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research-article2013
JADXXX10.1177/1087054713502079Journal of Attention DisordersHorowitz-Kraus

Article
Journal of Attention Disorders

Differential Effect of Cognitive Training on


2015, Vol. 19(6) 515­–526
© 2013 SAGE Publications
Reprints and permissions:
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DOI: 10.1177/1087054713502079

Children With ADHD and in Children With jad.sagepub.com

ADHD Comorbid With Reading Difficulties

Tzipi Horowitz-Kraus1,2

Abstract
The comorbidity of ADHD and reading difficulties (ADHD + RD) is believed to be a disability distinct from ADHD
alone, with unique challenges faced by individuals suffering from one disability versus the other. We aimed to examine
the differential effect of 8 weeks of cognitive training on reading abilities and on executive functions, through use of the
Wisconsin task, in children with ADHD and in children with ADHD + RD. Greater impairments in reading and executive
functions, especially in speed of processing, were found in the comorbid group at baseline. The comorbid group showed
greater improvements in most measures after training as well. We propose that the cognitive training used in the present
study affected not only the immediate abilities of executive functioning but also the secondary ability of reading, especially
in the comorbid group, by improving in particular, speed of processing. We suggest that a differential approach should be
taken when treating children with ADHD + RD versus treating ADHD children. (J. of Att. Dis. 2015; 19(6) 515-526)

Keywords
ADHD, executive functions, reading difficulties, training

Introduction processing (Willcutt, Doyle, Nigg, Faraone, & Pennington,


2005), working memory, shifting between tasks, inhibition
ADHD is a highly prevalent disorder estimated to affect a (Willcutt et al., 2001), verbal auditory working memory
range of 2.2% to 17.8% of school-aged children in the (Vakil, Blachstein, Wertman-Elad, & Greenstein, 2011),
United States and in Europe (Skounti, Philalithis, & and all timed executive functions (Katz, Brown, Roth, &
Galanakis, 2007). These individuals suffer from excessive Beers, 2011). They exhibit a greater reading impairment, in
inattention and impulsivity, starting in childhood and often decoding and orthographic tasks (Willcutt et al., 2005), and
persisting into adolescence and adulthood (Faraone, their reading impairment is accompanied by a phonologi-
Sergeant, Gillberg, & Biederman, 2003; Mannuzza, Klein, cal deficit (Purvis & Tannock, 2000). This group also is
Bessler, Malloy, & LaPadula, 1993). These impairments known to have greater psychological, behavioral, and emo-
result in an inability to sit still in class, a tendency to answer tional problems than RD and ADHD groups exhibits sepa-
questions before they have been fully asked, and to have rately, suggesting that ADHD + RD is a distinct disorder (for
difficulty in organizing oneself and one’s schoolwork, all of review, see Mattison & Mayes, 2012; Sexton, Gelhorn, Bell,
which contribute to academic failures and reading difficul- & Classi, 2011). We recently pointed at these distinct cogni-
ties (Greven, Rijsdijk, Asherson, & Plomin, 2012). Reading tive profiles using electroencephalogram (EEG) recordings
difficulties manifest mainly as inaccurate, slow reading and (Horowitz-Kraus, 2013): children with ADHD + RD
they are known to be related to deficits in executive func- showed smaller event-related potential (ERP) components
tions (Biederman et al., 2004; Jacobson et al., 2011). (Error-related Negativity, N100 and N400 components),
However, children who suffer from ADHD and reading dis-
abilities (i.e., children with an ADHD + RD comorbidity) 1
University of Haifa, Israel
exhibit more severe deficits in all domains than do children 2
Cincinnati Children’s Hospital Medical Center, OH, USA
with only ADHD (Rucklidge & Tannock, 2002).
Specifically, ADHD + RD children experience more severe Corresponding Author:
Tzipi Horowitz-Kraus, Cincinnati Children’s Research Foundation,
deficits than ADHD children in a number of executive func-
Pediatric Neuroimaging Research Consortium, 3333 Burnet Ave.,
tions: naming (Rucklidge & Tannock, 2002), speed of Cincinnati, OH 45229-3039, USA.

