Abstract
Atypical sensory features are frequently observed in individuals with autism spectrum disorder (ASD) as uncontrollable and less predictable sensory stimuli are thought to be stressful for them. To quantify distal indicators of cardiac vagus nerve activity, which is associated with top-down self-regulatory capacity, during sensory tasks as a stress state in children with ASD, we conducted an exploratory study to measure phasic high-frequency components of heart rate variability (phasic HF-HRV) during less controllable tactile/auditory sensory tasks in 37 children with ASD (aged 6–12 years) and 37 typically developing (TD) children. Only children with ASD showed increased HF-HRV values from the resting state to the task (i.e., phasic HF-HRV augmentation) during both less controllable tactile/auditory sensory tasks. In TD children, decreased phasic HF-HRV values were observed to cope with the task demand during the less-controllable-tactile task. These findings suggest that increased phasic HF-HRV values in response to less controllable sensory stimuli may reflect atypical physiological regulation during sensory stimulation in children with ASD.
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References
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders: DSM-IV-TR (4th ed.). APA. American Psychiatric Association.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders: DSM-5 (5th ed., pp.50–59). Washington, D.C: APA. American Psychiatric Association.
Baker, J. K., Fenning, R. M., Erath, S. A., Baucom, B. R., Messinger, D. S., Moffitt, J., Kaeppler, A., & Bailey, A. (2020). Respiratory sinus arrhythmia, parenting, and externalizing behavior in children with autism spectrum disorder. Autism, 24(1), 109–120. https://doi.org/10.1177/1362361319848525
Baker, J. K., Fenning, R. M., Erath, S. A., Baucom, B. R., Moffitt, J., & Howland, M. A. (2018). Sympathetic Under-Arousal and Externalizing Behavior Problems in Children with Autism Spectrum Disorder. Journal of Abnormal Child Psychology, 46(4), 895–906. https://doi.org/10.1007/s10802-017-0332-3
Bazelmans, T., Jones, E. J. H., Ghods, S., Corrigan, S., Toth, K., Charman, T., & Webb, S. J. (2019). Heart rate mean and variability as a biomarker for phenotypic variation in preschoolers with autism spectrum disorder. Autism Research, 12(1), 39–52. https://doi.org/10.1002/aur.1982
Beker, S., Foxe, J. J., & Molholm, S. (2021). Oscillatory entrainment mechanisms and anticipatory predictive processes in children with autism spectrum disorder. Journal of Neurophysiology, 126(5), 1783–1798. https://doi.org/10.1152/jn.00329.2021
Ben-Sasson, A., Hen, L., Fluss, R., Cermak, S. A., Engel-Yeger, B., & Gal, E. (2009). A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(1), 1–11. https://doi.org/10.1007/s10803-008-0593-3
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(6), 623–648. https://doi.org/10.1111/j.1469-8986.1997.tb02140.x
Berntson, G. G., Norman, G.J., Hawkley, L.C., & Cacioppo, J.T. (2008). Cardiac autonomic balance versus cardiac regulatory capacity. Psychophysiology, 45(4), 643–652. https://doi.org/10.1111/j.1469-8986.2008.00652.x
Bharath, R., Moodithaya, S. S., Bhat, S. U., Mirajkar, A. M., & Shetty, S. B. (2019). Comparison of physiological and biochemical autonomic indices in children with and without autism spectrum disorders. Medicina (Kaunas), 55(7). https://doi.org/10.3390/medicina55070346
Boyd, B. A., Baranek, G. T., Sideris, J., Poe, M. D., Watson, L. R., Patten, E., & Miller, H. (2010). Sensory features and repetitive behaviors in children with autism and developmental delays. Autism Research, 3(2), 78–87. https://doi.org/10.1002/aur.124
Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74(2), 144–53. https://doi.org/10.1016/j.biopsycho.2006.09.005
Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45(3), 101–112. https://doi.org/10.1002/dev.20020
Cascio, C. J., Lorenzi, J., & Baranek, G. T. (2016). Self-reported pleasantness ratings and examiner-coded defensiveness in response to touch in children with ASD: Effects of stimulus material and bodily location. Journal of Autism and Developmental Disorders, 46(5), 1528–1537. https://doi.org/10.1007/s10803-013-1961-1
