Impaired social communication is a primary characteristic of Autism Spectrum Disorder (ASD) (American Psychiatric Association, 2013) and may be the result of limitations in social cognition (e.g., Baron-Cohen, 1995) or social motivation (Chevallier et al., 2012). Underlying physiological factors may also impact the extent to which individuals with ASD engage with others in social situations. For example, there is considerable evidence that social interactions are highly stressful for children with ASD (Lopata et al., 2008; Corbett et al., 2010). It may be this exaggerated stress response that drives, in part, reductions in social engagement. There is also significant prevalence of sensory dysfunction in ASD (Rogers et al., 2003; Kern et al., 2006; Tomchek and Dunn, 2007; Ben-Sasson et al., 2009), and these hyper- and/or hypo- sensory sensitivities may further contribute to atypical patterns of social interaction.

Compared to typically developing (TD) peers, children with ASD tend to interact less with other children (Corbett et al., 2010, 2012) and engage in less cooperative play (Corbett et al., 2014b), instead showing a preference to engage in self-play (Humphrey and Symes, 2011). There is also evidence that individuals with ASD have abnormal preferences for interpersonal distance (IPD), including both standing too close or preferring more distance relative to TD peers (Kennedy and Adolphs, 2014; Lough et al., 2015; Perry et al., 2015). As children with ASD become more aware of their limitations in social skills with age (Knott et al., 2006), later peer interactions may be characterized by exacerbated social stress (Schupp et al., 2013). As a result of this stress, these children may display increased avoidance behaviors characterized by decreased social motivation to interact with peers. This notion is supported by research showing that higher cortisol response to a novel social interaction was associated with reduced social communication among children with ASD (Corbett et al., 2014b).

The hypothalamic-pituitary-adrenal (HPA) axis is a highly regulated system that is responsible for maintaining homeostasis via maintenance of a diurnal rhythm, activation in response to stress or threat, and restoration of basal activity via negative feedback mechanisms. Cortisol, an important stress hormone, serves as a measurable indicator of HPA regulation, increasing in concentration after exposure to stressors (Herman and Cullinan, 1997). Cortisol also shows a diurnal rhythm of fluctuating concentration, throughout the day. Typically, diurnal cortisol values are at peak levels in the morning and slowly decline to lowest levels in the evening. In ASD, the diurnal rhythm appears to be altered, such that children with ASD have lower morning cortisol and higher evening cortisol values relative to TD children (Corbett et al., 2008, 2009). Further, many children with ASD show an increased response to stress, as indicated by higher cortisol levels, when interacting with unfamiliar peers (Lopata et al., 2008; Corbett et al., 2010). This stress response appears to be tied to level of social cognition, as those with highest cortisol values tend to show less social motivation (Corbett et al., 2014b). It is important to note, however, that this response is considerably variable within the ASD population (Lopata et al., 2008; Schupp et al., 2013). This suggests the possibility of interactions with other characteristics, which may explain part of the high variability in psychosocial stress response as seen in ASD.

Sensory processing abnormalities are now considered a core symptom of ASD under the Restrictive and Stereotypic Behaviors criteria of the DSM-5 (American Psychiatric Association, 2013). Sensory behaviors have historically been divided into four patterns, including sensory hypo-reactivity, hyper-reactivity, sensory seeking, and sensory avoidance (Dunn, 2001; Ben-Sasson et al., 2009). Complexity arises from the fact that many individuals with ASD will show several of these patterns at one time, with mixed patterns being displayed across sensory domains (Baranek et al., 2006; Tomchek and Dunn, 2007; Lidstone et al., 2014). Recent conceptualizations, therefore, have attempted to classify sensory processing abnormalities in ASD into specific subtypes (Lane et al., 2011, 2014; Uljarević et al., 2016), such as sensory adaptive, sensory moderate, and sensory severe (Uljarević et al., 2016).

Emerging research demonstrates a relationship between sensory sensitivities and arousal/anxiety in ASD. In one study, children with ASD showed lower morning cortisol relative to TD peers, which was associated with higher parent-reported stress as measured by the Stress Survey Schedule (SSS) (Corbett et al., 2009). Similarly, morning cortisol was associated with various domains of sensory functioning derived from the Short Sensory Profile—a parent-reported indicator of sensory sensitivities—(SSP; Dunn, 1999) painting a complex picture based on individual profiles (Corbett et al., 2009). Other studies investigating sensory profiles in ASD have also found relationships between sensory responsivity and anxiety (Green et al., 2012; Lidstone et al., 2014; Wigham et al., 2015; Uljarević et al., 2016), repetitive behaviors and stereotyped movements (Gabriels et al., 2008; Gal et al., 2010; Lidstone et al., 2014), and intolerance of uncertainty (Chamberlain et al., 2013; Wigham et al., 2015). Furthermore, a sample of TD young adults showed a correlation between sensory sensitivity and increased interpersonal distance (Perry et al., 2016), suggesting some role of sensory processing in social behavior. Currently, however, there is limited research that attempts to elucidate the impact of sensory dysfunction on social motivation and communication, especially in a naturalistic play setting.

