Sensory behaviours relation to core features

4.1.3.1 Why the relation to core features is important to study:

The large proportion of research on sensory behaviours focuses on the pattern or number of behaviours in individuals with ASD in comparison to typically developing individuals or other clinical conditions as described in Section 4.1.1. Very little research has focussed on the relation between the core features of ASD and sensory behaviours. This is important to consider for several reasons. Firstly, the sensory system is the system in which individuals acquire information about the world, which in turn allows the individuals to respond and adapt to their environment (cf Hilton et al., 2010), impairments in sensory functioning may therefore have huge impacts on an individual’s ability to interact with others. This has been argued as a reason to consider sensory behaviours as a primary impairment in ASD (e.g. Baranek, Parham, & Bodfish, 2005; Iarocci & McDonald, 2006; Rogers & Ozonoff, 2005) and research has found early sensory behaviours in infancy and toddlerhood predict poorer language and social interaction abilities and later ages (DeGangi, Breinbauer, Roosevelt, Porges, & Greenspan, 2000). A strong relation between sensory and social interaction would support this proposal and highlight a key area for further exploration of the aetiology of ASD. Equally, no evidence of such a relation may indicate that the social impairments in ASD are independent of the sensory behaviours present in the majority of individuals with ASD or that sensory may be best categorised as a repetitive behaviour.

Secondly, one possibility is that sensory features have been overlooked because of the strong assumption that they are “just” one type of repetitive behaviour that is seen in ASD. The conceptual overlap between sensory and repetitive behaviours is important to consider. The description of the repetitive and restricted behaviour domain in DSM-IV-TR (APA, 1994) such as “stereotyped and repetitive motor mannerisms” and “persistent preoccupation with parts of objects” allow sensory behaviours to also be captured within the description of Autistic Disorder (DSM-IV-TR, APA, 1994) and such the sensory behaviours are categorised within the non-social aspects of ASD. In addition, the repetitive nature of the behaviours seen in ASD such as motor stereotypies and self-injury have been predicted to provide an intrinsic sensory stimulation to the individual (Lovaas et al., 1987). However, the relation or lack of association between sensory and repetitive behaviours is important for diagnostic criteria, pathogenesis and treatment strategies as described by (Boyd et al., 2010, p. 2):

101 Strong relationships (as indicated by a high degree of co-occurrence) may

suggest that additional descriptions of sensory symptoms should be added to the diagnostic criteria for autism to better characterize the clinical phenotype. Further, robust linkages may indicate shared neurobiological mechanisms underlie these behavioural features, or that similar intervention approaches could be used to treat both classes of behaviours. In contrast, weak relationships may suggest these behaviours are more distinct than previously thought and that differential treatment approaches and taxonomies are needed, possibly because of dissimilar pathogenesis. (page 2).

Although, sensory behaviours have consistently been found to correlate with overall autism severity (Adamson et al., 2006; Ben-Sasson et al., 2009; Kern et al., 2007), these findings do not specify the contribution of the individual core features of ASD (social interaction, communication and repetitive behaviour) in the relation with sensory behaviour. The research below indicates why it is proposed that sensory features may be related to the core features of ASD, and reviews the limited research on the associations between sensory behaviours and the core features of ASD. No research has investigated the link between each core features of ASD and sensory behaviours independently of the effects of the other core features. This is important to consider given the conceptual overlap with sensory and repetitive behaviours; both social and repetitive behaviours are found in individuals with ASD, therefore, a relation between sensory and social behaviours may only reflect the fact that sensory is related to repetitive behaviours which in turn are related to social impairments in ASD (as they co-occur).

The original theory of Ornitz and Ritvo (1968) proposed that sensory behaviours may have a causal role in the presentation of repetitive behaviours. The argument was that brainstem

abnormalities resulted in states of arousal, which changed from over-excitation to over-inhibition. It was suggested that in order to compensate for these arousal inconsistencies, individuals engaged in repetitive and restricted behaviours. These repetitive behaviours allowed them to manage their arousal state by increasing order or predictability. These sensory and repetitive behaviours also impede communication and social interaction, which at that time were considered to be secondary symptoms of the condition. This theory has not received much attention in the ASD literature but would predict that there would be strong associations between sensory and repetitive behaviours and although sensory behaviours may also be associated with social interaction and communication scores, these may be smaller than the effects with repetitive behaviours.

