Abstract
Emotion dysregulation is common among individuals with autism spectrum disorder (ASD). This study examined the relationship between emotion dysregulation and resting heart rate variability (HRV), a marker of the autonomic nervous system, in ASD adolescents. Resting HRV data were collected from ASD (n = 23) and typically developing (TD) adolescents (n = 32) via short-term electrocardiogram. Parents/caregivers reported participants’ level of emotion dysregulation with the Emotion Dysregulation Inventory (EDI). Controlling for the effects of age and gender, regression analyses revealed moderating effects of group, suggesting that lower resting HRV was more strongly associated with greater emotion dysregulation in ASD than TD adolescents. The results support the view that disruptions in autonomic functioning may contribute to emotion dysregulation in ASD.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmed, S. P., Bittencourt-Hewitt, A., & Sebastian, C. L. (2015). Neurocognitive bases of emotion regulation development in adolescence. Developmental Cognitive Neuroscience, 15, 11–25. https://doi.org/10.1016/j.dcn.2015.07.006.
Aldao, A., Gee, D. G., De Los Reyes, A., & Seager, I. (2016). Emotion regulation as a transdiagnostic factor in the development of internalizing and externalizing psychopathology: current and future directions. Development and Psychopathology, 28(4pt1), 927–946. https://doi.org/10.1017/S0954579416000638.
American Psychiatric Association. (2013). Diagnostic and statistical Manual of Mental Disorders (5th ed).). American Psychiatric Publishing.
Appelhans, B. M., & Luecken, L. J. (2006). Heart rate variability as an index of regulated emotional responding. Review of General Psychology, 10(3), 229–240. https://doi.org/10.1037/1089-2680.10.3.229.
Appelhans, B. M., & Luecken, L. J. (2008). Heart rate variability and pain: associations of two interrelated homeostatic processes. Biological psychology, 77(2), 174–182.
Arora, I., Bellato, A., Ropar, D., Hollis, C., & Groom, M. J. (2021). Is autonomic function during resting-state atypical in Autism: a systematic review of evidence. Neuroscience & Biobehavioral Reviews, 125, 417–441. https://doi.org/10.1016/j.neubiorev.2021.02.041.
Bal, E., Harden, E., Lamb, D., Van Hecke, A. V., Denver, J. W., & Porges, S. W. (2010). Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state. Journal of Autism and Developmental Disorders, 40(3), 358–370. https://doi.org/10.1007/s10803-009-0884-3.
Beauchaine, T. P., & Thayer, J. F. (2015). Heart rate variability as a transdiagnostic biomarker of psychopathology. International Journal of Psychophysiology, 98(2), 338–350. https://doi.org/10.1016/j.ijpsycho.2015.08.004.
Benevides, T. W., & Lane, S. J. (2015). A review of cardiac autonomic measures: considerations for examination of physiological response in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(2), 560–575. https://doi.org/10.1007/s10803-013-1971-z.
Berkovits, L., Eisenhower, A., & Blacher, J. (2017). Emotion regulation in young children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 47(1), 68–79. https://doi.org/10.1007/s10803-016-2922-2.
Buchhorn, R., Conzelmann, A., Willaschek, C., Störk, D., Taurines, R., & Renner, T. J. (2012). Heart rate variability and methylphenidate in children with ADHD. ADHD Attention Deficit and Hyperactivity Disorders, 4(2), 85–91. https://doi.org/10.1007/s12402-012-0072-8.
Cai, R. Y., Richdale, A. L., Dissanayake, C., & Uljarević, M. (2019). Resting heart rate variability, emotion regulation, psychological wellbeing and autism symptomatology in adults with and without autism. International Journal of Psychophysiology, 137, 54–62. https://doi.org/10.1016/j.ijpsycho.2018.12.010.
Cai, R. Y., Richdale, A. L., Uljarević, M., Dissanayake, C., & Samson, A. C. (2018). Emotion regulation in autism spectrum disorder: where we are and where we need to go. Autism Research, 11(7), 962–978. https://doi.org/10.1002/aur.1968.
