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Journal of Clinical Child & Adolescent Psychology

ISSN: 1537-4416 (Print) 1537-4424 (Online) Journal homepage: http://www.tandfonline.com/loi/hcap20

Emotion Dysregulation Across Emotion Systems in


Attention Deficit/Hyperactivity Disorder

Erica D. Musser & Joel T. Nigg

To cite this article: Erica D. Musser & Joel T. Nigg (2017): Emotion Dysregulation Across
Emotion Systems in Attention Deficit/Hyperactivity Disorder, Journal of Clinical Child &
Adolescent Psychology, DOI: 10.1080/15374416.2016.1270828

To link to this article: http://dx.doi.org/10.1080/15374416.2016.1270828

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Published online: 19 Jan 2017.

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Download by: [FU Berlin] Date: 20 January 2017, At: 09:07


Journal of Clinical Child & Adolescent Psychology, 00(00), 1–13, 2017
Copyright © Society of Clinical Child & Adolescent Psychology
ISSN: 1537-4416 print/1537-4424 online
DOI: 10.1080/15374416.2016.1270828

Emotion Dysregulation Across Emotion Systems in


Attention Deficit/Hyperactivity Disorder
Erica D. Musser
Department of Psychology, Florida International University

Joel T. Nigg
Department of Psychiatry, Oregon Health & Science University

Children with attention deficit/hyperactivity disorder (ADHD) display alterations in both emotion
reactivity and regulation. One mechanism underlying such alternations may be reduced coherence
among emotion systems (i.e., autonomic, facial affect). The present study sought to examine this.
One hundred children (50 with ADHD combined presentation), 7–11 years of age (62% male, 78%
White), completed an emotion induction and suppression task. This task was coded for facial affect
behavior across both negative and positive emotion eliciting task conditions. Electrocardiogram and
impedance cardiography data were acquired throughout the task. Time-linked coherence of facial
affect behavior and autonomic reactivity and regulation were examined during the induction
conditions using hierarchical linear modeling. Although ADHD and typically developing children
did not differ with respect to rates of facial affect behavior displayed (all Fs < 2.09, ps > .29), the
ADHD group exhibited reduced coherence between facial affect behavior and an index of para-
sympathetic functioning (i.e., respiratory sinus arrhythmia), γ10 = –0.03, SE = 0.02, t(138) = –1.96,
p = .05. In contrast, children in the control group displayed a significant, positive, γ10 = 0.06,
SE = 0.01, t(138) = 4.07, p < .001, association between facial affect behavior and respiratory sinus
arrhythmia. Children with ADHD may receive conflicting emotional signals at the levels of facial
affective behavior and parasympathetic functioning when compared to typically developing youth.
Weakened coherence among these emotion systems may be an underlying mechanism of emotion
dysregulation in ADHD. Implications for etiology and treatment are discussed.

There is increasing recognition of the importance of emo- well-established, empirical investigations of mechanisms
tion reactivity and regulation in attention deficit/hyperac- contributing to disruptions in emotion reactivity and reg-
tivity disorder (ADHD). A recent meta-analysis of 77 ulation in ADHD are still relatively few. Identifying such
studies, including more than 32,000 youth, suggests that mechanisms would potentially allow for the development
ADHD is uniquely associated with both elevated emotion of novel treatments, as well as improvements in treatment
reactivity (weighted effect size [ES] d = .95) and emotion matching, given the heterogeneity observed in the disorder
dysregulation (weighted ES d = .80), with ESs similar in (Karalunas et al., 2014).
magnitude to those observed in studies of ADHD and Identifying such mechanisms requires both care and spe-
executive dysfunction (weighted ES d = .46–.69 range; cificity. Both emotion reactivity and regulation are multi-
Graziano & Garcia, 2016). Although the link between systemic, multidimensional constructs, which encapsulate a
ADHD and emotion-related dysfunction is increasingly broad range of processes (Gross & Jazaieri, 2014; Rosen,
Epstein, & van Orden, 2013; Thompson, 2011). For exam-
ple, recent work from our lab has demonstrated that ADHD
Correspondence should be addressed to Erica D. Musser, 11200 SW 8th is associated with both altered sympathetic-based emotion
Street, AHC 4 455, Miami, FL 33199. E-mail: emusser@fiu.edu reactivity (i.e., indexed via cardiac preejection period [PEP];
Color versions of one or more of the figures in the article can be found
Karalunas et al., 2014; Musser et al., 2011) and altered
online at www.tandfonline.com/hcap.
Supplemental data for this article can be accessed at http://dx.doi.org/ parasympathetic-based emotion regulation (i.e., indexed
10.1080/15374416.2016.1270828. via respiratory sinus arrhythmia [RSA]; Karalunas et al.,
2 MUSSER AND NIGG

