Early caregiving stress exposure moderates the relation between respiratory sinus arrhythmia reactivity at 1 month and biobehavioral outcomes at age 3

Psychophysiology

Volumn 53, Issue 1, 2016, Pages 83-96

  Conradt, Elisabeth ^a   Beauchaine, Theodore ^b   Abar, Beau ^c   Lagasse, Linda ^d,e   Shankaran, Seetha ^f   Bada, Henrietta ^g   Bauer, Charles ^h   Whitaker, Toni ⁱ   Hammond, Jane ^j   Lester, Barry ^d,e  

^a UNIVERSITY OF UTAH   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d WOMEN AND INFANTS HOSPITAL   (United States)

^e BROWN UNIVERSITY   (United States)

^f WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF KENTUCKY   (United States)

^h UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^j RTI INTERNATIONAL   (United States)

more..

Author keywords

Heart rate; Individual differences; Infants children

Indexed keywords

CAREGIVER; CHILD BEHAVIOR; DRUG DEPENDENCE; FEMALE; FOLLOW UP; HUMAN; INFANT; MALE; MENTAL STRESS; PHYSIOLOGY; POVERTY; PRESCHOOL CHILD; PROBLEM BEHAVIOR; PSYCHOLOGY; RESPIRATORY SINUS ARRHYTHMIA;

CAREGIVERS; CHILD BEHAVIOR; CHILD, PRESCHOOL; FEMALE; FOLLOW-UP STUDIES; HUMANS; INFANT; MALE; POVERTY; PROBLEM BEHAVIOR; RESPIRATORY SINUS ARRHYTHMIA; STRESS, PSYCHOLOGICAL; SUBSTANCE-RELATED DISORDERS;

EID: 84952700625     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/psyp.12569     Document Type: Article

References (85)