Chalmers, J. A., Quintana, D. S., Abbott, M. J., & Kemp, A. H. (2014). Anxiety disorders are associated with reduced heart rate variability: a meta-analysis. Frontiers in Psychiatry, 5(80), 1–11. https://doi.org/10.3389/fpsyt.2014.00080.
Chan, R. W. S., & Liu, W. S. (2008a). The Adolescent Autism Spectrum Quotient (AQ)https://docs.autismresearchcentre.com/tests/AQ_Adolescent_Chinese.pdf
Chan, R. W. S., & Liu, W. S. (2008b). The Adult Autism Spectrum Quotient (AQ)https://docs.autismresearchcentre.com/tests/AQ_Chinese.pdf
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum.
Conner, C. M., Golt, J., Shaffer, R., Righi, G., Siegel, M., & Mazefsky, C. A. (2021). Emotion dysregulation is substantially elevated in autism compared to the general population: impact on psychiatric services. Autism Research, 14(1), 169–181. https://doi.org/10.1002/aur.2450.
Conner, C. M., White, S. W., Beck, K. B., Golt, J., Smith, I. C., & Mazefsky, C. A. (2019). Improving emotion regulation ability in autism: the emotional awareness and skills enhancement (EASE) program. Autism, 23(5), 1273–1287. https://doi.org/10.1177/1362361318810709.
Croen, L. A., Zerbo, O., Qian, Y., Massolo, M. L., Rich, S., Sidney, S., & Kripke, C. (2015). The health status of adults on the autism spectrum. Autism, 19(7), 814–823. https://doi.org/10.1177/1362361315577517.
Daluwatte, C., Miles, J. H., Christ, S. E., Beversdorf, D. Q., Takahashi, T. N., & Yao, G. (2013). Atypical pupillary light reflex and heart rate variability in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 43(8), 1910–1925. https://doi.org/10.1007/s10803-012-1741-3.
Dijkhuis, R. R., Ziermans, T., van Rijn, S., Staal, W., & Swaab, H. (2019). Emotional arousal during social stress in young adults with autism: insights from heart rate, heart rate variability and self-report. Journal of Autism and Developmental Disorders, 49(6), 2524–2535. https://doi.org/10.1007/s10803-019-04000-5.
Edmiston, E. K., Jones, R. M., & Corbett, B. A. (2016). Physiological response to social evaluative threat in adolescents with autism spectrum disorder. Journal of autism and developmental disorders, 46(9), 2992–3005. https://doi.org/10.1007/s10803-016-2842-1.
Eisenberg, N., & Spinrad, T. L. (2004). Emotion-related regulation: sharpening the definition. Child Development, 75(2), 334–339. https://doi.org/10.1111/j.1467-8624.2004.00674.x.
Elias, R., & White, S. W. (2018). Autism goes to college: understanding the needs of a student population on the rise. Journal of Autism and Developmental Disorders, 48(3), 732–746. https://doi.org/10.1007/s10803-017-3075-7.
Flachaire, E. (2005). Bootstrapping heteroskedastic regression models: wild bootstrap vs. pairs bootstrap. Computational Statistics & Data Analysis, 49(2), 361–376. https://doi.org/10.1016/j.csda.2004.05.018.
Frye, R. E., Vassall, S., Kaur, G., Lewis, C., Karim, M., & Rossignol, D. (2019). Emerging biomarkers in autism spectrum disorder: a systematic review. Annals of Translational Medicine, 7(23), 792. https://doi.org/10.21037/atm.2019.11.53.
Greenlee, J. L., Stelter, C. R., Piro-Gambetti, B., & Hartley, S. L. (2021). Trajectories of Dysregulation in Children with Autism Spectrum Disorder. Journal of Clinical Child & Adolescent Psychology, 50(6), 858–873. https://doi.org/10.1080/15374416.2021.1907752.
Guy, L., Souders, M., Bradstreet, L., DeLussey, C., & Herrington, J. D. (2014). Brief report: emotion regulation and respiratory sinus arrhythmia in autism spectrum disorder. Journal of Autism and Developmental Disorders, 44(10), 2614–2620. https://doi.org/10.1007/s10803-014-2124-8.
