Advanced search
Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 27, 2024 - Issue 1
Submit an article Journal homepage
154
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Genotypic variation in the promoter region of the CRH-248 gene interacts with early rearing experiences to disrupt the development of the HPA axis in infant rhesus macaques (Macaca mulatta)

Elizabeth K. Wooda Department of Psychiatry, Oregon Health & Science University, Portland, OR, USACorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0001-6407-295XView further author information
ORCID Icon,
S. Andrew Astonb Department of Neuroscience, Brigham Young University, Provo, UT, USAORCID Iconhttps://orcid.org/0000-0002-3409-8486View further author information
ORCID Icon,
Patrick H. O’Connellc Department of Psychology, Brigham Young University, Provo, UT, USAView further author information
,
Elia Hafenb Department of Neuroscience, Brigham Young University, Provo, UT, USAView further author information
,
Andrea N. Skowboc Department of Psychology, Brigham Young University, Provo, UT, USAView further author information
,
Melanie L. Schwandtd Laboratory of Clinical and Translational Studies, National Institute on Alcohol Abuse and Alcoholism, Poolesville, MD, USAORCID Iconhttps://orcid.org/0000-0002-8355-4900View further author information
ORCID Icon,
Stephen G. Lindelle Laboratory of Neurogenetics, Section of Comparative Behavioral Genomics, National Institute on Alcohol Abuse and Alcoholism, NIH, Rockville, MD, USAView further author information
,
Ellie Smithc Department of Psychology, Brigham Young University, Provo, UT, USAORCID Iconhttps://orcid.org/0000-0001-6340-1926View further author information
ORCID Icon,
Miranda Johnsonb Department of Neuroscience, Brigham Young University, Provo, UT, USAORCID Iconhttps://orcid.org/0000-0002-5340-7600View further author information
ORCID Icon,
Zachary Baronb Department of Neuroscience, Brigham Young University, Provo, UT, USAORCID Iconhttps://orcid.org/0000-0002-7154-8466View further author information
ORCID Icon,
Natalia Gabriellec Department of Psychology, Brigham Young University, Provo, UT, USAORCID Iconhttps://orcid.org/0000-0003-2668-6023View further author information
ORCID Icon,
Christina S. Barre Laboratory of Neurogenetics, Section of Comparative Behavioral Genomics, National Institute on Alcohol Abuse and Alcoholism, NIH, Rockville, MD, USAView further author information
,
Stephen J. Suomif Laboratory of Comparative Ethology, National Institute of Child Health and Human Development, Poolesville, MD, USAView further author information
,
David Goldmane Laboratory of Neurogenetics, Section of Comparative Behavioral Genomics, National Institute on Alcohol Abuse and Alcoholism, NIH, Rockville, MD, USAORCID Iconhttps://orcid.org/0000-0002-1724-5405View further author information
ORCID Icon &
J. Dee Higleyb Department of Neuroscience, Brigham Young University, Provo, UT, USAORCID Iconhttps://orcid.org/0000-0002-3745-3893View further author information
ORCID Icon show all
Article: 2377272 | Received 04 Sep 2023, Accepted 25 Jun 2024, Published online: 17 Jul 2024

References

  • Ainsworth, M. S. (1979). Infant–mother attachment. American Psychologist, 34(10), 932–937. https://doi.org/10.1037/0003-066X.34.10.932
  • Almasy, L., & Blangero, J. (1998). Multipoint quantitative-trait linkage analysis in general pedigrees. American Journal of Human Genetics, 62(5), 1198–1211. https://doi.org/10.1086/301844
  • Barr, C. S., Dvoskin, R. L., Gupte, M., Sommer, W., Sun, H., Schwandt, M. L., Lindell, S. G., Kasckow, J. W., Suomi, S. J., Goldman, D., Higley, J. D., & Heilig, M. (2009). Functional CRH variation increases stress-induced alcohol consumption in primates. Proceedings of the National Academy of Sciences of the United States of America, 106(34), 14593–14598. https://doi.org/10.1073/pnas.0902863106
