Abstract
Understanding whether and how the absence of positive relationships may predict longer-term physical health outcomes is central to building a working conceptual model of the interplay of social and physical development across the lifespan. This study sought to examine the extent to which difficulties establishing positive social relationships from adolescence onward serve as long-term predictors of low adult vagal tone, which in turn has been linked to numerous long-term health problems. A diverse community sample of 141 individuals was followed via multiple methods and reporters from age 13 to 29. Across this span, social relationship quality was assessed via close friend and peer reports, observations of romantic interactions, and self-reported romantic relationship satisfaction. A range of potential personality and functional covariates was also considered. Vagal tone while at rest was assessed at age 29. Adult vagal tone was predicted across periods as long as 16 years by: adolescents’ difficulty establishing themselves as desirable companions among peers; early adults’ inability to establish strong close friendships; and lack of warmth in romantic relationships as an adult. Poor early adult friendship quality statistically mediated the link from adolescent peer difficulties to adult vagal tone. A range of potential confounding factors was examined but was not linked to vagal tone. Within the limits of the correlational design of the study, robust connections between adult vagal tone and social relationship quality from adolescence onward suggest at least a possible mechanism by which relationship difficulties may get ‘under the skin’ to influence future physiological functioning.

Similar content being viewed by others
References
Achenbach, T. M., & Edelbrock, C. S. (1991). Manual for the child behavior checklist/4-18 and 1991 profile. University of Vermont Department of Psychiatry
Albert, D., Chein, J., & Steinberg, L. (2013). The teenage brain peer influences on adolescent decision making. Current Directions in Psychological Science, 22, 114–120
Allen, J. P., Porter, M. R., McFarland, C. F., Marsh, P. A., & McElhaney, K. B. (2005a). The two faces of adolescents’ success with peers: Adolescent popularity, social adaptation, and deviant behavior. Child Development, 76, 747–760
Allen, J. P., Porter, M. R., McFarland, F. C., Hare, A., Miga, E., & Schad, M. (2005b). Autonomy and relatedness coding manual for adolescent-romantic partner dyads. University of Virginia
Allen, J. P., Porter, M. R., McFarland, F. C., McElhaney, K. B., & Marsh, P. A. (2007). The relation of attachment security to adolescents’ paternal and peer relationships, depression, and externalizing behavior. Child Development, 78, 1222–1239
Allen, J. P., Uchino, B. N., & Hafen, C. A. (2015). Running with the pack: Teen peer-relationship qualities as predictors of adult physical health. Psychological Science, 26, 1574–1583
Allen, J. P., Loeb, E. L., Tan, J. S., Narr, R. K., & Uchino, B. N. (2017). The body remembers: Adolescent conflict struggles predict adult interleukin-6 levels. Development and Psychopathology (Online Version)
Allen, J. P., Narr, R. K., Kansky, J., & Szwedo, D. E. (2020). Adolescent peer relationship qualities as predictors of long-term romantic life satisfaction. Child Development, 91, 327–340
Allen, J. P., Narr, R. K., Nagel, A. G., Costello, M. A., & Guskin, K. (2021). The connection project: Changing the peer environment to improve outcomes for marginalized adolescents. Development & Psychopathology, 33, 647–657
Arbuckle, J. L. (1996). Full information estimation in the presence of incomplete data. In G. A. M. R. E. Schumaker (Ed.), Advanced structural modeling: Issues and Techniques (pp. 243–277). Erlbaum
Bagwell, C. L., Schmidt, M. E., Newcomb, A. F., & Bukowski, W. M. (2001). Friendship and peer rejection as predictors of adult adjustment. In D. W. Nangle & C. A. Erdley (Eds.), New directions in child development: The role of friendship in psychological adjustment (pp. 25–49). Jossey-Bass.
Beauchaine, T. P., & Thayer, J. F. (2015). Heart rate variability as a transdiagnostic biomarker of psychopathology. International Journal of Psychophysiology., 98, 338–350.
Ben-Shlomo, Y., & Kuh, D. (2002). A life course approach to chronic disease epidemiology: Conceptual models, empirical challenges and interdisciplinary perspectives. International Journal of Epidemiology, 31, 285–293.
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993). Cardiac psychophysiology and autonomic space in humans: Empirical perspectives and conceptual implications. Psychological Bulletin, 114, 296.
