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Child Development, November/December 2013, Volume 84, Number 6, Pages 19541966

Inhibitory Control During Emotional Distraction Across Adolescence and


Early Adulthood
Julia E. Cohen-Gilbert and Kathleen M. Thomas
University of Minnesota

This study investigated the changing relation between emotion and inhibitory control during adolescence. One
hundred participants between 11 and 25 years of age performed a go-nogo task in which task-relevant stimuli
(letters) were presented at the center of large task-irrelevant images depicting negative, positive, or neutral scenes
selected from the International Affective Picture System. Longer reaction times for negative trials were found
across all age groups, suggesting that negative but not positive emotional images captured attention across this
age range. However, age differences in accuracy on inhibitory trials suggest that response inhibition is more
readily disrupted by negative emotional distraction in early adolescence relative to late childhood, late adoles-
cence, or early adulthood.

Social and cognitive demands change dramatically (Adleman et al., 2002; Huizinga, Dolan, & van der
during adolescence as individuals become indepen- Molen, 2006; Marsh et al., 2006), and go-nogo tasks
dent from their caregivers and move into a highly (Eigsti et al., 2006; Hooper, Luciana, Conklin, &
nuanced social context dominated by peers. During Yarger, 2004). In parallel with these increases in
these transitional years, adolescents increasingly inhibitory capacity, neuroimaging data show contin-
must learn to self-regulate and to make decisions in ued development across adolescence in frontal brain
the absence of adult supervision. This task is made circuits critical to successful cognitive control (Casey,
more difcult by motivational and affective changes Jones, & Hare, 2008; Durston et al., 2006; Giedd et al.,
that begin early in the second decade of life (Arnett, 1999; Gogtay et al., 2004; Luna, Padmanabhan, &
1999; Dahl, 2001; Romeo, 2003; Spear, 2000; Steinberg OHearn, 2010; Sowell, Thompson, Holmes, Jernigan,
et al., 2006). During this same period, the regulatory & Toga, 1999; Sowell, Trauner, Gamst, & Jernigan,
cognitive capacities necessary for overriding intense 2002; Toga, Thompson, & Sowell, 2006). The rela-
emotions and desires develop slowly, not reaching tively late consolidation of such neural circuits may
adult levels until a decade or so after affective contribute to poor impulse regulation in adolescence.
changes begin (Spear, 2000). The gap between the This lack of effective inhibitory control, in turn, can
onset of emotional changes and the full maturation lead to dangerous risk-taking behaviors commonly
of inhibitory control may contribute to a window of observed in adolescence, such as drunk driving,
risk for emotional dysregulation and potentially illicit drug use, and unprotected sex. Thus, a better
deleterious impulsive actions in early adolescence. understanding of inhibitory control during adoles-
Inhibitory control is a critical executive skill that cence and the factors that contribute to its disruption
allows individuals to withhold maladaptive impul- is of considerable value to public health.
sive responses in favor of successful goal-directed In addition to limited impulse control, many
behavior. Performance on a variety of tasks requiring adolescents contend with heightened emotional
response inhibition has been found to improve intensity and volatility (Arnett, 1999; Buchanan,
steadily throughout adolescence including anti- Eccles, & Becker, 1992; Petersen et al., 1993; Stein-
saccade tasks (Luna & Sweeney, 2004), Stroop tasks berg et al., 2006). Adolescents, relative to other age
groups, report increased mood variability, increased
This study was supported by the Center for Neurobehavioral self-consciousness, reduced positive affect, and
Development (NIH T32 MH73129) and the Center for Cognitive increased duration and potency of negative
Sciences (NIH T32 HD007151) at the University of Minnesota. emotions (Larson & Ham, 1993; Petersen et al.,
The authors thank Christina Shoaf, Daniel Rinker, and Tim Hop-
penrath for assistance with data collection, and Marisa Silveri,
Jennifer Wenner, and Ruskin Hunt for editorial comments.
Correspondence concerning this article should be addressed to 2013 The Authors
Julia E. Cohen-Gilbert, McLean Imaging Center, McLean Hospi- Child Development 2013 Society for Research in Child Development, Inc.
tal, 115 Mill Street, Mail Stop 204, Belmont, MA 02478. Electronic All rights reserved. 0009-3920/2013/8406-0012
mail may be sent to jcohen@mclean.harvard.edu. DOI: 10.1111/cdev.12085
Inhibitory Control During Emotional Distraction 1955

