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The effect of environmental distractors incorporation into a CPT on sustained attention and ADHD diagnosis among adolescents

Authors:
  • Faculty of Health Sciences Ben-Gurion University of the Negev Beer Sheva

Abstract and Figures

Diagnosis of ADHD in adolescents involves specific challenges. Conventional CPT's may fail to consistently distinguish ADHD from non-ADHD due to insufficient cognitive demands. The aim of this study was to explore whether the incorporation of environmental distractors into a CPT would increase its ability to distinguish ADHD from non-ADHD adolescents. New Method: Using the rate of omission errors as a measure of difficulty in sustained attention, this study examined whether ADHD adolescents are more distracted than controls and which type of distractors is more effective in terms of ADHD diagnosis. The study employed the MOXO-CPT version which includes visual and auditory stimuli serving as distractors. Participants were 176 adolescents aged 13-18 years, 133 diagnosed with ADHD and 43 without ADHD. Results and Comparison with existing methods: Results showed that ADHD adolescents produced significantly more omission errors in the presence of pure visual distractors and the combination of visual and auditory distractors than in no-distractors conditions. Distracting stimuli had no effect on CPT performance of non-ADHD adolescents. ROC analysis further demonstrated that the mere presence of distractors improved the utility of the test. This study provides evidence that incorporation of environmental distractors into a CPT is useful in term of ADHD diagnosis. ADHD adolescents were more distracted than controls by all types of environmental distractors. ADHD adolescents were more distracted by pure visual distractors and by the combination of distractors than by pure auditory ones.
Content may be subject to copyright.
Journal
of
Neuroscience
Methods
222 (2014) 62–
68
Contents
lists
available
at
ScienceDirect
Journal
of
Neuroscience
Methods
jou
rn
al
h
om
epa
ge
:
www.elsevier.com/locate/jneumeth
Clinical
Neuroscience
The
effect
of
environmental
distractors
incorporation
into
a
CPT
on
sustained
attention
and
ADHD
diagnosis
among
adolescents
Itai
Bergera,,
Hanoch
Cassutob
aThe
Neuro-Cognitive
Center,
Pediatric
Division,
Hadassah-Hebrew
University
Medical
Center,
Jerusalem,
Israel
bPediatric
Neurology
Clinic,
Leumit
HMO,
Jerusalem,
Israel
h
i
g
h
l
i
g
h
t
s
Adolescents
with
ADHD
are
more
easily
distracted
than
controls.
Incorporation
of
environmental
distractors
improves
CPT
validity.
Visual
distractors
are
more
beneficial
in
terms
of
ADHD
diagnosis
than
auditory
distractors.
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
31
July
2013
Received
in
revised
form
17
October
2013
Accepted
18
October
2013
Keywords:
ADHD
CPT
Adolescents
Distractors
Omission
Sustained
attention
a
b
s
t
r
a
c
t
Background:
Diagnosis
of
ADHD
in
adolescents
involves
specific
challenges.
Conventional
CPT’s
may
fail
to
consistently
distinguish
ADHD
from
non-ADHD
due
to
insufficient
cognitive
demands.
The
aim
of
this
study
was
to
explore
whether
the
incorporation
of
environmental
distractors
into
a
CPT
would
increase
its
ability
to
distinguish
ADHD
from
non-ADHD
adolescents.
New
method:
Using
the
rate
of
omission
errors
as
a
measure
of
difficulty
in
sustained
attention,
this
study
examined
whether
ADHD
adolescents
are
more
distracted
than
controls
and
which
type
of
distractors
is
more
effective
in
terms
of
ADHD
diagnosis.
The
study
employed
the
MOXO-CPT
version
which
includes
visual
and
auditory
stimuli
serving
as
distractors.
Participants
were
176
adolescents
aged
13–18
years,
133
diagnosed
with
ADHD
and
43
without
ADHD.
Results
and
comparison
with
existing
methods:
Results
showed
that
ADHD
adolescents
produced
signif-
icantly
more
omission
errors
in
the
presence
of
pure
visual
distractors
and
the
combination
of
visual
and
auditory
distractors
than
in
no-distractors
conditions.
Distracting
stimuli
had
no
effect
on
CPT
performance
of
non-ADHD
adolescents.
ROC
analysis
further
demonstrated
that
the
mere
presence
of
distractors
improved
the
utility
of
the
test.
Conclusions:
This
study
provides
evidence
that
incorporation
of
environmental
distractors
into
a
CPT
is
useful
in
term
of
ADHD
diagnosis.
ADHD
adolescents
were
more
distracted
than
controls
by
all
types
of
environmental
distractors.
ADHD
adolescents
were
more
distracted
by
pure
visual
distractors
and
by
the
combination
of
distractors
than
by
pure
auditory
ones.
© 2013 The Authors. Published by Elsevier B.V. All rights reserved.
1.
Introduction
Attention-deficit
hyperactivity
disorder
(ADHD)
is
among
the
most
common
neurobehavioral
disorders
of
childhood.
In
approx-
imately
60%
of
children
with
ADHD,
symptoms
persist
into
This
is
an
open-access
article
distributed
under
the
terms
of
the
Creative
Commons
Attribution
License,
which
permits
unrestricted
use,
distribution,
and
reproduction
in
any
medium,
provided
the
original
author
and
source
are
credited.
Corresponding
author
at:
The
Neuro-Cognitive
Center,
Pediatric
Division
Hadassah-Hebrew
University
Medical
Center,
P.O.
