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Psychiatry Research
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A R T I C L E I N F O A B S T R A C T
Keywords: Emotional interference control refers to the ability to remain focused on goal-oriented processes when
Attention-Deficit/Hyperactivity Disorder confronted with disrupting but irrelevant emotional stimuli, a process that may be impaired in children and
(ADHD) adults with attention deficit/hyperactivity disorder (ADHD). However, emotional interference levels are known
Emotion regulation to be associated with trait anxiety, and patients with ADHD often display elevated levels of trait anxiety, such as
Emotional interference
these may have confounded previous findings of decreased emotional interference control in this population. In
Working memory, Interference control
the present study, male and female 8–13 years old (mean =11.0 years) children with ADHD (n=33) and
typically developing (TD) children (n=24) performed a visual emotional working memory (n-back) task with 2
memory loads and three different background pictures (neutral/positive/negative), and trait anxiety measures
were obtained. Children with ADHD performed less well, and displayed increased emotional interference in the
presence of aversive distractors when compared with TD children. Contrary to our expectations, trait anxiety did
not mediate the association between diagnostic group membership and the degree of emotional interference
control; however, co-morbid ODD was associated with decreased levels of emotional interference in ADHD.
Future research should aim at characterizing the mechanisms subtending decreased emotional interference
control in the ADHD population.
⁎
Correspondence to: Laboratoire de Psychopathologie et Neuropsychologie, Université Paris 8, 2 rue de la Liberté, 93526 Saint-Denis, France.
E-mail address: t.villemonteix@gmail.com (T. Villemonteix).
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Thomas Villemonteix and Ivo Marx equally contributed to this manuscript.
http://dx.doi.org/10.1016/j.psychres.2017.04.027
Received 26 July 2016; Received in revised form 28 February 2017; Accepted 15 April 2017
Available online 18 April 2017
0165-1781/ © 2017 Elsevier B.V. All rights reserved.
T. Villemonteix et al. Psychiatry Research 254 (2017) 1–7
arousing stimuli, and to do so flexibly (Shaw et al., 2014). Emotional emotional responses in healthy (Klumpp et al., 2011; Krug and Carter,
interference control, in particular, refers to the ability to control and 2012) and clinical (Holtmann et al., 2013; Wessing et al., 2017)
minimize the disrupting effect of irrelevant emotional stimuli on goal- samples. As subjects with ADHD display elevated levels of trait anxiety
oriented processes (Cohen et al., 2016). In everyday life, people are (Gonzalez-Castro et al., 2015) and subjects with high trait anxiety
continually exposed to potentially emotion-arousing stimuli, ranging display increased susceptibility to interference, trait anxiety might
from internal sensations like an upset stomach to external events, such serve as a mediator between ADHD and impaired emotional interfer-
as facial expressions or verbal utterances. Due to its salience (i.e. ence control.
relevance for long-term goals and survival of the individual), this In the present study, we seek to compare children with an ADHD
emotional material tends to undergo preferential attentional processing diagnosis and TD children in their ability to cope with emotional
(Vuillemier et al., 2005). When not relevant for the on-going task, it distractors while performing an emotional n-back task, and to explore
may cause emotional distraction, by interfering with appropriate task- the effect of trait anxiety on emotional interference measures in this
related cognitive, behavioural, or affective functioning (Iordan et al., population. Our hypotheses are as follow: i) we expect all children to
2013). display increased response times and decreased performance accuracy
Considering the core symptoms of ADHD and their association with as a function of task difficulty and when confronted with emotional
emotional dysregulation symptoms, it has been hypothesized that pictures. ii) we hypothesize that children with ADHD will display
children with ADHD may be characterized by deficits in emotional increased response times and lower performance accuracy in compar-
interference control. An increased susceptibility to distraction is one of ison to TD children (Martinussen et al., 2005). iii) we expect patients to
the core behavioural diagnostic criteria of ADHD (American Psychiatric be more distractible by task-irrelevant emotional stimuli, as indicated
Association, 2013), associated with broad impairment across multiple by longer response times and decreased performance accuracy under
domains, including cognitive functioning, interpersonal relationships, emotionally arousing conditions in comparison to TD children. iv) we
and health (e.g. increasing risk for accidents and associated injuries; hypothesize that trait and state anxiety will mediate the association
Barkley and Cox, 2007; Higginbotham and Bartling, 1993; Maedgen between ADHD and increased susceptibility to emotional distractors.