Heathers, J. A. (2014). Everything Hertz: methodological issues in short-term frequency-domain HRV. Frontiers in Physiology, 5(177), 1–15. https://doi.org/10.3389/fphys.2014.00177.
Hudson, C. C., Hall, L., & Harkness, K. L. (2019). Prevalence of depressive disorders in individuals with autism spectrum disorder: a meta-analysis. Journal of Abnormal Child Psychology, 47(1), 165–175. https://doi.org/10.1007/s10802-018-0402-1.
Kaufmann, T., Sütterlin, S., Schulz, S. M., & Vögele, C. (2011). ARTiiFACT: a tool for heart rate artifact processing and heart rate variability analysis. Behavior Research Methods, 43(4), 1161–1170. https://doi.org/10.3758/s13428-011-0107-7.
Klusek, J., Roberts, J. E., & Losh, M. (2015). Cardiac autonomic regulation in autism and fragile X syndrome: a review. Psychological Bulletin, 141(1), 141. https://doi.org/10.1037/a0038237.
Koenig, J., Kemp, A. H., Beauchaine, T. P., Thayer, J. F., & Kaess, M. (2016). Depression and resting state heart rate variability in children and adolescents—A systematic review and meta-analysis. Clinical Psychology Review, 46, 136–150. https://doi.org/10.1016/j.cpr.2016.04.013.
Laborde, S., Mosley, E., & Thayer, J. F. (2017). Heart rate variability and cardiac vagal tone in psychophysiological research–recommendations for experiment planning, data analysis, and data reporting. Frontiers in psychology, 8, 213. https://doi.org/10.3389/fpsyg.2017.00213.
La Rovere, M. T., Pinna, G. D., Maestri, R., Mortara, A., Capomolla, S., Febo, O., & Cobelli, F. (2003). Short-term heart rate variability strongly predicts sudden cardiac death in chronic heart failure patients. Circulation, 107(4), 565–570. https://doi.org/10.1161/01.CIR.0000047275.25795.17.
Lecavalier, L. (2006). Behavioral and emotional problems in young people with pervasive developmental disorders: relative prevalence, effects of subject characteristics, and empirical classification. Journal of Autism and Developmental Disorders, 36, 1101–1114. https://doi.org/10.1007/s10803-006-0147-5.
Liu, R. Y. (1988). Bootstrap procedures under some non-iid models. The Annals of Statistics, 16(4), 1696–1708. https://doi.org/10.1214/aos/1176351062.
Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism diagnostic observation schedule–2nd edition (ADOS-2).Los Angeles, CA: Western Psychological Corporation, 284.
Lugnegård, T., Hallerbäck, M. U., & Gillberg, C. (2011). Psychiatric comorbidity in young adults with a clinical diagnosis of Asperger syndrome. Research in Developmental Disabilities, 32(5), 1910–1917. https://doi.org/10.1016/j.ridd.2011.03.025.
Malik, M. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use: Task force of the European Society of Cardiology and the North American Society for Pacing and Electrophysiology. Annals of Noninvasive Electrocardiology, 1(2), 151–181. https://doi.org/10.1111/j.1542-474X.1996.tb00275.x.
Mazefsky, C. A., Herrington, J., Siegel, M., Scarpa, A., Maddox, B. B., Scahill, L., & White, S. W. (2013). The role of emotion regulation in autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 52(7), 679–688. https://doi.org/10.1016/j.jaac.2013.05.006.
Mazefsky, C. A., Yu, L., White, S. W., Siegel, M., & Pilkonis, P. A. (2018). The emotion dysregulation inventory: psychometric properties and item response theory calibration in an autism spectrum disorder sample. Autism Research, 11(6), 928–941. https://doi.org/10.1002/aur.1947.
Mazzone, L., Ruta, L., & Reale, L. (2012). Psychiatric comorbidities in asperger syndrome and high functioning autism: diagnostic challenges. Annals of General Psychiatry, 11(1), 1–13. https://doi.org/10.1186/1744-859X-11-16.