1993). In fact, studies employing self-report scales reduction in impulsive errors with age on neutral
have found as many as 20%50% of adolescents cues while adolescents showed proportionally
meeting conventional adult criteria for clinically signif- higher impulsive errors on positive trials relative to
icant depression (Kessler, Avenevoli, & Merikangas, both children and adults (Somerville, Hare, &
2001; Petersen et al., 1993). Though interview-based Casey, 2011). Results from neuroimaging studies
studies report more modest rates of adolescent have also suggested developmental changes in the
depression (Kessler & Walters, 1998), adolescence is impact of emotion on cognitive control during ado-
unquestionably a period of elevated risk for the lescence. These ndings include increased activation
onset of mood disorders and other forms of psycho- of emotion-processing limbic areas in adolescents
pathology. Many of these disorders, including relative to other age groups in response to fearful
depression, social anxiety, eating disorders, and sub- faces, both during a go-nogo task (Hare et al., 2008)
stance abuse, feature altered emotional responding and during passive viewing (Monk et al., 2003).
and insufcient or maladaptive emotion regulation Increased activity in regulatory regions in the same
as key symptoms. age group has been observed when the task
Gender differences in psychopathology also required ignoring emotional aspects of the stimulus
emerge during the early teen years (Angold, Costel- (Monk et al., 2003). Elevation in an ERP index of
lo, & Worthman, 1998; Kessler et al., 2001). Among inhibitory demands (the N2 component) has been
the most salient changes is the shift from equal found in adolescents but not children in response to
incidence of depression in girls and boys during a negative emotion induction during performance
late childhood to a much higher prevalence of of a go-nogo task (Lewis, Lamm, Segalowitz,
depression in adolescent girls relative to their male Stieben, & Zelazo, 2006). Together, these behavioral
peers (Angold, Erkanli, Silberg, Eaves, & Costello, and imaging studies suggest heightened sensitivity
2002). Male adolescents, however, are more likely to emotional information during performance of
than females to show increased severity of conduct inhibitory control tasks during adolescence relative
problems during adolescence and are more likely to to other ages. However, the majority of these tasks
engage in criminal activity such as vandalism and require participants to identify facial expressions of
petty theft (Steinberg et al., 2006). Thus, it remains emotion, an ability that may also change across
clear that the emotional changes that occur during adolescence (McGivern, Andersen, Byrd, Mutter, &
adolescence are not equivalent for both genders. Reilly, 2002; Thomas et al., 2001), making it difcult
The timing and gender disparities of these emo- to distinguish between the disruption of inhibitory
tional changes suggest a role for pubertal hormones control by the presence of emotional content and
and their effects on both body and brain. However, developmental changes in the identication and
among both healthy and disordered populations, interpretation of facial expressions. Furthermore,
only a small portion of the variability in adolescent most existing studies on the interaction of emotion
emotional experience can be accounted for by and inhibitory control in adolescence have not
hormonal changes (Brooks-Gunn, Garber, & Paikoff, examined potential differences in effects of emo-
1994; Brooks-Gunn & Warren, 1989) and the etiol- tional stimuli at multiple age points within adoles-
ogy of adolescent mood changes continues to be cence, a far from homogeneous developmental
the source of much speculation. Further variability period.
may be due to cognitive and neurological develop- This study aims to further characterize the
ment during this period. changing interface between inhibitory control and
Emotions must frequently be regulated cogni- emotion during normative adolescent development.
tively to permit adaptive behavior, such as when Specically, we examine potential differences in the
anger must be controlled or temptation avoided. To impact of task-irrelevant emotional background
date, only a few studies have attempted to measure images on inhibitory control in a go-nogo task in
the impact of emotion on inhibitory control in multiple age groups across adolescence and into
healthy adolescents. Studies using facial expressions early adulthood. By subdividing adolescence into
of emotion as stimuli in a go-nogo task have found multiple age groups, we aimed to discern whether
slower responding to fear faces in adolescents com- go-nogo performance was more disrupted by dis-
pared to adults (Hare et al., 2008), as well as steady tracting emotional content during the early adoles-
improvements in both emotion discrimination and cent period during which many emotional changes
inhibitory control in the presence of emotional stim- occur. Alternately, the disruptive quality of the
uli across adolescence (Tottenham, Hare, & Casey, images could decrease gradually between childhood
2011). A similar go-nogo study reported a linear and adulthood as inhibitory control matures. We
1956 Cohen-Gilbert and Thomas

