Introduction
Sensory processing involves a cascade of events including the registration, organization, and interpretation of incoming information from the senses (Suarez,
2012). Inability to properly process visual, auditory, tactile, olfactory, gustatory, and proprioceptive input from the environment leads to sensory hyper- or hypo-sensitivity, and to difficulties modulating behavior (Koziol et al.,
2011). Importantly, hypo- and hyper-sensory-sensitivity can occur simultaneously in an individual and may be present across multiple sensory domains (Baranek,
2002). Sensory abnormalities (SAs) are surprisingly common among school-aged children. A recent epidemiological study estimated that 8% of school-aged children experience SAs (Jussila et al.,
2020), with higher rates reported in some studies (16.5%; Ben-Sasson et al.,
2009). SAs affect 35%–95% of children with developmental disorders, including autism spectrum disorder (ASD) (Rogers & Ozonoff,
2005; Allen & Casey,
2017). SAs can affect daily functioning, learning, and social skills (Bar-Shalita et al.,
2008; Koenig & Rudney,
2010; Elbasan et al.,
2012; Dunn,
2014; Miller et al.,
2017) and may account for some of the heterogeneity in social functioning among school-age children but further research is needed.
Social functioning (an individual’s behavior in a social environment, social skills and interactions with others; Green,
1996; Yager & Ehmann,
2006; Beauchamp & Anderson,
2010), is critical during school-age because of its association with academic achievement (Malecki & Elliott,
2002; Walker & Nabuzoka,
2007) and emotional well-being (Nangle et al.,
2003; Lodder et al.,
2017). Children with SAs demonstrate problems with social functioning such as poor social problem-solving, reduced empathic concern, and difficulty reading social cues (Ben-Sasson et al.,
2009; Cosbey et al.,
2012). Greater challenges interacting with peers during play than children with TD have also been reported (Cosbey et al.,
2012; Armstrong et al.,
2013). Children with SAs were shown to differ from TD peers on a number of dimensions related to social functioning during recess (Cosbey et al.,
2012). Children with SAs engaged in significantly less social play and experienced more frequent and prolonged conflict with peers during play than children with TD. Children with SAs also made fewer relationship repair attempts (e.g., apologizing), were sought out less frequently for play, and demonstrated more difficulty responding to social cues (e.g., responding to cues of boredom, annoyance, or disinterest) than TD peers. Although this study was small (12 per group), the observational data provides some of the first direct evidence of social functioning deficits in children with SAs in a naturalistic environment with peers.
The relationship between SAs and social functioning has been studied more extensively in children with ASD. SAs across multiple sensory modalities (vision, hearing, taste, touch) are associated with a range of social functioning difficulties including reading social cues, responding to other’s social bids, and understanding the emotions of others (see Thye et al.,
2018 for review). For example, greater atypical visual exploration in children with ASD was found to be associated with lower scores on measures of social skills (Hellendoorn et al.,
2014). Increased social impairments on the Autism Diagnostic Observation Schedule (ADOS) and Autism Diagnostic Interview, Revised (ADI-R) were related to increased tactile hypo-responsiveness and tactile sensory seeking behaviors in children with ASD (Foss-Feig et al.,
2012). Additionally, atypical processing of emotion in voices (e.g., discriminating happy versus angry) may impact processing of socially relevant auditory information (Fan & Cheng,
2014). Finally, worse olfactory identification has been associated with greater difficulties maintaining conversations (Bennetto et al.,
2007). However, even in this population, significant gaps in the literature exist. A majority of the evidence comes from laboratory-based studies, using experimental measures of sensory processing, limiting the generalizability of the results. Parent report has also demonstrated associations between SAs and social functioning difficulties in children with ASD, providing convergent evidence for laboratory-based findings (Liss et al.,
2006; Hilton et al.,
2007; Baker et al.,
2008).
