Specificity of autonomic arousal to anxiety in children with autism spectrum disorder

Anxiety is one of the most concerning comorbidities in autism spectrum disorder (ASD) due to its high prevalence, negative impact on physical and psychological well‐being, and interaction with core deficits of ASD. Current assessment and treatment of anxiety, which rely on the observation of behavior and self‐reports, are often ineffective as ASD is associated with deficits in communication and diminished introspective ability. In this light, autonomic nervous system (ANS) activity has been suggested as a marker of physiological arousal associated with anxiety. However, physiological arousal measured by ANS indices also occurs with other cognitive and emotional processes, and it is unclear whether anxiety‐related arousal can be differentiated from that related to other cognitive processes. To address this gap, we investigated the use of linear and nonlinear classification techniques for differentiating anxiety‐related arousal from arousal due to three cognitive processes (attention, inhibitory control, and social cognition) and physical activity based on electrocardiography signal features. Our results indicate that over 80% classification accuracy can be achieved, suggesting that ANS response can be used as a specific marker of anxiety‐related arousal in a subgroup of children with ASD who demonstrate an increase in heart rate in response to anxiogenic stimuli. Autism Res 2016, 9: 491–501. © 2015 International Society for Autism Research, Wiley Periodicals, Inc.

[1]  A. Lewis,et al.  Special teaching for special children? Pedagogies for inclusion , 2004, Educational and Child Psychology.

[2]  Mircea Miclea,et al.  Reduced heart rate variability and vagal tone in anxiety: Trait versus state, and the effects of autogenic training , 2009, Autonomic Neuroscience.

[3]  Scott Bellini Social Skill Deficits and Anxiety in High-Functioning Adolescents With Autism Spectrum Disorders , 2004 .

[4]  H. Engeland,et al.  Autonomic and Neuroendocrine Responses to a Psychosocial Stressor in Adults with Autistic Spectrum Disorder , 2006, Journal of autism and developmental disorders.

[5]  Ian H. Witten,et al.  Data Mining: Practical Machine Learning Tools and Techniques, 3/E , 2014 .

[6]  S. Porges,et al.  Cardiac vagal tone and sustained attention in school-age children. , 1994, Psychophysiology.

[7]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[8]  R. Mccraty,et al.  The effects of emotions on short-term power spectrum analysis of heart rate variability . , 1995, The American journal of cardiology.

[9]  A. Malliani,et al.  Heart rate variability. Standards of measurement, physiological interpretation, and clinical use , 1996 .

[10]  F. Wilhelm,et al.  Identifying anxiety states using broad sampling and advanced processing of peripheral physiological information. , 2006, Biomedical sciences instrumentation.

[11]  R. Lang,et al.  Treatment of anxiety in autism spectrum disorders using cognitive behaviour therapy: A systematic review , 2010, Developmental neurorehabilitation.

[12]  Arsenio Veicsteinas,et al.  Heart rate variability and autonomic activity at rest and during exercise in various physiological conditions , 2003, European Journal of Applied Physiology.

[13]  Harald Martinsen,et al.  Anxiety in people diagnosed with autism and intellectual disability: Recognition and phenomenology , 2011 .

[14]  A. Gilchrist,et al.  Social and Psychiatric Functioning in Adolescents with Asperger Syndrome Compared with Conduct Disorder , 2000, Journal of autism and developmental disorders.

[15]  A. Cowley,et al.  Autonomic Control of Cardiac Function , 2004 .

[16]  Digby Tantam,et al.  Psychological Disorder in Adolescents and Adults with Asperger Syndrome , 2000 .

[17]  J. Tulen,et al.  Characterization of stress reactions to the Stroop Color Word Test , 1989, Pharmacology Biochemistry and Behavior.

[18]  R. Rapee,et al.  Treating Anxiety Disorders in Children with High Functioning Autism Spectrum Disorders: A Controlled Trial , 2007, Journal of autism and developmental disorders.

[19]  Eden R Martin,et al.  Exome sequencing of extended families with autism reveals genes shared across neurodevelopmental and neuropsychiatric disorders , 2014, Molecular Autism.

[20]  V. Ramachandran,et al.  Autonomic responses of autistic children to people and objects , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  F. J. V. van Steensel,et al.  Anxiety Disorders in Children and Adolescents with Autistic Spectrum Disorders: A Meta-Analysis , 2011, Clinical child and family psychology review.

[22]  Azadeh Kushki,et al.  Functional autonomic nervous system profile in children with autism spectrum disorder , 2014, Molecular Autism.

[23]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[24]  G. Breithardt,et al.  Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. , 1996 .

[25]  L. Mulder,et al.  The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: a review with emphasis on a reanalysis of previous studies. , 2013, Psychophysiology.

[26]  P. Ekman,et al.  Autonomic nervous system activity distinguishes among emotions. , 1983, Science.

