Sensory Overresponsivity

Home , Prenatal stress, Sensory processing

CHAPTER 19

Timothy W. Soto Vivian M. Ciaramitaro Alice S. Carter

Sensory overresponsivity (SOR) is character- Theoretical Orientations of Sensory Processing ized by extreme or atypical negative reactions to sensory stimuli across one or more sensory Sensory processing issues were first described domains (Dunn, 1999; Interdisciplinary Coun- in 1963 by Anna Jean Ayres, who was trained cil on Developmental and Learning Disorders as an occupational therapist and educational [ICDL], 2005; Lane, 2002; Parham & Mailloux, psychologist, to explain, assess, and treat the 2004; Reynolds & Lane, 2008). Broadly, there behavioral and learning challenges experi- are several hypothesized models that explain enced and expressed by children with various the neurological and behavioral underpinnings disabilities by relating neurological processing of atypical sensory processing. SOR is one par- of and behavioral responses to sensory stimuli ticular manifestation of sensory dysfunction; (Miller, Anzalone, Lane, Cermak, & Osten, it often co-occurs with psychiatric disorders 2007). Ayres (1985) used the term “sensory (i.e., attention-deficit/hyperactivity disorder integration” (SI) to describe these phenomena. [ADHD], generalized anxiety disorder, oppo- Underlying the developmental component of sitional defiant disorder) (Ben-Sasson, Soto, SI theory is the assumption that learning stems Heberle, Carter, & Briggs-Gowan, 2017; Carter, from one’s ability to detect, process, and use Ben-Sasson, & Briggs-Gowan, 2011; Conelea, sensory information from the environment and Carter, & Freeman, 2014) and is characterized from one’s movement to plan and organize be- as a possible symptom of autism spectrum dis- havior (Bundy, Lane, & Murray, 2002). More order (ASD) within the repetitive and restrictive specifically, individuals differ in their way of behavior criteria of DSM-5 (American Psychi- processing information from the visual, audito- atric Association, 2013). SOR also occurs and is ry, tactile, vestibular, proprioceptive, gustatory, associated with clinical impairment without co- and olfactory senses (Huebner & Dunn, 2001). morbid psychiatric or neurocognitive disorders Since Ayres’s initial work in SI, theoretical (Carter et al., 2011). We review in this chapter models and research evidence for this construct the theoretical orientations that have framed have been further developed, and through the SOR as a disorder, and current developmental advancement of such models, the operational- and neurocognitive understandings of sensory ization and clinical characterization of SOR has processing within and across the senses (i.e., become better understood. multimodal processing), and discuss potential The following three described models that

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. future directions for research. have evolved from Ayres’s initial work provide

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the foundation for the primary ways in which sponsivity (SOR), which describes exaggerated, sensory processing, particularly SOR, is cur- rapid onset and/or prolonged reactions to senso- rently conceptualized and measured. First, ry stimulation (e.g., distress from loud noises); Winnie Dunn’s (1997) conceptual model of sen- (2) sensory underresponsivity (SUR), which ex- sory processing combines neurological thresh- plains unawareness or slow response to sensory olds of responding (low or high) with self-reg- input (e.g., not noticing extreme changes in tem- ulation behavioral strategies (passive or active), perature); and (3) sensory seeking (SS), which and includes four hypothesized patterns: sen- describes craving of, and interest in, sensory sation seeking, sensation avoiding, poor reg- experiences that are prolonged or intense (e.g., istration, and sensitivity to stimuli (i.e., SOR). engaging in repeated, rhythmical movements) The model suggests that individuals with low (ICDL, 2005; Miller, Anzalone, et al., 2007). neurological thresholds need less stimulation These patterns are not mutually exclusive and than those with high neurological thresholds to may co-occur in individual children across notice and respond to input. Indeed, high levels sensory modalities (Baranek et al., 2006; Liss, of stimulation may be aversive for individuals Saulnier, Fein, & Kinsbourne, 2006). For our with low neurological thresholds. Individuals purposes in this chapter, while the previously with active self-regulation strategies attempt to stated terms are used when referencing specific control sensory input through active behaviors, studies, the term “sensory dysfunction” is used whereas those with passive self-regulation strat- to describe abnormal sensory processing in a egies respond to the input as it occurs. Varia- general sense. tions of these four patterns are common in the broader population and do not always represent dysfunction. Mechanisms Underlying Sensory Dysfunction Second, Baranek, Reinhartsen and Wan- namaker (2001) developed a model of sensory Although sensory dysfunction may involve processing, which postulates that hyper- and hypersensitivity, hyposensitivity, or an atypi- hyporesponsive sensory modulation behavioral cal interaction and/or integration of informa- patterns may result from shifts in two sensory tion between sensory systems, the majority of processing thresholds: sensory aversion and studies considering the neural basis of sensory sensory orienting. According to their model, dysfunction in developmental disorders have optimal engagement in play and other activi- focused on a single sensory modality and on ties is determined by the width between the two neural mechanisms underlying hypersensitiv- thresholds. Moreover, Baranek and colleagues ity, or SOR. In SOR, behavioral responses to theorize that the width between the orientation sensory stimuli across one or more sensory do- and aversion thresholds is determined by both mains are exaggerated or negative (Dunn, 1999; child characteristics (e.g., attention, affect) and ICDL, 2005; Lane, 2002; Parham & Mailloux, external factors (e.g., environmental and con- 2004; Reynolds & Lane, 2008; Zero to Three, textual features, caregiver interactions). They 2016). This may arise from the nervous system further suggest that this optimal band of en- overenhancing or failing to weaken neural re- gagement may be narrower in individuals who sponsiveness to sensory input. have sensory dysfunction (e.g., children with SOR or autism), leading to variations and fluc- Atypical Sensory Adaptation tuations in responses. Third, and more recently, Miller, Anzalone, Evidence suggests that neural mechanisms for and colleagues (2007) proposed a diagnostic weakening neural responses to sensory input, classification of sensory dysfunction called sen- sensory adaptation, may be dysfunctional in sory processing disorder (SPD), which includes several disorders when SOR is comorbid, such three patterns: (1) sensory discrimination disor- as in children with ASD, and individuals with der (SDD)—difficulty processing and/or inter- social anxiety or schizophrenia. Adaptation is preting sensory information; (2) sensory-based a powerful mechanism, allowing our nervous motor disorder (SMBD)—a motor challenge systems to remain most sensitive and respon- with an underlying sensory basis, such as pos- sive to novel, nonredundant, information via a tural disorder and dyspraxia; and (3) sensory weakening or dampening of responsiveness to modulation disorder (SMD). SMD disorder is repeated, redundant stimuli. For example, adap-

