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doi:10.1111/j.1469-7610.2009.02168.x
Department of Psychology, Hunter College, The City University of New York, USA; 2Department of Psychology, Stony
Brook University, Stony Brook, NY, USA
Background: The ability to modulate emotional responses, or emotion regulation, is a key mechanism in
the development of mood disruptions. Detection of a neural marker for emotion regulation thus has the
potential to inform early detection and intervention for mood problems. One such neural marker may be
the late positive potential (LPP), which is a scalp-recorded event-related potential reflecting facilitated
attention to emotional stimuli. In adults, the LPP is reduced following use of cognitive emotion regulation
strategies such as reappraisal. No studies to date have examined the LPP in relation to cognitive emotion
regulation in children, and whether the LPP is related to parent-report measures of emotion regulation and
mood disruptions. Methods: To examine this question, high-density electroencephalograph (EEG) was
recorded from 20 children (M age = 87.8 months, SD = 18.02; 10 girls) while they viewed unpleasant
emotional pictures following either a directed negative or neutral interpretation of the picture. Results: As predicted, the LPP was smaller following neutral versus negative interpretations at
posterior recording sites, except for younger girls (aged 56). The timing of this effect was later than that
reported in studies with adults. For all children, greater modulation of the LPP by neutral interpretations
was associated with reduced anxious-depressed symptoms, whereas larger LPPs for both interpretation
types were associated with greater mood symptoms and worse parent-reported emotion regulation. Conclusions: Results suggest that the LPP may represent a clinically relevant neural marker for
emotion regulation and mood disruptions. Keywords: Emotion regulation, EEG, biomarker, ERP, late
positive potential. Abbreviations: LPP: late positive potential; ERP: event-related potential.
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Method
Participants
Participants were twenty-five 5- to 10-year-old children
(12 male, 13 female). There were ten 5-to 6-year-olds,
six 7- to 8-year-olds, and four 9- to 10-year-olds. We
chose to include this age range because early school age
is a period marked by the cognitive and neural development needed to perform well under the attentional
processing demands imposed by the experimental task
(Casey et al., 2000). Data from 5 subjects (3 females)
were excluded due to movement artifacts leading to
poor quality EEG recording. The final sample of 20 was
comprised of 10 males (mean age = 85.60 months,
SD = 14.95) and 10 females (mean age = 90.00 months, SD = 21.24). All participants families were
paid $50 for their participation.
Stimulus materials
A total of 30 developmentally appropriate pictures were
selected from the International Affective Picture System
(IAPS; Lang, Bradley, & Cuthbert, 2005). These pictures
depicted unpleasant scenes (e.g., disaster scenes,
frightening animals).1
The task was administered on a Pentium D class
computer, using Presentation software (Neurobehavioral Systems, Inc., Albany, CA) to control the presentation and timing of all stimuli. Each picture was
displayed in color and occupied the entirety of a 19-in
(48.26 cm) monitor. At a viewing distance of approximately 24 in (60.96 cm), each picture occupied
approximately 40 of visual angle horizontally and
vertically.
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Anterior
Fpz
Fp1
AF7
F7
FT7
Left
T7
ActiveTwo BioSemi system (BioSemi, Amsterdam, Netherlands). Recordings were taken from 64 scalp electrodes
based on the 10/20 system, as well as two electrodes
placed on the left and right mastoids. The electrooculogram (EOG) generated from blinks and eye movements
was recorded from four facial electrodes: two approximately 1 cm above and below the subjects left eye, one
approximately 1 cm to the left of the left eye, and one
approximately 1 cm to the right of the right eye. As per
BioSemis design, the ground electrode during acquisition was formed by the Common Mode Sense active
electrode and the Driven Right Leg passive electrode.
EEG and EOG signals were sampled at 512 Hz. All
data were re-referenced off-line to an average mastoid
reference and filtered with a high pass frequency of
.2 Hz and a low pass frequency of 30 Hz. The EEG was
segmented for each trial, beginning 500 ms before each
picture onset and continuing for 2500 ms. The raw EEG
epochs were passed through a computerized artifact
scan batch to correct artifacts using Brain Electrical
Source Analysis version 5.1 (BESA; MEGIS Software
GmbH, Munich, Germany). After artifact correction,
trials that still included EEG or EOG activity with a
voltage step of more than 50 lV between sampling
points, or trials with voltages remaining above 100 lV,
were excluded from further analysis.
