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\begin{document}

\title{Piloting a Battery to Evaluate Parasympathetic Reactivity and
Externalizing Behaviors during Early Childhood in Autism Spectrum
Disorder}



\author[1]{Yael Braverman}%
\author[1]{Madison Surmacz}%
\author[1]{Gina Schnur}%
\author[2]{Nasim Sheikhi}%
\author[1]{Susan Faja}%
\affil[1]{Boston Children's Hospital}%
\affil[2]{Northeastern University - Boston Campus}%


\vspace{-1em}



  
  \date{May 25, 2024}


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\selectlanguage{english}
\begin{abstract}
Background Respiratory Sinus Arrhythmia Reactivity (RSA-R) correlates
both positively and negatively with externalizing behavior in autistic
individuals. These inconsistencies may result from task-based
differences. Furthermore, RSA-R is understudied in young autistic
children, despite particular challenges with externalizing behavior.
This pilot study measured RSA-R in 4-to 6-year-olds, across two
time-points, using four validated tasks with matched baseline and
challenge periods. Methods RSA and parent-reported externalizing
behavior were collected from 17 children (Mage=5.57 years). RSA-R was
measured by the difference score of the challenge task minus its
corresponding comparison task. Correlations were computed to evaluate
relationships between RSA-R and behavior. Results RSA was reliably
measured for 3/4 tasks (.694 [?] ICCs [?] .896). Only RSA-R during a social
task correlated with externalizing behavior. These results support using
a battery that measures a range of challenges, differing in social
demands, to characterize how arousal contributes to emotion regulation
demands among young autistic children.%
\end{abstract}%



\sloppy


\textbf{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 \& Obradovi\selectlanguage{polish}ć, \selectlanguage{english}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:

\textbf{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.

\textbf{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.

\textbf{Materials \& methods}

\textbf{Participants}

Participants were recruited from a larger, ongoing study of cognitive
control development in early childhood at {[}details omitted for
double-anonymized peer review{]}. Participants were originally recruited
using research registries, community events and advocacy groups,
clinics, early intervention programs, and word of mouth. Exclusionary
criteria included medical disorders or medications impacting the central
nervous system, a history of seizures or seizure medication, inability
to complete parent questionnaires or testing in English, prolonged
prenatal substance exposure, and significant sensory or motor
impairments or major physical abnormalities which limited ability to
complete the testing battery.

Participants included 19 verbal autistic children (16 male) aged 3.9 to
6.8 years (M\textsubscript{age} = 5.6, SD = 0.82 years) at their initial
visit. Sixteen children returned for the follow-up visit aged 4.0 to 6.9
years (M\textsubscript{age} = 5.6 SD = 0.89). All participants used
flexible phrase speech and had an age equivalent of at least 18 months
as assessed via the Visual Reception domain of the Mullen Scales of
Early Learning (MSEL; Mullen, 1995) as part of their participation in
the larger study within the previous two years. Diagnosis of an autism
spectrum disorder was determined using the ADOS-2 (Lord, Luyster, et
al., 2012, Lord, Rutter et al., 2012) and the ADI-R (Rutter et al.,
2003; Kim \& Lord, 2012) and DSM-5 criteria (American Psychiatric
Association, 2013) based on expert judgment of a licensed clinical
psychologist11During the COVID-19 pandemic, the CARS-2 was added to the
protocol to further confirm that children met standardized criteria for
an autism spectrum disorder.. Sample characteristics are reported in
Table 1.

\textbf{Procedure}

The Institutional Review Board at {[}details omitted for
double-anonymized peer review{]} approved all study procedures and all
parents provided written consent for their children to participate.
Table 1 provides demographic and measure characteristics, respectively.
Prior to study visits, families were provided with a social story and
habituation protocol to familiarize children with the physiological
recording equipment. Caregivers and their children completed two visits
to the lab separated by 4-6 weeks. During both visits children completed
the MacArthur Reactivity protocol (MRP; Bush et al. 2011). If children
were comfortable, ECG was recorded during the MRP. Parents completed the
Behavior Assessment System for Children (BASC) Parent Rating Scale --
Preschool or Child (PRS-P or PRS-C, respectively).

\textbf{Measures}

\emph{Externalizing Behavior - Behavior Assessment System for
Children-Second Edition (BASC-2)}

Externalizing Behavior (EB) was measured via parent report using the
Externalizing Problems composite on the Behavior Assessment System for
Children (BASC-2, Reynolds \& Kamphaus, 2004). The preschool form used
with 2- to 5-year-olds (PRS-P) yields an externalizing composite
comprised of the Hyperactivity and Aggression subscales. The child form
used with 6- to 11-year-olds (PRS-C) yields an externalizing comprised
of the Hyperactivity, Aggression, and Conduct subscales.