and Carlson, 2000). Deficits in emotional interference control may
contribute to distractibility, as well as to other core symptoms of the 2. Methods
inattentive cluster, such as careless mistakes, inattentive listening and
forgetfulness in daily activities. Furthermore, a frequent and/or more 2.1. Participants
intense automatic attentional capture by emotional stimuli could
multiply the risk of displaying inappropriate levels of emotional Fifty-eight children aged eight to thirteen years participated in the
responses, leading to emotional dysregulation symptoms. To identify study. Children with ADHD were recruited from the outpatient clinic at
deficits in attentional control of emotional stimuli in children with an Robert-Debré Hospital, Paris, France. TD participants were recruited
ADHD diagnosis may therefore contribute to explain the core symptoms through word of mouth by the experimenters. The Kiddie Schedule for
of the disorder, in particular emotional dysregulation. Affective Disorders and Schizophrenia for School Aged Children-
Recent research has started to use executive functioning tasks Present and Lifetime Version (K-SADS-PL; Endicott and Spitzer, 1978)
together with distracting emotional components to study emotional was completed at screening for each participant to confirm the
interference control in ADHD populations. For example, López-Martín diagnosis according to DSM-IV-R criteria in children with ADHD, and
et al. (2013) first investigated the effect of irrelevant emotional to ensure that TD children presented no psychiatric condition. More-
distractors on goal-directed information processing in children with over, parents of each child participant in the study completed the
ADHD and typically developing (TD) children. Scalp event-related ADHD Rating Scale IV (ADHD-RS-IV; DuPaul et al., 1998). Intellectual
potentials were recorded while participants performed a digit categor- quotient was evaluated using an abbreviated version of the Wechsler
ization task with positive, neutral, and negative stimuli. Emotional Intelligence Scale for Children (fourth edition), including four subtests:
distractors were found to be associated with longer response times and similarities, matrix reasoning, letter-number sequencing and symbol
with greater anterior N2 amplitudes in the ADHD group only, support- search (Grégoire 2009). The exclusion criteria for all participants were
ing the hypothesis that emotional distractibility is increased in children an IQ lower than 70, a current affective or anxiety disorder, a
with ADHD. In a recent study characterized by a limited statistical neurological disorder, and previous head injury. One participant with
power (i.e. limited number of trials), Van Cauwenberge et al. (2015) ADHD refused to pursue the experimental task after the first three
used an emotional working-memory task to study emotional interfer- blocks and was therefore excluded from the study. The final sample
ence in children with ADHD and TD children and failed to report consisted of 33 children with ADHD (26 combined type, 7 inattentive
significant group-by-diagnostic interaction, despite a noticeable trend type) and 24 TD children. Seven children in the ADHD group had a
in the data for reaction times measures. Finally, in an adult sample, comorbid oppositional defiant disorder (ODD), and four families (two
Marx and colleagues (2011) implemented a working memory (‘n-back’) children with ADHD and two TD children) also reported a learning
task that requires attentional control of emotional distractors in disorder. Seven children with ADHD were taking methylphenidate at
patients with ADHD vs. healthy controls. Lowly arousing distractors the time of the study but were out of medication for a minimum of 24 h
were found to decrease performance accuracy in the ADHD group, (immediate release methylphenidate) or 48 h (delayed release methyl-
whereas healthy adults only showed decreased performance in the phenidate) prior to testing. All children with combined type ADHD
presence of highly arousing negative distractors. scored above the 90th percentile on the total scale of the ADHD-RS-IV.