Box
24035,
Mount
Scopus,
Jerusalem
91240,
Israel.
Tel.:
+972
2
584
4903;
fax:
+972
2
532
8963.
E-mail
address:
itberg@hadassah.org.il
(I.
Berger).
adolescence
and
may
continue
into
adulthood
(Faraone
et
al.,
2006;
Kessler
et
al.,
2006).
Assessment
of
ADHD
is
always
a
complex
task,
which
requires
comprehensive
investigation
of
mul-
tiple
sources,
such
as
clinical
interviews,
observations,
reports
of
parents
and
teachers,
psycho-educational
assessment,
and
neuro-developmental
examination.
However,
diagnosis
of
ADHD
in
adolescents
involves
specific
challenges
and
obstacles.
One
of
the
difficulties
is
the
complex
presentation
of
the
syndrome
in
adolescence.
Research
suggests
that
the
symptoms
manifestation
of
ADHD
changes,
sometimes
dramatically,
with
developmen-
tal
course:
while
hyperactivity
often
declines
by
adolescence,
attention
deficits
appear
to
remain
more
constant,
and
impulsi-
vity
transforms
into
more
overt
difficulties
in
executive
functions
(Wasserstein,
2005).
In
addition,
ADHD
in
adolescents
and
adults
0165-0270/$
see
front
matter ©
2013 The Authors. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.jneumeth.2013.10.012
I.
Berger,
H.
Cassuto
/
Journal
of
Neuroscience
Methods
222 (2014) 62–
68 63
is
commonly
nestled
with
other
psychiatric
comorbidities,
such
as
substance
abuse,
antisocial
behaviour,
learning
disabilities,
con-
duct
disorders,
mood
and
anxiety
disorders
(Brown,
2000).
Another
common
problem
of
evaluating
ADHD
in
adolescence
stems
from
typical
biases
of
adolescents
in
self-reports
scales.
Adolescents
are
considered
poor
self-observers
and
often
tend
to
underestimate
their
problems
(Barkley
et
al.,
1991;
Wasserstein,
2005).
The
agree-
ment
between
adolescents
and
their
parents
regarding
the
type
of
symptoms
was
found
to
be
low
(Rasmussen
et
al.,
2002).
Due
to
the
subjective
nature
of
these
instruments,
computer-
ized
continuous
performance
tests
(CPT)
are
frequently
employed
in
clinical
and
diagnostic
settings
(Edwards
et
al.,
2007).
Typical
CPT
task
requires
the
participant
to
sustain
attention
over
a
continuous
stream
of
stimuli
(single
letters,
shapes
or
digits
which
are
pre-
sented
serially)
and
to
respond
to
a
pre-specified
target
(Kelip
et
al.,
1997;
Shalev
et
al.,
2011).
Traditionally,
inattention
is
assessed
in
CPT
by
the
number
of
omission
errors,
indicating
the
number
of
times
the
target
was
presented,
but
the
participant
did
not
respond,
or
by
its
“inverse”
measure
calculating
relative
accuracy
(the
num-
ber
of
correct
hits
out
of
the
total
targets
presented).
Contextual
factors,
such
as
distracting
stimuli
in
the
environment,
can
con-
tribute
to
increased
inattention
(Adams
et
al.,
2011;
Blakeman,
2000;
López-Martín
et
al.,
2013).
Therefore,
sustained
attention
can
be
broadly
characterized
as
the
ability
to
concentrate
on
a
specific
stimulus
over
a
period
of
time
while
excluding
distracting
stimuli
(Shalev
et
al.,
2011).
Despite
the
popularity
of
the
CPT
in
clinical
contexts,
many
authors
have
identified
concerns
about
its
reliability
and
validity
in
the
diagnosis
of
ADHD.
Test–retest
reliability
of
the
CPT
varied
considerably
across
studies.
Several
CPT’s,
such
as
the
Test
of
Variables
of
Attention
(T.O.V.A.)
(Greenberg
and
Kindschi,
1998)
and
the
Conners
CPT-II
(Conners,
2000)
do
not
report
test–retest
reliability.
In
others,
such
as
the
AX’
CPT
test,
test–retest
reliability
ranged
between
0.14
and
0.94,
dependent
on
CPT
indices.
Omission
errors
tend
to
have
the
lower
reliability
measures
while
commission
errors
and
response
times
have
moderate
or
high
measures
(Ogundele
et
al.,
2011).
CPT’s
are
often
criticized
for
their
low
sensitivity
and
specificity
rates
(less
than
70%)
(Edwards
et
al.,
2007;
McGee
et
al.,
2000;
Riccio
et
al.,
2001;
Skounti
et
al.,
2007).
Many
authors
have
questioned
its
ability
to
consistently
discriminate
ADHD
children
from
normal
controls,
psychiatric
controls
or
learning
disabilities
(DeShazo
et
al.,
2001;
Dickerson
Mayes
et
al.,
2001;
Ogundele
et
al.,
2011;
Schachar
et
al.,
1998;
Skounti
et
al.,
2007).
Others
reported
a
weak
associa-
tion
between
CPT
performance
and
behavioural
indices
of
ADHD
(Christensen
and
Joschko,
2001;
Epstein
et
al.,
2009;
McGee
et
al.,
2000).
The
validity
of
the
CPT
in
the
diagnosis
of
ADHD
is
even
more
controversial
among
teenagers
(Robin,
1998).
The
Degraded
Stimulus
Continuous
Performance
Test
(DS-CPT)
was
found
to
be
insensitive
to
identifying
sustained
attention
deficits
in
adolescent
populations
and
failed
to
discriminate
ADHD
from
controls
(Rund
et
al.,
1998).