\emph{Emotion Regulation Paradigm - MacArthur Reactivity Protocol (MRP)}

The MacArthur Reactivity Protocol (Bush et al. 2011) includes challenges
across four different task domains and paired baseline tasks. Challenges
include a social task (talking with an experimenter); a cognitive task
(digit span); a sensory task (receiving two drops of lemon juice on the
tongue); and an emotional task (watching an age-appropriate video clip
intended to elicit fear). Baseline tasks include talking about pictures
in a book for the social domain, an easier digit span task in the
cognitive domain, identifying a drop of water for the sensory domain,
and watching a neutral video clip for the emotional domain. Baseline
tasks were designed to account for the psychomotor demands of the
corresponding challenge task and each task lasted up to two minutes.

\emph{ECG collection and RSA-R quantification}

RSA-R was extracted from each participant's electrocardiogram (ECG)
using the following steps. ECG was acquired continuously at 2000 Hz
using a BIOPAC MP150 system with ECG 100C amplifiers and analyzed
offline using the AcqKnowledge 5.0.6 software (Biopac Systems, 2018).
The ECG signal was recorded during the MacArthur Reactivity Protocol
using the ECG100C amplifier with three pre-gelled Ag/AgCl electrodes
with a lead II configuration.

Offline, ECG signals were bandpass filtered using an FIR filter from 0.5
to 35 Hertz. Next, R-R intervals were extracted for the ECG signal using
a modified Pan-Tompkins QRS detector (Pan \& Tompkins, 1985) and
resampled to 8hz after cubic spline interpolation. Data were then
visually inspected for movement artifacts or incorrect identification of
the QRS complex by the scoring algorithm.

RSA values were computed using a fast Fourier transform with a hamming
window within the respiratory frequency band that corresponded to the
participant's age (0.2-1.0Hz for children under six, 0.15-0.5Hz for
children six and older; Boyce et al., 2001, Gentzler et al. 2009). RSA
values were computed in 60 second epochs and log transformed. RSA during
the first and last 60 seconds was averaged for each baseline and
challenge task, respectively. RSA reactivity (RSA-R) reflected the
difference score for each challenge task minus its corresponding
comparison task11The psychometric properties of using a regression
residual are preferable, but more difficult to interpret. We computed
all analyses with both difference scores and with the regression
residual and all results were identical. Difference scores are reported
to increase ease of interpretation..

\emph{Analytic plan}

We characterized the feasibility of ECG collection in this sample (Aim
1) by computing the percent of collected, and subsequently usable, ECG
data for each MRP task across both visits. For participants with usable
ECG data at both visits, we ran intraclass correlations with RSA values
for corresponding tasks at visits 1 and 2 to assess the test-retest
stability of each RSA measure (Aim 1). ICC values were interpreted as
poor (\textless{} 0.4), fair (0.4-0.59), good (0.6-0.74), and excellent
(0.75-1.0; Cicchetti, 1994). Finally, for tasks with adequate ICCs, we
tested whether RSA-R related with concurrent externalizing behavior (Aim
2) at visit 1 via bivariate Pearson's correlations. Before conducting
analyses, we first confirmed that age and developmental level were not
related to RSA or externalizing scores.

According to Bujang \& Baharum~(2017) with~ 80\% power, 15 subjects with
data at both timepoints are required to detect an ICC of 0.6 (i.e.,
good). Seven subjects with data at both timepoints are required to
detect an ICC of 0.8 (i.e., excellent reliability). For Aim 2, data from
25 children would enable detection of a large effect size (\selectlanguage{romanian}ƒ2~= 0.35)
with power of 0.8 and~\selectlanguage{greek}α\selectlanguage{english}~= 0.05. Fewer children with required language
levels were available to participate given the COVID pandemic, so we may
not detect all large effects for concurrent validity estimates. Given
the study was designed to pilot the initial feasibility and stability,
we believe the data reported could still be useful for planning future
studies.

\textbf{Results}

\emph{Feasibility and Stability of MRP}

Feasibility (\% acquired data) and Stability (ICC) for each MRP task are
reported in Table 2. At each visit, most of our sample tolerated
application of the ECG equipment and provided data. In addition, RSA
values during three of the four challenge tasks had good or excellent
stability. Specifically, RSA stability during the social (.694, 95\% CI
{[}.197 .907{]}) and emotional (.693, 95\% CI {[}.157 .940{]})
challenges fell in the good range, and the cognitive challenge had
excellent stability (.817 {[}.424 .951{]}). In contrast, the sensory
challenge did not yield adequate feasibility with only 10 participants
completing both visits and stability in the fair range (.490, p
\textgreater{} .05).