2014; Musser et al., 2011). Further, these alterations in disrupted in the context of positive or other emotional con-
autonomic functioning appear during both induction and texts unanswered.
suppression of both negative and positive emotions Here, we seek to open this line of investigation with the
(Karalunas et al., 2014; Musser et al., 2011). first examination of emotion systems coherence in children
Crucially, however, this does not complete the picture. with ADHD. Recent theory suggests that mechanisms
Emotion reactivity and regulation are also multidimensional underlying disruptions in emotion reactivity and regulation
in terms of the presence of multiple emotion response sys- are likely shared across many domains of psychopathology
tems (e.g., facial affective behavior, subjective experience, (Gross & Jazaieri, 2014; Insel et al., 2010). Therefore, like
and autonomic nervous system (ANS) and central nervous depression, disruptive behavior disorders, and schizophre-
system responding; Ekman, 2016), which raises important nia, we hypothesize that ADHD will be related to reduced
questions about how these multiple systems work together coherence of emotion systems during emotionally evocative
or interact with one another. The functionalist theory of situations.
emotion proposes that coherence, or coordination among At a higher order, emotion responses have been demon-
an individual’s emotional response systems as the emotion strated to cluster into positive affect (e.g., happiness, excite-
unfolds over time, is a key mechanism involved in adaptive ment) or negative affect (e.g., sadness, anxiety; Lindquist,
emotion reactivity and regulation (Lench, Bench, Darbor, & Satpute, Wager, Weber, & Barrett, 2015). Other models sug-
Moore, 2015; Livingston, Kahn, & Berkman, 2015). The gest that emotional responses cluster into approach (e.g., hap-
same theory proposes that weak coherence, or poor coordi- piness) or avoidance (e.g., fear) domains (e.g., Carver, 2006;
nation across emotional response systems, increases the Carver, Johnson, & Joorman, 2009). Important to note,
probability of experiencing conflicting emotional signals although positive affect is generally associated with approach,
and, thus, maladaptive responding to emotional cues and anger may be a negative approach-based emotion (Carver &
emotion-related psychopathology (Ekman, 1992a, 1992b; Harmon-Jones, 2009). In the case of ADHD, theories have
Lench et al., 2015; Livingston et al., 2015; Mauss, Evers, proposed dysfunction both the negative and positive valence
Wilhelm, & Gross, 2006). domains, as well as some theories proposing dysfunction
In support of the proposal that poor coherence underlies specifically in the negative approach/anger domain (for a
psychopathology, weak coherence of emotional systems has review, see Nigg, 2006). This claim has received some empiri-
been reported in studies of adults with depression and cal support with findings of a diminished parasympathetic
schizophrenia (Kring, Smith, & Neale, 1993; Sloan et al., regulatory response to negative emotion induction and an
1994). In addition, one prior study has been conducted with exaggerated parasympathetic regulatory response to positive
children with disruptive behavior disorders (i.e., conduct emotion induction among children with ADHD (Musser et al.,
disorder [CD] and oppositional defiant disorder [ODD]; 2011). Furthermore, recent work by Karalunas and colleagues
Marsh, Beauchaine, & Williams, 2008). Each of these dis- (2014; in a partially overlapping sample) reveals that patterns
orders has also been characterized by disruptions in both of autonomic-linked emotion responding that are specific to
emotion reactivity and regulation (Kring et al., 1993; Marsh either the negative or positive valence domains may help to
et al., 2008; Sloan et al., 1994). Coherence is presumed to explain some of the behavioral heterogeneity observed in
increase over time with development (Lench et al., 2015; ADHD. Thus, the present study examined emotional response
Livingston et al., 2015). However, this has yet to be exam- coherence in the context of both negative and positive emotion
ined in the context of developmental psychopathology induction.
except for one preliminary, cross-sectional study (Marsh In the present study, two hypotheses were examined. H1:
et al., 2008). Children with ADHD will show weaker statistical correspon-
In the only prior study to examine emotion response dence (i.e., coherence) between emotion response systems
coherence among children with disruptive behavior disor- including autonomic reactivity and facial affective behavior,
ders, Marsh and colleagues (2008) examined time-linked during both negative and positive emotion induction, when
coherence of sad facial expressions and autonomic reactivity compared to typically developing youth. Thus, a Group (i.e.,
in the context of an emotionally evocative film clip. This ADHD or control) × Facial Affect Behavior (i.e., negative and/
study included a sample of 31 boys with disruptive behavior or positive affect) two-way interaction was examined in pre-
disorders and 23 controls, 9–13 years of age (Marsh et al., dicting autonomic functioning in both the parasympathetic
2008). Reduced coherence among sad facial affect behavior (i.e., RSA) and sympathetic (i.e., PEP) branches. H2:
and autonomic reactivity across both the parasympathetic Statistical correspondence (i.e., coherence) between auto-
and sympathetic branches was observed. However, the small nomic nervous system activity and facial affective behavior
sample size did not allow for an examination of ADHD will be specific to task context (i.e., negative induction vs.
symptoms or diagnoses, specifically. Further, coherence positive induction) for typically developing youth (but not for
among emotional systems was examined only in the context children with ADHD). That is, it is expected that positive facial
of negative (i.e., sad) emotion induction, leaving questions affect will be associated with autonomic functioning during
regarding whether emotion systems coherence may be positive induction, whereas negative facial affect behavior will
EMOTION DYSREGULATION ACROSS EMOTION SYSTEMS IN ADHD 3

be associated with autonomic functioning during negative Families were recruited from the greater Portland,
induction for typically developing youth. Thus, a Group (i.e., Oregon, metropolitan area through commercial mailings to
ADHD or control) × Condition Type (i.e., negative or positive all households in the community with children in the target
induction) × Facial Affective Behavior (i.e., negative and/or age range, as well as via public advertising. The local
positive facial affect) three-way interaction interaction was Institutional Review Board approved the study. Parents pro-
also examined in predicting autonomic functioning in both vided written informed consent, and children provided writ-
the parasympathetic (i.e., RSA) and sympathetic (i.e., PEP) ten assent. Parents and children were compensated for their
branches. time. All procedures conformed to the Ethical Principles of
Psychologists and Code of Conduct (APA, 2010).
Families volunteering for the study passed through a
METHOD multigate screening process to establish eligibility and diag-
nostic group assignment following procedures identical to
Participants those described in detail elsewhere (Musser et al., 2011) At
the first gate, basic rule outs were checked (see the upcom-
Participants were 100 children, 7 to 11 years of age (M
ing section). At the second gate, parents completed a struc-
age = 8.59, SD = 1.24 years). Fifty met Diagnostic and
tured, diagnostic interview (Kiddie Schedule for Affective
Statistical Manual of Mental Disorders (5th ed.; DSM-5;
Disorders and Schizophrenia for School-Aged Children–
American Psychiatric Association [APA], 2013) criteria for
Epidemiologic Version [KSADS-E]; Puig-Antich & Ryan,
ADHD combined presentation (ADHD), and 50 were typi-
1996), and parents and teachers completed standardized
cally developing comparison youth. Siblings were not
rating scales. Children completed an IQ screener and stan-
included in this sample. Table 1 displays demographic and
dardized rating scales. In addition, clinical observers wrote
diagnostic characteristics. The age range was selected, as
detailed notes. Finally, a clinical diagnostic team (i.e., a
this is the age of typical onset of ADHD and to ensure
board-certified psychiatrist and licensed clinical psycholo-
confirmed onset before age 12 (APA, 2013).
gist) independently reviewed all information to arrive at a
diagnosis using DSM-IV (APA, 1994) and DSM-5 criteria
(the children included here met criteria by both DSM-IV and
Recruitment and Identification Procedures
DSM-5). Interrater agreement was acceptable with (k > .70

