Journal of Clinical Child & Adolescent Psychology

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

Neural Processing of Threat Cues in Young

Children With Attention-Deficit/Hyperactivity
Symptoms

Chaia Flegenheimer, Claudia Lugo-Candelas, Elizabeth Harvey & Jennifer M.

McDermott

To cite this article: Chaia Flegenheimer, Claudia Lugo-Candelas, Elizabeth Harvey & Jennifer
M. McDermott (2017): Neural Processing of Threat Cues in Young Children With Attention-Deficit/
Hyperactivity Symptoms, Journal of Clinical Child & Adolescent Psychology

To link to this article: http://dx.doi.org/10.1080/15374416.2017.1286593

Published online: 03 Mar 2017.

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Download by: [University of Newcastle, Australia] Date: 24 March 2017, At: 06:44
Journal of Clinical Child & Adolescent Psychology, 0(0), 1–9, 2017
Copyright © 2017 Society of Clinical Child & Adolescent Psychology
ISSN: 1537-4416 print/1537-4424 online
DOI: 10.1080/15374416.2017.1286593

Neural Processing of Threat Cues in Young Children

With Attention-Deficit/Hyperactivity Symptoms
Chaia Flegenheimer
Department of Psychological and Brain Sciences, University of Massachusetts Amherst

Claudia Lugo-Candelas
Department of Psychological and Brain Sciences, University of Massachusetts Amherst and
Division of Child and Adolescent Psychiatry, Columbia University Medical Center/New York State
Psychiatric Institute

Elizabeth Harvey and Jennifer M. McDermott

Department of Psychological and Brain Sciences, University of Massachusetts Amherst

A growing literature indicates that attention deficit/hyperactivity disorder (ADHD)

involves difficulty processing threat-related emotion faces. This deficit is especially
important to understand in young children, as threat emotion processing is related to
the development of social skills and related behavioral regulation. Therefore, the current
study aimed to better understand the neural basis of this processing in young children
with ADHD symptoms. Forty-seven children between 4 and 7 years of age were included
in the analysis, 28 typical developing and 19 with clinically significant levels of ADHD
hyperactive/impulsive symptoms. Participants completed a passive affective face-viewing
task. Event-related potentials were assessed for each emotion, and parental report of child
behavior and emotion regulation abilities was assessed. Children with ADHD symptoms
showed altered N170 modulation in response to specific emotion faces, such that the
N170 was less negative in response to fearful compared to neutral faces, whereas
typically developing children showed the opposite pattern. Groups did not differ in
reactivity to anger or non-threat-related emotion faces. The N170 difference in fearful
compared to neutral faces correlated with reported behavior, such that less fear reactivity
predicted fewer prosocial behaviors. Abnormalities in the underlying neural systems for
fear processing in young children with ADHD symptoms may play an important role in
social and behavioral deficits within this population.