Cascio, C. J., Moore, D., & McGlone, F. (2019). Social touch and human development. Developmental Cognitive Neuroscience, 35, 5–11. https://doi.org/10.1016/j.dcn.2018.04.009
Chang, M. C., Parham, L. D., Blanche, E. I., Schell, A., Chou, CP., Dawson, M., & Clark, F. (2012). Autonomic and behavioral responses of children with autism to auditory stimuli. American Journal of Occupational Therapy, 66(5), 567–576. https://doi.org/10.5014/ajot.2012.004242
Cheng, Y. C., Huang, Y. C., & Huang, W. L. (2020). Heart rate variability in individuals with autism spectrum disorders: A meta-analysis. Neuroscience & Biobehavioral Reviews, 118, 463–471. https://doi.org/10.1016/j.neubiorev.2020.08.007
Condy, E. E., Scarpa, A., & Friedman, B. H. (2017). Respiratory sinus arrhythmia predicts restricted repetitive behavior severity. Journal of Autism and Developmental Disorders, 47(9), 2795–2804. https://doi.org/10.1007/s10803-017-3193-2
Constantino, J. N., & Gruber C. P. (2007). Social Responsiveness Scale (SRS): manual. Western Psychological Services.
Constantino, J. N., & Gruber C. P. (2012). Social Responsiveness Scale - second edition (SRS-2): manual. Western Psychological Services.
Corbett, B. A., Muscatello, R. A., & Blain, S. D. (2016). Impact of sensory sensitivity on physiological stress responses and novel peer interaction in children with and without autism spectrum disorder. Frontiers in Neuroscience, 10, 278. https://doi.org/10.3389/fnins.2016.00278/full
Daluwatte, C., Miles, J. H., Sun, J., & Yao, G. (2015). Association between pupillary light reflex and sensory behaviors in children with autism spectrum disorders. Research in Developmental Disabilities, 37, 209–215. https://doi.org/10.1016/j.ridd.2014.11.019
Danesh, A. A., Howery, S., Aazh, H., Kaf, W., & Eshraghi, A. A. (2021). Hyperacusis in autism spectrum disorders. Audiology Research, 11(4), 547–556. https://doi.org/10.3390/audiolres11040049
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(1), 16–32. https://doi.org/10.1037/a0020626
Fenning, R. M., Erath, S.A., Baker, J. K., Messinger, D. S., Moffitt, J., Baucom, B. R., & Kaeppler, A. K. (2019) Sympathetic-parasympathetic interaction and externalizing problems in children with autism spectrum disorder. Autism Research, 12(12), 1805–1816. https://doi.org/10.1002/aur.2187
Fernández-Andrés, M. I., Pastor-Cerezuela, G., Sanz-Cervera, P., & Tárraga-Mínguez, R. (2015). A comparative study of sensory processing in children with and without autism spectrum disorder in the home and classroom environments. Research in Developmental Disabilities, 38, 202–212. https://doi.org/10.1016/j.ridd.2014.12.034
Green, S. A., Hernandez, L., Tottenham, N., Krasileva, K., Bookheimer, S. Y., & Dapretto, M. (2015). Neurobiology of sensory overresponsivity in youth with autism spectrum disorders. JAMA Psychiatry, 72(8), 778–786. https://doi.org/10.1001/jamapsychiatry.2015.0737
Green, S. A., Rudie, J. D., Colich, N. L., Wood, J. J., Shirinyan, D., Hernandez, L., & Bookheimer, S. Y. (2013). Overreactive brain responses to sensory stimuli in youth with autism spectrum disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 52(11), 1158–1172. https://doi.org/10.1016/j.jaac.2013.08.004
Grossman, P., & Taylor, E. W. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74(2), 263–285. https://doi.org/10.1016/j.biopsycho.2005.11.014
Hatfield, T. R., Brown, R. F., Giummarra, M. J., & Lenggenhager, B. (2019). Autism spectrum disorder and interoception: Abnormalities in global integration? Autism, 23(1), 212–222. https://doi.org/10.1177/1362361317738392
Hilton, C. L., Harper, J. D., Kueker, R. H., Lang, A. R., Abbacchi, A. M., Todorov, A., & Lavesser, P. D. (2010). Sensory responsiveness as a predictor of social severity in children with high functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 40(8), 937–945. https://doi.org/10.1007/s10803-010-0944-8
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(8):1049–61. https://doi.org/10.1007/s10802-009-9341-1
