10.1016/j.physbeh.2015.02.053
Denson, T. F., Mehta, P. H., & Tan, D. H. (2013). Endogenous testosterone and cortisol jointly influence reactive aggression in women. Psychoneuroendocrinology, 38, 416424. doi:10.1016/j.psyneuen.2012.07.003
Dismukes, A. R., Johnson, M. M., Vitacco, M. J., Iturri, F., & Shirtcliff, E. A. (2015). Coupling of the HPA and HPG axes in the context of early life adversity in incarcerated male adolescents. Developmental Psychobiology, 57, 705718. doi:10.1002/dev.21231
Duchesne, A., Liu, A., Jones, S. L., Laplante, D. P., & King, S. (2017). Childhood body mass index at 5.5 years mediates the effect of prenatal maternal stress on daughters' age at menarche: Project Ice Storm. Journal of Developmental Origins of Health and Disease, 8, 168177. doi:10.1017/S2040174416000726
Eatough, E. M., Shirtcliff, E. A., Hanson, J. L., & Pollak, S. D. (2009). Hormonal reactivity to MRI scanning in adolescents. Psychoneuroendocrinology, 34, 12421246. doi:10.1016/j.psyneuen.2009.03.006
Ebling, F. J. P., & Cronin, A. S. (1998). Manipulations of glutamatergic (N-methyl-D-aspartate receptor) neurotransmission alter the rate of photoperiodically regulated sexual maturation in the male Siberian hamster. Biology of Reproduction, 58, 17. doi:10.1095/biolreprod58.1.1
Entringer, S., Buss, C., Shirtcliff, E. A., Cammack, A. L., Yim, I. S., Chicz-DeMet, A., … Wadhwa, P. D. (2010). Attenuation of maternal psychophysiological stress responses and the maternal cortisol awakening response over the course of human pregnancy. Stress, 13, 258268. doi:10.3109/10253890903349501
Entringer, S., Kumsta, R., Hellhammer, D. H., Wadhwa, P. D., & Wust, S. (2009). Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Hormones and Behavior, 55, 292298. doi:10.1016/j.yhbeh.2008.11.006
Fekedulegn, D. B., Andrew, M. E., Burchfiel, C. M., Violanti, J. M., Hartley, T. A., Charles, L. E., & Miller, D. B. (2007). Area under the curve and other summary indicators of repeated waking cortisol measurements. Psychosomatic Medicine, 69, 651659. doi:10.1097/PSY.0b013e31814c405c
Gerra, G., Zaimovic, A., Avanzini, P., Chittolini, B., Giucastro, G., Caccavari, R., … Brambilla, F. (1997). Neurotransmitter-neuroendocrine responses to experimentally induced aggression in humans: Influence of personality variable. Psychiatry Research, 66, 3343. doi:10.1016/S0165-1781(96)02965-4
Glover, V., O'Connor, T. G., & O'Donnell, K. (2010). Prenatal stress and the programming of the HPA axis. Neuroscience and Biobehavioral Reviews, 35, 1722. doi:10.1016/j.neubiorev.2009.11.008
Granger, D. A., Shirtcliff, E. A., Booth, A., Kivlighan, K. T., & Schwartz, E. B. (2004). The “trouble” with salivary testosterone. Psychoneuroendocrinology, 29, 12291240. doi:10.1016/j.psyneuen.2004.02.005
Grant, K. A., McMahon, C., Austin, M. P., Reilly, N., Leader, L., & Ali, S. (2009). Maternal prenatal anxiety, postnatal caregiving and infants' cortisol responses to the still-face procedure. Developmental Psychobiology, 51, 625637. doi:10.1002/dev.20397
Gutteling, B. M., de Weerth, C., & Buitelaar, J. K. (2004). Maternal prenatal stress and 4-6 year old children's salivary cortisol concentrations pre- and post-vaccination. Stress, 7, 257260. doi:10.1080/10253890500044521
Gutteling, B. M., de Weerth, C., & Buitelaar, J. K. (2005). Prenatal stress and children's cortisol reaction to the first day of school. Psychoneuroendocrinology, 30, 541549. doi:10.1016/j.psyneuen.2005.01.002
Han, G., Miller, J. G., Cole, P. M., Zahn-Waxler, C., & Hastings, P. D. (2015). Adolescents' internalizing and externalizing problems predict their affect-specific HPA and HPG axes reactivity. Developmental Psychobiology, 57, 769785. doi:10.1002/dev.21268
Hayes, A. F. (2009). Beyond Baron and Kenny: Statistical mediation analysis in the new millennium. Communication Monographs, 76, 408420. doi:10.1080/03637750903310360
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis. New York: Guilford Press.