Growing evidence suggests that attention deficit/hyperac-
tivity disorder (ADHD) involves significant social cogni-
tion deficits, including compromised understanding of
facial expressions of emotion (Aspan et al., 2014;
Graziano & Garcia, 2016; Uekermann et al., 2010).
Efficient threat-related processing (i.e., fearful and
angry faces) relates to the development of prosocial
Correspondence should be addressed to Jennifer M. McDermott,
Department of Psychological and Brain Sciences, University of
Massachusetts, Amherst, Tobin 415/135 Hicks Way, Amherst, MA 01003.
E-mail: mcdermott@psych.umass.edu
behaviors (Marsh, Kozak, & Ambady, 2007), whereas
deficits may contribute to social difficulties often asso-
ciated with ADHD (Hoza, 2007; Wehmeier, Schacht, &
Barkley, 2010). Thus, understanding deficits in affective
face processing in ADHD may allow for a more nuanced
understanding of maladaptive social behaviors in this
population (Boo & Prins, 2007).
Emotion processing in general, and threat-related pro-
cessing specifically, has been widely studied in typically
developing children using a temporally sensitive measure
of neural activity called event-related potentials (ERPs).
An early ERP component of emotion processing is the
2 FLEGENHEIMER ET AL.
N170, a negative going deflection between 125 and
300 ms poststimulus presentation that is thought to be
face specific (Bentin, Allison, Puce, Perez, & McCarthy,
1996). Evident in early childhood through adulthood, the
N170 is an excellent measure of face processing across
development (Batty & Taylor, 2006). This component is
particularly sensitive to threat-related emotions, with
enhanced N170 reactivity to fearful (Blau, Maurer,
Tottenham, & McCandliss, 2007) and angry (Bediou,
Eimer, d’Amato, Hauk, & Calder, 2009) faces compared
to neutral faces. In addition, N170 reactivity is linked
with social behaviors in adults; larger N170s to emo-
tional faces are associated with higher empathy trait
scores (Choi et al., 2014). These patterns underscore
the connections between neural processing of emotion
faces and the development of prosocial skills.
To date, few studies have examined the N170 and
threat-related emotion processing among individuals
with ADHD, and results have been contradictory. Work
in adults with ADHD indicates less N170 modulation
between threat-related and non-threat-related emotional
faces compared to typically developing (TD) peers
(Ibáñez et al., 2011). Moreover, this deficit in N170
modulation correlates with deficits in theory of mind
and working memory. However, a recent study found
that the direction of the N170 modulation pattern to
threat versus nonthreat emotion faces differed such that
adults with ADHD displayed an enhanced N170 to
angry versus happy expressions, whereas TD adults
exhibited the opposite pattern of reactivity (Raz &
Dan, 2015). Similarly, adolescents with ADHD exhibit
an enhanced N170 to angry and fearful faces compared
to TD peers (Williams et al., 2008). In contrast, a study
of older children (8–13 years) found that those with
ADHD did not show differences in N170 modulation
to emotional faces (including fear, anger, disgust, joy,
and neutrality) compared to TD peers (Tye et al., 2014).
The differences in the tasks used—active labeling of
emotional faces versus passive viewing—could contri-
bute to the differing N170 results as emotion labeling
can increase N170 amplitudes (Herbert, Sfärlea, &
Blumenthal, 2013).
No studies to date have explored neural processing of
emotional faces in young children with ADHD symp-
toms. It is imperative to understand the effects of ADHD
symptomatology in young children because of the sig-
nificance of this developmental period for social and
emotional growth (Shonkoff & Phillips, 2000).
Previous research has shown that ADHD symptomatol-
ogy often begins during the preschool years (Applegate
et al. 1997) and remains stable over time (Riddle et al.,
2013). Moreover, the preschool years may be an impor-