Berntson, G. G., Thomas Bigger Jr, J., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., Nagaraja, H. N., Porges, S. W., Saul, J. P., Stone, P. H., & Van Der Molen, M. W. (1997). Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology, 34, 623–648
Binkley, P. F., Nunziata, E., Haas, G. J., Nelson, S. D., & Cody, R. J. (1991). Parasympathetic withdrawal is an integral component of autonomic imbalance in congestive heart failure: Demonstration in human subjects and verification in a paced canine model of ventricular failure. Journal of the American College of Cardiology, 18, 464–472.
Blakemore, S.-J., & Mills, K. L. (2014). Is adolescence a sensitive period for sociocultural processing? Annual Review of Psychology, 65, 187–207.
Bowlby, J. (1969/1982). Attachment and loss (Vol. 1). Basic Books
Bowlby, J. (1980) Attachment and loss: Vol. 3: Loss, sadness and depression. Basic Books
Braune, H.-J., & Geisendörfer, U. (1995). Measurement of heart rate variations: Influencing factors, normal values and diagnostic impact on diabetic autonomic neuropathy. Diabetes Research and Clinical Practice, 29, 179–187.
Brosschot, J. F., Verkuil, B., & Thayer, J. F. (2016). The default response to uncertainty and the importance of perceived safety in anxiety and stress: An evolution-theoretical perspective. Journal of Anxiety Disorders, 41, 22–34.
Brosschot, J. F., Verkuil, B., & Thayer, J. F. (2017). Exposed to events that never happen: Generalized unsafety, the default stress response, and prolonged autonomic activity. Neuroscience & Biobehavioral Reviews, 74, 287–296.
Bukowski, W. M., Hoza, B., & Boivin, M. (1993). Popularity, friendship, and emotional adjustment during early adolescence. New Directions for Child and Adolescent Development, 1993, 23–37.
Cacioppo, J. T., Malarkey, W. B., Kiecolt-Glaser, J. K., Uchino, B. N., Sgoutas-Emch, S. A., Sheridan, J. F., Berntson, G. G., & Glaser, R. (1995). Heterogeneity in neuroendocrine and immune responses to brief psychologicalstressors as a function of autonomic cardiac activation. Psychosomatic Medicine, 57, 154–164.
Centers for Disease Control and Prevention. (2017). Four domains of chronic disease prevention. Author.
Charles, S. T., Reynolds, C. A., & Gatz, M. (2001). Age-related differences and change in positive and negative affect over 23 years. Journal of Personality and Social Psychology, 80, 136.
Christensen, J. H., Toft, E., Christensen, M. S., & Schmidt, E. B. (1999). Heart rate variability and plasma lipids in men with and without ischaemic heart disease. Atherosclerosis, 145, 181–186.
Cicchetti, D. V., & Sparrow, S. A. (1981). Developing criteria for establishing interrater reliability of specific items: Applications to assessment of adaptive behavior. American Journal of Mental Deficiency, 86, 127–137.
Coan, J. A., & Sbarra, D. A. (2015). Social baseline theory: The social regulation of risk and effort. Current Opinion in Psychology, 1, 87–91.
Coie, J. D., Dodge, K. A., & Coppotelli, H. (1982). Dimensions and types of social status: A cross age perspective. Developmental Psychology, 18, 121–132.
Donoho, C. J., Seeman, T. E., Sloan, R. P., & Crimmins, E. M. (2015). Marital status, marital quality, and heart rate variability in the MIDUS cohort. Journal of Family Psychology, 29, 290.
Freedman, B. J., Rosenthal, L., Donahoe, C. P., Schlundt, D. G., & McFall, R. M. (1978). A social-behavioral analysis of skill deficits in delinquent and nondelinquent adolescent boys. Journal of Consulting & Clinical Psychology, 46, 1448–1462.
Furman, W., & Buhrmester, D. (1985). Childrens’ perceptions of the personal relationships in their social networks. Developmental Psychology, 21, 1016–1024.
Furman, W., & Collibee, C. (2014). A matter of timing: Developmental theories of romantic involvement and psychosocial adjustment. Development and Psychopathology, 26, 1149–1160.
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., Hare, T. A., Bookheimer, S. Y., & Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience, 33, 4584–4593.
Goff, B., Gee, D. G., Telzer, E. H., Humphreys, K. L., Gabard-Durnam, L., Flannery, J., & Tottenham, N. (2013). Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience, 249, 129–138.