Hayes, A. F., & Preacher, K. J. (2010). Quantifying and testing indirect effects in simple mediation models when the constituent paths are nonlinear. Multivariate Behavioral Research, 45, 627660. doi:10.1080/00273171.2010.498290
Hermans, E. J., Putman, P., Baas, J. M., Koppeschaar, H. P., & van Honk, J. (2006). A single administration of testosterone reduces fear-potentiated startle in humans. Biological Psychiatry, 59, 872874. doi:10.1016/j.biopsych.2005.11.015
Herrenkohl, L. R. (1979). Prenatal stress reduces fertility and fecundity in female offspring. Science, 206, 10971099. doi:10.1126/science.573923
Herrenkohl, L. R. (1986). Prenatal stress disrupts reproductive-behavior and physiology in offspring. Annals of the New York Academy of Sciences, 474, 120128. doi:10.1111/j.1749-6632.1986.tb28003.x
Hollingshead, A. B. (1973). Medical sociology: A brief review. Milbank Memorial Fund Quarterly Health and Society, 51, 531542.
Huizink, A. C., Bartels, M., Rose, R. J., Pulkkinen, L., Eriksson, C. J. P., & Kaprio, J. (2008). Chernobyl exposure as stressor during pregnancy and hormone levels in adolescent offspring. Journal of Epidemiology and Community Health, 62, e5. doi:10.1136/jech.2007.060350
Kapoor, A., Dunn, E., Kostaki, A., Andrews, M. H., & Matthews, S. G. (2006). Fetal programming of hypothalamo-pituitary-adrenal function: Prenatal stress and glucocorticoids. Journal of Physiology, 572(Pt. 1), 3144. doi:10.1113/jphysiol.2006.105254
Kapoor, A., & Matthews, S. G. (2011). Testosterone is involved in mediating the effects of prenatal stress in male guinea pig offspring. Journal of Physiology, 589(Pt. 3), 755766. doi:10.1113/jphysiol.2010.200543
Khan-Dawood, F. S., Choe, J. K., & Dawood, M. Y. (1984). Salivary and plasma bound and “free” testosterone in men and women. American Journal of Obstetrics and Gynecology, 148, 441445. doi:10.1016/0002-9378(84)90723-3
Khoury, J. E., Gonzalez, A., Levitan, R. D., Pruessner, J. C., Chopra, K., Basile, V. S., … Atkinson, L. (2015). Summary cortisol reactivity indicators: Interrelations and meaning. Neurobiology of Stress, 2, 3443. doi:10.1016/j.ynstr.2015.04.002
King, S., Dancause, K., Turcotte-Tremblay, A. M., Veru, F., & Laplante, D. P. (2012). Using natural disasters to study the effects of prenatal maternal stress on child health and development. Birth Defects Research, 96, 273288. doi:10.1002/bdrc.21026
King, S., & Laplante, D. P. (2005). The effects of prenatal maternal stress on children's cognitive development: Project Ice Storm. Stress, 8, 3545. doi:10.1080/10253890500108391
King, S., & Laplante, D. P. (2015). Using natural disasters to study prenatal maternal stress in humans. Advances in Neurobiology, 10, 285313. doi:10.1007/978-1-4939-1372-5_14
Kinsley, C., & Svare, B. (1988). Prenatal stress alters maternal aggression in mice. Physiology & Behavior, 42, 713. doi:10.1016/0031-9384(88)90252-1
Kirschbaum, C., Wust, S., & Hellhammer, D. (1992). Consistent sex-differences in cortisol responses to psychological stress. Psychosomatic Medicine, 54, 648657.
