Tilburg University
The late positive potential (LPP)
McLean, Mia; Van Den Bergh, B.R.H.; Baart, Martijn; Vroomen, Jean; van den Heuvel,
Marion
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International Journal of Psychophysiology
DOI:
10.1016/j.ijpsycho.2020.06.005
Publication date:
2020
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Citation for published version (APA):
McLean, M., Van Den Bergh, B. R. H., Baart, M., Vroomen, J., & van den Heuvel, M. (2020). The late positive
potential (LPP): A neural marker of internalizing problems in early childhood. International Journal of
Psychophysiology, 155, 78-86. https://doi.org/10.1016/j.ijpsycho.2020.06.005
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International Journal of Psychophysiology 155 (2020) 78–86
Contents lists available at ScienceDirect
International Journal of Psychophysiology
journal homepage: www.elsevier.com/locate/ijpsycho
The late positive potential (LPP): A neural marker of internalizing problems
in early childhood
T
Mia A. McLeana, Bea R.H. Van den Berghb,c, Martijn Baartd,e, Jean Vroomend,
⁎
Marion I. van den Heuveld,
a
Department of Pediatrics, University of British Columbia, Canada
Health Psychology, University of Leuven (KU Leuven), Leuven, Belgium
c
Department of Welfare, Public Health and Family, Flemish Government, Brussels, Belgium
d
Department of Cognitive Neuropsychology, Tilburg University, Tilburg, the Netherlands
e
Basque Center on Cognition, Brain and Language (BCLB), 20009 San Sebastian, Spain
b
A R T I C LE I N FO
A B S T R A C T
Keywords:
Late positive potential
EEG
Internalizing problems
Preschoolers
Background: One potentially relevant neurophysiological marker of internalizing problems (anxiety/depressive
symptoms) is the late positive potential (LPP), as it is related to processing of emotional stimuli. For the first
time, to our knowledge, we investigated the value of the LPP as a neurophysiological marker for internalizing
problems and specific anxiety and depressive symptoms, at preschool age.
Method: At age 4 years, children (N = 84) passively viewed a series of neutral, pleasant, and unpleasant pictures
selected from the International Affective Pictures System. Affective picture processing was measured via the LPP
(EEG recorded) and mothers reported on child behavior via the Child Behavior Checklist 1 ½ - 5 (internalizing,
DSM-anxiety, DSM-affective/depression subscales). Difference scores between the neutral and affective pictures
(i.e., neutral-pleasant and neutral-unpleasant) were computed for posterior, central and anterior brain locations
for early (300-700 ms), middle (700-1200 ms) and late (1200-2000 ms) time windows.
Results: Greater LPP difference scores for pleasant images in the anterior recording site, in the middle time
window, were associated with greater internalizing behaviors. Greater DSM-anxiety symptoms were associated
with greater LPP difference scores for unpleasant and pleasant images. After correcting for multiple testing, only
the association between greater DSM-affective/depression symptoms and greater LPP difference scores for unpleasant images in the anterior recording site (early time window) remained significant.
Discussion: Our study has identified a potential neural marker of preschool internalizing problems. Children with
larger LPPs to unpleasant images may be at greater risk of internalizing problems, potentially due to an increased
emotional reactivity.
Internalizing problems (e.g. anxiety, depressive symptoms) are the
most common mental health problem reported by children. In preschool through early school years, approximately one-fifth of children
experience internalizing problems and specific anxiety disorders
(Beesdo et al., 2009; Dittman et al., 2011; Paulus et al., 2015; Whalen
et al., 2017). At preschool age anxiety disorders are more prevalent,
however, clinical depression is being more widely recognized and diagnosed at this age (Whalen et al., 2017). Child internalizing behaviors
are characterized by greater behavioral expression of negative emotions
(De Pauw and Mervielde, 2010) and altered neural processing of negative or threatening stimuli (Fu and Pérez-Edgar, 2019) such that
those children excessively attend to negative or threatening information
(Bar-Haim et al., 2007; Daleiden and Vasey, 1997). Research
⁎
investigating how neurophysiological measures relate to real-world
functioning and behavior can help elucidate functional brain correlates
associated with internalizing problems.
Event-related brain potentials (ERPs) recorded from the scalp
through non-invasive electroencephalography (EEG) can be used to
study engagement with emotional stimuli with excellent temporal resolution (on the order of milliseconds). They are therefore ideal for
studying neural processes underlying dysfunctional emotional processing related to clinical and sub-clinical internalizing problems. The late
positive potential (LPP) is an ERP component which provides a neural
measure of emotional processing (Hajcak et al., 2012). It indexes sustained attention towards motivationally salient stimuli that can be reliably assessed across development, from early childhood (Hua et al.,
Corresponding author at: Department of Cognitive Neuropsychology, Tilburg University, Warandelaan 2, 5037AB Tilburg, the Netherlands.