Similarly,
Rucklidge
(2006)
reported
that
the
Conners
CPT-II
(Conners,
2000)
failed
to
identify
many
adolescents
with
ADHD,
and
was
generally
more
sensitive
to
ADHD
in
males
than
in
females.
Recently,
Diamond
et
al.
(2012)
have
demonstrated
that
the
correlation
between
neurologist’s
impression
of
the
presence
of
attention
deficit
and
the
T.O.V.A.
scores
was
weaker
in
ado-
lescents
(ages
13–18)
than
in
younger
children
(ages
6–12).
The
Gordon
Diagnostic
System
(GDS;
Gordon
and
Mettelman,
1987),
which
is
the
only
CPT
that
has
been
researched
specifically
with
adolescents
(also
approved
by
the
FDA),
successfully
discriminated
ADHD
adolescents
from
controls
on
the
vigilance
task,
but
not
on
the
distractibility
task
(Robin,
1998).
Barkley
(1991)
has
shown
low
correlations
between
CPT
perfor-
mance
of
adolescents
and
other
measures
of
ADHD
such
as
parents
and
teachers
rating
scales.
It
was
suggested
that
the
ecological
validity
of
the
CPT
in
adolescent
samples
is
weaker
than
in
younger
children
and
that
this
shortcoming
is
crucial
where
prediction
to
school
behaviour
may
be
desired.
Barkley
(1991)
emphasized
the
need
to
improve
the
ecological
validity
of
the
CPT
by
evaluating
the
child’s
behaviour
in
more
natural
settings.
Nevertheless,
even
when
noise-generated
CPT
was
employed
(Uno
et
al.,
2006),
the
sensitivity
of
the
test
to
ADHD
in
older
children
(ages
10–12)
was
lower
than
in
younger
children
(ages
7–9).
The
authors
suggested
that
the
differences
in
attention
span
between
ADHD
and
normal
controls
are
reduced
to
a
level
undetectable
by
CPT,
as
a
result
of
developmental
changes.
Another
possible
explanation
for
the
insensitivity
of
CPT
in
adolescents
is
the
constant
pace
of
stimuli
presentation.
Because
the
inter-stimulus
interval
in
traditional
CPT
is
typically
fixed,
it
makes
the
task
too
easy
for
adolescents
who
quickly
figure
out
the
timing
of
stimulus
appearance
(Robin,
1998).
Further
support
for
the
ceiling
effect
in
CPT
performance
of
adolescents
arrives
from
imaging
study
that
compared
brain
activation
patterns
in
adoles-
cents
with
and
without
ADHD
while
performing
an
attentional
CPT
(Epstein
et
al.,
2009).
The
two
groups
performed
similarly
and
activated
similar
regions
during
performance,
but
children
with
ADHD
appear
to
maintain
the
use
of
right
prefrontal
regions
beyond
what
is
observed
among
normal
controls.
The
difficulty
to
detect
group
behavioural
differences
was
attributed
to
the
low
cognitive
demands
of
the
task.
Taken
together,
these
findings
suggest
that
conventional
CPT’s
may
fail
to
consistently
distinguish
ADHD
from
non-ADHD
teenagers
due
to
insufficient
cognitive
demands
and
may
not
reflect
the
conditions
in
school.
The
aim
of
this
study
was
to
explore
whether
the
incorporation
of
environmental
distractors
into
a
CPT
would
increase
its
ability
to
distinguish
ADHD
adolescents
from
controls
(ages
13–18).
Assum-
ing
that
distracting
stimuli
have
an
effect
on
sustained
attention
by
increasing
the
rate
of
omission
errors
in
CPT,
we
hypothesized
that
adolescents
with
ADHD
would
perform
significantly
more
omission
errors
than
their
non-ADHD
peers
in
the
presence
of
distracting
stimuli.
We
also
examined
which
type
of
distractors
would
be
more
effective
in
terms
of
ADHD
diagnosis.
2.
Methods
2.1.
Participants
Participants
were
176
adolescents
aged
13–18
years,
118
were
boys
and
58
girls.
The
clinical
ADHD
group
was
composed
of
133
participants
previously
diagnosed
with
ADHD
(Mean
age
=
14.64,
S.D.
=
1.43),
and
the
control
group
included
43
participants
without
ADHD
(Mean
age
=
15.08,
S.D.
=
1.71).
Participants
in
the
ADHD
group
were
recruited
from
adolescents
referred
to
the
out-patient
clinics
of
a
Neuro-Cognitive
Centre,
based
in
a
tertiary
care
university
hospital.
The
referrals
to
the
centre
were
made
by
paediatrician,
general
practitioner,
teacher,
psychologist,
or
parents.
The
following
were
the
inclusion
criteria
for
participants
in
the
ADHD
group.
Each
participant
met
the
criteria
for
ADHD
according
to
DSM-
IV-TR
criteria
[American
Psychiatric
Association
(APA),
2000],
as
assessed
by
a
certified
paediatric
neurologist.
The
diagnostic
procedure
included
completion
of
a
semi-structured
interview
(adolescent
and
parents)
fulfilling
the
diagnostic
guidelines
as
described
in
the
clinical
practice
guideline
for
the
diagnosis,
eval-
uation,
and
treatment
of
ADHD
in
children
and
adolescents
by
the
American
Academy
of
Paediatrics
(Wolraich
et
al.,
2011)
and
mandatory
rating
scales
for
home
and
school
(DuPaul
et
al.,
1998),
as
well
as
medical/neurological
examination.