tant period for the development of comorbid psycho-
pathology in children with ADHD (Harvey, Breaux, &
Lugo-Candelas, 2016). The present study focuses on 4-
to 7-year-old children, which corresponds with one of
the landmark longitudinal studies of ADHD symptoma-
tology in young children (Chronis et al., 2003).
In this study we (a) examine N170 amplitude to threat-
related faces in young children with and without ADHD
symptoms and (b) assess the relation between threat proces-
sing and social-emotional and behavioral functioning.
Understanding threat processing in young children with
ADHD symptoms may elucidate how social cognition def-
icits contribute to emotional competence difficulties in chil-
dren with ADHD symptoms. Moreover, identifying early
neural markers of social-emotional and behavioral difficul-
ties in children with ADHD may contribute to the develop-
ment of low-cost physiological measures that may have
utility in clinical child assessments (De Los Reyes &
Aldao, 2015).
Recognizing that ADHD is considered an extreme
end of a behavioral spectrum (Larsson, Anckarsater,
Rastam, Chang, & Lichtenstein, 2012), we recruited
children with and without elevated ADHD symptoms
using a clinical diagnostic interview. This approach
allowed for exploration of ADHD symptom-related dif-
ferences through both classical groupings (those with
ADHD symptoms vs. TD) and a dimensional view in
line with Research Domain Criteria principles, namely,
the overall number of hyperactive/impulsive symptoms
(Shaw et al., 2011). Children with ADHD symptoms
were hypothesized to exhibit attenuated processing of
threat-related faces compared to TD peers. It was also
postulated that ERP reactivity to emotional faces, parti-
cularly threat-related emotional faces, would correlate
with parental reports of children’s social-emotional
difficulties.
METHOD
Participants
Children between 4 and 7 years old (M = 77.83 months,
SD = 9.44) were recruited at the University of
Massachusetts Amherst via advertisements placed in pedia-
trician offices, community centers, and local preschools. Of
the 68 children initially recruited, nine were excluded due to
equipment failure, three did not follow instructions, six
showed excessive noise in their EEG data, and two were
at least 3 standard deviations away from the mean on key
variables. The final sample included 28 TD children (18
male) and 19 children with ADHD symptoms (14 male).
Excluded participants did not significantly differ from those
included on parental education (p = .29), parental age
(p = .42), gender distribution (p = .66), child age
(p = .29), hyperactive symptoms (p = .35), inattentive
symptoms (p = .27), or oppositional defiant disorder
(ODD) symptoms (p = .93).
 NEURAL PROCESSING OF THREAT CUES IN YOUNG CHILDREN
Children were included in the ADHD symptoms
group if they demonstrated six or more hyperactivity/
impulsivity symptoms on the Diagnostic Interview
Schedule for Children (Shaffer, Fisher, Lucas, Dulcan,
& Schwab-Stone, 2000), at least three of which occurred
at both home and at school/daycare. Participants with
three or fewer hyperactive/impulsive symptoms were
recruited for the TD group. This symptom cutoff is in
line with ADHD combined presentation and predomi-
nantly hyperactive/impulsive presentation.
Hyperactivity/impulsivity symptoms were chosen as
inclusion criteria because ADHD predominantly inatten-
tive presentation has a later average age of onset
(Applegate et al., 1997). Of the 19 children recruited
for the ADHD symptoms group, 13 showed symptoms
consistent with predominantly hyperactive/impulsive
presentation and six showed symptoms in line with
ADHD combined presentation. Thirteen children in the
ADHD symptoms group and five of the TD children
displayed four or more ODD symptoms. Children were
not eligible for this study if they had comorbidities that
would interfere with their ability to do the task (e.g.,
autism).
