Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T01:40:31.485Z Has data issue: false hasContentIssue false
  • English
  • Français

Elevated infant cortisol is necessary but not sufficient for transmission of environmental risk to infant social development: Cross-species evidence of mother–infant physiological social transmission

Published online by Cambridge University Press:  11 January 2021

Rosemarie E. Perry ,
Stephen H. Braren ,
Maya Opendak ,
Annie Brandes-Aitken ,
Divija Chopra ,
Joyce Woo ,
Regina Sullivan ,
Clancy Blair  and
Family Life Project Key Investigators
Rosemarie E. Perry*
Affiliation:
Department of Applied Psychology, New York University, New York, NY, USA
Stephen H. Braren
Affiliation:
Department of Applied Psychology, New York University, New York, NY, USA
Maya Opendak
Affiliation:
Emotional Brain Institute, Nathan Kline Institute & Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
Annie Brandes-Aitken
Affiliation:
Department of Applied Psychology, New York University, New York, NY, USA
Divija Chopra
Affiliation:
Department of Applied Psychology, New York University, New York, NY, USA
Joyce Woo
Affiliation:
Emotional Brain Institute, Nathan Kline Institute & Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
Regina Sullivan
Affiliation:
Emotional Brain Institute, Nathan Kline Institute & Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
Clancy Blair
Affiliation:
Department of Applied Psychology, New York University, New York, NY, USA Department of Population Health, New York University School of Medicine, New York, NY, USA
*
Author for Correspondence: Rosemarie E. Perry, RP: New York University, Department of Applied Psychology, 627 Broadway, Room 810, New York, NY 10012; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Environmental adversity increases child susceptibility to disrupted developmental outcomes, but the mechanisms by which adversity can shape development remain unclear. A translational cross-species approach was used to examine stress-mediated pathways by which poverty-related adversity can influence infant social development. Findings from a longitudinal sample of low-income mother–infant dyads indicated that infant cortisol (CORT) on its own did not mediate relations between early-life scarcity-adversity exposure and later infant behavior in a mother-child interaction task. However, maternal CORT through infant CORT served as a mediating pathway, even when controlling for parenting behavior. Findings using a rodent “scarcity-adversity” model indicated that pharmacologically blocking pup corticosterone (CORT, rodent equivalent to cortisol) in the presence of a stressed mother causally prevented social transmission of scarcity-adversity effects on pup social behavior. Furthermore, pharmacologically increasing pup CORT without the mother present was not sufficient to disrupt pup social behavior. Integration of our cross-species results suggests that elevated infant CORT may be necessary, but without elevated caregiver CORT, may not be sufficient in mediating the effects of environmental adversity on development. These findings underscore the importance of considering infant stress physiology in relation to the broader social context, including caregiver stress physiology, in research and interventional efforts.

Keywords

cortisolcorticosteroneearly-life adversityearly-life stressmother–infantsocial transmission
Type
Special Section 2: Early Adversity and Development: Contributions from the Field
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1696 - 1714
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Authors contributed equally as first authors to this manuscript

†

Authors contributed equally as last authors to this manuscript

References

Ahnert, L., Gunnar, M. R., Lamb, M. E., & Barthel, M. (2004). Transition to child care: Associations with infant–mother attachment, infant negative emotion, and cortisol elevations. Child Development, 75, 639–650. doi: 10.1111/j.1467-8624.2004.00698.xCrossRefGoogle ScholarPubMed
Asok, A., Bernard, K., Roth, T. L., Rosen, J. B., & Dozier, M. (2013). Parental responsiveness moderates the association between early-life stress and reduced telomere length. Development and Psychopathology, 25, 577–585. doi: 10.1017/S0954579413000011CrossRefGoogle ScholarPubMed
Avishai-Eliner, S., Gilles, E., Eghbal-Ahmadi, M., Bar-El, Y., & Baram, T. (2001). Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. Journal of Neuroendocrinology, 13, 799–807. doi:10.1046/j.1365-2826.2001.00698.xCrossRefGoogle Scholar
Badanes, L. S., Watamura, S. E., & Hankin, B. L. (2011). Hypocortisolism as a potential marker of allostatic load in children: Associations with family risk and internalizing disorders. Development and Psychopathology, 23, 881–896. doi: 10.1017/S095457941100037XCrossRefGoogle ScholarPubMed
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., … Nestler, E. J. (2010). Early life programming and neurodevelopmental disorders. Biological Psychiatry, 68, 314–319. doi: 10.1016/j.biopsych.2010.05.028CrossRefGoogle ScholarPubMed