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J., & Taverne, M. A. (2006). Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Hormones and Behavior, 49, 663672. doi:10.1016/j.yhbeh.2005.12.008
Laplante, D. P., Barr, R. G., Brunet, A., Galbaud du Fort, G., Meaney, M. L., Saucier, J. F., … King, S. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research, 56, 400410. doi:10.1203/01.PDR.0000136281.34035.44
Laplante, D. P., Brunet, A., Schmitz, N., Ciampi, A., & King, S. (2008). Project Ice Storm: Prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 10631072. doi:10.1097/CHI.0b013e31817eec80
Laplante, D. P., Zelazo, P. R., Brunet, A., & King, S. (2007). Functional play at 2 years of age: Effects of prenatal maternal stress. Infancy, 12, 6993.
Liening, S. H., Stanton, S. J., Saini, E. K., & Schultheiss, O. C. (2010). Salivary testosterone, cortisol, and progesterone: Two-week stability, interhormone correlations, and effects of time of day, menstrual cycle, and oral contraceptive use on steroid hormone levels. Physiology & Behavior, 99, 816. doi:10.1016/j.physbeh.2009.10.001
Lincoln, G. A., & Wu, F. C. W. (1991). Luteinizing-hormone responses to N-Methyl-D,L-aspartate during a photoperiodically-induced reproductive-cycle in the ram. Journal of Neuroendocrinology, 3, 309317. doi:10.1111/j.1365-2826.1991.tb00307.x
Lutz, J. B., Rampacek, G. B., Kraeling, R. R., & Pinkert, C. A. (1984). Serum luteinizing-hormone and estrogen profiles before puberty in the gilt. Journal of Animal Science, 58, 686691.
Marchlewska-Koj, A., Kruczek, M., Kapusta, J., & Pochron, E. (2003). Prenatal stress affects the rate of sexual maturation and attractiveness in bank voles. Physiology & Behavior, 79, 305310. doi:10.1016/S0031-9384(03)00099-4
Matchock, R. L., Dorn, L. D., & Susman, E. J. (2007). Diurnal and seasonal cortisol, testosterone, and DHEA rhythms in boys and girls during puberty. Chronobiology International, 24, 969990. doi:10.1080/07420520701649471
Mazur, A., & Booth, A. (2014). Testosterone is related to deviance in male army veterans, but relationships are not moderated by cortisol. Biological Psychology, 96, 7276. doi:10.1016/j.biopsycho.2013.11.015
Mehta, P. H., & Josephs, R. A. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58, 898906. doi:10.1016/j.yhbeh.2010.08.020
Montoya, E. R., Terburg, D., Bos, P. A., & van Honk, J. (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motivation and Emotion, 36, 6573. doi:10.1007/s11031-011-9264-3
Nuckolls, K. B., Kaplan, B. H., & Cassel, J. (1972). Psychosocial assets, life crisis and the prognosis of pregnancy. American Journal of Epidemiology, 95, 431441. doi:10.1093/oxfordjournals.aje.a121410
O'Connor, T. G., Ben-Shlomo, Y., Heron, J., Golding, J., Adams, D., & Glover, V. (2005). Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biological Psychiatry, 58, 211217. doi:10.1016/j.psyneuen.2011.12.016
O'Donnell, K., O'Connor, T. G., & Glover, V. (2009). Prenatal stress and neurodevelopment of the child: Focus on the HPA axis and role of the placenta. Developmental Neuroscience, 31, 285292. doi:10.1159/000216539
Pfattheicher, S. (2017). Illuminating the dual-hormone hypothesis: About chronic dominance and the interaction of cortisol and testosterone. Aggressive Behavior, 43, 8592. doi:10.1002/ab.21665
Plant, T. M., Gay, V. L., Marshall, G. R., & Arslan, M. (1989). Puberty in monkeys is triggered by chemical-stimulation of the hypothalamus. Proceedings of the National Academy of Sciences of the Unites States of America, 86, 25062510.
