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Journal of Neuropsychology (2016)


2016 The British Psychological Society
www.wileyonlinelibrary.com

Emotional stimuli facilitate time perception in


children with attention-deficit/hyperactivity
disorder
Mohammad A. Nazari1*, Mohammad M. Mirloo2, Mazaher Rezaei3
and Mojtaba Soltanlou4,5
1
Cognitive Neuroscience Laboratory, Department of Psychology, University of
Tabriz, Iran
2
Department of Psychology, University of Tabriz, Iran
3
Departments of Psychiatry and Clinical Psychology, Zanjan University of Medical
Sciences, Iran
4
Graduate Training Centre of Neuroscience/IMPRS for Cognitive and Systems
Neuroscience, Tuebingen, Germany
5
Department of Psychology, University of Tuebingen, Germany
The aim of this study was to compare the effect of different emotional stimuli (neutral,
positive, and negative) on time perception in children with attention-deficit/hyperactivity
disorder (ADHD) and normal children in dual-task form. Five hundred and ninety-nine
students from primary schools were randomly selected. The Conners Teacher Rating
Scale (CTRS) questionnaire was completed by teachers. A total of 100 children with a
score above the cut-off point for the CTRS were further assessed using the Child
Symptom Inventory-4 (CSI-4). A total of 34 children with ADHD and 31 controls
completed an emotional time discrimination task in two blocks of 1000 and 2000 ms
duration. Children were asked to compare three image groups: neutral with neutral,
neutral with positive, and neutral with negative images. Children with ADHD had
significantly better performance in the emotional time discrimination task across all
conditions when compared with controls: On average, discrimination thresholds were
approximately 35 ms shorter for the children with ADHD. Our results indicate that
children with ADHD have higher sensitivity to time relative to controls in a situation in
which they must distribute resources between temporal and emotional processing. On
the basis of the interference effect and the working memory capacity hypothesis, this
dividing of attention causes a decrease of time accuracy in normal children.

The attention-deficit/hyperactivity disorder (ADHD) is one of the most common reasons for
child referral to mental health service centres (Faraone, Sergeant, Gillberg, & Biederman,
2003; Quartier, Zimmermann, & Nashat, 2010). It is characterized by inappropriate levels
of inattention, impulsivity, and hyperactivity (American Psychiatric Association, 2000).
Almost all models proposed for ADHD have considered this disorder as an executive
dysfunction disorder or frontal lobe syndrome (Brown, 2006). However, Barkley (1997)

*Correspondence should be addressed to Mohammad A. Nazari, Department of Psychology, University of Tabriz, 29 Bahman St.,
Tabriz 5166616471, (email: alinazari@tabrizu.ac.ir).

DOI:10.1111/jnp.12111
2 Mohammad A. Nazari et al.

