Abstract
Children with Attention-Deficit/Hyperactivity Disorder (ADHD) experience deficits in emotion regulation that can be measured physiologically under environmental stress conditions by examining respiratory sinus arrhythmia (RSA), a marker of parasympathetic nervous system (PNS) withdrawal. The current pilot study examined the impact of comorbid internalizing disorders and comorbid Oppositional Defiant Disorder (ODD) on emotion regulation in children with ADHD by measuring RSA as an indicator of dysregulated emotional reactivity. Twenty-four 7–10 year old children with ADHD participated in the current study. Children completed a 5-min resting attending baseline while electrocardiogram data (ECG) were recorded to examine baseline RSA. Children then completed a stress inducing, blocked goal, Card Sorting Task to measure RSA reactivity to stress. Results revealed a significant effect of internalizing disorder status on RSA difference score, F (1, 18) = 5.83, p = .03, η2 = .25. Children in the comorbid internalizing disorder group had a significantly greater decrease in RSA from the baseline time period to the card sorting task. There was no significant effect of ODD diagnostic status on RSA difference score, p > .05. The results of this preliminary study suggest that among children with ADHD, the presence of a comorbid internalizing disorder predicts greater withdrawal of the PNS. These findings represent an important step in understanding autonomic functioning of children with ADHD and comorbid disorders.
Similar content being viewed by others
References
Albano, A. M., & Kendall, P. C. (2002). Cognitive behavioural therapy for children and adolescents with anxiety disorders: Clinical research advances. International Review of Psychiatry, 14, 129–134. https://doi.org/10.1080/0954026022013264.
American Academy of Pediatrics. (2011). ADHD: Clinical practice guideline for the diagnosis, evaluation, and treatment of attention-deficit/hyperactivity disorder in children and adolescents. Pediatrics, 128, 1–16. https://doi.org/10.1542/peds.2011-2654.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders: DSM-IV-TR. Washington, DC: American Psychiatric Association.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: American Psychiatric Association.
Anastopoulos, A. D., Smith, T. F., Garrett, M. E., Morrissey-Kane, E., Schatz, N. K., Sommer, J. L.,... Ashley-Koch, A. (2011). Self regulation of emotion, functional impairment, and comorbidity among children with ADHD. Journal of Attention Disorders, 15, 583–592. https://doi.org/10.1177/1087054710370567.
Barkley, R. A. (1997). Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD. Psychological Bulletin, 121, 65–94. https://doi.org/10.1037/0033-2909.121.1.65.
Barkley, R. A. (Ed.). (2015). Attention-deficit hyperactivity disorder: A handbook for diagnosis and treatment. New York: The Guilford Press.
Barkley, R., DuPaul, G. J., & McMurray, M. B. (1990). Comprehensive evaluation of attention deficit disorder with and without hyperactivity as defined by research criteria. Journal of Consulting and Clinical Psychology, 58, 775–789.
Beauchaine, T. P. (2012). Physiological markers of emotional and behavioral dysregulation in externalizing psychopathology. Monographs of the Society for Research in Child Development, 77, 79–86. https://doi.org/10.1111/j.1540-5834.2011.00665.x.
Beauchaine, T. P., Katkin, E., Strassberg, Z., & Snarr, J. (2001). Disinhibitory psychopathology in male adolescents.pdf. Journal of Abnormal Psychology, 110, 610–624.
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.
Berntson, G. G., Lozano, D. L., Chen, Y., & Cacioppo, J. T. (2004). Where to Q in PEP. Psychophysiology, 41, 333–337. https://doi.org/10.1111/j.1469-8986.2004.00156.x.
Berntson, G. G., Bigger, J. T., Eckberg, D. L., 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. https://doi.org/10.1111/j.1469-8986.1997.tb02140.x.
Biederman, J., Spencer, T. J., Petty, C., Hyder, L. L., O'Connor, K. B., Surman, C. B., & Faraone, S. V. (2012). Longitudinal course of deficient emotional self-regulation CBCL profile in youth with ADHD: Prospective controlled study. Neuropsychiatric Disease and Treatment, 8, 267–276. https://doi.org/10.2147/NDT.S29670.