Platje, E., Popma, A., Vermeiren, R. R., Doreleijers, T. A., Meeus, W. H., van Lier, P. A., … Jansen, L. M. (2015). Testosterone and cortisol in relation to aggression in a non-clinical sample of boys and girls. Aggressive Behavior, 41, 478487. doi:10.1002/ab.21585
Popma, A., Vermeiren, R., Geluk, C. A., Rinne, T., van den Brink, W., Knol, D. L., … Doreleijers, T. A. (2007). Cortisol moderates the relationship between testosterone and aggression in delinquent male adolescents. Biological Psychiatry, 61, 405411. doi:10.1016/j.biopsych.2006.06.006
Putman, P., Hermans, E., & van Honk, J. (2004). Emotional stroop performance for masked angry faces: It's BAS, not BIS. Emotion, 4, 305311. doi:10.1037/1528-3542.4.3.305
Qiu, A., Anh, T. T., Li, Y., Chen, H., Rifkin-Graboi, A., Broekman, B. F. P., … Meaney, M. J. (2015). Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants. Translational Psychiatry, 5, e508. doi:10.1038/tp.2015.3
Quaiser-Pohl, C., Jansen, P., Lehmann, J., & Kudielka, B. M. (2016). Is there a relationship between the performance in a chronometric mental-rotations test and salivary testosterone and estradiol levels in children aged 9–14 years? Developmental Psychobiology, 58, 120128. doi:10.1002/dev.21333
Raizada, R. D. S., & Kishiyama, M. M. (2010). Effects of socioeconomic status on brain development, and how cognitive neuroscience may contribute to levelling the playing field. Frontiers in Human Neuroscience, 4. doi:10.3389/neuro.09.003.2010
Raver, C. C. (2004). Placing emotional self-regulation in sociocultural and socioeconomic contexts. Child Development, 75, 346353. doi:10.1111/j.1467-8624.2004.00676.x
Rilling, J. K., Worthman, C. M., Campbell, B. C., Stallings, J. F., & Mbizva, M. (1996). Ratios of plasma and salivary testosterone throughout puberty: Production versus bioavailability. Steroids, 61, 374378. doi:10.1016/0039-128X(96)00043-8
Rivier, C., & Rivest, S. (1991). Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis—Peripheral and central mechanisms. Biology of Reproduction, 45, 523532. doi:10.1095/biolreprod45.4.523
Ryzhavskii, B. Y., Sokolova, T. V., Fel'dsherov, Y. I., Uchakina, R. V., Sapozhnikov, Y. A., & Malysheva, E. N. (2001). Effect of emotional stress in pregnant rats on brain development of their progeny. Bulletin of Experimental Biology and Medicine, 132, 737740. doi:10.1023/A:1013017625656
Sandman, C. A., Wadhwa, P. D., Chicz-DeMet, A., Dunkel-Schetter, C., & Porto, M. (1997). Maternal stress, HPA activity, and fetal/infant outcome. Neuropeptides in Development and Aging, 814, 266275. doi:10.1111/j.1749-6632.1997.tb46162.x
Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308, 648652. doi:10.1126/science.1106477
Sar, M., Lubahn, D. B., French, F. S., & Wilson, E. M. (1990). Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology, 127, 31803186. doi:10.1210/endo-127-6-3180
