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Autonomic Dysregulation During Sensory Stimulation in Children with Autism Spectrum Disorder

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Abstract

Autonomic nervous system (ANS) activity during sensory stimulation was measured in 59 children with autism spectrum disorder (ASD) ages 6–9 in comparison to 30 typically developing controls. Multivariate comparisons revealed significant differences between groups in the respiratory sinus arrhythmia (parasympathetic measure) vector of means across sensory stimuli (p = 0.02) and in change from domain to domain (p = 0.01). Sympathetic activity, measured by pre-ejection period, did not differ significantly between groups, although it was higher in ASD participants. Findings suggest that participants with ASD demonstrated a different pattern of parasympathetic activity during sensory stimulation. Findings are discussed in relation to the biological mechanisms of sensory processing in autism, insight into the autism phenotype, and the utility of ANS activity as an outcomes marker.

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Notes

  1. Behavioral sensory reactivity is defined based on the DSM-5 Autism Spectrum Disorder diagnostic criteria description: “hyper-or hyporeactivity to sensory input or unusual interest in sensory aspects of the environment” such as “apparent indifference to pain/temperature, adverse response to specific sounds or textures, excessive smelling or touching of objects, visual fascination with lights or movements” (APA 2013).

  2. Eleven subjects (19 %) screened positively for anxiety, 12 screened positively for ADHD (20 %), 11 for Oppositional Defiant Disorder (19 %), 35 for Specific Phobia (59 %), and 1 for Major Depressive Disorder (2 %).

  3. The QRS complex is the electrical signal representing ventricular depolarization on an electrocardiogram (ECG). The Q, R, and S waves occur successively, with the Q being the first negative deflection, followed by a positive inflection (R-wave), with the next negative deflection being the S wave (Das and Zipes 2012).

  4. Children with ASD who refused electrodes, requested to stop testing, or skipped a protocol domain (ASD-Stopped, n = 18) were not significantly different than ASD-Completed (n = 40) in respect to mean age [F(1,57) = 1.07, p = 0.30] or cognitive level [F(1,48) = 0.15, p = 0.70] although the ASD-Stopped were more likely to have parent-reported dysfunction on the Underresponsivity/Seek Sensation domain z-score [ASD-Stopped M = −3.7, SD = 1.6, ASD-Completed M = −2.6, SD = 2.0, F(1,56) = 4.07, p = .05] and the Visual/Auditory Sensitivity domain z-score [ASD-Stopped M = −2.0, SD = 1.2, ASD-Completed M = −1.1, SD = 1.5, F(1,56) = 4.38, p = 0.04] of the SSP.

References

  • Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42(1), 64–78. doi:10.1002/dev.10082.

    Article  PubMed  Google Scholar 

  • American Psychiatric Association (APA). (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Association.

  • Baker, A. E. Z., Lane, A., Angley, M. T., & Young, R. L. (2008). The relationship between sensory processing patterns and behavioral responsiveness in autistic disorder: A pilot study. Journal of Autism and Developmental Disorders, 38, 867–875. doi:10.1007/s10803-007-0459-0.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Baranek, G. T., Boyd, B. A., Poe, M. D., David, F. J., Watson, L. R., & MacLean, W. E., Jr. (2007). Hyperresponsive sensory patterns in young children with autism, developmental delay, and typical development. American Journal on Mental Retardation, 112(4), 233–245.

    Article  PubMed  Google Scholar 

  • Baranek, G. T., David, F. J., Poe, M. D., Stone, W. L., & Watson, L. R. (2006). Sensory experiences questionnaire: Discriminating sensory features in young children with autism, developmental delays, and typical development. Journal of Child Psychology and Psychiatry and Allied Disciplines, 47(6), 591–601.

    Article  Google Scholar 

  • Barry, R. J., & James, A. J. (1988). Coding of stimulus parameters in autistic, retarded, and normal children: Evidence for a two-factor theory of autism. International Journal of Psychophysiology, 6(2), 139–149.

    Article  PubMed  Google Scholar 

  • Ben-Sasson, A., Cermak, S. A., Orsmond, G. I., Tager-Flusberg, H., Carter, A. S., Kadlec, M. B., et al. (2007). Extreme sensory modulation behaviors in toddlers with autism spectrum disorders. American Journal of Occupational Therapy, 61(5), 584.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Ben-Sasson, A., Soto, T. W., Martinez-Pedraza, F., & Carter, A. S. (2013). Early sensory over-responsivity in toddlers with autism spectrum disorders as a predictor of family impairment and parenting stress. Journal of Child Psychology and Psychiatry. doi:10.1111/jcpp.12035.