Baram, T. Z., Davis, E. P., Obenaus, A., Sandman, C. A., Small, S. L., Solodkin, A., & Stern, H. (2012). Fragmentation and unpredictability of early-life experience in mental disorders. American Journal of Psychiatry, 169, 907–915. doi:10.1176/appi.ajp.2012.11091347CrossRefGoogle ScholarPubMed
Barr, G. A., Moriceau, S., Shionoya, K., Muzny, K., Gao, P., Wang, S., & Sullivan, R. M. (2009). Transitions in infant learning are modulated by dopamine in the amygdala. Nature Neuroscience, 12, 1367. doi: 10.1038/nn.2403CrossRefGoogle ScholarPubMed
Barrett, J., & Fleming, A. S. (2011). Annual research review: All mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. Journal of Child Psychology and Psychiatry, 52, 368–397. doi:10.1111/j.1469-7610.2010.02306.xCrossRefGoogle Scholar
Beebe, B. (2017). My journey in infant research and psychoanalysis: Microanalysis, a social microscope. Moments of meeting in psychoanalysis (pp. 13–44). New York: Routledge.Google Scholar
Bernard, K., Zwerling, J., & Dozier, M. (2015). Effects of early adversity on young children's diurnal cortisol rhythms and externalizing behavior. Developmental Psychobiology, 57, 935–947. doi:10.1002/dev.21324CrossRefGoogle Scholar
Bernier, A., Carlson, S. M., & Whipple, N. (2010). From external regulation to self-regulation: Early parenting precursors of young children's executive functioning. Child Development, 81, 326–339. doi:10.1111/j.1467-8624.2009.01397.xCrossRefGoogle ScholarPubMed
Blair, C. (2010). Stress and the development of self-regulation in context. Child Development Perspectives, 4, 181–188. doi: 10.1111/j.1750-8606.2010.00145.xCrossRefGoogle ScholarPubMed
Blair, C., Berry, D., Mills-Koonce, R., Granger, D., & Investigators, F. L. P. (2013). Cumulative effects of early poverty on cortisol in young children: moderation by autonomic nervous system activity. Psychoneuroendocrinology, 38, 2666–2675. doi:10.1016/j.psyneuen.2013.06.025CrossRefGoogle ScholarPubMed
Blair, C., Granger, D. A., Kivlighan, K. T., Mills-Koonce, R., Willoughby, M., Greenberg, M. T., … Fortunato, C. K. (2008). Maternal and child contributions to cortisol response to emotional arousal in young children from low-income, rural communities. Developmental Psychology, 44, 1095. doi: 10.1037/0012-1649.44.4.1095CrossRefGoogle ScholarPubMed
Blair, C., Granger, D. A., Willoughby, M., Mills-Koonce, R., Cox, M., Greenberg, M. T., … FLP Investigators (2011b). Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood. Child Development, 82, 1970–1984. doi: 10.1111/j.1467-8624.2011.01643CrossRefGoogle Scholar
Blair, C., & Raver, C. C. (2012). Child development in the context of adversity: experiential canalization of brain and behavior. American Psychologist, 67, 309–318. doi: 10.1037/a0027493CrossRefGoogle ScholarPubMed
Blair, C., & Raver, C. C. (2016). Poverty, stress, and brain development: New directions for prevention and intervention. Academic Pediatrics, 16, S30–S36. doi: 10.1016/j.acap.2016.01.010CrossRefGoogle ScholarPubMed
Blair, C., Raver, C. C., Granger, D., Mills-Koonce, R., Hibel, L., & Investigators, F. L. P. (2011a). Allostasis and allostatic load in the context of poverty in early childhood. Development and Psychopathology, 23, 845–857. doi:10.1017/S0954579411000344CrossRefGoogle Scholar
Blaze, J., & Roth, T. L. (2013). Exposure to caregiver maltreatment alters expression levels of epigenetic regulators in the medial prefrontal cortex. International Journal of Developmental Neuroscience, 31, 804–810. doi: 10.1016/j.ijdevneu.2013.10.001CrossRefGoogle ScholarPubMed
Bornstein, M. H. (2013). Mother–Infant Attunement: A Multilevel Approach. In Haley, M. H. B. (Ed.), The infant mind: Origins of the social brain (pp. 266–300). New York, NY: The Guilford Press.Google Scholar
Braren, S. H., Perry, R. E., Ursache, A., & Blair, C. (2019). Socioeconomic risk moderates the association between caregiver cortisol levels and infant cortisol reactivity to emotion induction at 24 months. Developmental Psychobiology, 61, 573–591. doi: 10.1002/dev.21832CrossRefGoogle ScholarPubMed
Brooks-Gunn, J., & Duncan, G. J. (1997). The effects of poverty on children. Future Child, 7, 55–71. doi: 10.2307/1602387CrossRefGoogle ScholarPubMed
Callaghan, B. L., Gee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., … Caldera, C. (2019). Decreased amygdala reactivity to parent cues protects against anxiety following early adversity: An examination across 3 years. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4, 664–671. doi: 10.1016/j.bpsc.2019.02.001Google ScholarPubMed
Callaghan, B. L., Sullivan, R. M., Howell, B., & Tottenham, N. (2014). The international society for developmental psychobiology Sackler symposium: Early adversity and the maturation of emotion circuits—A cross-species analysis. Developmental Psychobiology, 56, 1635–1650. doi: 10.1002/dev.21260CrossRefGoogle Scholar
Cameron, J. L. (2001). Critical periods for social attachment: Deprivation and neural systems in rhesus monkeys. Social Research in Child Development Abstr, 2, 054.Google Scholar
Carew, S. J., Mukherjee, B., MacIntyre, I. T., Ghosh, A., Li, S., Kirouac, G. J., … Yuan, Q. (2018). Pheromone-induced odor associative fear learning in rats. Scientific Reports, 8, 1–10. doi: 10.1038/s41598-018-36023-wCrossRefGoogle ScholarPubMed
