Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T05:28:16.737Z Has data issue: false hasContentIssue false
  • English
  • Français

Mother–infant cortisol attunement: Associations with mother–infant attachment disorganization

Published online by Cambridge University Press:  14 January 2019

Jaclyn A. (Ludmer) Nofech-Mozes ,
Brittany Jamieson ,
Andrea Gonzalez  and
Leslie Atkinson
Jaclyn A. (Ludmer) Nofech-Mozes
Affiliation:
Department of Psychology, Ryerson University, Toronto, ON, Canada
Brittany Jamieson
Affiliation:
Department of Psychology, Ryerson University, Toronto, ON, Canada
Andrea Gonzalez
Affiliation:
Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, ON, Canada
Leslie Atkinson*
Affiliation:
Department of Psychology, Ryerson University, Toronto, ON, Canada
*
Author for correspondence: Leslie Atkinson, Department of Psychology, Ryerson University, 350 Victoria Street, M5B 2K3, Toronto, Ontario, Canada; Email: atkinson@psych.ryerson.ca.
Get access Rights & Permissions [Opens in a new window]

Abstract

This study explores the conceptualization of mother–infant cortisol attunement both theoretically and empirically, and its association with mother–infant attachment disorganization. In a community sample (N = 256), disorganization and cortisol were assessed during the Strange Situation Procedure (SSP) at infant age 17 months. Salivary cortisol was collected at baseline, and 20 and 40 min after the SSP. We utilized three statistical approaches: correlated growth modeling (probing a simultaneous conceptualization of attunement), cross-lagged modeling (probing a lagged, reciprocal conceptualization of attunement), and a multilevel model difference score analysis (to examine the pattern of discrepancies in mother–infant cortisol values). Correlated growth modeling revealed that disorganized, relative to organized, dyads had significant magnitude of change over time, such that, among disorganized dyads, as mothers had greater declines in cortisol, infants had greater increases. The difference score analysis revealed that disorganized, relative to organized, dyads had a greater divergence between maternal and infant cortisol values, such that maternal values were lower than infant values. Disorganized attachment status was not significantly associated with attunement when conceptualized as reciprocal and lagged in the cross-lagged model. Findings suggest that mother–infant dyads in disorganized attachment relationships, who are by definition behaviorally misattuned, are also misattuned in their adrenocortical responses.

Keywords

attachmentattunementcortisoldisorganizedstrange situation
Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Issue 1 , February 2020 , pp. 43 - 55
Copyright
Copyright © Cambridge University Press 2019

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

*

Author Jaclyn (Ludmer) Nofech-Mozes has formerly published under the name Jaclyn Ludmer.

†

Authors Jaclyn Nofech-Mozes and Brittany Jamieson contributed equally to this article and should be considered co-first-authors.