hypothesized that the presence of emotional images obsessivecompulsive symptoms, interpersonal sensi-
(negative or positive) compared to nonemotional tivity, depression, anxiety, hostility, phobic anxiety,
images (neutral or scrambled) would disrupt per- paranoid ideation, and psychoticism, whereas the
formance to some extent in all age groups. We CBCL and YSR include measures of depression,
further predicted that this disruption would be somatic complaints, social problems, thought prob-
largest in the 13- to 14-year-old group, for whom lems, attention problems, rule-breaking behavior, and
emotional changes were underway and regulatory aggressive behavior. Participants who scored within
systems were still far from mature. We also the clinical range, as dened by available norms on
expected that the disruptive effect of emotional each measure, on any subscale of these question-
information may differ for males and females naires were removed from subsequent data analy-
within the early to mid-adolescent age groups, ses and replaced with new participants to produce
given the marked gender differences in emotional the nal sample of 100. Due to this secondary
development during adolescence. Such results screening, an additional 3 males were tested in the
would support the idea that the disruption of cog- 11- to 12-year-old group, 2 males and 1 female in
nitive control systems by emotional input may be the 13- to 14-year-old group, 1 male and 2 females
elevated in early adolescence relative to other ages in the 15- to 16-year-old group, 2 males and 2
and that this disruption may arise from an inter- females in the 18- to 19-year-old group, and 1 male
action between gradually maturing regulatory cog- and 2 females in the 20- to 25-year-old group. No
nitive systems and changes in emotional reactivity. participants were excluded based on task perfor-
mance. All recruitment and experimental proce-
dures were approved by the Institutional Review
Method Board of the University of Minnesota.
Participants
Behavioral Task
One hundred participants were included in the
sample: 20 participants (10 males) in each of ve age The behavioral paradigm combined an inhibitory
groups: 1112 years (Mage = 11.49), 1314 years (Mage control task (the go-nogo) with negative, positive,
= 13.98), 1516 years (Mage = 16.15), 1819 years (Mage and neutral images selected from the International
= 19.15), and 2025 years (Mage = 21.91). Young adult Affective Picture System (IAPS; Lang, Bradley, &
participants were recruited from the undergraduate Cuthbert, 2008). In this task, letters were presented
population of the University of Minnesota and sequentially in a small box at the center of the com-
received either payment or points toward class puter screen, while IAPS images were displayed in
credit as compensation for their time and effort. the background. Participants were instructed to
Adolescents were recruited through the Institute of ignore the emotional images and respond as quickly
Child Development at the University of Minnesota as possible with a button press to every one of the
from a list of local families who had expressed letters, except for a specic nogo stimulus: an X. The
interest in research opportunities for their children. letters used included P, H, R, S, T, and X. The Xs
The recruited sample was approximately 90% Cau- appeared on 25% of total trials such that participants
casian, 6% Asian, 3% African American, and 1% acquired a prepotent tendency to press and needed
Other. Adolescents were paid for their participation to actively inhibit their responses during nogo trials.
and parents were compensated for travel expenses. The task required sustained vigilance as well as con-
All participants were prescreened for previously scious control of a potentiated behavior.
diagnosed neurological and psychological dis- The IAPS is a collection of images selected to
orders, substance abuse or dependence, serious span a wide range of content. Each of these images
medical issues, and learning disabilities. While at has been rated by a large sample of adults using a
the lab, participants completed a series of standard- scale from 1 to 9 for each of two emotional dimen-
ized questionnaires that probed anxiety levels sions: arousal, ranging from not arousing (1) to
(State-Trait Anxiety Inventory [STAI] or STAIChild highly arousing (9), and valence, ranging from
[STAIC]), attention skills (Conners Adult ADHD unpleasant or negative (1) to pleasant or positive (9).
Rating Scales [CAARS] or Conners Parent Rating Normative ratings of the entire IAPS stimulus set
Scale), and general functioning (Symptom Checklist are not available for adolescents, though work with
90 [SCL90] or Achenbach Child Behavior Check- a subset of these images has suggested that subjec-
list [CBCL] and Youth Self-Report [YSR]). The tive ratings are not signicantly different between
SCL90 includes subscales measuring somatization, adult and adolescent age groups (McManis, Bradley,
Inhibitory Control During Emotional Distraction 1957

Berg, Cuthbert, & Lang, 2001). These images were


used as backgrounds for the go-nogo letter stimuli.
Images were selected to be appropriate for young
adolescents. Thus, the most arousing images (erot-
ica, mutilation images, and some violent scenes)
were removed from the set. From the remaining
images, we selected 120 different images with
highly positive valence ratings (average valence rat-
ing = 7.32, average arousal rating = 4.94), 120
images with highly negative valence ratings (aver-
age valence rating = 3.12, average arousal rat-
ing = 5.32), and 120 images that were as close to
the neutral rating as possible (average valence rat-
ing = 5.25, average arousal rating = 3.35). Due to
the naturally arousing nature of emotional stimuli
and restrictions on what content was considered Figure 1. Sample trials of the emotional go-nogo. Task-relevant
appropriate for our age groups of interest, it was letters were presented in a small box at the center of a back-
not possible to equate the three image groups in ground image selected from the International Affective Picture
System. Images were positive, negative, or neutral (positive
terms of arousal ratings. To create an emotionally
examples pictured here). Scrambled versions of these images
neutral control condition that did not include any were used as backgrounds in control blocks.
potentially distracting object information or valence,
each of the selected IAPS images was scrambled
using a 32 9 32 grid. The resulting images were
and 5, the background images were scrambled
visually complex but had no discernible object
images derived from the IAPS stimulus set. These
content.
scrambled runs were used to examine possible age
The task was presented using E-Prime (Psychol-
differences in practice and fatigue effects in the
ogy Software Tools Inc., Sharpsburg, PA) on a
absence of emotional background content. Through-
21-in. monitor. Participants were seated comfortably
out Runs 2, 3, and 4, backgrounds were
at a viewing distance of approximately 32 in. Back-
nonscrambled IAPS images. Because emotional
ground stimuli covered the entire screen. Trials
responding to any single image is likely to be
began with presentation of a white xation cross on
highly variable between individuals (e.g., some
a gray background for 500 ms. The xation screen
people like snakes while others fear them), the
was followed by an IAPS image presented alone for
images were grouped into blocks of 20 unique
350 ms before a small white box (0.4 in. 9 0.4 in.)
images each depicting the same valence: positive,
containing a black letter appeared in the center of
negative, or neutral. This ensured that across the
the screen. Both letter and background image
entire block, all participants were reasonably likely
remained on the screen for an additional 650 ms,
to respond in the expected valence direction and
completing the trial (see Figure 1). Images were
experience the intended emotional state. Within the
presented alone, prior to presentation of the letter
20-trial valence block, the order of image presenta-
stimulus to make it more difcult for participants
tion was randomized. Within each run of 120 trials,
to ignore picture content. Participants were
two blocks of each of the three valences was pre-
instructed to respond as quickly as possible by
sented. The order of valence blocks was counterbal-
pressing the space bar if the letter presented was
anced across participants. To reduce habituation to
any letter other than X (go trial). If the letter was
the background images, each IAPS image was pre-
an X, they were required to withhold their response
sented only once during the task.
(nogo trial). Responses (press or no press) and reac-
tion times were recorded by the computer.
Pubertal Status Measure
Participants completed the task in ve runs of
120 trials. Participants were given breaks to rest Participants were asked to complete the Petersen
their eyes after each run. In all ve runs, letter Pubertal Development Scale (Petersen, Crockett,
stimuli were presented in random order with the Richards, & Boxer, 1988), a self-report scale for
restriction that ve Xs occurred within each set of pubertal status. This questionnaire consists of ve
20 trials. Beyond this, there was no restriction on questions about specic puberty-related physical
how many Xs could appear in a row. In Runs 1 changes (e.g., growth spurt, body hair, skin
1958 Cohen-Gilbert and Thomas