Most research has focused on circumscribed domains of social functioning (i.e., adaptive functioning or reciprocal social behavior or peer relationships). However, social functioning is multi-faceted and a more comprehensive approach to understanding the relationship between SAs and social functioning is needed (Gree-Walker et al.,
1994; Beauchamp & Anderson,
2010). In addition, few studies have included measures of communication despite the fact that communication deficits explain variability in social functioning among children with developmental disabilities (Venter et al.,
1992; Leonard et al.,
2011; Park et al.,
2012; Staikova et al.,
2013). For example, in sample of 28 children with ADHD, language skills mediated the relationship between ADHD symptoms and social skills (Staikova et al.,
2013). Similarly, associations between communication and social skills have been found in children with ASD (Venter et al.
1992). Accounting for differences in communication skills could allow for better assessment of heterogeneity in social functioning.
The purpose of the present study was to (1) evaluate social functioning in children with SAs without developmental disabilities (2) contrast social functioning in children with SAs with two well-characterized, age-matched clinical comparison groups; children with ASD and TD, and (3) determine the relationship between SAs and social functioning across the full sample of children (SAs, ASD, TD) to better capture heterogeneity in SAs across clinical and non-clinical conditions.
Method
Participants were 135 children between the ages of 8–13 with SAs (n = 44), ASD (n = 43), and TD (n = 48) who participated in a larger study focused on understanding the biochemical, brain, and behavioral correlates of sensory sensitivity in school-age children (Social and Sensory Processing Study, see Sweigert et al.,
2020). Participant characteristics are presented in Table
1. Participants were recruited from the Seattle metropolitan area via flyers, online recruitment postings, and a research registry at the University of Washington. Participants were also recruited via medical records screening. Medical records were screened using key terms (e.g., sensory sensitivity) and prospective participants were sent a recruitment letter. All study procedures were approved by the University of Washington Human Subjects Division Institutional Review Board. Written informed consent was obtained from each participant’s parent and verbal assent was obtain from each participant.
Table 1
Participant characteristics
Sex (Male:Female) | 38:6 | | 39:4 | | 41:7 | | χ2 = 0.64 | .726 |
Race (White:Non-White) | 34:10 | | 36:7 | | 37:11 | | χ2 = 0.76 | .682 |
Age | 10.03 | 1.63 | 10.28 | 1.64 | 10.32 | 1.44 | 0.48 | .622 |
WASI FSIQ | 115.64 | 18.12 | 112.33 | 17.9 | 118.79 | 11.7 | 1.84 | .163 |
WASI PIQ | 113.02 | 16.8 | 114.91 | 14.33 | 115.06 | 13.02 | 0.265 | .768 |
WASI VIQ | 114.75 | 18.07 | 107.33 | 21.21 | 118.33 | 12.33 | 4.46 | .011 |
Vineland-II ABCd | 85.35 | 11.72 | 80.15 | 10.81 | 104.83 | 12.41 | 54.64 | < .001 |
Vineland-Communication d | 88.19 | 10.98 | 83.95 | 11.41 | 105.77 | 11.56 | 47.15 | < .001 |
Expressive (v-scale score) | 12.77 | 1.9 | 11.29 | 1.7 | 15.77 | 2.5 | 53.92 | < .001 |
Receptive (v-scale score) | 11.95 | 2.53 | 11.37 | 2.22 | 15.75 | 1.85 | 53.70 | < .001 |
Written (v-scale score) | 14.30 | 3.06 | 13.83 | 3.28 | 15.83 | 2.24 | 5.95 | .003 |
ADOS-2 CSS Totale | 3.16 | 2.94 | 7.12 | 1.95 | 1.46 | .82 | 123.14 | < .001 |
ADOS-2 Social Affect CSSf | 3.73 | 2.56 | 7.37 | 1.94 | 2.00 | 1.24 | 86.76 | < .001 |
ADOS-2 RRB CSSg | 3.50 | 2.26 | 6.67 | 2.33 | 1.77 | 1.77 | 61.85 | < .001 |
K-SADS ADHD | 26 | 59 | 21 | 49 | 0 | 0 | | |
K-SADS Anxiety | 12 | 27 | 11 | 26 | 0 | 0 | | |
K-SADS Depression | 7 | 16 | 0 | 0 | 0 | 0 | | |
K-SADS ODD | 5 | 11 | 3 | 7 | 0 | 0 | | |