  • Barr, C. S., Dvoskin, R. L., Yuan, Q., Lipsky, R. H., Gupte, M., Hu, X., Zhou, Z., Schwandt, M. L., Lindell, S. G., McKee, M., Becker, M. L., Kling, M. A., Gold, P. W., Higley, D., Heilig, M., Suomi, S. J., & Goldman, D. (2008). CRH haplotype as a factor influencing cerebrospinal fluid levels of corticotropin-releasing hormone, hypothalamic-pituitary-adrenal axis activity, temperament, and alcohol consumption in rhesus macaques. Archives of General Psychiatry, 65(8), 934–944. https://doi.org/10.1001/archpsyc.65.8.934
  • Barr, C. S., Newman, T. K., Lindell, S., Shannon, C., Champoux, M., Lesch, K. P., Suomi, S. J., Goldman, D., & Higley, J. D. (2004). Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Archives of General Psychiatry, 61(11), 1146–1152. https://doi.org/10.1001/archpsyc.61.11.1146
  • Barrett, C. E., Noble, P., Hanson, E., Pine, D. S., Winslow, J. T., & Nelson, E. E. (2009). Early adverse rearing experiences alter sleep-wake patterns and plasma cortisol levels in juvenile rhesus monkeys. Psychoneuroendocrinology, 34(7), 1029–1040. https://doi.org/10.1016/j.psyneuen.2009.02.002
  • Battaglia, M. (2013). Gene-environment interaction in panic disorder and posttraumatic stress disorder. Canadian Journal of Psychiatry. Revue Canadienne de Psychiatrie, 58(2), 69–75. https://doi.org/10.1177/070674371305800202
  • Bennett, A. J., Lesch, K. P., Heils, A., Long, J. C., Lorenz, J. G., Shoaf, S. E., Champoux, M., Suomi, S. J., Linnoila, M. V., & Higley, J. D. (2002). Early experience and serotonin transporter gene variation interact to influence primate CNS function. Molecular Psychiatry, 7(1), 118–122. https://doi.org/10.1038/sj.mp.4000949
  • Bernard, K., Zwerling, J., & Dozier, M. (2015). Effects of early adversity on young children’s diurnal cortisol rhythms and externalizing behavior. Developmental Psychobiology, 57(8), 935–947. https://doi.org/10.1002/dev.21324
  • Bick, J., & Nelson, C. A. (2017). Early experience and brain development. Wiley Interdisciplinary Reviews. Cognitive Science, 8(1–2), 1–2.
  • Blanca Mena, M. J., Alarcón, R., Arnau, J., Bono, R., Bendayan, R. (2017). Non-normal data: Is ANOVA still a valid option? Psicothema, 29(4), 552–557.
  • Bloch, M., Peleg, I., Koren, D., Aner, H., & Klein, E. (2007). Long-term effects of early parental loss due to divorce on the HPA axis. Hormones and Behavior, 51(4), 516–523. https://doi.org/10.1016/j.yhbeh.2007.01.009
  • Bowlby, J. (1969). Attachment and loss. Random House.
  • Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. (2009). Morning cortisol levels in preschool-aged foster children: Differential effects of maltreatment type. Developmental Psychobiology, 51(1), 14–23. https://doi.org/10.1002/dev.20333
  • Bunea, I. M., Szentágotai-Tătar, A., & Miu, A. C. (2017). Early-life adversity and cortisol response to social stress: a meta-analysis. Translational Psychiatry, 7(12), 1274. https://doi.org/10.1038/s41398-017-0032-3
  • Capitanio, J. P., Mendoza, S. P., Mason, W. A., & Maninger, N. (2005). Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta). Developmental Psychobiology, 46(4), 318–330. https://doi.org/10.1002/dev.20067
  • Carpenter, L. L., Tyrka, A. R., McDougle, C. J., Malison, R. T., Owens, M. J., Nemeroff, C. B., & Price, L. H. (2004). Cerebrospinal fluid corticotropin-releasing factor and perceived early-life stress in depressed patients and healthy control subjects. Neuropsychopharmacology: official Publication of the American College of Neuropsychopharmacology, 29(4), 777–784. https://doi.org/10.1038/sj.npp.1300375