Chen, E., Cohen, S., & Miller, G. E. (2010). How low socioeconomic status affects 2-year hormonal trajectories in children. Psychological Science, 21, 31–37. doi: 10.1177/0956797609355566CrossRefGoogle Scholar
Chen, E., & Paterson, L. Q. (2006). Neighborhood, family, and subjective socioeconomic status: How do they relate to adolescent health? Health Psychology, 25, 704. doi: 10.1037/0278-6133.25.6.704CrossRefGoogle ScholarPubMed
Clearfield, M. W., Carter-Rodriguez, A., Merali, A. R., & Shober, R. (2014). The effects of SES on infant and maternal diurnal salivary cortisol output. Infant Behavior and Development, 37, 298–304. doi: 10.1016/j.infbeh.2014.04.008CrossRefGoogle ScholarPubMed
Coe, C. L., Franklin, D., Smith, E. R., & Levine, S. (1982). Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiology & Behavior, 29, 1051–1057. doi: 10.1016/0031-9384(82)90297-9CrossRefGoogle ScholarPubMed
Cohen, M. M., Jing, D., Yang, R. R., Tottenham, N., Lee, F. S., & Casey, B. J. (2013). Early-life stress has persistent effects on amygdala function and development in mice and humans. Proceedings of the National Academy of Sciences, 110, 18274–18278. doi: 10.1073/pnas.1310163110CrossRefGoogle Scholar
Cox, M. (1997). Qualitative ratings: Parent/child interaction at 24-36 months of age. Unpublished coding manual.Google Scholar
Culbert, B. M., Gilmour, K. M., & Balshine, S. (2019). Social buffering of stress in a group-living fish. Proceedings of the Royal Society B, 286, 20191626. doi: doi.org/10.1098/rspb.2019.1626CrossRefGoogle Scholar
Curley, J. P., & Champagne, F. A. (2016). Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods. Frontiers in Neuroendocrinology, 40, 52–66. doi: 10.1016/j.yfrne.2015.11.001CrossRefGoogle ScholarPubMed
Dallman, M. F. (2007). Modulation of stress responses: how we cope with excess glucocorticoids. Experimental Neurology, 206, 179. doi: 10.1016/j.expneurol.2007.06.002CrossRefGoogle ScholarPubMed
Darmon, N., & Drewnowski, A. (2008). Does social class predict diet quality? American Journal of Clinical Nutrition, 87, 1107–1117. doi: 10.1093/ajcn/87.5.1107CrossRefGoogle ScholarPubMed
Davidson, R. J., & McEwen, B. S. (2012). Social influences on neuroplasticity: Stress and interventions to promote well-being. Nature Neuroscience, 15, 689–695. doi: 10.1038/nn.3093CrossRefGoogle ScholarPubMed
Davis, M., West, K., Bilms, J., Morelen, D., & Suveg, C. (2018). A systematic review of parent-child synchrony: It is more than skin deep. Developmental Psychobiology, 60, 674–691. doi:10.1002/dev.21743CrossRefGoogle ScholarPubMed
Debiec, J., & Sullivan, R. M. (2014). Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear. Proceedings of the National Academy of Sciences, 111, 12222–12227. doi: 10.1073/pnas.1316740111CrossRefGoogle ScholarPubMed
Doherty, T. S., Blaze, J., Keller, S. M., & Roth, T. L. (2017). Phenotypic outcomes in adolescence and adulthood in the scarcity-adversity model of low nesting resources outside the home cage. Developmental Psychobiology, 59, 703–714. doi: 10.1002/dev.21547CrossRefGoogle ScholarPubMed
Dozier, M., Stoval, K. C., Albus, K. E., & Bates, B. (2001). Attachment for infants in foster care: The role of caregiver state of mind. Child Development, 72, 1467–1477. doi: 10.1111/1467-8624.00360CrossRefGoogle ScholarPubMed
Duncan, G. J., Ziol-Guest, K. M., & Kalil, A. (2010). Early-childhood poverty and adult attainment, behavior, and health. Child Development, 81, 306–325. doi:10.1111/j.1467-8624.2009.01396.xCrossRefGoogle Scholar
Edgar, J., Held, S., Paul, E., Pettersson, I., Price, R. I. A., & Nicol, C. (2015). Social buffering in a bird. Animal Behaviour, 105, 11–19. doi: 10.1016/j.anbehav.2015.04.007CrossRefGoogle Scholar
Evans, G. W. (2004). The environment of childhood poverty. American Psychologist, 59, 77–92. doi: 10.1037/0003-066X.59.2.77CrossRefGoogle ScholarPubMed
Evans, G. W., & English, K. (2002). The environment of poverty: Multiple stressor exposure, psychophysiological stress, and socioemotional adjustment. Child Development, 73, 1238–1248. doi: 10.1111/1467-8624.00469CrossRefGoogle ScholarPubMed
Evans, G. W., & Schamberg, M. A. (2009). Childhood poverty, chronic stress, and adult working memory. Proceedings of the National Academy of Sciences, 106, 6545–6549. doi: 10.1073/pnas.0811910106CrossRefGoogle ScholarPubMed
Faturi, C. B., Tiba, P. A., Kawakami, S. E., Catallani, B., Kerstens, M., & Suchecki, D. (2010). Disruptions of the mother–infant relationship and stress-related behaviours: altered corticosterone secretion does not explain everything. Neuroscience & Biobehavioral Reviews, 34, 821–834. doi: 10.1016/j.neubiorev.2009.09.002CrossRefGoogle Scholar
Faustino, A. I., Tacão-Monteiro, A., & Oliveira, R. F. (2017). Mechanisms of social buffering of fear in zebrafish. Scientific Reports, 7, 44329. doi: 10.1038/srep44329CrossRefGoogle ScholarPubMed
Feldman, R. (2007). Parent–infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. Journal of Child Psychology and Psychiatry, 48, 329–354. doi:10.1111/j.1469-7610.2006.01701.xCrossRefGoogle ScholarPubMed
Feldman, R. (2012). Bio-behavioral synchrony: A model for integrating biological and microsocial behavioral processes in the study of parenting. Parenting, 12, 154–164. doi:10.1080/15295192.2012.683342CrossRefGoogle Scholar
