Examining the impact of prenatal maternal internalizing symptoms and socioeconomic status on children’s frontal alpha asymmetry and psychopathology

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EXAMINING THE IMPACT OF PRENATAL MATERNAL INTERNALIZING SYMPTOMS
AND SOCIOECONOMIC STATUS ON CHILDREN’S FRONTAL ALPHA ASYMMETRY
AND PSYCHOPATHOLOGY

by

Alexis Marie Hernandez

A Thesis Presented to the
FACULTY OF THE USC DANA AND DAVID DORNSIFE
COLLEGE OF LETTERS, ARTS AND SCIENCES
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
MASTER OF ARTS
(PSYCHOLOGY)

May 2023

Copyright 2023 Alexis Marie Hernandez

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TABLE OF CONTENTS
List of Tables ................................................................................................................................ iii
Abstract ......................................................................................................................................... iv
Chapter 1: Introduction ................................................................................................................... 1
1.1 Maternal Psychopathology and Child Internalizing and Externalizing
Problems ....................................................................................................................... 2
1.2 The Relation Between Frontal Alpha Asymmetry and Internalizing and
Externalizing Problems ................................................................................................. 2
1.3 Maternal Characteristics and Frontal Alpha Asymmetry ............................................. 4
1.4 The Present Study ......................................................................................................... 5

Chapter 2: Methods ......................................................................................................................... 8
2.1 Participants .................................................................................................................... 8
2.2 Procedure ...................................................................................................................... 9
2.3 EEG Data Acquisition................................................................................................... 9
2.4 EEG Preprocessing ....................................................................................................... 9
2.5 Measures ..................................................................................................................... 11
2.5.1 Maternal Depression and Anxiety Symptoms ............................................. 11
2.5.2 Maternal Socioeconomic Status ................................................................... 12
2.5.3 Frontal Alpha Asymmetry ........................................................................... 12
2.5.4 Child Internalizing and Externalizing Symptoms ........................................ 12
2.6 Data Analysis Plan ...................................................................................................... 13

Chapter 3: Results ......................................................................................................................... 15
3.1 Preliminary Analyses .................................................................................................. 15
3.2 Main Analyses ............................................................................................................ 17
3.3 Exploratory Analyses .................................................................................................. 20

Chapter 4: Discussion ................................................................................................................... 21
4.1 Maternal Characteristics ............................................................................................. 21
4.2 Frontal Alpha Asymmetry .......................................................................................... 22
4.3 Study Limitations, Implications, and Conclusions ..................................................... 24

References ..................................................................................................................................... 27

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LIST OF TABLES

Table 1. Descriptive Statistics for Children’s Sex and Race. Descriptive Statistics
for Mothers’ Race, Education, Health Insurance, and Marital Status .......................................... 16

Table 2. Mother and Child Descriptive Statistics of Variables of Interest;
Mother and Child Within and Between Correlations ................................................................... 17

Table 3. Mother Internalizing Symptoms at the Prenatal Period Predicting
Children’s frontal alpha asymmetry and Internalizing/Externalizing
Problems at 5, 7, 9, and 11 Years of Age (n = 415)...................................................................... 19

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Abstract
Prenatal maternal internalizing psychopathology (depression and anxiety) and
socioeconomic status (SES) have been independently associated with higher risk for
internalizing and externalizing problems in children. However, the mechanisms behind these
associations are not well understood. Numerous studies have linked greater right frontal alpha
asymmetry to psychopathology, especially internalizing problems. Even so, findings have been
mixed. Several studies have also linked maternal internalizing psychopathology to children’s
frontal alpha asymmetry. Additionally, emerging studies have linked SES in relation to
children’s frontal alpha asymmetry. Yet, only a few studies have examined these associations
within a longitudinal design, and most have used relatively small samples. The current
preregistered study utilizes data from a large study of young children (N=415; Meanage=7.27;
Rangeage=5-11 years) to examine the association between prenatal maternal internalizing
symptoms, children’s frontal alpha asymmetry, and behavior problems in a large sample of
children. Prenatal maternal internalizing symptoms did not predict children's frontal alpha
asymmetry and there was no association between frontal alpha asymmetry and behavior
problems. However, mothers’ internalizing symptoms during pregnancy predicted children’s
internalizing and externalizing outcomes. Non-preregistered analyses showed that lower prenatal
maternal SES predicted greater right frontal alpha asymmetry and increased externalizing and
internalizing problems. Results of this large, longitudinal study suggest that children’s alpha
asymmetry is not related to children’s internalizing or externalizing problems or predicted by
maternal internalizing symptoms in a community sample. Future research should examine the
impact of early SES on children’s frontal alpha asymmetry in high-risk samples.

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Chapter 1: Introduction
Internalizing and externalizing problems impact the child’s social, emotional, and cognitive
development, including difficulties in school, increased risk for physical health problems,
substance misuse, higher risk-taking behaviors, and suicide (Coleman et al., 2007; Jesulola et al.,
2015). One main influence on children’s negative internalizing and externalizing problems are
maternal characteristics during children’s early development such as maternal internalizing
psychopathology and socioeconomic status (SES; Bradley & Carwyn, 2002; Monk et al., 2019).
Prenatal maternal internalizing psychopathology, like depression and anxiety, have been found to
be associated with higher risk for internalizing and externalizing problems in children (Goodman
et al., 2011; Monk et al., 2019). In addition, studies have examined early SES in relation to
socioemotional problems in childhood (Bradely & Carwyn, 2002). Given these findings, it is
important to understand the mechanism behind the relationship between prenatal maternal
internalizing psychopathology symptoms, SES, and psychopathology risk in children. One
possible neurobiological mechanism that may act as a mediator in this relation is frontal alpha
asymmetry, which has been associated with psychopathology in children and adults (Allen &
Reznik, 2015; Thibodeau et al., 2006). Maternal characteristics like psychopathology and SES
may also play a role in the development of frontal alpha asymmetry; however, this research has
been mostly limited to concurrent relations and relatively small samples (e.g., Gatzke-Kopp et
al., 2014; Lopez-Duran et al., 2012; Mulligan et al., 2022; Peltola et al., 2014). Thus, the current
study aimed to address these gaps in the literature by examining the association between early
maternal internalizing symptoms, SES, children’s frontal alpha asymmetry, and internalizing and
externalizing outcomes in a large sample of children.