102 Research on the association between sensory and repetitive behaviours in ASD is limited to only seven studies at the time of writing (2014). In several studies using questionnaires, more repetitive behaviours have been shown to be associated with higher levels of sensory behaviour (Boyd, McBee, Holtzclaw, Baranek, & Bodfish, 2009; Chen, Rodgers, & McConachie, 2009) even when controlling for IQ (Gabriels et al., 2008). Further studies compared the relation with sensory behaviours across the different subtypes of repetitive behaviours (insistence on sameness and motor stereotypies) but these results are inconsistent across the different studies e.g. sensory hyper-responsivity was related to insistence on sameness behaviours but not motor stereotypies (Baranek, Foster, & Berkson, 1997), and hypo- rather than hyper-responsivity has been associated with motor behaviours (Gal, Dyck, & Passmore, 2010), whereas Boyd et al. (2010) found that repetitive behaviours were related to hyper-sensitivity but not sensory seeking or hypo-sensitivity. There are some limitations to using questionnaire methods. Gabriels et al (2008) describes that the most potentially confounding factor is the overlap of items between repetitive and sensory

behaviours. One example is the use of the item “touches items and people’” described as sensory seeking in the Short Sensory Profile (McIntosh et al., 1999) but it is rated as a compulsive behaviour on the Repetitive Behaviour Scale – Revised (Bodfish et al., 1999). However, the relation between sensory and repetitive behaviours remained even when all overlapping items were removed from both measures (Boyd et al., 2009).

In Study 4.2.1 overlapping items were removed in order to control for the conceptual overlap in sensory and repetitive behaviours. This further highlights why it is important to hold the effects of the other core features constant in such analyses in order to explore these relations independently. The multivariate design adopted in the current chapter overcomes this overlap in another way by exploring the relations between the core features of ASD, e.g. the repetitive and social aspects as well as their independent and combined associations with the sensory behaviours.

It has been shown that early regulatory disorders of sensory processing in infancy and toddlerhood predict poorer language and social interaction abilities and clinical diagnosis at later ages (DeGangi et al., 2000). In addition, atypical responses to sensory input in the first year of life have been shown to predict a later diagnosis of autism (Baranek, 1999; Osterling & Dawson, 1994); increased mouthing, aversion to touch and decreased visual orienting at 9-12 months distinguished individuals who went on to receive a clinical diagnosis of ASD (Baranek et al., 1999). This suggests that reactions to sensory input at a young age may lay developmental foundations for social

communication and language in individuals that go on to receive a diagnosis of ASD. These relations, however, have been even less studied than the association between sensory and repetitive

103 communication problems in individuals with ASD. The Social Responsiveness Scale (Constantino & Gruber, 2002) is a 65-item parent or teacher report (15-20 minutes) on an individual’s ability to engage in emotionally appropriate reciprocal social interaction. In children with high functioning ASD (N=36) and age-matched controls (N=26) between 6-10 years old, a strong positive relation was found between scores on the SRS and sensory scores across four quadrants for the Sensory Profile (Hilton, Graver, & LaVesser, 2007; Watson et al., 2011) and across different sensory modality scores (Hilton et al., 2010). Sensory Profile modality scores of multisensory responsiveness, proximal senses of oral sensory/olfactory and touch were strongest predictors of SRS score. This is the only study to investigate sensory modalities and social behaviours and was limited to high functioning children between 6-10 years old.

Sensory behaviours measured using another less recognised parent report sensory measure the Japanese Sensory Inventory-Revised (JSI-R; Ota, Tsuchida, & Miyajima, 2002) were also

significantly associated with social interaction deficits again measured using the SRS in a group of high functioning children (n=42 ASD and n=42 controls) in Japan (Matsushima & Kato, 2014). The JSI-R is a parent report questionnaire consisting of 147 items in eight sub-categories of vestibular (30 items), tactile (44 items), proprioception (11 items), auditory (15 items), visual (20 items), olfactory (5 items), taste (6 items), and other (16 items). Liss, Saulnier, Fein, and Kinsbourne (2006) also found positive correlations between sensory under-reactivity and sensory seeking on the one hand and social and communication scores from the VABS or Vineland Adaptive Behaviour Scales (Sparrow et al., 1989) on the other. However this association was not found for sensory over-reactivity. Finally, Baker et al. (2008) found specific relationships in 2-8 year old children with ASD with sensory problems and communication and socialisation as measured using the VABS.

In addition to the very limited work in this area, research has been limited to total SRS score or sub-scales from more general measures that are not specific to ASD and measuring the social interaction and communication deficits as described by the international classification systems may provide a more valid measure of the relation between sensory behaviours and the core features of ASD. Examining the relations between sensory and core symptoms of ASD with items that are specific to diagnosis would provide more comprehensible and explicit information about the relationships in ASD. If relations exist then it indicates that the sensory features have the ability to impact on the core features of ASD, which in turn suggest that shared biological mechanisms could underlie the behaviour presentation and that similar intervention programmes could be developed to target both sets of behaviours.

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4.1.3.2 Relation within associated features

An additional confound in understanding the association between core and sensory behaviours in ASD that has not been considered is the relation between sensory and the additional associated features of ASD. This is important to identify as it may provide insights into the

mechanism by which sensory may be impacting on the core features of ASD. For example, the theory of Ornitz and Ritvo (1968) refers to states of arousal in sensory processing, which may be psychologically distressing and that repetitive behaviours were a way of making the sensory world more predictable. This indicates that the impact of sensory on repetitive behaviour may also be influenced by the level of anxiety seen in the individual; anxiety and other emotional problems are one of the associated features also reported in ASD (e.g. J. A. Kim, Szatmari, Bryson, Streiner, & Wilson, 2000; Sukhodolsky et al., 2008). If analyses do not control for the additional

features/behavioural presentation within ASD then important associations may be overlooked by confounding variables.