Initial telephone screening interviews were conducted with parents to determine study eligibility and group assignment. All participants were required to have an FSIQ above 70 and not meet criteria for intellectual disability. 151 participants (50 SAs, 51 ASD, 50 TYP) were enrolled in the study after initial screening and were invited for an in-person evaluation. The SAs group all scored at or above two standard deviations above the mean of the normative sample (“much more than others”) on one or more sensory processing domains of the Child Sensory Profile, Second Edition (CSP-2; Dunn,
2014). Children in the SAs group were excluded if they reported a history of ASD, first-degree relative with ASD, or a known inherited genetic disorder during the initial screening interview. Children in the ASD group each had a previous ASD diagnosis. Children with ASD were excluded if they had a history of schizophrenia or other psychotic disorder or a known inherited genetic disorder. One child initially in the SAs group was transferred to the ASD group after the research assessment established that they met DSM-5 criteria for ASD. Children in the TD group were excluded for prior diagnosis of ASD, ADHD, intellectual disability, or other psychiatric/developmental disorder, having a first-degree relative with ASD, and any score on the CSP-2 at or above two standard deviations above the mean (“much more than others”).
Group assignment was confirmed through in-person evaluations by a licensed clinical psychologist or psychology graduate student under the supervision of the study’s lead licensed clinical psychologist (TS). All children in the ASD group met clinical best estimate (CBE) diagnosis using the Autism Diagnostic Interview, Revised (ADI-R; Lord et al.,
1994), Autism Diagnostic Observation Schedule, Second Edition (ADOS-2; Lord et al.,
2012), and DSM-5 ASD criteria (American Psychiatric Association,
2013). Children in the SAs and TD groups did not meet criteria for CBE diagnosis for ASD. The Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler,
1999) was used to assess cognition and intellectual performance. The Kiddie Schedule for Affective Disorders and Schizophrenia (K-SADS-PL DSM-5; Kaufman et al.,
1997) was used to screen for associated psychiatric conditions, as described above, for the children with ASD and TD. Seventeen participants were disqualified after an in-person clinical evaluation (e.g., FSIQ < 70, etc.) resulting in a final sample of 135 participants (44 SPD, 43ASD, 48 TD).
Descriptive information on participants is provided in Table
1. There were no group differences in age, gender, or race. On the WASI there were no significant group differences for FSIQ or PIQ but the ASD group had significantly lower VIQ scores than the TD group (
p = 0.01). On the K-SADS-PL DSM-5, nearly half of the sample of children with SAs demonstrated symptoms of ADHD, approximately one-third, symptoms of anxiety, a little less than a quarter, symptoms of depression, and over 10 percent reported symptoms of oppositional defiant disorder. Comparable rates of psychiatric symptoms were observed in the ASD group, with the exception of depressive symptoms. The TD group did not report any clinically significant symptoms on the K-SADS-PL DSM-5.
Discussion
This study investigated social functioning in school-age children with SAs, and a clinical comparison group of children with ASD and children with TD. Children with SAs demonstrated impairments in social functioning on standardized measures of reciprocal social behavior and social skills, with means scores on these measures falling within the moderate impairment range. When group differences were investigated, controlling for communication skills, children with SAs demonstrated worse social functioning than children with TD. Interestingly, their scores on standardized measures of social functioning were similar to children with ASD. These findings are consistent with prior research demonstrating lower than expected social skills in school-age children with SAs (Ben-Sasson et al.,
2009; Armstrong et al.,
2013).