believes that the major defect in this disorder is a deficit in behavioural inhibition that is
associated with four executive functions: working memory and time perception,
internalization of speech, emotional regulation, and reconstruction or formation of a new
and complex behavioural chain that can lead to self-regulation.
In Barkleys model, the ability to inhibit is the fundamental executive function upon
which other executive functions are developed. This model elaborates on the essential
linkages between inhibition and adequate development and functioning of all executive
functions (cited in Brown, 2006). Inhibition impacts these executive functions because
the first executive act must be the inhibition of responding (Barkley, Koplowitz,
Anderson, & McMurray, 1997; Barkley, Murphy, & Bush, 2001). The first executive
function that is influenced by response inhibition is the capacity to hold information in
working memory and use that information to direct a response. According to Barkleys
theory, inhibition aids working memory by allowing for a delay in response to an event and
by providing interference control. Consequently, deficits in working memory result in
secondary deficits in temporal information processing. This is because the time interval
must be maintained in working memory (Barkley et al., 1997, 2001). Behavioural
inhibition models suggest that the weak inhibition and the control of weak interference
influence working memory and consequently time processing (Barkley et al., 2001;
McGee, Brodeur, Symons, Andrade, & Fahie, 2004; Rubia et al., 2001).
Models of ADHD and clinical observation suggest that children with ADHD have sense
of time perception and time management deficits (Quartier et al., 2010). Empirically, this
deficit has been investigated using time production tasks (e.g., Barkley et al., 1997;
Cappella, Gentile, & Juliano, 1977) and time reproduction tasks (e.g., Barkley et al., 2001;
McGee et al., 2004; Rommelse, Oosterlaan, Buuitelaar, Faraone, & Sergeant, 2007; Smith,
Tyler, Rogeres, Newman, & Rubia, 2002; West et al., 2000). In these tasks, children with
ADHD performed less accurately (i.e., tended to underestimate target duration) and more
variably, especially as the target duration increased.
Using time discrimination tasks, Smith et al. (2002) concluded that the discrimination
threshold for children with ADHD was significantly higher compared to healthy controls.
A study conducted by Toplak, Rucklidge, Hetherington, John, and Tannock (2003)
challenged the common belief that sensorimotor processes in children with ADHD are
healthy (Barkley et al., 1997). Both visual and auditory stimuli were used in the time
discrimination task. The results showed that children with ADHD and children with
ADHD comorbid with a reading disability had higher thresholds in the visual time
discrimination task than the control group. Toplak and Tannock (2005) also administered
auditory and visual time discrimination tasks to adolescents with ADHD, who showed
higher discrimination thresholds than the control group on both visual (200 and
1,000 ms) and auditory tasks (200 and 1,000 ms). These group differences were largest in
the visual 1,000 ms task. Yang et al. (2007) investigated the relationship between
neurocognitive functions such as working memory, attention, inhibition, and cognitive
impairment in children with ADHD using a time discrimination task and showed that
children with ADHD had significantly higher thresholds than controls in long, medium,
and short periods.
In an excellent review, Toplak, Dockstader, and Tannock (2006) concluded that
although there is reasonable evidence to suggest that individuals with ADHD display
poorer performance in temporal information processing relative to controls, this
generalization must be interpreted cautiously, as different measurement methods (variety
of methods designed to quantify temporal information processing) and modalities (visual,
Emotion facilitates time perception in ADHD 3

auditory) and sample (children, adolescents or adults) have been used in research on this
topic.
On the other hand, current psychology literature has emphasized the centrality of
emotional factors in cognitive processes (Ochsner & Phelps, 2007), especially in time
perception (Tipples, 2008). Orme (1969) showed that pain and stress leads individuals to
underestimate time. Thayer and Schiff (1975) found that negative facial images cause
people to overestimate time. Watts and Sharrock (1984) found that phobic patients
demonstrate time overestimation when faced with fear-inducing stimuli. Droit-Volet,
Brunot, and Niedenthal (2004) showed that the viewing pictures of faces expressing
emotion was judged to be of longer duration than the viewing pictures of faces with
neutral expressions. Moreover, Yamada and Kawabe (2011) have provided evidence that
emotional processing modulates ongoing temporal processing even when the emotional
processing is unconscious.
In some studies on time perception, the International Affective Picture System (IAPS;
Angrilli, Cherubini, Pavese, & Manfredini, 1997; Lang, Bradley, & Cuthbert, 1995) was
used. Other studies used audio stimuli from International Affective Digital Sounds (IADS;
Bradley & Lang, 1999; Mella, Conty, & Pouthas, 2011; Noulhiane, Mella, Samson, Ragot, &
Pouthas, 2007). Yet others used emotional facial images (Droit-Volet et al., 2004; Effron,
Niedenthal, Gil, & Droit-Volet, 2006). Using different emotional stimuli, the aforemen-
tioned studies systematically showed that high arousal and viewing negative emotional
stimuli lead to time overestimation, and this effect was not observed for neutral control
stimuli. The researchers stated that this occurs because an aroused central nervous system
speeds up mechanisms that comprise the internal clock (Noulhiane et al., 2007).
Although several studies have been conducted on time perception impairment in
children with ADHD, the effect of emotion on time perception, especially in time
discrimination tasks, has not been investigated. In addition, all of the tasks that have been
used for investigating time discrimination in previous studies (Smith et al., 2002; Toplak &
Tannock, 2005; Toplak et al., 2003, 2006; Yang et al., 2007) contain simple images that
require less distribution of resources. Thus, pure time perception (in which attention is
allocated only for temporal processing) has been evaluated in these studies. The current
study aimed to further investigate time perception in children with ADHD using complex
images containing perceptual properties (i.e., salient colour distribution) and emotional
charges, in which attention should be distributed between temporal and non-temporal
processing.
Previous findings suggest that arousal and valence effects on time perception can
overwhelm the cognitive processes and attentional mechanisms involved in temporal
processing. In the other word, the degree of arousal generated by emotion accelerates/
decelerates the timer (the internal clock pacemaker), which results in longer/shorter
perceived duration (for a review, see Droit-Volet & Meck, 2007). In this line, it has been
shown that the administration of psychostimulants, such as methamphetamine, increases
arousal and leads to time overestimation, whereas the administration of antipsychotics,
such as haloperidol, decreases arousal and leads to time underestimation (Meck, 1996).
There is some evidence indicating that when non-temporal stimuli (e.g., emotional
events) are attended to, processing resources can be diverted away from temporal
processing. This causes subjective time distortion (Droit-Volet & Meck, 2007). Therefore,
it could be assumed that emotional effects override the attentional and perceptual
mechanisms. Considering the fact that attentional resource has an important impact on
time perception, particularly when non-temporal stimuli (e.g., emotional events) are
concurrently processed (Droit-Volet & Meck, 2007), and since children with ADHD suffer
4 Mohammad A. Nazari et al.