TABLE 1
Descriptive and Diagnostic Statistics for ADHD and Control Groups

Variable Controla ADHDb p Partial η2

Demographics
Age (Months; M, SD) 103.51 (15.04) 102.64 (14.69) .775 0.001
Gender (% Male) 52.0% 72.0% .015* 0.057
Race (% White) 76.0% 80.0% .632 0.003
Family Income ($K; M, SD) 99.5 (27.52) 78.13 (24.90) .016* 0.060
Stimulant Medication (% on Medication) 0.0% 40.0% < .001* 0.135

WISC-IV FSIQ (M, SD) 111.33 (11.48) 108.54 (14.05) .162 0.024
ADHD-RS T Scores–Parent (M, SD)
Hyperactive/Impulsive 43.65 (5.36) 71.61 (10.94) < .001* 0.745
Inattentive 43.48 (6.05) 73.09 (12.40) < .001* 0.719
Total 43.04 (5.34) 74.01 (11.10) .001* 0.779
Comorbid Disorders (%; K-SADSc)
Anxiety Disorder 26.0% 32.0% .651 0.004
Conduct Disorder 0.0% 4.0% .167 0.029
Oppositional Defiant Disorder 0.0% 22.0% < .001* 0.181

Note: For continuous variables, including age, family income, estimated Full-Scale IQ, Attention Deficit/Hyperactivity Disorder Rating Scale (ADHD-RS)
parent-rated subscales, and chi-square comparisons for categorical variables, including gender, race, child medication status, and comorbid disorders. WISC-IV
= Wechsler Intelligence Scale for Children; FSIQ = Full-Scale Intelligence Quotient (estimated); K-SADS = Kiddie Schedule of Affective Disorders and
Schizophrenia.
a
n = 50.
b
n = 50.
c
0% of the sample had autism, eating disorders, learning disorders, mood, posttraumatic stress disorder, psychosis, or substance use disorders.
*significant at p < .05.
4 MUSSER AND NIGG

for all disorders with base rates greater than 5%, including In the induction condition, children were asked to
ADHD). Disagreement was resolved by conference. facially mimic the emotion of the main character. This
A diagnosis of ADHD required that the child’s symptoms instruction was given for the first negative and first positive
had a cross-situational presentation, had evidence of impair- segment. In the suppression condition, the child was asked
ment, had onset by age 7 (so children would meet both to imagine what the main character was feeling but to keep
DSM-IV and DSM-5 criteria), and were not accounted for his or her face still, masking (suppressing) the emotion. This
by another disorder. Symptoms were counted as present if instruction was given for the second negative and second
endorsed by the parent on the KSADS-E or the teacher on positive segment. Thus, the same sequence of the four task
the ADHD Rating Scale. Further, children were required to conditions was presented to each child: (a) negative induc-
have elevated teacher and parent ratings of at least T > 65 on tion, (b) negative suppression, (c) positive induction, and (d)
at least one major subscale of the ADHD Rating Scale. To positive suppression. These conditions were not counter-
limit excessive false positives from the “or” algorithm, the balanced, as (a) it was important to end with positive emo-
teacher was able to contribute a maximum of two additional tion for human subjects’ welfare, (b) the film was a
symptoms (i.e., at least four symptoms had to be identified continuous story and changing the order would confound
on the KSADS-E); the “or” algorithm was invoked in only suppression with cognitive challenge to interpret the story,
four cases. This procedure was modified from that used in and (c) putting induction prior to suppression maximized the
the DSM-IV field trials and the MTA study (MTA suppression challenge.
Cooperative Group, 1999). Important to note, only the negative and positive emotion
induction conditions were utilized in the present study, as prior
Exclusion Criteria work suggests emotional suppression is associated with
reduced emotion response coherence across the domains of
Exclusion criteria included the uses of psychoactive med-
facial affect and autonomic responsivity (Gross & Levenson,
ications that could not be washed out for the study as
1993; Mauss, Levenson, McCarter, Wilhelm, & Gross, 2005).
described next (i.e., long-acting and nonstimulant psychia-
Further, the primary research question being addressed herein
tric medications, such as antidepressants), an estimated Full
is related to emotional coherence during emotional experience
Scale IQ less than 75, current major depressive episode,
rather than during the suppression of emotions.
lifetime mania or psychosis, pervasive developmental dis-
order, or learning disability. Other disorders were free to
Facial Action Coding System
vary.
After data collection was complete, children’s facial
Medication Washout affect was coded from recordings using a simplified version
of the Facial Action Coding System (Ekman, 1992b), for the
Prior to completing the tasks, children taking stimulant
negative and positive induction task segments, by two
medication (i.e., 40% of the ADHD group) completed a
research assistants masked to condition and child group
medication washout equivalent to a minimum of five half-
status. Forty percent of videos were coded for reliability
lives (i.e., 24–48 hr, depending on preparation).
(all ICCs > .85). For the purposes of this study, only six
facial affective behavior frequency domains were coded
Emotion Induction (and Suppression) Task (i.e., Facial Action Coding System was simplified to focus
on only six emotions intended to reflect positive [happiness]
Each child was recorded as they completed the Emotion
and negative [anger, anxiety, fear, and sadness] valence, as
Induction (and Suppression) Task (Musser et al., 2011). This
well as surprise). The full Facial Action Coding System has
involved watching four 2-min film clips taken from
been well validated with standard interrater reliabilities of
Homeward Bound (Dunham, 1993), a film about two dogs
α = .89 (Gross & Levenson, 1993).
and a cat who are separated from their child owners (nega-
tive emotion eliciting; 1ʹ25”–1ʹ29” of the film; during which
the animals are discouraged and one is injured) and reunited Physiological Recording
with their human family (positive emotion eliciting; 1ʹ32”–
Overview
1ʹ36” of the film, during which the animals happily find,
greet, and play with the as they are reunited family). Prior Disposable silver/silver-chloride electrodes were placed
work from our team has demonstrated the validity of these in a standard electrocardiogram (ECG) and impedance car-
conditions using the Self-Assessment Manikin Valence and diography (ICG) configuration. The ECG electrodes were
Arousal scales (Bradley & Lang, 1994) for each clip, and placed at the right collarbone and the tenth-left rib with a
this work has demonstrated that ADHD and typically devel- ground electrode placed at the tenth-right rib. For ICG, two
oping youth do not differ in their ratings of these clips (for voltage electrodes were placed below the suprasternal notch
validity data, see Musser et al., 2011). and xiphoid process, and two current electrodes were placed
on the back 3 to 4 cm above and below the placement of the
EMOTION DYSREGULATION ACROSS EMOTION SYSTEMS IN ADHD 5