changes). Each question was answered on a four- g2 = .108. No other signicant effects were found.
level ordinal response scale with the exception of a Follow-up contrasts between each age group (10
question about menstruation for girls, which is nec- contrasts, a = .005) revealed a no signicant differ-
essarily dichotomous (scored as either 1 or 4). This ences. However, given a signicant main effect of
scale was not completed by participants over age on practice or fatigue, this measure was entered
18 years of age. as a covariate in subsequent analyses.
The inuence of age, gender, and distracting
emotional information on nogo accuracy was exam-
Data Analysis
ined using a 5 (age group) 9 2 (gender) 9 4 (back-
Reaction time and response accuracy data for ground) mixed model analysis of covariance
both go and nogo trials were recorded for each (ANCOVA) with fatigue entered as a covariate. The
participant in all ve runs of the task. Accuracy on ANCOVA revealed main effects of background,
inhibitory (nogo) trials was used as our primary F(3, 267) = 15.85, p < .001, g2 = .151, and age
measure of inhibitory control. Successful discrimi- group, F(4, 89) = 18.90, p < .001, g2 = .459. Results
nation between go and nogo targets was measured also showed a signicant Background 9 Age
using d-prime, computed by subtracting the z-trans- Group interaction, F(12, 267) = 2.36, p = .007,
formed false alarm rate from the z-transformed hit g2 = .096, as well as a three-way Background 9
rate: d = z(H) z(F). Reaction times on correct go Age Group 9 Gender interaction, F(12, 267) = 1.82,
trials were analyzed as an index of attention cap- p = .045, g2 = .076. Nogo trial accuracy for
ture by the background image. Each measure was each age group and background is presented in
analyzed via mixed model analyses of variance Figure 2a and Table 1.
(ANOVAs) including age group (1112, 1314, 15 To further explore the three-way interaction
16, 1819, 2025 years) as a between-subject factor effect, a 2 (gender) 9 4 (background), mixed model
and trial background type (negative, positive, neu- ANOVA was performed for each of the ve age
tral, scrambled) as a within-subject factor. Green- groups (a = .01). These separate ANOVAs showed
house-Geisser corrections were used in cases where no main effects of gender, but found a main effect
Mauchlys test indicted a violation of the assump- of background in the 13- to 14-year-old, F(3,
tion of sphericity. Signicant effects revealed by the 51) = 14.59, p < .001, g2 = .462, and 15- to 16-year-
ANOVAs were followed up with post hoc tests that old, F(3, 51) = 4.63, p = .006, g2 = .214, age groups.
were Bonferroni corrected to account for multiple No signicant effect of background was found in
comparisons. For comparison with other back- the 11- to 12-, 18- to 19-, or 20- to 25-year-old age
ground conditions, performance on scrambled trials
was computed by averaging performance in runs
100
one and ve. Practice or fatigue was measured by a) b)
*
90
subtracting performance on run ve from perfor- *
Accuracy (%)

80
mance on Run 1 for each outcome measure. Negative

Relations between age, pubertal scores, and 70 Positive


Neutral
task performance were also examined via hierarchi- 60
Scrambled
cal linear regression. Relations between clinical 50

questionnaire measures and performance were also 40


11-12 13-14 15-16 18-19 20-25 Female Male
explored via linear regression. Assumptions of (Ages 15-16 only)
Age Group
normality, linearity, and equality of variance were
met in all cases. Figure 2. Accuracy on nogo trials. (a) Accuracy for all age
groups and background types. Accuracy was signicantly worse
on negative trials versus all three other trial types in the 13- to
14-year-old age group. No signicant main effects of emotion
Results
were found in the 11- to 12-, 18- to 19-, or 20- to 25-year-old age
Effects of Age and Gender on Inhibitory Control groups. (b) Accuracy on nogo trials for females and males in the
15- to 16-year-old age group. This age group showed both a sig-
Effects of fatigue or practice on nogo trial nicant main effect of emotion and a Gender 9 Emotion interac-
accuracy were examined via a 5 (age group) 9 2 tion. Females performed signicantly worse on negative trials
relative to scrambled and neutral trials. Males in this age group
(gender) ANOVA. Practice or fatigue was measured
showed no signicant differences in nogo accuracy based on trial
by subtracting nogo accuracy on Run 5 from nogo background. No other age groups showed a signicant overall
accuracy on Run 1 for each subject. Results revealed effect of background. Error bars show standard error.
a main effect of age group, F(4, 90) = 2.74, p = .034, *p < .01.
Inhibitory Control During Emotional Distraction 1959