ERPs were constructed by separately averaging the
two interpretation types (negative, neutral). For each
ERP average, the mean amplitude in the 500 ms window prior to picture onset served as the baseline. For
analyses of the LPP, the spatial dimensions of the data
set were reduced by creating eight clusters of electrodes
with five electrodes in each. There were three two-level
regional clusters: left versus right hemisphere, anterior
versus posterior, and inferior versus superior (Dien &
Santuzzi, 2005). The left/right anterior-superior clusters included electrodes AF3/4, F1/2, F3/4, FC1/2,
and FC3/4; the left/right anterior-inferior clusters were
defined by electrodes AF7/8, F5/6, F7/8, FC5/6, and
FT7/8; the left/right posterior-superior clusters
included CP1/2, CP3/4, P1/2, P3/4, and PO3/4; the
left/right posterior-inferior clusters included CP5/6,
P5/6, P7/8, PO7/8, and TP7/8. Figure 1 shows the
electrode positions. Based on visual inspection, the LPP
was defined as the mean amplitude in three time windows following stimulus onset for the picture after the
directed interpretation: 300600 ms (early window),
6001000 ms (middle window) and 10002000 ms (late
AF3
F5
F3
F1
Fz
AF8
AF4
AFz
F8
F6
F4
F2
FT8
FC5
FC3
FC1
FCz
FC2
FC4
FC6
C5
C3
C1
Cz
C2
C4
C6
CP5
CP3
CP1
CPz
CP2
CP4
CP6
TP7
P7
Psychophysiological recording and data reduction. EEG was continuously recorded using the
Fp2
P5
P9
PO7
P3
PO3
O1
P1
Pz
CMS
POz
Oz
P2
DRL
P4
PO4
P6
T8
Right
TP8
P8
P10
PO8
O2
Iz
Maternal report of child emotion regulation. Mothers completed the Emotion Regulation
Checklist (Shields & Cicchetti, 1998). This 24-item
questionnaire concerns childrens reactions to emotional challenges and regulation of a wide range of
emotions. Two subscales were calculated based on
measure developers guidelines, which have been
shown to converge with other measures of emotion
regulation (Shields & Cicchetti, 1998): emotion dysregulation (a = .70), which was comprised of items
including is prone to angry outbursts/tantrums easily
and exhibits wide mood swings; and positive regulation
(a = .60), comprised of items including can say when s/
he is feeling sad, angry or mad, fearful or afraid. Items
were rated on a 14 scale.
Results
The late positive potential (LPP)
Figure 2 presents the stimulus-locked LPPs at
anterior and posterior electrode clusters (the mean
amplitude of the 5 electrodes included in each
cluster).
Children were divided into younger and older
groups based on a median split. There were 10
younger children (aged 56) and 10 older children
(aged 710). There were 5 boys and 5 girls in each
age group. A 2 (Child Gender) 2 (Child Age) 2 (Left
HemisphereRight Hemisphere) 2 (Anterior-Pos-
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Figure 2 Stimulus-locked ERPs elicited by unpleasant pictures after negative or neutral interpretations at anteriorsuperior and anterior-inferior electrode clusters (top half of figure), and at posterior-superior and posterior-inferior
electrode clusters (bottom half of the figure). Stimulus-onset occurred at 0 ms
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
1378
Online Appendix B shows the scalp distribution of the negative minus neutral interpretation difference waveforms for
boys (top) and girls (bottom) in the time window of the early
LPP, middle LPP, and late LPP (from left to right).
Late window (1000 to 2000 ms). In the late window, the LPP was largest at anterior recording sites
(Anterior-Posterior F(1,16) = 29.45, p < .001, partial
g2 = .65), particularly in right superior versus left
superior
sensors
(Anterior-Posterior InferiorSuperior Hemisphere F(1,16) = 6.21, p < .05, partial g2 = .28; all post-hoc tests p < .05). Other main
effects and interactions did not reach significance.
Thus, by the late window, the LPP was maximal at
right superior-anterior sensors but was not sensitive
to interpretation type.
Maternal report of child affective individual
differences
Table 1 reports mean scores for child internalizing
and externalizing problems, specific mood symptoms
(withdrawn, anxious-depressed, and somatic complaints), and emotion regulation (positive regulation
and dysregulation). Because boys consistently
showed the expected modulation of the LPP via
reappraisal (in the middle window), we examined
whether boys and girls differed in terms of maternal
report of child mood problems and emotion regulation. No significant gender differences emerged.