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1.1 Maternal Psychopathology and Child Internalizing and Externalizing Problems
Mothers with elevated psychopathology symptoms have been shown to increase the risk
for internalizing and externalizing problems in children. For example, Dawson et al. (2003)
found that preschool children who had mothers with a history of depression had higher levels of
internalizing and externalizing problems compared to children of mothers without a history of
depression. In addition, in a review study, Monk et al. (2019) noted that children of mothers who
had higher anxiety during the prenatal stage had an increased risk for psychopathology such as
anxiety, depression, and hyperactivity. Research has examined numerous factors that may
account for the relationship between maternal psychopathology and children’s internalizing and
externalizing problems (Alink et al. 2009; Frigoletto et al., 2022). In general, research finds that
maternal psychopathology may disrupt typical mother-child interactions, the prenatal
environment, as well as increased genetic predisposition to internalizing psychopathology
(Goodman & Gotlib, 1999). One possible mechanism is that maternal psychopathology impacts
children’s approach and withdrawal tendencies (Peltola et al., 2014l; Thibodeau et al., 2006).
Moreover, these tendencies are theorized to be evident in children’s frontal brain activation.
1. 2 The Relation Between Frontal Alpha Asymmetry and Internalizing and Externalizing
Problems
Research examining approach and withdrawal motivation have linked these tendencies to
one’s own processing of affective emotions and behaviors (Davidson, 1999; Davidson & Fox,
1982; Peltola et al., 2014). More specifically, approach motivation is linked to the processing of
positive stimuli and anger whereas withdrawal motivation is linked to the processing of negative
internalizing affective emotions and behaviors (Davidson, 1999; Peltola et al., 2014). Studies
have examined the processing of affective emotions and behaviors, that is dependent upon

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approach and withdrawal motivation, using behavioral observations and self-repots in relation to
children’s internalizing and externalizing problems (e.g., Alink et al., 2009). Specifically,
approach motivation has been linked to externalizing problems whereas withdrawal motivation
has been linked to internalizing problems (Peltola et al., 2014). Even so, behavioral observations
and self-reports may not fully capture the underlying mechanisms related to these tendencies.
Thus, to thoroughly examine the underlying mechanisms of approach and withdrawal motivation
for children’s internalizing and externalizing problems, examining a neurobiological indicator
may help provide unique insight on these tendencies. One neurobiological risk factor, frontal
alpha asymmetry, may act as possible components that further link differing systems that are
dependent upon the characteristics that make-up children’s negative emotions and behaviors
(Coan & Allen, 2004).
Frontal alpha asymmetry is defined as differences of cortical activation in one
hemisphere in relation to the other (Davidson & Fox, 1982). Right frontal alpha asymmetry or
reduced frontal alpha asymmetry is linked to stimuli processing withdrawal motivation and the
processing of negative affect, whereas greater frontal alpha asymmetry or left frontal is linked to
approach motivation and the processing of positive affect (Davidson & Fox, 1982; Peltola et al.,
2014). Numerous studies have examined frontal alpha asymmetry in relation to psychopathology
risk. Greater right frontal alpha asymmetry has been linked to higher internalizing problems such
as depression risk, whereas greater left frontal alpha asymmetry has been inconsistently linked to
externalizing problems in children (Allen & Reznik, 2015; Thibodeau et al., 2006). However, a
meta-analysis that examined the relation between children’s frontal alpha asymmetry and
children’s negative outcomes found insignificant effect sizes for overall internalizing (d = .19)
and externalizing (d = .04) disorders (Peltola et al., 2014). It is important to note that most of the

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studies included in the meta-analysis used relatively small samples (M= 64.55; range: 24-135
children). Thus, more research with large samples is needed to better understand the relation
between frontal alpha asymmetry and internalizing and externalizing disorders in children.
1.3 Maternal Characteristics and Frontal Alpha Asymmetry
Studies have examined maternal characteristics (e.g., psychopathology, SES) as
predictors for children’s frontal alpha asymmetry. Numerous studies have found longitudinal
associations between early maternal psychopathology and children’s frontal alpha asymmetry
(e.g., Forbes et al., 2008; Lopez-Duran et al., 2012; Peltola et al., 2014). Goldstein et al. (2016)
found that children of mothers with depression showed greater right frontal alpha asymmetry
from three to six years of age, compared to children of mothers without depression. Additionally,
studies have also examined prenatal maternal psychopathology symptoms in relation to infant’s
frontal alpha asymmetry (Field et al., 2004; Field & Diego, 2009). A study by Field et al. (2004)
examining prenatal maternal psychopathology symptoms (e.g., depression, anxiety) and infants’
frontal alpha asymmetry found that infants of mothers with higher depressive or anxiety
symptoms during pregnancy showed right frontal alpha asymmetry. Furthermore, a recent study
by Hill et al. (2020) examined the intergenerational transmission of frontal alpha asymmetry
among mother-infant dyads and found moderate correlations between mothers’ and infants’
frontal alpha asymmetry, indicating narrow-sense heritability. This study also found that infants
of mothers with current depressive symptoms showed greater right frontal alpha asymmetry (Hill
et al., 2020). However, studies have not consistently found this association (e.g., Bruder et al.,
2005; Forbes et al., 2006). A study by Bruder et al. (2005) examined parent’s lifetime history of
depression as a predictor for frontal alpha asymmetry in their offspring (i.e., children and adults;
age range: 8-47 years) and found no differences between offspring of one or two parents with a