  • Carpenter, L. L., Tyrka, A. R., Ross, N. S., Khoury, L., Anderson, G. M., & Price, L. H. (2009). Effect of childhood emotional abuse and age on cortisol responsivity in adulthood. Biological Psychiatry, 66(1), 69–75. https://doi.org/10.1016/j.biopsych.2009.02.030
  • Carrion, V. G., Weems, C. F., Ray, R. D., Glaser, B., Hessl, D., & Reiss, A. L. (2002). Diurnal salivary cortisol in pediatric posttraumatic stress disorder. Biological Psychiatry, 51(7), 575–582. https://doi.org/10.1016/s0006-3223(01)01310-5
  • Champoux, M., Hibbeln, J. R., Shannon, C., Majchrzak, S., Suomi, S. J., Salem, N., & Higley, J. D. (2002). Fatty acid formula supplementation and neuromotor development in rhesus monkey neonates. Pediatric Research, 51(3), 273–281. https://doi.org/10.1203/00006450-200203000-00003
  • Claessens, S. E. F., Daskalakis, N. P., van der Veen, R., Oitzl, M. S., de Kloet, E. R., & Champagne, D. L. (2011). Development of individual differences in stress responsiveness: an overview of factors mediating the ­outcome of early life experiences. Psychopharmacology, 214(1), 141–154. https://doi.org/10.1007/s00213-010-2118-y
  • Coplan, J. D., Abdallah, C. G., Kaufman, J., Gelernter, J., Smith, E. L. P., Perera, T. D., Dwork, A. J., Kaffman, A., Gorman, J. M., Rosenblum, L. A., Owens, M. J., & Nemeroff, C. B. (2011). Early-life stress, corticotropin-releasing factor, and serotonin transporter gene: a pilot study. Psychoneuroendocrinology, 36(2), 289–293. https://doi.org/10.1016/j.psyneuen.2010.07.011
  • Coplan, J. D., Fathy, H. M., Jackowski, A. P., Tang, C. Y., Perera, T. D., Mathew, S. J., Martinez, J., Abdallah, C. G., Dwork, A. J., Pantol, G., Carpenter, D., Gorman, J. M., Nemeroff, C. B., Owens, M. J., Kaffman, A., & Kaufman, J. (2014). Early life stress and macaque amygdala hypertrophy: preliminary evidence for a role for the serotonin transporter gene. Frontiers in Behavioral Neuroscience, 8, 342. https://doi.org/10.3389/fnbeh.2014.00342
  • Corcoran, C. A., Pierre, P. J., Haddad, T., Bice, C., Suomi, S. J., Grant, K. A., Friedman, D. P., & Bennett, A. J. (2012). Long-term effects of differential early rearing in rhesus macaques: Behavioral reactivity in adulthood. Developmental Psychobiology, 54(5), 546–555. https://doi.org/10.1002/dev.20613
  • Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013). The three-hit concept of vulnerability and resilience: ­toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology, 38(9), 1858–1873. https://doi.org/10.1016/j.psyneuen.2013.06.008
  • Engel, M. L., & Gunnar, M. R. (2020). The development of stress reactivity and regulation during human development. International Review of Neurobiology, 150, 41–76. https://doi.org/10.1016/bs.irn.2019.11.003
  • Erickson, K., Gabry, K. E., Lindell, S., Champoux, M., Schulkin, J., Gold, P., Suomi, S. J., & Higley, J. D. (2005). Social withdrawal behaviors in nonhuman primates and changes in neuroendocrine and monoamine concentrations during a separation paradigm. Developmental Psychobiology, 46(4), 331–339. https://doi.org/10.1002/dev.20061
  • Ersig, A. L., Schutte, D. L., Standley, J., Leslie, E. J., Zimmerman, B., Hanrahan, K., Murray, J. C., & McCarthy, A. M. (2019). Genetic variants and the cortisol response in children: An exploratory study. Biological Research for Nursing, 21(2), 157–165. https://doi.org/10.1177/1099800419826315
  • Fahlke, C., Lorenz, J. G., Long, J., Champoux, M., Suomi, S. J., & Higley, J. D. (2000). Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcoholism, Clinical and Experimental Research, 24(5), 644–650. https://doi.org/10.1111/j.1530-0277.2000.tb02035.x