Table 1 g2 = .086. A strong trend was seen for a three-way,


Accuracy (%) on Nogo Trials for All Age Groups and Backgrounds: Background 9 Age Group 9 Gender interaction,
Mean (Standard Deviation) F(12, 270) = 1.78, p = .052, g2 = .073, but this effect
Age group Negative Positive Neutral Scrambled did not reach signicance. D-prime values for all age
groups and backgrounds are presented in Figure 3
1112 52.9 (17.7) 56.3 (19.0) 60.1 (15.4) 63.8 (15.0) and Table 2.
1314 64.3 (13.6) 74.8 (10.8) 73.8 (11.5) 77.3 0(9.7) The Background 9 Gender interaction was fol-
1516 75.8 (14.1) 81.2 (11.9) 81.5 (10.9) 79.4 0(9.5) lowed up using two repeated measures ANOVAs,
1819 80.8 (14.7) 83.1 (11.7) 83.1 (10.2) 83.5 0(9.6) one for each gender, with background as a between-
2025 87.7 0(9.6) 88.4 (12.3) 89.5 0(5.6) 89.5 0(9.0)
subject variable. Results showed highly signicant
effects of background in both gender groups:
females, F(3, 147) = 32.59, p < .001, g2 = .399, and
groups. In the 15- to 16-year-old age group only, an males, F(3, 147) = 11.90, p < .001, g2 = .195. For each
interaction effect between background and gender gender group, paired-samples t tests were used to
was also found, F(3, 51) = 7.52, p < .001, g2 = .307. contrast performance on each of the background
The main effect of background in the 13- to 14- types (six pairwise comparisons, a = .008). For
year-old group was followed up using six paired- females, d-prime values on negative trials were
samples t tests (a = .008). These comparisons
revealed signicant differences between negative
4.5
background trials and scrambled, t(19) = 6.19,
p < .001; neutral, t(19) = 3.91, p = .001; and positive, 4.0
*
t(19) = 3.69, p = .002, trials, with lower accuracy on 3.5 *
*
* *
** *
D-Prime

negative trials in each case. ** Negative


3.0 *
To explore the Background 9 Gender interaction 2.5 **
*
* Positive
in the 15- to 16-year-old age group, performance on * Neutral
2.0
each background type was compared via six Scrambled
1.5
paired-samples t tests (a = .008) for each gender
within this group. These analyses revealed that 1.0
females performed signicantly worse on negative 11-12 13-14 15-16 18-19 20-25
trials relative to scrambled, t(9) = 3.77, p = .004, Age Group
and neutral, t(9) = 3.49, p = .007, trials. In contrast, Figure 3. D-prime for all age groups and background types.
males in this group showed no signicant differ- Effects of trial background were seen in all but the oldest age
ences in nogo accuracy based on trial background group on this measure. The four younger groups all showed
type. Nogo trial accuracy for each gender in the signicantly poorer discrimination on negative versus scrambled
15- to 16-year-old age group, subdivided by back- background conditions. The two youngest groups (1112 and
1314 years) also showed signicantly poorer discrimination
ground, is presented in Figure 2b. on negative relative to positive and neutral conditions. In addi-
tion, the 13- to 14- and 18- to 19-year-old groups showed sig-
nicantly better performance on scrambled versus neutral
Effects of Age and Gender on Stimulus Discrimination conditions and the 13- to 14-year-old group alone also showed
signicantly better performance on scrambled relative to positive
Effects of fatigue and practice on d-prime were
background trials. Error bars show standard error.
examined via a 5 (age group) 9 2 (gender) *Signicantly different from negative, p < .01.
ANOVA. Results revealed no signicant effects.
Signicantly different from scrambled, p < .01.
Thus, this measure was not included as a covariate
in the subsequent d-prime analyses.
Table 2
The inuence of age and distracting emotional
D-Prime Values for All Age Groups and Backgrounds: Mean (Stan-
information on target discrimination, as measured
dard Deviation)
by d-prime, was examined via a 5 (age group) 9 2
(gender) 9 4 (background) mixed model ANOVA. Age group Negative Positive Neutral Scrambled
Results indicated main effects of both background,
F(3, 270) = 45.02, p < .001, g2 = .333, and age group, 1112 1.91 (0.73) 2.20 (0.67) 2.41 (0.49) 2.59 (0.65)
1314 2.50 (0.50) 2.91 (0.36) 2.86 (0.45) 3.22 (0.32)
F(4, 90) = 25.79, p < .001, g2 = .534, as well as a
1516 2.95 (0.55) 3.20 (0.55) 3.23 (0.46) 3.33 (0.42)
Background 9 Gender interaction, F(3, 270) = 3.47,
1819 3.12 (0.54) 3.26 (0.48) 3.22 (0.44) 3.46 (0.43)
p = .017, g2 = .037, and a Background 9 Age Group 2025 3.47 (0.50) 3.63 (0.56) 3.58 (0.33) 3.79 (0.53)
interaction effect, F(12, 270) = 2.12, p = .016,
1960 Cohen-Gilbert and Thomas