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516 Journal of Attention Disorders 19(6)

accompanied by lower executive function and reading abili- ADHD symptoms in children (aged 8-12 years) with ADHD
ties, as compared with ADHD children. We concluded that who underwent an executive functions training intervention
the executive processes in the comorbid group are more for 9 weeks, as compared with their ADHD peers in the
impaired than in the ADHD group, resulting in lessened waiting-list group (Green et al., 2012). The researchers
error-detection activation in reading and in impaired speed pointed at the effect of computerized games to increase the
of processing. The lower error-detection activation in read- motivation and engagement of participants, especially for
ing, thought to imply a lower awareness of reading errors, children with ADHD (Green et al., 2012). Gray et al. (2012)
might be one of the causes of the major impairment in read- showed that a working-memory training program for ado-
ing abilities in general (Horowitz-Kraus, 2013). The speed lescents (12-17 years old) with ADHD and learning disabil-
of processing deficits represent a longer time that elapses ity (LD) improved their working-memory, attention and
between the presentation of an external stimulus and a par- academic achievement (reading and math) as compared
ticipant’s response to it (Kail, 1991), which also could affect with those in an ADHD + LD group that trained in math.
overall reading abilities negatively. In light of these find- This study’s results conflicted with those of Green et al.
ings, and because pharmaceutical intervention (i.e., stimu- (2012), which found no effect on attention and academic
lant medication) is not always accepted by parents for measures in the ADHD group. Despite these research done
treatment of their children (see Hodgson, Hutchinson, & in this field, we have not found a study specifically compar-
Denson, 2012), and is not in favor for treating reading dif- ing the differential effect of executive functions training on
ficulties specifically (Antigas-Pallares, 2009), the present executive and reading measures between children with
study aims to find the differential effect of a cognitive train- ADHD + RD and children with only ADHD.
ing intervention on executive functions, as well as its effect The present study aimed to explore the effects of an
on reading measures, in children with ADHD + RD as com- 8-week executive functions training program on executive
pared with children with ADHD. functioning (immediate effect) and reading (near effect) mea-
Nonpharmacological interventions are becoming more sures in children with ADHD + RD and in children with
widely used for children with various learning disorders ADHD alone. We used the “Cognifit” game-based program
(Hodgson et al., 2012), as parents, children, and clinicians (CogniFit Ltd, 2008; see “Method” section). Executive abili-
are less willing to use medications (stimulants) for a child’s ties before and after training were measured using a comput-
treatment (Donnelly, Haby, Carter, Andrews, & Vos, 2004). erized version of the traditional Wisconsin task (see “Method”
Studies have examined the effect of cognitive training, but section), which has been shown to evaluate measures of
these have mostly been focused on children with ADHD executive functions effectively (Kimberg, D’Esposito, &
or with ADHD + RD/learning difficulties separately. Farah, 1997; Lezak, 1995; Milner, 1963). Reading ability
Intervention programs designed specifically to affect the was measured using standardized reading tests.
executive functions are important because of the known
strong negative associations between executive functions
and ADHD symptoms, psychopathology symptoms and Method
social problems (see Mattison & Mayes, 2012). Green and
Participants
colleagues (2012) showed that children with ADHD who
participated in an executive function (specifically, working This study included 28 age-matched participants (14 chil-
memory) training program for 25 days (90 sessions) showed dren diagnosed with ADHD, mean age 12.92 ± .65 years,
a significant decrease in ADHD symptoms and an increase 14 males), and 14 with ADHD + RD (the comorbid group;
in working-memory measures, as compared with the pla- mean age 13.19 ± .75 years, 12 males, 2 females); t(26) =
cebo-treatment group. The authors suggested that the pro- −1.02, ns, all matched for nonverbal IQ (90 and above) as
gram used in their study activated the prefrontal cortex, measured by the Raven Standard Progressive Matrices
which could lead to these generalized effects. Beck, Hanson, (Raven, 1969). All were native Hebrew speakers from a
Puffenberger, Berninger, and Berninger (2010) showed middle-class background, right-handed, with normal or
improvements in executive functions and attention symp- corrected-to-normal vision in both eyes, and all were found
toms in ADHD + RD participants following a working- to have normal hearing. We used the Conners’ Rating scale
memory training, as compared with a group of children for teenagers to match the participants for their attention
with ADHD + RD who did not undergo the training (a wait- scores, t(26) = .327, ns, and for their performance relative
ing-list group). In a meta-analysis study, Hodgson et al. to normal (Conners, 1989). All participants met the defini-
(2012) suggested that neurofeedback training reduced tion of ADHD as described in the Diagnostic and Statistical
ADHD symptoms in an experimental group as compared Manual of Mental Disorders (4th ed.; DSM-IV; American
with nontrained children with ADHD. Highlighting the role Psychiatric Association, 1994). No differences were found
of executive functions in ADHD, a pilot study demonstrated on attention measures between the females and the males
an increase in executive functions scores and a decrease in in the study.