from significant impairments of executive function (Brown, 2006) and behavioural


inhibition (Barkley, 1997), we investigated how perceptual and emotional effects
modulate time perception in children with ADHD when these effects are added to a pure
time discrimination task (as a concurrent non-temporal process).

Method
Participants
A total of 599 students were selected from primary schools in Zanjan, Iran, using a
multistage cluster random sampling method. Of the 599 children, 100 children scored
above the cut-off point in Conners Teacher Rating Scale (CTRS; greater than or equal to 18
points for hyperactivity and 14 for attention deficit). Parents completed the scales for
ADHD, oppositional defiant disorder, and conduct disorder from the CSI-4 after being
provided with guidance on the importance of careful completion. At this stage, 34
children (mean age: 8.58  1.28) were identified with ADHD. The children who were in
the extreme of CTRS subscales scores were considered to be healthy. At first, those who
obtained a score of 0 in CTRS were chosen (n = 81). Then, children were excluded if they
were not zero-rated on the ADHD scale of CSI-4 or if they had a history of neurological
disease or pervasive developmental disorder or were taking psychotropic drugs. As a
result, 31 children (mean age: 8.5  1.38) were included in the control group (Table 1).
All participants had normal or corrected-to-normal vision.

Instruments
Stimuli
The visual stimuli used to measure time discrimination thresholds were chosen from the
IAPS (Lang et al., 1995). Of these images, 20 were selected with different emotional
charges including six neutral images (with valence and arousal between 4 and 6), seven
negative images (with valence between 1 and 3 and arousal between 4 and 6), and seven
positive images (with valence between 6 and 9 and arousal between 4 and 6). A pilot study
was completed to investigate whether these images were categorized as neutral, positive,
or negative in terms of valence and arousal in Iranian children. For this purpose, 50
subjects, separate from the subjects of the main study and including 25 girls and 25 boys
Table 1. Demographic characteristics of groups

Group
ADHD Control

n % n %

Gender
Female 9 26.5 7 22.6
Male 25 73.5 24 77.4
Age (year)
7 7 20.6 9 29
8 12 35.3 7 22.6
9 7 20.6 7 22.6
10 4 11.8 4 12.9
11 4 11.8 4 12.9
Emotion facilitates time perception in ADHD 5

from five elementary educational levels (five girls and five boys from each grade), were
selected through convenience sampling. The age range of subjects was 711 years (mean
age  SD = 9  1.6 years). The subjects were asked to evaluate images individually in
terms of valence (pleasant/unpleasant) and arousal by means of the paper and pencil 5-
point scales self-assessment manikin (SAM) developed by Bradley and Lang (1994). After
making contact with the subjects and before conducting the main test, three images were
provided to subjects to familiarize them with the SAM. Based on the subjects evaluations,
four images with the highest emotional charge scores were chosen from 20 images. Two
pictures were used as neutral stimuli (slide No. 7042; mean valence rating 2.93, mean
arousal rating 2.15 and slide No. 7182; mean valence 3.03, mean arousal 3.05), one as a
negative stimulus (slide No. 2095; mean valence 1.45, mean arousal 3.95) and one as a
positive stimulus (slide No. 7250; mean valence 4.23, mean arousal 2.93).