\emph{Convergent Validity with Externalizing Behavior}

Externalizing behavior was negatively correlated with RSA-R recorded
during the social condition (\emph{r} = -.673\emph{, p} = .008). As
RSA-R decreased, indicating withdrawal, externalizing symptomatology
increased (see Figure 1). Externalizing behavior was not significantly
related to RSA-R measured during the cognitive or emotional conditions
(\emph{r} s \textless{} 0.468, \emph{p} s \textgreater{} .05).
Descriptive statistics of RSA-R across domains and correlations with
externalizing behavior can be found in Table 3.

\textbf{Discussion}

This study is the first to evaluate the feasibility of the MRP and
examine domain-specific RSA-R in relation to externalizing behaviors in
young autistic children. Physiological data collection was feasible for
young children, with adequate completion and good to excellent stability
of the cognitive, emotional, and social tasks, and lower completion rate
and stability of the sensory task (Aim 1). Increased RSA withdrawal
during a social challenge correlated with higher levels of externalizing
behavior (Aim 2). Taken together, our findings highlight the feasibility
of eliciting a reliable RSA response and underscore a potential
relationship between PNS reactivity in social contexts and externalizing
behaviors.

Our results support the use of the MRP. Acquisition rates suggestthat
the social, cognitive, and emotional tasks are feasible in young
autistic children with phrase speech or fluent language. Notably, fewer
children wore sensors for the full sensory condition (Visit 1: 68\%;
Visit 2: 63\%) compared with the other three tasks (79-84\%). Given
heightened sensory sensitivities in this population (Chistol et al.,
2018), gustatory sensory tasks may not be sufficiently feasible to
elicit a stable RSA signal. Nonetheless, additional task refinement to
increase acquisition rates may provide essential information about
sensory reactivity for a subgroup of young autistic children.

The negative relationship between externalizing behaviors and socially
elicited RSA-R highlights the value of measuring domain-specific
reactivity. Decreased RSA-R, or increased withdrawal, may reflect
physiological dysregulation and limited coping responses to challenging
situations (Graziano \& Derefinko, 2013; Mezzacappa et al., 1997;
Beauchaine, 2001). However, both RSA-withdrawal and reactivity may be
adaptive depending on the context (Fenning et al. 2019). Indeed,
3.5-year-olds with elevated internalizing behaviors and moderate
baseline RSA levels had fewer longitudinal externalizing problems than
those with high or low baseline RSA (Ugarte et al. 2021). Characterizing
physiological reactivity across domains could determine optimal
domain-specific or domain-independent responses.

The specificity of the relation between externalizing behavior and RSA-R
in the social domain replicates work in neurotypical individuals and may
highlight the battery's sensitivity to autism-specific regulatory
demands. In a meta-analysis, only tasks using negative emotional
reactivity RSA for non-autistic adults (Beauchaine et al., 2019).
Although cognitive and emotional differences may be impacted by the
heterogeneity of ASD, reduced social functioning is a core feature of
autism. Consequently, engaging in face-to-face interactions may place
the greatest self-regulatory demands on autistic children and best probe
reactivity. Indeed, difficulty adapting to social norms and reading
social cues has been linked to externalizing behaviors among autistic
individuals (Shea et al., 2018). Therefore, socially induced RSA may
reflect mechanisms linked with externalizing behaviors or better elicit
negative emotional reactivity amongst autistic children.

\emph{Limitations/Future Directions}

The current study has several limitations. Our pilot sample was
recruited from an ongoing longitudinal study, so feasibility may be
influenced by the familiar research setting or increased adherence to
habituation protocols at home. Still an unfamiliar team member
administered all procedures to ensure the social challenges were
comparable. The convenience sample also prevented concurrent measurement
of developmental level. Additionally, MRP task demands excluded children
using single or no words. Taken together, experimental design
modifications and larger sample sizes may elucidate how RSA relates to
externalizing behavior in a more representative sample of autistic
children.

Future studies may also benefit from collecting additional physiological
measures. While there is no ``gold-standard'' method for computing RSA,
methods are differentially impacted by artifact (Larsen et al., 2010;
Lewis et al., 2012) and by measuring RSA using obtained respiration
versus normative respiration levels (Graziano \& Derefinko, 2013).
Studies collecting both ECG and respiration could directly test the
impact of different RSA computation methods. Furthermore, given RSA and
behavioral outcomes may be dynamically impacted by co-occurring
sympathetic activity (Fenning et al., 2019), obtaining measures of PEP
or galvanic skin response could further elucidate relations between
physiological response and externalizing behavior.