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Horowitz-Kraus 517

Participants signed assents and their parents provided California). The MCST stimulus material consists of 24
written informed consent prior to the study. Both groups choice-cards that are to be matched during each trial with
were diagnosed as having ADHD or ADHD + RD at least 2 one of four target-cards, based on one of three stimulus
years prior to the study, with ADHD being the primary diag- dimensions, or “rules”: color, shape, or number of items on
nosis in both groups of participants. Diagnoses were veri- the card (see Horowitz-Kraus, 2012, for an illustration).
fied by a score of −1.5 or below on a standardized 1-min MCST stimuli were all presented at a visual angle of 4°
word reading test and through a normative reading battery, horizontally and 3.5° vertically, and remained on the screen
involving text read orally, which tests for accuracy and flu- until the participant responded. The colored geometrical
ency (Shany, Lachman, Shalem, Bahat, & Zeiger, 2006). figures were outlined in black against a white background
ADHD diagnoses were verified by a score of 6 out of 9 or and were identical in luminance. The trials, totaling 137,
more, for characteristics of ADHD existing for more than 6 were semirandomly arranged into 18 series, each marked
months, using the Conners’ attention/hyperactivity ques- by a new “rule,” and varying in length from 6 to 8 trials per
tionnaire (Conners, 1989). All participants attended a junior series, to avoid rule-switch anticipation. The correct sort-
high school for students with learning disabilities. Students ing rule was determined by an auditory cue delivered
were not medicated during training. within 1,500 to 2,000 ms after a participant’s response (200
ms duration, 10 ms rise/fall times; 65 dB SPL; 1000 Hz for
“stay” cues, 500 Hz for “shift” cues). Hence, each correct
Procedures trial was followed by a “stay” cue, and each error trial was
Participants were assessed within their school. Tests were followed by a “shift” cue. After a varying number of cor-
administered individually in a schoolroom, after school rect responses, the rule changed unpredictably, and the par-
hours, by the research team. The study was reviewed and ticipant had to adjust to the new rule (e.g., from shape to
approved by the Ethics Committee of the University of color, or from color to number, etc.). There was a fixed
Haifa. interval of 1,400 ms between the feedback onset and the
onset of the next trial. The full MCST design used in this
study is depicted in Horowitz-Kraus, 2012, modeled after
Behavioral and Experimental Measures Barcelo (2003).
Behavioral measures.  Ten tests were administered to mea- Mean reaction times and mean accuracy rates were
sure reading and executive functions in the two groups. obtained from correct and error trials. Error trials were ones
Reading ability was measured by several subtests: (A) in which the participant failed to select the correct target
decoding—1-min word test for children (Shany et al., response when the rule changed, or when the participant
2006), (B) oral reading task (Shany et al., 2006), (C) Read- failed to follow the instruction to switch or repeat the previ-
ing comprehension task (Shatil, Nevo, & Breznitz, 2008), ous trial. Shift trials were divided into two types of shifts:
and (D) orthographic automaticity (Parsing test; Breznitz, (a) first shift, in which the first cue announced the change in
1997). Executive functions were measured by (A) short- rule, and (b) second shift, in which the second cue announced
term memory and capacity—digit span subtest from the the change in rule (Barcelo, 2003).
Wechsler Adult Intelligence Scale-Third Edition (WAIS-III;
Wechsler, 1997), (B) grapho-motor speed of processing—
the coding subtest of the WAIS-III (Wechsler, 1997), (C)
Executive Functions Training
visual speed of processing—the symbol search subtest of Auditory, visual, and cross-modality working-memory
the WAIS-III (Wechsler, 1997), (D) naming ability (letters skills—naming, speed of processing, inhibition, simple reac-
and Rapid Alternating Stimulus naming; modeled after tion times, flexibility, divided attention, spatial ability, shift-
Denckla & Rudel, 1976; Wolf, Bally, & Morris, 1986) and ing, and attention—were all trained using the CogniFit
(E) spatial ability (CogniFit Ltd, 2008). Measures for gen- Personal Coach (CPC) Computerized Cognitive Program
eral ability, attention, reading, and word recognition were (CogniFit Ltd, 2008). This program includes a baseline cog-
administered prior to the experiment to verify each partici- nitive assessment (T1) that allows the training program to be
pant’s reading level, IQ, and attention ability. Each behav- individualized for each participant. Normative data from a
ioral testing session lasted approximately 1.5 hr. large database of previous users define the initial challenge
level of each of the training games/tasks used. Each training
Experimental measure: The Madrid Card-Sorting Test session includes a mixture of games/tasks aimed at training
(MCST). Executive abilities were examined using the executive functions. Each of the games/tasks has three levels
MCST, which is a computerized version of the traditional of difficulty—easy, moderate, and difficult. The training pro-
task-cuing Wisconsin Card Sorting Test (WCST; adapted gram and the level of the complexity within each domain
from Barcelo, 2003). Stimuli were presented by Presenta- were created for each participant according to a personal
tion software (Neurobehavioral Systems Inc., Albany, “Scheduled Training Option” (CogniFit Ltd, 2008), which