  • Bernal, M. E., & Miller, W. H. (1970). Electrodermal and cardiac responses of schizophrenic children to sensory stimuli. Psychophysiology, 7(2), 155–168.

    Article  PubMed  Google Scholar 

  • Berntson, G. G., Bigger, J. T., Eckberg, D. L., Grossman, P., Kaufman, P. G., Malik, M., et al. (1997). Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology, 34(6), 623–648.

    Article  PubMed  Google Scholar 

  • Berntson, G. G., Cacioppo, J. T., Binkley, P. F., Uchino, B. N., Quigley, K. S., & Fieldstone, A. (1994). Autonomic cardiac control. III. Psychological stress and cardiac response in autonomic space as revealed by pharmacological blockades. Psychophysiology, 31(6), 599–608.

    Article  PubMed  Google Scholar 

  • Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1991). Autonomic determinism: The modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychological Review, 98, 459–487. doi:10.1037/0033-295X.98.4.459.

    Google Scholar 

  • Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993). Respiratory sinus arrhythmia: Autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology, 30, 183–196.

    Google Scholar 

  • Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1995). The metrics of cardiac chronotropism: Biometric perspectives. Psychophysiology, 32, 162–171.

    Article  PubMed  Google Scholar 

  • Berntson, G. G., Lozano, D. L., Chen, Y., & Cacioppo, J. T. (2004). Where to Q in PEP. Psychophysiology, 41, 333–337. doi:10.1111/j.1469-8986.2004.00156.x.

    Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Das, M. K., & Zipes, D. P. (2012). Electrocardiography of arrhythmias: A comprehensive review. Philadelphia, PA: Elsevier/Saunders.

  • Gadow, K. D., & Sprafkin, J. N. (2002). Child symptom inventory 4: Screening and norms manual. Stony Brook, NY: Checkmate Plus.

  • Goodwin, M. S., Groden, J., Velicer, W. F., Lipsitt, L., Baron, G., Hofman, S. G., et al. (2006). Cardiovascular arousal in individuals with autism. Focus on Autism and Other Developmental Disabilities, 21, 100–123.

    Article  Google Scholar 

  • Goto, M., Nagashima, M., Baba, R., Nagano, Y., Yokota, M., Nishibata, K., et al. (1997). Analysis of heart rate variability demonstrates effects of development on vagal modulation of heart rate in healthy children. The Journal of Pediatrics, 130(5), 725–729.

    Article  PubMed  Google Scholar 

  • Grandin, T. (1992). An inside view of autism. In E. Schopler & G. B. Mesibov (Eds.), High functioning individuals with autism (pp. 105–126). New York: Plenum.

    Chapter  Google Scholar 

  • Hinnant, J. B., Elmore-Staton, L., & El-Sheikh, M. (2011). Developmental trajectories of respiratory sinus arrhythmia and preejection period in middle childhood. Developmental Psychobiology, 53(1), 59–68. doi:10.1002/dev.20487.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hirstein, W., Iversen, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings of the Royal Society Biological Sciences (Series B), 268(1479), 1883–1888.

    Article  Google Scholar 

  • Hoehn-Saric, R., & McLeod, D. R. (2000). Anxiety and arousal: Physiological changes and their perception. Journal of Affective Disorders, 61, 217–224. doi:10.1016/S0165-0327(00)00339-6.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Leekman, S. R., Nieto, C., Libby, S. J., Wing, L., & Gould, J. (2007). Describing the sensory abnormalities of children and adults with autism. Journal of Autism and Developmental Disorders, 37(5), 894–910.

    Article  Google Scholar 

  • Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659–685.

    Article  PubMed  Google Scholar 

  • Lozano, D. L., Norman, G., Knox, D., Wood, B. L., Miller, B. D., Emery, C. F., et al. (2007). Where to B in dZ/dt. Psychophysiology, 44, 113–119. doi:10.1111/j.1469-8986.2006.00468.x.

