Introduction
Autism spectrum disorder (ASD) is a neurodevelopmental disability characterized by the presence of restricted and repetitive behaviors and challenges with social communication (American Psychiatric Association, 2013). For autistic children, externalizing behaviors (e.g., aggression and hyperactivity) are more prevalent compared to neurotypical peers (McClintock, Hall, & Oliver, 2003, Mahan and Matson, 2011, Totsika et al. 2011) and are linked with worsened learning opportunities (Lauderdale-Litten et al., 2013), lower peer acceptance (Burt et al., 2008; Deater-Deckard., 2001), and poor quality of life (Kuhlthau et al. 2010). Externalizing behaviors also relate to ASD features, namely emotional response and social skills (Neuhaus et al., 2014; Mazefsky, Pelphrey, & Dahl, 2012; Samson, Hardan, Lee, Phillips, & Gross, 2015). Delineating biological measures of externalizing behavior may identify autistic children who would benefit from intervention and promote better educational and health-related outcomes.
Physiological measures can be particularly useful for characterizing externalizing behaviors in autistic children. Difficulties with social-emotional reciprocity and communication are hallmarks of ASD (American Psychiatric Association, 2013; Wimpory et al. 2007; Joseph and Tager-Flusberg 2004; Klin et al. 2007). Therefore, young autistic children may have trouble identifying or articulating their emotions to another individual. Emotion regulation is also impacted in ASD (Fenning et al. 2019) and relates to externalizing behaviors in older children (Ting and Weiss 2017). Physiological variables derived from heart rate relate to parent reports of externalizing behavior (Baker et al., 2019; Neuhaus et al., 2014), and, importantly, provide an objective measurement regardless of age, verbal ability, and diagnostic status.
One physiological measure linked with self-regulatory behaviors is respiratory sinus arrhythmia (RSA), an index of cardiac activity in the parasympathetic nervous system (PNS). The PNS slows heart rate through vagal nerve input, and RSA captures the variability of heart rate across respiration. RSA reactivity (RSA-R), also known as RSA withdrawal, reflects the change in RSA from baseline to a stressor. High RSA and RSA-R are thought to reflect greater PNS control and thus greater regulatory control in response to environmental stressors (Porges, 1995, 2007; Beauchaine et al. 2007, Gyurak and Ayduk, 2008; Scarpa et al., 2010).
While RSA has been identified as a reliable physiological measure of emotion regulation (Beauchaine et. al 2007, Boyce et al. 2001, Graziano & Derefinko, 2013), RSA-R and its relationship to externalizing behaviors in autism are poorly understood. Previous research in autism is mixed, with some evidence of a negative relation and some reports of no relation (Cheng et al., 2020, Neuhaus et al., 2014) In one study, the relation between RSA-R and externalizing behavior was moderated by negative parent behavior (Baker et al. 2019), highlighting the complex role of social-emotional factors in the expression of externalizing behavior by autistic children. RSA-R accounted for dysregulated behaviors beyond the presence of autism features (Baker et al., 2022), and its relation to externalizing behavior depended on co-occurring sympathetic activity levels (Fenning et al., 2019). While these initial findings suggest that RSA-R is relevant for externalizing behaviors in autistic samples, more work is needed to characterize RSA in young autistic children.
To best characterize RSA-R, batteries require appropriately matched challenge and comparison tasks. Challenge tasks across different domains (e.g., cognitive versus social) may differentially probe PNS reactivity (Burt & Obradović, 2013). Further, measuring RSA change from a challenge task in one modality to an unrelated baseline task does not account for domain-specific baseline responses (Bush et al., 2011; Kamarck, Jennings, and Mannick 1993) or differences in task-related artifacts (e.g., movement), which is particularly important when sampling from autistic children who may have poorer motor control (Licari et al. 2020; Liu & Breslin, 2013). While reactivity paradigms with challenge and matched comparison tasks across modalities are available (Bush et al., 2011; Kamarck and Lovallo, 2003), we could find no published studies using this design in young autistic children.
The current pilot study addressed these limitations by evaluating parasympathetic reactivity and externalizing behaviors in autistic children. Our aims included the following:
Aim 1: Evaluate the feasibility and stability of RSA measured via challenge and matched comparison tasks across four distinct domains: cognitive, social, emotional, and sensory.
Aim 2: Explore whether RSA-R elicited by tasks with feasible and stable RSA response relates to parent reported externalizing behavior.
Given the primary goal was evaluating a physiological battery for the first time in ASD, we had no hypotheses regarding specific task domains. Broadly, we hypothesized that for any tasks with stable RSA, lower RSA-R, indicative of greater RSA withdrawal and reduced emotion regulation, would relate to increased externalizing behavior.