\textbf{Conclusion}

The current study provides preliminary support for the use of a
domain-specific approach to examining RSA-R in autistic children. By
evaluating physiological responses during social, cognitive, emotional,
and sensory challenges, we can more precisely characterize how autistic
children self-regulate across contexts and identify what kinds of
physiological reactivity are most relevant for externalizing behavior
for autistic children. The current study is the first to find a
relationship between socially induced RSA-R and externalizing behavior
among young autistic children. Further, the feasibility of the current
protocol is encouraging for replication in a larger sample.
Understanding the physiological mechanisms underlying externalizing
behaviors supports the development of objective methods to identify
which children may respond best to behavioral support or intervention to
optimize behavioral outcomes.

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\textbf{Table 1. Sample Characteristics}\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
& N (\%)\tabularnewline
\vtop{\hbox{\strut \textbf{Assigned Sex} Male}\hbox{\strut Female}} & 16
(84.2\%) 3 (15.8\%)\tabularnewline
\vtop{\hbox{\strut \textbf{Race} American Indian/Alaskan
Native}\hbox{\strut Asian}\hbox{\strut Hawaiian/Pacific
Islander}\hbox{\strut Black/African
American}\hbox{\strut White/Caucasian}\hbox{\strut More than one
Race}\hbox{\strut Unknown/Unreported}\hbox{\strut Other}} & 0 (0.0\%) 2
(10.5\%) 0 (0.0\%) 2 (10.5\%) 14 (73.7\%) 0 (0.0\%) 0 (0.0\%) 1
(5.3\%)\tabularnewline
\vtop{\hbox{\strut \textbf{Ethnicity}
Non-Hispanic/Latine}\hbox{\strut Hispanic/Latine}} & 18 (94.7\%) 1
(5.3\%)\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 2. Feasibility and Stability of MRP}\selectlanguage{english}
\begin{longtable}[]{@{}llllll@{}}
\toprule
RSA by Task & V1 Wore sensor for full task N (\%) & V1 Data usable N
(\%) & V2 Wore sensor for full task N (\%) & V2 Data usable N (\%) & ICC
{[}95\% CI{]}\tabularnewline
Cognitive Challenge & 15 (79\%) & 14 (74\%) & 13 (81\%) & 13 (81\%) &
.817 {[}.424 .951{]}**\tabularnewline
Cognitive Comparison & 15 (79\%) & 14 (74\%) & 13 (81\%) & 13 (81\%) &
.784 {[}.344 .942{]}*\tabularnewline
Social Challenge & 16 (84\%) & 15 (79\%) & 13 (81\%) & 13 (81\%) & .694
{[}.197 .907{]}*\tabularnewline
Social Comparison & 16 (84\%) & 15 (79\%) & 13 (81\%) & 13 (81\%) & .896
{[}.660 .971{]}**\tabularnewline
Sensory Challenge & 13 (68\%) & 11 (58\%) & 10 (63\%) & 10 (63\%) & .490
{[}-.159 .843{]}\tabularnewline
Sensory Comparison & 15 (79\%) & 14 (74\%) & 13 (81\%) & 13 (81\%) &
.857 {[}.527 .962{]}**\tabularnewline
Emotional Challenge & 16 (84\%) & 14 (74\%) & 13 (81\%) & 13 (81\%) &
.693 {[}.157 .940{]}*\tabularnewline
Emotional Comparison & 16 (84\%) & 14 (74\%) & 13 (81\%) & 13 (81\%) &
.844 {[}.492 .959{]}**\tabularnewline
\bottomrule
\end{longtable}

\textbf{Note:} Feasibility is defined as the \% of children who
tolerated the sensor and provided usable data; Reliability is defined by
the ICC computed as single measure; T1 = Time 1; T2 = Time 2; * reflects
a \emph{p} -value less than .01, ** reflects a \emph{p} -value less than
.001. During the sensory task, participants were counted if they
completed both lemon juice tastes.

\textbf{Table 3. RSA-R Descriptives and Correlations with Externalizing
Behavior}\selectlanguage{english}
\begin{longtable}[]{@{}lll@{}}
\toprule
RSA-R Domain & Mean (Standard Deviation), Range & Correlation with BASC
Externalizing\tabularnewline
Social & .105 (.922), -1.40 to 2.00 & -.673**\tabularnewline
Emotional & -.21 (.021), -2.06 to 0.64 & .458\tabularnewline
Cognitive & .100 (.504), -0.72 to 1.22 & .468\tabularnewline
\bottomrule
\end{longtable}

\textbf{Note:} ** reflects a \emph{p-value} less than .001



\textbf{Figure 1. Externalizing Behavior Decreases with Increased Social
RSA-R}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Notes:} RSA-R in the Social Domain computed as the difference
between the Social challenge and Talking Baseline tasks, Externalizing
Behavior drawn from the BASC Externalizing Behavior T-score.

\subsubsection*{}

{\label{section}}

\selectlanguage{english}
\FloatBarrier
\end{document}