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518 Journal of Attention Disorders 19(6)

Table 1.  Means, Standard Deviations, and Results of t-Test for Reading Before (Test 1) and After (Test 2) Training.

T1 T2

  ADHD (A) ADHD + RD (B) ADHD (C) ADHD + RD (D)  

Test M (SD) M (SD) M (SD) M (SD) t-value Contrasts


Decoding— Accuracy 53.1 (27.47) 33.8 (17.47) 59.61 (31.05) 36.93 (19.68) 2.083* A>B
(number of correct
words per minute)
Fluency—Speed (seconds 1.1 (.85) 1.7 (1) 0.95 (.59) 1.19 (.633) −2.596* D<B
per word in oral text
reading)
Fluency—Accuracy 11.15 (7.88) 20.27 (15.45) 9.3 (4.46) 16.63 (16.67) 2.13* D<B
(number of errors in
the passage, out of 292
words)
  −2.05* B>A
Reading comprehension— −1.91 (2.41) −3.89 (3) −1.46 (2.85) −3.33 (3.15) 1.75* A>B
Accuracy (standard
score)
Orthography— Parsing 10.33 (4.59) 10.17 (4.1) 10.77 (6.33) 8.8 (4.11)  
speed (time in sec per
item)

*p < .05. **p < .01. ***p < .001.

was based on the participant’s performance on the baseline maze as fast as possible. An important feature of the
assessment. The level of challenge was further readjusted overall program is the Personal Coach, which offers
after each training session according to the participant’s insights and advice based on data from several ses-
progress. Each training session took 15 to 20 min. At the sions. For example, if a participant exhibits good
beginning of each task, the user read a description of the main visual memory abilities but poor auditory memory
cognitive skills that were being trained in that task and at the abilities, the Personal Coach will comment on the
end of each day’s training, the user could examine his or her skill difference and advise the participant to pay
performance on graphs that described his or her progress. special attention to auditory memory tasks.