Sarkar, P., Bergman, K., Fisk, N. M., O'Connor, T. G., & Glover, V. (2007). Amniotic fluid testosterone: Relationship with cortisol and gestational age. Clinical Endocrinology, 67, 743747. doi:10.1111/j.1365-2265.2007.02955.x
Sarrieau, A., Dussaillant, M., Agid, F., Philibert, D., Agid, Y., & Rostene, W. (1986). Autoradiographic localization of glucocorticosteroid and progesterone binding sites in the human post-mortem brain. Journal of Steroid Biochemistry, 25, 717721. doi:10.1016/0022-4731(86)90300-6
Scerbo, A. S., & Kolko, D. J. (1994). Salivary testosterone and cortisol in disruptive children: Relationship to aggressive, hyperactive, and internalizing behaviors. Journal of the American Academy of Child & Adolescent Psychiatry, 33, 11741184. doi:10.1097/00004583-199410000-00013
Sellers, J. G., Mehl, M. R., & Josephs, R. A. (2007). Hormones and personality: Testosterone as a marker of individual differences. Journal of Research in Personality, 41, 126138. doi:10.1016/j.jrp.2006.02.004
Shachar-Dadon, A., Schulkin, J., & Leshem, M. (2009). Adversity before conception will affect adult progeny in rats. Developmental Psychology, 45, 916. doi:10.1037/a0014030
Simerly, R. B., Chang, C., Muramatsu, M., & Swanson, L. W. (1990). Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. Journal of Comparative Neurology, 294, 7695. doi:10.1002/cne.902940107
Stanczyk, F. Z. (2006). Measurement of androgens in women. Seminars in Reproductive Medicine, 24, 7885. doi:10.1055/s-2006-939566
St.-Hilaire, A., Steiger, H., Liu, A. H., Laplante, D. P., Thaler, L., Magill, T., & King, S. (2015). A prospective study of effects of prenatal maternal stress on later eating-disorder manifestations in affected offspring: Preliminary indications based on the project ice storm cohort. International Journal of Eating Disorders, 48, 512516. doi:10.1002/eat.22391
Tilbrook, A. J., Turner, A. I., & Clarke, I. J. (2000). Effects of stress on reproduction in non-rodent mammals: The role of glucocorticoids and sex differences. Reviews of Reproduction, 5, 105113.
Tollenaar, M. S., Beijers, R., Jansen, J., Riksen-Walraven, J. M., & de Weerth, C. (2011). Maternal prenatal stress and cortisol reactivity to stressors in human infants. Stress, 14, 5365. doi:10.3109/10253890.2010.499485
Tsai, S. L., Seiler, K. J., & Jacobson, J. (2013). Morning cortisol levels affected by sex and pubertal status in children and young adults. Journal of Clinical Reseach in Pediatric Endocrinology, 5, 8589. doi:10.4274/Jcrpe.892
Turcotte-Tremblay, A. M., Lim, R., Laplante, D. P., Kobzik, L., Brunet, A., & King, S. (2014). Prenatal maternal stress predicts childhood asthma in girls: Project Ice Storm. Biomed Research International, 2014, 201717. doi:10.1155/2014/201717.