E-mail address: m.i.vdnheuvel@tilburguniversity.edu (M.I. van den Heuvel).
https://doi.org/10.1016/j.ijpsycho.2020.06.005
Received 21 January 2020; Received in revised form 16 May 2020; Accepted 11 June 2020
Available online 16 June 2020
0167-8760/ © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/BY/4.0/).
International Journal of Psychophysiology 155 (2020) 78–86
M.A. McLean, et al.
associated with greater LPP response to unpleasant images one year
prior (Kujawa et al., 2016).
Kessel et al., 2017b were the first to examine the discriminant validity of LPP amplitudes for pleasant, unpleasant and neutral images in
relation to child temperamental constructs associated with both depression and anxiety. The authors found that lower positive affectivity
(a hallmark of depressive symptoms) at 6 years was associated with
decreased LPP for pleasant but not unpleasant images at 9 years. Aspects of negative affectivity (fear, sadness) were more related to LPP
response to unpleasant images. Interestingly, greater fear (a correlate of
anxiety), was associated with greater LPP response to negative images
while greater sadness (more akin to depression) was associated with
decreased LPP amplitude to positive images. Relatedly, studies suggest
that children and adolescents of depressed parents display a blunted
LPP (Kessel et al., 2017a; Kujawa et al., 2012; Nelson et al., 2015) while
children of anxious parents display greater LPP between neutral and
unpleasant images only (Nelson et al., 2015). Yet, no study to date has
examined associations between LPP responses to emotional stimuli
(pleasant, unpleasant and neutral) and anxiety as well as specific depressive symptoms in preschool children.
To the best of our knowledge, research is yet to investigate whether
neural processing of emotion, as measured by the LPP in response to
both pleasant and unpleasant images, is associated with internalizing
problem behaviors and importantly, specific sub-dimensions of internalizing behaviors in children at preschool age. As part of a longitudinal
prospectively studied cohort, the current study examined neural reactivity to affective images (i.e. LPP) as a neurophysiological correlate
of internalizing behaviors in a non-clinical population of preschool
children. In line with our prior work in this cohort (van den Heuvel
et al., 2018) we examined the LPP across three scalp regions (Anterior,
Central, Posterior) at three time windows (Early, Middle, Late). We
hypothesized that children with higher LPP values to negative stimuli
relative to neutral, and lower response to pleasant stimuli have higher
internalizing problems measured using the Child Behavior Checklist,
CBCL 1 ½ - 5 (Achenbach and Rescorla, 2001). Given findings from the
adolescent and adult literature as well as emerging research in children,
we predicted that a lower response (lower LPP) to pleasant stimuli relative to neutral stimuli was associated with greater depressive symptoms as measured by the CBCL DSM-Oriented Affective problems subscale. Conversely, we expected a higher response (greater LPP) to unpleasant versus neutral stimuli to be associated with greater anxiety
symptoms (scores on the CBCL DSM-Oriented Anxiety problems subscale). No specific hypotheses regarding brain-behavior associations by
particular region and time windows were made, given the exploratory
nature of our research.
2014), through adolescence (Kujawa et al., 2013) and adulthood
(Moran et al., 2013). The LPP is a relative positivity in the ERP that
begins as early as 200 ms after stimulus onset and is pronounced at
centro-parietal recording sites. It is increased for emotional compared
with neutral stimuli ranging from pictures, faces and words. Changes in
amplitudes are evident throughout the duration of picture presentation.
As a temporal measure of emotional responsivity to stimuli, the LPP
is a potentially useful neurophysiological correlate of internalizing
problems. In adolescence through adulthood, altered LPP to emotional
stimuli has been associated with internalizing disorders, including anxiety and depression (Bunford et al., 2017; Foti et al., 2010; Kujawa
et al., 2015; MacNamara et al., 2016). Despite comorbidity (Kaufman
and Charney, 2000) the literature to-date suggests that LPP responsivity
may be related to anxious and depressive symptoms differentially, in
adolescence and adulthood (MacNamara et al., 2016; Sandre et al.,
2019; Weinberg and Sandre, 2018). Depressive symptoms have been
linked to reduced reactions to pleasant versus neutral faces and images
in adolescents and adults (MacNamara et al., 2016; Sandre et al., 2019;
Weinberg et al., 2016). Other work in early adolescence suggests those
with depression (Grunewald et al., 2019), as well as those at risk for
depression based on temperamental traits (Speed et al., 2015) may be
linked to reduced reactions to both pleasant and unpleasant faces, potentially reflecting a global disengagement from environmental stimuli
(Rottenberg et al., 2005). Finally, some work suggests that depressive
symptoms may be associated with greater LPP to emotional stimuli
(Burkhouse et al., 2017) and specifically, negatively valenced self-referential words (Auerbach et al., 2015; Speed et al., 2016). Differences
are likely due to the nature of the stimuli presented and age of participants. Considering anxiety, adolescents and adults consistently show
increased engagement with negative environmental stimuli as indexed
via greater LPP to unpleasant versus neutral images (Kujawa et al.,
2015; MacNamara et al., 2016, 2019).