Examples of the cognitive tasks used in the CPC program


Research Design and Procedure 
1. Visual memory task: Windows of an on-screen General ability, attention, reading, and word-recognition
house open in a certain sequence. The participant is tests were administered prior to the experiment to verify
asked to follow the exact sequence in which the that both groups met the criteria for ADHD and that the
windows open, and the length of the sequence varies children in the ADHD + RD group also met the criteria for
from task to task. reading difficulty (−1.5 standard score and below on stan-
2. Cross-modality memory task: Pictures and sounds dardized word and contextual reading tasks; see Shany et
of objects are presented to the participant sequen- al., 2006). In general, each behavioral testing session lasted
tially. The participant then has to recognize the approximately 1.5 hr (Table 1).
objects from an assortment of images, and recall During the experiment, the participant was seated in an
whether it was previously presented visually or isolated, sound-attenuated room. No interaction took place
auditorally. between the participant and experimenter during the WCST
3. Attention split task: The participant is presented administration. Visual stimuli were presented on a com-
with billiard balls, on two separate on-screen boards, puter screen located 1 m in front of the participant. Auditory
moving from one side of the screen to the other in stimuli (the feedback “correct” for “stay” or “wrong” for
different directions. The participant must click on “shift” in the WCST, and other auditory stimuli in the CTC
the balls before they hit the walls of the two boards. program) were presented via headsets from the computer at
4. Spatial perception task: The participant is presented a frequency of 2000 Hz. Participants then started their exec-
with a maze and must find his or her way in the utive functions training. All participants trained for 8 weeks,

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Horowitz-Kraus 519

Figure 1.  Accuracy rate (in percentage) for each stage of the Wisconsin task in individuals with ADHD before (Test 1) and after
(Test 2) training interventions.
Note. Figure 1 depicts accuracy rates (in percentage) and standard deviations before (Test 1, blue bars) and after (Test 2, red bars) training for individu-
als with ADHD in each stage of the Wisconsin task. The equations for the linear regression lines are listed in the bottom right corner (blue equation =
before training; red equation = after training).

Figure 2.  Accuracy rate (in percentage) for each stage of the Wisconsin task in individuals with ADHD + RD before (Test 1) and
after (Test 2) training interventions.
Note. Figure 2 depicts the accuracy rates (in percentage) and standard deviations before (Test 1, blue bars) and after (Test 2, red bars) training for indi-
viduals with ADHD + RD in each stage of the Wisconsin task. The equations for the linear regression lines are listed in the bottom right corner (blue
equation = before training; red equation = after training).

3 times per week, 15 to 20 min per training session on a by the Bonferroni method for multiple comparisons (α <
personal computer (for a total of 24 sessions). After com- .05). Regression analysis was also applied within groups to
pletion of the training, the participants were tested with the determine the differences in learning curves after training.
executive functions and reading batteries (see Table 1) and To verify the differences in variance between the partici-
on the Wisconsin task. This session lasted about 1.5 hr. pants before and following intervention, four paired t-test
analyses were conducted separately using the standard
deviation scores, for accuracy and for reaction times, for
Statistical Analysis each stage in the Wisconsin task for the two groups sepa-
Behavioral data (see “Behavioral measures” section rately. As the different reading and executive measures
description) were analyzed using independent t-test analy- assess different aspects (e.g., in reading: decoding task
ses. We used paired and independent t-test analyses to ana- measures phonological ability, Parsing—orthographical
lyze the Wisconsin task data before and after training ability, Oral reading—fluency and comprehension; in exec-
(Figures 1-4). Family-wise Type I error rates were corrected utive functions: the different subcomponents of the naming

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520 Journal of Attention Disorders 19(6)

Figure 3.  Reaction times (in ms) for error responses for each stage of the Wisconsin task in individuals with ADHD before (Test 1)
and after (Test 2) training interventions.
Note. Figure 3 depicts reaction times (in ms) and standard deviations for error responses on each stage of the Wisconsin task before (Test 1, blue
bars) and after (Test 2, red bars) training, for individuals with ADHD. The equations for linear regression lines are listed in the bottom right corner
(blue equation = before training; red equation = after training).

Figure 4.  Reaction times (in ms) for error responses at each stage of the Wisconsin task in individuals with ADHD + RD before
(Test 1) and after (Test 2) training interventions.
Note. Figure 4 depicts reaction times (in ms) and standard deviations for error responses at each stage of the Wisconsin task before (Test 1, blue
bars) and after (Test 2, red bars) training, for individuals with ADHD + RD. The equations for the linear regression lines are listed in the bottom right
corner (blue equation = before training; red equation = after training).

task examine different aspects, see Norton & Wolf, 2012), functions (see “Behavioral measures” section, executive
Pearson correlation was used to find associations between function measures, Variables A-E). Family-wise Type I
improvements in reading (see “Behavioral measures” sec- error rates were corrected by the Bonferroni method for
tion, reading measures, Variables A-D,) and in executive multiple comparisons (α < .05)

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Horowitz-Kraus 521

Table 2.  Means, Standard Deviations and Results of t-Test for Executive Functions Before (Test 1) and After (Test 2) Training.