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. classified into three types: (1) sensory over-re- tive mechanisms contribute to our ability to dis-

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tinguish between many exemplars of similar study, 11-year-old children were asked to dis- faces (Clifford & Rhodes, 2005). Adapting to criminate two facial identities when they had or noninformation stimuli also helps to highlight had not been previously adapted to an opposite the information in our environment of the high- identity face. Exposure to a given face identity est behavioral relevance, in which the allocation biased perception, resulting in an aftereffect of limited attentional and processing resources biased toward the opposite identity face. This should be optimized. Thus, a failure of adap- design allowed investigators to determine the tation maintains heightened responsiveness to degree of adaptation to faces independent of stimuli, failing to adjust the gain or sensitivity the ability of children to discriminate between to sensory inputs. A failure of adaptation also faces. While face identification was unimpaired limits the reprioritization of sensory process- in children with ASD—they could discriminate ing resources and the redirecting of attention to facial identities as well as controls—they exhib- allow recent spatial and temporal information ited weaker adaptation to faces. Interestingly, and sensory context to shape perception. Fi- there was a significant correlation between the nally, a failure of adaptation impairs short-term strength of adaptation and autistic symptom- sensory plasticity across sensory domains. atology, with weaker adaptation associated with Early on, before sensory processing disor- stronger symptomatology. ders were included in DSM-5 diagnostic crite- Webb and colleagues (2010) extended these ria for ASD, evidence suggested dysfunctional basic findings of atypical, weakened adapta- mechanisms of sensory adaptation in children tion to faces to a younger age group, toddlers with SOR, children who may have also suffered (18–30 months). To study this younger cohort, with ADHD, obsessive–compulsive disorder, or they used a standard developmental paradigm depression. Unlike controls, 5- to 12-year-olds of habituation (reviewed in Colombo & Mitch- with SOR showed a weaker reduction in the am- ell, 2008) and monitored changes in looking plitude of evoked brain responses, the P50 com- time with repeated stimulus presentation. Tod- ponent of the auditory evoked response poten- dlers with more severe autism symptomatology tial (ERP), following presentation of auditory showed a more severe reduction, or slowing, of stimulus pairs (Davies, Chang, & Gavin, 2009; habituation rates, or adaptation to faces but not Davies & Gavin, 2007). Auditory paired stimuli to houses. Slower rates of learning about faces allow the measurement of strength of adaptation (i.e., slower habituation) correlated with poorer or “sensory gating,” the weakening of responses social skills and verbal ability. to redundant or irrelevant information. Not only Given the findings of atypical adaptation in did children with SOR show a weakened abil- ASD, and in particular the differential findings ity to filter out repeated or irrelevant auditory for social versus nonsocial stimuli, one must information compared to controls, but unlike also consider the influence of atypical atten- controls, the capacity for sensory gating did not tion on such findings. Previous studies in adults improve with age (Davies & Gavin, 2007; Da- suggest that attention and adaptation can inter- vies et al., 2009). In adults, greater SOR symp- act. For example, attending to a low-level visual tomatology was associated with weaker or less feature, such as visual motion, can enhance efficient sensory gating, as indicated by weaker adaptation to visual motion for attended to suppression of brain responses (P50 and N100 stimuli relative to weaker adaptation under con- ERP components) to auditory stimuli (Kisley & ditions of passive viewing (Rezec, Krekelberg, Cornwell, 2006). & Dobkins, 2004). At the neuronal level, evi- Dysfunctional mechanisms of sensory ad- dence suggests that attention to low-level visual aptation also have been documented in several features, such as orientation, may increase the disorders that also exhibit SOR, most notably in adaptability of neurons, with more pronounced not only ASD and schizophrenia, both of which effects of attention on adaptation as one ascends are more prevalent in males, but also in anxiety, the visual hierarchy (see Boynton, 2004, for a which is more prevalent in females. For exam- review). Attention has also been shown to in- ple, male children with ASD show a reduction crease the gain of adaptation for more complex in adaptation to high-level visual information, visual stimuli, such as faces (e.g., Rhodes et al., the social cues contained in facial identity, 2011). Importantly, Ewing, Leach, Pellicano, compared to age- and ability-matched (verbal Jeffery, and Rhodes (2013) found that the re- and nonverbal) typically developing boys (Pel- duced adaptation to faces seen in children with