voltage electrodes. ECG and ICG were recorded continu- side of a cubicle-style barrier, able to see the child via a
ously throughout each of the baselines (2 min of rest and webcam but not viewable by the child. The child was
2 min of neutral baseline) and each of the task epochs instructed to be as still and quite as possible.
(2 min of negative induction and 2 min of positive induc- A neutral baseline period of approximately 2 min was
tion). The R-R series was sampled at 1000 Hz. Heart rate, presented between the negative and positive task conditions.
inner-beat-interval, and respiration rate were derived using The neutral baseline required the child to observe a set of 10
ECG and ICG data after data collection. Artifacts were neutral pictures from the International Affective Picture
examined and removed using MindWare Heart Rate System (including pictures of beads, tires, clouds, mush-
Variability and Impedance Cardiography v. 2.6 softwares rooms, a cup, dustpan, hydrant, lightbulb, pillar, and spoon;
completed by two raters with satisfactory interrater agree- Lang, Bradley, & Cuthbert, 1997) on a computer screen.
ment (k > .85 for each epoch). No between-group differ- Each picture was presented for 10 s. This baseline was used
ences were observed in the rate of artifacts (all ps > .50). to account for physiological responses associated with
orienting and attending to a stimulus (Jennings, van der
Respiratory Sinus Arrhythmia Molen, & Somsen, 1998). The Self-Assessment Mankin
Valence and Arousal scales were presented to children on
RSA was indexed by extracting the high-frequency com-
the computer screen between each picture, and responses
ponent (> 0.15 Hz) of the R-R peak time series. RSA has
were self-paced. Prior work from our team has demonstrated
good long-term temporal consistency and predicts vagal
the validity of these pictures as neutral using the Self-
control during pharmacological blockade (Berntson,
Assessment Mankin Valence and Arousal scales (Bradley
Cacioppo, & Quigley, 1993). RSA was derived using spec-
& Lang, 1994; for validity data, see Musser et al., 2011).
tral analysis of the R-R time series (Berntson et al., 1997;
Wilhelm, Grossman, & Roth, 2005) and processed in 30-s
epochs (i.e., four 30-s epochs per 2-min baseline and task Data Analysis Plan
condition), using MindWare Heart Rate Variability V. 2.6
Data Reduction for Primary Analyses
(MindWare, 2008a). The time series was detrended and
submitted to a Fourier transformation. The high-frequency First, to reduce concerns related to model oversaturation
band (ln(ms2)) was set over the respiratory frequency band and to enhance the likelihood that models would converge,
of 0.24 to 1.040 Hz. Respiratory rates and amplitudes were only the facial affect behavior codes and autonomic indexes
derived from the impedance cardiograph signal (Zo), ensur- obtained during the 1st min of each of the negative and
ing that these signals remained within the analytical band- positive induction conditions were utilized (i.e., two 30-s
width. RSA means and standard deviations for each of the epochs per task condition).
task conditions are reported by group in Table S1 in the Second, prior empirical work has supported a bifactor
online supplemental material. solution for emotion, including positive and negative
valence (Carver & Scheier, 1990; Lindquist et al., 2015).
Cardiac Preejection Period As such, models were examined including frequencies of
facial affective behavior domains of positive (happiness)
PEP was derived from ECG and ICG in 30-se epochs
and negative (anger, anxiety, sadness) valence. Frequency
(i.e., four 30-s epochs per 2-min baseline and task condi-
codes for fear and surprise were omitted from these models,
tion), using MindWare Impedance Cardiography V. 2.6
given that both fear and surprise were coded relatively
(MindWare, 2008b). This system allows for simultaneous
infrequently and there is evidence that surprise may load
editing of the data obtained from ECG and ICG. PEP was
on either positive or negative valence depending on context
indexed as the time interval (in milliseconds) from the onset
(Carver, 2006). Positive and negative valence facial affec-
of the Q-wave to the B point of the dZ/dt wave, using the
tive behavior were examined in a single model.
method outlined by Berntson, Lozano, Chen, and Cacioppo
In addition, to further probe the specificity of coherence
(2004). PEP means and standard deviations for each of the
between autonomic functioning and specific facial affective
task conditions are reported by group in Table S1.
behaviors, the frequencies of each the six, specific facial
affective behavior codes (i.e., anger, anxiety, fear, happi-
Physiological Baseline Conditions
ness, sadness, and surprise) were examined as predictors of
A resting baseline period of 2 min was presented before autonomic functioning via separate models for each. For
the Emotion Induction and Suppression Task. Prior to com- frequencies of each of the positive, negative, and specific
pleting the resting baseline condition, the electrodes were coded facial affect behavior domains arranged by task con-
placed on the child (as described previously), and the child dition and group, see Table S2.
was given the opportunity to engage in a period of play for
5 min. For the resting baseline period, the child was seated Primary analyses. Hierarchical linear modeling
in a quiet room with an experimenter seated on the other (HLM) was used to analyze levels of coherence among
6 MUSSER AND NIGG

indexes of emotion, including facial affective behavior β5j = γ50 + γ51(GROUPj)


