Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-22T19:09:39.244Z Has data issue: false hasContentIssue false

Transacting brains: testing an actor–partner model of frontal EEG activity in mother–infant dyads

Published online by Cambridge University Press:  27 October 2020

John E. Krzeczkowski*
Affiliation:
Neuroscience Graduate Program, McMaster University, Hamilton, ON, Canada
Ryan J. Van Lieshout
Affiliation:
Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, ON, Canada
Louis A. Schmidt
Affiliation:
Psychology, Neuroscience & Behaviour, McMaster University, Hamilton, ON, Canada
*
Author for Correspondence: John E. Krzeczkowski, Neuroscience Graduate Program, McMaster University, 1280 Main St W, Hamilton, ONL8S 4L8; E-mail: [email protected]

Abstract

Studies have long observed the bidirectional nature of mother–infant relationships. While behavioral studies have shown that mothers high in social avoidance tendencies can influence the development of these traits in their offspring, the neurophysiological mechanisms underlying this phenomenon, and the role that the infants play, are not well understood. Here we acquired frontal electroencephalogram asymmetry (FA) data simultaneously in 40 mother–infant dyads (Mage mother = 31.6 years; Mage infant = 9 months). Using an actor–partner interdependence model, we examined whether mother (or infant) resting-state FA predicted infant (or mother) FA during two subsequent emotion-eliciting conditions (happy and fear). Maternal social approach versus avoidance traits were assessed as moderators to examine the impact of maternal characteristics on these mother–infant FA relations. In dyads led by mothers with high social avoidance/low social approach characteristics, maternal resting-state FA predicted infant FA during both emotion-eliciting conditions. We did not observe any effects of infant FA on mothers. Therefore, we speculate that individual differences in FA patterns might be a putative brain mechanism through which socially avoidant mothers transfer affective/behavioral information to their infants.

Type
Regular Article
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.)