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history of depression and offspring of parents without a history of depression. Even so, most
studies examining this relation have been done only in small samples. In addition, early SES may
play a role for differences in frontal alpha asymmetry; although, only a few studies have
examined this relation (Gatzke-Kopp et al., 2014; Mulligan et al., 2022). A study by Gatzke-
Kopp et al. (2014) found that increased right frontal alpha asymmetry was associated with
increased internalizing symptoms in kindergarten aged children from a low SES background.
Though, to our knowledge, no study to date has examined early SES as a predictor for later
frontal alpha asymmetry in children. Therefore, research is still needed to examine if maternal
internalizing psychopathology symptoms and SES are longitudinally associated with children’s
frontal alpha asymmetry, especially in a large sample.
1.4 The Present Study
The current study aimed to examine if the longitudinal relations between prenatal
maternal characteristics including internalizing symptoms (e.g., depression, anxiety) and SES
and children’s internalizing and externalizing problems were mediated by children’s frontal
alpha asymmetry. Because internalizing and externalizing problems tend to be correlated
between individuals (Morales et al., 2020), we decided to examine relations to both internalizing
and externalizing problems even if externalizing problems have been inconsistently linked to left
frontal alpha asymmetry (Peltola et al., 2014). This hypothesis allowed us to test the specificity
of the relations with internalizing and externalizing problems. Specifically, we proposed the
following three hypotheses:
1. The first hypothesis predicted that higher prenatal maternal internalizing symptoms and
low SES would be associated with right frontal alpha asymmetry in children. In addition,
higher early maternal internalizing symptoms and low SES would be associated with

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higher internalizing and externalizing problems in children. This hypothesis is in line
with previous research finding associations between maternal internalizing
psychopathology, SES, and children’s internalizing and externalizing problems (Dawson
et al., 2003; Monk et al., 2019).
2. The second hypothesis predicted that right frontal alpha asymmetry in children would be
associated with higher internalizing problems. In addition, we did not expect a significant
association between right frontal alpha asymmetry and externalizing problems. Previous
research has found a relationship between right frontal alpha asymmetry and internalizing
problems (Allen & Reznik, 2015). Research examining the relationship between right
frontal alpha asymmetry and externalizing problems have not found a link between these
variables (Thibodeau et al., 2006). This finding suggests that the mechanisms of right
frontal alpha asymmetry are more linked to withdrawal and internalizing processes rather
than externalizing processes (Davidson & Fox, 1982).
3. The third hypothesis predicted that higher early maternal internalizing symptoms and low
SES would be associated with right alpha asymmetry which will be concurrently
associated with higher internalizing problems, supporting a significant mediation. We did
not expect to observe a significant mediation predicting child externalizing problems
given that the relation between alpha asymmetry and externalizing has not been
consistently found (Ashman et al., 2008; Feng et al., 2012; Peltola et al., 2014).
Therefore, we hypothesized a mediation between these variables for child internalizing
problems, while accounting for externalizing problems.
To note, we preregistered our analytic plan and hypothesized that early maternal
internalizing symptoms will predict children’s frontal alpha asymmetry as well as internalizing

7
and externalizing problems (https://osf.io/v2n6a). In addition, our analytic plan included
examining SES as a covariate. Given the significant findings of SES, we chose to examine SES
more carefully as another predictor of children's brain activity and behavioral outcomes. The
inclusion of SES in the hypotheses stated above was not preregistered.

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Chapter 2: Methods
2.1 Participants
The sample from the current study (N= 415; Mage= 7.27; SDage= 1.99; 221 girls) came
from a larger, pre-existing study from the National Institutes of Health’s Environmental
influences on Child Health Outcomes (ECHO) project examining environmental influences on
children’s health outcomes (Blaisdell et al., 2021; Gillman & Blaisdell, 2018). EEG data was
collected from two data sites in South Dakota, USA. Additional and detailed information from
the pre-existing study has been previously published (Dukes et al., 2014). From the larger, pre-
existing study, children participated in an EEG assessment at 5-, 7-, 9-, 11-years of age.
The sample of the study was predominantly White (79.76%), followed by American
Indian (12.77%), and other (7.47%). Children’s age distribution ranged from the following: 5-
year-old participants (N=126), 7-year-old participants (N=164), 9-year-old participants (N=69),
and 11-year-old participants (N=56). Monthly income reported were the following: 2.26% of
families earned less than $500; 6.13% earned between $501 to $1,000; 17.10% earned between
$1,001 to $2,000; 20.65% earned between $2,001 to $3,000; 18.71% earned between $3,001 to
$4,000; 16.13% earned between $4,001 to $5,000 and 19.03% earned above $5,000. Mothers’
education levels varied, but the majority completed college (1.27% reported some or completed
primary school, 12.34% reported some or completed high school, 27.85% reported some college,
40.19% completed college, and 18.35% reported post graduate school). In addition, 66.88% of
mothers reported having commercial health insurance (33.12% reported public assistance).
Lastly, maternal age highly varied (Mage=28.4, SDage=4.7, age range= 16-43 years).