Boyce, W. T., Quas, J., Alkon, A., Smider, N., Essex, M. J., & Kupjer, D. J. (2001). Autonomic reactivity and psychopathlogy in middle childhood. British Journal of Psychiatry, 179, 144–150. https://doi.org/10.1192/bjp.179.2.144.
Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavioral problems. Biological Psychology, 74, 144–153. https://doi.org/10.1016/j.biopsycho.2006.09.005.
Conners, C. K., Sitarenios, G., Parker, J. D. A., & Epstein, J. N. (1998). The revised Conners rating scale parent (CPRS-R): Factor structure, reliability, and criterion validity. Journal of Abnormal Child Psychology, 26, 257–268.
Crowell, S. E., Beauchaine, T. P., Gatske-Kopp, L., Sylvers, P., Mead, H., & Chipman-Chacon, J. (2006). Autonomic correlates of attention-deficit/hyperactivity disorder and oppositional defiant disorder in preschool children. Journal of Abnormal Psychology, 115, 174–178. https://doi.org/10.1037/0021-843X.115.1.174.
Elia, J., Ambrosini, P., & Berrettini, W. (2008). ADHD characteristics: Concurrent comorbidity patterns in children and adolescents. Child and Adolescent Psychiatry and Mental Health, 2, 1–9. https://doi.org/10.1186/1753-2000-2-15.
El-Sheikh, M., Hinnant, J. B., & Erath, S. (2011). Developmental trajectories of delinquency symptoms in childhood: The role of marital conflict and autonomic nervous system activity. Journal of Abnormal Psychology, 120, 16–32. https://doi.org/10.1037/a0020626.
Factor, P. I., Reyes, R. A., & Rosen, P. J. (2014). Emotional impulsivity in children with ADHD associated with comorbid-not ADHD-symptomatology. Journal of Psychopathology and Behavioral Assessment, 36, 530–541. https://doi.org/10.1007/s10862-014-9428-z.
Gentzler, A. L., Santucci, A. K., & Fox, N. A. (2009). Respiratory sinus arrhythmia predicts emotion regulation and depressive symptoms in at-risk and control children. Biological Psychology, 82, 156–163. https://doi.org/10.1016/j.biopsycho.2009.07.002.
Gross, J. J. (1998). The emerging field of emotion regulation: An integrative review. Review of General Psychology, 2, 271–299. https://doi.org/10.1037/1089-2680.2.3.271.
Gross, J. J., & Levenson, R. W. (1993). Emotional suppression: Physiology, self-report, and expressive behavior. Journal of Personality and Social Psychology, 64, 970–986. https://doi.org/10.1037/0022-3514.64.6.970.
Gruber, J., Oveis, C., Keltner, D., & Johnson, S. (2011). A discrete emotions approach to positive emotion disturbance in depression. Cognition and Emotion, 25, 40–52. https://doi.org/10.1080/02699931003615984.
Hannesdottir, D. K., & Ollendick, T. H. (2007). The role of emotion regulation in the treatment of child anxiety disorders. Clinical Child and Family Psychology Review, 10, 275–293. https://doi.org/10.1007/s10567-007-0024-6.
Herpertz, S. C., Wenning, B., Mueller, B., Qunaibi, M., Sass, H., & Herpertz-Dahlmann, M. (2001). Psychophysiological responses in ADHD boys with and without conduct disorder: Implications for adult antisocial behavior. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 1220–1230.
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, 1049–1061. https://doi.org/10.1007/s10802-009-9341-1.
Keenan, K. (2000). Emotion dysregulation as a risk factor for child psychopathology. Clinical Psychology: Science and Practice, 7, 418–434. https://doi.org/10.1093/clipsy.7.4.418.
Kopp, C. B. (1989). Regulation of distress and negative emotions: A developmental view. Developmental Psychology, 25, 343–354.
van Lang, D. J. N., Tulen, J. H. M., Kallen, V. L., Rosbergen, B., Dieleman, G., & Ferdinand, R. F. (2007) Autonomic reactivity in clinically referred children attention-deficit/hyperactivity disorder versus anxiety disorder. European Child & Adolescent Psychiatry, 16, 71–78. https://doi.org/10.1007/s00787-006-0575-y.
Larson, K., Russ, S. A., Kahn, R. S., & Halfon, N. (2011). Patterns of comorbidity, functioning, and service use in US children with ADHD, 2007. Pediatrics, 127, 462–470. https://doi.org/10.1542/peds.2010-0165.