Feldman, R. (2015). Sensitive periods in human social development: new insights from research on oxytocin, synchrony, and high-risk parenting. Development and Psychopathology, 27, 369–395. doi: 10.1017/S0954579415000048CrossRefGoogle ScholarPubMed
Feldman, R. (2017). The Neurobiology of human attachments. Trends in Cognitive Sciences, 21, 80–99. doi:10.1016/j.tics.2016.11.007CrossRefGoogle ScholarPubMed
Feldman, R., Greenbaum, C. W., Yirmiya, N., & Mayes, L. C. (1996). Relations between cyclicity and regulation in mother-infant interaction at 3 and 9 months and cognition at 2 years. Journal of Applied Developmental Psychology, 17, 347–365. doi: 10.1016/S0193-3973(96)90031-3CrossRefGoogle Scholar
Fernald, L. C., Burke, H. M., & Gunnar, M. R. (2008). Salivary cortisol levels in children of low-income women with high depressive symptomatology. Development and Psychopathology, 20, 423–436. doi: 10.1017/S0954579408000205CrossRefGoogle ScholarPubMed
Field, T. (2012). Relationships as Regulators. Psychology, 3, 467. doi: 10.4236/psych.2012.36066CrossRefGoogle Scholar
Finegood, E. D., Rarick, J. R., Blair, C., & Family Life Project Investigators (2017). Exploring longitudinal associations between neighborhood disadvantage and cortisol levels in early childhood. Development and Psychopathology, 29, 1649–1662. doi: 10.1017/S09554579417001304CrossRefGoogle ScholarPubMed
Fleming, A. S., & Li, M. (2002). Psychobiology of maternal behavior and its early determinants in nonhuman mammals. In Bornstein, M. H. (Ed.), Handbook of parenting: Biology and ecology of parenting (pp. 61–97). Mahwah, NJ: Lawrence Erlbaum Associates Publishers.Google Scholar
Frankenhuis, W. E., & Nettle, D. (2019). The Strengths of people in poverty. Current Directions in Psychological Science, 29, 16–2. doi:10.1177/0963721419881154CrossRefGoogle Scholar
Gee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., Shapiro, M., … Tottenham, N. (2014). Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence. Psychological Science, 25, 2067–2078. doi: 10.1177/0956797614550878CrossRefGoogle Scholar
Gottlieb, G. (1996). Developmental psychobiological theory. In Cairns, R. B., Elder, J. H., & Costello, E. J. (Eds.), Developmental science (pp. 63–77). New York, NY: Cambridge University Press.CrossRefGoogle Scholar
Granero, R., Louwaars, L., & Ezpeleta, L. (2015). Socioeconomic status and oppositional defiant disorder in preschoolers: parenting practices and executive functioning as mediating variables. Frontiers in Psychology, 6, 1412. doi:10.3389/fpsyg.2015.01412CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199–220. doi: 10.1016/S0306-4530(01)00045-2CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Fisher, P. A. (2006). Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Development and Psychopathology, 18, 651–677. doi: 10.1017/S0954579406060330CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Herrera, A. M. (2013). The development of stress reactivity: A neurobiological perspective. In Zelazo, P. D. (Ed.), The Oxford handbook of developmental psychology: Vol.2. Self and other (pp. 45–80). New York, NY: Oxford University Press.Google Scholar
Gunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015). Parental buffering of fear and stress neurobiology: Reviewing parallels across rodent, monkey, and human models. Social Neuroscience, 10, 474–47. doi: 10.1080/17470919.2015.1070198CrossRefGoogle ScholarPubMed
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173. doi:10.1146/annurev.psych.58.110405.085605CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Sullivan, R. M. (2017). The neurodevelopment of social buffering and fear learning: integration and crosstalk. Social Neuroscience, 12, 1–7. doi: 10.1080/17470919.2016.1151824CrossRefGoogle ScholarPubMed
Hackman, D. A., & Farah, M. J. (2009). Socioeconomic status and the developing brain. Trends in Cognitive Sciences, 13, 65–73. doi: 10.1016/j.tics.2008.11.003CrossRefGoogle ScholarPubMed
Hackman, D. A., Gallop, R., Evans, G. W., & Farah, M. J. (2015). Socioeconomic status and executive function: developmental trajectories and mediation. Developmental Science, 18, 686–702. doi: 10.1111/desc.12246CrossRefGoogle ScholarPubMed
Halevi, G., Djalovski, A., Kanat-Maymon, Y., Yirmiya, K., Zagoory-Sharon, O., Koren, L., & Feldman, R. (2017). The social transmission of risk: Maternal stress physiology, synchronous parenting, and well-being mediate the effects of war exposure on child psychopathology. Journal of Abnormal Psychology, 126, 1087–1103. doi: 10.1037/abn0000307CrossRefGoogle ScholarPubMed
Harrist, A. W., & Waugh, R. M. (2002). Dyadic synchrony: Its structure and function in children's development. Developmental Review, 22, 555–592. doi: 10.1016/S0273-2297(02)00500-2CrossRefGoogle Scholar
Hennessy, M. B., Kaiser, S., & Sachser, N. (2009). Social buffering of the stress response: diversity, mechanisms, and functions. Frontiers in Neuroendocrinology, 30, 470–482. doi: 10.1016/j.yfrne.2009.06.001CrossRefGoogle ScholarPubMed
Hennessy, M. B., Zate, R., & Maken, D. S. (2008). Social buffering of the cortisol response of adult female guinea pigs. Physiology & Behavior, 93, 883–888. doi: 10.1016/j.physbeh.2007.12.005CrossRefGoogle ScholarPubMed