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2.2 Procedure
Prior to collecting data, informed consent and informed assent was obtained through the
primary caregiver and child. Mothers filled out questionnaires pertaining to internalizing
symptoms as well as demographic information during pregnancy. During the first EEG
laboratory visit at either 5, 7, 9, or 11 years of age, mothers filled out questions assessing their
children’s behavioral problems. During the lab visit, children sat about 70 cm in front of a
computer screen while wearing an EEG net and completed a 3-minute baseline recording as part
of the EEG task altering between eyes open (EO) and eyes closed (EC), alternating every 30
seconds. Instructions for the task were presented in E-Prime 2.0.10 (Psychology Software Tools,
Pittsburgh, PA). Upon completion of the laboratory visit, the families received compensation and
children were given a small gift (e.g., toy). The larger, pre-existing study has been approved by
Avera’s Institutional Review.
2.3 EEG Data Acquisition
EEG data was collected using a 64-channel HydroCel Geodesic Sensor Net via EGI
software at 500 Hz (Net Station Version 5.4; Electrical Geodesics, Inc., Eugene, OR). In
addition, four face channels (61-64) on the nets were removed in order to measure other
psychophysiological measures such as heart rate. Impedance values were checked prior to data
collection for all of the EEG channels in order to confirm if they were below 50kΩ.
2.4 EEG Preprocessing
For EEG preprocessing, EEGLAB toolbox (Delorme & Makeig, 2004) were used with
custom MATLAB scripts (The MathWorks, Natick, MA) via procedures from the Maryland
Analysis of Developmental EEG (MADE) pipeline (Debnath et al., 2020, https://github.com/
ChildDevLab/MADE-EEG-preprocessing-pipeline). The preprocessing methods have been

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described in detail in previous publications (Morales et al., 2022). In short, continuous EEG data
was high-pass filtered offline at 0.3 Hz and low-pass filtered at 49 Hz. Additionally, bad
channels within the data set were identified and removed via EEGLAB plug-in FASTER (Nolan
et al., 2010). For the removal of ocular artifacts, an independent component analysis (ICA) was
performed on a copied data set at 1 second epochs. Moreover, noisy segments within the data
(e.g., muscle movement) were rejected using a combined voltage threshold of +/-1000 μV and
spectral threshold (range -100 dB to +30 dB) within the 20–40 Hz frequency band. If this
rejection process identified an artifact in more than 20% epochs for a given channel, the channel
was then removed from both the ICA copied dataset and original data set.
Using this dataset, ICA decomposition was performed, and ICA weights were then
copied back to the original continuous dataset (Debener et al., 2010). Using the Adjusted-
ADJUST algorithm, artificial ICs were removed from the original data set (Leach et al., 2020;
Mognon et al., 2011). Next, EEG data was split into 2 second epochs and went through two
additional steps of artifact rejection. The first step was to catch any residual ocular activity that
was not removed through ICA; epochs in which ocular channels (1, 5, 10, and 17) voltages that
exceeded ±150 μV were rejected. The second step interpolated any channels in which the epochs
from any non-ocular channel voltages exceeded ±125 μV. If more than 10% of the channels (not
considering globally rejected channels) exceeded ±125 μV, then the epoch was rejected instead.
If there were any missing channels, then they were interpolated using the spherical spline method
(Perrin et al., 1989). Lastly, the data were referenced to the average reference. Power spectra
were computed from the artifact-free epochs using Welch’s method from 1 to 49 Hz with a
hamming window in EEGLAB with a frequency resolution of 0.5 Hz.

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2.5 Measures
2.5.1 Maternal Depression and Anxiety Symptoms. Maternal depressive symptoms
were assessed during pregnancy using the Edinburgh Postnatal Depression Scale (EPDS; Cox et
al., 1987). This 10-item self-report questionnaire assessed the mother’s thoughts and emotions
within the past seven days for symptoms of postnatal depression. Each item had four multiple
choice answers that varied from negative to positive responses. Sample items included, “I have
felt sad or miserable” and “The thought of harming myself has occurred to me.” Responses from
the mothers were averaged to create the corresponding score. High scores indicated increased
levels of depression symptoms. The EPDS is a valid and reliable measure of maternal prenatal
depressive symptoms (Bergink et al., 2011). For the current study, the Cronbach’s alpha for
maternal depression was .82, showing high internal consistency.
Maternal anxiety symptoms were assessed using the Stress Spielberger State Anxiety
Scale (STAI; Spielberger et al., 1983). This 40-item self-report questionnaire assesses an
individual’s thoughts and emotions that coincide with either state (20 items) or trait (20 items)
anxiety symptoms. The format for each item is a 4-point Likert scale ranging from 1 meaning
“Not at all” to 4 meaning “Very much so.” The current study focused on both state and trait
anxiety items. Sample items that were assessed for state anxiety included, “I feel jittery” and “I
am tense”. Sample items that assessed trait anxiety included, “I feel like a failure” and “I feel
inadequate.” The responses were averaged in order to create the corresponding score for each
mother. High scores indicated high levels of state or trait anxiety symptoms. The STAI is a valid
measure of state and trait anxiety symptoms during pregnancy (Gunning et al., 2010). The
Cronbach’s alphas for maternal trait and state anxiety scores were .90 and .88, showing high
internal consistency.

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2.5.2 Maternal Socioeconomic Status. Maternal SES was assessed during pregnancy
using a self-reported demographic questionnaire. Mothers reported on their maternal education
level, monthly gross income, and type of health insurance. Highest level of education was
reported using different education levels ranging from 1 (some primary school) to 7 (post
graduate). Mothers reported their monthly gross income using a range of different income
options from 1(250) to 7 (>5,000). Lastly, type of health insurance was reported using two
different options (0 Commercial Health Insurance/Commercial HMO; 1 = Public Assistance).
These items (maternal education level, monthly gross income, and type of health insurance) were
combined as a factor variable for overall SES within our structural equation models.
2.5.3 Frontal Alpha Asymmetry. Children’s frontal alpha asymmetry was measured
using EEG data during Baseline (i.e., resting state) recording. We estimated relative alpha power
as the average of alpha power (7-13 Hz) over total power (1-50 Hz). The alpha power was then
averaged by the electrode clusters corresponding to F3 and F4 locations (F3: 9, 11, 12, 13, 14;
F4: 2, 3, 57, 59, 60). Analyses were performed for the EO condition. Lastly, asymmetry scores
were computed using differences between transformed power scores within the mid-frontal
region (lnF4–lnF3; Vincent et al., 2021). Positive scores indicated greater left frontal alpha
asymmetry whereas negative scores indicated greater right frontal alpha asymmetry.
2.5.4 Child Internalizing and Externalizing Symptoms. Children’s internalizing and
externalizing psychopathologies was assessed using the Strengths and Difficulties Questionnaire
(SDQ; Goodman, 1997). Mothers filled out a 25-item questionnaire pertaining to their child’s
thoughts, behaviors, and peer relations over the last six months. The format for each item is a 3-
point scale ranging from “Not true,” “Somewhat true,” to “Certainly true.” The SDQ is
composed of subscales that include emotional, conduct, hyperactivity, peer problems, and