Time discrimination
A computerized test to measure time discrimination was provided based on tests used in
previous studies (Marx, Hopcke, Berger, Wandschneider, & Herpertz, 2013; Smith et al.,
2002; Toplak & Tannock, 2005; Toplak et al., 2003; Yang et al., 2007). Method of
comparison was used to measure time discrimination thresholds: A pair of visual stimuli
with different durations was presented successively, and the subjects were asked to
identify the picture with the longer duration and to respond by pressing the left or right
button to indicate their choice.
First, a visual stimulus appeared on the left or right side of the monitor for a certain
period of time and then disappeared. Next, another visual stimulus appeared on the other
side of monitor. After the presentation of the two visual stimuli, a question (in Persian)
appeared on the monitor: Which image was displayed for longer on the screen? The
subjects responded by pressing either the right button or left button. The next trial began
only after the subject made a response. One of the two stimuli (the target stimulus) had a
fixed time period (e.g., 1,000 ms) and the other stimulus (the comparative stimulus) had
a variable time period (e.g., 1,200 ms). The position of these two stimuli was changed
randomly. Each trial consisted of one of the following comparisons: neutral image (target)
with positive image (comparative), neutral image (target) with negative image (compar-
ative), or neutral image (target) with neutral image (comparative). Thus, three image
groups (neutral/positive, neutral/negative, and neutral/neutral) were presented and
compared. To eliminate bias, the target stimulus was randomly presented as the first or
second image. Each group consisted of 20 trials (the same pair of images was used during
the 20 trials), and a total of 60 trials were carried out in each block.
Two different durations were used to present the target and comparative stimuli in two
blocks, separately. In one block, the duration of the target stimuli was 1,000 ms. In this
block, the duration of the comparative stimuli began at 1,200 ms and increased or
decreased by 20 ms increments in subsequent trials depending on the accuracy of the
participants response. For example, when the subjects made an incorrect response, the
duration of the comparative stimulus in the next trial increased by 20 ms, leading to a
greater difference in duration between the target and comparative stimuli. When the
subjects made a correct response, the duration of the comparative stimulus in the next trial
was decreased by 20 ms. In the second block, the duration of target stimulus was 2000 ms
and the duration of comparative stimulus began at 2,300 ms. In this block, the comparative
stimulus increased or decreased by 30 ms relative to the performance of the subjects. The
order of blocks was counterbalanced within subjects.
6 Mohammad A. Nazari et al.

Before the main test, the subjects completed several practice trials, until the subject
was completely familiar with the process. No feedback was given to the subject about
errors, processes, and decreases or increases in stimulus duration.

Procedure
Each child performed the time discrimination task at their school and was seated
comfortably in front of a laptop computer in a quiet room. Parents received detailed
information about the study protocol before giving informed consent. After being shown
the study apparatus, children verbally assented to participation. No monetary compen-
sation was given. Parents agreed to participate in the study and signed written consent
forms. This study approved by the local committee.

Data analysis
An updown transformed-response adaptive procedure was used to estimate the
threshold at which a participant could accurately discriminate the target duration from
the comparison duration. Each time an incorrect response was made, and the comparison
duration was increased, thus increasing the difference between the durations of the two
images. Conversely, where a correct response was made, the comparison duration was
decreased, thus reducing the difference between the durations of the two stimuli.
According to Levitt (1971), the increase or decrease that is provided as a result of subjects
response is considered to be a step. These steps form alternating runs of correct answers
and incorrect answers. In turn, they form reversals, which are conditions in which the
correct answers are changed to wrong answers and wrong answers are changed to correct
answers. The task continued either until the subject had reached six reversals, or until 20
trials had been completed, whichever occurred first. According to Smith et al. (2002),
thismethod is believed to be highly appropriate for use with children with ADHD since the
number of trials can be reduced to a maximum of 20. The level of discrimination threshold
was calculated using the mid-point average of seven runs.