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. licano, Jeffery, Burr, & Rhodes, 2007). In this ASD (ages 8–16 years) was not driven by an un-

derlying difference in the quantity or quality of al adaptation to emotional information early in attending to facial stimuli. pediatric social anxiety disorder warrants fur- Dysfunctional mechanisms of adaptation ther investigation. also manifest in adults with ASD, in whom ad- Complementary studies in animals investi- aptation to low-level sensory input such as au- gating the role of stress in sensory processing ditory loudness is reduced (Lawson, Aylward, dysfunction are providing important insights. White, & Rees, 2015) and the magnitude of For example, prenatal stress can yield subopti- reduced adaptation, as quantified by a reduced mal sensory processing for tactile and vestibu- BOLD signal following fMRI adaptation, can lar stimuli in neonatal monkeys (Schneider et correlate with individual differences in autistic al., 2017) and weakened adaptation to repeated traits (Ewbank et al., 2015). However, the dys- tactile stimuli in adult monkeys (Schneider et functional adaptation seen in adults with ASD al., 2008). Tactile overreactivity and poor ves- may not always be carried over, or maintained, tibular control in neonates were associated with from childhood, as compensatory mechanisms dysfunctional dopamine and serotonin regula- may come into play over the course of develop- tion. Greater sensory dysfuntion was linked to ment. For example, despite reduced adaptation the presence of a genetic variant for serotonin, to facial identity in children with ASD, adults the s allele genotype, rh5-HTTLPR, and to with ASD show facial adaptation effects similar greater upregulation of dopamine, D2R, bind- to those found in controls (Cook, Brewer, Shah, ing in the striatum, a possible compensatory & Bird, 2014). Importantly, although behavioral mechanism for low levels of synaptic dopamine differences in face adaptation were not found (Schneider et al., 2017). Interestingly, there was in adults, there may be underlying differences a significant relationship between D2R binding in neuronal responses that fail to reach thresh- in the striatum of the adult monkey and sen- old to manifest as overt behavioral differences sory functioning in the neonate, but only for or, alternatively, adults may be solving the task animals carrying the s allele for the serotonin differently, yielding the same behavior but via transporter genotype. These results suggest that utilization of different underlying mechanisms. mechanisms contributing to sensory processing Finally, dysfunctional adaptation has been dysfunction may involve complex interactions documented in other disorders that are frequent- between the dopamine and serotonin systems. ly comorbid with SOR, such as anxiety disor- Future work in animals and humans is required ders. Individuals with social anxiety disorder to identify the factors that contribute to main- display a persistent fear and anxiety in social or taining sensory dysfunction throughout devel- performance situations (DSM-5; American Psy- opment, from childhood into adulthood. chiatric Association, 2013). It has been suggest- Likewise, adults with schizophrenia spec- ed that the negative biases and hypervigilance trum disorders exhibit atypical adaptation to toward social stimuli seen in social anxiety (see auditory (e.g., Adler, Waldo, & Freedman, 1985) Heinrichs & Hofmann, 2011, for a review) may as well as visual and somatosensory (e.g., An- be perpetuated by weakened adaptation to emo- drade, Butler, Peters, Molholm, & Foxe, 2016) tional information, allowing the maintenance stimuli. It has been suggested that dysfunction- of enhanced sensitivity and overresponsiveness al adaptation may be a useful endophenotype to emotional information. In anxious children, for schizophrenia (Gottesman & Erlenmeyer- threatening emotional facial expressions en- Kimling, 2001). As highlighted by Foxe and hance brain responses, as measured by event- colleagues: “As an endophenotype, adaptation related potentials (Hum, Manassis, & Lewis, would lie closer to the ‘shared genetic risk’ con- 2013; Kujawa, MacNamara, Fitzgerald, Monk, tributing to the clinical state while being geneti- & Phan, 2015). Social anxiety status in adults cally less complex than higher-order symptoms moderates the processing of emotional facial and easier to objectively measure” (Andrade et expression, such that adults high in social anxi- al., 2016, p. 11). The developmental origins of ety show enhanced brain responses (greater such dysfunction requires further exploration. amplitude steady-state visual evoked potentials [ssVEPs]) to threatening compared to happy Atypical Multisensory Integration or neutral faces, an enhancement not seen in adults low in social anxiety (Weiser, McTeague, The previously discussed evidence provides a & Keil, 2011). The emergence of negative per- compelling mechanism, weakened adaptation,

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. ceptual biases and mechanisms of dysfunction- which may underlie some aspects of SOR oc-