  • Ferguson, B., Hunter, J. E., Luty, J., Street, S. L., Woodall, A., & Grant, K. A. (2012). Genetic load is associated with hypothalamic-pituitary-adrenal axis dysregulation in macaques. Genes, Brain, and Behavior, 11(8), 949–957. https://doi.org/10.1111/j.1601-183X.2012.00856.x
  • Greenough, W. T., Black, J. E., & Wallace, C. S. (1987). Experience and brain development. Child Development, 58(3), 539–559. https://doi.org/10.2307/1130197
  • Gunnar, M. R., Frenn, K., Wewerka, S. S., & Van Ryzin, M. J. (2009). Moderate versus severe early life stress: associations with stress reactivity and regulation in 10-12-year-old children. Psychoneuroendocrinology, 34(1), 62–75. https://doi.org/10.1016/j.psyneuen.2008.08.013
  • Gunnar, M. R., Morison, S. J., Chisholm, K., & Schuder, M. (2001). Salivary cortisol levels in children adopted from Romanian orphanages. Development and Psychopathology, 13(3), 611–628. https://doi.org/10.1017/s095457940100311x
  • Hengesch, X., Elwenspoek, M. M. C., Schaan, V. K., Larra, M. F., Finke, J. B., Zhang, X., Bachmann, P., Turner, J. D., Vögele, C., Muller, C. P., & Schächinger, H. (2018). Blunted endocrine response to a combined physical-cognitive stressor in adults with early life adversity. Child Abuse & Neglect, 85, 137–144. https://doi.org/10.1016/j.chiabu.2018.04.002
  • Higley, J. D., Hopkins, W. D., Thompson, W. W., Byrne, E. A., Hirsch, R. M., & Suomi, S. J. (1992). Peers as primary attachment sources in yearling rhesus monkeys (Macaca mulatta). Developmental Psychology, 28(6), 1163–1171. https://doi.org/10.1037/0012-1649.28.6.1163
  • Higley, J. D., Suomi, S. J., & Linnoila, M. (1992). A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biological Psychiatry, 32(2), 127–145. https://doi.org/10.1016/0006-3223(92)90016-s
  • Karlamangla, A. S., Merkin, S. S., Almeida, D. M., Friedman, E. M., Mogle, J. A., & Seeman, T. E. (2019). Early-life adversity and dysregulation of adult diurnal cortisol rhythm. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 74(1), 160–169. https://doi.org/10.1093/geronb/gby097
  • Keck, M. E., Kern, N., Erhardt, A., Unschuld, P. G., Ising, M., Salyakina, D., Müller, M. B., Knorr, C. C., Lieb, R., Hohoff, C., Krakowitzky, P., Maier, W., Bandelow, B., Fritze, J., Deckert, J., Holsboer, F., Müller-Myhsok, B., & Binder, E. B. (2008). Combined effects of exonic polymorphisms in CRHR1 and AVPR1B genes in a case/control study for panic disorder. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics, 147B(7), 1196–1204. https://doi.org/10.1002/ajmg.b.30750
  • Kinnally, E. L., & Capitanio, J. P. (2015). Paternal early experiences influence infant development through non-social mechanisms in Rhesus Macaques. Frontiers in Zoology, 12 Suppl 1(Suppl 1), S14. https://doi.org/10.1186/1742-9994-12-S1-S14
  • Koss, K. J., & Gunnar, M. R. (2018). Annual Research Review: Early adversity, the hypothalamic-pituitary-adrenocortical axis, and child psychopathology. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 59(4), 327–346. https://doi.org/10.1111/jcpp.12784
  • Koss, K. J., Hostinar, C. E., Donzella, B., & Gunnar, M. R. (2014). Social deprivation and the HPA axis in early development. Psychoneuroendocrinology, 50, 1–13. https://doi.org/10.1016/j.psyneuen.2014.07.028
  • Kuras, Y. I., Assaf, N., Thoma, M. V., Gianferante, D., Hanlin, L., Chen, X., Fiksdal, A., & Rohleder, N. (2017). Blunted diurnal cortisol activity in healthy adults with childhood adversity. Frontiers in Human Neuroscience, 11, 574. https://doi.org/10.3389/fnhum.2017.00574