Herzberg, M. P., & Gunnar, M. R. (2019). Early life stress and brain function: Activity and connectivity associated with processing emotion and reward. NeuroImage, 209, 116493. doi: 10.1016/j.neuroimage.2019.116493CrossRefGoogle ScholarPubMed
Hibel, L. C., Mercado, E., & Valentino, K. (2019). Child maltreatment and mother–child transmission of stress physiology. Child Maltreatment, 24, 340–352. doi: 10.1016/j.physbeh.2018.07.024CrossRefGoogle ScholarPubMed
Hibel, L. C., Trumbell, J. M., Valentino, K., & Buhler-Wassmann, A. C. (2018). Ecologically salient stressors and supports and the coordination of cortisol and salivary alpha-amylase in mothers and infants. Physiology & Behavior, 195, 48–57. doi: 10.1016/j.physbeh.2018.07.024CrossRefGoogle ScholarPubMed
Hill-Soderlund, A. L., Holochwost, S. J., Willoughby, M. T., Granger, D. A., Gariépy, J. L., Mills-Koonce, W. R., & Cox, M. J. (2015). The developmental course of salivary alpha-amylase and cortisol from 12 to 36 months: Relations with early poverty and later behavior problems. Psychoneuroendocrinology, 52, 311–323. doi: 10.1016/j.psyneuen.2014.08.011CrossRefGoogle ScholarPubMed
Hofer, M. A. (1984). Relationships as regulators: A psychobiologic perspective on bereavement. Psychosomatic Medicine, 46, 183–197. doi:10.1097/00006842-198405000-00001CrossRefGoogle ScholarPubMed
Hofer, M. A. (1994). Hidden regulators in attachment, separation, and loss. Monographs of the Society for Research in Child Development, 59, 192–207. doi:10.2307/1166146CrossRefGoogle ScholarPubMed
Holochwost, S. J., Gariépy, J.-L., Propper, C. B., Gardner-Neblett, N., Volpe, V., Neblett, E., & Mills-Koonce, W. R. (2016). Sociodemographic risk, parenting, and executive functions in early childhood: The role of ethnicity. Early Childhood Research Quarterly, 36, 537–549. doi: 10.1016/j.ecresq.2016.02.001CrossRefGoogle Scholar
Hostinar, C. E., Johnson, A. E., & Gunnar, M. R. (2015). Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Developmental Science, 18, 281–297. doi: 10.1111/desc.12195CrossRefGoogle ScholarPubMed
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the HPA axis: A review of animal models and human studies across development. Psychological Bulletin, 140, 256. doi: 10.1037/a0032671CrossRefGoogle ScholarPubMed
Ivy, A. S., Brunson, K. L., Sandman, C., & Baram, T. Z. (2008). Dysfunctional nurturing behavior in rat dams with limited access to nesting material: A clinically relevant model for early-life stress. Neuroscience, 154, 1132–1142. doi: 10.1016/j.neuroscience.2008.04.019CrossRefGoogle ScholarPubMed
Jessen, S. (2020). Maternal odor reduces the neural threat response in human infants. Developmental Cognitive Neuroscience, 45, 100858.CrossRefGoogle Scholar
Junod, A., Opendak, M., LeDoux, J. E., & Sullivan, R. M. (2019). Development of threat expression following infant maltreatment: Infant and adult enhancement but adolescent attenuation. Frontiers in Behavioral Neuroscience, 13, 130. doi:10.3389/fnbeh.2019.00130CrossRefGoogle ScholarPubMed
Karb, R. A., Elliott, M. R., Dowd, J. B., & Morenoff, J. D. (2012a). Neighborhood-level stressors, social support, and diurnal patterns of cortisol: The Chicago community adult health study. Social Science & Medicine, 75, 1038–1047. doi:10.1016/j.socscimed.2012.03.031CrossRefGoogle Scholar
Karb, R. A., Elliott, M. R., Dowd, J. B., & Morenoff, J. D. (2012b). Neighborhood-level stressors, social support, and diurnal patterns of cortisol: The Chicago community adult health study. Social Science & Medicine, 75, 1038–1047. doi:10.1016/j.socscimed.2012.03.031CrossRefGoogle Scholar
Keum, S., & Shin, H. S. (2019). Neural basis of observational fear learning: A potential model of affective empathy. Neuron, 104, 78–86. doi: j.neuron.2019.09.013CrossRefGoogle ScholarPubMed
Kikusui, T., Winslow, J. T., & Mori, Y. (2006). Social buffering: relief from stress and anxiety. Philosophical Transactions of the Royal Society B: Biological Sciences, 361, 2215–2228CrossRefGoogle ScholarPubMed
Kliewer, W., Reid-Quiñones, K., Shields, B. J., & Foutz, L. (2009). Multiple risks, emotion regulation skill, and cortisol in low-income African American youth: A prospective study. Journal of Black Psychology, 35, 24–43. doi: 10.1177/0095798408323355CrossRefGoogle Scholar
Kline, R. B. (2015). Principles and practice of structural equation modeling (4th ed.). New York, NY: Guilford Publications.Google Scholar
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, 59, 327–346. doi: 10.1111/jcpp.12784CrossRefGoogle ScholarPubMed
Lengua, L. J., Thompson, S. F., Moran, L. R., Zalewski, M., Ruberry, E. J., Klein, M. R., & Kiff, C. J. (2019). Pathways from early adversity to later adjustment: Tests of the additive and bidirectional effects of executive control and diurnal cortisol in early childhood. Development and Psychopathology, 33, 545–558. doi:10.1017/S0954579419000373.Google Scholar
Lipina, S. J., & Posner, M. I. (2012). The impact of poverty on the development of brain networks. Frontiers in Human Neuroscience, 6, 238. doi: 10.3389/fnhum.2012.00238CrossRefGoogle ScholarPubMed