Table 1 Descriptive statistics for mood disruptions and emotion regulation variables
Internalizing
Externalizing
Anxious-depressed
Withdrawn
Somatic complaints
Positive regulation
Dysregulation
SD
Range
46.80
50.75
52.60
51.95
54.45
3.29
2.12
10.71
12.75
3.46
5.03
6.56
.47
.54
2965
2869
5062
5070
5070
24
1.133.13
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Discussion
This was the first study to demonstrate that a cognitive emotion regulation strategy modulated the LPP
in children. Specifically, the LPP to unpleasant pictures was decreased when unpleasant pictures were
described in a more neutral versus negative manner.
This effect was significant in the middle window for
all children except younger girls (aged 56). In
addition, the amplitude of the LPP following directed
interpretations was associated with child emotional
well-being: larger amplitudes were correlated with
increased symptoms of anxiety, depression, somatic
complaints, and withdrawal, and greater signs of
emotion dysregulation. Taken together, results suggest that the LPP during cognitive emotion regulation
may be a clinically relevant biomarker for emotional
reactivity and regulation capacities related to mood
disruptions. In addition, although this studys small
sample size limited our ability to explore the effects
of gender and age and requires that we interpret
findings with caution, the LPP may be sensitive to
gender and age differences in the development and
pathophysiology of reactivity, regulation, and mood
problems. The goal of this study was to provide a
preliminary examination of the LPP as a new biomarker for emotion regulation in children. Future
research should examine links between the LPP and
Table 2 Correlations between mean LPP amplitudes and maternal report of child mood disruptions and emotion regulation
Child mood disruptions and emotion regulation
LPP
Early window
Neutral interpretation
Negative interpretation
Negative Neutral
Middle window
Neutral interpretation
Negative interpretation
Negative Neutral
Late window
Neutral interpretation
Negative interpretation
Negative Neutral
Internalizing
problems
Externalizing
problems
Anxious/
depressed
Somatic
complaints
Withdrawn/
depressed
Positive
regulation
Dysregulation
.28
.06
).37
.25
.13
).23
.49*
.20
).52*
.05
).09
).20
).08
).05
.06
.18
.19
).05
.08
.02
).09
.14
).13
).21
.11
.28
.15
.30
).16
).35
.04
).31
).29
).05
.27
.25
.12
).44*
).44*
.23
.54*
.28
.39
.46*
.04
.22
.21
).02
.24
.12
).10
.11
.55*
.35
.48*
.26
).19
).07
).15
).06
.15
.14
.)02
*p < .05.
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
1380
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Supplementary material
The following supplementary material is available for
this article:
Appendix A. Negative and neutral interpretations
for each picture (Word document)
Appendix B. Scalp distribution of the negative
minus neutral interpretation difference waveforms
(Word document)
This material is available as part of the online
article from:
http://www.blackwell-synergy.com/doi/abs/
10.1111/j.1469-7610.2009.02168.x
Please note: Blackwell Publishing are not responsible for the content or functionality of any supplementary materials supplied by the authors. Any
queries (other than missing material) should be
directed to the corresponding author for the article.
Acknowledgements
This research was supported by National Institutes
of Health (NIH) Grants 5T34 GM007823, 5K01
MH075764-02, and 5S06GM060654-04, the latter
two awarded to T.D. This publication was also made
possible by Grant RR03037 from the National Center
for Research Resources (NCRR), a component of the
NIH.
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Correspondence to
Tracy A. Dennis, Department of Psychology, Hunter
College, CUNY, New York, NY 10065, USA; Tel: (212)
Key points
It is known that the late positive potential (LPP) is enhanced when viewing emotionally arousing stimuli
and reduced when adults use cognitive emotion regulation strategies, such as reappraisal.
The current study is the first to document in children that manipulating the meaning of unpleasant
stimuli via reappraisal reduces the LPP to those unpleasant stimuli.
The current study is also the first to show that the degree to which the LPP is sensitive to reappraisal is
related to individual differences in emotion dysregulation, mood problems, and internalizing problems.
Clinical implications include the use of the LPP as a biomarker for affective risk, which might inform early
detection and intervention.
References
Achenbach, T.M., & Maruish, M.E. (1999). The Child
Behavior Checklist and related instruments. In M.E.
Maruish (Ed.), The use of psychological testing for
treatment planning and outcomes assessment (2nd
edn, pp. 429466). Mahwah, NJ: Lawrence Erlbaum
Associates.
Banaschewski, T., & Brandeis, D. (2007). Annotation:
What electrical brain activity tells us about brain
function that other techniques cannot tell us a child
psychiatric perspective. Journal of Child Psychology
and Psychiatry, 48, 415435.