1. Abidin, R. R. (1990). Parenting Stress Index (PSI). Charlottesville, VA: Pediatric Psychology Press.
2. Achenbach, T. M. (1992). Manual for the Child Behavior Checklist/2-3 and 1992 profile. Burlington: Department of Psychiatry, University of Vermont.
3. Adler, N. E., Boyce, T., Chesney, M. A., Cohen, S., Folkman, S., Kahn, R. L., & Syme, S. L. (1994). Socioeconomic status and health: The challenge of the gradient. American Psychologist, 49, 15-24.
4. Adler, N. E., Epel, E. S., Castellazzo, G., & Ickovics, J. R. (2000). Relationship of subjective and objective social status with psychological and physiological functioning: Preliminary data in healthy white women. Health Psychology, 19, 586-592. doi: 10.1037/0278-6133.19.6.586
5. Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42, 64-78. doi: 10.1002/dev.10082
6. Appleyard, K., Egeland, B., Dulmen, M. H., & Alan Sroufe, L. (2005). When more is not better: The role of cumulative risk in child behavior outcomes. Journal of Child Psychology and Psychiatry, 46, 235-245. doi: 10.1111/j.1469-7610.2004.00351.x
7. Ashman, S. B., Dawson, G., & Panagiotides, H. (2008). Trajectories of maternal depression over 7 years: Relations with child psychophysiology and behavior and role of contextual risks. Development and Psychopathology, 20, 55-77.
8. Barker, D. J. P. (1998). Mothers, babies and health in later life (2nd ed.). London, England: Churchill Livingstone.
9. Barker, D. J. P., & Osmond, C. (1986). Infant mortality, childhood nutrition and ischaemic heart disease in England and Wales. Lancet, 1, 1077-1081.
10. Beauchaine, T. P. (2001). Vagal tone, development, and Gray's motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13, 183-214.
11. Beauchaine, T. P. (2015). Respiratory sinus arrhythmia: A transdiagnostic biomarker of emotion dysregulation and psychopathology. Current Opinion in Psychology, 3, 43-47. doi: 10.1016/j.copsyc.2015.01.017
12. Beauchaine, T. P., Gatzke-Kopp, L., & Mead, H. K. (2007). Polyvagal theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence. Biological Psychology, 74, 174-184. doi: 10.1016/j.biopsycho.2005.08.008
13. Beauchaine, T. P., Gatzke-Kopp, L. M., Neuhaus, E., Chipman, J., Reid, M. J., & Webster-Stratton, C. (2013). Sympathetic- and parasympathetic-linked cardiac function and prediction of externalizing behavior, emotion regulation, and prosocial behavior among preschoolers treated for ADHD. Journal of Consulting and Clinical Psychology, 81, 481-493. doi: 10.1037/a0032302
14. Beauchaine, T. P., & McNulty, T. (2013). Comorbidities and continuities as ontogenic processes: Toward a developmental spectrum model of externalizing behavior. Development and Psychopathology, 25, 1505-1528. doi: 10.1017/S0954579413000746
15. Beauchaine, T. P., Neuhaus, E., Brenner, S. L., & Gatzke-Kopp, L. (2008). Ten good reasons to consider biological processes in prevention and intervention research. Development and Psychopathology, 20, 745-774. doi: 10.1017/S0954579408000369
16. Beauchaine, T. P., Neuhaus, E., Gatzke-Kopp, L. M., Reid, M. J., Brekke, A., Olliges, A., Webster-Stratton, C. (2015). Electrodermal responding predicts responses to, and may be altered by, preschool intervention for ADHD. Journal of Consulting and Clinical Psychology, 83, 293-303. doi: 10.1037/a0038405
17. Beauchaine, T. P., Neuhaus, E., Zalewski, M., Crowell, S. E., & Potapova, N. (2011). Effects of allostatic load on neural systems subserving motivation, mood regulation, and social affiliation. Development and Psychopathology, 23, 975-999. doi: 10.1017/S0954579411000459
18. Beauchaine, T. P., & Thayer, J. F. (2015). Heart rate variability as a transdiagnostic biomarker of psychopathology. International Journal of Psychophysiology.
19. Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Beck Depression Inventory. San Antonio, TX: The Psychological Corporation.
20. Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 289-300.
21. Berntson, G., Bigger, J., Eckberg, D., Grossman, P., Kaufmann, P. G., Malik, M., van der Molen, M. W. (1997). Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology, 34, 623-648. doi: 10.1111/j.1469-8986.1997.tb02140.x
