Introduction stimuli, the inadequate processing of multisensory input

Introduction

To successfully interact with our environment, we need the ability to perceive sensory information from the world and translate those into appropriate actions. However, for successful translation, we first need to organize and interpret the sensory stimuli to be able to form an appropriate response to the environmental demands, such as a movement. For optimal functioning, the sensory system receives information by more than just one sense. Perception is guided by the five sensory systems, vision, audition, olfaction, gustation, and somatosensation +add proprioceptive and vestibular balance and motor. The information we get from those multiple sensory sources can be complementary or redundant; successful sensory integration enables precise perception. Humans are not born with multisensory integration. This ability matures during childhood (Burr & Gori, 2012). While some early stages, such as head orientation towards an auditory stimulus occurs in early infancy (Neil, Chee?Ruiter, Scheier, Lewkowicz, & Shimojo, 2006), other sensory integration processes don’t mature until late childhood (Barutchu, Crewther, & Crewther, 2009; Gori, Del Viva, Sandini, & Burr, 2008).

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Sensory Processing Disorder

Sensory processing disorder (SPD) was first described by A. J. Ayres (1972) after systematic observations while working with children with learning disabilities. Based on Ayres, SPD is characterized by significant difficulties to organize or regulate sensory information by the nervous system. While there are naturally occurring variations in sensitivity and reactivity to sensory stimuli, the inadequate processing of multisensory input as described in SPD manifests in substantial problems in performance that prohibit optimal functioning and create dissonance with the environment (Ayres & Robbins, 2005). In contrast to a healthy, well-organized neural system that can process multisensory information and translate them into appropriate actions, it is assumed that SPD is rooted in an immature sensory system that is inefficient in neuronal signaling and organization. The resulting abnormal perception or experience of the environment or processing in the brain may lead to difficulties / adverse effects/ deficits in development, socio-emotional regulation, and academic performance (Ben-Sasson, Carter, & Briggs-Gowan, 2009).

While there is a growing body of research indicating that sensory dysfunction may qualify as an independent disorder, so far none of the major diagnostic classification systems (e.g., DSM-5, ICD-10) is acknowledging SPD as such (American Psychiatric Association, 2013). Though there is consensus that difficulties in sensory processing occur in children, opponents of the disorder claim that the observed symptoms are non-specific could be explained as comorbid phenomenon of other neurodevelopmental disorder and lack evidence to qualify for an independent diagnosis (Zimmer et al., 2012). So far, only the Diagnostic Classification of Mental Health and Developmental Disorders of Infancy and Early Childhood (DC: 0-3) has included SPD in their manual (Zero to Three, 2005).  Amid this controversy, a large-scale study including 706 typically developing kindergarten children found that an estimated 5.3 – 13.7% of children without other developmental delays meet criteria for SPD based on parent reports (Ahn, Miller, Milberger, & McIntosh, 2004). Additionally, sensory dysfunction is often a comorbid symptom in children with developmental disorders, such as autism spectrum disorder (ASD), as well as children affected by regulatory disorders, such as attention-deficit/hyperactivity disorder (ADHD). These groups show a significantly higher prevalence of sensory dysfunction compared to typically developing children, reported as high as 40 – 80% (Ahn et al., 2004; Kientz & Dunn, 1997).

Comorbidity. The occurrence of “sensory issues” in autism spectrum disorders is common and has been extensively described in the literature (see Ben-Sasson, Hen, Fluss, Cermak, Engel-Yeger, & Gal, 2009 for meta-analysis). Tomchek and Dunn (2007) reported in a study including 562 children between the age of 3-6 years that children with ASD show a significant different sensory pattern compared to matched typically developing children. The groups differed most significant in subcategories of hypo-responsiveness and sensation-seeking. Similarly, another study found a unique pattern of hypo-responsiveness to sensory stimuli in children with autism as young as 5-months, compared to healthy controls as well as children with other developmental disorders (DD), (Baranek, David, Poe, Stone, & Watson, 2006).  On the other hand, hyper-responsiveness manifested quite similar in ASD and DD children and was distinguishable to the neurotypical controls. Additionally, the observed pattern of over-responsiveness was related to estimated developmental age in those two groups (ASD and DD). Since 2013, sensory impairments are included in the Repetitive and Restricted Behaviors Impairment category to diagnose ASD in the DSM-5 (American Psychiatric Association, 2013). But related sensory disabilities are not just comorbid with developmental disorders; atypical processing is as well reported in individuals with schizophrenia, especially in the auditory and visual domain (Javitt, 2009). High sensitivity to sensory processing was found to be correlated to avoidance behaviors in social anxiety disorder (Hofmann & Bitran, 2007).