64 I.
Berger,
H.
Cassuto
/
Journal
of
Neuroscience
Methods
222 (2014) 62–
68
Fig.
1.
Definition
of
the
time
line
target
and
non-target
stimuli
were
presented
for
500,
1000
or
4000
ms.
Each
stimulus
was
followed
by
a
void
period
of
the
same
duration.
The
stimulus
remained
on
the
screen
for
the
full
duration
regardless
the
response.
Distracting
stimuli
were
not
synchronized
with
target/non-target’s
onset
and
could
be
generated
during
target/non
target
stimulus
or
during
the
void
period.
Participants
in
the
control
group
were
randomly
recruited
from
regular
school
classes.
The
inclusion
criteria
for
participants
in
the
control
group
were:
(1)
score
below
the
clinical
cut
off
point
for
ADHD
symptoms
on
ADHD/DSM-IV
Scales
(APA,
2000;
DuPaul
et
al.,
1998)
and
(2)
absence
of
academic
or
behavioural
problems
based
on
parents
and
teachers
reports.
For
this
purpose
the
parents
and
teachers
were
asked
to
state
(with
the
informed
consent)
that
there
are
no
behavioural/academic/social
difficulties.
Given
these
conditions,
no
additional
physical/neurological
examination
was
administered.
Assigning
participants
to
ADHD/non-ADHD
groups
based
on
parents
and
teachers
ratings
of
ADHD
symptoms
is
a
common
and
reliable
method
in
the
literature
(e.g.,
Berwid
et
al.,
2005;
Uno
et
al.,
2006;
Van
Mourik
et
al.,
2007).
Exclusion
criteria
for
all
participants
were:
abnormal
mental
ability,
other
chronic
(mental,
health
or
developmental)
condition,
chronic
use
of
medications,
and
primary
psychiatric
diagnosis
(e.g.,
depression,
anxiety,
or
psychosis).
Since
we
worked
in
Jerusalem,
our
population
was
extremely
heterogeneous,
multicultural,
and
included
a
spectrum
of
families
with
regard
to
potentially
con-
founding
factors
correlated
with
the
diagnosis
of
ADHD
(Wolraich
et
al.,
2011).
All
participants
agreed
to
participate
in
the
study
and
their
parents
provided
a
written
informed
consent
to
the
study,
approved
by
the
Helsinki
committee
(IRB)
of
Hadassah-Hebrew
University
Medical
Centre
Jerusalem,
Israel.
2.2.
Measures
Measurement
of
adolescent
behaviour
the
parent
and
teacher
forms
of
the
ADHD/DSM-IV
scales
were
used
to
assess
the
level
of
participants’
ADHD
behaviours
(APA,
2000;
DuPaul
et
al.,
1998).
The
MOXO
Continuous
Performance
Test
the
study
employed
the
MOXO-CPT
version1(Berger
and
Goldzweig,
2010),
which
is
a
standardized
computerized
test
designed
to
diagnose
ADHD
related
symptoms.
The
test
included
visual
and
auditory
stimuli
that
serve
as
distractors.
The
total
duration
of
the
test
was
18.2
min,
and
it
is
composed
of
eight
levels
(136.5
s,
59
trials
each).
In
each
trial
a
stimulus
(target/non-target)
was
presented
for
500,
1000
or
4000
milli-
seconds
and
then
followed
by
a
“void”
period
of
the
same
duration
1The
term
‘MOXO’
derives
from
the
world
of
Japanese
martial
arts
and
means
a
‘moment
of
lucidity’.
It
refers
to
the
moments
preceding
the
fight,
when
the
warrior
clears
his
mind
from
distracting,
unwanted
thoughts,
and
feelings.
(Fig.
1).
The
stimulus
remained
on
the
screen
for
the
full
duration
no
matter
if
a
response
was
produced.
This
practice
allowed
the
mea-
suring
of
response
timing
(whether
the
response
occurred
during
stimulus
presentation
or
the
void
period)
as
well
as
the
accuracy
of
the
response.
In
each
level
34
target
and
25
non-target
stimuli
were
presented.
Both
target
and
non-target
stimuli
were
cartoon
pictures
that
do
not
include
any
letters.
The
absence
of
letters
is
important
given
the
fact
that
ADHD
patients
tend
to
have
learning
difficulties
(e.g.,
dyslexia,
dyscalculia)
that
may
be
confound
with
CPT
performance
(Seidman
et
al.,
2001).
The
stimuli
were
presented
sequentially
in
the
middle
of
a
computer
screen
and
the
participant
was
instructed
to
respond
as
quickly
as
possible
to
target
stimuli
by
pressing
the
space
bar
once,
and
only
once.
The
participant
was
also
instructed
not
to
respond
to
any
other
stimuli
except
the
target,
and
not
to
press
any
other
key
but
the
space
bar.
Test
level
and
distracting
stimuli-In
order
to
simulate
everyday
environment
of
adolescents,
the
MOXO-CPT
contained
distracting
stimuli.
This
feature
is
unique
to
this
specific
CPT.
Distractors
were
short
animated
video
clips
containing
visual
and
auditory
features
which
can
appear
separately
or
together.
This
enabled
to
present
three
types
of
distractions
that
characterize
everyday
environment:
(a)
visual
distractors
(e.g.,
animated
barking
dog);
(b)
auditory
dis-
tractors
(e.g.,
barking
sound);
and
(c)
combination
of
both
visual
and
auditory
distractors
(e.g.,
animated
barking
dog
with
the
sound
of
barking).