22. Bornstein, M. H., & Suess, P. E. (2000). Child and mother cardiac vagal tone: Continuity, stability, and concordance across the first 5 years. Developmental Psychology, 36, 54-65. doi: 10.1037/0012-1649.36.1.54
23. Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271-301.
24. Boyce, W. T., Sokolowski, M. B., & Robinson, G. E. (2012). Toward a new biology of social adversity. Proceedings of the National Academy of Sciences, 109, 17143-17148. doi: 10.1073/pnas.1121264109
25. Bradley, R. H., & Corwyn, R. F. (2002). Socioeconomic status and child development. Annual Review of Psychology, 53, 371-399. doi: 10.1146/annurev.psych.53.100901.135233
26. Brooker, R. J., Buss, K. A., Lemery-Chalfant, K., Aksan, N., Davidson, R. J., & Goldsmith, H. H. (2013). The development of stranger fear in infancy and toddlerhood: normative development, individual differences, antecedents, and outcomes. Developmental Science, 16, 864-878.
27. Brooks-Gunn, J., & Duncan, G. J. (1997). The effects of poverty on children. The Future of Children, 7, 55-71.
28. Bush, N. R., Alkon, A., Obradović, J., Stamperdahl, J., & Boyce, W. T. (2011). Differentiating challenge reactivity from psychomotor activity in studies of children's psychophysiology: Considerations for theory and measurement. Journal of Experimental Child Psychology, 110, 62-79. doi: 10.1016/j.jecp.2011.03.004
29. Bush, N. R., & Boyce, W. T. (2014). The contributions of early experience to biological development and sensitivity to context. In Handbook of Developmental Psychopathology (pp. 287-309). Springer US.
30. Buss, K. A., Hill Goldsmith, H., & Davidson, R. J. (2005). Cardiac reactivity is associated with changes in negative emotion in 24-month-olds. Developmental Psychobiology, 46, 118-132.
31. Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74, 144-153. doi: 10.1016/j.biopsycho.2006.09.005
32. Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45, 101-112. doi: 10.1002/dev.20020
33. Conradt, E., Abar, B., Sheinkopf, S., Lester, B., Lagasse, L., Seifer, R., Higgins, R. (2014). The role of prenatal substance exposure and early adversity on parasympathetic functioning from 3 to 6 years of age. Developmental Psychobiology, 56, 821-835. doi: 10.1002/dev.21155
34. Conradt, E., & Ablow, J. (2010). Infant physiological response to the still-face paradigm: Contributions of maternal sensitivity and infants' early regulatory behavior. Infant Behavior and Development, 33, 251-265. doi: 10.1016/j.infbeh.2010.01.001
35. Conradt, E., Measelle, J., & Ablow, J. C. (2013). Poverty, problem behavior, and promise: Differential susceptibility among infants reared in poverty. Psychological Science, 24, 235 -242. doi: 10.1177/0956797612457381.
36. Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience and Biobehavioral Reviews, 35, 1562-1592. doi: 10.1016/j.neubiorev.2010.11.007
37. Derogatis, L. R., & Coons, H. L. (1993). Self-report measures of stress (2nd ed.). New York: Free Press.
38. Dong, M., Anda, R. F., Felitti, V. J., Dube, S. R., Williamson, D. F., Thompson, T. J., Giles, W. H. (2004). The interrelatedness of multiple forms of childhood abuse, neglect, and household dysfunction. Child Abuse and Neglect, 28, 771-784.
39. Doussard-Roosevelt, J. A., Montgomery, L. A., & Porges, S. W. (2003). Short-term stability of physiological measures in kindergarten children: Respiratory sinus arrhythmia, heart period, and cortisol. Developmental Psychobiology, 43, 230-242. doi: 10.1002/dev.10136
40. El-Sheikh, M., & Hinnant, J. B. (2011). Marital conflict, respiratory sinus arrhythmia, and allostatic load: Interrelations and associations with the development of children's externalizing behavior. Development and Psychopathology, 23, 815-829. doi: 10.1017/S0954579411000320
41. El-Sheikh, M., Hinnant, B., & Erath, S. (2011). Developmental trajectories of delinquency symptoms in childhood: The role of martial conflict and autonomic nervous system activity. Journal of Abnormal Psychology, 120, 16-32.
42. Entringer, S., Buss, C., & Wadhwa, P. D. (2010). Prenatal stress and developmental programming of human health and disease risk: Concepts and integration of empirical findings. Current Opinion in Endocrinology, Diabetes, and Obesity, 17, 507-516. doi: 10.1097/MED.0b013e3283405921
43. Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002). Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biological Psychiatry, 52, 776-784.