Ismael, N., Lawson, L. M., & Hartwell, J. (2018). Relationship between sensory processing and participation in daily occupations for children with autism spectrum disorder: A systematic review of studies that used Dunn’s sensory processing framework. American Journal of Occupational Therapy, 72(3), 7203205030p1–7203205030p9. https://doi.org/10.5014/ajot.2018.024075
Ito, H., Tani, I., Yukihiro, R., Adachi, J., Hara, K., Ogasawara, M., & Tsujii, M. (2012). Validation of an interview-based rating scale developed in japan for pervasive developmental disorders. Research in Autism Spectrum Disorders, 6(4), 1265–1272. https://doi.org/10.1016/j.rasd.2012.04.002
Japanese WISC-IV Publication Committee. (2010). Nihonban WISC- IV Chinou Kensahou [Wechsler Intelligence Scale for Children - Japanese version] (4th ed). Nihon Bunka Kagakusha.
Jarrin, D. C., McGrath, J. J., Poirier, P., Séguin, L., Tremblay, R. E., Montplaisir, J. Y., & Séguin, J. R. (2015). Short-term heart rate variability in a population-based sample of 10-year-old children. Pediatric Cardiology, 36(1), 41–48. https://doi.org/10.1007/s00246-014-0962-y
Jung, J., Zbozinek, T. D., Cummings, K. K., Wilhelm, F. H., Dapretto, M., Craske, M. G., & Green, S. A. (2021). Associations between physiological and neural measures of sensory reactivity in youth with autism. Journal of Child Psychology and Psychiatry, 62(10), 1183–1194. https://doi.org/10.1111/jcpp.13387
Kaiser, M. D., Yang, D. Y., Voos, A. C., Bennett, R. H., Gordon, I., Pretzsch, C., & Pelphrey, K. A. (2016). Brain mechanisms for processing affective (and nonaffective) touch are atypical in autism. Cerebral Cortex, 26(6), 2705–2714. https://doi.org/10.1093/cercor/bhv125
Khurshid, S., Peng, Y., & Wang, Z. (2019). Respiratory sinus arrhythmia acts as a moderator of the relationship between parental marital conflict and adolescents' internalizing problems. Frontiers in Neuroscience, 13, 500. https://doi.org/10.3389/fnins.2019.00500/full
Klusek, J., Roberts, J. E., & Losh, M. (2015). Cardiac autonomic regulation in autism and fragile X syndrome: A review. Psychological Bulletin, 141(1), 141–175. https://doi.org/10.1037/a0038237
Kuiper, M. W. M., Verhoeven, E. W. M., & Geurts, H. M. (2017). Heart rate variability predicts inhibitory control in adults with autism spectrum disorders. Biological Psychology, 128, 141–152. https://doi.org/10.1016/j.biopsycho.2017.07.006
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/full
Lane, A. E., Young, R. L., Baker, A. E. Z., & Angley, M. T. (2010). Sensory processing subtypes in autism: Association with adaptive behavior. Journal of Autism and Developmental Disorders, 40(1), 112–122. https://doi.org/10.1007/s10803-009-0840-2
Lawson, R. P., Rees, G., & Friston, K. J. (2014). An aberrant precision account of autism. Frontiers in Human Neuroscience, 8, 302. https://doi.org/10.3389/fnhum.2014.00302/full
Lidstone, J., Uljarevic, M., Sullivan, J., Rodgers, J., McConachie, H., Freeston, M., & Leekam, S. (2014). Relations among restricted and repetitive behaviors, anxiety and sensory features in children with autism spectrum disorders. Research in Autism Spectrum Disorders, 8(2), 82–92. https://doi.org/10.1016/j.rasd.2013.10.001
Little, L. M., Ausderau, K., Sideris, J., & Baranek, G. T. (2015). Activity participation and sensory features among children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(9), 2981–2990. https://doi.org/10.1007/s10803-015-2460-3
Marcovitch, S., Leigh, J., Calkins, S. D., Leerks, E. M., O'Brien, M., & Blankson, A. N. (2010). Moderate vagal withdrawal in 3.5-year-old children is associated with optimal performance on executive function tasks. Developmental Psychobiology, 52(6), 603–608. https://doi.org/10.1002/dev.20462
Matsushima, K., Matsubayashi, J., Toichi, M., Funabiki, Y., Kato, T., Awaya, T., & Kato, T. (2016). Unusual sensory features are related to resting-state cardiac vagus nerve activity in autism spectrum disorders. Research in Autism Spectrum Disorders, 25, 37–46. https://doi.org/10.1016/j.rasd.2015.12.006
McIntosh, D. N., Miller, L. J., Shyu, V., & Dunn, W. (1999). Overview of the short sensory profile (SSP). In W. Dunn (Ed.), The sensory profile: User’s Manual (pp. 59–73). The Psychological Corporation.