Statistical analysis
The normality of time discrimination threshold distribution was checked with
KolmogorovSmirnov test for six variables (neutral-1,000 ms, positive-1,000 ms, nega-
tive-1,000 ms, neutral-2000 ms, positive-2000 ms, and negative-2000 ms), separately. A
three-way repeated measures multivariate analysis of variance was used on the thresholds,
with group (ADHD vs. control children) as the between-subject factor, and duration
(1,000 ms vs. 2000 ms) and emotion (neutral, positive, negative) as within-subject factors.

Results
As shown in Table 1, there were no significant group differences in age, t(63) = 0.023,
p > .05, or sex distribution (v2 = 0.132, p > .05).
Means and error bars for time discrimination thresholds are shown in Figure 1. A
repeated measures ANOVA demonstrated a main effect of duration, F(1, 63) = 187.83,
p < .001. Mean thresholds were 246.55 and 353.4 ms for short duration (1,000 ms) and
for long duration (2,000 ms), respectively. Therefore, across groups, larger intervals were
Emotion facilitates time perception in ADHD 7

Figure 1. Means with error bars (with 95% confidence interval) for the time discrimination thresholds
as a function of duration (1,000 ms: left panel; 2,000 ms: right panel), emotion (neutral, positive, negative),
and group (ADHD: grey/triangle line; Control: black/circle line). This figure shows that children with
ADHD had lower thresholds (better performance) in all conditions relative to controls.

required to successfully discriminate longer durations. The main effect of group was also
significant, F(1, 63) = 5.58, p = .021, indicating that children with ADHD displayed
significantly lower thresholds (mean = 282.377 ms) than healthy controls
(mean = 317.58 ms) across all of the discrimination thresholds. No other significant
main effect of emotion, F(2, 126) = 1.57, p = .21, or duration 9 group, F(1, 63) = 1.89,
p = .17, emotion 9 group, F(2, 126) = 0.58, p = .56, emotion 9 duration, F(2,
126) = 1.60, p = .20, or duration 9 emotion 9 group, F(2, 126) = 0.66, p = .51 inter-
actions were observed.

Discussion
The primary objective of the study was to identify the effect of different emotional stimuli
(neutral, positive, and negative) on the time perception of children with ADHD.
Consistent with previous studies (e.g., Toplak & Tannock, 2005), there was a significant
effect of duration, indicating that both ADHD and control groups exhibited larger
thresholds in the longer duration than in the shorter duration. This result is consistent
with the original Webers law, according to which the just noticeable difference between
two stimuli is proportional to the magnitude of the baseline stimulus (Killeen & Weiss,
1987), in accordance with the scalar property (Gibbon, 1977). Given that the
8 Mohammad A. Nazari et al.