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prosocial. The internalizing scale utilizes the emotional and peer problems subscales whereas the
externalizing scale utilizes the hyperactivity and conduct subscales.
The current study focused on the internalizing (10 items) and externalizing (10 items)
subscales. Sample items for internalizing items include “Many fears, easily scared” and “Picked
on or bullied by other youth.” Sample items for externalizing items include “often loses temper”
and “Easily distracted, concentration wanders” (Goodman, 1997). Mother responses from each
of the items were then averaged to create the corresponding subscale scores. High scores
indicated increased levels of internalizing and externalizing problems. The SDQ is a valid
measure for children’s internalizing and externalizing problems (Riso et al., 2010; Van Roy et
al., 2008). The Cronbach’s alphas for the internalizing and externalizing problem items were .67
and .84.
2.6 Data Analysis Plan
For model one, testing hypothesis one, separate path analyses were conducted for each
component of early maternal internalizing symptoms (i.e., predictor; maternal depression and
anxiety) as well as overall SES (i.e., predictor, monthly gross income, and type of maternal
health insurance) to examine their overall relations with alpha asymmetry, as well as
externalizing and internalizing symptoms. Another path analysis was used for model two, testing
hypothesis two, examining the relation between child frontal alpha asymmetry and internalizing
and externalizing problems. For model three, testing hypothesis three, a one path model was run
in order to examine the unique impacts of each predictor by evaluating their impact while
controlling for each other. Given the correlation within variables of maternal internalizing
symptoms, the main analysis combined maternal depression and state and trait anxiety into a one
factor variable (i.e., prenatal Maternal Internalizing symptoms). Maternal education level,

14
monthly gross income, and type of maternal health insurance were combined into a one factor
variable to better measure SES. Missing data was handled using full information maximum
likelihood (FIML) to account for missing data as well as reduce potential bias in the parameter
estimates (Enders & Bandalos, 2001).

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Chapter 3: Results
3.1 Preliminary Analyses
Tables 1 and 2 show the descriptive statistics for the variables of interest of the mother
and child participants. Furthermore, table 2 shows the zero-order correlations examining the
relation among the main variables. Mothers’ prenatal depression was positively correlated with
mothers’ prenatal state and trait anxiety. Mothers’ prenatal depression, state, and trait anxiety
were longitudinally associated with children’s higher internalizing and externalizing scores.
Lastly, children’s internalizing and externalizing scores were positively associated with each
other.
We examined if demographic variables (i.e., race, ethnicity, child sex, child age, maternal
age, maternal drinking, smoking, drug use, and opioids) were associated with the study variables.
The results showed no significant patterns of findings except for child sex and child age.
Therefore, child sex and age were added to the main path analyses.

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Table 1
Descriptive Statistics for Children’s Sex and Race. Descriptive Statistics for Mothers’ Race,
Education, Health Insurance, and Marital Status.
Child Variable n % Mother Variable n %
Sex Race
Female 221 53.25 White 343 82.65
Male 194 46.75 American Indian 54 13.01
Race Other 18 4.34
White 331 79.76 Ethnicity
American Indian 53 12.77 Non-Hispanic Latinx 401 96.63
Other 31 7.47 Hispanic Latinx 14 3.37
Ethnicity Health Insurance
Non-Hispanic Latinx 396 95.42 Commercial 210 50.60
Hispanic Latinx 19 4.58 Public Assistance 104 25.06
Missing 101 24.34
Married
Yes 299 72.05
No 17 4.10
Missing 99 23.85
Education
Some Primary School 1 0.24

Completed Primary
School 3 0.72
Some High School 15 3.61

Completed High
School 24 5.78
Some College 88 21.20
Completed College 127 30.60
Postgraduate 58 13.98
Missing 99 23.86
Note: Children’s descriptives were measured during infancy. Maternal descriptives were
measured during the prenatal period.

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Table 2
Mother and Child Descriptive Statistics of Variables of Interest; Mother and Child Within and
Between Correlations
Variable M SD N Min Max 1 2 3 4 5 6 7 8 9
1. Prenatal Maternal
Depression 4.45 3.45 411 0 17 -
2. Family Monthly
Income 3156.45 1438.93 310 250 5000 -0.23 -
3. Maternal Education 5.56 1.11 316 1 7 -0.04 0.56 -
4. Health insurance - - 314 - - 0.16 -0.55 -0.58 -
5. Prenatal Maternal
Trait Anxiety 29.17 7.51 411 20 63 0.69 -0.23 -0.07 0.19 -
6. Prenatal Maternal
State Anxiety 25.76 6.64 411 20 59 0.53 -0.19 -0.04 0.13 0.66 -
7. Child Alpha
Asymmetry Score -0.02 0.34 415 -1.13 1.02 0.02 -0.08 -0.15 0.13 0.00 0.00 -
8. Child
Externalizing 4.43 3.33 337 0 16 0.25 -0.26 -0.09 0.13 0.21 0.19 -0.04 -
9. Child
Internalizing 2.85 2.52 336 0 13 0.24 -0.26 -0.15 0.19 0.24 0.22 0.08 0.39 -

Note: Maternal depression and anxiety scores were measured during the prenatal period, child
frontal alpha asymmetry, internalizing, and externalizing problems were measured at 5, 7, 9, and
11 years of age. Health Insurance was coded as a categorical variable (0 = commercial health
insurance; 1 = public assistance).