The ADHD symptoms and TD groups did not differ in
child age (p = .58), gender distribution (p = .50), parental
age (p = .07), or parental education level (p = .53). The
sample was 81% European American and 19% multiethnic.
One child was prescribed Guanfacine, and one was taking 5
HTP. These drugs have duration of actions shorter than
12 hr (Biederman, Lopez, Boellner, & Chandler, 2001;
Taylor & Russo, 2009), and parents reported that medication
regimens were discontinued at least 48 hr prior to
participation.
Passive Face-Viewing Task
Participants completed an implicit face-viewing task,
with a nonface object (fish) interspersed throughout the
task (Batty & Taylor, 2006). Participants were instructed
to watch the faces and press a button whenever they saw
the fish. If they correctly pressed the button, a yellow
star was displayed for 500 ms. This paradigm promoted
implicit face viewing while ensuring that children main-
tained attention to the screen. Images of emotional faces
were taken from the NimStim face stimulus set
(Tottenham et al., 2009) and included equal numbers of
open- and closed-mouth images for fearful, sad, angry,
neutral, and happy faces and open-mouth images for
surprised faces. Participants were shown 181 faces
(approximately 30 for each emotion; 1,000 ms each)
and 25 cartoon fish (1,250 ms each) in a pseudorandom
order, with the fish appearing every two to 12 trials. The
task lasted approximately 10 min, with a break halfway
through. Groups did not significantly differ in task
3
accuracy, indicating similar levels of skill and attention
to the game (p = .14).
Electroencephalogram (EEG)
EEG was recorded using Ag-AgCl electrodes in a 64-chan-
nel Lycra Electro-Cap setup in accordance with the
International 10–20 System. Eye movements were regressed
from the data. Mastoid electrodes served as reference and
impedances were kept less than 50kΩ. Data were filtered
(0.01–100 Hz), amplified and digitized (1000 Hz), and then
filtered again during processing with a 30 Hz low-pass filter.
EEG was baseline corrected, and trials containing artifacts
(epochs exceeding an EEG voltage threshold of ±150μV)
were removed and excluded from analysis.
ERPs were constructed separately for each emotion.
Participants were excluded if they had fewer than 12 clean
epochs for each emotion. Peak amplitude was scored for the
P1 (the ERP component immediately prior to the N170)
between 0 and 200 ms after stimulus onset. The peak
amplitude for the N170 was scored between 125 and
300 ms after stimulus onset. A baseline of 200 ms before
stimulus onset was used for both measures. A peak-to-peak
measure of the N170, calculated as the difference between
the N170 and the P1, was used to account for any potential
differences driven by the preceding component. Consistent
with previous research (Tye et al., 2014; Williams et al.,
2008), the N170 was analyzed at temporal (TP8 and TP7)
and occipital (O2 and O1) sites.
Parent Measures
Behavior Assessment System for Children, Second
Edition
Parents completed the Behavior Assessment System for
Children, Second Edition, rating scale of child psycho-
pathology, which has demonstrated validity as a measure
of children’s behavior. The preschool version was used for
4- and 5-year-olds (Cronbach’s αs = .80–.85) and the child
version was used for 6- and 7-year-olds anxiety (Cronbach’s
αs = .82–.87; Reynolds & Kamphaus, 2010). Analyses used
T scores from the following subscales: Anxiety, Depression,
Adaptability, and Social Skills.
Emotion Regulation Checklist
The Emotion Regulation Checklist (ERC) is a parental
report measure of child emotion regulation skills comprising
24 items that are each assessed on a 4-point Likert scale and
yields two subscales: Lability (15 items; α = .900) and
Emotion Regulation (eight items; α = .626). The ERC has
demonstrated validity for both preschool-age (Shields et al.,
2001) and older (6–12 years; Shields & Cicchetti, 1997)
children.
4 FLEGENHEIMER ET AL.

