Atypical pupillary light reflex and heart rate variability in children with autism spectrum disorder

Journal of Autism and Developmental Disorders

Volumn 43, Issue 8, 2013, Pages 1910-1925

  Daluwatte, Chathuri ^a   Miles, Judith H ^b   Christ, Shawn E ^a,b   Beversdorf, David Q ^a,b   Takahashi, T Nicole ^b   Yao, Gang ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

Autism; Autonomic nervous system; Heart rate variability; Pupillary light reflex

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTISM; AUTISM DIAGNOSTIC INTERVIEW REVISED; AUTONOMIC NERVOUS SYSTEM; CHILD; CHILDHOOD DISEASE; CONTROLLED STUDY; ELECTROCARDIOGRAM; FEMALE; HEART RATE VARIABILITY; HUMAN; MAJOR CLINICAL STUDY; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; PUPIL; PUPIL REFLEX; PUPILLOGRAPHY; SCHOOL CHILD; AGE; COMPARATIVE STUDY; DEVELOPMENTAL DISORDER; HEART RATE; PATHOPHYSIOLOGY; PHYSIOLOGY; TIME; YOUNG ADULT;

ADOLESCENT; AGE FACTORS; AUTONOMIC NERVOUS SYSTEM; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DEVELOPMENTAL DISABILITIES; FEMALE; HEART RATE; HUMANS; MALE; REFLEX, PUPILLARY; TIME FACTORS; YOUNG ADULT;

EID: 84880274216     PISSN: 01623257     EISSN: 15733432     Source Type: Journal    
DOI: 10.1007/s10803-012-1741-3     Document Type: Article

References (58)

1. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Association. Text Revision.
2. Anderson, C. J.; & Colombo, J. (2009). Larger tonic pupil size in young children with autism spectrum disorder. Developmental Psychobiology, 51, 207-211.
3. Anderson, C.; Colombo, J.; & Shaddy, D. J. (2006). Visual scanning and pupillary responses in young children with Autism Spectrum Disorder. Journal of Clinical and Experimental Neuropsychology, 28, 1238-1256.
4. Anderson, C.; Colombo, J.; & Shaddy, D. J. (in press). Pupil and salivary indicators of autonomic dysfunction in autism spectrum disorder. Developmental Psychobiology, doi: 10.1002/dev.21051.
5. Appenzeller, O. (1999). The autonomic nervous system part I. Normal Functions: Elsevier.
6. 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, 358-370.
7. Bär, K. J.; Boettger, M. K.; Koschke, M.; Schulz, S.; Chokka, P.; Yeragani, V. K.; et al. (2007). Non-linear complexity measures of heart rate variability in acute schizophrenia. Clinical Neurophysiology, 118, 2009-2015.
8. Bär, K. J.; Boettger, M. K.; Schulz, S.; Harzendorf, C.; Agelink, M. W.; Yeragani, V. K.; et al. (2008). The interaction between pupil function and cardiovascular regulation in patients with acute schizophrenia. Clinical Neurophysiology, 119, 2209-2213.
9. Bär, K. J.; Schulz, S.; Koschke, M.; Harzendorf, C.; Gayde, S.; Berg, W.; et al. (2009). Correlations between the autonomic modulation of heart rate, blood pressure and the pupillary light reflex in healthy subjects. Journal of the Neurological Sciences, 279, 9-13.
10. Barbur, J. L. (2003). Learning from the pupil. In: WERNER, L. M. C. J. S. (ed.) The visual neurosciences. MIT Press Cambridge, MA.
11. Bashat, D. B.; Kronfeld-Duenias, V.; Zachor, D. A.; Ekstein, P. M.; Hendler, T.; Tarrasch, R.; et al. (2007). Accelerated maturation of white matter in young children with autism: A high b value DWI study. NeuroImage, 37, 40-47.
12. Berntson, G. G.; Bigger, J. T, Jr, Eckberg, D. L.; Grossman, P.; Kaufmann, P. G.; Malik, M.; et al. (1997). Heart rate variability: Origins methods, and interpretive caveats. Psychophysiology, 34, 623-648.
13. Bonnet, M. H.; & Arand, D. L. (1998). Heart rate variability in insomniacs and matched normal sleepers. Psychosomatic Medicine, 60, 610-615.
14. Bremner, F. (2009). Pupil evaluation as a test for autonomic disorders. Clinical Autonomic Research, 19, 88-101.
15. Clarke, R. J. (2007). Shaping the pupil's response to light in the hooded rat. Experimental Brain Research, 176, 641-651.
16. Constantino, J. N.; & Gruber, C. P. (2005). The social responsiveness scale (SRS) manual. Los Angeles: Western Psychological Services.
17. Daluwatte, C.; Miles, J. H.; & Yao, G. (2012). Simultaneously measured pupillary light reflex and heart rate variability in healthy children. Physiological Measurement, 33, 1043-1052.
18. Delaney, J. P. A.; & Brodie, D. A. (2000). Effects of short-term psychological stress on the time and frequency domains of heart-rate variability. Perceptual and Motor Skills, 91, 515-524.
19. Dockstader, C.; Gaetz, W.; Rockel, C.; & Mabbott, D. J. (2012). White matter maturation in visual and motor areas predicts the latency of visual activation in children. Human Brain Mapping, 33, 179-191.
20. Eaves, L. C.; Wingert, H. D.; Ho, H. H.; & Mickelson, E. C. R. (2006). Screening for autism spectrum disorders with the social communication questionnaire. Journal of Developmental and Behavioral Pediatrics, 27, S95-S103.
21. Fan, X.; Miles, J. H.; Takahashi, N.; & Yao, G. (2009a). Abnormal transient pupillary light reflex in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 1499-1508.
22. Fan, X.; Miles, J. H.; Takahashi, N.; & Yao, G. (2009b). Sex-specific lateralization of contraction anisocoria in transient pupillary light reflex. Investigative Ophthalmology & Visual Science, 50, 1137-1144.
23. Gamelin, F. X.; Baquet, G.; Berthoin, S.; & Bosquet, L. (2008). Validity of the polar S810 to measure R-R intervals in children. International Journal of Sports Medicine, 29, 134-138.
24. Geschwind, D. H.; & Levitt, P. (2007). Autism spectrum disorders: Developmental disconnection syndromes. Current Opinion in Neurobiology, 17, 103-111.
25. Goodie, J. L.; Larkin, K. T.; & Schauss, S. (2000). Validation of the polar heart rate monitor for assessing heart rate during physical and mental stress. Journal of Psychophysiology, 14, 159-164.
26. Kamath, M. V.; & Fallen, E. L. (1993). Power spectral analysis of heart rate variability: A noninvasive signature of cardiac autonomic function. Critical Reviews in Biomedical Engineering, 21, 245-311.
27. Kootz, J. P.; & Cohen, D. J. (1981). Modulation of sensory intake in autistic children: Cardiovascular and behavioral indices. Journal of the American Academy of Child Psychiatry, 20, 692-701.
28. Laeng, B.; Sirois, S.; & Gredeback, G. (2012). Pupillometry: A window to the preconscious? Perspective on Psychological Science, 7, 18-27.
29. Levy, M. N. (1990). Autonomic interactions in cardiac control. Annals of the New York Academy of Sciences, 601, 209-221.
30. Loewenfeld, I. E. (1999). The pupil: Anatomy, physiology, and clinical applications. Detroit: Wayne State University Press.