Loman, M. M., & Gunnar, M. R. (2010). Early experience and the development of stress reactivity and regulation in children. Neuroscience & Biobehavioral Reviews, 34, 867–876. doi: 10.1016/j.neubiorev.2009.05.007CrossRefGoogle ScholarPubMed
Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., … Barch, D. (2013). The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatrics, 167, 1135–1142. doi: 10.1001/jamapediatrics.2013.3139CrossRefGoogle ScholarPubMed
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2000). Child's stress hormone levels correlate with mother's socioeconomic status and depressive state. Biological Psychiatry, 48, 976–980. doi: 10.1016/S0006-3223(00)00965-3CrossRefGoogle ScholarPubMed
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2001). Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status. Development and Psychopathology, 13, 653–676. doi: 10.1017/S0954579401003133CrossRefGoogle ScholarPubMed
Masten, A. S., & Cicchetti, D. (2010). Developmental cascades. Developmental Psychopathology, 22, 491–495. doi: 10.1017/S0954579410000222CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44. doi: 10.1111/j.1749-6632.1998.tb09546.xCrossRefGoogle ScholarPubMed
McEwen, B. S., & Gianaros, P. J. (2011). Stress-and allostasis-induced brain plasticity. Annual Review of Medicine, 62, 431–445. doi: 10.1146/annurev-med-052209-100430CrossRefGoogle ScholarPubMed
McLoyd, V. C. (1998). Socioeconomic disadvantage and child development. American Psychologist, 53, 185–204. doi: 10.1037/0003-066X.53.2.185CrossRefGoogle ScholarPubMed
Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin, 133, 25–45. doi:10.1037/0033-2909.133.1.25CrossRefGoogle ScholarPubMed
Monfils, M. H., & Agee, L. A. (2019). Insights from social transmission of information in rodents. Genes, Brain and Behavior, 18, e12534. doi: 10.1111/gbb.12534CrossRefGoogle ScholarPubMed
Moriceau, S., Wilson, D. A., Levine, S., & Sullivan, R. M. (2006). Dual circuitry for odor–shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. Journal of Neuroscience, 26, 6737–6748. doi: 10.1523/JNEUROSCI.0499-06.2006CrossRefGoogle ScholarPubMed
Muthén, L. K., & Muthén, B. O. (1998-2012). Mplus User's Guide (7th ed.). Los Angeles, CA: Muthén & Muthén.Google Scholar
National Institute of Child Health and Human Development Early Child Care Research Network (NICHD ECCRN). (1999). Child care and mother-child interaction in the first 3 years of life. Developmental Psychology, 35, 1399–1413. doi: 10.1016/S0163-6383(03)00035-3CrossRefGoogle Scholar
Opendak, M., Robinson-Drummer, P., Blomkvist, A., Zanca, R. M., Wood, K., Jacobs, L., … Kirschner, E. (2019). Neurobiology of maternal regulation of infant fear: The role of mesolimbic dopamine and its disruption by maltreatment. Neuropsychopharmacology, 44, 1247–1257. doi: 10.1038/s41386-019-0340-9CrossRefGoogle ScholarPubMed
Opendak, M., & Sullivan, R. M. (2016). Unique neurobiology during the sensitive period for attachment produces distinctive infant trauma processing. European Journal of Psychotraumatology, 7, 31276. doi: 10.3402/ejpt.v7.31276CrossRefGoogle ScholarPubMed
Opendak, M., Theisen, E., Blomkvist, A., Hollis, K., Lind, T., Sarro, E., … Sullivan, R. M. (2020). Adverse caregiving in infancy blunts neural processing of the mother: Translating across species. Nature Communication, 11, 1–12. doi:10.1038/s41467-020-14801-3..CrossRefGoogle Scholar
Papousek, M. (2007). Communication in early infancy: an arena of intersubjective learning. Infant Behavior and Development, 30, 258–266. doi:10.1016/j.infbeh.2007.02.003CrossRefGoogle ScholarPubMed
Papoušek, H., & Papoušek, M. (2002). Intuitive parenting. In Bornstein, H. Marc, (Eds.), Handbook of parenting: Biology and ecology of parenting Vol. 2 (2nd ed). (pp. 183–203). Mahwah, NJ: Lawrence Erlbaum Associates Publishers.Google Scholar
Perry, R. E. (2019). Poverty and its impact: enhancing mechanistic research via a cross-species approach. In Lipina, S. J., & Segretin, M. S. (Eds.), Exploraciones neurocientíficas de la pobreza (pp. 230-254). Erice, Italy: International Mind, Brain and Education School (Ettore Majorana Foundation for Scientific Culture). ISBN 978-987-86-2055-8.Google Scholar
Perry, R. E., Blair, C., & Sullivan, R. M. (2017). Neurobiology of infant attachment: Attachment despite adversity and parental programming of emotionality. Current Opinion in Psychology, 17, 1–6. doi: 10.1016/j.copsyc.2017.04.022CrossRefGoogle ScholarPubMed
Perry, R. E., Braren, S. H., Rincón Cortés, M., Brandes-Aitken, A. N., Chopra, D., Sullivan, R. M., & Blair, C. (2019a). Enhancing executive functions through social interactions: Causal evidence using a cross-species model. Frontiers in Psychology, 10, 2472. doi: 10.3389/fpsyg.2019.02472CrossRefGoogle Scholar
Perry, R. E., Finegood, E. D., Braren, S. H., DeJoseph, M. L., Putrino, D. F., Wilson, D. A., … Blair, C., Family Life Project Key Investigators. (2019b). Developing a neurobehavioral animal model of poverty: Drawing cross-species connections between environments of scarcity-adversity, parenting quality, and infant outcome. Development and Psychopathology, 31, 399–418. doi: 10.1017/S095457941800007X.CrossRefGoogle Scholar
