Hostname: page-component-7c8c6479df-995ml Total loading time: 0 Render date: 2024-03-28T11:36:45.090Z Has data issue: false hasContentIssue false

Trajectories of internalizing symptoms across childhood: The roles of biological self-regulation and maternal psychopathology

Published online by Cambridge University Press:  25 November 2014

Lilly Shanahan*
Affiliation:
University of North Carolina at Chapel Hill
Susan D. Calkins
Affiliation:
University of North Carolina at Greensboro
Susan P. Keane
Affiliation:
University of North Carolina at Greensboro
Rachael Kelleher
Affiliation:
University of North Carolina at Greensboro
Rebecca Suffness
Affiliation:
University of North Carolina at Greensboro
*
Address correspondence and reprint requests to: Lilly Shanahan, Department of Psychology, University of North Carolina at Chapel Hill, CB 3270, Davie Hall, Chapel Hill, NC 27599-3270; E-mail: lilly_shanahan@unc.edu.

Abstract

Whether internalizing symptoms increase or remain at similar levels throughout childhood is currently not well understood. Moreover, the association between vagal regulation of cardiac activity and internalizing symptoms across childhood needs to be clarified. We used a multilevel conceptual framework to examine how children's vagal regulation of cardiac activity and mothers' internalizing symptoms were jointly associated with children's developmental trajectories of internalizing symptoms from ages 4 to 10 years old. Data came from 384 children who participated in an ongoing longitudinal study. Children and their mothers came to the research laboratory at ages 4, 5, 7, and 10. Mothers reported their children's and their own internalizing symptoms. Children's vagal regulation of cardiac activity was assessed during quiet baseline tasks and during challenge tasks. Multilevel models revealed that child internalizing symptoms increased from ages 4 to 10 years old, but only in females, and especially between ages 7 and 10. More vagal withdrawal in response to challenge was associated with more internalizing symptoms, particularly with more somatic symptoms. Associations between children's physiological regulation and internalizing symptoms differed by children's age, sex, and presence of maternal internalizing symptoms. Understanding associations between vagal regulation of cardiac activity and internalizing symptoms during childhood calls for fine-grained developmental analyses that take into account the heterogeneity of internalizing symptoms, as well as developmental phase, context, and gender.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2014 

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

Achenbach, T. M. (1992). Manual for the Child Behavior Checklist/2–3. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Achenbach, T. M., & Edelbrock, C. S. (1983). Manual for the Child Behavior Checklist and Child Behavior Profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Angold, A., Costello, E. J., & Worthman, C. M. (1998). Puberty and depression: The roles of age, pubertal status, and pubertal timing. Psychological Medicine, 28, 5161.CrossRefGoogle ScholarPubMed
Angold, A., Erkanli, A., Silberg, J., Eaves, L., & Costello, E. J. (2002). Depression scale scores in 8- to 17-year-olds: Effects of age and gender. Journal of Child Psychology and Psychiatry, 43, 10521063.CrossRefGoogle Scholar
Angold, A., & Worthman, C. W. (1993). Puberty onset of gender differences in rates of depression: A developmental, epidemiologic and neuroendocrine perspective. Journal of Affective Disorders, 29, 145158.Google Scholar
Antonijevic, I. A. (2006). Depressive disorders—Is it time to endorse different pathophysiologies. Psychoneuroendocrinology, 31, 115.Google Scholar
Bauer, D. J. (2007). Observations on the use of growth mixture models in psychological research. Multivariate Behavioral Research, 42, 757786.Google Scholar
Bauer, D. J., & Curran, P. J. (2003). Distributional assumptions of growth mixture models: Implications for over-extraction of latent trajectory classes. Psychological Methods, 8, 338363.CrossRefGoogle Scholar
Beauchaine, T. (2001). Vagal tone, development, and Gray's motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13, 183214.Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908.CrossRefGoogle ScholarPubMed
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, 5465.CrossRefGoogle ScholarPubMed