curring in individuals whether or not they also of the principle of inverse effectiveness, which suffer from ASD, social anxiety, or schizophre- predicts maximal integration across the senses nia. Weakened adaptation could account for when individual stimuli are only minimally SOR in any sensory domain: visual, auditory, effective (at or below threshold) if presented tactile or olfactory. However, adaptation studies individually. Most recently, researchers have to date have mostly focused on a given sensory begun to consider how stimulus intensity, or the domain in isolation. Yet our experience of the principle of inverse effectiveness, interacts with world is not one of disparate and unrelated sen- other factors influencing interactions across the sory events, which must be effortfully linked; senses, namely, the spatial (Nidiffer, Stevenson, rather it is one of integrated percepts. We do not Fister, Barnett, & Wallace, 2016) and/or tem- need to piece together the red color, the sweet poral (Fister et al., 2016) constraints governing taste, and the crunch to figure out that we are multisensory integration. eating an apple. We take for granted our ability A growing body of evidence suggests that to integrate information seamlessly across our mechanisms of multisensory integration may be senses, an integration that aids us in everyday dysfunctional in several disorders when SOR is activities. For example, at a noisy party, we tend comorbid, such as in individuals with ASD and to attend to the lips of the person speaking be- schizophrenia spectrum disorders. Thus, in ad- cause the visual information we obtain is cor- dition to problems in adaptation, dysfunctional related with the speech sounds being produced, interactions across sensory domains may be an and this can help us understand the speech bet- important factor to consider as an underlying ter. It is via the proper working of mechanisms mechanism contributing to SOR. of multisensory integration that we improve our In the realm of temporal coincidence, a rela- ability to perceive sensory information, such as tively small window in time, the temporal bind- our ability to comprehend speech in noisy en- ing window, indicates the likelihood that two vironments. stimuli across sensory modalities will be per- Furthermore, it is important to note that in- ceived as synchronous. The temporal binding formation in one sensory domain can interact window reflects individual differences in mul- with and influence our experience of another tisensory integration and can be highly vari- sensory domain. For example, a concurrent able across individuals (Stevenson, Zemtsov, sound can enhance visual responsivity, improv- & Wallace, 2012). The narrower the temporal ing visual contrast detection and altering neu- binding window, the fewer paired stimulus rophysiological signals in the alpha range (8–12 events are perceived as synchronous, yielding Hz) over occipital, or visual, cortical areas, a stronger ability to correctly distinguish asyn- and decreasing beta-band (14–20 Hz) coupling chronous from synchronous inputs. Thus, indi- between occipital and temporal cortical areas viduals with less reliable temporal processing, (Gleiss & Kayser, 2014). Thus, enhancing re- or a broader temporal binding window, exhibit sponsivity in one sensory domain, as is the case weaker multisensory integration. in SOR, could potentially yield atypical pro- In a recent study, Stevenson and colleagues cessing in a second sensory domain, and atypi- (2014) compared performance on several multi- cal interactions and integration across sensory sensory temporal processing tasks to relate the domains. efficiency of multisensory temporal processing Interactions across sensory domains are gov- with deficits in audio–visual speech integration. erned by rules optimizing sensory integration Children with ASD were compared to typically to enhance perception. Stein and colleagues developing controls (6- to 18-year-olds) across (Meredith & Stein, 1986; Stein, Huneycutt, & multiple multisensory tasks involving simple Meredith, 1988; Stein & Meredith, 1993) first and more complex visual and auditory stimuli. outlined these rules from neurophysiological In general, as stimulus complexity increased, evidence governing multisensory integration children showed less precise temporal process- in the superior colliculus: (1) spatial coinci- ing. Children with ASD showed a speech-spe- dence: inputs from different senses are spa- cific deficit in multisensory processing, with tially aligned; (2) temporal coincidence: inputs the strength of audio–visual speech binding from different senses occur synchronously in correlating with low-level multisensory tempo- time; and (3) weak individual inputs: inputs ral processing. from different senses are suboptimal, below, Deficient multisensory integration has also

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. or near threshold. This last rule is an example been found in adults diagnosed with schizo-

phrenia, who demonstrate reduced susceptibil- gration changes in development. Whereas the ity to multisensory illusions, indicative of less younger cohort of children with ASD showed efficient multisensory integration (Stekelen- severe deficits in the multisensory integration burg, Maes, Van Gool, Sitskoorn, & Vroomen, of seen and heard speech, such a deficit was ab- 2013; Vanes et al., 2016). sent in the older cohort of children with ASD, Importantly, studies find large individual who were entering adolescence. It remains to variability in the strength of multisensory inte- be seen whether such an amelioration in be- gration, especially for the integration of high- havior is accompanied by an amelioration in level, complex, social stimuli such as faces and neuronal responsiveness to multisensory input. voices. Thus, a classic paradigm used to study Furthermore, in children with ASD, the defi- multisensory processing is the McGurk effect, cits in speech recognition were more severe as in which there is a discrepancy between visual background noise increased, a condition known speech-related cues (lip movement) and audi- to improve speech recognition in typical con- tory speech-related cues (sounds), which yield trols (e.g., Ross, Saint-Armour, Leavitt, Javitt, a novel percept that combines information from & Foxe, 2007). Thus, the sweet spot yielding the two sensory channels (McGurk & MacDon- the most effective and strongest multisensory ald, 1976). Recent work in adult controls who integration within the temporal constraints of do not evidence psychopathology or neurode- seen and heard speech depends on the salience velopmental disorders suggests large individual of the sensory input, altered in this experimen- differences in the strength of the McGurk ef- tal design by embedding stimuli in noise. The fect at both behavioral (Mallick, Magnotti, & absence of such a sweet spot of enhanced in- Beauchamp, 2015) and neuronal levels (Nath & tegration in ASD may be one consequence of Beauchamp, 2012). Children (ages 6–16 years) overresponsivity to sensory input altering the with ASD also tend to show less efficient mul- dynamic between the spatial and temporal con- tisensory integration for high-level stimuli, straints involved in multisensory interactions as seen by a decreased susceptibility to the and the influence of stimulus salience on such McGurk effect (Gelder, Vroomen, & van der constraints. The behavioral and neuronal de- Heide, 1991; Smith & Bennetto, 2007). Inter- velopment of such influences warrant further estingly, studies tend to find enhanced or un- investigation. impaired multisensory processing for simple, or nonsocial, multisensory stimuli compared to impaired processing for more complex, social, Measurement and Assessment multisensory stimuli, such as those used for the of Sensory Processing McGurk effect (e.g., Bertone, Mottron, Jelenic, & Faubert, 2003). However, some studies indi- Various measures of sensory processing, in- cate that children with ASD (7- to 16-year-olds) cluding SOR, have been developed from these may be less efficient at multisensory integra- conceptual models. The most common measure tion even for simple, nonlinguistic, and non- of sensory processing in children is the parent facial stimuli at behavioral and neuronal levels questionnaire, for example, the Sensory Profile (Brandwein et al., 2013). Thus, the complexity (Dunn, 1999), the Short Sensory Profile (McIn- of the information, not just stimulus intensity or tosh, Miller, Shyu, & Dunn, 1999), and the Sen- the temporal and spatial relationships between sory Experiences Questionnaire (Baranek et stimuli, can provide a detriment or benefit to al., 2006). A meta-analysis (Ben-Sasson et al., sensory processing, worsening or enhancing 2009) revealed that most studies of sensory pro- sensitivity. cessing in ASD rely on the Sensory Profile or Finally, one must take into account the dy- adapted versions of the Sensory Profile, specifi- namic nature of the developing system, a con- cally, the Infant–Toddler Sensory Profile (ITSP; sideration that is often difficult to tease out Dunn, 2002) for children ages 7–36 months old. given the large age range of children included However, alternative parent-report measures in most studies. In a comprehensive study, in- of sensory responses have been used (e.g., Ba- volving a large sample of 84 children with ASD ranek et al., 2006; Talay-Ongan & Wood, 2000; and 142 typically developing age-matched con- see Ben-Sasson et al., 2009, for a review). trols, Foxe and colleagues (2015) used a cross- Based on Dunn’s (1997) model, the Sensory sectional design spanning children ages 5–12 Profile was developed and normed on 1,037