found to be signicantly lower than on all three other were seen, d-prime values were highest in the scram-
background types: positive, t(49) = 3.98, p < .001; bled background condition and lowest in the nega-
neutral, t(49) = 5.02, p < .001; and scrambled, tive background condition, with values on positive
t(49) = 8.81, p < .001. Values were also signicantly and neutral conditions falling in between. The two
higher for scrambled trials relative to both positive, youngest age groups showed signicant differences
t(49) = 6.41, p < .001, and neutral, t(49) = 4.54, between the negative condition compared to positive
p < .001, ones. Males displayed a similar pattern of and neutral conditions that were not seen in the older
results, with performance on negative trials being groups.
signicantly poorer than on positive, t(49) = 3.68,
p = .001; neutral, t(49) = 2.79, p = .007; and scram-
Effects of Age and Gender on Reaction Time
bled, t(49) = 5.50, p < .001, trials. Performance on
scrambled trials was also signicantly higher com- A 5 (age group) 9 2 (gender) ANOVA was used
pared to neutral trials, t(49) = 3.05, p = .004, though to examine group differences in the effects of fati-
the difference between scrambled and positive trials gue and practice on go trial reaction time. No sig-
did not reach signicance. Independent-samples nicant effects were found, so this variable was not
t tests contrasting performance between males and included in subsequent analyses.
females for each background type revealed no signif- To examine the effects of age and emotion on go
icant gender differences in d-prime. trial reaction time, a 5 (age group) 9 2 (gen-
The Background 9 Age group interaction was der) 9 4 (background) mixed model ANOVA was
followed up using ve repeated measures ANOVAs, run. Main effects were found for background, F(2.4,
one for each age group, to look at the effects of trial 220) = 58.93, p < .001, g2 = .396, and age group,
background on d-prime. Using a signicance criteria F(4, 90) = 2.51, p = .048, g2 = .100. There were no
of a = .01 to correct for multiple comparisons, signi- signicant interaction effects. Mean reaction times
cant effects of background were found in all but for all age groups and background types are pre-
the eldest age groups: 1112 years, F(3, 57) = 18.51, sented in Table 3 and Figure 4.
p < .001, g2 = .494; 1314 years, F(3, 57) = 18.29, p < The main effect of age group was followed up
.001, g2 = .491; 1516 years, F(2.0, 38.1) = 7.01, p = using 10 post hoc contrasts (a = .005). However, no
.003, g2 = .270; 1819 years, F(3, 57) = 5.13, p = .003, signicant differences between individual age
g2 = .213. For each of these four age groups, groups were found. Descriptively, reaction times
paired-samples t tests were used to contrast dis- improved from ages 11 to 16, with no appreciable
crimination on each of the background types improvements beyond that age. The main effect of
(a = .008). In the 11- to 12-year-old group, d-prime background was explored further via six paired-
was found to be signicantly lower for negative rel- samples t tests (a = .008), comparing reaction times
ative to all three other background types: positive, for each background type. These tests revealed that
t(19) = 3.02, p = .003; neutral, t(19) = 4.62, p < .001; reaction times were signicantly longer for negative
and scrambled, t(19) = 6.15, p < .001. This group trials compared to scrambled, t(99) = 10.47, p < .001;
also showed signicantly lower d-prime values for neutral, t(99) = 8.08, p < .001; and positive,
positive relative to scrambled trials, t(19) = 5.19, t(99) = 9.63, p < .001, trials. Reaction times were also
p < .001. In the 13- to 14-year-old group, d-prime found to be signicantly faster on scrambled trials,
was found to be signicantly lower for negative rel- when compared to neutral, t(99) = 4.53, p < .001,
ative to positive, t(19) = 4.25, p < .001, and scram- and positive, t(99) = 4.76, p < .001, trials.
bled, t(19) = 7.10, p < .00, trials. In this age group,
d-prime values were also signicantly higher on
scrambled trials compared to positive, t(19) = 4.73, Table 3
Reaction Time (ms) Data for All Age Groups and Backgrounds:
p < .001, and neutral, t(19) = 3.87, p = .001, trials. In
Mean (Standard Deviation)
the 15- to 16-year-old group, d-prime was signi-
cantly lower on negative relative to scrambled trials Age
only, t(19) = 3.78, p = .001. Likewise, in the 18- to Group Negative Positive Neutral Scrambled
19-year-old group, d-prime for negative trials was
signicantly lower than for scrambled trials, t(19) = 1112 416 (88) 401 (75) 399 (73) 390 (63)
1314 404 (40) 391 (36) 390 (35) 378 (25)
3.12, p = .006. This group also showed signicantly
1516 376 (24) 360 (19) 363 (23) 354 (21)
lower d-prime values for neutral relative to scram-
1819 378 (54) 366 (56) 366 (57) 361 (54)
bled trials, t(19) = 3.19, p = .005. In summary, in all 2025 385 (37) 368 (31) 368 (32) 364 (23)
but the eldest group, where no signicant effects
Inhibitory Control During Emotional Distraction 1961