Overall,
eight
different
distractors
were
included,
each
of
them
could
appear
as
pure
visual,
pure
auditory
or
as
a
combination
of
them.
Different
levels
of
the
MOXO-CPT
were
characterized
by
a
different
set
of
distractors:
levels
1
and
8
did
not
include
any
distractors
but
only
target
and
non-target
stimuli,
levels
2
and
3
contained
pure
visual
stimuli,
levels
4
and
5
contained
pure
audi-
tory
stimuli,
and
levels
6
and
7
contained
a
combination
of
visual
and
auditory
stimuli.
Each
distractor
was
presented
for
8
s,
with
a
fixed
interval
of
0.5
s
between
two
distractors.
Distractors’
onset
was
not
synchronized
with
target/non-target’s
onset
and
could
be
generated
during
target/non
target
stimulus
or
during
the
void
period.
Visual
distractors
appeared
at
one
of
four
spatial
locations
on
the
sides
of
the
screen:
down,
up,
left
or
right.
The
sequence
of
distractors
and
their
exact
position
on
the
display
were
constant
for
each
level.
The
burden
of
the
distracting
stimuli
increased
at
the
odd
number
levels;
in
the
2nd,
4th,
and
6th
level
only
one
distractor
was
presented
at
a
time,
while
in
the
3rd,
5th,
and
7th
level
two
distractors
were
presented
simultaneously.
I.
Berger,
H.
Cassuto
/
Journal
of
Neuroscience
Methods
222 (2014) 62–
68 65
Table
1
Differences
in
omission
errors
between
ADHD
and
non-ADHD
adolescents.
Distractors
type
ADHD
(N
=
143)
Non-ADHD
(N
=
33)
Difference
t(172)
M
S.D.
M
S.D.
No
distractors
2.17
0.44
0.58
1.22
4.51,
p
<
0.05
Visual
distractors
3.56
3.24
1.02
2.09
4.61,
p
<
0.001
Auditory
distractors
2.46
2.95
0.81
2.14
3.17,
p
<
0.05
Combination
of
visual
and
auditory
distractors 3.92 3.49 0.88
2.45
5.13,
p
<
0.001
M
=
mean;
S.D.
=
standard
deviation.
Performance
indices
the
MOXO-CPT
included
four
perfor-
mance
indices:
attention,
timing,
impulsivity,
and
hyperactivity.
For
detailed
description
of
performance
indices
see
Supplementary
A.
2.3.
Procedure
In
the
current
study,
the
test
was
administered
by
a
technician
who
made
sure
that
the
participant
understood
the
instructions.
The
technician
was
present
throughout
the
entire
session.
All
participants
(including
the
ADHD
group)
were
drug
naïve
(not
med-
icated
at
all)
before
and
during
their
participation
in
the
study.
2.4.
Data
analyses
All
analyses
were
conducted
with
SAS
software
for
Windows
version
9.2.
A
p-value
of
0.05
was
considered
statistically
significant.
First,
Chi-square
analysis
and
t-test
for
unpaired
samples
were
used
to
examine
group
differences
in
background
variables.
Second,
effects
of
background
variables,
ADHD,
and
test
level
on
omission
errors
were
examined
through
a
Linear
Repeated
Measures
model
with
Tukey’s
correction
for
multiple
comparisons.
Omission
errors
were
the
dependant
variable,
whereas
age,
gender,
group,
level,
and
level
×
group
interaction
were
the
independent
variables.
Between
and
within
group
effects
were
measured
in
every
CPT
condition
(no
distractors,
visual
distractors,
auditory
distractors
and
a
combina-
tion
of
visual
and
auditory
distractors).
For
this
purpose,
every
two
identical
levels
were
combined:
levels
1
and
8
(no
distractors),
lev-
els
2
and
3
(visual
distractors),
levels
4
and
5
(auditory
distractors)
and
levels
6
and
7
(combination
of
visual
and
auditory
distractors).
To
determine
which
type
of
distractors
was
more
useful
in
terms
of
ADHD
diagnosis,
we
calculated
the
areas
under
the
receiver
oper-
ating
characteristic
(ROC)
curves.
After
a
ROC
was
generated
for
each
distractor
type,
chi-square
tests
were
performed
in
order
to
compare
the
utility
of
different
test
conditions
in
the
diagnosis
of
ADHD.
3.
Results
3.1.
Effects
of
distractors
on
omission
errors
in
ADHD
and
non-ADHD
adolescents
In
order
to
study
the
added
value
of
the
incorporation
of
dis-
tractors
in
the
CPT
for
a
better
differentiation
between
ADHD
and
controls
a
linear
repeated
measures
model
with
Tukey’s
correction
for
multiple
comparisons
was
conducted.
This
model
included:
(a)
between
groups
analysis
of
the
differ-
ences
in
the
rate
of
omission
errors
between
ADHD
and
non-ADHD
adolescents
and
(b)
within-group
analysis
of
the
differences
in
omission
errors
between
no
distractors
conditions
and
the
three
conditions
which
contained
distractors
(visual,
auditory
and
a
com-
bination
of
them).
First,
analyses
showed
that
both
gender
[F(1,
172)
=
5.26,
p
<
0.05]
and
age
[F(1,
172)
=
9.10,
p
<
0.01]
were
asso-
ciated
with
CPT
performance.
That
is,
boys
and
younger
children
demonstrated
higher
omission
errors.