    Article  PubMed  Google Scholar 

  • Marco, E. J., Hinkley, L. B., Hill, S. S., & Nagarajan, S. S. (2011). Sensory processing in autism: A review of neurophysiologic findings. Pediatric Research, 69((5 Pt 2)), 48R–54R. doi:10.1203/PDR.0b013e3182130c54.

    Article  PubMed Central  PubMed  Google Scholar 

  • Martinmaki, K., Rusko, H., Kooistra, L., Kettunen, J., & Saalasti, S. (2006). Intraindividual validation of heart rate variability indexes to measure vagal effects on hearts. American Journal of Physiology-Heart and Circulatory Physiology, 290(2), H640–H647.

    Article  PubMed  Google Scholar 

  • McIntosh, D. N., Miller, L. J., & Shyu, V. (1999). Development and validation of the short sensory profile. In W. Dunn (Ed.), The sensory profile: User’s manual (pp. 59–73). San Antonio, TX: Psychological Corporation.

    Google Scholar 

  • Mindware Technologies, Ltd. (2011). Impedance cardiography application (IMP ver 3.0.1) and reference manual [software]. Gahanna, OH. Publisher website: http://www.mindwaretech.com.

  • Ming, X., Julu, P. O. O., Brimacombe, M., Connor, S., & Daniels, M. L. (2005). Reduced cardiac parasympathetic activity in children with autism. Brain and Development, 27(7), 509–516.

    Article  PubMed  Google Scholar 

  • Minshew, N. J., Sweeney, J., & Luna, B. (2002). Autism as a selective disorder of complex information processing and underdevelopment of neocortical systems. Molecular Psychiatry, 7(Suppl 2), S14–S15. doi:10.1038/sj.mp.4001166.

    Article  PubMed  Google Scholar 

  • Nance, P. W., & Hoy, C. S. (1996). Assessment of the autonomic nervous system. Physical Medicine and Rehabilitation, 10(1), 15–35.

    Google Scholar 

  • O’Riordan, M., & Passetti, F. (2006). Discrimination in autism within different sensory modalities. Journal of Autism and Developmental Disorders, 36(5), 665–675.

    Article  PubMed  Google Scholar 

  • O’Neill, M., & Jones, R. S. P. (1997). Sensory-perceptual abnormalities in autism: A case for more research? Journal of Autism and Developmental Disorders, 27(3), 283–293.

    Article  PubMed  Google Scholar 

  • Palkovitz, R. J., & Wiesenfeld, A. R. (1980). Differential autonomic responses of autistic and normal children. Journal of Autism and Developmental Disorders, 10(3), 347–360.

    Article  PubMed  Google Scholar 

  • Porges, S. W. (2005). The vagus: A mediator of behavioral and physiologic features. In M. L. Bauman & T. L. Kemper (Eds.), The neurobiology of autism (2nd ed., pp. 65–78). Baltimore and London: The Johns Hopkins University Press.

    Google Scholar 

  • Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74(2), 116–143.

    Article  PubMed Central  PubMed  Google Scholar 

  • Porges, S. W., Doussard-Roosevelt, J. A., & Maiti, A. K. (1994). Vagal tone and the physiological regulation of emotion. Monograph of the Society for Research in Child Development, 59(167), 186.

    Google Scholar 

  • Porges, S. W., Macellaio, M., Stanfill, S. D., McCue, K., Lewis, G. F., Harden, E. R., et al. (2012). Respiratory sinus arrhythmia and the auditory processing in autism: Modifiable deficits of an integrated social engagement system? International Journal of Psychophysiology, 88, 261–270. doi:10.1016/j.ijpsycho.2012.11.009.

    Article  PubMed Central  PubMed  Google Scholar 

  • Psychology Software Tools, Inc. (2012). E-Prime 2.0 [software]. Publisher website: http://www.pstnet.com/eprime.cfm.

  • Raiford, S. E., Weiss, L. G., Rolfhus, E., & Coalson, D. (2005). Global Ability Index. WISC-IV Technical Report #4. San Antonio, TX: Harcourt Assessment, Inc.

  • Robertson, A. E., & Simmons, D. R. (2013). The relationship between sensory sensitivity and autistic traits in the general population. Journal of Autism and Developmental Disorders, 43, 775–784. doi:10.1007/s10801-012-1608-7.

    Article  PubMed  Google Scholar 

  • 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 Disabilities, 33(6), 631–642.