44. Evans, G. W., & Kim, P. (2007). Childhood poverty and health cumulative risk exposure and stress dysregulation. Psychological Science, 18, 953-957.
45. Evans, G. W., & Kim, P. (2012). Early childhood poverty and adult chronic physiological stress: The mediating role of childhood cumulative risk exposure. Psychological Science, 23, 979-983. doi: 10.1177/0956797612441218
46. Evans, G. W., & Kim, P. (2013). Childhood poverty, chronic stress, self-regulation, and coping. Child Development Perspectives, 7, 43-48. doi: 10.1111/cdep.12013
47. Field, T., Diego, M., Dieter, J., Hernandez-Reif, M., Schanberg, S., Kuhn, C., Bendell, D. (2004). Prenatal depression effects on the fetus and the newborn. Infant Behavior and Development, 27, 216-229. doi: 10.1016/j.infbeh.2003.09.010
48. Fisher, P. A., Lester, B. M., DeGarmo, D. S., Lagasse, L. L., Lin, H., Shankaran, S., Higgins, R. (2011). The combined effects of prenatal drug exposure and early adversity on neurobehavioral disinhibition in childhood and adolescence. Development and Psychopathology, 23, 777-788. doi: 10.1017/S0954579411000290
49. Gatzke-Kopp, L. M. (2016). Diversity and representation: Key issues for psychophysiological science. Psychophysiology, 53, 3-13.
50. Gatzke-Kopp, L. M., Greenberg, M., & Bierman, K. (2015). Children's parasympathetic reactivity to specific emotions moderates response to intervention for early-onset aggression. Journal of Clinical Child & Adolescent Psychology, 44, 291-304.
51. Grossman, P. (1983). Respiration, stress and cardiovascular function. Psychophysiology, 20, 284-300. doi: 10.1111/j.1469-8986.1983.tb02156.x
52. Harnish, J. D., Dodge, K. A., Valente, E., & the Conduct Problems Prevention Research Group. (1995). Mother-child interaction quality as a partial mediator of the roles of maternal depressive symptomatology and socioeconomic status in the development of child behavior problems. Child Development, 66, 739-753.
53. Hastings, P. D., Sullivan, C., McShane, K. E., Coplan, R. J., Utendale, W. T., & Vyncke, J. D. (2008). Parental socialization, vagal regulation, and preschoolers' anxious difficulties: Direct mothers and moderated fathers. Child Development, 79, 45-64.
54. Hertzman, C. (1999). The biological embedding of early experience and its effects on health in adulthood. Annals of the New York Academy of Sciences, 896, 85-95.
55. Hinnant, J. B., Elmore-Staton, L., & El-Sheikh, M. (2010). Developmental trajecotires of respiratory sinus arrhythmia and preejection period in middle childhood. Developmental Psychobiology, 53, 59-68.
56. Hollingshead, A. B. (1975). Four Factor Index of Social Status. New Haven, CT: Yale University Press.
57. Holochwost, S. J., Gariépy, J.-L., Propper, C. B., Mills-Koonce, W. R., & Moore, G. A. (2014). Parenting behaviors and vagal tone at six months predict attachment disorganization at twelve months. Developmental Psychobiology, 56, 1423-1430. doi: 10.1002/dev.21221
58. Hostinar, C. E., & Gunnar, M. R. (2013). The developmental effects of early life stress: An overview of current theoretical frameworks. Current Directions in Psychological Science, 22, 400-406. doi: 10.1177/0963721413488889
59. Jennings, J. R., Berg, W. K., Hutcheson, J. S., Obrist, P., Porges, S., & Turpin, G. (1981). Publication guidelines for heart rate studies in man. Psychophysiology, 18, 226-231. doi: 10.1111/j.1469-8986.1981.tb03023.x
60. Johnston-Brooks, C. H., Lewis, M. A., Evans, G. W., & Whalen, C. K. (1998). Chronic stress and illness in children: the role of allostatic load. Psychosomatic Medicine, 60, 597-603.
61. Kishiyama, M. M., Boyce, W. T., Jimenez, A. M., Perry, L. M., & Knight, R. T. (2008). Socioeconomic disparities affect prefrontal function in children. Journal of Cognitive Neurosocience, 21, 1106-1115. doi: 10.1162/jocn.2009.21101
62. Lepore, S. J., Revenson, T. A., Weinberger, S. L., Weston, P., Frisina, P. G., Roberston, R., Cross, W. (2006). Effects of social stressors on cardiovascular reactivity in black and white women. Annals of Behavioral Medicine, 31, 120-127.
63. Lester, B. M., & Tronick, E. Z. (2004). The neonatal intensive care unit network neurobehavioral scale procedures. Pediatrics, 113, 641-667.