However,
ADHD
group
did
not
differ
from
the
non-ADHD
group
in
age
[t(174)
=
1.48,
p
=
0.097]
or
gender
distributions
[2(1,
N
=
176)
=
0.19,
p
=
0.662].
When
controlling
for
age
and
gender,
group
affiliation
had
a
significant
effect
on
the
rate
of
omission
errors
[F(1,
172)
=
28.45,
p
<
0.001].
As
can
be
seen
in
Table
1,
ADHD
adolescents
demon-
strated
higher
rate
of
omission
errors
than
their
unaffected
peers
in
all
CPT
conditions
(no
distractors,
visual
distractors,
auditory
dis-
tractors
and
a
combination
of
visual
and
auditory
distractors).
Most
importantly,
group
×
level
interaction
revealed
that
the
difference
between
the
two
groups
varied
as
a
function
of
task
demands
[F(3,
172)
=
4.98,
p
<
0.01].
Within-groups
analysis
indicated
that
in
the
ADHD
group,
omission
errors
were
significantly
higher
in
the
presence
of
visual
distractors
and
the
combination
of
visual
and
auditory
distractors
than
in
no-distractors
conditions.
The
pres-
ence
of
pure
auditory
distractors
did
not
increase
the
amount
of
omission
errors
as
compared
to
no-distractors.
In
the
control
group,
distracting
stimuli
had
no
effect
on
CPT
performance
as
compared
to
no-distractors
conditions
(Table
2).
3.2.
ROC
analyses
The
discriminant
ability
of
different
distractors
types
was
eval-
uated
by
a
Receiver
Operating
Characteristic
(ROC)
curve
analysis
(Fig.
2).
ROC
analysis
summarizes
diagnostic
efficiency
with
the
area
under
the
curve
(AUC)
statistic.
First,
ROC
analyses
revealed
that
the
mere
presence
of
dis-
tractors
(AUC
=
0.890)
significantly
improved
the
AUC
of
the
test,
as
compared
to
the
absence
of
distractors
(AUC
=
0.784)
[2(1,
N
=
176)
=
8.51,
p
<
0.01].
Specifically,
the
AUC
of
combined
visual
and
auditory
distractors
was
the
highest
(AUC
=
0.867).
The
com-
bination
of
distractors
significantly
improved
the
utility
of
the
test
in
the
diagnosis
of
ADHD
as
compared
to
no-distractors
[2(1,
N
=
176)
=
5.35,
p
<
0.05].
Pure
visual
(AUC
=
0.846)
and
pure
auditory
(AUC
=
0.772)
distractors
did
not
yield
any
diagnostic
Table
2
Level
Differences
in
omission
errors
within
each
study
group.
Comparison
t(172)
ADHD
(N
=
143)
Non-ADHD
(N
=
33)
No
distractors
vs.
visual
distractors
6.59,
p
<
0.0001
1.20,
N.S.
No
distractors
vs.
auditory
distractors
1.30,
N.S.
0.60,
N.S.
No
distractors
vs.
combined
distractors
6.65,
p
<
0.0001
0.65,
N.S.
Visual
distractors
vs.
auditory
distractors
5.70,
p
<
0.0001
0.62,
N.S.
Visual
distractors
vs.
combined
distractors
1.40,
N.S.
0.30,
N.S.
Auditory
distractors
vs.
combined
distractors
6.12,
p
<
0.0001
0.17,
N.S.
66 I.
Berger,
H.
Cassuto
/
Journal
of
Neuroscience
Methods
222 (2014) 62–
68
Fig.
2.
ROC
analyses.
advantage
over
no-distractors
conditions.
Although
the
combina-
tion
of
visual
and
auditory
distractors
was
favourable
in
terms
of
sensitivity
and
specificity
in
comparison
to
pure
auditory
distrac-
tors
[2(1,
N
=
176)
=
12.92,
p
<
0.001],
it
was
not
beneficial
over
pure
visual
distractors
[2(1,
N
=
176)
=
0.64,
N.S.].
4.
Discussion
This
study
investigated
the
effects
of
environmental
distractors
on
sustained
attention
of
ADHD
and
non-ADHD
adolescents
(ages
13–18).
Results
showed
that
ADHD
adolescents
demonstrated
higher
rates
of
omission
errors
than
their
unaffected
peers
in
all
CPT
conditions.
In
addition,
ADHD
adolescents
produced
significantly
more
omission
errors
in
the
presence
of
pure
visual
distractors
and
the
combination
of
visual
and
auditory
distractors
than
in
no-distractors
conditions.
In
contrast,
distracting
stimuli
had
no
effect
on
CPT
performance
of
non-ADHD
adolescents.
Findings
from
ROC
analysis
further
demonstrated
that
independently
of
distrac-
tors
type,
impending
distractors
in
CPT
significantly
improved
the
sensitivity
and
specificity
of
the
test.
It
is
known
that
a
variety
of
visual
and
auditory
stimuli
exists
in
the
everyday
environment
of
ADHD
children
and
that
prob-
lematic
behaviour
first
appear
in
the
presence
of
such
stimuli.
Thus,
our
results
support
the
idea
that
ADHD
is
indeed
marked
by
high
distractibility
and
that
teenagers
with
ADHD
have
difficulties
to
sustain
attention
in
the
presence
of
irrelevant
environmental
stimuli.
These
findings
are
in
line
with
studies
of
younger
chil-
dren
with
ADHD,
which
demonstrated
high
distractibility
during
CPT
and
non-CPT
tasks
(Adams
et
al.,
2011;
Gumenyuk
et
al.,
2005;
Parsons
et
al.,
2007;
Pelham
et
al.,
2011).