In children, as young as preschool age (Hua et al., 2014; van den
Heuvel et al., 2018) the LPP has been found to be sensitive to emotional
stimuli (Hua et al., 2014; Kujawa et al., 2013) with pleasant and unpleasant images eliciting significantly larger LPP amplitudes than
neutral pictures. Emotional stimuli may be processed differently by
young children compared to adults. Research suggests that children
display a strong ‘negativity bias’, perceiving negativity or threat in
ambiguous situations or neutral facial expressions (Marusak et al.,
2016; Tottenham et al., 2013) with greater bias potentially linked to the
development of internalizing behaviors. Yet, very little work has examined the relationships between observed behavior and neurophysiology with respect to the LPP in early development. This is surprising
given the potential utility of non-invasive brain-behavior research for
treatment intervention during early childhood, at symptom onset.
Studies in childhood that have examined the LPP in relation to internalizing behaviors have done so by comparing responses to neutral
stimuli to either unpleasant or pleasant stimuli. Across studies (DeCicco
et al., 2012; Dennis and Hajcak, 2009), greater LPP amplitudes for
unpleasant in comparison to neutral stimuli showed small but significant associations with greater anxious-depressed symptoms (Dennis
and Hajcak, 2009) and greater anxiety in children aged 5–10 years
(DeCicco et al., 2012). Recently, Whalen et al. (2020) found that children with preschool-onset Major Depressive Disorder displayed reduced
responding to pleasant stimuli. These studies further our understanding
of the LPP as a correlate of internalizing behaviors, but are unable to
assess the discriminate validity of the LPP. Of the studies that have
examined LPP response in relation to both pleasant and unpleasant in
comparison to neutral images during childhood, no associations between behavioral assessments and LPP response to pleasant versus
neutral images were established. One study by Solomon et al., (2012)
found that enhanced LPP response while passively viewing unpleasant
compared to neutral images was associated with observed fearful behavior, but not maternal-reported fearfulness or anxiety at 5–7 years.
Similarly, greater internalizing symptoms at age 10 years were
1. Methods
1.1. Participants
The present study is part of the Prenatal Early Life Stress (PELS)
study—a prospective pregnancy cohort study conducted at Tilburg
University, the Netherlands. The study was approved by the medical
ethical committee of the St Elisabeth Hospital, Tilburg, the Netherlands,
and was conducted in full compliance with the Helsinki Declaration. All
participating mothers and partners provided informed consent. For the
current study, we analyzed the data of participants with complete child
EEG data and maternal-report of child behavior at 4 years.
Data from 84 four-year-olds (mean age = 48 months, S.D. = 0.81,
40 boys) were included in the current study. Of the 103 four-year-olds
that were assessed with EEG, 19 were excluded from analyses due
missing questionnaire data (N = 6), technical problems (N = 4), fussiness/excessive movement (N = 5), low number of artifact free trials
(< 20 trials; N = 3), and due to cortical visual impairment (N = 1). An
earlier analysis of the EEG data from these children was previously
published in van den Heuvel et al. (2018).
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International Journal of Psychophysiology 155 (2020) 78–86
M.A. McLean, et al.
three regions: posterior (PO4, PO8, O2, Oz, POz, PO3, PO7, and O1),
central (C4, C6, CP6, Cz, CPz, C3, C5, and CP5), and anterior (FC4, F4,
F6, Fpz, AFz, FC3, F3, and F5).
1.2. Measurements
1.2.1. Child behavior
Mothers reported on the child's behavior using the Child Behavior
Checklist 1½ - 5 years (CBCL/1 ½-5; Achenbach and Rescorla, 2001).