Bosch, N. M., Riese, H., Dietrich, A., Ormel, J., Verhulst, F. C., & Oldehinkel, A. J. (2009). Preadolescents' somatic and cognitive–affective depressive symptoms are differentially related to cardiac autonomic function and cortisol: The TRAILS study. Psychological Medicine, 71, 944950. doi:10.1097/PSY.0b013e3181bc756b Google Scholar
Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., Kupfer, D. J., et al. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144150.CrossRefGoogle ScholarPubMed
Bronfenbrenner, U. (1979). The ecology of human development: Experiment by nature and design. Cambridge, MA: Harvard University Press.Google Scholar
Bryk, A. S., & Raudenbush, S. W. (1987). Application of hierarchical linear models to assessing change. Psychological Bulletin, 101, 147158.Google Scholar
Bryk, A. S., & Raudenbush, S. W. (1992). Hierarchical linear models: Applications and data analysis methods (Vol. 1). Newbury Park, CA: Sage.Google Scholar
Burt, K. B., & Obradović, J. (2013). The construct of psychophysiological reactivity: Statistical and psychometric issues. Developmental Review, 33, 2957.Google Scholar
Cairns, R. B., & Cairns, B. D. (1994). Lost and found: I. Recovery of subjects in longitudinal research. In Cairns, R. B. & Cairns, B. D. (Eds.), Lifelines and risks: Pathways of youth in our time (1st ed.). New York: Cambridge University Press.Google Scholar
Cairns, R. B., Elder, G. H. J., & Costello, E. J. (1996). The making of developmental science. In Cairns, R. B., Elder, G. H. J., & Costello, E. J. (Eds.), Developmental science (Vol. 20, pp. 223234). New York: Cambridge University Press.Google Scholar
Calkins, S. D., Blandon, A. Y., Williford, A. P., & Keane, S. P. (2007). Biological, behavioral, and relational levels of resilience in the context of risk for early childhood behavior problems. Development and Psychopathology, 19, 675700.Google Scholar
Calkins, S. D., Dedmon, S. E., Gill, K. L., Lomax, L. E., & Johnson, L. M. (2002). Frustration in infancy: Implications for emotion regulation, physiological processes, and temperament. Infancy, 3, 175197. doi:10.1207/S15327078IN0302_4 CrossRefGoogle ScholarPubMed
Calkins, S. D., & Fox, N. A. (2002). Self-regulatory processes in early personality development: A multilevel approach to the study of childhood social withdrawal and aggression. Development and Psychopathology, 14, 477498.Google Scholar
Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74, 144153.Google Scholar
Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45, 101112.Google Scholar
Christie, K. A., Burke, J. D., Regier, D. A., Rae, D. S., Boyd, J. H., & Locke, B. Z. (1988). Epidemiologic evidence for early onset of mental disorders and higher risk of drug abuse in young adults. American Journal of Psychiatry, 145, 971975.Google ScholarPubMed
Cicchetti, D. (2008). A multiple-levels-of-analysis perspective on research in development and psychopathology. In Beauchaine, T. & Hinshaw, S. (Eds.), Child and adolescent psychopathology (pp. 2757). Hoboken, NJ: Wiley.Google Scholar
Cicchetti, D., & Blender, J. A. (2006). A multiple-levels-of-analysis perspective on resilience: Implications for the developing brain, neural plasticity, and preventive interventions. Annals of the New York Academy of Sciences, 1094, 248258.Google Scholar
Cicchetti, D., & Dawson, G. (2002). Multiple levels of analysis. Development and Psychopathology, 14, 417420.Google Scholar
Cicchetti, D., & Rogosch, F. A. (1999). Psychopathology as risk for adolescent substance use disorders: A developmental psychopathology perspective. Journal of Clinical Child Psychology, 28, 355365.Google Scholar
Colder, C., Mott, J., & Berman, A. (2002). The interactive effects of infant activity level and fear on growth trajectories of early childhood behavior problems. Development and Psychopathology, 14, 123.CrossRefGoogle ScholarPubMed
Collins, P. Y., Patel, V., Joestl, S. S., March, D., Insel, T. R., Daar, A. S., et al. (2011). Grand challenges in global mental health. Nature, 475, 2730.Google Scholar
Costello, E. J., Worthman, C., Erkanli, A., & Angold, A. (2007). Prediction from low birthweight to female adolescent depression: A test of competing hypotheses. Archives of General Psychiatry, 64, 338344.Google Scholar