Parsons
et
al.
(2007),
who
used
a
virtual
reality
technology
to
simulate
every-
day
distractibility
in
ADHD,
have
shown
that
during
distracting
conditions,
ADHD
children
were
more
hyperactive
and
produced
more
omission
errors
on
the
Conners’
CPT-II
as
compared
to
non-
ADHD
children.
On
the
other
hand,
our
findings
are
inconsistent
with
other
studies
which
indicated
that
auditory
and
visual
distrac-
tors
did
not
impair
cognitive
performance
of
ADHD
children
or
even
improved
it
(Abikoff
et
al.,
1996;
Uno
et
al.,
2006;
Van
Mourik
et
al.,
2007).
This
diversity
may
result
from
the
type
of
distractors
used.
While
some
studies
have
used
neutral
stimuli
(neutral
tone/letter)
as
distractors
(Gordon
and
Mettelman,
1987;
Uno
et
al.,
2006;
Van
Mourik
et
al.,
2007),
the
MOXO-CPT
used
more
ecologically
valid
stimuli
that
are
typically
found
in
the
child’s
environment.
Since
ADHD
children
have
more
difficulties
in
filtering
meaningful
distractors
(Blakeman,
2000)
they
may
fail
to
inhibit
response
to
relevant,
everyday
stimuli
rather
than
to
neutral
information.
Another
factor
that
may
contribute
to
the
high
distractibility
of
ADHD
adolescents
in
this
study
is
the
method
of
distractors
presentation.
In
several
studies,
auditory
distractors
served
as
a
background
noise
while
children
performed
another
cognitive
task
(Abikoff
et
al.,
1996;
Pelham
et
al.,
2011).
In
contrast,
distractors
in
the
MOXO-CPT
vary
in
their
type,
in
their
length
of
presentation
and
in
their
location
on
the
screen.
This
mode
of
presentation
did
not
allow
adjustment
or
de-sensitization
to
the
distractors,
therefore
kept
them
salient.
The
current
study
revealed
that
the
distractibility
of
ADHD
ado-
lescents
varied
across
the
distractors’
modality.
The
fact
that
visual
stimuli
appeared
as
more
potent
distractors
for
ADHD
adolescents
than
auditory
distractors
is
consistent
across
studies
with
ADHD
children
(Pelham
et
al.,
2011).
The
most
straightforward
hypothe-
sis
is
that
because
the
MOXO-CPT
is
a
visual
task
that
includes
visual
input
and
processing,
it
might
be
more
vulnerable
to
visual
distrac-
tors
that
use
the
same
cognitive
modality
(Wickens,
1984,
2002).
It
is
also
possible
that
due
to
impaired
visual
attention
in
ADHD
(Kofler
et
al.,
2008),
additional
visual
information
easily
overload
the
cognitive/physiological
system,
thus
interfering
with
perfor-
mance
(Armstrong,
1993;
Armstrong
and
Greenberg,
1990).
The
effect
of
auditory
distractors
on
ADHD
children
and
adoles-
cent
remains
unclear.
While
the
current
study
failed
to
show
any
effect
of
auditory
distractors
on
cognitive
performance
in
ADHD
adolescents,
others
have
found
that
auditory
distractors
could
either
interfere
or
improve
it
(Abikoff
et
al.,
1996;
Pelham
et
al.,
2011;
Söderlund
et
al.,
2007).
Uno
et
al.
(2006)
who
specifically
tested
the
effect
of
auditory
noise
on
CPT
performance,
found
that
ADHD
children
produced
fewer
omission
errors
in
the
presence
of
auditory
noise
than
in
the
no-noise
condition.
The
positive
effect
of
distracting
auditory
stimuli
on
the
cognitive
performance
of
ADHD
patients
is
usually
attributed
to
the
increased
arousal
provoked
by
a
novel
signal
(Uno
et
al.,
2006;
Van
Mourik
et
al.,
2007).
It
is
possible
that
distractors
in
the
MOXO-CPT
failed
to
improve
atten-
tion
in
ADHD
adolescents
because
of
the
little
information
they
conveyed
for
the
participant.
It
has
been
suggested
(Parmentier
et
al.,
2010)
that
the
degree
to
which
a
novel,
unexpected
auditory
sound
may
optimize
performance
depends
on
the
amount
of
infor-
mation
it
conveys.
When
a
novel
sound
predicts
another
relevant
stimulus,
the
system
can
take
advantage
of
the
auditory
distrac-
tors
to
improve
its
functioning.
In
contrast
to
other
CPT
(Uno
et
al.,
2006;
Van
Mourik
et
al.,
2007)
distractors
in
the
MOXO-CPT
did
not
precede
the
target
or
were
generated
stimulatingly
with
it,
but
rather
were
unsynchronized
with
it.
This
fact
may
lower
the
extent
to
which
the
sound
included
information
necessary
to
opti-
mize
performance
and
may
explain
why
auditory
distractors
did
not
improve
sustained
attention
in
our
study.
Several
limitation
of
this
study
should
be
considered.
First,
par-
ticipation
in
the
study
was
based
on
a
voluntary
agreement
of
children
and
their
parents.
This
self-selected
sampling
strategy
tends
to
be
biased
towards
favouring
more
cooperative
and
moti-
vated
individuals.
Therefore,
it
is
impossible
to
determine
whether
this
sample
also
represents
other
children
that
were
not
recruited
and
whether
cooperation
is
confounded
with
ADHD
variables.