Data Analysis Dan (2015), difference scores were created for each indivi-
dual emotion (fear, angry, sad, surprise, happy) compared to
Repeated measures analyses of covariance (ANCOVAs)
neutral. Follow-up analyses showed that the Group ×
were run to determine whether children with and without
Emotion interaction in the right hemisphere was driven by
ADHD symptoms differed in neural reactivity to emotional
the fear-neutral difference score, t(45) = –2.82, p = .007,
faces, controlling for ODD status (1 = four or more ODD
d = 0.86. Exploratory analysis revealed that this fear-neutral
symptoms; 0 = three or fewer ODD symptoms) and for the
group difference was larger at site TP8, t(45) = –2.70,
number of epochs accumulated for each emotion. Type of
p = .010, d = 0.76, than at site O2, t(45) = –1.63,
emotional face (happy, surprise, sad, fear, angry, and neu-
p = .110, d = 0.49. In children with ADHD symptoms,
tral) was the within-subjects factor, group (ADHD symp-
the N170 was attenuated to fear compared to neutral faces
toms vs. TD) served as the between-subjects factor, and
at site TP8, whereas TD children showed the opposite
N170 (P1 to N170 peak-to-peak amplitude) served as the
pattern (see Figure 1). No other difference scores were
dependent variable. Greenhouse-Geisser correction was
significant (see Table 2).
applied where appropriate. Follow-up paired-samples t
Next, multiple regressions were performed to determine
tests and independent samples t tests were used to interpret
if ODD symptoms uniquely predicted N170 changes at sites
interaction effects, with an alpha of .01 to limit Type 1 error.
TP8 and O2 (Table 3). The models were trimmed by remov-
Multiple regressions with hyperactivity, inattention, and
ing the predictor variables with higher p values, which
ODD symptoms were run to determine whether symptomol-
included both inattentive symptoms and ODD symptoms.
ogy uniquely predicted N170 differences. Due to multicol-
Hyperactive symptoms positively predicted changes in
linearity among the hyperactivity, inattention, and ODD
N170 fear-neutral scores at site TP8. No interactions
symptoms (see correlations in Table 1), model trimming
emerged between hyperactivity, inattention, and ODD
was used to find the symptom type that best predicted
symptoms.
changes in N170 amplitude. Hierarchical regressions were
then run to explore whether N170 differences predicted
social and emotional problems, controlling for ADHD and Relations Between ERP Measures and Social-
ODD symptoms. Hyperactivity, inattention, and ODD Emotional/Behavioral Functioning
symptoms were entered in Step 1, with N170 differences
Hierarchical regressions were conducted to determine
entered in Step 2; emotion regulation, lability, depression,
whether the N170 fear difference score predicted children’s
anxiety, adaptability, and social skills each served as out-
social-emotional and behavioral functioning beyond ADHD
come variables.
and ODD symptomatology (see Table 4). When ADHD
For the ANCOVA and follow-up t tests, the sample was
symptoms and ODD status were accounted for, the N170
sufficient to detect large-sized effects (f = 0.26 for the
difference score for fear at site TP8 was inversely related to
ANCOVA and d = 1.05 for t tests) with .80 power. The
both social skills and emotion regulation.
sample was sufficient to detect medium-large sized effects
(r = .39) with .80 power for correlations.
DISCUSSION
RESULTS
This study uniquely shows neural deficits in reactivity to
fearful faces in young children with ADHD symptoms.
Descriptive Statistics
Moreover, it reveals a direct link between altered fear pro-
Correlations were calculated between the symptom types cessing and social-emotional/behavioral difficulties in
(hyperactive, inattentive, and ODD), N170 emotion-neutral young children. Combined, these findings are critical for
difference scores at site TP8 and O2 (described next), and informing the development of early interventions that can
the scores from the ERC and Behavior Assessment System be applied before complicating factors (i.e., accumulating
for Children, Second Edition social problems and the development of comorbid psychia-
(Table 1). High correlations were found between hyper- tric disorders) interfere (Halperin, Bedard, & Curchack-
active, inattentive, and ODD symptoms. Lichtin, 2012).
In line with previous studies of older children and adoles-
cents with ADHD (Tye et al., 2014; Williams et al., 2008),
N170: Reactivity to Emotional Faces in Children With
young children with ADHD symptoms demonstrated an atte-
and Without ADHD Symptoms
nuated N170 to fearful compared to neutral faces, whereas
A significant Group × Emotion interaction emerged for right TD peers showed the opposite pattern of reactivity. Given
hemisphere sites TP8 and O2, F(5, 185) = 2.66, p = .02, that fear processing is important for socially driven beha-
η2p = .067. No effects were found for left hemisphere sites vioral regulation skills (e.g., social referencing; Camras &
TP7 and O1. Based on methods used previously by Raz and Sachs, 1991) and is correlated with the development of
 TABLE 1
Means, Standard Deviations, and Intercorrelations of Symptom Counts, N170 Difference Scores, and Emotion Regulation Checklist and Behavior Assessment System for Children, Second
Edition, Scores