Miller, L. J., & Reisman, j.e., McIntosh, D.N., Simon, J. (2001). Sensory Challenge Protocol. In S. S. Roley, E. I. Blanche, & R. C. Schaaf (Eds.), Understanding the nature of sensory integration with diverse populations (pp. 85–88). Therapy Skill Builders.
O'Connor, K. (2012). Auditory processing in autism spectrum disorder: A review. Neuroscience & Biobehavioral Reviews, 36(2), 836–854. https://doi.org/10.1016/j.neubiorev.2011.11.008
Pellicano, E., & Burr, D. (2012). When the world becomes 'too real': A bayesian explanation of autistic perception. Trends in Cognitive Sciences, 16(10), 504–510. https://doi.org/10.1016/j.tics.2012.08.009
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
Rodgers, J., Glod, M., Connolly, B., & McConachie, H. (2012). The relationship between anxiety and repetitive behaviours in autism spectrum disorder. Journal of Autism and Developmental Disorders, 42(11), 2404–2409. https://doi.org/10.1007/s10803-012-1531-y
Ramshur, J. T. (2010). Welch PSD in analysis software HRVAS. http://sourceforge.net/projects/hrvas/
Rogers, S. J., Hepburn, S., & Wehner, E. (2003). Parent reports of sensory symptoms in toddlers with autism and those with other developmental disorders. Journal of Autism and Developmental Disorders, 33(6), 631–642. https://doi.org/10.1023/B:JADD.0000006000.38991.a7
Schaaf, R. C., Benevides, T. W., Leiby, B. E., & Sendecki, J. A. (2015). Autonomic dysregulation during sensory stimulation in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(2), 461–472. https://doi.org/10.1007/s10803-013-1924-6
Schoen, S. A., Miller, L. J., Brett-Green, B. A., & Nielsen, D. M. (2009). Physiological and behavioral differences in sensory processing: A comparison of children with autism spectrum disorder and sensory modulation disorder. Frontiers in Integrative Neuroscience, 3, 29. https://doi.org/10.3389/neuro.07.029.2009/full
South, M., & Rodgers, J. (2017). Sensory, emotional and cognitive contributions to anxiety in autism spectrum disorders. Frontiers in Human Neuroscience, 11. https://doi.org/10.3389/fnhum.2017.00020/full
Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Circulation, 93(5), 1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043
Tavassoli, T., Bellesheim, K., Tommerdahl, M., Holden, J. M., Kolevzon, A., & Buxbaum, J. D. (2016). Altered tactile processing in children with autism spectrum disorder. Autism Research, 9(6), 616–620. https://doi.org/10.1002/aur.1563
Thapa, R., Pokorski, I., Ambarchi, Z., Thomas, E., Demayo, M., Boulton, K, Guastella, A. J. (2021). Heart rate variability in children with autism spectrum disorder and associations with medication and symptom severity. Autism Research, 14(1), 75–85. https://doi.org/10.1002/aur.2437
Thayer, J. F., & Lane, R. D. (2009). Claude bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 33(2), 81–88. https://doi.org/10.1016/j.neubiorev.2008.08.004
Thye, M. D., Bednarz, H. M., Herringshaw, A. J., Sartin, E. B., & Kana, R. K. (2018). The impact of atypical sensory processing on social impairments in autism spectrum disorder. Developmental Cognitive Neuroscience, 29, 151–167. https://doi.org/10.1016/j.dcn.2017.04.010
Tillmann, J., Uljarevic, M., Crawley, D., Dumas, G., Loth, E., Murphy, D., . . . the AIMS-2-TRIALS LEAP group. (2020). Dissecting the phenotypic heterogeneity in sensory features in autism spectrum disorder: a factor mixture modelling approach. Molecular Autism, 11(1), 67. https://doi.org/10.1186/s13229-020-00367-w