Data from the internalizing scale of the CBCL and the DSM-IV anxiety
(anxiety symptoms) and affective disorder (depressive symptoms)
subscales are reported here. Mothers rate how true statements regarding the child's behavior are from 0 = Not True, 1 = Somewhat or
Sometimes True, to 2 = Very True or Often True. The CBCL-Internalizing
total raw score is calculated as the sum of the responses to 36 statements, while the DSM anxiety and affective disorders sum responses to
10 statements for each subscale. The CBCL-Internalizing as well as
DSM-IV disorder subscales demonstrate strong psychometric qualities
including strong reliability and validity (Achenbach and Rescorla,
2001). The CBCL-internalizing subscale showed strong internal consistency (Cronbach's α = 0.82). Internal consistencies for the CBCLaffective disorder (Cronbach's α = 0.58) and CBCL-anxiety disorder
subscales (Cronbach's α = 0.55) were acceptable, considering the low
number of items on each scale (10 items).
1.2.4. Statistical analyses
The ERPs in response to the Neutral stimuli were not correlated with
the Internalizing problems, DSM-anxiety or DSM-affective symptoms at
any of the three scalp regions (Anterior, Central, Posterior) at any of the
time windows (Early, Middle, Late), all ps > .05 (FDR-corrected;
Benjamini and Hochberg, 1995), and were considered a within-subject
base-line. We therefore subtracted the ERPs in response to the Neutral
stimuli from the ERPs in response to the Pleasant and Unpleasant stimuli, and analyzed the relationship with Internalizing problems and the
DSM-anxiety and DSM-affective symptoms subscales via Pearson's correlations. Analyses were corrected for multiple testing by using FDRcorrection (Benjamini and Hochberg, 1995), controlling per hypotheses
(Internalizing, DSM-anxiety, DSM-affective disorder), per region
(Anterior, Central, Posterior), per stimulus (pleasant, unpleasant). Significant correlations were followed-up with linear regression models
including all LPP windows (Early, Middle, Late). This allowed us to
partial out the variance related to the voltage change over time within a
scalp area and type of LPP difference wave. All analyses were performed in SPSS (IBM; version 24).
1.2.2. Affective picture processing
Ninety age-appropriate pictures were taken from the International
Affective Picture System (IAPS; Lang et al., 2008). Thirty contained
neutral household objects or nature scenes, 30 ‘pleasant’ pictures depicted candy and happy scenes, and 30 ‘unpleasant’ pictures depicted
accidents and scary animals. All pictures were randomly displayed on a
19-in CRT monitor (2000 ms, full-screen mode: 1280 × 1024 px,
ISI = 500 ms) via the E-Prime software (version 2.0.8.74, Psychology
Software Tools, Pittsburgh, PA). The experimenter sat next to the
children during the passive viewing task. During the experiment, EEG
was recorded (see below for details), and after the experiment (which
was embedded in a longer 2-h assessment), children received a small
reward. Internal consistencies for LPP scores for neutral, pleasant and
unpleasant stimuli were strong (all Cronbach α's = 0.99).
2. Results
2.1. Descriptive statistics
Overall, the current cohort represents a non-clinical, typically developing population. In total, 11 children scored in the borderline
clinical range for internalizing problems (13.1%), with 5 of these
children meeting clinical levels (6%). For depressive symptoms, 11
children scored within the borderline clinical range (13.1%) and four of
them scored within the clinical range (4.8%). For DSM-anxiety problems, a total of six children scored within the borderline clinical range
(7.1%) and none of the children met criteria for clinical anxiety
symptoms. Scores on the CBCL-internalizing subscale were more highly
correlated with DSM-anxiety disorder subscale (r = 0.78), than DSMaffective disorder subscale (r = 0.60). DSM-affective and anxiety disorder subscales were correlated r = 0.56, suggesting each subscale was
assessing related but independent child symptoms. Independent t-tests
showed no differences in CBCL-subscale scores for boys and girls
(p's > .05). Descriptive statistics are displayed in Tables 1 and 2.
1.2.3. EEG
The electroencephalogram was recorded with BioSemi ActiveTwo
amplifiers (www.biosemi.com) at a sampling rate of 512 Hz, via 64electrodes mounted in an elastic cap according to the extended
International 10–20 system. The EEG was referenced on-line with the
active Common Mode Sense electrode (CMS) and passive ground electrode (Driven Right Leg electrode; DRL). Two additional electrodes
were placed on the mastoids, which were used for offline re-referencing. The data were (pre-)processed with the BrainVision Analyzer 2
(Brain Products, Munich, Germany) and the MATLAB (version R2012b,
The Mathworks, Inc.) based EEGLAB package (version 13.0.1; Delorme
and Makeig, 2004). After re-referencing the data (based on the average
of the mastoids), independent component analysis (ICA) implemented
in EEGLAB was used to identify and remove components that captured
blinks and eye-movements. The data were filtered off-line with a zerophase Butterworth bandpass 0.1–30 Hz (slope 24 dB) filter. Subsequently, the data were segmented into epochs of 2400 ms which included a 400 ms pre-stimulus period. Artifacts were identified as epochs
in which there was a voltage change of > 200 μV/200 ms, > 75 μV/ms,
or < 0.2 μV/100 ms, and those epochs were excluded from analyses.