Crowell, S. E., Beauchaine, T. P., McCauley, E., Smith, C. J., Stevens, A. L., & Sylvers, P. (2005). Psychological, autonomic, and serotonergic correlates of parasuicide among adolescent girls. Development and Psychopathology, 17, 11051127.Google Scholar
Curran, P. J., & Bauer, D. J. (2011). The disaggregation of within-person and between-person effects in longitudinal models of change. Annual Review of Psychology, 62, 583619.Google Scholar
Dantzer, R., Konsman, J. P., Bluthé, R. M., & Kelley, K. W. (2000). Neural and humoral pathways of communication from the immune system to the brain: Parallel or convergent? Autonomic Neuroscience, 85, 6065.Google Scholar
Deković, M., Buist, K. L., & Reitz, E. (2004). Stability and changes in problem behavior during adolescence: Latent growth analysis. Journal of Youth and Adolescence, 33, 112.Google Scholar
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 15621592. doi:10.1016/j.neubiorev.2010.11.007 Google Scholar
Derogatis, L. R. (1986). Manual for the Symptom Checklist 90—Revised (SCL-90R). Baltimore, MD: Author.Google Scholar
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, 230242.Google Scholar
Egger, H. L., & Angold, A. (2006). Common emotional and behavioral disorders in preschool children: Presentation, nosology, and epidemiology. Journal of Child Psychiatry and Psychology, 47, 313337.Google Scholar
Ellis, B., & Boyce, W. T. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271301.Google Scholar
Essex, M. J., Armstrong, J. M., Burk, L. R., Goldsmith, H. H., & Boyce, W. T. (2011). Biological sensitivity to context moderates the effects of the early teacher–child relationship on the development of mental health by adolescence. Development and Psychopathology, 23, 149161.Google Scholar
Fortunato, C. K., Gatzke-Kopp, L. M., & Ram, N. (2013). Associations between respiratory sinus arrhythmia reactivity and internalizing and externalizing symptoms are emotion specific. Cognitive, Affective, & Behavioral Neuroscience, 13, 238251.Google Scholar
Friedman, B. H. (2007). An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology, 74, 185199.Google Scholar
Galambos, N. L., Barker, E. T., & Almeida, D. M. (2003). Parents do matter: Trajectories of change in externalizing and internalizing problems in early adolescence. Child Development, 74, 578594.Google Scholar
Gazelle, H., & Druhen, M. J. (2009). Anxious solitude and peer exclusion predict social helplessness, upset affect, and vagal regulation in response to behavioral rejection by a friend. Developmental Psychology, 45, 10771096. doi:10.1037/a0016165 Google Scholar
Gazelle, H., & Ladd, G. W. (2003). Anxious solitude and peer exclusion: A diathesis–stress model of internalizing trajectories in childhood. Child Development, 74, 257278.CrossRefGoogle ScholarPubMed
Ge, X., Conger, R., & Elder, G. (2001). Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms. Developmental Psychology, 37, 404417.Google Scholar
Ge, X., Natsuaki, M. N., & Conger, R. D. (2006). Trajectories of depressive symptoms and stressful life events among male and female adolescents in divorced and nondivorced families. Development and Psychopathology, 18, 253273.CrossRefGoogle ScholarPubMed
Gentzler, A. L., Santucci, A. K., Kovacs, M., & Fox, N. A. (2009). Respiratory sinus arrhythmia reactivity predicts emotion regulation and depressive symptoms in at-risk and control children. Biological Psychology, 82, 156163. doi:10.1016/j.biopsycho.2009.07.002 Google Scholar
Goodman, S. H., & Gotlib, I. H. (1999). Risk for psychopathology in the children of depressed mothers: A developmental model for understanding mechanisms of transmission. Psychological Review, 106, 485490.CrossRefGoogle ScholarPubMed
Graziano, P., & Derefinko, K. (2013). Cardiac vagal control and children's adaptive functioning: A meta-analysis. Biological Psychology, 94, 2237.CrossRefGoogle ScholarPubMed
Herman-Giddens, M. E. (2006). Recent data on pubertal milestones in United States children: The secular trend toward earlier development. International Journal of Andrology, 29, 241246.Google Scholar
Herman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., et al. (1997). Secondary sexual characteristics and menses in young girls seen in office practice: A study from the Pediatric Research in Office Settings Network. Pediatrics, 99, 505512.Google Scholar