31. Lord, C.; Rutter, M.; & Couteur, A. L. (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.
32. Lord, C.; Rutter, M.; Goode, S.; Heemsbergen, J.; Jordan, H.; Mawhood, L.; et al. (1989). Autism diagnostic observation schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185-212.
33. Lowenstein, O.; & Loewenfeld, I. E. (1950). Mutual role of sympathetic and parasympathetic in shaping of the pupillary reflex to light; pupillographic studies. Archives of Neurology and Psychiatry, 64, 341-377.
34. Malik, M. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. Circulation, 93, 1043-1065.
35. Martineau, J.; Hernandeza, N.; Hiebelb, L.; Rochéa, L.; Metzgerb, A.; & Bonnet-Brilhaulta, F. (2011). Can pupil size and pupil responses during visual scanning contribute to the diagnosis of autism spectrum disorder in children? Journal of Psychiatric Research, 45, 1077-1082.
36. Massin, M.; & von Bernuth, G. (1997). Normal ranges of heart rate variability during infancy and childhood. Pediatric Cardiology, 18, 297-302.
37. Mathewson, K. J.; Drmic, I. E.; Jetha, M. K.; Bryson, S. E.; Goldberg, J. O.; Hall, G. B.; et al. (2011). Behavioral and cardiac responses to emotional stroop in adults with autism spectrum disorders: Influence of medication. Autism Research, 4, 98-108.
38. McCulloch, D. L.; & Skarf, B. (1991). Development of the human visual system: Monocular and binocular pattern VEP latency. Investigative Ophthalmology & Visual Science, 32, 2372-2381.
39. Ming, X.; Bain, J. M.; Smith, D.; Brimacombe, M.; Gold Von-Simson, G.; & Axelrod, F. B. (2011). Assessing autonomic dysfunction symptoms in children: A pilot study. Journal of Child Neurology, 26, 420-427.
40. 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, 509-516.
41. Montano, N.; Ruscone, T.; Porta, A.; Lombardi, F.; Pagani, M.; & Malliani, A. (1994). Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt. Circulation, 90, 1826-1831.
42. Mukai, S.; & Hayano, J. (1995). Heart rate and blood pressure variabilities during graded head-up tilt. Journal of Applied Physiology, 78, 212-216.
43. Neuhuber, W.; & Schrödl, F. (2011). Autonomic control of the eye and the iris. Autonomic Neuroscience: Basic and Clinical, 165, 67-79.
44. Nunan, D.; Gay, D.; Jakovljevic, D. G.; Hodges, L. D.; Sandercock, G. R. H.; & Brodie, D. A. (2009). Validity and reliability of short-term heart-rate variability from the Polar S810. Medicine and Science in Sports and Exercise, 41, 243-250.
45. Palkovitz, R. J.; & Wiesenfeld, A. R. (1980). Differential autonomic responses of autistic and normal children. Journal of Autism and Developmental Disorders, 10, 347-360.
46. Porto, L. G. G.; & Junqueira, L. F, Jr. (2009). Comparison of time-domain short-term heart interval variability analysis using a wrist-worn heart rate monitor and the conventional electrocardiogram. PACE: Pacing and Clinical Electrophysiology, 32, 43-51.
47. Raven, J.; Raven, J. C.; & Court, J. H. (1996). Manual for Raven's progressive matrices and vocabulary scales. Oxford: Oxford Psychologists Press.
48. Rubin, L. S. (1961). Patterns of pupillary dilatation and constriction in psychotic adults and autistic children. The Journal of Nervous and Mental Disease, 133, 130-142.
49. Silvetti, M. S.; Drago, F.; & Ragonese, P. (2001). Heart rate variability in healthy children and adolescents is partially related to age and gender. International Journal of Cardiology, 81, 169-174.
50. Steyn, H. S.; & Ellis, S. M. (2009). Estimating an effect size in one-way multivariate analysis of variance (MANOVA). Multivariate Behavioral Research, 44, 106-129.
51. Thayer, J. F.; & Sternberg, E. (2006). Beyond heart rate variability: Vagal regulation of allostatic systems. Annals of the New York Academy of Sciences, 1088, 361-372.
52. Toichi, M.; & Kamio, Y. (2003). Paradoxical autonomic response to mental tasks in autism. Journal of Autism and Developmental Disorders, 33, 417-426.
53. van Engeland, H.; Roelofs, J. W.; Verbaten, M. N.; & Slangen, J. L. (1991). Abnormal electrodermal reactivity to novel visual stimuli in autistic children. Psychiatry Research, 38, 27-38.
54. Vissers, M. E.; Cohen, M. X.; & Geurts, H. M. (2012). Brain connectivity and high functioning autism: A promising path of research that needs refined models, methodological convergence, and stronger behavioral links. Neuroscience and Biobehavioral Reviews, 36, 604-625.
55. Wagner, J. B.; Hirsch, S. B.; Vogel-Farley, V. K.; Redcay, E.; & Nelson, C. A. (in press). Eye-tracking, autonomic, and electrophysiological correlates of emotional face processing in adolescents with autism spectrum disorder. Journal of Autism and Developmental Disorders, doi: 10.1007/s10803-012-1565-1.
56. Wechsler, D. (1991). Wechsler intelligence scale for children third edition manual. New York: The Psychological Corporation.
57. Weinstein, M.; Ben-Sira, L.; Levy, Y.; Zachor, D. A.; Itzhak, E. B.; Artzi, M.; et al. (2011). Abnormal white matter integrity in young children with autism. Human Brain Mapping, 32, 534-543.
58. Yeragani, V. K.; Pohl, R.; Berger, R.; Balon, R.; Ramesh, C.; Glitz, D.; et al. (1993). Decreased heart rate variability in panic disorder patients: A study of power-spectral analysis of heart rate. Psychiatry Research, 46, 89-103. Stroke