Tomchek, S. D., & Dunn, W. (2007). Sensory processing in children with and without autism: A comparative study using the short sensory profile. American Journal of Occupational Therapy, 61(2), 190–200. https://doi.org/10.5014/ajot.61.2.190
Tomchek, S. D., Little, L. M., & Dunn, W. (2015). Sensory pattern contributions to developmental performance in children with autism spectrum disorder. American Journal of Occupational Therapy, 69(5), 1–10. https://doi.org/10.5014/ajot.2015.018044
Tonhajzerova, I., Ondrejka, I., Ferencova, N., Bujnakova, I., Grendar, M., Olexova, L. B., Visnovcova, Z. (2021). Alternations in the cardiovascular autonomic regulation and growth factors in autism. Physiological Research, 70(4), 551–561.
Tsujii, M. (Ed.). (2015). Nihonban Kankaku Purofairu Yuzamanyuaru [The Sensory profile - Japanese version: User’s manual] (pp. 20–30, 92–127). Japan: Nihon Bunka Kagakusha (in Japanese).
van Laarhoven, T., Stekelenburg, J. J., Eussen, M. L. J. M., & Vroomen, J. (2019). Electrophysiological alterations in motor-auditory predictive coding in autism spectrum disorder. Autism Research, 12(4), 589–599. https://doi.org/10.1002/aur.2087
Vasa, R. A., Keefer, A., McDonald, R. G., Hunsche, M. C., & Kerns, C. M. (2020). A scoping review of anxiety in young children with autism spectrum disorder. Autism Research, 13(12), 2038–2057. https://doi.org/10.1002/aur.2395
Wang, X., Liu, B., Xie, L., Yu, X., Li, M., & Zhang, J. (2016). Cerebral and neural regulation of cardiovascular activity during mental stress. BioMedical Engineering OnLine, 15. https://doi.org/10.1186/s12938-016-0255-1
Wigham, S., Rodgers, J., South, M., McConachie, H., & Freeston, M. (2015). The interplay between sensory processing abnormalities, intolerance of uncertainty, anxiety and restricted and repetitive behaviours in autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(4), 943–952. https://doi.org/10.1007/s10803-014-2248-x
Yu, X., Zhang, J., Xie, D., Wang, J., & Zhang, C. (2009). Relationship between scalp potential and autonomic nervous activity during a mental arithmetic task. Autonomic Neuroscience, 146(1–2), 81–86. https://doi.org/10.1016/j.autneu.2008.12.005
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We would like to thank the participants and their parents for their contributions to this study. This work was supported by Grants-in-Aid for Scientific Research (KAKEN; 15K01414) from the Japan Society for the Promotion of Science. The funding source had no role in the design of the study, the collection, analysis, or interpretation of data, or the writing of the manuscript.
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Our work was founded by Grants-in-Aid for Scientific Research (KAKEN; 15K01414) from the Japan Society for the Promotion of Science. The funding source had no role in the design of the study; the collection, analysis, or interpretation of data; or the writing of the manuscript. The authors have no relevant financial or non-financial interests to disclose.
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Matsushima, K., Matsubayashi, J., Toichi, M. et al. Atypical Physiological Response to Less Controllable Sensory Stimulation in Children with ASD. Res Child Adolesc Psychopathol 50, 1363–1377 (2022). https://doi.org/10.1007/s10802-022-00927-z
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DOI: https://doi.org/10.1007/s10802-022-00927-z