450 and ADHD scores from the Conners Parent Rating


430
Scale, and anxious-depressed, withdrawn-depressed,
Reaction Time (msec)

and affective problems measures from the YSR. Of


410 these measures, state anxiety was found to predict
Negative
390 Positive nogo accuracy in the negative, F(1, 58) = 5.47,
Neutral p = .023, adjusted R2 = .070, and positive, F(1, 58) =
370
Scrambled 5.94, p = .018, adjusted R2 = .077, background con-
350 ditions, with accuracy increasing in each case with
330 increased reported state anxiety. No other signi-
11-12 13-14 15-16 18-19 20-25 cant relations were found between questionnaire
Age Group measures and task performance measures in this
age group.
Figure 4. Reaction times on correct go trials for all age groups In the adult group (1825 years), analyses
and background types. A main effect of background suggests
included the following questionnaire measures: state
that reaction times were signicantly longer for negative trials
relative to positive, neutral, and scrambled trials across the age and trait anxiety scores from the STAI, inattention
range studied. Error bars show standard error. and impulsivity scores from the CAARS, and
depression, anxiety and phobic anxiety scores from
the SCL90. As in the adolescent group, state anxi-
ety was found to predict nogo accuracy on negative,
Puberty and Task Performance
F(1, 38) = 6.27, p = .017, adjusted R2 = .119, and
Puberty scores were found to be highly corre- positive, F(1, 38) = 4.45, p = .042, adjusted
lated with age (r = .75, p < .001). Hierarchical R2 = .081, as well as scrambled, F(1, 38) = 6.31,
regressions performed for each performance mea- p = .016, adjusted R2 = .120, background conditions.
sure (nogo accuracy, d-prime, and reaction time) on In this age group, however, accuracy decreased with
each background condition (negative, positive, increased state anxiety. Negative relations were also
neutral, scrambled), showed no signicant predic- found between impulsivity scores and performance
tive value of pubertal score beyond age. Within the on positive trials as measured by both nogo accu-
adolescent sample (ages 1116 years) from whom racy, F(1, 36) = 5.10, p = .030, adjusted R2 = .100,
pubertal scores were collected, age consistently and d-prime, F(1, 36) = 8.75, p = .005, adjusted
showed higher correlations with performance on all R2 = .173. No other signicant relations between
measures and in all conditions than did pubertal questionnaire measures and task performance were
score. found.

Associations Between Task Performance and


Questionnaire Measures Discussion
Standardized questionnaires were administered Results of this study replicate previous research
mainly as a screening tool, used to detect and showing improvements in response inhibition with
exclude participants who were experiencing clinical age throughout adolescence (e.g., Casey et al., 1997;
levels of psychopathological symptoms in the Durston et al., 2002; Hooper et al., 2004; Johnstone,
absence of a formal diagnosis. However, a number Pleffer, Barry, Clarke, & Smith, 2005; Rubia et al.,
of the measures derived from these questionnaires 2006). This nding is consistent with a protracted
tap into constructs that are potentially relevant to development of inhibitory control that continues
task performance, even within a normative range of well into the adolescent years and contradicts sug-
scores. These possible relations were explored via gestions that response inhibition is fully developed
regression analyses. Because different, age-appropri- by the end of childhood (Paus, 2005; Paus, Kesha-
ate measures were administered to subjects under van, & Giedd, 2008).
age 18 years versus 18 and over, regression analy- Results of this study supported the prediction
ses were performed separately for these two age that younger adolescents, when required to exert
groups. inhibitory control over a potentiated response, are
In the adolescent sample (ages 1116 years), the more readily disrupted by emotional information
following questionnaire measures were included than are older adolescents and adults. Furthermore,
in the regression analyses: state anxiety and trait anx- emotional inputs appear to derail regulatory efforts
iety scores from the STAIC, cognitive impulsivity more easily in this age range even when the
1962 Cohen-Gilbert and Thomas

emotion information is not directly relevant to the particularly among girls (Dalgleish et al., 2003; Joor-
regulatory task. This effect, however, was limited to mann, Talbot, & Gotlib, 2007; Taghavi, Neshat-
negative images. Positive images, conversely, did Doost, Moradi, Yule, & Dagleish, 1999). Studies
not signicantly disrupt response inhibition, as have also found that performance on emotional go-
measured by nogo trial accuracy in the age range nogo tasks differs between healthy and clinically
tested. The lack of a signicant impact of positive depressed or anxious adolescents (Han et al., 2012;
images on this aspect of task performance may be Ladouceur et al., 2006). Similar performance effects
due to slightly lower arousal levels evoked by the have been found between healthy and mood-dis-
positive relative to the negative images (4.94 on the ordered adolescents on a memory task in which
vs. 5.32, respectively, on the Self-Assessment IAPS images were used as backgrounds for letter
Manikin [SAM] scale) or could reect the inuence stimuli (Ladouceur et al., 2005). Evidence of a
of an automatic orienting response to potentially change in emotional information processing in this
dangerous stimuli on negative trials that is difcult study and its deleterious impact on inhibitory con-