Children with < 20 artifact free trials for each condition (neutral,
pleasant, unpleasant) were not included in the analysis, and the average
number of trials per participant were 25 (neutral pictures), 26 (pleasant
pictures), and 25 (unpleasant pictures). Epochs were averaged for each
stimulus category, and the resulting ERPs were baseline-corrected to
the average amplitude in the 400 ms pre-stimulus period. Following
prior work examining ERPs in the current cohort (van den Heuvel et al.,
2018) and others Solomon et al. (2012), mean LPP amplitudes were
exported to SPSS for three time windows: early (300–700 ms), middle
(700–1200 ms) and late (1200–2000 ms). We averaged the LPP over
2.2. Neural responses to affective pictures in four-year-olds
As demonstrated by van den Heuvel et al. (2018), in the same
sample, four-year-olds are able to detect differences between affective
and neutral pictures. The stimulus-locked ERPs in response to neutral,
pleasant and unpleasant pictures in our sample of four-year-olds are
presented in Fig. 1, with mean and standard deviations presented in
Table 2. Fig. 2 shows the scalp distribution LPP waves for each stimulus
type. Note that for the anterior and central regions the LPP is mirrored,
resulting in negative-going waveforms for the LPP. As a result, higher
LPP amplitudes for these areas are defined as more negative values (cf.
van den Heuvel et al., 2018).1 In the current paper, we examined
whether individual differences in these LPP amplitudes, assessed as
difference scores, predict internalizing behaviors.
1
More specifically, as with our prior analysis of this data (van den Heuvel
et al., 2018), four-year-olds showed higher LPP amplitudes to affective (pleasant and unpleasant) pictures compared to neutral stimuli at posterior electrode
sites (Early, Middle, Late time windows, p's < .001). The LPP amplitudes did
not differ between affective and neutral pictures at anterior and central recording sites at the group level, as established in van den Heuvel et al. (2018).
80
International Journal of Psychophysiology 155 (2020) 78–86
M.A. McLean, et al.
related to the DSM-affective sub-scale. Larger differences between LPP
amplitude of neutral and unpleasant stimuli are associated with higher
scores on the DSM-affective sub-scale.
Table 1
Descriptive statistics for outcome variables.
Variable
M (SD)
a
Internalizing behaviors (raw score)
CBCL DSM-affective subscalea (raw score)
CBCL DSM-anxiety subscale a (raw score)
a
6.64 (5.32)
1.79 (1.87)
2.17 (1.93)
3. Discussion
In the current study we set out to examine the Late Positive
Potential (LPP) as a potential neurophysiological marker for internalizing behaviors in children at preschool age. Considering internalizing behaviors, we observed that children with greater internalizing
behaviors attend more to pleasant stimuli. Interestingly, when examining LPP responses separately for anxiety and depressive symptoms,
we observed that children high in anxiety display higher neural responses to both pleasant and unpleasant images relative to neutral
images, while children high in depressive symptoms displayed only
higher responses to unpleasant images. Importantly, when correcting
for multiple testing, only the association between child depressive
symptoms and unpleasant images remained significant. Findings suggest that a pattern of emotional reactivity to unpleasant images may be
associated with depressive symptoms in young children.
CBCL 1 ½ - 5 years.
Table 2
Means and standard deviations for LPP amplitudes for emotional and neutral
stimuli for the three regions.