[27]  Tom Chau,et al.  Investigating the Autonomic Nervous System Response to Anxiety in Children with Autism Spectrum Disorders , 2013, PloS one.

[28]  Elisabeth L Hill,et al.  Understanding autism: insights from mind and brain. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  C. Collet,et al.  Autonomic nervous system response patterns specificity to basic emotions. , 1997, Journal of the Autonomic Nervous System.

[30]  Ramon Pallàs-Areny,et al.  A novel robust index to assess beat-to-beat variability in heart rate time-series analysis , 2001, IEEE Transactions on Biomedical Engineering.

[31]  Armando Barreto,et al.  Non-intrusive Physiological Monitoring for Automated Stress Detection in Human-Computer Interaction , 2007, ICCV-HCI.

[32]  Jennifer Healey,et al.  Toward Machine Emotional Intelligence: Analysis of Affective Physiological State , 2001, IEEE Trans. Pattern Anal. Mach. Intell..

[33]  Stephen H. Boutcher,et al.  Cardiovascular response to Stroop: Effect of verbal response and task difficulty , 2006, Biological Psychology.

[34]  J. Gillis,et al.  Autism and the Physiology of Stress and Anxiety , 2006 .

[35]  M. Toichi,et al.  Paradoxical Autonomic Response to Mental Tasks in Autism , 2003, Journal of autism and developmental disorders.

[36]  Tom Chau,et al.  Classification of Activity Engagement in Individuals with Severe Physical Disabilities Using Signals of the Peripheral Nervous System , 2012, PloS one.

[37]  R. Krauss,et al.  Facial and autonomic manifestations of the dimensional structure of emotion , 1984 .

[38]  K. H. Kim,et al.  Emotion recognition system using short-term monitoring of physiological signals , 2004, Medical and Biological Engineering and Computing.

[39]  Matthias Gamer,et al.  Functional imaging of sympathetic activation during mental stress , 2010, NeuroImage.

[40]  J. Wood,et al.  Cognitive Behavioral Treatment of Comorbid Anxiety Disorders and Social Difficulties in Children with High-Functioning Autism: A Case Report , 2007, Journal of Contemporary Psychotherapy.

[41]  I. Rapin,et al.  The autistic-spectrum disorders. , 1999, The New England journal of medicine.

[42]  S. Baron-Cohen,et al.  Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[43]  Matthew S. Goodwin,et al.  Cardiovascular Arousal in Individuals With Autism , 2006 .

[44]  R. Schachar,et al.  The persistence of cognitive deficits in remitted and unremitted ADHD: a case for the state-independence of response inhibition , 2013, Journal of child psychology and psychiatry, and allied disciplines.

[45]  Lawrence Scahill,et al.  Anxiety in children and adolescents with autism spectrum disorders. , 2009, Clinical psychology review.

[46]  Changchun Liu,et al.  Physiology-based affect recognition for computer-assisted intervention of children with Autism Spectrum Disorder , 2008, Int. J. Hum. Comput. Stud..

[47]  Mizanur Khondoker,et al.  Differences in HPA-axis and heart rate responsiveness to psychosocial stress in children with autism spectrum disorders with and without co-morbid anxiety , 2014, Psychoneuroendocrinology.

[48]  A. Malliani,et al.  Cardiovascular Neural Regulation Explored in the Frequency Domain , 1991, Circulation.

[49]  Otto Appenzeller Primer on the Autonomic Nervous System Edited by David Robertson, Phillip A. Low and Ronald J. Polinsky, Academic Press, 1996. HB £59.00; PB £29.00 (xv + 343 pages) ISBN HB 0 12 589760 X; PB 0 12 589761 8 , 1997, Trends in Neurosciences.

[50]  Rosalind W. Picard Future affective technology for autism and emotion communication , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[51]  H. Engeland,et al.  Differentiation between Autism and Multiple Complex Developmental Disorder in Response to Psychosocial Stress , 2003, Neuropsychopharmacology.

[52]  G. Billman The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance , 2013, Front. Physio..

[53]  Sylvia D. Kreibig,et al.  Autonomic nervous system activity in emotion: A review , 2010, Biological Psychology.

[54]  Willis J. Tompkins,et al.  A Real-Time QRS Detection Algorithm , 1985, IEEE Transactions on Biomedical Engineering.

[55]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

[56]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[57]  C. Frith,et al.  A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory , 1996, Neuropsychologia.

[58]  J. Reaven,et al.  Children with high-functioning autism spectrum disorders and co-occurring anxiety symptoms: implications for assessment and treatment. , 2009, Journal for specialists in pediatric nursing : JSPN.

[59]  Willis J. Tompkins,et al.  Quantitative Investigation of QRS Detection Rules Using the MIT/BIH Arrhythmia Database , 1986, IEEE Transactions on Biomedical Engineering.

[60]  Emer P. Doheny,et al.  SHIMMER™: An extensible platform for physiological signal capture , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.