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

1. Hyp Symptoms
2. Inatten Symptoms .80**
3. ODD Symptoms .66** .58**
4. TP8 Fear Difference .36* .27† .27†
5. O2 Fear Difference .29* .17 .08 .25†
6. TP8 Angry Difference .19 .15 .05 .78** −.01
7. O2 Angry Difference .26† .11 −.12 −.01 .59** .07
8. TP8 Sad Difference .08 −.02 .07 .74** −.06 .77** −.14
9. O2 Sad Difference .19 .09 .05 .31* .61** .21 .45** .36*
10. TP8 Surprise .24 .09 .23 .73** .09 .61** −.15 .71** .12
Difference
11. O2 Surprise .32* .19 .17 .14 .48** −.04 .35* −.07 .26† .31*
Difference
12. TP8 Happy Difference .25† .13 .31* .58** .06 .54** −.18 .59** .22 .72** .17
13. O2 Happy Difference .23 −.03 .13 .29† .26† .25† .31* .19 .31* .34* .56** .37*
14. Lability .77** .66** .69** .36* .01 .19 −.03 .18 .06 .20 .06 .24 .02
15. Emot. Regulation −.34* −.26† −.24 −.44** −.03 −.24 −.02 −.35* −.25† −.29† −.07 −.31* −.09 −.58**
16. Anxiety −.06 −.07 .04 −.00 −.28† −.05 −.24 −.11 −.42** .08 −.11 −.01 −.16 .14 .01
17. Dep. .19 .22 .25 .07 −.09 .19 .06 .12 −.03 .14 .08 −.04 −.02 .43** −.15 .45**
18. Adapt. −.51** −.52** −.44** −.39* .01 −.25 −.02 −.21 −.10 −.16 .08 −.12 .14 −.75** .60** −.26 −.26†
19. Social Skills −.33* −.41** −.21 −.42** −.01 −.30† −.12 −.33* −.22 −.14 .06 −.15 .10 −.54** .75** .23 .01 .66**
M 3.36 2.70 2.89 .30 .12 .83 .30 −.11 .17 .89 .72 .80 .61 1.87 3.44 47.00 48.76 47.19 48.55
SD 3.50 2.95 2.22 5.20 5.05 4.65 4.17 5.40 4.12 5.37 4.54 5.43 3.66 .52 .35 7.15 6.62 10.24 9.07

Note: Hyp = Hyperactive; Inatten = Inattentive; ODD = oppositional defiant disorder; TP = temporal; O = occipital; Emot = Emotion; Dep = Depression; Adapt = Adaptability.
†
p < .10. *p < .05. **p < .01.
NEURAL PROCESSING OF THREAT CUES IN YOUNG CHILDREN
5
6 FLEGENHEIMER ET AL.

FIGURE 1 N170 event-related potentials (ERPs) for typically developing children (A; left) and children with ADHD symptoms (B; right) at site TP8. N170
ERPs are in response to faces with the following emotions: fear (dashed), angry (dotted), and neutral (solid).

TABLE 2
Average N170 Peak-to-Peak Scores in Response to Emotional Compared to Neutral Faces

ADHD Symptoms Typically Developing Differences

Site Difference Score M (μV) SD M (μV) SD t p d

TP8 Fear 2.63 6.11 −1.28 3.84 −2.70 .01* .77

Anger 2.04 6.43 0.02 2.74 −1.29 .21 .41
Sad 0.90 7.29 −0.80 3.61 −1.06 .29 .30
Happy 2.67 6.95 −0.46 3.74 −1.80 .08† .56
Surprise 2.46 6.41 −0.18 4.35 −1.68 .10† .48
O2 Fear 1.55 4.57 −0.85 5.20 −1.63 .11 .49
Anger 1.14 4.37 −0.26 4.00 −1.13 .26 .33
Sad 1.35 4.20 −0.63 3.94 −1.65 .11 .49
Happy 1.00 4.29 0.34 3.23 −0.60 .55 .17
Surprise 2.05 3.99 −0.17 4.74 −1.68 .10† .51

Note: ADHD = attention deficit/hyperactivity disorder; TP = temporal; O = occipital.

†
p < .10. *p ≤ .01.