(modified Facial Action Coding System ratings) and phy- β6j = γ60 + γ61(GROUPj)
siological measures (RSA and PEP, in separate models) to
where ANSij represents RSA (and PEP in a separate model),
test the hypothesis that children with ADHD would show
POSITIVE FACIAL AFFECT ij represents the frequency of
weaker statistical coherence among indexes of emotion,
positive facial affective behavior, NEGATIVE FACIAL
including autonomic reactivity and facial affect. All models
AFFECTij represents the frequency of negative facial affec-
were analyzed in HLM 6.0 (Raudenbush, Bryk, Cheong, &
tive behavior, TASK CONDITIONi is a dummy-coded vari-
Congdon, 2004).
able representing whether the stimulus condition involved
The outcome variables were ANS activity (i.e., RSA,
negative = –1 or positive = 1 emotional stimuli, POSITIVE
PEP in separate models). At Level 1, three types of vari-
ACIAL AFFECT 1*TASK CONDITIONij represents the
ables were included in the model simultaneously. First,
interaction of positive facial affective behavior frequency
facial affective behavior (i.e., positive and negative valence)
and task condition (i.e., negative vs. positive induction),
was treated as a predictor of ANS activity (first for RSA,
NEGATIVE FACIAL AFFECT *TASK CONDITIONij repre-
then PEP in a separate model). Second, the stimulus condi-
sents the interaction of negative facial affective behavior
tion (i.e., negative and positive induction) was included as a
frequency and task condition (i.e., negative vs. positive
dummy-coded variable (negative = –1, positive = 1). Third,
induction). Finally, GROUPj is a dummy-coded variable
the interaction term of the type of stimulus condition with
representing ADHD = 1 or control = –1 group status.
the coded facial affective behavior rating was included at
Thus, two primary models were examined, including a
Level 1 to examine the prediction of ANS activity (i.e.,
RSA as an outcome of interest in the first model and PEP
RSA, then PEP) by frequency of facial affective behavior
as an outcome of interest in the second model.
by stimulus valence. Thus, the model examined statistical
Finally, modified models for each of the six specific
coherence during conditions of negative induction com-
facial affective behaviors (utilizing only a single
pared to positive induction.
SPECIFIC FACIAL AFFECT FREQUENCY and
At Level 2, group effects were tested using a dummy-
SPECIFIC FACIAL AFFECT FREQUENCY*TASK
coded time invariant variable (1 = ADHD, 0 = control). It
CONDITION term) were examined for both RSA and PEP.
was expected that the associations between ANS activity
(i.e., RSA and PEP) and facial affective behavior (i.e.,
positive and negative valence) would be moderated by an
RESULTS
across-level, three-way interaction—Group (i.e., ADHD or
control, Level 2) × Stimulus Valence Condition Type (i.e.,
Preliminary Analyses
negative or positive, Level 1) × Facial Affective Behavior
(i.e., positive and negative valence, Level 1), which would Descriptive and Diagnostic Overview of Sample
represent a task-specific response pattern. For example, it
Descriptive and diagnostic statistics are reported for by group
was expected that positive-valence facial affective behavior
in Table 1. Groups did not differ reliably with respect to age,
would predict ANS activity under positive induction,
race, IQ, or presence of either anxiety or CD diagnosis. Groups
whereas negative valence facial affective behavior would
differed in gender ratio (more boys in the ADHD than control
predict ANS activity under negative induction for the con-
group), and family income (families of ADHD children earning
trol group. Further, it was hypothesized that these associa-
less than control children). In addition, 40% of the ADHD
tions would be diminished in the ADHD group.
sample was prescribed a stimulant medication, and 22% of the
Thus, the full equations for the bi-factor (i.e., positive/
ADHD sample met criteria for ODD diagnosis. Important to
negative) models were as follows:
note, the inclusion of age, anxiety or CD diagnosis, gender,
income, IQ, medication status, or race did not alter the primary
Level 1:
results. As such, for simplicity and to reduce model oversatura-
ANSij = β0j + β1j (TIMEij) + β2j(POSITIVE FACIAL
tion, all models are presented without these potential covariates.
AFFECTij) + β3j(NEGATIVE FACIAL AFFECTij) + β4j
However, ODD diagnosis emerged as a relevant covariate such
(TASK CONDITIONij) + β5j(POSITIVE FACIAL
that when included, patterns of significance were altered. As
AFFECT*TASK CONDITIONij) + β6j(NEGATIVE FACIAL
such, results are presented with the inclusion of ODD diagnosis
AFFECT*TASK CONDITIONij) + rij
as a Level 2, time-invariant covariate.
Level 2:
β0j = γ00 + γ01(GROUPj) + u0j Primary Analyses
β1j = γ10 + γ11(GROUPj)
β2j = γ20 + γ21(GROUPj) To test the primary hypotheses that (a) children with ADHD
β3j = γ30 + γ31(GROUPj) would show weaker statistical correspondence (i.e., coher-
β4j = γ40 + γ41(GROUPj) ence) among indexes of positive emotion (i.e., autonomic
EMOTION DYSREGULATION ACROSS EMOTION SYSTEMS IN ADHD 7