Early
M
Middle
SD
M
Late
SD
M
SD
Anterior
Pleasant
Unpleasant
Neutral
−23.84
−22.16
−23.12
9.56
8.90
8.56
−13.62
−12.88
−12.32
8.94
8.82
7.75
−6.84
−8.06
−8.21
9.37
6.45
8.19
Central
Pleasant
Unpleasant
Neutral
−22.48
−21.34
−21.16
8.58
7.22
6.72
−10.95
−11.28
−9.36
8.22
7.53
6.57
−5.54
−6.58
−6.40
9.23
5.95
7.26
Posterior
Pleasant
Unpleasant
Neutral
23.31
21.82
18.95
12.10
11.94
11.21
19.34
17.54
13.33
10.73
11.35
10.00
15.63
15.65
10.92
10.43
9.94
9.88
3.1. Depressive symptoms
When considering maternal-rated child depressive symptoms,
greater LPP to unpleasant relative to neutral images, early in processing
in the anterior scalp region, showed a small association with greater
symptom severity. DSM-affective symptoms were not associated with
greater LPP difference between pleasant and neutral stimuli. Taken
together, our findings contrast Rottenberg's (2005) emotional insensitivity context hypothesis which has been supported by much literature – showing reduced reactions to both pleasant and unpleasant
stimuli in depressive adolescents and adults (Hill et al., 2019; Sandre
et al., 2019; Weinberg et al., 2016). Findings also differ to recent empirical assessments in children that suggest blunted LPP to positive
images to be related to lower positive affectivity and greater sadness at
age 6–9 years (Kessel et al., 2017a), as well as preschool-onset major
depressive disorder assessed at 4–7 years (Whalen et al., 2020). Inconsistencies could have also been introduced due to differences in
outcomes assessed (temperament, symptoms, clinical diagnoses).
It is difficult to directly compare our research to much research in
children, given that the majority of studies in children have only examined depressive symptoms and LPP amplitude in relation to positive
but not negative images. Our finding is, however, consistent with the
few studies that have examined LPP difference waves considering both
positive and negative relative to neutral stimuli in children. This research has established associations between larger LPPs in relation to
unpleasant but not pleasant images during early processing, and anxious-depressed symptoms at 10 years (Dennis and Hajcak, 2009), as
well as in adolescents when presented with emotional self-referential
words (Auerbach et al., 2015). Children of depressed mothers similarly
show enhanced LPP response to negative stimuli (Speed et al., 2016).
Collectively, these findings support the negative potentiation hypothesis, where by negative mood evokes enhanced responses to negativelyvalenced cues in the environment (Beck, 1976). Children who display
depressive symptoms may excessively attend to negative or threatening
information, with negative mood potentially leading one to be hypersensitive or primed to react more so to negative stimuli in their
environment (Scher et al., 2005). As reviewed by Platt et al. (2017),
behavioral studies suggest that depression in childhood and adolescence is characterized by an attention and interpretation bias for negative stimuli. From early childhood onwards, attention towards negative stimuli for those displaying depressive symptoms is evident.
Interestingly, as with our previous work in this cohort (van den
Heuvel et al., 2018) our finding was specific to LPP difference waves in
the anterior region. Other work in children and adults has established
LPP-behavior associations primarily in posterior scalp regions (e.g.,
2.3. Internalizing behaviors
Results of correlation analyses between LPP values and child internalizing problems showed that the amplitude of the Middle Pleasant
– Neutral LPP difference wave was significantly associated with
Internalizing problems, such that greater difference scores were associated with greater Internalizing behaviors (Table 3). However, the
correlation did not survive correction for multiple testing. No other
significant associations were found.
2.4. DSM-IV anxiety subscale
As displayed in Table 4, when considering the DSM anxiety subscale, difference scores of the Pleasant – Neutral LPP in the anterior
region were negatively associated with anxiety problems in the middle
time-window. This association indicates that a larger difference in LPP
response to neutral and pleasant pictures is related to more anxiety
issues. In addition, greater difference scores in the Unpleasant – Neutral
LPP condition were associated with greater anxiety problems, in the
early time-window, anterior region. However, none of the significant
associations remained significant after correction for multiple testing.
2.5. DSM-IV affective subscale
Analyses examining correlations with DSM-affective (depressive)
symptoms showed two significant correlations in the early time window
(Table 5). In both anterior and central regions during the early time
window, the more negative the difference wave was (and thus, the more
negative the Unpleasant ERP was relative to the Neutral ERP), the
greater the depressive symptoms were. While the correlation in the
central area did not survive FDR-corrections for multiple testing, the
correlation in the anterior window did (Fig. 3).
To partial out the variance related to the voltage change over time
within the anterior scalp area, a regression model was run with unpleasant-neutral LPP difference scores in each time window (Early,
Middle, Late). In line with the correlation analyses, only the amplitude
of the Early difference wave (β = −0.45, p = .006) was significantly
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International Journal of Psychophysiology 155 (2020) 78–86
M.A. McLean, et al.
Fig. 1. ERP responses to neutral (blue/solid lines), pleasant (green/dashed lines) and unpleasant (red/dotted lines) pictures for posterior, central and anterior
electrode sides. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2. Scalp distribution of neutral (A), pleasant (B) and unpleasant (C) LPP waveforms across early, middle and late time windows.
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M.A. McLean, et al.
Table 3
Correlations between LPP difference waves and internalizing problems.