duration 9 group effect was not significant, one can conclude that the scalar property is
present in control subjects as well as in children with ADHD. This suggests that the
internal clock was not affected in children with ADHD.
An unanticipated finding was that children with ADHD showed lower discrimination
thresholds across all conditions. This suggests that children with ADHD had significantly
higher temporal discrimination sensitivity than controls, differing by approximately
35 ms. This result differs from previous studies (Smith et al., 2002; Toplak & Tannock,
2005; Toplak et al., 2003, 2006; Yang et al., 2007) that reported that children with ADHD
have a higher discrimination threshold compared to typical children.
A possible explanation for this unexpected finding may be the presence of a
concurrent non-temporal process. Previous studies have used simple shapes such as
circles or squares as visual stimuli, whereas the images used in this study included pictures
with complex features (spatial properties and semantic information) as well as emotional
charges. In this kind of task, a person will perform two tasks simultaneously, temporal and
non-temporal processing, in which attention should be distributed between two
processes (Brown, 1997). On the other hand, it is well documented that emotion affects
time perception (Droit-Volet & Meck, 2007). Yamada and Kawabe (2011) have shown that
the presentation of visible as well as invisible emotional pictures modulated the perceived
duration of a visible target stimulus, indicating that conscious and unconscious emotional
processing have an impact on temporal processing. As mentioned above, the stimuli that
we applied in our study consisted of emotional, but not simple, pictures. Even if it has
been implicitly processed, could have created a dual-task-like situation.
On the other hand, on the basis of the interference effect (see Brown, 1997 for a
review), individuals who process temporal information while also performing a
concurrent task are placed in a dual-task situation in which they must allocate resources
between temporal and non-temporal processes. During a dual task, the sharing of
attentional resources with non-temporal processing, and thus decreased attention
allocated to time processing, generally decreases the accuracy of time perception when
compared with a mono-task (Block, Hancock, & Zakay, 2010; Brown, 2008; Grondin,
2010). Individual differences in working memory capacity have been also shown to
influence time perception accuracy. Woehrle and Magliano (2012) compared the
perception of temporal duration in individuals with high and low working memory
capacity using a dual-task paradigm. In their study, participants engaged in a math task. At
any time during the task, the participants could indicate when they felt, a pre-specified
duration had passed. They found that when performing the dual task, individuals with low
working memory capacity had more difficulty maintaining focus on the non-temporal
task. However, participants with low working memory capacity were more accurate than
high-capacity participants on the timing task. They interpreted their findings in the
framework of the working memory capacity hypothesis, according to which working
memory moderates attentional resources trade-off between performances on two
concurrent tasks. Therefore, individuals with high working memory capacity would
take longer to signal the end of duration than low-capacity participants, and consequently
be less accurate in their temporal judgments (p. 315). In this line, they suggested that
participants with high/low working memory capacity allocate their attentional resources
differently for the two tasks, particularly for longer durations (Woehrle & Magliano, 2012).
Considering working memory deficits in children with ADHD (Barkley et al., 1997, 2001;
Martinussen, Hayden, Hogg-Johnson, & Tannock, 2005), we suggest that the explanation
of Woehrle and Magliano (2012) might be applicable to our finding. It could be that
children with ADHD focus their attention on temporal dimension, whereas typical
Emotion facilitates time perception in ADHD 9

children have simultaneously shared their attention resources between temporal and non-
temporal processing (spatial properties, e.g., salient colour distribution, or semantic
information of pictures). This dividing of attention, which usually occurs in dual tasks,
causes a decrease of time discrimination accuracy in normal children. However, we
emphasize that this interpretation needs to be further investigated by comparing the
performance of two groups in concurrent non-temporal processing (the degree of
engagement in emotional processing) by measuring, for instance, skin conductance
response to IAPS pictures while completing the time discrimination task). We
hypothesize that if attentional resources are more consumed by the alternative non-
temporal (in this case, emotional) aspect of pictures for the normal children than for the
ADHD children, they should be more aroused relative to normal children. This hypothesis
has a value for investigation in the future studies.
Overall, we elaborate that adding non-temporal processing (e.g., perceptual or
emotional properties) to the time perception task leads to an unexpected finding indicating
that children with ADHD show better performance in the time discrimination compared to
the controls. This finding suggests that time perception might be a sensitive indicator of the
basic features of stimuli. Considering the paucity of research conducted on time
discrimination in children with ADHD and varying results due to the different types of
stimuli used and the method of sampling, the present study is the first of its kind and more
research in this area is needed. Furthermore, in future studies, comparison of mono-task
and dual-task assessments of time discrimination would provide additional information.

Limitations
The current study has several limitations. The main limitation is that the selection of
samples was based solely on two questionnaires rated by teachers and parents. In spite of
the validity of these two instruments in diagnosing ADHD, the lack of a diagnostic
interview limits the generalization of our findings to children with subclinical ADHD
symptoms. The lack of working memory, IQ and attention assessment in both groups,
especially in children with ADHD is another limitation, and hence there were not ample
data for testing the interactive effects among cognitive abilities, emotional pictures, and
temporal processing. These important variables have to be elaborated by further
investigation.

Acknowledgements
We would like to thank all participating children and their parents as well as the involved
school teachers and principals. Finally, we thank Dr Jude Morton for language correction and
Barbara Peysakhovich for the proofreading of the manuscript.

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Received 15 September 2015; revised version received 17 July 2016

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