Martel, M. M., & Nigg, J. T. (2006). Child ADHD and personality/temperament traits of reactive and effortful control, resiliency, and emotionality. Journal of Child Psychology and Psychiatry and Allied Disciplines, 47, 1175–1183. https://doi.org/10.1111/j.1469-7610.2006.01629.x.
Maughan, B., Rowe, R., Messer, J., Goodman, R., & Meltzer, H. (2004). Conduct disorder and oppositional defiant disorder in a national sample: Developmental epidemiology. Journal of Child Psychology and Psychiatry, 45, 609–621. https://doi.org/10.1111/j.1469-7610.2004.00250.x.
Mauss, I. B., Bunge, S. A., & Gross, J. J. (2007). Automatic emotion regulation. Social and Personality Psychology Compass, 1, 1–22. https://doi.org/10.1111/j.1751-9004.2007.00005.x.
Musser, E. D., Backs, R. W., Schmitt, C. F., Ablow, J. C., Measelle, J. R., & Nigg, J. (2011). Emotion regulation via the autonomic nervous system in children with attention- deficit/hyperactivity disorder (ADHD). Journal of Abnormal Child Psychology, 39, 841–852. https://doi.org/10.1007/s10802-011-9499-1.
Newman, J., & Wallace, J. (1993). Diverse pathways to deficient self-regulation: Implications for disinhibitory psychopathology in children. Clinical Psychology Review, 13, 699–720.
Nigg, J. T. (2001). Is ADHD a disinhibitory disorder? Psychological Bulletin, 127, 571–598. https://doi.org/10.1037/0033-2909.127.5.571.
Okado, I., Mueller, C. W., & Nakamura, B. J. (2013). Positive negative affect in clinic-referred youth with ADHD. Journal of Attention Disorders. https://doi.org/10.1177/1087054713478466.
Palomba, D., Sarlo, M., Angrilli, A., Mini, A., & Stegagno, L. (2000). Cardiac responses associated with affective processing of unpleasant stimuli. International Journal of Psychophysiology, 36, 45–47.
Pang, K. C., & Beauchaine, T. P. (2013). Longitudinal patterns of autonomic nervous system responding to emotion evocation among children with conduct problems and/or depression. Developmental Psychobiology, 55, 698–706. https://doi.org/10.1002/dev.21065.
Porges, S. W. (2001). The polyvagal theory: Phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146. https://doi.org/10.1016/S0167-8760(01)00162-3.
Qu, M., Zhang, Y., Webster, J. G., & Tompkins, W. J. (1986). Motion artifact from spot and band electrodes during impedance cardiography. IEEE Transactions on Biomedical Engineering, 33, 1029–1036. https://doi.org/10.1109/TBME.1986.325869.
Richards, J. E. (1995). Reliability of respiratory sinus arrhythmia in R-R intervals, in 14-, 20-, and 26-week-old infants. Infant Behavior and Development, 18, 155-161. Retrieved from: https://doi.org/10.1016/0163-6383(95)90045-4.
Rosen, P. J., Walerius, D. M., Fogleman, N. D., & Factor, P. I. (2015). The association of emotional lability and emotional and behavioral difficulties among children with and without ADHD. Attention Deficit and Hyperactivity Disorders, 7, 281–294.
Shaffer, D., Fisher, P., Lucas, C. P., Dulcan, M. K., & Schwab-Stone, M. E. (2000). NIMH diagnostic interview schedule for children version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 39, 28–38.
Shaw, P., Stringaris, A., Nigg, J., & Leibenluft, E. (2014). Emotion dysregulation in attention deficit hyperactivity disorder. American Journal of Psychiatry, 171, 276–293. https://doi.org/10.1176/appi.ajp.2013.13070966.
Sobanski, E., Banaschewski, T., Asherson, P., Buitelaar, J., Chen, W., Franke, B., et al. (2010). Emotional lability in children and adolescents with attention deficit/hyperactivity disorder (ADHD): Clinical correlates and familial prevalence. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51, 915–923. https://doi.org/10.1111/j.1469-7610.2010.02217.x.
Stringaris, A., & Goodman, R. (2009a). Mood lability and psychopathology in youth. Psychological Medicine, 39, 1237–1245. https://doi.org/10.1017/S0033291708004662.