References

Ainsworth, M. D. S., Blehar, M. C., Waters, E., & Wall, S. (1978). Patterns of attachment: A psychological study of the strange situation. Hillside, NJ: Erlbaum.Google Scholar
Atkinson, L., Gonzalez, A., Kashy, D. A., Santo Basile, V., Masellis, M., Pereira, J., … Levitan, R. (2013). Maternal sensitivity and infant and mother adrenocortical function across challenges. Psychoneuroendocrinology, 38, 2943–2951.CrossRefGoogle ScholarPubMed
Atkinson, L., Jamieson, B., Khoury, J., Ludmer, J., & Gonzalez, A. (2016). Stress physiology in infancy and early childhood: Cortisol flexibility, attunement and coordination. Journal of Neuroendocrinology, 28, 1–12.CrossRefGoogle ScholarPubMed
Bakermans-Kranenberg, M. J., van IJzendoorn, M. H., Mesman, J., Alink, L. R. A., & Juffer, F. (2008). Effects of an attachment-based intervention on daily cortisol moderated by dopamine receptor D4: A randomized control trial on 1- to 3-year-olds screened for externalizing behavior. Development and Psychopathology, 20, 805–820.CrossRefGoogle Scholar
Beebe, B., Jaffe, J., Markese, S., Buck, K., Chen, H., Cohen, P., … Feldstein, S. (2010). The origins of 12-month attachment: A microanalysis of 4-month mother–infant interaction. Attachment & Human Development, 12, 3–141.CrossRefGoogle ScholarPubMed
Bernard, K., Dozier, M., Bick, J., Lewis-Morrarty, E., Lindhiem, O., & Carlson, E. (2012). Enhancing attachment organization among maltreated children: Results of a randomized clinical trial. Child Development, 83, 623–636.CrossRefGoogle ScholarPubMed
Bernard, N. K., Kashy, D. A., Levendosky, A. A., Bogat, G. A., & Lonstein, J. S. (2016). Do different data analytic approaches generate discrepant findings when measuring mother–infant HPA axis attunement? Developmental psychobiology, 59, 174–184.CrossRefGoogle ScholarPubMed
Bright, M. A., Granger, D. A., & Frick, J. E. (2012). Do infants show a cortisol awakening response? Developmental Psychobiology, 54, 736–743.CrossRefGoogle ScholarPubMed
Collins, L. M., Schafer, J. L., & Kam, C. (2001). A comparison of inclusive and restrictive strategies in modern missing data procedures. Psychological Methods, 6, 330–351.CrossRefGoogle ScholarPubMed
Crockett, E. E., Holmes, B. M., Granger, D. A., & Lyons-Ruth, K. (2013). Maternal disrupted communication during face-to-face interaction at 4 months: Relation to maternal and infant cortisol among at-risk families. Infancy, 18, 1111–1134.CrossRefGoogle ScholarPubMed
Davis, E. P., & Granger, D. A. (2009). Developmental differences in infant salivary alpha-amylase and cortisol responses to stress. Psychoneuroendocrinology, 34, 795–804.CrossRefGoogle ScholarPubMed
Davis, M., & Emory, E. (1995). Sex differences in neonatal stress reactivity. Child Development, 66, 14–27.CrossRefGoogle ScholarPubMed
De Weerth, C., & van Geert, P. (2002). A longitudinal study of basal cortisol in infants: Intra-individual variability, circadian rhythm and developmental trends. Infant Behavior and Development, 25, 375–398.CrossRefGoogle Scholar
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–391.CrossRefGoogle ScholarPubMed
Dozier, M., Peloso, E., Lewis, E., Laurenceau, J. P., & Levine, S. (2008). Effects of an attachment-based intervention on the cortisol production of infants and toddlers in foster care. Development and psychopathology, 20, 845–859.CrossRefGoogle ScholarPubMed
Dozier, M., Peloso, E., Lindhiem, O., Gordon, M. K., Manni, M., Sepulveda, S., … Levine, S. (2006). Preliminary evidence from a randomized clinical trial: Intervention effects on foster children's behavioral and biological regulation. Journal of Social Issues, 62, 767–785.CrossRefGoogle Scholar
Feldman, R. (2006). From biological rhythms to social rhythms: Physiological precursors of mother-infant synchrony. Developmental Psychology, 42, 175–188. doi:10.1037/0012-1649.42.1.175CrossRefGoogle ScholarPubMed
Feldman, R. (2012). Bio-behavioral synchrony: A model for integrating biological and microsocial behavioral processes in the study of parenting, Parenting: Science and Practice, 12, 154–164.CrossRefGoogle Scholar