Bishop, S., Duncan, J., Brett, M., & Lawrence, A.D.
(2004). Prefrontal cortical function and anxiety: Controlling attention to threat-related stimuli. Nature
Neuroscience, 7, 184188.
Brooks-Gunn, J., & Warren, M.P. (1989). Biological and
social contributions to negative affect in young
adolescent girls. Child Development, 60, 4055.
Casey, B.J., Giedd, J.N., & Thomas, K.M. (2000).
Structural and functional brain development and its
relation to cognitive development. Biological Psychology, 54, 241257.
Cole, P.M., Martin, S.E., & Dennis, T.A. (2004).
Emotion regulation as a scientific construct:
Methodological challenges and directions for child
development research. Child Development, 75, 317
333.
Compton, R.J. (2003). The interface between emotion
and attention: A review of evidence from psychology
and neuroscience. Behavioral and Cognitive Neuroscience Reviews, 2, 115129.
Cuthbert, B.N., Schupp, H.T., Bradley, M.M., Birbaumer, N., & Lang, P.J. (2000). Brain potentials in
affective picture processing: Covariation with autonomic arousal and affective report. Biological Psychology, 52, 95111.
Davidson, R.J., Pizzagalli, D., Nitschke, J.B., & Putnam, K. (2002). Depression: Perspectives from affective neuroscience. Annual Review of Psychology, 53,
545574.
Derryberry, D., & Reed, M.A. (2002). Anxiety-related
attentional biases and their regulation by attentional
control. Journal of Abnormal Psychology, 111, 225
236.
Hall, G.B.C., Witelson, S.F., Szechtman, H., & Nahmias, C. (2004). Sex differences in functional activation patterns revealed by increased emotion
processing demands. Neuroreport, 15, 219223.
Hare, T.A., Tottenham, N., Galvan, A., Voss, H.U.,
Glover, G.H., & Casey, B.J. (2008). Biological substrates of emotional reactivity and regulation in
adolescence during an emotional gonogo task. Biological Psychiatry, 63, 927934.
Kalisch, R., Wiech, K., Herrmann, K., & Dolan, R.J.
(2006). Neural correlates of self-distraction from
anxiety and a process model of cognitive emotion
regulation. Journal of Cognitive Neuroscience, 18,
12661276.
Kieras, D.E., Meyer, D.E., Ballas, J.A., Lauber, E.J.,
Braver, T.S., Cohen, J.D., et al. (2000). VII: Computational modeling of control. In S. Monsell, & J. Driver
(Eds.), Control of cognitive processes: Attention and
performance XVIII (pp. 679751). Cambridge, MA: The
MIT Press.
Ladouceur, C.D., Dahl, R.E., & Carter, C.S. (2007).
Development of action monitoring through adolescence into adulthood: ERP and source localization.
Developmental Science, 10, 874891.
Lang, P.J., Bradley, M.M., & Cuthbert, B.N. (2005).
International Affective Picture System (IAPS): Affective
ratings of pictures and instruction manual. Gainesville, FL: University of Florida.
Levesque, J., Joanette, Y., Mensour, B., Beaudoin, G.,
Leroux, J.M., Bourgouin, P., et al. (2004). Neural
basis of emotional self-regulation in childhood.
Neuroscience, 129, 361369.
Lewis, M.D., Lamm, C., Segalowitz, S.J., Stieben, J., &
Zelazo, P.D. (2006). Neurophysiological correlates of
emotion regulation in children and adolescents.
Journal of Cognitive Neuroscience, 18, 430443.
Lewis, M.D., Todd, R.M., & Honsberger, M.J.M. (2007).
Event-related potential measures of emotion regulation in early childhood. Neuroreport: For Rapid
Communication of Neuroscience Research, 18, 6165.
Miltner, W.H.R., Trippe, R.H., Krieschel, S., Gutberlet,
I., Hecht, H., & Weiss, T. (2005). Event-related brain
potentials and affective responses to threat in spider/
snake-phobic and non-phobic subjects. International
Journal of Psychophysiology, 57, 4352.
Moser, J.S., Hajcak, G., Bukay, E., & Simons, R.F.
(2006). Intentional modulation of emotional responding to unpleasant pictures: An ERP study. Psychophysiology, 43, 292296.
Ochsner, K.N., Bunge, S.A., Gross, J.J., & Gabrieli,
J.D.E. (2002). Rethinking feelings: An fMRI study of
1383