64. Mayet, S., Groshkova, T., Morgan, L., MacCormack, T., & Strang, J. (2008). Drugs and pregnancy-outcomes of women engaged with a specialist perinatal outreach addictions service. Drug and Alcohol Review, 27, 497-503.
65. McEwen, B. S., & Gianaros, P. J. (2010). Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease. Annals of the New York Academy of Sciences, 1186, 190-222. doi: 10.1111/j.1749-6632.2009.05331.x
66. McEwen, B. S., & Stellar, E. (1993). Stress and the individual: Mechanisms leading to disease. Archives of Internal Medicine, 153, 2093-2101.
67. Meaney, M. J., Szyf, M., & Seckl, J. R. (2007). Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in Molecular Medicine, 13, 269-277.
68. 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.
69. Moore, G. A., & Calkins, S. D. (2004). Infants' vagal regulation in the still-face paradigm is related to dyadic coordination of mother-infant interaction. Developmental Psychology, 40, 1068-1080. doi: 10.1037/0012-1649.40.6.1068
70. Obradović, J. (2012). How can the study of physiological reactivity contribute to our understanding of adversity and resilience processes in development? Development and Psychopathology, 24, 371-387. doi: 10.1017/S0954579412000053
71. Obradović, J., Bush, N. R., Stamperdahl, J., Adler, N. E., & Boyce, W. T. (2010). Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Development, 81, 270-289. doi: 10.1111/j.1467-8624.2009.01394.x
72. Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A polyvagal theory. Psychophysiology, 32, 301-318. doi: 10.1111/j.1469-8986.1995.tb01213.x
73. Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116-143. doi: 10.1016/j.biopsycho.2006.06.009
74. Propper, C. B. (2013). The early development of vagal tone: Effects of poverty and elevated contextual risk. In V. Maholmes & R. B. King (Eds.), Oxford handbook of poverty and child development (pp. 103-123). New York: Oxford University Press.
75. Propper, C. B., & Holochwost, S. J. (2013). The influence of proximal risk on the early development of the autonomic nervous system. Developmental Review, 33, 151-167.
76. Propper, C., Moore, G. A., Mills-Koonce, W. R., Halpern, C. T., Hill-Soderlund, A. L., Calkins, S. D., Cox, M. (2008). Gene-environment contributions to the development of infant vagal reactivity: The interaction of dopamine and maternal sensitivity. Child Development, 79, 1377-1394.
77. Rose, S. L., Rose, S. A., & Feldman, J. F. (1989). Stability of behavior problems in very young children. Development and Psychopathology, 1, 5-19.
78. Sandman, C. A. (2015). Fetal exposure to placental corticotropin-releasing hormone (pCRH) programs developmental trajectories. Peptides. Epub ahead of print.
79. Shankaran, S., Bauer, C. R., Bada, H. S., Lester, B. M., Wright, L. L., & Katsikiotis, V. (1996). Maternal Lifestyle Study: Patterns of cocaine use in term pregnancy and effect on birthweight. Pediatric Research, 39, 279. doi: 10.1203/00006450-199604001-01684
80. Shonkoff, J. P., Boyce, W. T., & McEwen, B. S. (2009). Neuroscience, molecular biology, and the childhood roots of health disparities: Building a new framework for health promotion and disease prevention. Journal of the American Medical Association, 301, 2252-2259. doi: 10.1001/jama.2009.754
81. Skowron, E. A., Cipriano-Essel, E., Gatzke-Kopp, L. M., Teti, D. M., & Ammerman, R. T. (2014). Early adversity, RSA, and inhibitory control: Evidence of children's neurobiological sensitivity to social context. Developmental Psychobiology, 56, 964-978.
82. Smith, D. K., Johnson, A. B., Pears, K. C., Fisher, P. A., & DeGarmo, D. S. (2007). Child maltreatment and foster care: Unpacking the effects of prenatal and postnatal parental substance use. Child Maltreatment, 12, 150-160.
83. Suess, P. E., Porges, S. W., & Plude, D. J. (1994). Cardiac vagal tone and sustained attention in school-age children. Psychophysiology, 31, 17-22. doi: 10.1111/j.1469-8986.1994.tb01020.x
84. Yumoto, C., Jacobson, S. W., & Jacobson, J. L. (2008). Fetal substance exposure and cumulative environmental risk in an African American cohort. Child Development, 79, 1761-1776.
85. Zisner, A. R., & Beauchaine, T. P. (2015). Midbrain neural mechanisms of trait impulsivity. The Oxford Handbook of Externalizing Spectrum Disorders, 184.