Taken together, a limited number of behavioural studies seem to Participants with predominantly inattentive type of ADHD either scored
support the idea that a high level of emotional interference is associated above the 90th percentile on the total scale of the ADHD-RS-IV, or
with ADHD. However, when investigating emotional interference above the 90th percentile on the inattention subscale of the ADHD-RS-
control in ADHD patients, one should take into account the increased IV. TD children all scored below threshold on the ADHD-RS-IV in total
levels of anxiety symptoms that have been consistently reported in this score and in the subscales of inattention and impulsivity/hyperactivity.
group (Graetz et al., 2001; Gonzalez-Castro et al., 2015; Skogli et al., Finally, both diagnostic groups did not differ with regard to gender, χ2
2013). This seems especially important as subjects with high anxiety =.31, p=.58, ns. Demographic and clinical sample characteristics are
levels are known to display dysfunctional emotional control (Bishop presented in Table 1.
et al., 2004; MacNamara et al., 2011). More precisely, high levels of The study was carried out in accordance with the latest version of
trait anxiety have been associated with increased response times in the the Declaration of Helsinki. Each child and her/his parents gave their
presence of emotional distractors and reduced top-down regulation of consent to participate in this study reviewed and accepted by the local
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T. Villemonteix et al. Psychiatry Research 254 (2017) 1–7
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T. Villemonteix et al. Psychiatry Research 254 (2017) 1–7
Table 2
Descriptive statistics for the emotional N-back task performance.
1-back
neu 1.92 .57 2.27 .34
neg 1.86 .57 2.11 .40
pos 1.97 .50 2.18 .33
2-back
neu 1.34 .60 1.77 .55
neg 1.39 .64 1.70 .55
pos 1.32 .74 1.75 .48
M SD M SD F(1,53) F(1,53) F(1,53) F(2,106) F(2,106)
1-back
neu 739.16 200.38 666.09 196.94
neg 867.70 273.56 656.53 109.77
pos 772.83 253.11 675.76 142.52
2-back
neu 801.23 258.62 706.74 193.95
neg 981.81 311.94 811.28 221.64
pos 811.81 259.14 752.38 191.69
ADHD = Subjects with ADHD, CON = Controls. Group = between-subjects effect of experimental group membership, N-back = within-subjects effect of task difficulty, N-back x Group
= within-between-subjects interaction effect, Emotion = within-subjects effect of the emotional salience of the background picture stimuli, Emotion x Group = within-between-subjects
interaction effect. M = Mean, SD = Standard Deviation. neu = neutral pictures, neg = negative emotional salience, pos = positive emotional salience. All values are raw uncorrected
means. *p < .05, **p < .01, *** p < .001. Descriptive statistics for hits and false alarms are reported in the Supplementary material.
sures for the mediation analyses, we calculated difference scores for RT (54) =−1.07, p=.87, ns; positive vs. negative: t(54) =3.68, p=.002).
and d′ in the negative condition when compared with the neutral Children with ADHD responded slower than TD children, F(1,53)
condition (emotional interference scores). Correlations between state/ =6.74, p=.01, ηp2 =.11 (Table 2).