3.2 Main Analyses
The first hypothesis stated that higher early maternal internalizing symptoms and low
SES would be associated with right frontal alpha asymmetry in children. Additionally, higher
early maternal internalizing symptoms and low SES were hypothesized to be associated with
higher internalizing and externalizing problems in children. Results from the path models are
shown in Table 3 and Figure 1. Results indicated prenatal maternal internalizing symptoms did
not predict children’s right frontal alpha asymmetry (p = 0. 478). Similarly, when examining
each component of maternal internalizing symptoms separately (depression, and state and trait

18
anxiety), there were no significant relations with children’s frontal alpha asymmetry scores.
However, prenatal maternal internalizing symptoms was found to be associated with children’s
externalizing (b = 0.229, p < 0.001) and internalizing problems (b = 0.23, p < 0.001). Separate
analyses showed that similar results were found for each component of maternal internalizing
symptoms (depression, and state and trait anxiety) predicting children’s internalizing and
externalizing problems (not shown). Finally, results revealed that prenatal SES was predictive of
children’s internalizing (b = -0.23, p = 0.004) and externalizing (b = -0.164, p = 0.019) problems.
In addition, there was a significant negative association between prenatal SES predicting
children’s right frontal alpha asymmetry scores (b = -0.17, p = 0.006), such that children lower in
SES showed right frontal alpha asymmetry.
The second hypothesis stated that right frontal alpha asymmetry in children would be
associated with higher internalizing problem scores. Additionally, we did not expect a significant
association between children’s right frontal alpha asymmetry and externalizing problems. Path
analyses were conducted to examine the effects of child’s alpha asymmetry on internalizing and
externalizing problems. The results revealed non-significant findings between children's frontal
alpha asymmetry and internalizing and externalizing problems (see Table 3 and Figure 1).
Children’s right frontal alpha asymmetry was not significantly associated with either
internalizing or externalizing problems.
The third hypothesis stated that higher early maternal internalizing symptoms and low
SES would be associated with right alpha asymmetry, which would be associated with higher
internalizing problems, supporting a significant mediation. We did not expect to observe a
significant mediation of the relation between early maternal internalizing symptoms, low SES,
and child externalizing problems. All predictors were examined in one model. Results revealed

19
no significant mediation between early maternal internalizing symptoms and SES predicting
children’s frontal alpha asymmetry for internalizing and externalizing problems (see Table 3 and
Figure 1).

Table 3
Mother Internalizing Symptoms at the Prenatal Period Predicting Children’s frontal alpha
asymmetry and Internalizing/Externalizing Problems at 5, 7, 9, and 11 Years of Age (n = 415)
Predictors/Outcome β b SE z p CI Lower CI Upper
Model 1
Child Absolute Asymmetry
Child Sex -0.05 -0.03 0.03 -1.08 0.281 -0.096 0.031
Child Age 0.02 0.003 0.01 0.34 0.734 -0.014 0.019
Prenatal Maternal
Internalizing Symptoms -0.04 -0.005

0.01

-0.71 0.478 -0.020 0.009
Prenatal SES -0.17 -0.07 0.03 -2.73 0.006 -0.121 -0.02
Child Internalizing

Child Sex 0.03 0.13 0.27 0.50 0.615 -0.392 0.648
Child Age -0.01 -0.02 0.07 -0.23 0.817 -0.154 0.123
Prenatal Maternal
Internalizing Symptoms 0.23 0.22

0.06

3.80 0.000 0.110 0.342
Child Absolute Asymmetry 0.05 0.371

0.42

0.89 0.374 -0.439 1.189
Prenatal SES -0.23 -0.69 0.24 -2.89 0.004 -1.190 -0.254
Child Externalizing

Child Sex -0.266 -1.776 0.34 -5.22 0.000 -2.451 -1.105
Child Age -0.179 -0.299 0.09 -3.41 0.001 -0.47 -0.126
Prenatal Maternal
Internalizing Symptoms 0.229 0.294

0.07

3.97 0.000 0.155 0.441
Child Absolute Asymmetry -0.062 -0.606

0.51

-1.18 0.239 -1.606 0.378
Prenatal SES -0.164 -0.652 0.28 -2.34 0.019 -1.236 -0.147

20
Note: Maternal Internalizing Symptoms: Mothers depression, state, and trait anxiety from
prenatal period; Children frontal alpha asymmetry: Children’s frontal alpha asymmetry scores at
5, 7, 9, and 11 years of age; Children Internalizing and Externalizing: Children’s internalizing
and externalizing scores at 5, 7, 9, and 11 years of age; Family income variable was mean-
centered

Figure 1: Prediction for Hypotheses

3.3 Exploratory Analyses
Because the peak and range of alpha oscillations may vary across age and individuals
(Bazanova & Vernon, 2014; Sander et al., 2012), in an exploratory analysis, we employed novel
ways of characterizing the power spectrum by using specparam (Donoghue et al., 2021). The
specparam algorithm removes the 1/f component of the spectrum and uses an iterative procedure
to identify peaks (e.g., alpha peaks). Alpha power was derived as the most prominent peak in the
5-15 Hz range after removing the 1/f component for each individual, rather than using a
frequency range across all individuals. Path analyses were conducted as with the traditionally
computed alpha. Results from this exploratory analysis revealed the same significant and non-
significant effects as shown in the main path analyses, suggesting that differences in how alpha
power is estimated does not significantly influence the results.