References

Allen, J. J. B., Coan, J. A., & Nazarian, M. (2004). Issues and assumptions on the road from raw signals to metrics of frontal EEG asymmetry in emotion. Biological Psychology, 67, 183218.CrossRefGoogle ScholarPubMed
Allen, J. J. B., & Reznik, S. J. (2015). Frontal EEG asymmetry as a promising marker of depression vulnerability: Summary and methodological considerations. Current Opinion in Psychology, 28, 9397.CrossRefGoogle Scholar
Atkinson, L., Gonzalez, A., Kashy, D. A., Santo Basile, V., Masellis, M., Pereira, J., Chisholm, V., et al. (2013). Maternal sensitivity and infant and mother adrenocortical function across challenges. Psychoneuroendocrinology, 38, 29432951.CrossRefGoogle ScholarPubMed
Atzaba-Poria, N., Deater-Deckard, K., & Bell, M. A. (2017). Mother–child interaction: Links between mother and child frontal electroencephalograph asymmetry and negative behavior. Child Development, 88, 544554.CrossRefGoogle ScholarPubMed
Atzil, S., Gao, W., Fradkin, I., & Barrett, L. F. (2018). Growing a social brain. Nature Human Behaviour, 2, 624636.CrossRefGoogle ScholarPubMed
Bell, M. A. (2002). Power changes in infant EEG frequency bands during a spatial working memory task. Psychophysiology, 39, 450458.CrossRefGoogle ScholarPubMed
Bell, R. Q. (1979). Parent, child, and reciprocal influences. American Psychologist, 34, 821826.CrossRefGoogle Scholar
Bernard, N. K., Kashy, D. A., Levendosky, A. A., Bogat, G. A., & Lonstein, J. S. (2017). Do different data analytic approaches generate discrepant findings when measuring mother–infant HPA axis attunement? Developmental Psychobiology, 59, 174184.CrossRefGoogle ScholarPubMed
Brooker, R. J., Neiderhiser, J. M., Leve, L. D., Shaw, D. S., Scaramella, L. V., & Reiss, D. (2015). Associations between infant negative affect and parent anxiety symptoms are bidirectional: Evidence from mothers and fathers. Frontiers in Psychology, 6, 110.CrossRefGoogle ScholarPubMed
Cacioppo, J. T., Gardner, W. L., & Bernston, G. G. (1999). The affect system: Form follows function. Journal of Personality and Social Psychology, 76, 839855.CrossRefGoogle Scholar
Campbell, M. J., Schmidt, L. A., Santesso, D. L., Van Ameringen, M., Mancini, C. L., & Oakman, J. M. (2007). Behavioral and psychophysiological characteristics of children of parents with social phobia: A pilot study. International Journal of Neuroscience, 117, 605616.CrossRefGoogle ScholarPubMed
Cheek, J. M., & Buss, A. H. (1981). Shyness and sociability. Journal of Personality and Social Psychology, 41, 330339.CrossRefGoogle Scholar
Clauss, N. J., Byrd-Craven, J., Kennison, S. M., & Chua, K. J. (2018). The roles of mothers’ partner satisfaction and mother-infant communication duration in mother-infant adrenocortical attunement. Adaptive Human Behavior and Physiology, 4, 91107.CrossRefGoogle Scholar
Coan, J. A., & Allen, J. J. B. (2004). Frontal EEG asymmetry as a moderator and mediator of emotion. Biological Psychology, 67, 749.CrossRefGoogle ScholarPubMed
Cook, W. L., & Kenny, D. A. (2005). The actor–partner interdependence model: A model of bidirectional effects in developmental studies. International Journal of Behavioral Development, 29, 101109.CrossRefGoogle Scholar
Cooper, P. J., & Eke, M. (1999). Childhood shyness and maternal social phobia: A community study. British Journal of Psychiatry, 174, 439443.CrossRefGoogle ScholarPubMed
Coplan, R. J., Arbeau, K. A., & Armer, M. (2008). Don't fret, be supportive! maternal characteristics linking child shyness to psychosocial and school adjustment in kindergarten. Journal of Abnormal Child Psychology, 36, 359371.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, 11111134.CrossRefGoogle ScholarPubMed
Davidson, R. J. (2000). Affective style, psychopathology, and resilience: Brain mechanisms and plasticity. American Psychologist, 55, 12141230.CrossRefGoogle ScholarPubMed
Deater-Deckard, K., Li, M., & Bell, M.A. (2015). Multifaceted emotion regulation, stress and affect in mothers of young children. Cognition and Emotion, 30, 444457.CrossRefGoogle ScholarPubMed
Degnan, K. A., Henderson, H. A., Fox, N. A., & Rubin, K. H. (2008). Predicting social wariness in middle childhood: The moderating roles of childcare history, maternal personality and maternal behavior. Social Development, 17, 471487.CrossRefGoogle Scholar
de Rosnay, M., Cooper, P. J., Tsigaras, N., & Murray, L. (2006). Transmission of social anxiety from mother to infant: An experimental study using a social referencing paradigm. Behaviour Research and Therapy, 44, 11651175.CrossRefGoogle ScholarPubMed
Diaz, A., & Bell, M. A. (2012). Frontal EEG asymmetry and fear reactivity in different contexts at 10 months. Developmental Psychobiology, 54, 536545.CrossRefGoogle ScholarPubMed
Diego, M. A., Field, T., Jones, N. A., & Hernandez-Reif, M. (2006). Withdrawn and intrusive maternal interaction style and infant frontal EEG asymmetry shifts in infants of depressed and non-depressed mothers. Infant Behavior and Development, 29, 220229.CrossRefGoogle ScholarPubMed
Diego, M. A., Jones, N. A., & Field, T. (2010). EEG in 1-week, 1-month and 3-month-old infants of depressed and non-depressed mothers. Biological Psychology, 83, 714.CrossRefGoogle ScholarPubMed