  • Laryea, G., Arnett, M. G., & Muglia, L. J. (2012). Behavioral studies and genetic alterations in Corticotropin-Releasing Hormone (CRH) neurocircuitry: Insights into human psychiatric disorders. Behavioral Sciences (Basel, Switzerland), 2(2), 135–171. https://doi.org/10.3390/bs2020135
  • Lee, R., Geracioti, T. D., Kasckow, J. W., & Coccaro, E. F. (2005). Childhood trauma and personality disorder: positive correlation with adult CSF corticotropin-releasing factor concentrations. The American Journal of Psychiatry, 162(5), 995–997. https://doi.org/10.1176/appi.ajp.162.5.995
  • Levine, S. (1962). Plasma-free corticosteroid response to electric shock in rats stimulated in infancy. Science (New York, NY), 135(3506), 795–796. https://doi.org/10.1126/science.135.3506.795-a
  • McLaughlin, K. A., Sheridan, M. A., Tibu, F., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2015). Causal effects of the early caregiving environment on development of stress response systems in children. Proceedings of the National Academy of Sciences of the United States of America, 112(18), 5637–5642. https://doi.org/10.1073/pnas.1423363112
  • Morris, M. C., & Rao, U. (2013). Psychobiology of PTSD in the acute aftermath of trauma: Integrating research on coping, HPA function and sympathetic nervous system activity. Asian Journal of Psychiatry, 6(1), 3–21. https://doi.org/10.1016/j.ajp.2012.07.012
  • Nelson, C. A., Scott, R. D., Bhutta, Z. A., Harris, N. B., Danese, A., & Samara, M. (2020). Adversity in childhood is linked to mental and physical health throughout life. BMJ (Clinical Research ed.), 371, m3048. https://doi.org/10.1136/bmj.m3048
  • Newman, T. K., Syagailo, Y. V., Barr, C. S., Wendland, J. R., Champoux, M., Graessle, M., Suomi, S. J., Higley, J. D., & Lesch, K.-P. (2005). Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biological Psychiatry, 57(2), 167–172. https://doi.org/10.1016/j.biopsych.2004.10.012
  • Ouellet-Morin, I., Odgers, C. L., Danese, A., Bowes, L., Shakoor, S., Papadopoulos, A. S., Caspi, A., Moffitt, T. E., & Arseneault, L. (2011). Blunted cortisol responses to stress signal social and behavioral problems among maltreated/bullied 12-year-old children. Biological Psychiatry, 70(11), 1016–1023. https://doi.org/10.1016/j.biopsych.2011.06.017
  • Ressler, K. J., Bradley, B., Mercer, K. B., Deveau, T. C., Smith, A. K., Gillespie, C. F., Nemeroff, C. B., Cubells, J. F., & Binder, E. B. (2010). Polymorphisms in CRHR1 and the serotonin transporter loci: gene x gene x environment interactions on depressive symptoms. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics, 153B(3), 812–824. https://doi.org/10.1002/ajmg.b.31052
  • Robin, R. W., Chester, B., Rasmussen, J. K., Jaranson, J. M., & Goldman, D. (1997). Prevalence and characteristics of trauma and posttraumatic stress disorder in a southwestern American Indian community. The American Journal of Psychiatry, 154(11), 1582–1588. https://doi.org/10.1176/ajp.154.11.1582
  • Sanchez, M. M. (2006). The impact of early adverse care on HPA axis development: nonhuman primate models. Hormones and Behavior, 50(4), 623–631. https://doi.org/10.1016/j.yhbeh.2006.06.012
  • Sánchez, M. M., Noble, P. M., Lyon, C. K., Plotsky, P. M., Davis, M., Nemeroff, C. B., & Winslow, J. T. (2005). Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biological Psychiatry, 57(4), 373–381. https://doi.org/10.1016/j.biopsych.2004.11.032
  • Santarelli, S., Zimmermann, C., Kalideris, G., Lesuis, S. L., Arloth, J., Uribe, A., Dournes, C., Balsevich, G., Hartmann, J., Masana, M., Binder, E. B., Spengler, D., & Schmidt, M. V. (2017). An adverse early life environment can enhance stress resilience in adulthood. Psychoneuroendocrinology, 78, 213–221. https://doi.org/10.1016/j.psyneuen.2017.01.021