This
limitation
is
typical
to
most
clinic-based
ADHD
studies
around
the
world
(Gau
et
al.,
2010;
Lee
and
Ousley,
2006).
In
addition,
the
clinics
from
which
ADHD
children
were
recruited
were
based
in
I.
Berger,
H.
Cassuto
/
Journal
of
Neuroscience
Methods
222 (2014) 62–
68 67
tertiary
care
hospital.
This
population
has
heterogeneous
back-
ground
characteristics
including
those
correlates
of
ADHD.
Finally,
the
exclusion
of
ADHD
children
with
severe
comorbidities
may
limit
the
generalization
of
our
results.
Overall,
our
findings
showed
that
independently
of
distractor
type,
ADHD
teenagers
were
more
distracted
than
healthy
con-
trols
during
CPT
performance,
ADHD
adolescents
produced
more
omission
errors
in
the
presence
of
visual
environmental
stimuli
or
the
combination
of
visual
and
auditory
stimuli
in
comparison
to
no-distractors
conditions.
In
terms
of
ADHD
diagnosis,
the
mere
presence
of
distractors
improved
the
utility
of
the
test
relative
to
no
distractors.
Visual
environmental
stimuli
emerged
as
better
distractors
than
auditory
ones
and
combining
visual
and
auditory
distractors
was
not
beneficial
in
terms
of
validity,
as
compared
to
pure
visual
dis-
tractors.
In
contrast
to
the
majority
of
cognitive
tasks,
distracting
stimuli
in
the
MOXO-CPT
were
external
to
the
task
(i.e.,
not
conflicting
with
task
demands).
The
fact
that
adolescents
with
ADHD
were
distracted
by
external
stimuli
suggests
that
in
everyday
life
these
individuals
may
be
more
distracted
by
irrelevant
stimuli
in
the
classroom
(e.g.,
someone
talks
in
the
next
room)
rather
than
back-
ground
stimuli
(e.g.,
music)
or
distractors
that
are
part
of
the
cognitive
task.
Hence,
reducing
irrelevant
environmental
stimuli
or
learning
how
to
regulate
their
influence
on
attention
functions,
may
assist
adolescents
with
ADHD
in
coping
with
distractibility
problems.
Finally,
this
study
lends
further
support
for
using
the
CPT
as
an
aiding
tool
in
the
diagnosis
of
ADHD
in
teenagers,
once
employ-
ing
appropriate
task
demands
that
better
simulate
distractibility
in
everyday
life.
Future
research
should
address
the
diagnostic
utility
of
the
test
in
larger
spectrum
of
age
and
in
different
populations
(e.g.,
ADHD
with
comorbid
features).
Another
question
that
should
be
further
explored
is
how
dis-
tractibility
is
marked
in
different
subtypes
of
ADHD.
Previous
studies
examining
ADHD
subtype
differences
in
neuropsycholo-
gical
functioning
are
limited
and
inconsistent
(Booth
et
al.,
2007;
Lockwood
et
al.,
2001;
Nikolas
and
Nigg,
2013;
Schwenck
et
al.,
2009)
It
has
been
long
debated
whether
one
category
is
capa-
ble
to
describe
the
high
heterogeneity
in
symptom
presentation
and
impairments
of
ADHD
(Nigg
et
al.,
2010).
Moreover,
it
is
still
unclear
whether
different
ADHD
subtypes
reflect
unique
configura-
tions
of
the
syndrome
or
simply
various
degrees
of
behavioural
and
neuropsychological
weaknesses
(Nikolas
and
Nigg,
2013).
Thus,
it
would
be
highly
important
to
examine
if
specific
subtypes
of
ADHD
are
more
distracted
than
others
(Keage
et
al.,
2006;
Mayes
et
al.,
2009).
While
some
authors
suggested
that
distractibility
relates
to
difficulty
in
response
inhibition
(Oades
et
al.,
2002)
and
therefore
characterizes
ADHD
predominantly
hyperactive
and
combined
subtypes
(Carlson
and
Mann,
2000;
Lahey
et
al.,
1997),
others
proposed
that
distractibility
has
more
to
do
with
inattentive-
ness
problems,
hence
is
more
expected
in
ADHD
predominantly
inattentive
subtype
(McBurnett
et
al.,
2001;
Milich
et
al.,
2001).
It
is
a
purpose
of
future
research,
and
beyond
the
scope
of
this
study,
to
explore
the
neuropsychological
correlates
of
distractibility
in
CPT
and
how
they
are
pronounced
in
different
ADHD
sub-
types.
Although
the
current
study
points
out
a
potential
association
between
distractibility
and
inattention,
the
effect
of
distractors
on
other
CPT
measures
(e.g.,
commission
errors)
is
equally
important.
Conflicts
of
interest
statement
Itai
Berger
serves
in
the
scientific
advisory
board
to
Neuro-Tech
Solutions
Ltd.
Hanoch
Cassuto
declared
no
potential
conflicts
of
interest
with
respect
to
this
study.
Acknowledgments
The
authors
wish
to
thank
Dr.
Ortal
Slobodin
for
her
efficient
help
and
skills
and
to
Merav
Aboud
and
Julia
Melamed
for
their
kind
and
professional
attitude
towards
the
participating
adolescents
and
their
families.
Appendix
A.
Supplementary
data
Supplementary
data
associated
with
this
article
can
be
found,
in
the
online
version,
at
http://dx.doi.org/10.1016/j.jneumeth.
2013.10.012.
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