Driscoll, K. A., Schatschneider, C., Mcginnity, K., & Modi, A. C. (2012). Application of dyadic data analysis in pediatric psychology: Cystic fibrosis health-related quality of life and anxiety in child–caregiver dyads. Journal of Pediatric Psychology, 37, 605611.CrossRefGoogle 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 and Allied Disciplines, 48, 329354.CrossRefGoogle ScholarPubMed
Field, T. (1992). Infants of depressed mothers. Development and Psychopathology, 4, 4966.CrossRefGoogle Scholar
Field, T. (2011). Prenatal depression effects on early development: A review. Infant Behavior and Development, 34, 114.CrossRefGoogle ScholarPubMed
Field, T. (2018). Postnatal anxiety prevalence, predictors and effects on development: A narrative review. Infant Behavior and Development, 51, 2432.CrossRefGoogle ScholarPubMed
Field, T., Healy, B., Goldstein, S., Perry, S., Bendell, D., Field, T., Healy, B., et al. (1988). Infants of depressed mothers show “depressed” behavior even with nondepressed adults. Child Development, 59, 15691579.CrossRefGoogle ScholarPubMed
Fox, N. A. (1991). If it's not left, it's right: electroencephalograph asymmetry and the development of emotion. American Psychologist, 46, 863872.CrossRefGoogle Scholar
Fox, N. A. (1994). Dynamic cerebral-processes underlying emotion regulation. Monographs of the Society for Research in Child Development, 59, 152166.CrossRefGoogle ScholarPubMed
Garcia, R. L., Kenny, D. A., & Ledermann, T. (2015). Moderation in the actor–partner interdependence model. Personal Relationships, 22, 829.CrossRefGoogle Scholar
Goldsmith, H. H., & Campos, J. J.. (1982). Toward a theory of infant temperament. In Emde, R.N., & Harmon, R.J. (Eds.), The development of attachment and affiliative systems (pp. 161193). Boston, MA: Springer.CrossRefGoogle Scholar
Granat, A., Gadassi, R., Gilboa-Schechtman, E., & Feldman, R. (2016). Maternal depression and anxiety, social synchrony, and infant regulation of negative and positive emotions. Emotion, 17, 1127.CrossRefGoogle ScholarPubMed
Harmon-Jones, E., & Gable, P. A. (2017). On the role of asymmetric frontal cortical activity in approach and withdrawal motivation: An updated review of the evidence. Psychophysiology, 1, 123.Google Scholar
Hendrix, C. L., Stowe, Z. N., Newport, D. J., & Brennan, P. A. (2018). Physiological attunement in mother–infant dyads at clinical high risk: The influence of maternal depression and positive parenting. Development and Psychopathology, 30, 623634.CrossRefGoogle ScholarPubMed
Hibel, L. C., Granger, D. A., Blair, C., & Cox, M. J. (2009). Intimate partner violence moderates the association between mother-infant adrenocortical activity across an emotional challenge. Journal of Family Psychology, 23, 615625.CrossRefGoogle ScholarPubMed
Hibel, L. C., Granger, D. A., Blair, C., & Finegood, E. D. (2015). Maternal–child adrenocortical attunement in early childhood: Continuity and change. Developmental Psychobiology, 57, 8395.CrossRefGoogle ScholarPubMed
Jones, N. A., Field, T., Fox, N. A., Davalos, M., Malphurs, J., Carraway, K., Schanberg, S., et al. (1997). Infants of intrusive and withdrawn mothers. Infant Behavior and Development, 20, 175186.CrossRefGoogle Scholar
Killeen, L. A., & Teti, D. M. (2012). Mothers’ frontal EEG asymmetry in response to infant emotion states and mother-infant emotional availability, emotional experience, and internalizing symptoms. Development and Psychopathology, 24, 921.CrossRefGoogle ScholarPubMed
Kim, P., Strathearn, L., & Swain, J. E. (2016). The maternal brain and its plasticity in humans. Hormones and Behavior, 77, 113123.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, 521538.CrossRefGoogle ScholarPubMed
Leong, V., Byrne, E., Clackson, K., Georgieva, S., Lam, S., & Wass, S. (2017). Speaker gaze increases information coupling between infant and adult brains. Proceedings of the National Academy of Sciences of the United States of America, 114, 1329013295.CrossRefGoogle ScholarPubMed
Lusby, C. M., Goodman, S. H., Bell, M. A., & Newport, D. J. (2014). Electroencephalogram patterns in infants of depressed mothers. Developmental Psychobiology, 56, 459473.CrossRefGoogle ScholarPubMed
Miskovic, V., Campbell, M. J., Santesso, D. L., Van Ameringen, M., Mancini, C. L., & Schmidt, L. A. (2011). Frontal brain oscillatory coupling in children of parents with social phobia: A pilot study. Journal of Neuropsychiatry and Clinical Neurosciences, 23, 111114.CrossRefGoogle ScholarPubMed
Miskovic, V., & Schmidt, L. A. (2012). Social fearfulness in the human brain. Neuroscience and Biobehavioral Reviews, 36, 459478.CrossRefGoogle ScholarPubMed
Nofech-Mozes, J. A., Jamieson, B., Gonzalez, A., & Atkinson, L. (2018). Mother-infant cortisol attunement: Associations with mother–infant attachment disorganization. Development and Psychopathology, 32, 4355.CrossRefGoogle Scholar
Ostlund, B. D., Measelle, J. R., Laurent, H. K., Conradt, E., & Ablow, J. C. (2017). Shaping emotion regulation: attunement, symptomatology, and stress recovery within mother–infant dyads. Developmental Psychobiology, 59, 1525.CrossRefGoogle ScholarPubMed