Time-window
Pleasant – Neutral LPP
Unpleasant – Neutral LPP
Region
Region
Anterior
Early
Middle
Late
Central
Posterior
Anterior
Central
Posterior
r
p
r
p
r
p
r
p
r
p
r
p
−0.211
−0.241⁎a
−0.003
.054
.027
.977
−0.138
−0.179
0.022
.212
.103
.844
−0.024
0.046
0.115
.828
.680
.299
−0.163
−0.157
−0.012
.137
.155
.915
−0.191
−0.178
−0.037
.081
.106
.742
−0.114
−0.024
−0.001
.301
.827
.995
Note.
⁎
p < .05.
a
Correlation no longer significant after FDR-correction for multiple testing.
3.2. Anxiety and internalizing behaviors
Whalen et al., 2020), based on prior literature, or as is often the case,
where LPP difference waves are maximal. Considering our finding, it
may be important that in future research, central and anterior scalpregions, in addition to posterior regions, are also examined, even if
differences are not maximal in these regions. Finally, findings were
established in the early time window, suggesting this process of sustained engagement to emotional content of stimuli is likely automatic in
nature, in service of basic survival by motivational systems (Lang et al.,
1997).
Differences in the association between neural responses to affective
images and depression may exist, dependent upon developmental stage.
It is important to consider the possibility that both disengagement from
as well as sensitivity towards one's environment in the form of alterations to LPP responses to emotional stimuli, may be associated with the
development of depressive symptoms across childhood through adolescence. While we find evidence to support a tendency to attend to
negative stimuli as associated with depressive symptomatology from an
early age in our study, heterogeneity in the long-term function of this
neural correlate may be dependent upon early temperamental biases
(Kessel et al., 2017a), early life experiences (van den Heuvel et al.,
2018), parenting environment (Liu and Pérez-Edgar, 2018), and those
continually exposed to negative experiences (Kindt, 2001). It is also
possible that the LPP develops in conjunction with other dysregulation
processes such as neuroendocrine disruptions (Alomari et al., 2015;
Ursache and Blair, 2015). Given the dearth of longitudinal studies examining development of multiple neurophysiological dysregulated
processes in conjunction with environmental exposures within individuals, it is difficult to situate our findings within developmental
theoretical frameworks of cognitive biases and threat perception in atrisk and depressive populations. This is an exciting avenue for future
research.
We failed to find brain-behavior links between LPP amplitudes to
emotional stimuli and anxiety symptoms as well as internalizing behaviors. Findings of no association between LPP responses to pleasant
images and these behavioral outcomes, are in line with previous studies
in children (Kujawa et al., 2016; Solomon et al., 2012) and adults
(MacNamara et al., 2019; Weinberg et al., 2016). It is, however, surprising that we did not establish an association between LPP difference
waves for negative relative to neutral images, and preschool-age internalizing behaviors, nor anxiety symptoms given this is a consistent
finding in the literature across development (Auerbach et al., 2015;
Kujawa et al., 2016; Speed et al., 2016). Findings are also inconsistent
with research examining the nature of attentional biases (Fu and PérezEdgar, 2019; Liu and Pérez-Edgar, 2018), neurophysiological correlates
of anxiety symptoms (DeCicco et al., 2012; Kujawa et al., 2015), and
temperamental fearfulness (Kessel et al., 2017b; Solomon et al., 2012)
in anxiety and internalizing behaviors, which suggest that children
exert greater attentional resources towards negative stimuli. Still, as is
the case in our study, no associations between broad internalizing behaviors in relation to LPP difference waves have been established in
children aged 6–9 years (Dennis and Hajcak, 2009). Together with our
findings for depressive symptoms, it is clear that ongoing research is
needed to determine the utility and specificity of the LPP as a neural
marker of internalizing behaviors as well as clinical symptoms of anxiety and depressive symptoms across childhood.
3.3. Strengths, limitations and future research
There are multiple strengths of this study. Building on prior work
(van den Heuvel et al., 2018), we have examined LPP in relation to
pleasant, unpleasant and neutral stimuli, in a comparatively large cohort of children. Furthermore, in line with adult literature, we examined not only overall internalizing behaviors but the specific DSM-IV
Table 4
Correlations between LPP difference waves and the anxiety symptoms sub-scale.
Time-window
Pleasant – Neutral LPP
Unpleasant – Neutral LPP
Region
Region
Anterior
Early
Middle
Late
Central
Posterior
Anterior
Central
Posterior
r
p
r
p
r
p
r
p
r
p
r
p
−0.187
−0.216
0.098
.088
.048⁎a
.375
−0.137
−0.186
0.085
.215
.091
.440
−0.024
0.010
0.132
.826
.927
.231
−0.233
−0.187
0.035
.033⁎a
.089
.750
−0.212
−0.212
−0.038
.053
.053
.734
−0.107
−0.084
−0.045
.331
.445
.682
Note.