Field, T. M., Scafidi, F., Pickens, J., Prodromidis, M., Pelaez-Nogueras, M., Torquati, J., … Kuhn, C. (1998). Polydrug-using adolescent mothers and their infants receiving early intervention. Adolescence, 33, 117–144.Google ScholarPubMed
Fisher, D. B., Serbin, L. A., Stack, D. M., Ruttle, P. L., Ledingham, J. E., & Schwartzman, A. E. (2007). Intergenerational predictors of diurnal cortisol secretion in early childhood. Infant and Child Development, 16, 151–170.CrossRefGoogle Scholar
Fries, E., Hesse, J., Hellhammer, J., & Hellhammer, D. H. (2005). A new view on hypocortisolism. Psychoneuroendocrinology, 30, 1010–1016.CrossRefGoogle ScholarPubMed
Genazzani, A. R., Lemarchand-Beraud, T. H., Aubert, M. L., Felber, J. P., Muller, A., Lavanchy, M., & Gomez, J. (1975). Pattern of plasma ACTH, hGH, and cortisol during menstrual cycle. Journal of Clinical Endocrinology & Metabolism, 41, 431–437.CrossRefGoogle ScholarPubMed
Goldberg, S., Grusec, J., & Jenkins, J. M. (1999). Confidence in protection: Arguments for a narrow definition of attachment. Journal of Family Psychology, 13, 475–483.CrossRefGoogle Scholar
Goldberg, S., Levitan, R., Leung, E., Masellis, M., Basile, V, Nemeroff, C. B., & Atkinson, L. (2003). Stability of baseline and stress cortisol concentrations in 12–18-month-old infants: Issues of time, location, and stressor. Biological Psychiatry, 54, 719–726.CrossRefGoogle Scholar
Gustafsson, P. E., Anckarsäter, H., Lichtenstein, P., Nelson, N., & Gustafsson, P. A. (2010). Does quantity have a quality all its own? Cumulative adversity and up- and down-regulation of circadian salivary cortisol levels in healthy children. Psychoneuroendocrinology, 35, 1410–1415.CrossRefGoogle ScholarPubMed
Hertsgaard, L., Gunnar, M., Erickson, M. F., & Nachmias, M. (1995). Adrenocortical responses to the Strange Situation in infants with disorganized/disoriented attachment relationships. Child Development, 66, 1100–1106.CrossRefGoogle ScholarPubMed
Hesse, E., & Main, M. (2000). Disorganized infant, child, and adult attachment: Collapse in behavioral and attentional strategies. Journal of the American Psychoanalytic Association, 48, 1097–1127.CrossRefGoogle ScholarPubMed
Hibel, L. C., Granger, D. A., Blair, C., Cox, M. J., & Family Life Project Key Investigators. (2009). Intimate partner violence moderates the association between mother-infant adrenocortical activity across emotional challenge. Journal of Family Psychology, 23, 615–625.CrossRefGoogle ScholarPubMed
Hibel, L. C., Granger, D. A., Blair, C., Finegood, E. D., & Family Life Project Key Investigators. (2015). Maternal-child adrenocortical attunement in early childhood: Continuity and change. Developmental Psychobiology, 57, 83–95.CrossRefGoogle ScholarPubMed
Hibel, L. C., & Mercado, E. (2017). Marital conflict predicts mother-to-infant adrenocortical transmission. Child Development, 1–16. doi:10.1111/cdev.13010Google ScholarPubMed
Hruschka, D. J., Khort, B. A., & Worthman, C. M. (2005). Estimating between- and within- individual variation in cortisol levels using multilevel models. Psychoneuroendocrinology, 30, 698–714.CrossRefGoogle ScholarPubMed
Isabella, R. A., & Belsky, J. (1991). Interactional synchrony and the origins of infant-mother attachment: A replication study. Child Development, 62, 373–384.CrossRefGoogle ScholarPubMed
Jansen, J., Biejers, R., Riksen-Walraven, M., & de Weerth, C. (2010). Cortisol reactivity in young infants. Psychoneuroendocrinology, 35, 329–338.CrossRefGoogle ScholarPubMed
Juffer, F., Bakermans-Kranenburg, M. J., & IJzendoorn, M. H. (2005). The importance of parenting in the development of disorganized attachment: Evidence from a preventive intervention study in adoptive families. Journal of Child Psychology and Psychiatry, 46, 263–274.CrossRefGoogle ScholarPubMed
Kenny, D. A., & Kashy, D. A. (2011). Dyadic data analysis using multilevel modeling. In Hox, J. & Roberts, J. K. (Eds.), Handbook of advanced multilevel analysis (pp. 335–370). New York: Taylor & Francis Group.Google Scholar
Kenny, D. A., Kashy, D. A., & Cook, W. L. (2006). Dyadic data analysis. New York: Cambridge University Press.Google Scholar