TABLE 3
Linear Regression Models of Attention Deficit/Hyperactivity Disorder and ODD Symptomology Predicting N170 Fear Difference Scores

Full Model Trimmed Model

Site Predictor Variables B (SE) β p R 2

B (SE) β p R2

TP8 .131 .128*

Hyperactive symptoms .526 (.386) .354 .180 .531 (.206) .358 .014
Inattentive symptoms −.086 (.424) −.049 .840 — — —
ODD symptoms .151 (.448) .064 .738 — — —
O2 .115 .085*
Hyperactive symptoms .771 (.378) .535 .048* .419 (.205) .291 .047
Inattentive symptoms −.264 (.416) −.154 .530 — — —
ODD symptoms −.415 (.439) −.182 .350 — — —

Note: ODD = oppositional defiant disorder; TP = temporal; O = occipital.

*p < .05.

prosocial behaviors (Marsh et al., 2007), altered affective face The N170 is postulated to originate, at least in part, from
processing in children with ADHD symptoms may be tied to the fusiform gyrus, an area of the brain that specializes in
heightened social and emotional difficulties (Graziano & facial recognition (Deffke et al., 2007). In turn, the fusiform
Garcia, 2016). gyrus is thought to connect to the amygdala, a key neural
 NEURAL PROCESSING OF THREAT CUES IN YOUNG CHILDREN 7

TABLE 4
Hierarchical Linear Regression Models of N170 Fear Difference Scores Predicting Parent Rating Scales (Emotion Regulation Checklist and
Behavior Assessment System for Children, Second Edition) Accounting for Attention Deficit/Hyperactivity Disorder Hyperactive and Inattentive
Symptoms and ODD Symptoms

Model 1 Model 2

Parent Rating Scale Predictor Variables B (SE) β p B (SE) β p

Lability
Hyperactive symptoms .077 (.025) .521 .003** .088 (.025) −.593 .001**
Inattentive symptoms .010 (.027) .054 .726 .005 (.026) −.027 .856
ODD symptoms .073 (.028) .311 .014** .062 (.028) −.264 .030*
Fear difference score:
Site O2 −.022 (.010) −.214 .026*
Site TP8 .012 (.009) −.121 .206
R2 –.650** –.696**
ΔR2 –.046†
Emotion Regulation
Hyperactive symptoms −.035 (.026) −.354 .185 −.029 (.026) −1.102 .277
Inattentive symptoms .005 (.029) −.044 .856 .006 (.027) –.201 .842
ODD symptoms −.005 (.030) −.030 .878 .003 (.029) –.110 .913
Fear difference score:
Site O2 .010 (.010) –.939 .353
Site TP8 −.026 (.010) −2.644 .012*
R2 −.115 –.248*
ΔR2 –.133*
Anxiety
Hyperactive symptoms −.201 (.627) −.321 .750 .016 (.653) –.008 .981
Inattentive symptoms −.173 (.688) −.251 .803 −.207 (.684) –.087 .764
ODD symptoms .473 (.716) −.661 .512 .269 (.718) –.081 .710
Fear difference score:
Site O2 −.396 (.233) –.287 .098
Site TP8 .085 (.236) –.062 .721
R2 .016 .089
ΔR2 .073
Depression
Hyperactive symptoms −.139 (.563) .563 .806 −.058 (.606) −.030 .924
Inattentive symptoms .325 (.619) .619 .603 .313 (.635) .142 .625
ODD symptoms .640 (.643) .643 .326 .562 (.666) .184 .405
Fear difference score:
Site O2 −.150 (.216) −.118 .492
Site TP8 .035 (.219) −.027 .875
R2 −.072 −.084
ΔR2 −.012
Adaptability
Hyperactive symptoms −.605 (.755) −.203 .428 −.456 (.767) −.153 .556
Inattentive symptoms −.857 (.830) −.252 .308 −.970 (.803) −.285 .235
ODD symptoms −.731 (.863) −.154 .402 −.504 (.843) −.107 .553
Fear difference score:
Site O2 .334 (.274) −.169 .231
Site TP8 −.567 (.277) −.289 .048*
R2 –.303* —.388*
ΔR2 –.085+
Social Skills
Hyperactive symptoms −.027 (.728) −.010 .971 .276 (.719) −.105 .703
Inattentive symptoms −1.375 (.799) −.456 .094 −1.538 (.753) −.511 .049*
ODD symptoms .350 (.831) −.083 .676 .538 (.790) −.128 .501
Fear difference score:
Site O2 .229 (.257) −.131 .378
Site TP8 −.688 (.260) −.396 .012*
R2 –.175† —.313*
ΔR2 —.138*

Note: ODD = oppositional defiant disorder; O = occipital; TP = temporal.

