Top

Research on Child and Adolescent Psychopathology

Gepubliceerd in:

23-04-2022

Atypical Physiological Response to Less Controllable Sensory Stimulation in Children with ASD

Auteurs: Kanae Matsushima, Jun Matsubayashi, Motomi Toichi, Yasuko Funabiki, Takeo Kato, Tomonari Awaya, Reiko Tsuchida, Toshihiro Kato

Gepubliceerd in: Research on Child and Adolescent Psychopathology | Uitgave 10/2022

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.

vorige artikel Social Support and Nonsuicidal Self-injury among adolescent Psychiatric Inpatients

Alleen toegankelijk voor geautoriseerde gebruikers

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

Titel: Atypical Physiological Response to Less Controllable Sensory Stimulation in Children with ASD
Auteurs: Kanae Matsushima
Jun Matsubayashi
Motomi Toichi
Yasuko Funabiki
Takeo Kato
Tomonari Awaya
Reiko Tsuchida
Toshihiro Kato
Publicatiedatum: 23-04-2022
Uitgeverij: Springer US
Gepubliceerd in: Research on Child and Adolescent Psychopathology / Uitgave 10/2022
Print ISSN: 2730-7166
Elektronisch ISSN: 2730-7174
DOI: https://doi.org/10.1007/s10802-022-00927-z

Bohn Stafleu van Loghum

Deel dit onderdeel of sectie (kopieer de link)

Abstract

Log in om toegang te krijgen

Andere artikelen Uitgave 10/2022

Within-person Relations between Domains of Socio-emotional Development during Childhood and Adolescence

The Impact of ADHD on Maternal Quality of Life

Pathways from Maternal Harsh Discipline Through Rumination to Anxiety and Depression Symptoms: Gender and Normativeness of Harsh Discipline as Moderators

Longitudinal Associations Among Low-Income Mothers’ and Fathers’ Parenting and Relationships with Children and Adolescent Depression

Correction to: Secret Agent Society: A Randomized Controlled Trial of a Transdiagnostic Youth Social Skills Group Treatment

The Two-Factor Structure of the Parent Cognitive Error Questionnaire: A Measure of Parental Cognitive Errors in Relation to Child Problems