McLaughlin, K. A., Hatzenbuehler, M. L., Mennin, D. S., & Nolen-Hoeksema, S. (2011). Emotion dysregulation and adolescent psychopathology: a prospective study. Behaviour Research and Therapy, 49(9), 544–554. https://doi.org/10.1016/j.brat.2011.06.003.
Ming, X., Julu, P. O., Brimacombe, M., Connor, S., & Daniels, M. L. (2005). Reduced cardiac parasympathetic activity in children with autism. Brain and Development, 27(7), 509–516. https://doi.org/10.1016/j.braindev.2005.01.003.
Neuhaus, E., Bernier, R., & Beauchaine, T. P. (2014). Brief report: social skills, internalizing and externalizing symptoms, and respiratory sinus arrhythmia in autism. Journal of Autism and Developmental Disorders, 44(3), 730–737. https://doi.org/10.1007/s10803-013-1923-7.
O’Connor, M. F., Allen, J. J., & Kaszniak, A. W. (2002). Autonomic and emotion regulation in bereavement and depression. Journal of Psychosomatic Research, 52(4), 183–185. https://doi.org/10.1016/S0022-3999(02)00292-1.
Pace-Schott, E. F., Amole, M. C., Aue, T., Balconi, M., Bylsma, L. M., Critchley, H., & VanElzakker, M. B. (2019). Physiological feelings. Neuroscience & Biobehavioral Reviews, 103, 267–304. https://doi.org/10.1016/j.neubiorev.2019.05.002.
Picci, G., & Scherf, K. S. (2015). A two-hit model of autism: adolescence as the second hit. Clinical Psychological Science, 3(3), 349–371. https://doi.org/10.1177/2167702614540646.
Porges, S. W. (2003). The polyvagal theory: phylogenetic contributions to social behavior. Physiology & Behavior, 79(3), 503–513. https://doi.org/10.1016/S0031-9384(03)00156-2.
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74(2), 116–143. https://doi.org/10.1016/j.biopsycho.2006.06.009.
Porges, S. W., Macellaio, M., Stanfill, S. D., McCue, K., Lewis, G. F., Harden, E. R., & Heilman, K. J. (2013). Respiratory sinus arrhythmia and auditory processing in autism: modifiable deficits of an integrated social engagement system? International Journal of Psychophysiology, 88(3), 261–270. https://doi.org/10.1016/j.ijpsycho.2012.11.009.
Powers, A., & Casey, B. J. (2015). The adolescent brain and the emergence and peak of psychopathology. Journal of Infant Child and Adolescent Psychotherapy, 14(1), 3–15. https://doi.org/10.1080/15289168.2015.1004889.
Prizant, B. M., & Laurent, A. (2011). Behavior is not the issue: an emotional regulation perspective on problem behavior—part one of a part-two article. Autism Spectrum Quarterly, 1, 29–30.
Raven, J., Rust, J., Chan, F., & Zhou, X. (2018). Raven’s 2 progressive Matrices, Clinical Edition (raven’s 2). Pearson.
Samson, A. C., Phillips, J. M., Parker, K. J., Shah, S., Gross, J. J., & Hardan, A. Y. (2014). Emotion dysregulation and the core features of autism spectrum disorder. Journal of Autism and Developmental Disorders, 44(7), 1766–1772. https://doi.org/10.1007/s10803-013-2022-5.
Shaffer, F., & Ginsberg, J. P. (2017). An overview of heart rate variability metrics and norms. Frontiers in Public Health, 258. https://doi.org/10.3389/fpubh.2017.00258.
Shaffer, F., McCraty, R., & Zerr, C. L. (2014). A healthy heart is not a metronome: an integrative review of the heart’s anatomy and heart rate variability. Frontiers in psychology, 5, 1040. https://doi.org/10.3389/fpsyg.2014.01040.
Singh, N. N., Lancioni, G. E., Singh, A. D., Winton, A. S., Singh, A. N., & Singh, J. (2011). Adolescents with Asperger syndrome can use a mindfulness-based strategy to control their aggressive behavior. Research in Autism Spectrum Disorders, 5(3), 1103–1109. https://doi.org/10.1016/j.rasd.2010.12.006.