Group comparison, controlling for communication skills, also revealed that children with SAs experienced more conflict with their peer-playmates than children with TD. Children with SAs and children with ASD experienced similar levels of conflict during play with peer-playmates. Although level of conflict with peer-playmates was assessed through parent report, this finding converges with existing evidence using observations of peer interactions (Cosbey et al.,
2012). Higher levels of conflict are associated with fewer interactions with peers in children with SAs (Cosbey et al.,
2012), children with TD (Gottman,
1983; Ladd,
1992), and children with ASD (Frankel & Mintz,
2011) and is associated with peer rejection (McElwain et al.,
2010). This could mean that children with SAs have fewer opportunities to develop their social skills due to reduced peer interactions and may experience more rejection than their socially skilled peers. High rates of co-occurring psychological symptoms in the SAs group may also have contributed to difficulties with peer interactions and, more generally, with social functioning. Future research will be needed to explore this idea further.
We found that children with SAs required more parent support during play interactions with peer-playmates than children with TD and a similar level of support as children with ASD. Parental support activities involved support with managing conflict and emotions, understanding social rules, and providing help with foundational play skills. To our knowledge, this is the first study reporting on parent support activities during play with peer-playmates in children with SAs. These findings are consistent with prior research in which parent support was increased for children with ASD (Estes et al.,
2018). Direct parent involvement during peer interactions may be a sign of poorer social skills (Mikami et al.,
2010). In the current study, increased parent support was associated with decreased social skills and increased impairments in reciprocal social behavior, providing some initial support for this theory.
Trend-level differences in Number of Peer-Playmates was found. Number of peer-playmates, as measured by parent report, were similar in children with SAs and children with TD and both groups had a greater Number of Peer-Playmates than children with ASD. Although prior research has suggested that children with ASD have fewer peer-relationships than children with TD (Petrina et al.,
2014), it is surprising that children with SAs had more peer-playmates than children with ASD, especially in light of similarities in social functioning. Although there is significant heterogeneity in ASD, differences between children with SAs and ASD in number of peer-playmates could be due to differences in motivation to seek out peer-playmates (Calder et al.,
2013; Sedgewick et al.,
2016). Children with SAs, despite having social challenges, were perhaps more motivated to spend time with peers engaged in play dates. Differences in restricted and repetitive behaviors (RRB) may also account for differences in number of peer-playmates (Jones et al.,
2017). For example, children with ASD may be more focused on discussing special interests than on socializing when interacting with peers or may have difficulties developing relationships with peers due to behavioral rigidities (e.g., needing to direct the play of others). To explore this possibility in the current sample, correlations between RRBs and number of peer-playmates were calculated for each group separately, but no significant relationships were found. However, no research, to our knowledge, has reported on the number of peer-playmates in children with SAs and possible explanations about differences across groups need to be explored further.
Similarities in social functioning and presence of sensory abnormalities in the SAs and ASD groups might suggest that children with SAs lie somewhere along the autism spectrum or have characteristics of the broader autism phenotype (BAP). To date, studies on BAP traits have primarily focused on relatives of children with ASD and adult populations (Ozonoff et al.,
2014; Landry & Chouinard,
2016; Rubenstein & Chawla,
2018). Further research is needed to determine whether BAP traits might extend to children without a family history of ASD such as the SAs group in this study. Further, it is notable that in the SAs group the overall calibrated severity score on the ADOS-2, an index of autism-related symptoms, fell in the low range. Suggesting that, unlike children with ASD, social functioning in children with SAs is not impaired in the context of a one-on-one interaction with an examiner. Future research is needed to understand the impact of different contexts on social functioning and, more generally, the concordant and discordant features of children with SAs and ASD.
The third aim of the study was to determine the relationship between SAs and social functioning by examining SAs on a continuum across the entire sample of children. We found that increased SAs were associated with worse reciprocal social behavior and social skills, explaining a moderate to small proportion of unique variance (33% and 6% respectively) after accounting for communication skills. The current findings are congruent with prior research in children with ASD where moderate to strong relationships between SAs and reciprocal social behavior (Hilton et al.,
2007,
2010) and social skills (Liss et al.,
2006) were found. It is notable that the strongest relationships were apparent between SAs and reciprocal social behavior (as measured by the SRS) compared with social skills (as measured by the Vineland) across these studies, a pattern also reflected in our own data. This could reflect measurement overlap between the CSP-2 and SRS-2 (see limitations section for further discussion) or clarify the specific components of social functioning that are most affected by SAs. Our findings also extend prior research by examining associations between SAs and social functioning across a broader sample of children than has been previously investigated (i.e., including children with SAs).