    Article  Google Scholar 

  • Rogers, S. J., & Ozonoff, S. (2005). Annotation: What do we know about sensory dysfunction in autism? A critical review of empirical evidence. Journal of Child Psychology and Psychiatry, 46(12), 1255–1268.

    Article  PubMed  Google Scholar 

  • Rutter, M., Bailey, A., Berument, S. K., Lord, C., & Pickles, A. (2003). Social Communication Questionnaire. Los Angeles: Western Psychological Services.

    Google Scholar 

  • Salomon, K. (2005). Respiratory sinus arrhythmia during stress predicts resting respiratory sinus arrhythmia 3 years later in a pediatric sample. Health Psychology, 24(1), 68.

    Article  PubMed  Google Scholar 

  • Salomon, K., Matthews, K. A., & Allen, M. T. (2000). Patterns of sympathetic and parasympathetic reactivity in a sample of children and adolescents. Psychophysiology, 37(6), 842–849. doi:10.1111/1469-8986.3760842.

    Google Scholar 

  • Schaaf, R. C., Toth-Cohen, S., Johnson, S. L., Outten, G., & Benevides, T. W. (2011). The everyday routines of families of children with autism examining the impact of sensory processing difficulties on the family. Autism, 15(3), 373–389.

    Article  PubMed  Google Scholar 

  • Schoen, S., Miller, L. J., Brett-Green, B., & Nielsen, D. (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, 1–11. doi:10.3389/neuro.07.029.2009.

    Article  Google Scholar 

  • Stevens, S., & Gruzelier, J. (1984). Electrodermal activity to auditory stimuli in autistic, retarded, and normal children. Journal of Autism and Developmental Disorders, 14(3), 245–260.

    Article  PubMed  Google Scholar 

  • Toichi, M., & Kamio, Y. (2003). Paradoxical autonomic response to mental tasks in autism. Journal of Autism and Developmental Disorders, 33(4), 417–426.

    Article  PubMed  Google Scholar 

  • Tomchek, S. D., & Dunn, W. (2007). Sensory processing in children with and without autism: A comparative study using the short sensory profile. The American Journal of Occupational Therapy, 61(2), 190–200.

    Article  PubMed  Google Scholar 

  • van Engeland, H., Roelofs, J. W., Verbeten, M. N., & Slagen, J. L. (1991). Abnormal electrodermal reactivity to novel visual stimuli in autistic children. Psychiatry Research, 38(1), 27–38.

    Article  PubMed  Google Scholar 

  • Wechsler, D. (2003). Wechsler Intelligence Scale for children (4th ed.). San Antonio, TX: Harcourt Assessment, Inc.

    Google Scholar 

  • Woodard, C. R., Goodwin, M. S., Zelazo, P. R., Aube, D., Scrimgeour, M., Ostholthoff, T., et al. (2012). A comparison of autonomic, behavioral, and parent-report measures of sensory sensitivity in young children with autism. Research in Autism Spectrum Disorders, 6, 1234–1246. doi:10.1016/j.rasd.2012.03.012.

    Article  Google Scholar 

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Acknowledgments

Funding for this project was provided by the National Institute for Child Health and Development, Grant 5R03HD055972-02: Physiological and Behavioral Characterization of Sensory Dysfunction in Autism (PI: Schaaf). We would like to thank the children and families who participated in this study, our graduate students who assisted in data collection and entry including Xinmei Wen, Amy Harant, Stephanie Riggins, Marianne Conway, Marietta VanNess, Sarah Merhaut, Kate Oser, Shainna Davis, and Molly Crowe; as well as the Department of Occupational Therapy, Jefferson School of Health Professions who supported this project.

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  1. Department of Occupational Therapy, Jefferson School of Health Professions, Thomas Jefferson University, 901 Walnut Street, 6th Floor, Philadelphia, PA, 19107, USA

    Roseann C. Schaaf & Teal W. Benevides

  2. Division of Biostatistics, Department of Pharmacology and Experimental Therapeutics, Thomas Jefferson University, Philadelphia, PA, USA

    Benjamin E. Leiby & Jocelyn A. Sendecki

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  1. Roseann C. Schaaf
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Schaaf, R.C., Benevides, T.W., Leiby, B.E. et al. Autonomic Dysregulation During Sensory Stimulation in Children with Autism Spectrum Disorder. J Autism Dev Disord 45, 461–472 (2015). https://doi.org/10.1007/s10803-013-1924-6

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