Khoury, J. E., Gonzalez, A., Levitan, R., Masellis, M., Vincenzo, B., & Atkinson, L. (2015). Infant emotion regulation strategy moderates relations between self-reported maternal depressive symptoms and infant HPA activity. Infant and Child Development, 25, 64–83. doi:10.1002/icd.1916Google Scholar
Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1995). Preliminary evidence for reduced cortisol responsivity to psychological stress in women using oral contraceptive medication. Psychoneuroendocrinology, 20, 509–514.CrossRefGoogle ScholarPubMed
Kraemer, G. W. (1992). A psychobiological theory of attachment. Brain and Behavior Sciences, 15, 493–541.CrossRefGoogle ScholarPubMed
Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for categorical data. Biometrics, 33, 159–174.CrossRefGoogle ScholarPubMed
Lasikiewicz, N., Hendrickx, H., Talbot, D., & Dye, L. (2008). Exploration of basal diurnal salivary cortisol profiles in middle-aged adults: Associations with sleep quality and metabolic parameters. Psychoneuroendocrinology, 33, 143–151.CrossRefGoogle ScholarPubMed
Laurent, H. K., Ablow, J. C., & Measelle, J. (2011). Risky shifts: How the timing and course of mothers' depressive symptoms across the perinatal period shape their own and infant's stress response profiles. Development and Psychopathology, 23, 521–538.CrossRefGoogle ScholarPubMed
Leclère, C., Viaux, S., Avril, M., Achard, C., Chetouani, M., Missonnier, S., & Cohen, D. (2014). Why synchrony matters during mother-child interactions: A systematic review. PLOS ONE, 9, e113571.CrossRefGoogle ScholarPubMed
Letourneau, N., Watson, B., Duffett-Leger, L., Hegadoren, K., & Tryphonopoulos, P. (2011). Cortisol patterns of depressed mothers and their infants are related to maternal-infant interactive behaviours. Journal of Reproductive and Infant Psychology, 29, 439–459. doi:10.1080/02646838.2011.649474CrossRefGoogle Scholar
Ludmer, J. A., Jamieson, B., Gonzalez, A., Levitan, R., Kennedy, J., Villani, V., … Atkinson, L. (2017). Maternal DRD2, SLC6A3, and OXTR genotypes as potential moderators of the relation between maternal history of care and maternal cortisol secretion in the context of mother-infant separation. Biological Psychology, 129, 154–164.CrossRefGoogle ScholarPubMed
Luijk, M. P., Saridjan, N., Tharner, A., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Jaddoe, V. W., … Tiemeier, H. (2010). Attachment, depression, and cortisol: Deviant patterns in insecure-resistant and disorganized infants. Developmental Psychobiology, 52, 441–452.CrossRefGoogle ScholarPubMed
Lyons-Ruth, K., Bronfman, E., & Parsons, E. (1999). Atypical attachment in infancy and early childhood among children at developmental risk: Part IV. Maternal frightened, frightening, or atypical behavior and disorganized infant attachment patterns. Monographs of the Society for Research in Child Development, 64, 67–96.CrossRefGoogle ScholarPubMed
Lyons-Ruth, K., & Jacobvitz, D. (2016). Attachment disorganization: Genetic factors, parenting contexts, and developmental transformation from infancy to adulthood. In Cassidy, J. & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research, and clinical applications (pp. 666–697). New York: Guildford Press.Google Scholar
Madigan, S., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Moran, G., Pederson, D. R., & Benoit, D. (2006). Unresolved states of mind, anomalous parental behavior, and disorganized attachment: A review and meta-analysis of a transmission gap. Attachment and Human Development, 8, 89–111.CrossRefGoogle ScholarPubMed
Main, M., & Solomon, J. (1986). Discovery of an insecure-disorganized/disoriented attachment pattern. In Brazelton, T. B. & Yogman, M. W. (Eds.), Affective development in infancy (pp. 95–124). Westport, CT: Ablex.Google Scholar
Main, M., & Solomon, J. (1990). Procedures for identifying infants as disorganized/disoriented during the Ainsworth Strange Situation. In Greenberg, M. T., Cicchetti, D., & Cummings, E. M. (Eds.), Attachment in the preschool years: Theory, research, and intervention. Chicago: University of Chicago Press.Google Scholar
Makel, M. C., Plucker, J. A., & Hegarty, B. (2012). Replications in psychology research: How often do they really occur? Perspectives on Psychological Science, 7, 537–542.CrossRefGoogle ScholarPubMed