trait anxiety measures and emotional interferences scores were also Additionally, there was an interaction effect between diagnostic
calculated. As associations between trait anxiety and dysfunctional group membership and emotional salience of the distractors, F(2,106)
emotional interference control may be stronger under high executive =3.98, p=.02, ηp2 =.07. In the presence of negative distractors, t(54)
control demands (Choi et al., 2012), analyses were conducted for the 1- =3.49, p=.001, but not in the presence of neutral, t(54) =1.85,
back and 2-back conditions separately. p=.07, ns, or positive, t(55) =1.70, p=.10, ns, distractors, children
with ADHD displayed increased response times when compared with
3. Results TD children (ADHD; neutral: M =770.19 ms, SD =175.70 ms; nega-
tive: M =924.75 ms, SD =178.70 ms; positive: M =792.32 ms, SD
3.1. Performance accuracy =156.74 ms; controls: neutral: M =686.41 ms, SD =175.70 ms;
negative: M =733.91 ms, SD =210.78 ms; positive: M =714.07 ms,
Repeated measures ANOVA on performance accuracy with the SD =184.87 ms). Post-hoc paired-samples t-tests revealed that this
diagnostic group (subjects with ADHD; TD children) as the between- effect was driven by differential response patterns between experi-
subjects factor and working memory load (1-back; 2-back) and emo- mental groups: While TD children displayed a stable response pattern
tional salience of the distractors (neutral; negative; positive) as the across all emotional conditions (all ps > .05), children with ADHD
within-subject factors revealed main effects for working memory load displayed prolonged RTs in the negative condition when compared with
and the diagnostic group: All children displayed higher performance the neutral and positive distractor condition (negative vs. neutral: t(31)
accuracy in the 1-back condition when compared with the 2-back =−4.30, p < .001; negative vs. positive: t(32) =3.64, p=.001; neutral
condition, F(1,55) =78.58, p < .001, ηp2 =.59 (Table 2). Overall, vs. positive: t(31) =−.64, p=.53, ns). No further significant effects
children with ADHD displayed decreased performance accuracy when emerged (all ps > .05).
compared with TD children, F(1,55) =12.49, p=.001, ηp2 =.19. The All significant between-subjects effects are displayed in Fig. 1, and
same pattern of results emerged when hits and false alarms were the between-within subjects interaction effect with regard to RT is
analyzed separately (see Supplementary material). No further signifi- displayed in Fig. 2. Please note that for the response time, the adjusted
cant main or interaction effects emerged (all ps > .05). mean values from the ANCOVA were chosen to visualize the experi-
mental effects.
3.2. Response times
3.3. Analyses of covariates
The same analysis as described above was conducted on response
times. As a result, we found main effects for working memory load, F Comorbid ODD status displayed a significant effect in the between-
(1,53) =10.02, p=.003, ηp2 =.16, and emotional salience, F(2,106) subjects model, F(1,51) =7.63, p=.008, ηp2 =.13, and RT group
=10.94, p < .001, ηp2 =.17. All subjects responded faster in the 1-back differences in effects size increased from ηp2 =.11 to ηp2 =.17.
condition when compared with the 2-back condition, and post-hoc Moreover, comorbid ODD status significantly interacted with the
analyses revealed that all subjects responded faster in the neutral and in emotional salience levels, F(2,102) =3.82, p=.03, ηp2 =.07. Post-hoc
the positive condition when compared with the negative condition univariate ANCOVAs which were conducted for each salience level
(neutral vs. negative: t(54) =−4.29, p < .001; neutral vs. positive: t separately with the diagnostic group as the between-subjects factor and
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T. Villemonteix et al. Psychiatry Research 254 (2017) 1–7
*** **
CON ADHD
Fig. 1. Group Differences in Emotional N-back Task Performance. CON = control group, ADHD = ADHD group. d′ = discriminability score, ms = response time in milliseconds. All
charts are based on estimated marginal means. *p < .05, **p < .01, ***p < .001.
ODD status as the covariate revealed a significant impact of ODD status As an auxiliary analysis, we performed the same computations for
on RT in the negative, F(1,53) =10.42, p=.002, ηp2 =.16, and in the state anxiety, controlling for trait anxiety. Here, we found a direct effect
positive, F(1,54) =6.72, p=.01, ηp2 =.11, but not in the neutral of diagnostic group membership on one of our two measures of
condition, F(1,53) =2.85, p=.10, ns. As a result, the interaction effect emotional interference (RT) in the 1-back condition (ADE =184.21,
between diagnostic group membership and emotional salience level BCa 95% CI =47.80; 375.35, p=.01) and in the 2-back condition (ADE
increased from ηp2 =.07 to ηp2 =.17. In fact, it became evident that =173.73, BCa 95% CI =24.43; 353.21, p=.03), whereas the indirect
response time differences between the diagnostic groups were no longer effects via state anxiety as a mediator were not significant (1-back:
present only in the negative condition, but now in all three emotional ACME =−10.46, BCa 95% CI =−61.68; 13.49, p=.56; 2-back: ACME
conditions when ODD status was taken into account, but it was still =−8.04, BCa 95% CI =−65.19; 45.01, p=.84). No direct or mediated
mostly pronounced in the negative condition (neutral: F(1,53) =5.42, effects emerged for d′.
p=.02, ηp2 =.09; negative: F(1,53) =18.52, p < .001, ηp2 =.26; Finally, correlations between state anxiety and emotional interfer-
positive: F(1,54) =6.35, p=.02, ηp2 =.11). ences measures, and trait anxiety and emotional interference measures
were not significant (all p's > .05).