Perry, N. B., Dollar, J. M., Calkins, S. D., & Bell, M. A. (2018). Developmental cascade and transactional associations among biological and behavioral indicators of temperament and maternal behavior. Child Development, 89, 17351751.CrossRefGoogle ScholarPubMed
Pesonen, A. K., Raiikkonen, K., Heinonen, K., Komsi, N., Jarvenpaa, A. L., & Strandberg, T. (2008). A transactional model of temperamental development: Evidence of a relationship between child temperament and maternal stress over five years. Social Development, 17, 326340.CrossRefGoogle Scholar
Reznik, S. J., & Allen, J. J. B. (2018). Frontal asymmetry as a mediator and moderator of emotion: An updated review. Psychophysiology, 55, 132.CrossRefGoogle Scholar
Sameroff, A. (2009). The transactional model. In Sameroff, A. (Ed.), The transactional model of development: How children and contexts shape each other (pp. 321). Washington, DC: American Psychological Association.CrossRefGoogle Scholar
Schmidt, L. A. (1999). Frontal brain electrical activity in shyness and sociability. Psychological Science, 10, 316320.CrossRefGoogle Scholar
Schmidt, L. A., & Fox, N. A. (1995). Individual differences in young adults shyness and sociability: Personality and health correlates. Personality and Individual Differences, 19, 455462.CrossRefGoogle Scholar
Schmidt, L. A., & Trainor, L. J. (2001). Frontal brain electrical activity (EEG) distinguishes valence and intensity of musical emotions. Cognition and Emotion, 15, 487500.CrossRefGoogle Scholar
Schmidt, L. A., Trainor, L. J., & Santesso, D. L. (2003). Development of frontal electroencephalogram (EEG) and heart rate (ECG) responses to affective musical stimuli during the first 12 months of post-natal life. Brain and Cognition, 52, 2732.CrossRefGoogle ScholarPubMed
Sethre-Hofsead, L., Stansbury, K., & Rice, M. A. (2002). Attunement of mother and child adrenocortical response to child challenge. Psychoneuroendocrinology, 27, 731747.CrossRefGoogle Scholar
Smith, C. L., Diaz, A., Day, K. L., & Bell, M. A. (2016). Infant frontal electroencephalogram asymmetry and negative emotional reactivity as predictors of toddlerhood effortful control. Journal of Experimental Child Psychology, 142, 262273.CrossRefGoogle ScholarPubMed
Statistics Canada. (2001). Census Topic-based tabulations Catalogue no. 95F0436XCB2001009. Retrieved April 14, 2019, from https://www12.statcan.gc.ca/english/census01/home/Index.cfmGoogle Scholar
Stein, A., Craske, M. G., Lehtonen, A., Harvey, A., Savage-McGlynn, E., Davies, B., Goodwin, J., et al. (2012). Maternal cognitions and mother-infant interaction in postnatal depression and generalized anxiety disorder. Journal of Abnormal Psychology, 121, 795809.CrossRefGoogle ScholarPubMed
Sutton, S. K., & Davidson, R. J. (1997). Prefrontal brain asymmetry: A biological substrate of the behavioral approach and inhibition systems. Psychological Science, 8, 204210.CrossRefGoogle Scholar
Theall-Honey, L. A., & Schmidt, L. A. (2006). Do temperamentally shy children process emotion differently than nonshy children? Behavioral, psychophysiological, and gender differences in reticent preschoolers. Developmental Psychobiology, 1, 187196.CrossRefGoogle Scholar
Thorson, K. R., West, T. V., & Mendes, W. B. (2017). Measuring physiological influence in dyads: A guide to designing, implementing, and analyzing dyadic physiological studies. Psychological Methods, 23, 595616.CrossRefGoogle ScholarPubMed
Tronick, E., & Beeghly, M. (2011). Infants’ meaning-making and the development of mental health problems. American Psychologist, 66, 107119.CrossRefGoogle ScholarPubMed
Tronick, E., & Reck, C. (2009). Infants of depressed mothers. Harvard Review of Psychiatry, 17, 147156.CrossRefGoogle ScholarPubMed
Wang, H., Mai, X., Han, Z. R., Hu, Y., & Lei, X. (2018). Linkage between parent–child frontal resting electroencephalogram (EEG) asymmetry: The moderating role of emotional parenting. Journal of Child and Family Studies, 27, 29902998.CrossRefGoogle Scholar
Wass, S. V. (2018). How orchids concentrate? The relationship between physiological stress reactivity and cognitive performance during infancy and early childhood. Neuroscience and Biobehavioral Reviews, 90, 3449.CrossRefGoogle ScholarPubMed
Waters, S. F., West, T. V., Karnilowicz, H. R., & Mendes, W. B. (2017). Affect contagion between mothers and infants: Examining valence and touch. Journal of Experimental Psychology: General, 146, 10431051.CrossRefGoogle Scholar
Waters, S. F., West, T. V., & Mendes, W. B. (2014). Stress contagion: Physiological covariation between mothers and infants. Psychological Science, 25, 934942.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Krzeczkowski et al. supplementary material

Krzeczkowski et al. supplementary material 1

Download Krzeczkowski et al. supplementary material(Image)
Image 79.1 KB
Supplementary material: File

Krzeczkowski et al. supplementary material

Krzeczkowski et al. supplementary material 2

Download Krzeczkowski et al. supplementary material(File)
File 31.2 KB
Supplementary material: Image

Krzeczkowski et al. supplementary material

Krzeczkowski et al. supplementary material 3

Download Krzeczkowski et al. supplementary material(Image)
Image 125.6 KB