Finally, we found that SAs were associated with increased peer conflict and parent support after accounting for communication skills but were not related to Number of Peer-Playmates. Previous research, to our knowledge, has not reported on the relationship between SAs and these specific aspects of social functioning in children with and without TD. One interpretation of our results is that SAs prevent children from being fully engaged in social interactions (Doble & Magill-Evans,
1992). They may be distracted by SAs or may spend their cognitive resources compensating for sensory processing disruptions, the consequence of which may be fewer resources for recognizing social cues, managing their own emotions, and adequately managing conflict as it arises.
Social skills interventions targeting both broader (e.g., reading social cues) and specific social skills (e.g., how to respond when a conflict during play arises) may be beneficial for children with SAs. Although there is little empirical evidence on social skills interventions in children with SAs without ASD, research on social skills interventions in children with ASD could be considered to support children with SAs. Peer-mediated and school-based interventions have resulted in improved social skills and peer interactions among school-aged children with ASD (Kasari et al.,
2012; Locke et al.,
2019). A school-based intervention program that combines individualized social skills instruction, in vivo practice of learned social skills, and peer support may be particularly beneficial (Locke et al.,
2019). Importantly, there is evidence suggesting that the presence of co-occurring psychiatric symptoms could affect social skills interventions. For example, Antshel et al. (
2011) found that children with ASD and children with ASD and co-occurring anxiety showed improved social skills after a 10-week social skills intervention focused on conversational skills and social problem solving but that children with ASD and co-occurring ADHD did not. This study demonstrated that children with SAs have higher rates of co-occurring psychiatric symptoms, in particular ADHD. Thus, designing and implementing interventions that address co-occurring psychiatric disorders may be critical to improve social skills for children with SAs.
Limitations
Several limitations in the current study should be noted. Small numbers of non-white and female participants limits generalizability of the results. Our findings may be most relevant for verbally fluent children with Average to High Average intellectual functioning since this sample did not include children with intellectual disability. Research including children across the entire spectrum of intellectual functioning is needed to provide further insight into the nature of the relationship between sensory abnormalities and social functioning. Further, it is possible that the use of the WASI instead of the WASI-II could have resulted in a slight over-estimate of IQ scores, which would have been consistent across all groups in the study (Trahan et al.,
2018). Additional, clinical characterization of children with SAs with respect to intervention history, school supports, SES, and family environment will also be important in future studies.
The measure of peer interaction, the PSCQ, limits parents report to a maximum of five peer-playmates. This allows parents to provide greater detail about each peer-playmate. However, it limits the PSCQ as a quantitative measure as it may not capture the full variability in number of peer-playmates. Future research could better address this question by adding a measure of the total number of peer-playmates for each child. It should also be noted that the SRS-2 probes sensory experiences, however, given the small number of items (< 3 of 65), these did not likely influence the results. Finally, measurement of sensory symptoms relied solely on parent-report. There may be differences between direct observation of SAs using laboratory-based tests versus parent report (Schoen et al.,
2009). However, parent-report provides an ecologically valid assessment of SAs. Thus, future research should consider including both. Cross-informant ratings may offer further insight into social functioning across different social contexts. For example, there is some suggestion that in children with ASD teachers may report better skills in responding to and maintaining social interactions than parents (Murray et al.,
2009).
In our sample, there were high rates of co-occurring psychiatric symptoms in the SAs group. Future research should investigate the relationship between co-occurring psychiatric symptoms and social functioning in children with SAs given evidence that social functioning problems are associated with ADHD (Maedgen & Carlson,
2000), anxiety (Riby et al.,
2014), and depression (Verboom et al.,
2014). Although it was outside of the scope of the current paper to investigate of the relationship between all co-occurring psychiatric symptoms and social functioning, future research is needed to evaluate the relationship of social functioning to other types of psychiatric symptoms beyond those evaluated in this study.
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