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. and 13–15, to consider how multisensory inte- typically developing children ages 3–10 years,

and includes three areas (sensory process- measures phenotypic variation in sensory mod- ing, modulation, and behavioral/emotional re- ulation dysfunction across sensory domains in sponses), nine factor scores (sensory seeking, children ages 4–18 years. Both the observation- emotionally reactive, low endurance/tone, oral al and questionnaire components of the Sensory sensitivity, inattention/distractibility, poor reg- Processing Scale measure sensory processing istration, sensory sensitivity, sedentary, fine variations across an array of sensory experi- motor/perceptual), and four quadrants (low ences, including SOR. registration, sensory seeking, sensory sensitivity, sensory avoiding). The four quadrants of the Sensory Profile are based on Dunn’s previ- Prevalence ously described model of sensory processing. It also measures aspects of emotion, attention, Rates of SOR reported across studies vary and motoric responses to sensation in the en- depending on factors such as chronological vironment. Children with SOR would be rated age, developmental level, modality assessed, as having elevated sensory sensitivity on this response pattern subtype, and method of sen- measure. sory measurement. For example, in a study of The Sensory Experiences Questionnaire sensory symptoms of infant/toddler boys with (Baranek, 1999c; Baranek et al., 2006), an- fragile X syndrome at 9, 12, and 18 months other parent-report questionnaire, measures of age, Baranek, Boyd, Poe, David, and Wat- hypo- and hyperresponsive sensory patterns in son (2007) found risk for or deficient levels of the contexts of daily activities of children be- sensory processing in over 70% of the sample tween ages 6 months and 6 years. The measure when using observational measures (Sensory yields summary scores of these two response Processing Assessment), whereas parent report patterns in social and nonsocial contexts. Un- (Sensory Experiences Questionnaire) yielded like the Sensory Profile, the Sensory Experi- much lower percentages (0% at 9 months vs. ences Questionnaire was validated on typically over 40% at 54 months). Ben-Sasson and col- developing children, as well as children with leagues (2008, 2009) reported that rates of SOR autism and developmental delays (Baranek et ranged from 10–17% for typically developing al., 2006). Children with SOR would be rated as children in an epidemiological study. Of the showing the hyperresponsive patterns. group with elevated SOR symptoms measured The Sensory Processing Assessment (Ba- in tactile and auditory domains, 76.4% demon- ranek, 1999b) is an observational, play-based strated difficulties only in the tactile domain. measure of sensory response patterns (hypo- Similarly, Tomcheck and Dunn (2007) found and hyperresponsiveness) designed for children that 16% of their 3- to 5-year-old typically de- with autism and developmental delays between veloping sample had total sensory scores in the ages 6 months and 6 years. It is administered in “probable to definite difference” range, while a laboratory setting and tests children’s behav- Leekam, Nieto, Libby, Wing, and Gould (2007) ioral responses to social and nonsocial sensory reported that 33% of their typically developing stimuli across three modalities: auditory, visu- sample between ages 3 and 11 years had sen- al, and tactile. Children are rated on the degree sory symptoms. Regardless of the variability in to which they approach and/or avoid novel toys, rates of SOR across studies, as noted by sev- orient to various sensory stimuli in social and eral researchers, a smaller percentage of indi- nonsocial contexts across three sensory modali- viduals with typical development experience ties, habituate to a repeated auditory stimulus, SOR when compared to individuals with ASD and display repetitive and stereotyped behav- (Ben-Sasson et al., 2008; Dahlgren & Gillberg, iors. 1989; Tomchek & Dunn, 2007), and those with The Sensory Overresponsivity Scales, an no other co-occurring psychiatric or neurode- observational measure of SOR for individuals velopmental disorders are often only affected in from age 3 years through adulthood, was ini- one modality (e.g., Ben-Sasson et al., 2009). tially detailed in a pilot study (Schoen, Miller, & Green, 2008) and recently updated and re- named as the Sensory Processing Scale As- Course sessment (Schoen, Miller, & Sullivan, 2014). The Sensory Processing Scale Assessment and Ben-Sasson, Carter, and Briggs-Gowan (2010)