Perry, R. E., Rincón-Cortés, M., Braren, S. H., Brandes-Aitken, A. N., Opendak, M., Pollonini, G., … Sullivan, R. M. (2019c). Corticosterone administration targeting a hypo-reactive HPA axis rescues a socially-avoidant phenotype in scarcity-adversity reared rats. Developmental Cognitive Neuroscience, 40, 100716. doi: 10.1016/j.dcn.2019.100716CrossRefGoogle Scholar
Perry, R., & Sullivan, R. M. (2014). Neurobiology of attachment to an abusive caregiver: Short-term benefits and long-term costs. Developmental Psychobiology, 56, 1626–1634. doi: 10.1016/j.copsyc.2017.04.022CrossRefGoogle Scholar
Preacher, K. J., & Hayes, A. F. (2008). Effect size measures for mediation models: quantitative strategies for communicating indirect effects. Behavioral Research Methods, 40, 879–891. doi: 10.1037/a0022658CrossRefGoogle Scholar
Raineki, C., Morgan, E. J., Ellis, L., & Weinberg, J. (2019a). Glucocorticoid receptor expression in the stress-limbic circuitry is differentially affected by prenatal alcohol exposure and adolescent stress. Brain Research, 1718, 242–251. doi: 10.1016/j.brainres.2019.05.019CrossRefGoogle Scholar
Raineki, C., Moriceau, S., & Sullivan, R. (2010). Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biological Psychiatry, 67, 1137–1145. doi: 10.1016/j.biopsych.2009.12.019CrossRefGoogle Scholar
Raineki, C., Opendak, M., Sarro, E., Showler, A., Bui, K., McEwen, B. S., … Sullivan, R. M. (2019b). During infant maltreatment, stress targets hippocampus, but stress with mother present targets amygdala and social behavior. Proceedings of the National Academy of Sciences, 116, 22821–22831. doi: 10.1073/pnas.1907170116CrossRefGoogle Scholar
Raineki, C., Rincón-Cortés, M., Belnoue, L., & Sullivan, R. M. (2012). Effects of early-life abuse differ across development: Infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala. The Journal of Neuroscience, 32, 7758–7765. doi:10.1523/jneurosci.5843-11.2012CrossRefGoogle ScholarPubMed
Rickenbacher, E., Perry, R. E., Sullivan, R. M., & Moita, M. A. (2017). Freezing suppression by oxytocin in central amygdala allows alternate defensive behaviours and mother-pup interactions. Elife, 6, e24080. doi: 10.7554/eLife.24080CrossRefGoogle ScholarPubMed
Rincón-Cortés, M., Barr, G. A., Mouly, A. M., Shionoya, K., Nuñez, B. S., & Sullivan, R. M. (2015). Enduring good memories of infant trauma: rescue of adult neurobehavioral deficits via amygdala serotonin and corticosterone interaction. Proceedings of the National Academy of Sciences of the United States of America, 112, 881–886. doi:10.1073/pnas.1416065112CrossRefGoogle ScholarPubMed
Rincón-Cortés, M., & Sullivan, R. M. (2016). Emergence of social behavior deficit, blunted corticolimbic activity and adult depression-like behavior in a rodent model of maternal maltreatment. Translational Psychiatry, 6, e930. doi: 10.1038/tp.2016.205CrossRefGoogle Scholar
Robinson-Drummer, P. A., Opendak, M., Blomkvist, A., Chan, S., Tan, S., Delmer, C., … Chopra, D. (2019). Infant trauma alters social buffering of threat learning: emerging role of prefrontal cortex in preadolescence. Frontiers in Behavioral Neuroscience, 13, 132. doi:10.3389/fnbeh.2019.00132CrossRefGoogle ScholarPubMed
Rosenfeld, P., Suchecki, D., & Levine, S. (1992). Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neuroscience & Biobehavioral Reviews, 16, 553–568. doi: 10.1016/S0149-7634(05)80196-4CrossRefGoogle ScholarPubMed
Roth, T. L., & Sullivan, R. M. (2005). Memory of early maltreatment: Neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biological Psychiatry, 57, 823–831. doi: 10.1016/j.biopsych.2005.01.032CrossRefGoogle ScholarPubMed
Roth, T. L., & Sweatt, D. J. (2011). Annual research review: epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development. Journal of Child Psychology and Psychiatry, 52, 398–408. doi: 10.1111/j.1469-7610.2010.02282.xCrossRefGoogle ScholarPubMed
Sapolsky, R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research Reviews, 11, 65–76. doi: 10.1016/0165-0173(86)90010-XCrossRefGoogle Scholar
Schreiber, J. E., Shirtcliff, E., Van Hulle, C., Lemery-Chalfant, K., Klein, M. H., Kalin, N. H., … Goldsmith, H. H. (2006). Environmental influences on family similarity in afternoon cortisol levels: twin and parent-offspring designs. Psychoneuroendocrinology, 31, 1131–1137. doi: 10.1016/j.psyneuen.2006.07.005CrossRefGoogle ScholarPubMed
Seltzer, L. J., Ziegler, T. E., & Pollak, S. D. (2010). Social vocalizations can release oxytocin in humans. Proceedings of the Royal Society B: Biological Sciences, 277, 2661–2666. doi: 10.1098/rspb.2010.0567CrossRefGoogle ScholarPubMed
Sevelinges, Y., Moriceau, S., Holman, P., Miner, C., Muzny, K., Gervias, R., … Sullivan, R. M. (2007). Enduring effects of infant memories: infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biological Psychiatry, 62, 1070–1079. doi:10.1016/j.biopsych.2007.04.025CrossRefGoogle ScholarPubMed
Shionoya, K., Moriceau, S., Bradstock, P., & Sullivan, R. M. (2007). Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups. Hormones and Behavior, 52, 391–400. doi: 10.1016/j.yhbeh.2007.06.004CrossRefGoogle ScholarPubMed
Shrout, P. E., & Bolger, N. (2002). Mediation in experimental and nonexperimental studies: new procedures and recommendations. Psychological Methods, 7, 422–445. doi: 10.1037/1082-989X.7.4.422CrossRefGoogle ScholarPubMed