The current study sought to investigate between-group differences in biobehavioral profiles of psychosocial stress following play with unfamiliar peers, in conjunction with sensory profiles. In order to elucidate the impact of sensory dysfunction on stress and social interaction, the current study sought to measure social engagement during a Peer Interaction Paradigm (PIP) (Corbett et al., 2010) and then to compare social behavior to stress and sensory profiles, as indicated by measures of cortisol and parent reports of stress and sensory sensitivity. It was hypothesized that children with ASD would have greater cortisol in response to play, relative to TD peers. Furthermore, it was hypothesized that cortisol response would be positively correlated with both increased parent-reported stress and sensory sensitivity.

Demographic information for each group is presented in Table 1, including age, cognitive, and diagnostic information. Descriptive statistics for SSP, SSS, and cooperative play (separated by group) are listed in Table 2. Using independent samples t-tests, there were significant between-group differences on the SSP [t₍₇₈₎ = 140.44, p < 0.0001] and the SSS [t₍₇₇₎ = 109.32, p < 0.0001], showing greater parent-reported stress and sensory sensitivity in the ASD group, compared to the TD group.

In order to assess group differences in social behavior, the percent duration of cooperative play during the solicited play period T4 of the PIP was compared between groups, using independent samples t-tests. Results revealed a significant difference between groups in percent duration of cooperative play [t₍₈₃₎ = 8.349, p = 0.005], showing that children with ASD engage in significantly less cooperative play than TD peers.

Descriptive statistics for cortisol at baseline, during play, and after play are shown in Table 3. Analysis of covariance (ANCOVA) was conducted to examine the effect of group on stress (cortisol levels during cooperative play with peers), while controlling for baseline values. Results indicate a significant group difference in cortisol during play (S3) with peers [F_{(1, 77)} = 5.77, p = 0.02]. There was also a significant group difference in cortisol after play (S4) [F_{(1, 77)} = 4.78, p = 0.03].

In consideration of these group differences, Pearson product correlations were calculated to assess the relations between physiological stress (cortisol), sensory functioning (SSP), and parent-report stress (SSS). Cortisol during play was negatively correlated with scores on the SSP (r = −0.24, p = 0.03) and positively correlated with scores on the SSS (r = 0.27, p = 0.02). Therefore, as cortisol levels increased during the PIP, SSP scores decreased (indicating greater sensory dysfunction) and global stress as measured by the SSS increased.

Moderation analysis was conducted to examine the impact of diagnosis on the relation between stress (cortisol) and sensory (SSP) functioning. Results show that diagnosis was a significant moderator of the association between SSP and cortisol at baseline (S1) [ΔR² = 0.01, F_{(1, 76)} = 8.46, p = 0.0047], the beginning of play (S2) [ΔR² = 0.06, F_{(1, 76)} = 4.85, p = 0.03], during play (S3) [ΔR² = 0.02, F_{(1, 76)} = 3.94, p = 0.05], and after play (S4) [ΔR² = 0.05, F_{(1, 76)} = 3.95, p = 0.05]. Figure 2 shows the moderating effect of diagnosis on the relation between SSP and cortisol, indicating that the negative correlation observed between cortisol and sensory functioning in the total sample is driven by the ASD group, whereas the opposite trend appears to hold true for the TD group.

In order to examine the impact of sensory sensitivity on play, we examined the association between SSP score and percent duration spent in cooperative play during the solicited play period, T4. There was a trend level positive association between cooperative play and total SSP (r = 0.197, p = 0.07). This association suggests that more sensory impairment was associated with less time spent in cooperative play (lower scores on the SSP are indicative of greater sensory dysfunction).

In an effort to further assess the impact of sensory sensitivity on play, post-hoc correlational analyses were conducted for individual domains of the SSP along with time spent in cooperative play. Scores on the Auditory domain were significantly positively correlated with cooperative play (r = 0.218, p = 0.04), while Underresponsive/Seeks Sensation correlated with play at a trend level (r = 0.196, p = 0.07).

While challenges in reciprocal social interaction are synonymous with ASD, sensory dysfunction and heightened stress are often found as well. Thus, the current study sought to examine the impact of sensory dysfunction on stress and social engagement with unfamiliar peers in children with and without ASD. The study utilized measures of social interaction (cooperative play) and physiological arousal (cortisol) during peer play using the PIP (Corbett et al., 2010) to assess the associations of social behavior and physiological stress with parent reports of stress and sensory sensitivity. It was hypothesized that children with ASD would show greater levels of salivary cortisol in response to play, relative to TD peers. Furthermore, it was hypothesized that cortisol response would be positively correlated with both increased parent-reported stress and sensory sensitivity. Therefore, the current study sought to further investigate biobehavioral profiles following play with unfamiliar peers with an emphasis on the impact of sensory sensitivity.