Copyright @ 2019. The Guilford Press. All rights reserved. May not be reproduced in any form without permission from the publisher, except fair uses permitted under U.S. or applicable copyright law. Inventory (Schoen, Miller, & Sullivan, 2017) conducted the only known longitudinal, epi-

demiological study documenting the normal evated rates of sensory symptoms compared to developmental course of SOR with 521 typi- typically developing peers. However, the rates cally developing children. They studied sensory in other psychiatric and neurodevelopmental sensitivity, which is a comparable construct to disability groups are not as high as those ob- SOR, as measured by the Infant–Toddler Social served among individuals with ASD. Indeed, and Emotional Assessment (ITSEA; Carter & given the high prevalence of unusual sensory Briggs-Gowan, 2006) at three time points (Year processing in ASD, this has become a criteri- 1: 11–24 months; Year 2: 23–42 months; Year on for the presence of restricted and repetitive 3: 31–51 months) and SOR using the Sensory behaviors in the DSM-5 (American Psychiat- Overresponsivity Scales (Schoen et al., 2008) ric Association, 2013), precluding diagnosis of during the fourth assessment period, when chil- both ASD and SOR. dren were ages 7–10 years. Results indicated The most substantial knowledge of sensory stability in ITSEA sensitivity (i.e., SOR) scores symptoms in individuals with ASD comes from across the first 3 years, with initial infant sensi- research involving samples of preschoolers tivity patterns and change in sensitivity through through adults. Several studies note the high toddlerhood/preschool years predicting SOR prevalence of sensory differences in preschool- status in elementary school-age children. Chil- ers with ASD compared to those with typical dren with elevated overresponsivity in elemen- development, ranging from 58 to 100% (e.g., tary school had higher levels of sensitivity in Dahlgren & Gillberg, 1989; Provost, Crowe, infancy and a unique early trajectory. Addition- Acree, Osbourn, & McClain, 2009; Tomchek ally, 30–33% of children with elevated SOR in & Dunn, 2007; Watling, Dietz, & White, 2001). elementary school showed evidence of higher Two studies (Provost et al., 2009; Watling et al., sensitivity levels in early childhood. Further- 2001) found that preschoolers with ASD com- more, one-third of children with elevated SOR pared to age- and gender-matched preschoolers at ages 1–2 years old, had SOR at school age, and with typical development differed on eight out more than 50% of children with elevated SOR at of 10 Sensory Profile factors, and 83% of the 3- agd 3 years had SOR at the elementary school to 6-year-olds with ASD had worse scores on at time point. These results suggest not only per- least one Sensory Profile factor. Moreover, Ba- sistence but also desistance of sensory signs in ranek and colleagues (2006) reported that 69% early childhood. In addition, a large percentage of children with ASD (ages 23 to 80 months) ex- of children in this sample who were identified hibited significant sensory symptoms, whereas as having SOR at the elementary school age Tomchek and Dunn (2007) found that 95% of were not identified early on. This may be evi- 3- to 5-year-olds with ASD had probable or dence of a later onset of SOR or limitations of definite differences on their total Short Senso- the assessment tools. Ultimately, these results ry Profile score. Dahlgren and Gillberg (1989) suggest that additional longitudinal research is reported that 100% of 3-year-olds with autism needed to better understand the development of in their sample had auditory processing diffi- SOR across the lifespan. Moreover, additional culties, whereas Jasmin and colleagues (2009) work is especially needed on the multiple senso- found that 58% of 3- to 4-year-olds with ASD ry modalities in which SOR may emerge across had a Sensory Profile total score in the atypi- time in typically developing children. Indeed, cal range, and 94% had atypical responses on the majority of work on sensory symptoms has at least one item or factor. Ultimately, while been done with individuals who have been di- rates can vary based on the sensory dimensions agnosed with other disorders, and particularly and scores reported, there is a distinction in among individuals with ASD. rates of sensory dysfunction between children with ASD and those with developmental delay or typical development. Furthermore, there Comorbidity are specific differences in SOR presentation between children with typical development, As previously mentioned, sensory symptoms children with developmental delay, and those are not unique to ASD. Individuals with other with ASD. For example, children with ASD clinical and developmental disorders (DD) such demonstrate more extreme hyporesponsiveness as fragile X syndrome, language impairment, than children with other developmental delays ADHD, anxiety disorders, developmental de- (Baranek et al., 2006; Miller Reisman, McIn-