Skinner, E. A., Kindermann, T. A., Connell, J. P., & Wellborn, J. G. (2009). Engagement and disaffection as organizational constructs in the dynamics of motivational development. In Wentzel, K. & Vigfield, A. (Eds.), Handbook of motivation at school (pp. 223–245). New York: Routledge.Google Scholar
Stanton, M. E., & Levine, S. (1988). Maternal modulation of infant glucocorticoid stress responses: Role of age and maternal deprivation. Psychobiology, 16, 223–228. doi: 10.3758/BF03327311CrossRefGoogle Scholar
Stanton, M. E., & Levine, S. (1990). Inhibition of infant glucocorticoid stress response: specific role of maternal cues. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology, 23, 411–426. doi: 10.1002/dev.420230504CrossRefGoogle ScholarPubMed
Stanton, M. E., Patterson, J. M., & Levine, S. (1985). Social influences on conditioned cortisol secretion in the squirrel monkey. Psychoneuroendocrinology, 10, 125–134. doi: 10.1016/0306-4530(85)90050-2CrossRefGoogle ScholarPubMed
Suchecki, D., Nelson, D. Y., Van Oers, H., & Levine, S. (1995). Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: effects of maternal deprivation. Psychoneuroendocrinology, 20, 169–182. doi: 10.1016/0306-4530(94)00051-BCrossRefGoogle ScholarPubMed
Sullivan, R. M., & Perry, R. E. (2015). Mechanisms and functional implications of social buffering in infants: Lessons from animal models. Social Neuroscience, 10, 500–511. doi: 10.1002/dev.21260CrossRefGoogle ScholarPubMed
Suor, J. H., Sturge-Apple, M. L., Davies, P. T., Cicchetti, D., & Manning, L. G. (2015). Tracing differential pathways of risk: Associations among family adversity, cortisol, and cognitive functioning in childhood. Child Development, 86, 1142–1158. doi: 10.1111/cdev.12376CrossRefGoogle ScholarPubMed
Tottenham, N., Shapiro, M., Flannery, J., Caldera, C., & Sullivan, R. M. (2019). Parental presence switches avoidance to attraction learning in children. Nature Human Behaviour, 3, 1070–1077. doi: 10.1038/s41562-019-0656-9CrossRefGoogle ScholarPubMed
Upton, K. J., & Sullivan, R. M. (2010). Defining age limits of the sensitive period for attachment learning in rat pups. Developmental Psychobiology, 52, 453–464. doi: 10.1002/dev.20448CrossRefGoogle ScholarPubMed
Ursache, A., Noble, K. G., & Blair, C. (2015). Socioeconomic status, subjective social status, and perceived stress: Associations with stress physiology and executive functioning. Behavioral Medicine, 41, 145–154. doi: 10.1080/08964289.2015.1024604CrossRefGoogle ScholarPubMed
Van Hulle, C. A., Shirtcliff, E. A., Lemery-Chalfant, K., & Goldsmith, H. H. (2012). Genetic and environmental influences on individual differences in cortisol level and circadian rhythm in middle childhood. Hormones and Behavior, 62, 36–42. doi: 10.1016/j.yhbeh.2012.04.014CrossRefGoogle ScholarPubMed
Vernon-Feagans, L., & Cox, M. (2013). The Family Life Project: An epidemiological and developmental study of young children living in poor rural communities. Monographs of the Society for Research in Child Development, 78, 1–150.CrossRefGoogle ScholarPubMed
Walker, C. D., Bath, K. G., Joels, M., Korosi, A., Larauche, M., Lucassen, P. J., … Taché, Y. (2017). Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential. Stress, 20, 421–448. doi: 10.1080/10253890.2017.1343296CrossRefGoogle ScholarPubMed
Waters, S. F., West, T. V., & Mendes, W. B. (2014). Stress contagion: physiological covariation between mothers and infants. Psychological Science, 25, 934–942. doi:10.1177/0956797613518352CrossRefGoogle ScholarPubMed
Welch, M. G., Firestein, M. R., Austin, J., Hane, A. A., Stark, R. I., Hofer, M. A., … Myers, M. M. (2015). Family nurture intervention in the neonatal intensive care unit improves social-relatedness, attention, and neurodevelopment of preterm infants at 18 months in a randomized controlled trial. Journal of Child Psychology and Psychiatry, 56, 1202–1211. doi: 10.1111/jcpp.12405CrossRefGoogle Scholar
Wiener, S. G., Johnson, D. F., & Levine, S. (1987). Influence of postnatal rearing conditions on the response of squirrel monkey infants to brief perturbations in mother-infant relationships. Physiology & Behavior, 39, 21–26. doi: 10.1016/0031-9384(87)90339-8CrossRefGoogle ScholarPubMed
Yoshikawa, H., Aber, J. L., & Beardslee, W. R. (2012). The effects of poverty on the mental, emotional, and behavioral health of children and youth: implications for prevention. American Psychologist, 67, 272–284. doi: 10.1037/a0028015CrossRefGoogle ScholarPubMed
Zalewski, M., Lengua, L. J., Kiff, C. J., & Fisher, P. A. (2012). Understanding the relation of low income to HPA-axis functioning in preschool children: cumulative family risk and parenting as pathways to disruptions in cortisol. Child Psychiatry & Human Development, 43, 924–942. doi:10.1007/s10578-012-0304-3CrossRefGoogle ScholarPubMed
Zelenko, M., Kraemer, H., Huffman, L., Gschwendt, M., Pageler, N., & Steiner, H. (2005). Heart rate correlates of attachment status in young mothers and their infants. Journal of the American Academy of Child & Adolescent Psychiatry, 44, 470–476. doi: 10.1097/01.chi.0000157325.10232.b1CrossRefGoogle ScholarPubMed