Goldberg, L. R., Johnson, J. A., Eber, H. W., Hogan, R., Ashton, M. C., Cloninger, C. R., & Gough, H. G. (2006). The international personality item pool and the future of public-domain personality measures. Journal of Research in Personality, 40, 84–96.
Goswick, R. A., & Jones, W. H. (1982). Components of loneliness during adolescence. Journal of Youth and Adolescence, 11, 373.
Gouin, J.-P., Zhou, B., & Fitzpatrick, S. (2015). Social integration prospectively predicts changes in heart rate variability among individuals undergoing migration stress. Annals of Behavioral Medicine, 49, 230–238.
Harter, S. (1988). Manual for the self-perception profile for adolescents. University of Denver.
Hayes, A. F. (2019). Introduction to mediation, moderation, and conditional process analysis, second edition: A regression-based approach. ProQuest Ebook Central. http://ebookcentral.proquest.com/lib/uva/detail.action?docID=5109647). Guilford
Hoetink, A. E., Faes, T. J., Schuur, E. H., Gorkink, R., Goovaerts, H. G., Meijer, J. H., & Heethaar, R. M. (2002). Comparing spot electrode arrangements for electric impedance cardiography. Physiological Measurement, 23, 457.
Holt-Lunstad, J., Uchino, B. N., Smith, T. W., & Hicks, A. (2007). On the importance of relationship quality: The impact of ambivalence in friendships on cardiovascular functioning. Annals of Behavioral Medicine, 33, 278–290.
Holt-Lunstad, J., Robles, T. F., & Sbarra, D. A. (2017). Advancing social connection as a public health priority in the United States. American Psychologist, 72, 517–530.
Institute of Medicine. (2012). Accelerating progress in obesity prevention: Solving the weight of the nation. Author.
Johnson, M., Deardorff, J., Davis, E. L., Martinez, W., Eskenazi, B., & Alkon, A. (2017). The relationship between maternal responsivity, socioeconomic status, and resting autonomic nervous system functioning in Mexican American children. International Journal of Psychophysiology, 116, 45–52.
Kazdin, A. E. (1990). Childhood depression. Journal of Child Psychology & Psychiatry & Allied Disciplines, 31, 121–160.
Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (1993). The ‘Trier Social Stress Test’–a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76–81.
Kobak, R. R., & Sceery, A. (1988). Attachment in late adolescence: Working models, affect regulation and representations of self and others. Child Development, 59, 135–146.
Koenig, J., & Thayer, J. F. (2016). Sex differences in healthy human heart rate variability: A meta-analysis. Neuroscience & Biobehavioral Reviews, 64, 288–310.
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, 432–436.
Kovacs, M., & Beck, A. T. (1977). An empirical clinical approach toward a definition of childhood depression. Raven Press.
La Greca, A. M., & Lopez, N. (1998). Social anxiety among adolescents: Linkages with peer relations and friendships. Journal of Abnormal Child Psychology, 26, 83–94.
Litvack, D. A., Oberlander, T. F., Carney, L. H., & Saul, J. P. (1995). Time and frequency domain methods for heart rate variability analysis: A methodological comparison. Psychophysiology, 32, 492–504.
Lizotte, A. J., Chard-Wierschem, D. J., Loeber, R., & Stern, S. B. (1992). A shortened Child Behavior Checklist for delinquency studies. Journal of Quantitative Criminology, 8, 233–245.
Maier, S. F., & Watkins, L. R. (1998). Cytokines for psychologists: Implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychological Review, 105, 83.
McElhaney, K. B., Antonishak, J., & Allen, J. P. (2008). They like me, they like me not: Popularity and adolescents’ perceptions of acceptance predicting changing social functioning over time. Child Development, 79, 720–731.
McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiology Review, 87, 873–904.
Moore, D., & Schultz, N. R. (1983). Loneliness at adolescence: Correlates, attributions, and coping. Journal of Youth and Adolescence, 12, 95.
Narr, R. K., Allen, J. P., Tan, J. S., & Loeb, E. L. (2019). Close friendship strength and broader peer group desirability as differential predictors of adult mental health. Child Development, 90, 298–313.
Oudekerk, B. A., Allen, J. P., Hessel, E. T., & Molloy, L. E. (2015). The cascading development of autonomy and relatedness from adolescence to adulthood. Child Development, 86, 472–485.