Autism is characterized by prevalence of sensory dysfunction (Rogers et al., 2003; Kern et al., 2006; Tomchek and Dunn, 2007; Ben-Sasson et al., 2009) and increased stress, especially during social interactions (Lopata et al., 2008; Corbett et al., 2010). In the current study, children with ASD showed both increased sensory dysfunction and parent-reported stress, relative to their TD peers. Research has shown that both altered sensory sensitivity and stress have deleterious effects on the overall functioning of children with ASD, especially given their potential associations with a variety of challenges, such as poor response to change (e.g., Chamberlain et al., 2013; Wigham et al., 2015) and anxiety (Green et al., 2012; Lidstone et al., 2014; Wigham et al., 2015; Uljarević et al., 2016).

In addition to group differences in sensory sensitivity and parent-reported stress, differences in salivary cortisol response were observed. Consistent with previous reports (Corbett et al., 2010, 2012, 2014b; Schupp et al., 2013), the ASD group had significantly greater physiological arousal in response to social interaction relative to the TD group, as indicated by higher cortisol levels both during and after the PIP. The increased arousal suggests that children with ASD may perceive social interaction with peers to be more stressful, compared to TD peers. Moreover, cortisol response was significantly correlated with parent-reported stress suggesting that heightened physiological reactions to peer interaction are also associated with a global pattern of elevated stress. Findings add to a growing body of work showing dysregulated patterns of stress in youth with ASD, both in terms of global and diurnal stress (Corbett et al., 2008, 2009), as well as stress in response to social interaction (e.g., Corbett et al., 2014b).

In light of observing group differences for both physiological stress and sensory sensitivity, we explored correlations between these variables. Significant associations were found between cortisol and SSP, such that higher cortisol in response to play was associated with greater sensory impairment. Moderation analyses were conducted to determine whether the correlation was driven by group status. Results showed that ASD diagnosis was a significant moderator of this relation, such that sensory dysfunction was associated with increased salivary cortisol response to peer interaction in the ASD group only. Moreover, this relationship held for cortisol levels at each time point of collection, including baseline cortisol as well as before, during, and after play. Interestingly, the TD group appeared to have the opposite relationship between cortisol and sensory functioning (Figure 2), implying that the negative impact of sensory sensitivity on stress reactivity during play is unique to ASD. In other words, greater levels of sensory dysfunction in ASD may lead to increased physiological stress. Thus, it appears that the symptom profile of ASD ostensibly contributes to enhanced reactivity to the environment, which can be manifested in both sensory and physiological functioning. The question still remains whether or not these relationships between stress and sensory sensitivity are bi-directional or whether a uni-directional model exists, such that one symptom precedes and drives the other.

When assessing group differences in cooperative play, the ASD group engaged in significantly less cooperative play, relative to the TD group. This is in line with previous findings that children with ASD tend to engage less than their TD peers during the PIP (e.g., Corbett et al., 2014b). While factors such as social cognition (Baron-Cohen, 1995; Corbett et al., 2014a) and social motivation (Chevallier et al., 2012; Corbett et al., 2014b) appear to play a significant role in explaining group differences in social engagement, sensory dysfunction may also have an impact on social behavior. For example, sensory sensitivity was recently shown to associate with interpersonal distance in TD individuals (Perry et al., 2016). In order to better understand the potential impact of sensory sensitivity on play behavior in ASD, duration spent in cooperative play was analyzed along with sensory processing scores. While overall sensory dysfunction was not associated with play behavior, auditory sensitivity was significantly correlated with play.

Adults with ASD have shown impairments in auditory localization through an inability to use prior perceptual experience to locate sounds (Skewes and Gebauer, 2016). Difficulties in auditory processing and orienting to a stimulus may be linked to emergence of impairments in social and communication behaviors early in development (Osterling et al., 2002). As such, children with ASD fail to orient to stimuli, especially critical social stimuli such as response to their own name (Dawson et al., 1998). It is possible that the inability to attend to stimuli is due, in part, to altered auditory processing, resulting in reduced early social interactions through a lack of joint attention with the caregiver. According to the Enactive Mind hypothesis (Klin et al., 2003), limited early social experiences may contribute to the social communication deficits that characterize ASD. Therefore, if sensory sensitivity alters one's experience in the physical world, interactions in the social world may be absent, incomplete, or unpredictable among children with ASD, thus leading to difficulties in social communication and cognition. While this is an intriguing theory for connecting the sensory and social symptoms of ASD, a great deal of empirical evidence is needed to test for direct links between sensory and social functioning in ASD.

The named authors made significant contributions to the investigation and manuscript. Specifically, BC conceptualized the study design, outlined the organization of the manuscript, guided the literature search, ran data analysis, provided interpretation to the findings, and made significant contributions to the final manuscript. RM read the extant literature, synthesized the results, contributed to interpretation of the findings, and co-wrote the initial draft of the manuscript. SB participated in the acquisition, analysis, and interpretation of the physiological and behavioral data, and contributed to the writing of the manuscript. All authors read and approved the content of the work.

This work was supported by National Institute of Mental Health R01 MH085717 awarded to BC.