The Role of Sensitive Periods. Atypical sensory processing is more common in children born preterm (Anday, Cohen, Kelley, & Hoffman, 1989; Kessenich, 2003; Wiener, Long, DeGangi, & Battaile, 1996) as well as previously institutionalized children (Cermak & Daunhauer, 1997; Wilbarger, Gunnar, Schneider, & Pollak, 2010). The increased prevalence suggests that maturation of the underdeveloped nervous system in preterm infants may play a role. Likewise, early adverse experiences, such as caregiver deprivation or lack of optimal stimulation during early development in institutionalized children, seem to be involved in the inefficient organization of sensory information. The importance of sensitive periods for the maturation of sensory pathways has been shown by Hubel and Wiesel (1970). In their landmark studies with cats, they demonstrated that monocular and binocular closure during sensitive periods leads to a significant decrease in neuronal connections of the deprived eye with limited to no recovery. The effect was only observed over a specific developmental timeframe; further, after maturation of the visual system, the experiment caused no detectable effects. But not just early deprivation of sensory experiences impacts developmental trajectories. Earlier stimulation of sensory systems that usually develop later can influence the maturation of others. For example, surgical eye-opening in rat pups on postnatal day (PN) 7, eight days before this occurs naturally, compromises the development of the earlier developing olfactory system (Turkewitz & Kenny, 1985). Moreover, artificial early visual stimulation starting on PN7 alters behavioral changes rat pups usually show about the same time as eye-opening occurs naturally (Kenny & Turkewitz, 1986). This indicates that not only deprivation during sensitive periods can have a significant impact on the maturation of sensory processing. The natural limitation of sensory input during development can be linked to the optimal organization and maturation of other sensory systems. On the other hand, premature stimulation of one system can impair the neurodevelopment of another. Thus, not just deprivation and stimulation, but their timing and the possible hierarchical order of sensory development seem to impact species-typical organization and maturation of sensory processing.

The role of early experiences for sensory integration in human development has been shown, for example, with the McGurk effect (McGurk & Power, 1980). The effect occurs when conflicting sensory input is given. For example, a subject listens to a spoken phoneme, while another phoneme is visually pronounced by a speaker. The majority of participants reports hearing a third phoneme, a mix between the auditory and the visually processed one. This illusion, caused by multisensory fusion can be observed in typically developing children as well as in deaf-born children who received cochlear implants during early infancy. However, children with congenital deafness whose hearing was restored after 30 months of age showed a significant visual dominance in the paradigm, indicating that the sensory integration as observed in the McGurk effect is not innate but develops based on experience during early childhood (Schorr, Fox, van Wassenhove, & Knudsen, 2005).

 

Hence, sensory processing disorders may hint to a neuromaturational problem during sensitive periods such as deprivation or lack of stimulation or so.

Not clear whether those effects are permanent or transient if children affected cam catch up (therapy indicates at least a bit).

 

Developmental Profile

 

Count risk factors such as preterm birth, male gender, birth weight

Ask prevalence is high in preterm born infants and they can be specially targeted, comorbidity doesn’t play so much a role, really want to exclude comorbidity as otherwise not able to see as separate disorder, data available from preterms as interesting population to study, and there is ample evidence that maturation plays a huuuuuuge role we will use them as proxy for this developmental profile for SPD will

 

 