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143.
Robles, T. F., Slatcher, R. B., Trombello, J. M., & McGinn, M. M. (2014). Marital quality and health: A meta-analytic review. Psychological Bulletin, 140, 140.
Roisman, G. I., Masten, A. S., Coatsworth, J. D., & Tellegen, A. (2004). Salient and emerging developmental tasks in the transition to adulthood. Child Development, 75, 123–133.
Romeo, R. D. (2010). Adolescence: A central event in shaping stress reactivity. Developmental Psychobiology, 52, 244–253.
Russell, D., Peplau, L. A., & Cutrona, C. E. (1980). The revised UCLA Loneliness Scale: Concurrent and discriminant validity evidence. Journal of Personality and Social Psychology, 39, 472–480.
Sack, M., Hopper, J. W., & Lamprecht, F. (2004). Low respiratory sinus arrhythmia and prolonged psychophysiological arousal in posttraumatic stress disorder: Heart rate dynamics and individual differences in arousal regulation. Biological Psychiatry, 55, 284–290.
Sapolsky, R. M. (2004). Why zebras don't get ulcers: The acclaimed guide to stress, stress-related diseases, and coping-now revised and updated. Macmillan
Schreier, H. M., Schonert-Reichl, K. A., & Chen, E. (2013). Effect of volunteering on risk factors for cardiovascular disease in adolescents: A randomized controlled trial. Journal of the American Medical Association: Pediatrics, 167, 1–6.
Schroeder, E. B., Liao, D., Chambless, L. E., Prineas, R. J., Evans, G. W., & Heiss, G. (2003). Hypertension, blood pressure, and heart rate variability: The atherosclerosis risk in communities (ARIC) study. Hypertension, 42, 1106–1111.
Smith, T. W., Deits-Lebehn, C., Williams, P. G., Baucom, B. R., & Uchino, B. N. (2020). Toward a social psychophysiology of vagally mediated heart rate variability: Concepts and methods in self-regulation, emotion, and interpersonal processes. Social and Personality Psychology Compass, 2020, e12516.
Spielberger, C. D., Sydeman, S. J., Owen, A. E., & Marsh, B. J. (1999). Measuring anxiety and anger with the State-Trait Anxiety Inventory (STAI) and the State-Trait Anger Expression Inventory (STAXI). In M. E. Maruish (Ed.), The use of psychological testing for treatment planning and outcomes assessment (pp. 993–1021). Lawrence Erlbaum Associates Publishers.
Steinberg, L., & Monahan, K. C. (2007). Age differences in resistance to peer influence. Developmental Psychology., 43, 1531–1543.
Thayer, J. F., & Lane, R. D. (2007). The role of vagal function in the risk for cardiovascular disease and mortality. Biological Psychology, 74, 224–242.
Thayer, J. F., Yamamoto, S. S., & Brosschot, J. F. (2010). The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. International Journal of Cardiology, 141, 122–131.
Uchino, B. N. (2009). What a lifespan approach might tell us about why distinct measures of social support have differential links to physical health. Journal of Social and Personal Relationships, 26, 53–62.
Ziegler, D., Laude, D., Akila, F., & Elghozi, J.-L. (2001). Time-and frequency-domain estimation of early diabetic cardiovascular autonomic neuropathy. Clinical Autonomic Research, 11, 369–376
Zimmer-Gembeck, M. J., Nesdale, D., Webb, H. J., Khatibi, M., & Downey, G. (2016). A longitudinal rejection sensitivity model of depression and aggression: Unique roles of anxiety, anger, blame, withdrawal and retribution. Journal of Abnormal Child Psychology, 44, 1291–1307
Acknowledgements
This study was supported by grants from the National Institute of Child Health and Human Development and the National Institute of Mental Health (R37HD058305 & R01-MH58066).
Funding
The funding was provided by Eunice Kennedy Shriver National Institute of Child Health and Human Development (Grant Nos. R37HD058305, R01HD058305), National Institute of Mental Health (Grant No. R01-MH58066).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
Human subject protections were followed along with IRB review.
Informed consent
All participants or their parents provided informed consent.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Allen, J.P., Loeb, E.L., Davis, A.A. et al. Getting under the skin: long-term links of adolescent peer relationship difficulties to adult vagal tone. J Behav Med 45, 690–701 (2022). https://doi.org/10.1007/s10865-022-00334-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10865-022-00334-1