⁎
p < 0.05.
a
Correlation no longer significant after FDR-correction for multiple testing.
83
International Journal of Psychophysiology 155 (2020) 78–86
M.A. McLean, et al.
Table 5
Correlations between LPP difference waves and the affective (depressive) symptoms sub-scale.
Time-window
Pleasant – Neutral LPP
Unpleasant – Neutral LPP
Region
Region
Anterior
Early
Middle
Late
Central
r
p
−0.114
−0.032
0.134
.300
.772
.225
Posterior
Anterior
r
p
r
p
r
−0.119
−0.093
0.100
.281
.398
.364
0.000
0.113
0.166
.997
.306
.131
−0.277
−0.115
0.006
Central
p
⁎
.011
.299
.960
Posterior
r
−0.238
−0.151
0.000
⁎a
p
r
p
.029
.169
.997
−0.121
−0.003
0.024
.274
.982
.827
Note.
⁎
p < .05.
a
Correlation no longer significant after FDR-correction for multiple testing.
extend our findings. Our ability to determine relationships at clinical
levels of symptoms is limited, due to the largely non-clinical sample of
children and relatively small range in scores across CBCL subscales.
Finally, maternal report of child behavior and EEG assessments were
collected at the same age. Longitudinal studies collecting both EEG and
behavioral data (maternal report or objective assessment) at multiple
points across early childhood are warranted, in order to determine the
direction of effects. This work will also help determine the utility of the
LPP as a marker of internalizing behaviors across early childhood.
anxiety and affective disorder subscales. The use of a well validated and
widely used maternal report of behavior, enabled us to compare our
results to that of prior work in older children.
It is important to acknowledge limitations of the current study. In
line with prior work in this cohort (van den Heuvel et al., 2018), the
LPP amplitudes did not differ between affective and neutral pictures at
anterior and central recording sites at the group level; differences were
only established at the posterior recording sites. However, as shown in
the current paper, individual differences in LPP difference waves across
regions, are potentially useful markers of child behavior. Because we
used a validated picture set of scenes including negative, positive and
neutral stimuli, a potential limitation is the wide variety of unique
stimuli the children were presented with. The unpleasant stimuli included “fearful” as well as “sad” stimuli, and some pictures may
therefore represent a bias to “threat”, while others may be more saliently depicting “sad” stimuli. It is possible that sub-group analyses of
these scenes may yield different results given that anxiety symptoms
may be more strongly related to threat biases. We did not collect valence and arousal of stimuli information. Such information would have
assisted in validating the stimuli, in line with prior work in this field
(Dennis and Hajak , 2009). Future studies should look to replicate and
4. Conclusions
This study examined the value of the LPP in response to affective
images in young children as a neural marker for internalizing problem
behaviors. Our study demonstrated that greater early LPP responses to
negative images were associated with depressive symptoms in preschoolers. Overall, the predictive value of the LPP in young children is
likely not sufficient for clinical purposes. However, given our findings
differ to that of work in middle childhood and adolescents, our study
highlights the importance of examining the nature of neurophysiological markers of behavior across development. We therefore encourage
Fig. 3. Correlation between the Anterior Early LPP Unpleasant – Neutral ERP difference waves and affective (depressive) symptoms.
Note: the association was still significant when the extreme value on the CBCL affective problems was winzorized (r = −0.248, p = .023).
84
International Journal of Psychophysiology 155 (2020) 78–86
M.A. McLean, et al.
replication and extension of our study. Ultimately, research into
childhood neural markers for psychopathology can help improve longterm outcomes, through the improvement of diagnostic tools and development of novel mechanistic interventions that impact these neurophysiological correlates and behavioral processes.
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Funding sources
The PELS study is supported by the national funding agencies of the
European Science Foundation (EuroSTRESS - PELS - 99930AB6-0CAC423B-9527-7487B33085F3) participating in the Eurocores Program
EuroSTRESS programme, i.e., the Brain and Cognition Programme of
the Netherlands Organisation for Scientific Research (NWO) for the
Netherlands. BVdB is project leader of the PELS study. BVdB was financially supported by European Commission Seventh Framework
Programme (FP7—HEALTH. 2011.2.2.2-2 BRAINAGE, grant agreement
no: 279281). MvdH is supported by a Veni grant from the Dutch
Organization for Scientific Research (NWO; VI.Veni.191G.025).
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