Tang, Y. Y., Ma, Y., Fan, Y., Feng, H., Wang, J., Feng, S., & Fan, M. (2009). Central and autonomic nervous system interaction is altered by short-term meditation. Proceedings of the National Academy of Sciences, 106(22), 8865–8870. https://doi.org/10.1073/pnas.0904031106
Tang, Y. Y., Hölzel, B. K., & Posner, M. I. (2015). The neuroscience of mindfulness meditation. Nature Reviews Neuroscience, 16(4), 213–225. https://doi.org/10.1038/nrn3916.
Thapa, R., Alvares, G. A., Zaidi, T. A., Thomas, E. E., Hickie, I. B., Park, S. H., & Guastella, A. J. (2019). Reduced heart rate variability in adults with autism spectrum disorder. Autism Research, 12(6), 922–930. https://doi.org/10.1002/aur.2104.
Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, I. I. I., J. J., & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neuroscience & Biobehavioral Reviews, 36(2), 747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009.
Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61(3), 201–216. https://doi.org/10.1016/s0165-0327(00)00338-4.
Thompson, R. A., Lewis, M. D., & Calkins, S. D. (2008). Reassessing emotion regulation. Child Development Perspectives, 2(3), 124–131. https://doi.org/10.1111/j.1750-8606.2008.00054.x.
Tobaldini, E., Nobili, L., Strada, S., Casali, K. R., Braghiroli, A., & Montano, N. (2013). Heart rate variability in normal and pathological sleep. Frontiers in physiology, 4, 294. https://doi.org/10.3389/fphys.2013.00294.
Tsuji, H., Venditti Jr, F. J., Manders, E. S., Evans, J. C., Larson, M. G., Feldman, C. L., & Levy, D. (1996). Determinants of heart rate variability. Journal of the American College of Cardiology, 28(6), 1539–1546. https://doi.org/10.1016/S0735-1097(96)00342-7.
Van Hecke, A. V., Lebow, J., Bal, E., Lamb, D., Harden, E., Kramer, A., Denver, J., Bazhenova, O., & Porges, S. W. (2009). Electroencephalogram and heart rate regulation to familiar and unfamiliar people in children with autism spectrum disorders. Child Development, 80(4), 1118–1133. https://doi.org/10.1111/j.1467-8624.2009.01320.x.
Wang, J., Barstein, J., Ethridge, L. E., Mosconi, M. W., Takarae, Y., & Sweeney, J. A. (2013). Resting state EEG abnormalities in autism spectrum disorders. Journal of neurodevelopmental disorders, 5(1), 1–14. https://doi.org/10.1186/1866-1955-5-24.
Wechsler, D. (2014). Wechsler Adult Intelligence Scale-Fourth Edition (Hong Kong). Zhuhai, Guangdong, China: King-May Psychological Assessment Technology Development Limited Company.
Wechsler, D. (2010). Wechsler Intelligence Scale for Children-Fourth Edition (Hong Kong). Zhuhai, Guangdong, China: King-May Psychological Assessment Technology Development Limited Company.
White, S. W., Mazefsky, C. A., Dichter, G. S., Chiu, P. H., Richey, J. A., & Ollendick, T. H. (2014). Social-cognitive, physiological, and neural mechanisms underlying emotion regulation impairments: understanding anxiety in autism spectrum disorder. International Journal of Developmental Neuroscience, 39, 22–36. https://doi.org/10.1016/j.ijdevneu.2014.05.012.
Wong, S. W., Massé, N., Kimmerly, D. S., Menon, R. S., & Shoemaker, J. K. (2007). Ventral medial prefrontal cortex and cardiovagal control in conscious humans. Neuroimage, 35(2), 698–708. https://doi.org/10.1016/j.neuroimage.2006.12.027.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing Interests
The authors have no relevant competing interests to declare.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chiu, H., Ip, I., Ching, F. et al. Resting Heart Rate Variability and Emotion Dysregulation in Adolescents with Autism Spectrum Disorder. J Autism Dev Disord 54, 1482–1493 (2024). https://doi.org/10.1007/s10803-022-05847-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-022-05847-x