Hinnant, J. B., & El-Sheikh, M. (2009). Children's externalizing and internalizing symptoms over time: The role of individual differences in patterns of RSA responding. Journal of Abnormal Child Psychology, 37, 10491061. doi:10.1007/s10802-009-9341-1 Google Scholar
Hipp, J. R., & Bauer, D. J. (2006). Local solutions in the estimation of growth mixture model. Psychological Methods, 11, 3653.Google Scholar
Hoffman, L., & Stawski, R. S. (2009). Persons as contexts: Evaluating between-person and within-person effects in longitudinal analysis. Research in Human Development, 6, 97120.CrossRefGoogle Scholar
Hollingshead, A. B. (1975). Four Factor Index of Social Status. Unpublished manuscript, Yale University.Google Scholar
Kasch, K. L., & Klein, D. N. (1996). The relationship between age at onset and comorbidity in psychiatric disorders. Journal of Nervous and Mental Disease, 184, 703707.Google Scholar
Keenan, K., Shaw, D. S., Walsh, B., Delliquadri, E., & Giovannelli, J. (1997). DSM-III-R disorders in preschool children from low-income families. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 620627.CrossRefGoogle ScholarPubMed
Kok, B. E., & Fredrickson, B. L. (2010). Upward spirals of the heart: Autonomic flexibility, as indexed by vagal tone, reciprocally and prospectively predicts positive emotions and social connectedness. Biological Psychology, 85, 432436.Google Scholar
Konsman, J. P., Parnet, P., & Dantzer, R. (2002). Cytokine-induced sickness behaviour: Mechanisms and implications. Trends in Neuroscience, 25, 154159.CrossRefGoogle ScholarPubMed
Kovacs, M. (1996). Presentation and course of major depressive disorder during childhood and later years of the life span. Journal of the American Academy of Child & Adolescent Psychiatry, 35, 705715.Google Scholar
Kovacs, M., & Paulauskas, S. L. (1984). Developmental stage and the expression of depressive disorders in children: An empirical analysis. In Cicchetti, D. & Schneider-Rosen, K. (Eds.), Childhood depression (pp. 5980). San Francisco, CA: New Directions for Child Development.Google Scholar
Kuo, M., Mohler, B., Raudenbush, S. L., & Earls, F. J. (2000). Assessing exposure to violence using multiple informants: Application of hierarchical linear model. Journal of Child Psychology and Psychiatry, 41, 10491056.Google Scholar
Laird, N. M., & Ware, J. H. (1982). Random-effects models for longitudinal data. Biometrics, 38, 963974.Google Scholar
Little, R., & Rubin, D. (1987). Statistical analysis with missing data. New York: Wiley.Google Scholar
Lovejoy, M. C., Graczyk, P. A., O'Hare, E., & Neuman, G. (2000). Maternal depression and parenting behavior: A meta-analytic review. Clinical Psychology Review, 20, 561592.CrossRefGoogle ScholarPubMed
Magnusson, D. (1999a). Holistic interactionism: A perspective for research on personality development. In Pervin, L. A. & John, O. P. (Eds.), Handbood of personality: Theory and research (2nd ed., pp. 219247). New York: Guilford Press.Google Scholar
Magnusson, D. (1999b). On the individual: A person-oriented approach to developmental research. European Psychologist, 4, 205218.Google Scholar
Marsland, A. L., Gianaros, P. J., Prather, A. A., Jennings, J. R., Neumann, S. A., & Manuck, S. B. (2007). Stimulated production of proinflammatory cytokines covaries inversely with heart rate variability. Psychosomatic Medicine, 69, 709716.Google Scholar
Nezlek, J. B. (2007). A multilevel framework for understanding relationships among traits, states, situations and behaviors. European Journal of Personality, 21, 789810.Google Scholar
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, 371387.CrossRefGoogle Scholar
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, 270289.CrossRefGoogle ScholarPubMed
Pavlov, V. A., & Tracey, K. J. (2004). Neural regulators of innate immune responses and inflammation. Cellular and Molecular Life Sciences, 61, 23222331.Google Scholar
Perry, N. B., Nelson, J. A., Swingler, M. M., Leerkes, E. M., Calkins, S. D., Marcovitch, S., et al. (2013). The relation between maternal emotional support and child physiological regulation across the preschool years. Developmental Psychobiology, 55, 382394.CrossRefGoogle ScholarPubMed
Porges, S. W. (2003). The polyvagal theory: Phylogenetic contributions to social behavior. Physiology & Behavior, 79, 503513.Google Scholar
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116143.Google Scholar
