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.