Urbanski, H. F., & Ojeda, S. R. (1987). Activation of luteinizing-hormone-releasing hormone-release advances the onset of female puberty. Neuroendocrinology, 46, 273276. doi:10.1159/000124831
Van den Bergh, B. R. H., van Calster, B., Smits, T., van Huffel, S., & Lagae, L. (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology, 33, 536545. doi:10.1038/sj.npp.1301450
van Honk, J., Peper, J. S., & Schutter, D. J. (2005). Testosterone reduces unconscious fear but not consciously experienced anxiety: Implications for the disorders of fear and anxiety. Biological Psychiatry, 58, 218225. doi:10.1016/j.biopsych.2005.04.003
Viau, V. (2002). Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. Journal of Neuroendocrinology, 14, 506513. doi:10.1046/j.1365-2826.2002.00798.x
Viau, V., Soriano, L., & Dallman, M. F. (2001). Androgens alter corticotropin releasing hormone and arginine vasopressin mRNA within forebrain sites known to regulate activity in the hypothalamic-pituitary-adrenal axis. Journal of Neuroendocrinology, 13, 442452. doi:10.1046/j.1365-2826.2001.00653.x
Viguie, C., Caraty, A., Locatelli, A., & Malpaux, B. (1995). Regulation of luteinizing-hormone-releasing hormone (Lhrh) secretion by melatonin in the ewe: 2. Changes in N-methyl-D,L-aspartic acid-induced Lhrh release during the stimulation of luteinizing-hormone secretion by melatonin. Biology of Reproduction, 52, 11561161. doi:10.1095/biolreprod52.5.1156
Vomsaal, F. S., Quadagno, D. M., Even, M. D., Keisler, L. W., Keisler, D. H., & Khan, S. (1990). Paradoxical effects of maternal stress on fetal steroids and postnatal reproductive traits in female mice from different intrauterine positions. Biology of Reproduction, 43, 751761. doi:10.1095/biolreprod43.5.751
Walder, D. J., Laplante, D. R., Sousa-Pires, A., Veru, F., Brunet, A., & King, S. (2014). Prenatal maternal stress predicts autism traits in 61/2 year-old children: Project Ice Storm. Psychiatry Research, 219, 353360. doi:10.1016/j.psychres.2014.04.034
Ward, I. L., & Weisz, J. (1980). Maternal stress alters plasma testosterone in fetal males. Science, 207, 328329. doi:10.1126/science.7188648
Ward, I. L., & Weisz, J. (1984). Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology, 114, 16351644. doi:10.1210/endo-114-5-1635
Weiss, D. S., & Marmar, C. R. (1997). The impact of event-scale-revised. New York: Guilford Press.
Weisz, J., Brown, B. L., & Ward, I. L. (1982). Maternal stress decreases steroid aromatase activity in brains of male and female rat fetuses. Neuroendocrinology, 35, 374379. doi:10.1159/000123410
Welker, K. M., Lozoya, E., Campbell, J. A., Neumann, C. S., & Carre, J. M. (2014). Testosterone, cortisol, and psychopathic traits in men and women. Physiology & Behavior, 129, 230236. doi:10.1016/j.physbeh.2014.02.057
Witt, W. P., Cheng, E. R., Wisk, L. E., Litzelman, K., Chatterjee, D., Mandell, K., & Wakeel, F. (2014). Maternal stressful life events prior to conception and the impact on infant birth weight in the United States. American Journal of Public Health 104(Suppl. 1), S81S89. doi:10.2105/AJPH.2013.301544
Worthman, C. M., Stallings, J. F., & Hofman, L. F. (1990). Sensitive salivary estradiol assay for monitoring ovarian function. Clinical Chemistry, 36, 17691773.
Yehuda, R., Engel, S. M., Brand, S. R., Seckl, J., Marcus, S. M., & Berkowitz, G. S. (2005). Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the world trade center attacks during pregnancy. Journal of Clinical Endocrinology & Metabolism, 90, 41154118. doi:10.1210/jc.2005-0550
Yu, Y. Z., & Shi, J. X. (2009). Relationship between levels of testosterone and cortisol in saliva and aggressive behaviors of adolescents. Biomedical and Environmental Sciences, 22, 4449. doi:10.1016/S0895-3988(09)60021-0
Zaidan, H., & Gaisler-Salomon, I. (2015). Prereproductive stress in adolescent female rats affects behavior and corticosterone levels in second-generation offspring. Psychoneuroendocrinology, 58, 120129. doi:10.1016/j.psyneuen.2015.04.013
Zilioli, S., Ponzi, D., Henry, A., & Maestripieri, D. (2015). Testosterone, cortisol and empathy: Evidence for the dual-hormone hypothesis. Adaptive Human Behavior and Physiology, 1, 421433. doi:10.1007/s40750-014-0017-x

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