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Although children with ASD are not generally velopmental delays, possibly showing the early more hyperresponsive than those with other de- emergence of a hyporesponsive pattern of sen- velopmental delays (Baranek et al., 2006; Rog- sory processing; (2) were more likely to show ers & Ozonoff, 2005), they are more likely to aversive responses to social touch, perhaps demonstrate co-occurring hyporesponsiveness symptomatic of an emerging hyperresponsive and hyperresponsiveness than children with pattern; and (3) engaged in more mouthing of other developmental delays (Baranek et al., objects, perhaps an early symptom of a senso- 2006). Therefore, their SOR symptoms may be ry-seeking pattern. Interestingly, these sensory more likely to come to the attention of profes- symptoms were apparent prior to the time that sionals due to their co-occurrence with other most parents had any concerns about their in- sensory symptoms. fants who were later diagnosed with ASD. Wat- In studies assessing SOR across older and son and colleagues (2011) postulated that Ba- broader age ranges of individuals with ASD, ranek’s findings suggest that abnormalities in prevalence tends to be higher than that in early developing sensory processing symptoms younger and narrower age ranges of samples. in infants with ASD may lead to consequences Sensory difficulties were reported in 94% of a in other developmental domains. sample of 3- to 11-year-olds with ASD (Leekam, While Baranek’s (1999a) study highlights Nieto, Libby, Wing, & Gould, 2007; Study 1), the importance of early detection of SOR in 92.5% of 200 children and adults with ASD be- children with ASD, there are several method- tween ages 32 months and 38 years (Leekam et ological weaknesses that should be considered al., 2007; Study 2), and 85% of 99 items on the when interpreting the results. For example, Sensory Profile for 3- to 13-year-olds with ASD video samples may be a narrow representation were endorsed for sensory difficulties com- of children’s behaviors; that is, parents preselect pared to a typically developing control group the situations that may favor pleasant situations (Kientz & Dunn, 1996). Less is known about and special achievements, and avoid videotap- the prevalence of sensory symptoms during ing children during uneventful, unpredictable, the first 2–3 years of life for those who will re- or adverse conditions—a process that may ob- ceive an ASD diagnosis, although Ben-Sasson scure certain symptoms. Moreover, sampling and Carter (2013) found that including sensory a range of situations in 10 minutes provided a regulatory markers in addition to social com- cross-section of age and behavior but did not munication and repetitive behaviors enhanced allow for the detailed analyses of infrequent or screening for children with ASD at 12 months context-specific situations. In addition, some of of age. Baranek and colleagues (2006) found the behaviors listed as sensory, such as requiring that 69% of parents of children with ASD be- multiple prompts to respond to a name call, may tween ages 23 and 80 months reported sen- reflect specific deficits in social motivation, sory difficulties on the Sensory Experiences such that additional nonsocial underresponsive- Questionnaire, but this age range spans from ness is necessary to confirm the presence of a toddlerhood through school age. Other studies sensory, rather than social, symptom. Further have indicated that about 83% of toddlers with research is needed to determine the effects of ASD under the age of 3 had sensory problems, various contexts on the specific behaviors of whereas 65% of toddlers and preschoolers with interest in this study, using more rigorous meth- developmental delay had typical Short Sensory odological designs (e.g., longitudinal), carefully Profile scores (Wiggins, Robins, Bakeman, & matched comparison groups, and stimuli that Adamson, 2009). can distinguish atypical sensory from atypical Through a retrospective video analysis of social patterns of responding. sensory–motor behaviors of toddlers with ASD, Baranek (1999a) found that sensory symptoms differentiate infants who will later be diagnosed Treatment with autism from infants with other developmental delays or with typical development. Spe- Similar to the measurement of sensory pro- cifically, Baranek found that infants later diag- cessing, interventions designed for SOR also nosed with autism (1) required more prompts stem from Ayres’s work on sensory integration before responding to a name call and were less (Ayres, 1972, 1979; Koomar & Bundy, 1991; likely to orient to visual stimuli introduced into Parham & Mailloux, 2004). More specifical-

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principles from neuroscience, developmental Anzalone (1997) define three elements to a sen- psychology, occupational therapy, and educa- sory integrative approach when working with tion: (1) Sensorimotor development is foun- children with ASD: (1) helping parents under- dational for learning; (2) the interaction of the stand their child’s behavior and foster nurturing individual with the environment shapes brain relationships; (2) helping parents and teachers development; (3) the nervous system is capable modify the environment so that it matches the of change (i.e., plasticity); and (4) meaningful child’s sensory needs; and (3) helping children sensory–motor activity can change circuitry. organize responses to sensory input. Although new findings and knowledge dem- Although sensory integration therapy is onstrate that the nervous system is even more prevalent in practice, very few studies of this complex and integrated than Ayres and others approach or similar occupational therapy tech- believed at the time, many of the principles on niques with children with and without ASD which Ayres built the theory of sensory integra- have been shown to be efficacious in reducing tion are still central to the application of current sensory symptoms. Recent systematic reviews sensory integration interventions. This knowl- examining the efficacy of sensory integra- edge has been strengthened by basic research tion therapy (clinic-based interventions) and demonstrating that structural and physiologi- sensory-based (classroom-based) interventions cal, as well as molecular and cellular, changes broadly indicate that clinic-based interventions in neural functions are possible, and that mean- for children with ASD following manualized ingful sensory–motor activities can change cir- protocols show more promise than school-based cuitry due to plasticity (Merzenich et al., 1984; interventions that are often specifically tailored Greenough, Black, & Wallace, 1987; Kandel for each child (Case-Smith, Weaver, & Fristad, & Jessell, 1995; Kempermann & Gage, 1999; 2015; Lang et al., 2012). Studies of sensory- McKenzie, Nagarajan, Roberts, Merzenich, & based interventions indicate limited efficacy. Byl, 2003). Miller, Coll, and Schoen (2007) conducted a Sensory integration therapy aims to focus di- randomized controlled trial on children with rectly on the neurological processing of sensory sensory modulation disorder (including SOR) information as a foundation for learning higher- and found positive effects for sensory integra- level (motor or academic) skills. Through so- tion therapy on child performance using goal matosensory and vestibular activities actively attainment scaling. Although small randomized controlled or sought out by the child, the nervous controlled trials resulted in positive effects for system is thought to be able to better modulate, sensory integration therapies, additional rigor- organize, and integrate information from the ous trials using manualized protocols for sen- environment, which in turn provides a founda- sory integration therapy are needed to evaluate tion for further adaptive responses and higher- effects for children with and without ASD and order learning. Other necessary components of sensory processing problems. the sensory integration therapy model include Furthermore, there is a noticeable lag in the a child-centered approach, scaffolding, facili- consensus regarding the merits of the previous- tating progressively more sophisticated adap- ly mentioned sensory interventions due to lim- tive motor responses, and engaging the child ited rigorous methodologically sound research. in affectively meaningful and developmentally Researchers of SOR have offered several poten- appropriate play interactions. Treatment goals tial reasons for such a lag. Schaaf and Miller may center on improving sensory processing (2005) purport that one reason for this lag is that to either develop better sensory modulation as the science of occupational therapy is relatively related to attention and behavioral control, or new compared to fields such as psychology and integrate sensory information to form better medicine, with longer traditions of research and perceptual schemas and practical abilities as trained scientists. Traditionally, training in oc- a precursor for academic skills, social interac- cupational therapy has focused on service deliv- tions, or more independent functioning. ery of practical interventions and only recently Sensory integration approaches have been has begun incorporating research into training. applied specifically to children with ASD, par- Given the treatment-focused lens in which most ticularly via services to remediate behaviors providers are trained, it is not surprising that indicative of sensory defensiveness and intol- most of the reviewed studies include individual- erances (Ayres & Tickle, 1980; Baranek, 1998; ized interventions with very small sample sizes.