†
p < .10. *p ≤ .05. **p ≤ .01.
8 FLEGENHEIMER ET AL.
structure in both fear processing and social cognition, and
together they serve as part of an emotion-processing net-
work (Leppanen & Nelson, 2009). Indeed, Vuilleumier and
colleagues (2004) found that patients with amygdala lesions
demonstrated less neural activity in their fusiform cortex
when presented with fearful faces compared to other lesion
patients and healthy peers. Previous studies have also shown
abnormalities within the amygdalae of ADHD patients
(Frodl et al., 2010; Posner et al., 2011). Although the
N170 does not directly assess amygdala activity, attenuated
processing of fearful faces in young children with ADHD
symptoms may relate to deficits in the amygdala–fusiform
connection, which may contribute to the social and beha-
vioral difficulties reported.
Overall, these findings indicate that altered processing
of facial emotions is a key element in the social develop-
ment of young children with ADHD symptoms and high-
light the importance this area of focus for future studies
exploring both ADHD assessment and interventions (De
Los Reyes & Aldao, 2015). Although interventions are
being developed to help with emotion face-processing
deficits in young children with autism (Golan et al.,
2010), this approach has yet to be applied to children
with ADHD symptoms. Given growing evidence of a
fear-processing deficit in ADHD symptomatology, similar
emotion-processing interventions focusing on effective
social behavior and emotion regulation may be advanta-
geous for this population and may lower risk of comorbid
social anxiety and depression (Wehmeier et al., 2010).
In contrast to findings in adults with ADHD, no group
differences emerged for the processing of angry faces in our
sample (Raz & Dan, 2015). One possible explanation for
this discrepancy is that the N170 has been shown to demon-
strate greater modulation to emotion faces at later stages of
development (Batty & Taylor, 2006); thus, differences in
reactivity to angry faces may be subtler in the current
study’s age range. It is also possible that ADHD-related
differences in processing angry faces may not appear until
later in development. Further research is needed to deter-
mine which of these factors contribute to the age-related
differences found in anger processing among individuals
with ADHD symptoms.
Although the current study focused on young children
who met ADHD hyperactive/impulsive symptom criteria, it
is unclear whether participants met full diagnostic criteria
for ADHD. Furthermore, it is unclear whether these results
may differ between ADHD hyperactive/impulsive and
ADHD combined presentations, as there was not enough
power to examine these subgroups separately. Future work
should incorporate a multi-informant assessment of ADHD
symptomatology to better determine ADHD diagnosis, and
longitudinal research is needed to follow progression of
ADHD symptoms, face processing, and social functioning
over development. In addition, this study was cross-sec-
tional, so mediation models could not be explored as
temporal precedence could not be established (Maxwell &
Cole, 2007); future longitudinal studies should explore the
possibility of fear processing mediating the relation between
ADHD symptoms and social and emotional difficulties.
Finally, the sample was relatively homogenous in race and
socioeconomic status due to the demographics of the popu-
lation in which the study took place.
Overall, the findings support the growing notion that
ADHD involves distinct deficits in processing certain
types of threat-related emotional faces. Specifically, fear-
processing deficits emerged as a possible element in the
development of social difficulties among individuals with
ADHD symptoms. Future interventions focusing on fear-
processing abilities in children with ADHD symptoms may
help to enhance prosocial behaviors in this population and
reduce the risk for related comorbidities, including anxiety
and depression.
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