Atypical pupillary light reflexes (PLR) has been observed in children with autism spectrum disorders (ASD), which suggests potential autonomic nervous system (ANS) dysfunction in ASD. ANS is also involved in modulating sensory processing and sensory dysfunction has been widely reported in children with ASD. However, the potential association between physiological measurements of PLR and behavioral observations (e.g. sensory behaviors) has not been examined extensively in literature. In this study, we investigated the potential correlation between PLR and frequently observed sensory behaviors in children with ASD. We found a significant association between PLR constriction amplitude and a set of sensory behaviors in the ASD group but not in typically developing children. Children with ASD who showed more atypical sensory behaviors also had smaller PLR constriction amplitudes. A smaller PLR constriction amplitude suggests lower parasympathetic modulation. This observation implies that some atypical sensory behaviors in children with ASD could be associated with decreased parasympathetic modulation.
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 and 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 and 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 and 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 and 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 and 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.
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. Performing the PLS regression with a complete Sensory Profile (Dunn, 2002 and Robertson and Simmons, 2013) is expected to better elucidate the association of different sensory behaviors with measures of ANS dysfunction.