One strand of research has investigated the role of sensory behaviours in adaptive

behaviour. It has been suggested that successful sensory integration is an essential tool in children’s development (Bundy et al., 2007; Kranowitz, 2005). Baker et al (2008) found a negative relationship between daily living skills and sensory behaviours; more sensory problems were found in individuals with low daily living skills. Such difficulties have also been shown to be related to high levels of depression and anxiety in children with ASD (Ben-Sasson et al., 2009; Goldsmith, Van Hulle, Arneson, Schreiber, & Gernsbacher, 2006; Mazurek, Vasa, et al., 2013; Pfeiffer, Kinnealey, Reed, & Herzberg, 2005) and furthermore with behavioural difficulties (e.g. Rogers et al., 2003) and maladaptive behaviours (Baker et al., 2008). Not all research shows such significant relationships. Robinson and Magill-Evans (2009) found no significant relationship between scores of the Short Sensory Profile and daily living skills as measured by the Self Care Functional Skills scale of the Paediatric Evaluation of Disability Inventory in young children with ASD. Similar results were found by Jasmin et al. (2009) in that there was no significant difference between total Sensory Profile scores and daily living skills as measured by the Vinelands Adaptive Behaviour Schedule in 35 children with ASD. This area has been widely overlooked in the current literature and may be essential in understanding the patterns of behaviours between core and sensory behaviours as well as how associated behaviours interact with these.

Across all the work assessing the relations between sensory and other behaviours there is a limit to how age and IQ are controlled for. Although some studies have taken the effect of age and IQ on sensory features into account (e.g. Boyd et al., 2010) others have failed to do so which may be influencing the correlational analyses. In addition, many studies do not control for effects of core

105 features when examining the relationship between sensory and associated behaviours and vice versa. It is imperative to look at the relative power of all variables in analyses to best understand the pattern of behaviours.

4.1.3.3 Effect of age and ability level

The findings across chronological age and IQ are mixed and these individual characteristics are likely to impact on the associations between core and sensory features if they are not properly understood and controlled for in statistical analyses. In a sample of 3-56 year olds, sensory problems were found to be less frequent in older individuals, there were less differences reported between ASD and TD individuals at an older age (Kern et al., 2006) and correlations between sensory behaviours and ASD severity were found in children but not adolescents or adults (Kern et al., 2007). However, in a sample of children below 14 years old, sensory behaviours were more prevalent in the 10-14 year old group than the 6-9 year old group, which in turn showed more than the 4-5 year old group (Talay-Ongan & Wood, 2000).

Other work concludes that the pattern of sensory symptoms across the lifespan may be dependent on the categorisation according to Dunn (1997, see above). In a meta-analysis of 14 studies, Ben-Sasson et al (2009) found that scores for hyper-sensitivity and sensory seeking increased up to the ages of 6-9 years old and decreased after 9 years old, however, patterns were less consistent for hypo-sensitivity. Differences have also been shown across modalities, with proximal and auditory sensory abnormalities remaining consistently high across a sample of 3-38 year olds, whereas visual symptoms were found to decrease with age (Leekam et al., 2007).

There is also much discrepancy across ability level with some studies finding no effect of Sensory Profile scores and developmental level (Baker et al., 2008; Baranek et al., 2006; Kientz & Dunn, 1997; Lane, Young, Baker, & Angley, 2010; Rogers et al., 2003). However, it has also been shown that sensory behaviours were significantly higher in individuals with lower IQs for scores on hypo-sensitivity, hyper-sensitivity, sensory avoidance but not sensory seeking (Crane et al., 2009). In addition, visual symptoms were also more likely to be found in individuals with a lower IQ (Leekam et al., 2007).

4.1.3.4 Summary of research on Sensory and core features of ASD

The literature so far on sensory behaviours in ASD has found that sensory behaviours are very frequent in individuals with ASD in children (e.g. Leekam et al., 2007; Tomchek & Dunn, 2007) but this is mixed in adults (Kern et al., 2007; Crane et al., 2009). In terms of what role the sensory behaviours play in the behavioural manifestation of ASD, the strongest finding in the literature on

106 sensory behaviours is the association between repetitive and sensory behaviour (e.g. Boyd et al., 2009), however, relations have also been found between social and communication symptoms and sensory behaviours (Hilton et al., 2007). Research on the relation between sensory behaviour and core features is limited in that each core feature has been examined independently of the additional core features; Study 4.2.1 aimed to overcome this by examining the core features in combination, this study also examined the effects of age, IQ, gender and associated features to best understand the role of sensory behaviours.