Middlemiss, W., Granger, D. A., Goldberg, W., & Nathans, L. (2012). Asynchrony of mother-infant hypothalamic-pituitary-adrenal axis activity following extinction of infant crying responses induced during the transition to sleep. Early Human Development, 88, 227–232.CrossRefGoogle ScholarPubMed
Milligan, K., Atkinson, L., Trehub, S. E., Benoit, D., & Poulton, L. (2003). Maternal attachment and the communication of emotion through song. Infant Behavior & Development, 26, 1–13.CrossRefGoogle Scholar
Pereira, J., Vickers, K., Atkinson, L., Gonzalez, A., Wekerle, C., & Levitan, R. (2012). Parenting stress mediates between maternal maltreatment history and maternal sensitivity in a community sample. Child Abuse & Neglect, 36, 433–437.CrossRefGoogle Scholar
Raudenbush, S. W., & Bryk, A. S. (2002). Hierarchical linear models: Applications and data analysis methods (2nd ed.). Thousand Oaks, CA: Sage.Google Scholar
Raudenbush, S. W., Bryk, A. S., Cheong, Y. F., Congdon, R., & du Toit, M. (2011). HLM 7: Hierarchical linear and nonlinear modelling. Lincolnwood, IL: Scientific Software International.Google Scholar
Reeves, J. W., Fisher, A. J., Newman, M. G., & Granger, D. A. (2016). Sympathetic and hypothalamic-pituitary-adrenal asymmetry in generalized anxiety disorder. Psychophysiology, 53, 951–957.CrossRefGoogle ScholarPubMed
Rutter, M., & Sroufe, L. A. (2000). Developmental psychopathology: Concepts and challenges. Development and Psychopathology, 12, 265–296.CrossRefGoogle ScholarPubMed
Sethre-Hofstad, L., Stansbury, K., & Rice, M. A. (2002). Attunement of maternal and child adrenocortical response to child challenge. Psychoneuroendocrinology, 27, 731–747.CrossRefGoogle ScholarPubMed
Spanglar, G., Schieche, M., Ilg, U., Maier, U., & Ackermann, C. (1994). Maternal sensitivity as an external organizer for biobehavioral regulation in infancy. Developmental Psychobiology, 27, 425–437.CrossRefGoogle Scholar
Sugawara, J., Tarumi, T., & Tanaka, H. (2010). Effect of mirthful laughter on vascular function. American Journal of Cardiology, 106, 856–859.CrossRefGoogle ScholarPubMed
Toth, S. L., Sturge-Apple, M. L., Rogosch, F. A., & Cicchetti, D. (2015). Mechanisms of change: Testing how preventative interventions impact psychological and physiological stress functioning in mothers in neglectful families. Development and Psychopathology, 27, 1661–1674.CrossRefGoogle ScholarPubMed
Tronick, E. Z., Als, H., Adamson, L., Wise, S., & Brazelton, T. B. (1978). The infant's response to entrapment between contradictory messages in face-to-face interaction. Journal of American Academy of Child Psychiatry, 17, 1–13.CrossRefGoogle ScholarPubMed
Tu, M. T., Lupien, S. J., & Walker, C. D. (2006). Multiparity reveals the blunting effect of breastfeeding on physiological reactivity to psychological stress. Journal of Neuroendocrinology, 18, 494–503.CrossRefGoogle ScholarPubMed
Urizar, G. G., & Muñoz, R. F. (2011). Impact of a prenatal cognitive-behavioral stress management intervention on salivary cortisol levels in low-income mothers and their infants. Psychoneuroendocrinology, 36, 1480–1494.CrossRefGoogle ScholarPubMed
van Bakel, H. J. A., & Riksen-Walraven, J. M. (2008). Adrenocortical and behavioural attunement in parents with 1-year-old infants. Developmental Psychobiology, 50, 196–201.CrossRefGoogle ScholarPubMed
van Cauter, E., Leproult, R., & Kupfer, D. J. (1996). Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol. Journal of Clinical Endocrinology & Metabolism, 81, 2468–2473.Google ScholarPubMed
West, M., & George, C. (1999). Abuse and violence in intimate adult relationships: New perspectives from attachment theory. Attachment and Human Development, 1, 137–156.CrossRefGoogle ScholarPubMed
Wüst, S., Federenko, I., Hellhammer, D. H., & Kirschbaum, C. (2000). Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrinology, 25, 707–720.CrossRefGoogle ScholarPubMed
Zeanah, C. H., Danis, B., Hirshberg, L., Benoit, D., Miller, D., & Heller, S. S. (1999). Disorganized attachment associated with partner violence: A research note. Infant Mental Health Journal, 20, 77–86.3.0.CO;2-S>CrossRefGoogle Scholar