reactivity and facial affective behavior) during positive (γ41 = −0.05, SE = 0.01), –(282) = –3.81, p < .001,
induction and (b) children with ADHD would show weaker emerged, suggesting that coherence between negative
statistical correspondence among indexes of negative emo- facial affect behavior and RSA was moderated by group
tion during negative induction, when compared to controls, status (when collapsed across negative and positive induc-
two separate (i.e., one for RSA and one for PEP) two-level tion task conditions). Specifically, the association between
models were constructed. negative facial affect behavior and RSA for controls was
positive (γ10 = 0.06, SE = 0.01), t(138) = 4.07, p < .001,
Predicting RSA From ADHD, Positive and Negative whereas the association between negative facial affect
Facial Affective Behavior, and Task Condition behavior and RSA for the ADHD group was negative
and failed to reach significance (γ10 = –0.03, SE = 0.02),
Full model details are provided in Table 2. Only exam-
t(138) = –1.96, p = .05 (Figure 1). Thus, it appears that
inations of the hypotheses are noted in the text. Specifically,
ADHD children have reduced coherence between RSA and
the three-way interactions predicting RSA from Positive
negative facial affect compared to typically developing
Facial Affective Behavior × Task Condition × Group and
youth, irrespective of the nature of the emotional context.
Negative Facial Affective Behavior × Task Condition ×
Group were examined. As noted in the hypotheses, positive
Predicting PEP From ADHD, Positive and Negative
facial affect was of interest during the positive emotion
Facial Affective Behavior, and Task Condition
induction condition and negative facial affect was of interest
during the negative emotion induction condition. Full model details are provided in Table 2. With PEP as
With respect to positive facial affective behavior, the the outcome variable of interest, there was a main effect of
Group × Positive Facial Affective Behavior × Task the ODD covariate (γ02 = –4.29, SE = 1.97), t(99) = –2.18,
Condition (i.e., positive vs. negative induction) three-way p = .03 (see Table 2). An examination of PEP grand means
interaction was significant (γ51 = –0.03, SE = 0.01), t according to ODD diagnostic status reveals that children
(288) = −2.15, p = .03. However, when ODD diagnosis without a diagnosis of ODD (M = 96.60, SD = 10.07) had
was included in the model as a Level 2, time-invariant significantly greater PEP across task conditions compared to
covariate, this three-way interaction became nonsignificant children with ODD (M = 91.23, SD = 8.81), F(1, 99) = 3.18,
(γ51 = –0.02, SE = 0.01), t(282) = –1.56, p = .11. None of p = .04. However, for PEP, none of the other main effects or
the other main effects or two-way or three-way interactions two-way or three-way interactions (including those related
involving positive facial affect behavior were significant, all to ADHD diagnoses) were significant predictors (all
ts(282) < 1.70, all ps > .10. Thus, positive facial affect ts < 1.5, ps > .11; see Table 2).
behavior was not considered further in this model.
A different pattern emerged for Negative facial affective
Individual Emotion Specificity Checks
behavior. In contrast to the primary hypothesis, the Group
× Negative Facial Affect Behavior × Task Condition three- To examine whether children with ADHD show weaker
way interaction was nonsignificant (γ61 = –0.01, statistical correspondence among indexes of each of the
SE = 0.01), t(282) = –0.94, p = .35. However, in support six specific emotions based on task condition, similar two-
of the weakened coherence hypothesis, a significant Group level models to those previously described were constructed
× Negative Facial Affect Behavior two-way interaction (with RSA and PEP in separate models). However, in these
Beta coefficient for the association between RSA and

0.08

0.06

0.04
negative facial affect

0.02

-0.02

-0.04

-0.06
Control ADHD

FIGURE 1 Hierarchical linear modeling results of correspondence (standardized beta weights) between negative facial affective behavior type and
respiratory sinus arrhythmia (RSA) across induction conditions (negative and positive collapsed). Note: ADHD = attention deficit/hyperactivity disorder.
8
TABLE 2
Hierarchical Linear Models of Group, Facial Affective Behaviors, and Task Condition Predicting Autonomic Response Primary Analyses Secondary Analyses

Positive (1) and Negative (2)a (γ, SE) Angerb (γ, SE) Anxiousc (γ, SE) Happyd (γ, SE) Sade (γ, SE) Surprisef (γ, SE)

Outcome: RSA Interceptg 6.03, 0.38** 6.22, 0.46** 6.34, 0.36** 6.19, 0.39** 6.06, 0.46**
6.04, 0.38**
Intercept × ADHDh 0.17, 0.20 0.06, 0.20 0.01, 0.19 0.13, 0.19 0.04, 0.20
0.12, 0.20
MUSSER AND NIGG