21
Chapter 4: Discussion
The purpose of the current study was to examine whether children’s frontal alpha
symmetry mediated the associations between prenatal maternal internalizing symptoms and SES
on children’s internalizing and externalizing problems. This study was the first to examine the
longitudinal impact of prenatal maternal internalizing symptoms and SES on children’s frontal
alpha asymmetry and examined their relations to children’s internalizing symptoms in a large
sample. Results involving prenatal SES revealed a significant association with children’s frontal
alpha asymmetry as well as with internalizing and externalizing problems. In addition, mothers’
prenatal internalizing symptoms predicted later internalizing and externalizing problems in their
children. Alpha asymmetry did not relate to children’s internalizing symptoms. Follow-up
exploratory analyses revealed non-significant associations between maternal internalizing
symptoms and children’s frontal alpha asymmetry even when using novel analysis of their alpha
asymmetry scores. However, SES was still predictive of children's frontal alpha asymmetry.
Overall, the results suggest that children’s alpha asymmetry is not longitudinally related to
mothers’ internalizing symptoms or concurrently related to children’s internalizing and
externalizing problems. Results revealed interesting findings in the associations between early
SES, children’s frontal alpha asymmetry and their internalizing and externalizing problems,
supporting some of our non-preregistered hypotheses.
4.1 Maternal Characteristics
Maternal internalizing symptoms and SES were found to be significantly associated with
children’s internalizing and externalizing problems. More specifically, higher maternal
internalizing symptoms during pregnancy predicted higher internalizing and externalizing
problem scores in children. Additionally, lower SES during the prenatal stage predicted higher
internalizing and externalizing scores in children. These findings are consistent with previous

22
literature that separately reported associations between early maternal internalizing symptoms,
SES, and children’s negative outcomes (e.g., Bradely & Corwyn, 2002; Goodman et al., 2001;
Dawson et al., 2003; Monk et al., 2019). Lastly, exploratory analyses showed that prenatal
maternal internalizing symptoms and SES did not interact to predict alpha asymmetry or
children’s behavior problems.
4.2 Frontal Alpha Asymmetry
Children’s frontal alpha asymmetry did not mediate the relation between maternal
internalizing symptoms, SES, and children’s internalizing and externalizing problems. First,
maternal internalizing symptoms scores during pregnancy did not predict children’s frontal alpha
asymmetry at 5 to 11 years of age. This result differed from some of the previous research that
found associations between early maternal internalizing symptoms predicting children’s right
frontal alpha asymmetry in relation to negative childhood outcomes (Forbes et al., 2008; Lopez-
Duran et al., 2012). Even so, other studies also have not found significant results. For example, a
study by Bruder et al. (2005) did not find a significant association between parental
psychopathology and children’s frontal alpha asymmetry. There are several reasons for the
inconsistency across studies. First, previous studies examining this relation have had relatively
small samples (Forbes et al., 2008; Lopez-Duran et al., 2012), reducing power and increasing the
likelihood of false positives. Second, studies have also measured maternal psychopathology in
different ways such as examining childhood onset depression (Forbes et al., 2006), clinical
diagnosis of depression (Lopez-Duran et al., 2012), or lifetime history of depression (Bruder et
al. 2005). Previous studies that found significant associations between early maternal
psychopathology and children’s frontal alpha asymmetry tended to examine children of mothers
with diagnosed depression (either during childhood and/or lifetime history) compared to children

23
of mothers without a history of depression (e.g., Feng et al., 2012; Forbes et al., 2008; Lopez-
Duran et al., 2012). Our current study only examined maternal internalizing symptoms and most
mothers had a relatively low number of symptoms. Associations between early maternal
psychopathology and children’s frontal alpha asymmetry seem to be found more often when
mothers have a diagnosis of psychopathology; thus, future studies should examine differences
between mothers with a diagnosis compared to mothers with internalizing symptoms.
When examining SES as a predictor for children’s frontal alpha asymmetry, results
indicated that lower SES was predicted of children’s right frontal alpha asymmetry. This finding
is in line with previous studies that reported concurrent relations between low SES and right
frontal alpha asymmetry (Gatzke-Kopp et al., 2014). The current study extends those findings by
examining this relation longitudinally. However, children’s frontal alpha asymmetry did not
mediate the relationship between SES and children’s internalizing and externalizing problems.
This is one of the first studies to examine this mediation as well as prenatal SES predicting
children’s frontal alpha asymmetry. Thus, future research is still needed to better understand the
relation between SES and children’s frontal alpha asymmetry. For example, future studies could
examine what factors mediate the relation between SES and alpha asymmetry, and SES and later
psychopathology.
Results showed a non-significant relationship between children’s frontal alpha
asymmetry and their internalizing and externalizing problems. In addition, given the non-
significant association between frontal alpha asymmetry and children’s internalizing and
externalizing problems, there was no support for the mediation. This non-significant finding is
counter to previous research that reported a relation between children’s right frontal alpha
asymmetry and their internalizing problems (e.g., Feng et al., 2012; Thibodeau et al., 2006).

24
However, a meta-analysis by Peltola et al. (2014) found non-significant associations between
children’s frontal alpha asymmetry and their internalizing and externalizing problems. Findings
from the current study provide further support that frontal alpha asymmetry may not be a robust
predictor for socio-emotional problems in children. Additionally, the current study examined
frontal alpha asymmetry using resting state EEG data; there have been studies that measured
frontal alpha asymmetry scores while presenting stimuli. A study by Mulligan et al. (2022)
examined the relation between frontal alpha asymmetry and children’s externalizing problems
while being presented with a stressor task. The study found that children who had higher
externalizing problems showed left frontal alpha asymmetry during the stressor task. Resting
state data was also collected by the researchers; they did not find any association between frontal
alpha asymmetry and externalizing problems when examining resting state data (Mulligan et al.,
2022). In addition, studies have indicated that anger, an emotion related to externalizing
behavior, is more closely associated with left frontal alpha asymmetry due to trait-like approach
motivation tendencies (Harmon-Jones & Allen, 1998). The current study only examined
differences in brain activation during the resting state; therefore, there may have been potential
differences in alpha asymmetry if participants were presented with a task that elicited an
affective state. Thus, future research should examine if it is more beneficial to measure frontal
alpha asymmetry during a stressor related task rather than just during resting state.
4.3 Study Limitations, Implications, and Conclusions
There are several limitations for the current study. The current study was a relatively low-
risk sample. The majority of mothers had predominantly low internalizing symptoms as well as
the children being low in internalizing and externalizing problems. Future research should
include a more diverse sample size with a wider range of SES, maternal internalizing symptoms,