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meet the individual sensory needs of the par- cians studying sensory processing disorders ticipants; however, replicability and standard- and neuroscientists studying multisensory pro- ization of treatment is challenging within this cessing. We believe that pursuing translational research framework. Moreover, most of the research in this area can advance both basic studies provide limited follow-up after inter- neuroscience and improve the lives of individu- vention; thus, it is not known whether positive als with SOR, who are clinically impaired by effects are sustained in the long term (Baranek, their hypersensitivities to sensory phenomena. 2002). Ultimately, these methodological short- comings decrease the likelihood of standardiza- tion of and confidence in the efficacy of many REFERENCES sensory treatments for children with SOR. Adler, L. E., Waldo, M. C., & Freedman, R. (1985). Neurophysiologic studies of sensory gating in Conclusions schizophrenia: Comparison of auditory and visual responses. Biological Psychiatry, 20, 1284–1296. American Psychiatric Association. (2013). Diagnostic Individuals differ in their ways of processing in- and statistical manual of mental disorders (5th ed.). formation from the auditory, tactile, vestibular, Arlington, VA: Author. proprioceptive, gustatory, and olfactory senses Andrade, G. N., Butler, J. S., Peters, G. A., Molholm, (Huebner & Dunn, 2001), and sensory dys- S., & Foxe, J. J. (2016). Atypical visual and somato- function occurs when individuals process and/ sensory adaptation in schizophrenia-spectrum disor- or modulate sensory input abnormally. There ders. Translational Psychiatry, 6, e804. is strong evidence that for some individuals, Ayres, A. J. (1963). The development of perceptual– hypersensitivity to specific sensory inputs, as motor abilities: A theoretical basis for treatment of occurs when individuals suffer from SOR, can dysfunction. American Journal of Occupational disrupt learning and interfere with participa- Therapy, 17, 221–225. tion in social relationships and developmentally Ayres, A. J. (1972). Improving academic scores through sensory integration. Journal of Learning Disabili- expected activities. Individuals with a range of ties, 5, 338–343. other psychiatric and neurodevelopmental dis- Ayres, A. J. (1979). Sensory integration and the child. abilities, such as ASD, schizophrenia, obses- Los Angeles: Western Psychological Services. sive–compulsive disorder, and social anxiety Ayres, A. J. (1985). Developmental dyspraxia and adult disorder have increased risk for SOR, but SOR onset apraxia. Torrance, CA: Western Psychological also occurs as a clinically impairing condi- Services. tion in isolation. Unfortunately, the empirical Ayres, A. J., & Tickle, L. S. (1980). Hyper-responsivity literature offers very little information about to touch and vestibular stimuli as a predictor of posi- the clinical course of, or optimal interventions tive response to sensory integration procedures by for, individuals with SOR, especially young autistic children. American Journal of Occupational children. There is a greater evidence base for Therapy, 34, 375–381. individuals with ASD whose symptomatology Baranek, G. (1998). Sensory processing in persons with autism and developmental disabilities: Con- includes sensory hypersensitivities. As recogni- siderations for research and clinical practice. Sen- tion of SOR as a clinical entity has advanced, sory Integration Special Interest Section Quarterly, as evidenced by inclusion in the DC:0–5 sys- 21, 1–3. tem (Zero to Three, 2016), there have also been Baranek, G. T. (1999a). Autism during infancy: A retro- major advances in studying putative neural spective video analysis of sensory–motor and social substrates of sensory dysfunction, including behaviors at 9–12 months of age. Journal of Autism difficulties in adaptation, sensory gating, and and Developmental Disorders, 29(3), 213–224. multisensory integration that can aid in under- Baranek, G. T. (1999b). Sensory Experiences Question- standing SOR. Advances in both questionnaire naire (SEQ). Unpublished manuscript, University of and observational assessments of SOR, as well North Carolina at Chapel Hill, Chapel Hill, NC. as eye tracking and noninvasive brain imaging Baranek, G. T. (1999c). Sensory Processing Assessment for Young Children (SPA). Unpublished manuscript, technologies, offer a plethora of directions for University of North Carolina at Chapel Hill, Chapel future study of mechanisms that may underlie Hill, NC. SOR, as well as mechanisms, mediators, and Baranek, G. T. (2002). Efficacy of sensory and motor moderators of evidence-based interventions. In interventions for children with autism. Journal of 2009, Miller, Nielsen, Schoen, and Brett-Green Autism and Developmental Disorders, 32, 397–422. Baranek, G. T., Boyd, B. A., Poe, M. D., David, F. J., &

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