Association between pupillary light reflex and sensory behaviors in children with autism spectrum disorders
Introduction
Autism spectrum disorders (ASDs) are complex developmental disorders with symptoms in social functioning, communication, and restricted or repetitive behaviors. Multiple atypical neurological and behavioral measures have been found in ASD. We recently discovered that children with ASD showed significantly different pupillary light reflex (PLR) than typically developing children (Fan et al., 2009, Daluwatte et al., 2013). PLR measures the dynamic changes in pupil size induced by optical luminance changes. Children with ASD showed multiple atypical PLR parameters including longer latency, less constriction amplitude, and shorter constriction/redilation times. We also found a significant age effect in PLR latency in children with typical development that was not observed in children with ASD (Daluwatte et al., 2013).
The pupil size is controlled by two antagonist iris muscles, the sphincter and dilator, which produce pupil constriction and dilation, respectively. The sphincter is mainly innervated by the parasympathetic nervous system and the dilator innervated by the sympathetic system (Barbur, 2004). The sympathetic tract passes through the ciliary ganglion without synapsing and emerges as the long ciliary nerves entering the eye along the optic nerve. These postganglionic sympathetic nerves travel within the suprachorodial space to innervate the iris dilator muscle (Appenzeller, 1999). The preganglionic parasympathetic nerve branches off to the ciliary ganglion and emerges as several short ciliary nerves which innervate the iris sphincter muscle (Appenzeller, 1999). Due to such underlying control mechanisms from the autonomic nervous system (ANS), PLR provides a simple yet reliable clinical assessment of ANS dysfunction (Barbur, 2004, Bremner, 2009).
In addition to pupillary pathway, ANS dysfunction in cardiovascular system has also been reported in children with ASD (Bal et al., 2010, Ming et al., 2005, Ming et al., 2011). In fact, ANS in general is involved in a multitude of physiological and behavioral activities beyond the pupillary and cardiovascular controls. For example, ANS is known to play a role in modulating the sensory processing (Kootz and Cohen, 1981, Saper, 2002, Vallbo et al., 1979). Human senses can be divided into five traditional groups (vision, auditory, taste, smell, and touch) and various non-traditional senses such as temperature and pain. Sensory system is an essential part of the neurological system that transduces the physical world to our perception. There are four basic patterns in sensory processing: low registration, sensory seeking, sensory sensitivity, and sensation avoiding (Dunn, 1997). Abnormality in sensory processing has been frequently reported in children with ASD (Kientz and Dunn, 1997, Klintwall et al., 2011, Tomchek and Dunn, 2007). For example, children with ASD avoid auditory stimulation by withdrawal while seeking for proprioceptive and vestibular stimulation by repetitive behaviors such as rocking, spinning, or flapping their hands (Case-Smith & Bryan, 1999). While identifying atypical sensory behaviors in ASD, it is also important to understand its association with physiological measures to better understand the causes and effects of such atypical sensory behaviors in ASD.
Due to the widespread implication of ANS dysfunction in ASD, it is valuable to understand whether different ANS measures may be correlated with atypical sensory behaviors observed in ASD. Indeed, Woodard et al. (2012) recently reported an association between sensory processing and heart rate responses to a variety of sensory stimuli in children with ASD. We investigated in this study the potential association between PLR and atypical sensory behaviors observed in children with ASD. We hypothesize that some atypical sensory behaviors observed in children with ASD are associated with PLR parameters because both are regulated by the ANS.
Section snippets
Participants
Data on frequently observed atypical sensory behaviors in children with ASD were collected from a group of children who participated in a PLR study (Daluwatte et al., 2013). Children with ASD (referred to as the “ASD” group) were recruited from regional autism clinics and their diagnoses were evaluated and confirmed by the pediatrician and/or neuropsychologist. Children with typical development (referred to as the “TD” group) were recruited from the local community. All children in the TD group
Results
The obtained Cronbach's coefficient of alpha was 0.9 for the ASD group and 0.8 for the TD group, suggesting the total sensory score was a reliable measure of sensory behaviors in both groups. The mean and standard deviations of the total sensory score in the ASD and TD groups were 98.5 ± 16.5 and 131.1 ± 8.8, respectively. The ASD group had a significantly lower total sensory score than that of the TD group (p < 0.05 in Wilcoxon Rank Sum test), indicating greater atypical sensory behaviors in
Discussion
Our results substantiate that children with ASD commonly have significant sensory dysfunction compared with children of typical development. Such sensory dysfunction may be caused or exacerbated by autonomic nervous system dysfunction. We found that ASD children with more atypical sensory behaviors (i.e. lower sensory scores) also had smaller PLR constriction amplitudes (Fig. 1). The fact that atypical sensory behavior was only associated with the PLR constriction underscores the notation that
Conclusion
In summary, we studied associations between PLR with atypical sensory behaviors in children with ASD and typical development. For children with ASD the degree of sensory dysfunction significantly correlated with decreased PLR constriction amplitude. Such correlations were not observed in children with typical development. These results suggest that abnormal sensory behavior is associated with ANS dysfunction in ASD. One limitation of this study was the limited number of sensory questions used.
Acknowledgements
This study was partially supported by National Institute of Neurological Disorders and Stroke (1R21NS070299-01) and Department of Defense Autism Research Program (DoD W81XWH-10-1-0474). Views and opinions of, and endorsements by the authors do not reflect those of the NIH-NINDS or the Department of Defense.
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