25
and children’s internalizing and externalizing symptoms. In addition, we only examined parental
internalizing symptoms and SES and did not account for changes between pregnancy and when
the child was 5 to 11 years of age.
Despite these limitations, results from this study suggest several theoretical and practical
implications. First, the current study was the first to examine the longitudinal impact of maternal
internalizing symptoms and SES on children’s frontal alpha asymmetry in relation to their
internalizing and externalizing problems in a large sample. The significant findings of early
maternal internalizing symptoms and SES predicting higher internalizing and externalizing
problems in children add to a large corpus of studies highlighting the importance of early
maternal characteristics on later socioemotional outcomes. Nonetheless, our findings suggest that
frontal alpha asymmetry is not a mediator of these relations. Future studies should try to identify
other factors that may underlie or ameliorate such relations. Moreover, our findings still
highlight the need for interventions during pregnancy in order to combat these risk factors. Thus,
results from the current study can be used to further advocate for early intervention programs for
pregnant mothers that may help alleviate or reduce internalizing symptoms as well as better
financial assistance during pregnancy.
In terms of future directions, samples should include more variability within SES and
maternal internalizing symptoms as well as children with internalizing and externalizing
problems. Examining mothers with clinical diagnosis of depression and/or anxiety may also lead
to different results. Additionally, future research should compare differences in internalizing
symptoms and SES from pregnancy and when EEG is recorded in order to examine possible
differences that may also impact children’s internalizing and externalizing problems. Studies
have examined these risk factors concurrently with children’s internalizing and externalizing

26
problems. Overall, results from the present study show potential next steps for future research to
further examine prenatal maternal internalizing symptoms, SES, children’s frontal alpha
asymmetry, and internalizing and externalizing problems.
Overall, the current study highlights the importance of examining various sources of
maternal characteristics that independently predict children's frontal alpha asymmetry as well as
internalizing and externalizing problems. More research is needed to further examine the impact
of early SES on children’s frontal alpha asymmetry and their role in the development of
internalizing and externalizing outcomes. In addition, this study contributes to the growing body
of research examining prenatal risk factors on children’s socioemotional outcomes. Our study in
a large community sample suggests that alpha asymmetry at rest is not a strong correlate of
children’s internalizing or externalizing problems. Future research should examine other
neurobiological factors that mediate the link between prenatal risk factors and their socio-
emotional development.

27
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Vincent, K. M., Xie, W., & Nelson, C. A. (2021). Using different methods for calculating frontal
alpha asymmetry to study its development from infancy to 3 years of age in a large longitudinal
sample. Developmental Psychobiology, 63(6). https://doi.org/10.1002/dev.22163

Abstract (if available)

Abstract Prenatal maternal internalizing psychopathology (depression and anxiety) and socioeconomic status (SES) have been independently associated with higher risk for internalizing and externalizing problems in children. However, the mechanisms behind these associations are not well understood. Numerous studies have linked greater right frontal alpha asymmetry to psychopathology, especially internalizing problems. Even so, findings have been mixed. Several studies have also linked maternal internalizing psychopathology to children’s frontal alpha asymmetry. Additionally, emerging studies have linked SES in relation to children’s frontal alpha asymmetry. Yet, only a few studies have examined these associations within a longitudinal design, and most have used relatively small samples. The current preregistered study utilizes data from a large study of young children (N=415; Meanage=7.27; Rangeage=5-11 years) to examine the association between prenatal maternal internalizing symptoms, children’s frontal alpha asymmetry, and behavior problems in a large sample of children. Prenatal maternal internalizing symptoms did not predict children's frontal alpha asymmetry and there was no association between frontal alpha asymmetry and behavior problems. However, mothers’ internalizing symptoms during pregnancy predicted children’s internalizing and externalizing outcomes. Non-preregistered analyses showed that lower prenatal maternal SES predicted greater right frontal alpha asymmetry and increased externalizing and internalizing problems. Results of this large, longitudinal study suggest that children’s alpha asymmetry is not related to children’s internalizing or externalizing problems or predicted by maternal internalizing symptoms in a community sample. Future research should examine the impact of early SES on children’s frontal alpha asymmetry in high-risk samples.

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University of Southern California Dissertations and Theses

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Pregnancy in the time of COVID-19: effects on perinatal mental health, birth, and infant development

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Creator Hernandez, Alexis Marie (author)

Core Title Examining the impact of prenatal maternal internalizing symptoms and socioeconomic status on children’s frontal alpha asymmetry and psychopathology

School College of Letters, Arts and Sciences

Degree Master of Arts

Degree Program Psychology

Degree Conferral Date 2023-05

Publication Date 04/07/2023

Defense Date 03/31/2023

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag children psychopathology,EEG,frontal alpha asymmetry,maternal internalizing symptoms,OAI-PMH Harvest,socioeconomic status

Format theses (aat)

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Morales, Santiago (committee chair), Manis, Frank (committee member), (Schwartz, David)

Creator Email alexismh@usc.edu,hernandez.alexis234@gmail.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-oUC112956339

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Legacy Identifier etd-HernandezA-11587

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Rights Hernandez, Alexis Marie

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Source 20230410-usctheses-batch-1018 (batch), University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

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