Intercept × ODDi 0.38, 0.23 0.45, 0.34 0.44, 0.23 0.38, 0.25 0.65, 0.34
0.45, 0.26
Timej 0.05, 0.13 −0.02, 0.14 −0.08, 0.12 −0.02, 0.13 −0.01, 0.14
0.04, 0.13
Time × ADHD −0.03, 0.07 0.01, 0.06 0.04, 0.07 −0.01, 0.07 0.02, 0.06
–0.01, 0.07
Time × ODD 0.01, 0.09 −0.02, 0.11 −0.01, 0.08 0.01, 0.09 −0.06, 0.11
–0.01, 0.09
Task Conditionk −0.43, 0.24 −0.09, 0.16 −0.17, 0.20 −0.08, 0.16 −0.11, 0.17
–0.17, 0.18
Task Condition × ADHD 0.07, 0.11 −0.05, 0.07 −0.06, 0.09 −0.01, 0.07 −0.05, 0.07
–0.05, 0.09
Task Condition × ODD 1.13, 0.20 0.06, 0.12 0.18, 0.17 0.01, 0.11 0.11, 0.12
0.08, 0.12
Facial Affect 1l 0.06, 0.04 0.51, 0.17* 0.05, 0.04 0.07, 0.09 −0.54, 0.23
0.10, 0.03**
Facial Affect 1 × ADHD −0.01, 0.02 −0.15, 0.06* −0.01, 0.02 −0.04, 0.03 0.05, 0.05
−0.05, 0.01*
Facial Affect 1 × ODD −0.02, 0.03 −0.04, 0.12 −0.02, 0.04 < 0.01, 0.09 0.22, 0.22
< 0.01, 0.02
Facial Affect 2m 0.10, 0.03** — — — —
Facial Affect 2 × ADHD −0.05, 0.01** — — — —
Facial Affect 2 × ODD < 0.01, 0.01 — —
Facial Affect 1 × Task Condition 0.07, 0.04 0.26, 0.18# 0.05, 0.04 −0.07, 0.07 −0.28, 0.22
0.03, 0.03
Facial Affect 1 × Task Condition × ADHD −0.02, 0.01* −0.13, 0.06* −0.01, 0.01 −0.04, 0.04 −0.04, 0.05
< 0.01, 0.02
Facial Affect 1 × Task Condition × ODD −0.03, 0.03 0.12, 0.12 −0.02, 0.04 0.12, 0.09 0.31, 0.20
–0.01, 0.01
Facial Affect 2 × Task Condition 0.03, 0.02 — — — —
Facial Affect 2 × Task Condition × ADHD −0.01, 0.01 — — — —
Facial Affect 2 × Task Condition × ODD < 0.01, 0.02 — — —
Outcome: Cardiac PEP Intercept 104.27, 3.47** 103.95, 4.13** 103.37, 3.29** 104.71, 3.25** 102.25, 4.18
102.95, 3.17**
Intercept × ADHD −1.17, 1.70 −1.43, 1.84 −0.56, 1.63 −1.61, 1.64 −1.06, 1.84
–1.43, 1.63
Intercept × ODD −4.29, 1.97* −4.31, 3.04 −4.82, 1.97* −4.20, 1.99* −3.59, 3.06
–3.39, 1.82
Time −1.11, 1.06 −1.08, 1.29 −0.75, 1.01 −1.59, 0.98 −0.41, 1.29
–0.66, 0.98
Time × ADHD −0.25, 0.51 −0.11, 0.58 −0.50, 0.47 −0.06, 0.48 −0.27, 0.57
–0.11, 0.48
Time × ODD 1.03, 0.72 1.06, 0.95 1.25, 0.69 1.28, 0.73 0.82, 0.94
0.69, 0.69
Task Condition −0.80, 2.48 0.71, 1.47 0.60, 1.58 −0.34, 2.06 1.61, 1.24 −0.10, 1.50
Task Condition × ADHD −0.18, 0.91 0.23, 0.66 0.28, 0.66 −0.03, 0.79 0.26, 0.67 0.53, 0.66
Task Condition × ODD 1.11, 1.93 −0.95, 1.07 −0.71, 0.80 0.02, 1.60 −1.56, 0.88 −0.90, 1.07
Facial Affect 1 0.34, 0.54 −1.10, 1.56 0.14, 0.32 0.14, 0.60 −2.75, 0.90* 1.20, 2.07
Facial Affect 1 × ADHD 0.24, 0.15 0.87, 0.53 −0.02, 0.15 0.35, 0.20 0.28, 0.27 −0.61, 0.49
Facial Affect 1 × ODD −0.61, 0.42 −1.51, 1.06 −0.03, 0.22 −0.61, 0.41 2.07, 0.70* 0.70, 1.93
Facial Affect 2 −0.04, 0.33 — — — — —
Facial Affect 2 × ADHD 0.01, 0.13 — — — — —
Facial Affect 2 × ODD −0.04, 0.23 — — — — —
Facial Affect 1 × Task Condition 0.48, 0.46 −0.86, 1.58 0.14, 0.29 0.29, 0.50 0.25, 0.71 1.05, 1.93
Facial Affect 1 × Task Condition × ADHD 0.12, 0.19 0.82, 0.53 0.04, 0.12 0.21, 0.23 −0.09, 0.28 −0.66, 0.47
Facial Affect 1 × Task Condition × ODD −0.50, 0.42 −1.31, 1.07 −0.22, 0.11* −0.44, 0.48 −0.29, 0.58 0.77, 1.77
Facial Affect 2 × Task Condition 0.06, 0.25 — — — —
Facial Affect 2 × Task Condition × ADHD 0.05, 0.10 — — — —
Facial Affect 2 × Task Condition × ODD −0.23, 0.17 — — — —

Note: Hierarchical linear modeling (HLM) was used to predict the outcome variables (i.e., respiratory sinus arrhythmia [RSA] and preejection period [PEP], in separate models) just listed. The predictors
included in each model include the unstandardized beta weight for the predictor of interest.
a
Positive (1) and Negative (2): Models including facial affect behavior frequency domains of both positive (i.e., Facial Affect 1) and negative affect (i.e., Facial Affect 2).
b
Angry: Models including facial affect behavior frequency domain of anger.
c
Anxious: Models including facial affect behavior frequency domain of anxious.
d
Happy: Models including facial affect behavior frequency domain of happy.
e
Sad: Models including facial affect behavior frequency domain of sad.
f
Surprise: Models including facial affect behavior frequency domain of surprise.
g
Intercept: The intercept of each of the individual models being examined.
h
ADHD = attention deficit/hyperactivity disorder group status
i
ODD = oppositional defiant disorder group status
j
Time: 30-s epoch of task time.
k
Task condition: Negative induction versus positive induction condition.
l
Facial Affect 1*: First (or only) facial action coding system frequency.
m
Facial Affect 2: Second (not included in specific emotion models) facial action coding system frequency.
*p < .05. **p < .01.
— indicates that this specific main effect or interaction was not considered in the included specific emotion model.
EMOTION DYSREGULATION ACROSS EMOTION SYSTEMS IN ADHD
9
10 MUSSER AND NIGG