to override (Carretie, Martn-Loeches, Hinojosa, & trol within a healthy population of young adoles-
Mercado, 2001). Although other studies have cents suggests one possible mechanism contributing
reported increased disruption of inhibitory control to the elevated risk of psychopathology within this
by positive stimuli during adolescence (e.g., Somer- age group.
ville et al., 2011), these studies have used emotional It is worth noting, however, that relations found
information such as facial expressions as the distin- between the clinical questionnaire measures of
guishing factor between targets and nontarget depressive and anxiety symptoms and task perfor-
stimuli. Therefore, it is possible that the enhanced mance were minimal in the adolescent group.
tendency observed in adolescence to approach these Furthermore, state anxiety measures were found to
positive stimuli is more relevant when attention is correlate with improved accuracy on inhibitory
deliberately focused on emotional content. Alterna- trials within the adolescent group. This counterintu-
tively, such effects may be specic to social cues itive effect might be the result of young participants
such as facial expressions of emotion. Results of this who are more anxious in the research setting being
study do suggest that adolescents may not have as more invested in performing well while under a
much difculty deliberately diverting attention researchers observation, but this conclusion is
away from positive information as they do with highly speculative. The limited range of variability
negative content, a hypothesis supported by some in questionnaire measures may account for the
existing research (e.g., Monk et al., 2003). absence of signicant relations between other mood
In the mid-adolescent group (ages 1516 years), and attention measures and performance. Results in
females were found to have poorer inhibitory con- the adult group were more intuitive, showing
trol during distraction by negative emotional infor- increases in impulsive errors with increased ratings
mation, whereas males of the same age showed no of state anxiety and impulsivity.
effect of emotional backgrounds on nogo accuracy. Unlike inhibitory control, successful discrimina-
This result closely parallels ndings in the clinical tion of go and nogo stimuli, as measured by
literature that show marked gender differences in d-prime, showed signicant differences due to back-
the prevalence or depression and anxiety symptoms ground emotion in all but the eldest age group. This
in early to mid-adolescence (Angold et al., 2002; pattern of ndings suggests that the presence of
Ge, Lorenz, Conger, Elder, & Simons, 1994; Kessler images, and negative images in particular, does ren-
et al., 2001). This nding suggests a possible dif- der this go-nogo task more difcult for individuals
culty ignoring emotionally negative information in up through age 19, at least, though performance on
pubertal females that can impact cognitive control. the four background types becomes increasingly
Such a negative information processing bias, partic- similar with increasing age (see Figure 3). Unlike
ularly in association with reduced inhibitory con- inhibitory control, target discrimination appears to
trol, could inuence mood and constitute a risk be affected by the presence of any discernible image
factor for multiple forms of psychopathology. Mul- in most of the groups, indicated by better perfor-
tiple studies have established the contribution of mance on scrambled trials relative to picture trials.
emotional information processing in the risk for Differences in average reaction time on go trials
mood disorders in adulthood (see Mathews & revealed relatively little in the way of develop-
MacLeod, 2004, for a review) and some data mental change. Despite an overall main effect of
suggest a negative processing bias may also con- age group, individual comparisons of reaction
tribute to the risk for such disorders in adolescence, times between age groups revealed no signicant
Inhibitory Control During Emotional Distraction 1963

differences. This is most likely because the rela- monal measures of puberty, and is less uncomfort-
tively large within-group variability rendered more able for adolescent subjects, more direct pubertal
subtle between-group differences more difcult to measures could provide more nuanced information
detect. Descriptively, reaction times appear to on the role of puberty in emotional and cognitive
improve with age until reaching a plateau around changes.
1516 years of age. Across age groups, negative tri- The presentation of scrambled trials only in the
als showed signicantly slower reaction times rela- rst and last runs of the task was designed to allow
tive to all other trial types while scrambled trials for the detection of age differences in fatigue and
showed signicantly faster reaction times. This practice effects between age groups. However, this
pattern of results suggests that the negative images distribution of trials makes comparisons between
were at least somewhat salient in all ve age scrambled and nonscrambled trials more difcult.
groups. The slowed responding on the negative Placement and the beginning and end of the task
trials suggests that these images captured attention likely increased the impact of practice and fatigue
to a greater degree than other image types across on scrambled relative to other trial types. Neverthe-
the studied age range, including early adulthood. less, performance on these trials was consistently
The key difference, however, is that the older age better than on those presenting coherent images,
groups were still able to maintain high rates of even in the absence of signicant practice effects,
nogo trial accuracy, even while distracted by the suggesting that the absence of a coherent image
negative emotional information. This pattern of made for an easier task.
results suggests that age-related accuracy differ- Future studies would likely benet from inclu-
ences on negative versus other trial types are less sion of measures of alcohol and drug use, given the
likely a consequence of the emotional stimuli being relevance of substance use to inhibitory control,
more salient in the younger age groups and more particularly in adolescence. While only a small
likely an indication of an immature capacity for number of adolescent subjects reported drinking
cognitive control in emotionally distracting situa- without parental supervision and only one reported
tions. This result provides insight into the cognitive illicit drug use, frequency and magnitude of use
mechanisms at play when adolescents must regu- were not measured. Alcohol and drug use was not
late behavior in day-to-day situations, where measured in the young adult sample, where it was
unrelated emotion may prevent optimal cognitive likely more common.
functioning and decision making. Ultimately, this study only addresses a single
measure of inhibitory control, and more specically
the inhibition of a prepotent motor response. Natu-
Limitations and Future Directions
rally, impulsive decisions and actions taken by
It is not clear from this study whether the adolescents in their day-to-day lives are governed
increased disruptiveness of negative images in the by more complex and nuanced mechanisms than
13- to 14-year-old age groups and in 15- to 16-year- those that govern performance of a go-nogo task.
old females was due to reduced capacity for top- Factors such as the ability to weigh options, resolve
down control of attention and action, or by conicting inputs, and consider immediate versus
increased salience of the emotional information for more distant future rewards likely contribute to
these age groups. Future studies of the neural and adolescent behavior and continue to mature well
physiological correlates of these differences should beyond childhood. Personally relevant emotions are
help clarify the contributions of immature regulatory also more likely to impact behavior, compared to
abilities and increased emotionality to this effect. the presentation of emotional imagesthough our
However, emotional reactivity and emotion regula- reactions to such images may vary based on per-
tion are such intrinsically interwoven and mutually sonal relevance. Nevertheless, this protocol, despite
inuential processes that their contributions to its relative simplicity, does reveal potentially mean-
behavior are extremely difcult to distinguish. It is ingful age and gender differences in inhibitory con-
likely that both factors inuence performance to trol during emotional distraction.
some degree.
Another shortcoming of this study was the use
Conclusion
of a self-report-based measure of pubertal status as
opposed to a physical exam or hormonal measures. This study contributes to our understanding of
Although the Peterson scale has been shown to be how emotional information, even information that
moderately correlated with physiological and hor- is irrelevant to a given executive task, may still
1964 Cohen-Gilbert and Thomas

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