Porges, S. W., Doussard-Roosevelt, J. A., Portales, A. L., & Greenspan, S. I. (1996). Infant regulation of the vagal “brake” predicts child behavior problems: A psychobiological model of social behavior. Developmental Psychobiology, 29, 697712.Google Scholar
Porges, S. W., & Furman, S. A. (2011). The early development of the autonomic nervous system provides a neural platform for social behavior: A polyvagal perspective. Infant and Child Development, 20, 106118.Google Scholar
Raison, C. L., Capuron, L., & Miller, A. H. (2006). Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends in Immunology, 27, 2431.Google Scholar
Richters, J. E. (1997). The Hubble hypothesis and the developmentalist's dilemma. Development and Psychopathology, 9, 193229.Google Scholar
Rottenberg, J., Chambers, A. S., Allen, J. J., & Manber, R. (2007). Cardiac vagal control in the severity and course of depression: The importance of symptomatic heterogeneity. Journal of Affective Disorders, 103, 173179.Google Scholar
SAS Institute Inc. (2008). SAS/STAT® Software: Version 9.2 (Computer software). Cary, NC: Author.Google Scholar
Schafer, J. L. (1997). Analysis of incomplete multivariate data. London: Chapman & Hall.Google Scholar
Schmidt, L., Fox, N., Schulkin, J., & Gold, P. W. (1999). Behavioral and psychophysiological correlates of self-presentation in tempermentally shy children. Developmental Psychobiology, 35, 119135.3.0.CO;2-G>CrossRefGoogle Scholar
Shanahan, L., Copeland, W. E., Angold, A., & Costello, E. J. (2011). Child-, adolescent-, and young adult-onset depressions: Differential risk factors in development? Psychological Medicine, 41, 22652274.Google Scholar
Shelby, G. D., Shirkey, K. C., Sherman, A. L., Beck, J. E., Haman, K., Shears, A. R., et al. (2013). Functional abdominal pain in childhood and long-term vulnerability to anxiety disorders. Pediatrics, 132, 475482. doi:10.1542/peds.2012-2191 Google Scholar
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17, 167184.CrossRefGoogle ScholarPubMed
Shonkoff, J. P., & Garner, A. S. (2012). The lifelong effects of early childhood adversity and toxic stress. Pediatrics, 129, e232e246.CrossRefGoogle ScholarPubMed
Sroufe, L. A., & Rutter, M. (1984). The domain of developmental psychopathology. Child Development, 55, 1729.Google Scholar
Sterba, S. K., & Bauer, D. J. (2010). Matching method with theory in person-oriented developmental psychopathology research. Development and Psychopathology, 22, 239254. doi:10.1017/S0954579410000015 Google Scholar
Sterba, S. K., Prinstein, M. J., & Cox, M. J. (2007). Trajectories of internalizing problems across childhood: Heterogeneity, external validity, and gender differences. Development and Psychopathology, 19, 345366.Google Scholar
Stoddard, J., Stringaris, A., Brotman, M. A., Montville, D., Pine, D. S., & Leibenluft, E. (2013). Irritability in child and adolescent anxiety disorders. Depression and Anxiety. Advance online publication. doi:10.1002/da.22151 Google Scholar
Stringaris, A. (2011). Irritability in children and adolescents: A challenge for DSM-5. European Child and Adolescent Psychiatry, 20, 6166. doi:10.1007/s00787-010-0150-4 Google Scholar
Stringaris, A., Zavos, H., Leibenluft, E., Maughan, B., & Eley, T. C. (2012). Adolescent irritability: Phenotypic associations and genetic links with depressed mood. American Journal of Psychiatry, 169, 4754. doi:10.1176/appi.ajp.2011.10101549 Google Scholar
Thayer, J. F., & Sternberg, E. M. (2006). Beyond heart rate variability: Vagal regulation of allostatic systems. Annals of the New York Academy of Sciences, 1088, 361372.CrossRefGoogle ScholarPubMed
Thayer, J. F., & Sternberg, E. M. (2010). Neural aspects of immunomodulation: Focus on the vagus nerve. Brain, Behavior, and Immunity, 24, 12231228.Google Scholar
Twenge, J. M., & Nolen-Hoeksema, S. K. (2002). Age, gender, race, SES, and birth cohort differences on the Children's Depression Inventory. Journal of Abnormal Psychology, 111, 578588.Google Scholar
Wood, J. J., McLeod, B. D., Sigman, M., Hwang, W.-C., & Chu, B. C. (2003). Parenting and childhood anxiety: Theory, empirical findings, and future directions. Journal of Child Psychology and Psychiatry, 44, 134151.Google Scholar
Zahn-Waxler, C., Klimes-Dougan, B., & Slattery, M. J. (2000). Internalizing problems of childhood and adolescence: Prospects, pitfalls, and progress in understanding the development of anxiety and depression. Development and Psychopathology, 12, 443466.Google Scholar