***
*
*
CON ADHD
Fig. 2. Group Differences in Emotional N-back Task Performance Depending on Emotional Distractor Quality. CON = control group, ADHD = ADHD group. ms = response time in
milliseconds. Neu = neutral pictures, Neg = negative emotional salience, Pos = positive emotional salience. All charts are based on estimated marginal means. *p < .05, **p < .01,
***p < .001.
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T. Villemonteix et al. Psychiatry Research 254 (2017) 1–7
compared with the negative condition (effect of emotional salience), low CU traits have consistently been found to exhibit hyperactivity in
supporting validity of our experimental task. In addition, we found that the amygdala when processing negative stimuli, whereas the opposite
children with ADHD displayed prolonged response times and decreased pattern has been found in youths with DBD and high CU traits (Baker
performance accuracy when compared with the TD children, thus et al., 2015). Future studies should therefore examine ODD and CU
replicating WM deficits in children and adolescents with ADHD traits as potential mediators of increased vs. decreased emotion
(Martinussen et al., 2005). interference in children with ADHD.
More interestingly, we were able to detect increased emotional The results of the present study should be interpreted in the light of
interference in the ADHD group: When compared with TD children, several limitations. First, our sample was characterized by a limited
children with ADHD displayed increased response times in the presence sample size to conduct mediation analyses (Fritz and McKinnon 2007),
of aversive distractors, contingent on a salience-specific increase of although mediation effects have been reported in ADHD in samples of
their response times in this condition: Whereas TD children displayed a similar (Mary et al., 2016) or smaller (Rints et al., 2015) sizes. The lack
stable performance across all salience levels, children with ADHD of significant mediation effect may therefore reflect a type-2 error.
decelerated specifically in the presence of negative distractors. This Second, the experimental design used in the present study consisted of
finding is in line with previous studies documenting an increased emotional blocks presented in a random order. In this context, potential
emotional distractibility in children and adults with ADHD (Marx et al., carry-over effects between positive vs. negative vs. neutral emotional
2011; Lopez-Martin et al., 2013). In particular, similarly to one blocks could not be controlled for. Such carry-over effects may have
previous study in children, we found emotional distractors to cause reduced the magnitude of our findings. Third, each experimental
prolonged response times in patients with ADHD while not affecting condition (i.e. memory load X emotional condition) only consisted of
performance accuracy (Lopez-Martin et al., 2013), whereas the oppo- 28 picture presentation. This number chosen to ensure that the task
site pattern, i.e. decreased performance accuracy but normal response duration was acceptable for children may have reduced the statistical
times, has been reported in the only previous emotional n-back study on power to detect memory load X emotional condition and memory load
ADHD in adults (Marx et al., 2011). We hypothesize that these age- X emotional condition X group interactions. Fourth, data on the
related differences may be explained by differences in task difficulty physical properties of the images, such as luminance, color composi-
between the age groups, as indicated by larger performance accuracy z- tion, contrast or complexity were not available for the IAPS pictures.