models, each of the six facial affect behaviors that were DISCUSSION
coded (i.e., anger, anxiety, fear, happiness, sadness, and
surprise) were examined separately. This study examined the coherence of facial affect behavior
and autonomic indices of emotion reactivity and regulation
Predicting RSA From ADHD, Specific Facial in children with and without ADHD. The two-factor struc-
Affective Behavior, and Task Condition ture of emotion valence (i.e., positive vs. negative valence)
used here reflects that described in previous literature
Full model details are provided in Table 2 for each of
(Carver & Scheier, 1990; Lindquist et al., 2015).
the models examined (excluding the model for fear, as
this model failed to converge). Of each of the models The primary hypothesis was that children with ADHD
examined, only the model including anger resulted in a would show weaker coherence among indexes of emotion
significant Group × Facial Affect Behavior × Task reactivity and regulation, including autonomic reactivity and
Condition three-way interaction predicting RSA facial affect behavior, when compared to typically develop-
(γ41 = −0.13, SE = 0.06), t(288) = −2.16, p = .03 (see ing children, during induction of both negative and positive
Table 2). In decomposing the three-way interaction emotions. Specifically, it was hypothesized that reduced
according to group, for controls the two-way interaction coherence between positive facial affect behavior and ANS
of Angry Facial Affect Behavior × Task Condition was activity (both RSA and PEP) would be more salient in the
significant (γ41 = 0.06, SE = 0.01), t(138) = 4.07, positive induction condition, whereas reduced coherence
p < .001, whereas the two-way interaction failed to failed between negative facial affect behavior and ANS activity
to reach significance for the ADHD group (γ41 = –0.12, would be more salient in the negative induction condition
SE = 0.18), t(138) = −0.65, p = .51. Further decomposi- (for both RSA and PEP). This double dissociation was
tion of the significant two-way interaction between Angry largely the case, in the parasympathetic domains, but with
Facial Affect Behavior × Task Condition for controls some important caveats.
according to task condition revealed that angry facial Specifically, during the positive emotion induction
affect behavior was significantly associated with RSA in condition, facial expressions of positive emotion were
the negative task induction condition (γ21 = 0.49, associated with PNS withdrawal (i.e., decreased RSA)
SE = 0.11), t(48) = 4.41, p < .001, but not the positive for typically developing children. However, the opposite
induction task condition (γ21 = 0.05, SE = 0.05), t pattern emerged for children with ADHD, such that posi-
(48) = 0.92, p = .363. tive emotions were associated with increased PNS activity
(i.e., increased RSA). This is congruent with theories
In addition, there was also a significant two-way inter- suggesting that children with ADHD may misinterpret
action of anxious facial affective behavior by group positive emotions and treat them as something aversive,
(γ31 = −0.04, SE = 0.01), t(288) = −2.97, p = .003 (see which needs to be regulated (Braaten & Rosen, 2000;
Table 2). Decomposition by group revealed, the associa- Cohen & Strayer, 1996; Izard et al., 2001). In addition,
tion between anxious facial affect and RSA for controls these results are supportive of several theories of the roles
was positive (γ20 = 0.05, SE = 0.02), t(149) = 2.81, of temperament in ADHD have suggested that disruptions
p = .006, whereas the association between negative facial in the positive emotion domain may be particularly sali-
affect behavior and RSA for the ADHD group was nega- ent to ADHD (Martel, 2009; Nigg, 2006). Important to
tive and failed to reach significance (γ20 = –0.03, note, however, with the inclusion of ODD as a covariate
SE = 0.02), t(149) = −1.89, p = .06. in this model, the pattern of significance no longer held.
Each of the other main effects, two-way, and three-way That is, when ODD was included as a covariate in this
interactions predicting RSA across each of the models model, there was no effect of ADHD diagnosis on posi-
examining specific facial affective facial behaviors were tive emotion.
nonsignificant (all ts < 1.6, ps > .10; see Table 2). The examination of negative facial affect revealed an
important caveat. In contrast to our hypothesis, there was
Predicting PEP From ADHD, Specific Facial no specificity with respect to task condition, but rather a
Affective Behavior, and Task Condition positive association between negative facial affect and
Again, full model details are provided in Table 2. For parasympathetic functioning was observed across task
each of the models examining the five facial affect beha- conditions for the control group but not the ADHD
viors with PEP as the outcome variable of interest, none group. Thus, in children with ADHD, coherence between
of the main effects, two-way or three-way interactions facial affect behavior and parasympathetic functioning
involving ADHD reached significance (all ts < 1.5, was diminished across both positive and negative induc-
ps > .10; see Table 2). tion conditions. However, given that RSA is believed to
EMOTION DYSREGULATION ACROSS EMOTION SYSTEMS IN ADHD 11

be a physiological index of emotion regulation abilities changes across childhood and into adolescence. Third, the
(Beauchaine, 2001; Beauchaine et al., 2007; Porges, stimuli used to elicit “negative” and “positive” emotions
2001, 2007), discordance between RSA and negative were somewhat generic. Although the majority of children
affective behavior suggests that physiological dysregula- rated the negative clip as eliciting sadness and the majority
tion may play a central role in the inappropriate negative of children rated the positive clip as eliciting happiness, there
affect displayed by some children with ADHD. That is, were some individual differences in these reports, though no
the diminished association between physiological emotion significant differences emerged according to group. Stimuli
response and negative affect behavior may help to explain designed to elicit more “pure” and specific emotions may
why some children with ADHD are prone to displays of yield stronger results (Levenson, 1992).
inappropriate negative affect and/or irritability. With In conclusion, our findings are in line with the primary
decoupled physiological and behavioral responses to assumption of the functionalist theory of emotion, which
affective challenges, children with ADHD may receive suggests that coherence across emotion systems enhances
conflicting information regarding their emotional experi- adaptiveness. Here, youth with ADHD displayed a more
ence, resulting in inappropriate displays of negative affect poorly coordinated emotion systems. These findings are
and reduced ability to respond appropriately to the emo- consistent with hypotheses that ADHD is a disorder that
tion (Fabes, Eisenberg, Karbon, Troyer, & Switzer, 1994). involves alterations of emotion reactivity and regulation in
When individual facial affect behaviors were examined, addition to difficulties in cognition and behavior.
reduced coherence between facial affect and parasympa- The findings are clinically relevant in that they demon-
thetic functioning among children with ADHD appeared to strate the importance of teaching children with ADHD
be specific to anger and anxiety. This is of interest, given skills in the areas of emotion in addition to behavioral
prior work demonstrating the important role that both anger/ and cognitive coping. Specifically, if these results are
frustration/irritability (Shaw, Stringaris, Nigg, & Leibenluft, replicated, it may be beneficial to work clinically with
2014; Sullivan et al., 2015) and anxiety (Krone & Newcorn, children with ADHD to develop the skills to better inter-
2015; Pliszka, 2000) play in ADHD. pret the variety of emotional signals they receive or to
In contrast to our hypotheses, neither facial affect beha- develop skills to better integrate responses across emo-
vior nor ADHD appeared to be significantly associated with tional systems.
the index of sympathetic functioning (i.e., PEP). However,
this may be in line with prior literature that has linked PEP
to beta-adrenal functioning and response to reward specifi- FUNDING
cally. Thus, it may be that the task conditions utilized here
were insufficient to engage these processes. This study was funded by the National Institute of Mental
These primary findings of reduced coherence between para- Health (R01 MH059105, R01 MH086654).
sympathetic functioning and facial affect cannot be attributed
to a lack of emotional responding among the children with
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