  • Schäfer, I., Teske, L., Schulze-Thüsing, J., Homann, K., Reimer, J., Haasen, C., Hissbach, J., & Wiedemann, K. (2010). Impact of childhood trauma on hypothalamus-pituitary-adrenal axis activity in alcohol-dependent ­patients. European Addiction Research, 16(2), 108–114. https://doi.org/10.1159/000294362
  • Schneider, M. L., & Suomi, S. J. (1992). Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatta): Developmental changes, behavioral stability, and early experience. Infant Behavior and Development, 15(2), 155–177. https://doi.org/10.1016/0163-6383(92)80021-L
  • Shannon, C., Champoux, M., & Suomi, S. J. (1998). Rearing condition and plasma cortisol in rhesus monkey infants. American Journal of Primatology, 46(4), 311–321. https://doi.org/10.1002/(SICI)1098-2345(1998)46:4<311::AID-AJP3>3.0.CO;2-L
  • Sheikh, H. I., Kryski, K. R., Smith, H. J., Hayden, E. P., & Singh, S. M. (2013). Corticotropin-releasing hormone system polymorphisms are associated with children’s cortisol reactivity. Neuroscience, 229, 1–11. https://doi.org/10.1016/j.neuroscience.2012.10.056
  • Smoller, J. W., Rosenbaum, J. F., Biederman, J., Kennedy, J., Dai, D., Racette, S. R., Laird, N. M., Kagan, J., Snidman, N., Hirshfeld-Becker, D., Tsuang, M. T., Sklar, P. B., & Slaugenhaupt, S. A. (2003). Association of a genetic marker at the corticotropin-releasing hormone locus with behavioral inhibition. Biological Psychiatry, 54(12), 1376–1381. https://doi.org/10.1016/s0006-3223(03)00598-5
  • Smoller, J. W., Yamaki, L. H., Fagerness, J. A., Biederman, J., Racette, S., Laird, N. M., Kagan, J., Snidman, N., Faraone, S. V., Hirshfeld-Becker, D., Tsuang, M. T., Slaugenhaupt, S. A., Rosenbaum, J. F., & Sklar, P. B. (2005). The corticotropin-releasing hormone gene and behavioral inhibition in children at risk for panic disorder. Biological Psychiatry, 57(12), 1485–1492. https://doi.org/10.1016/j.biopsych.2005.02.018
  • Sproul Bassett, A. M., Wood, E. K., Lindell, S. G., Schwandt, M. L., Barr, C. S., Suomi, S. J., & Higley, J. D. (2020). Intergenerational effects of mother’s early rearing experience on offspring treatment and socioemotional development. Developmental Psychobiology, 62(7), 920–931. https://doi.org/10.1002/dev.21959
  • Tyrka, A. R., Wier, L., Price, L. H., Ross, N., Anderson, G. M., Wilkinson, C. W., & Carpenter, L. L. (2008). Childhood parental loss and adult hypothalamic-pituitary-adrenal function. Biological Psychiatry, 63(12), 1147–1154. https://doi.org/10.1016/j.biopsych.2008.01.011
  • Wolf, E. J., Mitchell, K. S., Logue, M. W., Baldwin, C. T., Reardon, A. F., Humphries, D. E., & Miller, M. W. (2013). Corticotropin releasing hormone receptor 2 (CRHR-2) gene is associated with decreased risk and severity of posttraumatic stress disorder in women. Depression and Anxiety, 30(12), 1161–1169. https://doi.org/10.1002/da.22176
  • Wood, E. K., Champoux, M., Lindell, S. G., Barr, C. S., Suomi, S. J., & Higley, J. D. (2020). Neonatal temperament and neuromotor differences are predictive of adolescent alcohol intake in rhesus monkeys (Macaca mulatta). American Journal of Primatology, 82(11), e23043. https://doi.org/10.1002/ajp.23043
  • Young, J. J., Silber, T., Bruno, D., Galatzer-Levy, I. R., Pomara, N., & Marmar, C. R. (2016). Is there progress? An overview of selecting biomarker candidates for major depressive disorder. Frontiers in Psychiatry, 7, 72. https://doi.org/10.3389/fpsyt.2016.00072
  • Zhang, B. (2017). Consequences of early adverse rearing experience (EARE) on development: insights from non-human primate studies. Zoological Research, 38(1), 7–35. https://doi.org/10.13918/j.issn.2095-8137.2017.002

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.