Infancy. Abnormal sensory processing is diagnosed in children with behavioral or developmental impairments. Several prospective studies aimed to identify early markers for the later development of abnormal sensory integration. Rahkonen and colleagues (Rahkonen et al., 2015) followed 42 preterm infants over the course of two years. White and grey matter anomalies of MRI scan data, obtained at full-term equivalent age were compared to level of neuromaturation and the Infant Toddler Sensory Profile (ITSP) at two years of term-corrected age. As reported in older children before (Wickremasinghe, Rogers, Johnson, Shen, Barkovich, & Marco, 2013), patterns of low registration were of high prevalence for abnormal sensory behavior. Moreover, 52% of all participants showed an atypical sensory profile in the ITSP, deviating at least one standard deviation from the normative sample. Abnormal sensation seeking at two years of corrected age was significantly related to observed atypical structures in white and gray matter of the term-equivalent age MRI. A large-scale study with 243 preterm infants showed as well that the low registration factor from the ITSP has a high prevalence at two years of age (Eeles, Anderson, Brown, Lee, Boyd, Spittle, & Doyle, 2013b). The factor includes items such as “Doesn’t notice when arm is touched,” “Doesn’t perceive facial expressions,” “Decreased awareness of pain and temperature” (Dunn & Brown, 1997). Abnormal scores on the low registration factor were related to metal and psychomotor developmental indexes and predicted poorer language outcomes. Preterm children showed more abnormal patterns on the ITSP compared to term-born infants. Additionally, male sex and abnormal white matter structures in MRI indicated higher risk for impairments in sensory processing at two years of age (Eeles, Anderson, Brown, Lee, Boyd, Spittle, & Doyle, 2013a). Only one study used the Test of Sensory Function in Infants (TSFI), which allows for increased accuracy as it does not only rely on parental report as the ITSP. Using the TSFI, Chorna et al. (2014) report that 82% of the 72 infants included showed abnormal sensory processing in at least one test score. Ocular-motor control was linked to white matter injuries, and overall, male gender, white matter anomalies, and gestational age were related to poorer outcomes in sensory processing.

Preschool Age. A meta-analysis suggests that the reported symptoms of sensory dysfunction increase until the preschool age in individuals later diagnosed with ASD (Ben-Sasson, Hen, et al., 2009). But only a few studies look at this age group in preterm or normally developing children. In a cross-sectional study, Adams and colleagues (2015) found that abnormal sensory integration is more prevalent in preschool children that were born preterm (37%) compared to term-born children (12%). Further, poor sensory processing was associated with executive function evaluated based on performance in a six tasks battery.

School Age. In a cross-sectional study following 107 children from infancy (1-4 years) to childhood (4-8 years) the prevalence of sensory processing impairments was stable (Wickremasinghe et al., 2013). While the occurrence of abnormal scores in tactile, auditory, and vestibular sensory systems was increased for children that were born premature, no other neurodevelopmental risk factors could be identified. In a sample of male 8- to 12-year-olds Chang et al. (2014) used diffusion tensor imaging (DTI) to investigate the role of whiter matter. Children with diagnosis of SPD showed lower in connectivity between white matter tracts in parietal-occipital regions compared to healthy controls. The region is associated with perception and sensory integration. Further, the connectivity of white matter tracts was significantly related to auditory and attention scores, as well as working memory performance. Those findings were replicated in a mixed-gender cohort, relating white matter microstructure in the parietal region with direct measures of sensory processing in auditory and tactile systems (Chang et al., 2016). Sensory gating refers to the brain’s ability to integrate complementary stimuli, hence a mechanism to attenuate sensitivity to sensory stimuli and can be detected using EEG. Davies and Gavin (2007) reported that school-aged children with SPD showed significant less sensory gating than typically developing children. Further, age and sensory gating were significantly associated, but only in typically developing children. Based on EEG data the researchers were able to predict psychopathology with an accuracy of 86%. Further investigation of sensory gating showed that compared to adults and to typically developing children, children with SPD followed a different maturational pattern and repeatedly failed to selectively filter sensory stimuli (Davies, Chang, & Gavin, 2009).

 

Neuronal Substrates

Most studies that compare biomarkers with either parental reports or direct assessment of sensory processing in children find association between white matter structure and sensory functioning. It can be assumed that high-risk abnormalities can be detected in MRI scans at birth and linked to later impairments in sensory processing based on ITSP factors such as low registration and sensation seeking (Chorna et al., 2014; Eeles et al., 2013a; Rahkonen et al., 2015). Those results are consistent with studies using DTI technology, identifying microstructural differences in white matter tracts in the posterior cerebral regions in school-aged children that are directly liked to alterations in sensory processing (Chang et al., 2014; Chang et al., 2016; Owen et al., 2013). Accordingly, abnormal white matter structure could be associated with the etiology of SPD, and future studies should investigate predictive value for development and severity of diagnosis. Also, two studies indicate that the development of sensory gating significantly differs in children with SPD. Further investigation into EEG patterns and their developmental trajectories in sensory processing disorders could establish this as a promising and cost-efficient biomarker.

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