Stringaris, A., & Goodman, R. (2009b). Longitudinal outcome of youth oppositionality: Irritable, headstrong, and hurtful behaviors have distinctive predictions. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 404-412. Retrieved from: https://doi.org/10.1097/CHI.0b013e3181984f30.
Thompson, R. A. (1994). Emotion regulation: A theme in search of definition. Monographs of the Society for Research in Child Development, 59, 25–52.
Thompson, E. R. (2007). Development and validation of an internationally reliable short-form of the positive and negative affect schedule (PANAS). Journal of Cross-Cultural Psychology, 38, 227–242.
Vasilev, C. A., Crowell, S. E., Beauchaine, T. P., Mead, H. K., & Gatzke-Kopp, L. M. (2009). Correspondence between physiological and self-report measures of emotion dysregulation: A longitudinal investigation of youth with and without psychopathology. Journal of Child and Adolescent Psychiatry, 50, 1357–1364. https://doi.org/10.1111/j.1469-7610.2009.02172.x.
Vitiello, B. (2008). Understanding the risk of using medications for attention deficit hyperactivity disorder with respect to physical growth and cardiovascular function. Child and Adolescent Psychiatric Clinics of North America, 17, 459–474. https://doi.org/10.1016/j.chc.2007.11.010.
Watson, D., Clark, L., & Carey, G. (1988). Positive and negative affectivity and their relation to anxiety and depressive disorders. Journal of Abnormal Psychology, 97, 346–353.
Waxmonsky, J. G., Wymbs, F. A., Pariseau, M. E., Belin, P. J., Waschbusch, D. A., Babocsai, L., … Pelham, W. E. (2013). A novel group therapy for children with ADHD and severe mood dysregulation. Journal of Attention Disorders, 17, 527–541. https://doi.org/10.1177/1087054711433423.
West, D., Claes, S., & Deboutte, D. (2009). Differences in hypothalamic-pituitary-adrenal axis functioning among children with ADHD predominantly inattentive and combined types. European Child and Adolescent Psychiatry, 18, 543–553.
Whelan, Y. M., Stringaris, A., Maughan, B., & Barker, E. D. (2013). Developmental continuity of oppositional defiant disorder subdimensions at age 8, 10, and 13 years and their distinct psychiatric outcomes at age 16 years. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 961–969.
Wolraich, M. L., Feurer, I., Hannah, J. N., Pinnock, T. Y., & Baumgaertel, A. (1998). Obtaining systematic teacher report of disruptive behavior disorders utilizing the DSM-IV. Journal of Abnormal Child Psychology, 26, 141–152.
Wolraich, M. L., Lambert, W., Doffing, M. A., Bickman, L., Simmons, T., & Worley, K. (2003). Psychometric properties of the Vanderbilt ADHD Diagnostic Parent Rating Scale in a referred population. Journal of Pediatric Psychology, 28, 559–568. https://doi.org/10.1093/jpepsy/jsg046.
Zalewski, M., Lengua, L. J., Wilson, A. C., Trancik, A., & Baznit, A. (2011). Emotion regulation profiles, temperament, and adjustment problems in preadolescents. Child Development, 82, 951–966. https://doi.org/10.1111/j.1467-8624.2011.01575.x.
Zeman, J., Cassano, M., Perry-Parrish, C., & Stegall, S. (2006). Emotion regulation in children and adolescents. Journal of Developmental & Behavioral Pediatrics, 27, 155–168.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Author information
Authors and Affiliations
Contributions
All authors contributed significantly to the revision of this manuscript.
Corresponding author
Ethics declarations
Ethical Approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
This article does not contain any studies with animals performed by any of the authors.
Conflict of Interest
Kirsten D. Leaberry, Paul J. Rosen, Nicholas D. Fogleman, Danielle M. Walerius, and Kelly E. Slaughter declare that they have no conflict of interest.
Experimental Participants
This article contains studies with human participants. Experimental participants provided informed consent for study participation.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Leaberry, K.D., Rosen, P.J., Fogleman, N.D. et al. Physiological Emotion Regulation in Children with ADHD with and without Comorbid Internalizing Disorders: a Preliminary Study. J Psychopathol Behav Assess 40, 452–464 (2018). https://doi.org/10.1007/s10862-018-9644-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10862-018-9644-z