scores in adults when compared with children (mean (SD) performance Uncontrolled differences associated with these parameters may have
accuracy in adults: 3.61 (.78), in children: 1.63 (.59); Marx et al., represented a confounding factor when comparing different emotional
2011). Indeed, previous research suggests that increased task difficulty conditions in the present study (Marchewka et al., 2014). Fifth,
may represent a shield against distraction, by promoting focal-task although several studies have shown that the pictures taken from the
engagement, reducing the neural processing of distracting stimuli, and IAPS elicit emotional responses in adults and children (McManis et al.,
potentiating the capability to block their influence on attentional 2001; Waters et al., 2005; Sharp et al., 2006), it should be noted that
processes (Halin et al., 2014; Hughes et al., 2013; Sörqvist et al., 2016). the participants of the present study did not subjectively rate the
Although both ADHD (Marx et al., 2011) and trait anxiety (Klumpp pictures at the end of the task. It is therefore unclear whether a
et al., 2011; Krug and Carter, 2012) are associated with decreased particular set of pictures was responsible for the results obtained in this
control of interfering emotional stimuli, and increased levels of trait study, and whether participants of different ages of gender may have
anxiety have been observed in those with ADHD (Gonzalez-Castro et al., been differently affected. Finally, since our study was based on DSM-IV
2015), trait anxiety did not mediate the relationship between ADHD criteria, we did not consider disruptive mood dysregulation disorder
diagnosis and decreased emotional interference control in our study. (DMDD) as a potential comorbidity. Considering the key symptoms of
Furthermore, in the present sample, we failed to evidence a correlation DMDD (i.e. chronic, severe irritability and anger), children with ADHD
between trait or state anxiety measures and emotional interference +DMDD may represent a distinct group in terms of both emotion
scores. One possible explanation for this discrepancy with previous regulation and emotional interference control deficits (Hommer et al.,
findings lies in the type of negative emotional stimuli that were 2014). Future studies should compare children with ADHD and children
presented. Here, negative stimuli comprised sad, threatening and with ADHD/DMMD in their ability to cope with emotional interfer-
fearful stimuli of different types (e.g. faces, situations, animals), ences, using more recent and better characterized picture datasets
whereas previous studies used threatening (Klumpp et al., 2011; (Marchewka et al., 2014). Nevertheless, our study was also character-
Wessing et al., 2017) or fearful (Klumpp et al., 2011) faces, which ized by several strengths, being conducted in an ADHD sample
may represent more salient stimuli for participants with high trait comprising a majority of medication-naïve children (79%), ruling out
anxiety levels. Taking the presence or absence of ODD into account, our to a large degree potential MPH long-term effects in our data, and no
exploratory analyses suggest that comorbid ODD in the ADHD group other DSM-IV-R psychiatric comorbidities than ODD, which contributes
may mask a specific RT deficit in the presence of emotional distractors to the specificity of our results.
when compared to non-emotional distractors. This finding is in line In conclusion and in line with previous findings, we found that
with previous studies suggesting that reduced amygdala responsiveness children with ADHD displayed decreased emotional interference con-
to aversive cues may play a role in the development of ODD and CD trol, especially in the presence of aversive distractors (as measured by
(Herpertz et al., 2005; Sterzer et al., 2005; Masi et al., 2014; Matthys our experimental task). Contrary to our expectations, the relationship
et al., 2013). In particular, Sterzer et al. (2005) reported deactivations between ADHD diagnosis and decreased emotional interference control
in the left amygdala and in the anterior cingulate cortex in adolescents was not mediated by trait anxiety, which was also increased in our
with CD compared with control subjects when viewing negative ADHD sample. Future research should investigate which psychological
pictures, and Masi et al. (2014) found children and adolescents with and neurobiological processes may mediate the relationship between
ADHD and ODD/CD to rate negative IAPS pictures as less aversive than the bottom-up processing of emotionally interfering stimuli and emo-
healthy subjects. However, contradictory findings have also been tion dysregulation symptoms.
reported in two previous studies documenting an increased emotional
responsiveness to (Herpertz et al., 2008) and an increased distractibility
by (Euler et al., 2014) negative picture stimuli in children and Conflict of interest
adolescents with ODD/CD and different rates of comorbid ADHD when
compared with healthy populations. One recent review suggests that We report no conflict of interest.
these inconsistent results may partly result from variations in callous-
unemotional (CU) traits across samples. Indeed, youths with DBD and
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T. Villemonteix et al. Psychiatry Research 254 (2017) 1–7