T1 T2

  ADHD (A) ADHD + RD (B) ADHD © ADHD + RD (D)  

Measure M (SD) M (SD) M (SD) M (SD) t-value Contrasts


Naming—RAS (time is seconds) 37.68 (9.38) 44.98 (7.12) 35.3 (10.2) 41.81 (7.31) −1.884* A<B
Naming—Letters (time is 34.14 (6.87) 40.46 (5.93) 30.53 (7.17) 35.63 (4.36) 3.09** A>C
seconds)
  2.9* B>D
  −2.048* B>A
Symbol search (standard score) 6.23 (2.2) 4.72 (2.14) 7.53 (2.96) 5.45 (2.58) −2.623* C>A
Symbol search (number of 23.46 (5.63) 20.81 (3.99) 27 (5.61) 24.63 (4.24) −2.822* C>A
correct responses)
  −3.464* D>B
Digit span (standard score) 5.38 (2.56) 4.36 (1.91) 6.38 (2.56) 4.18 (2.71) −2.55* C>A
Digit span forward (highest 5.3 (.63) 5.09 (1.04) 5.3 (.63) 4.72 (.78)  
number of digits reached)
Digit span backwards (highest 3.53 (0.87) 3.36 (0.8) 4 (0.81) 3.81 (1.07) −2.144* C>A
number of digits reached)
Digit symbol (standard score) 5.3 (1.97) 3.27 (1.73) 5.23 (3.94) 3.63 (1.68) 3.002** A>B
Digit symbol (number of 40.46 (8.32) 32.63 (7.44) 42.76 (15.61) 37.27 (5.83) −2.519* D>B
correct responses)
  2.846** A>B
Spatial perception (standard 0.83 (1.09) 0.86 (1.58) 0.81 (0.94) 1.54 (1.14) −2* D>B
score)

*p < .05. **p < .01. ***p < .001.

Results Executive functions. Between-group analyses showed that


children with ADHD + RD showed improved speed of pro-
Baseline Behavioral Measures (Test 1) cessing measures after the intervention (e.g., faster naming
Reading. In general, children with ADHD + RD showed letters, and greater accuracy in symbol search and digit
greater difficulties in several reading measures (signifi- symbol) and better spatial perception scores. Children in the
cantly less words were read accurately, lower comprehen- ADHD group showed improved memory measures as well
sion scores were achieved, and a trend of slower and as an improvement in parts of the speed of processing mea-
less-accurate oral reading was observed) than children with sures (faster letter naming, and greater accuracy and stan-
ADHD (Table 1). dard score in symbol search; Table 2).
After intervention, baseline differences between the
Executive functions. Participants with ADHD + RD were ADHD and ADHD + RD children in words reading and
also significantly slower than the ADHD group in parts of reading comprehension disappeared, as was observed in the
the speed of processing battery (naming letters and naming between-group comparisons analysis. Also, no differences
rapid alternating stimulus test [RAS] speed and coding in speed for naming RAS and letters, or in digit symbol,
test). Although in some cases the ADHD + RD group exhib- were observed after training between the two groups.
ited lower scores than the ADHD group (symbol search,
digit span, and spatial perception), no significant differ- The Effect of Executive Functions Training on
ences were found in these parameters (i.e., which are listed Performance in the Wisconsin Task
in the parentheses) between the groups (Table 2).
Accuracy rate. Overall, both groups demonstrated a higher
learning curve along the Wisconsin task, which can be seen in
The Effect of Intervention (Test 2) the positive slope of the linear regression line. No significant
Reading. Children in the ADHD + RD group showed an differences in accuracy were found within the groups or
increase in speed and accuracy in oral reading following between groups before or after the executive training. No dif-
training, whereas the ADHD group showed no significant ferences in standard deviations before and after intervention
effect in reading measures (Table 1). were found within the groups (see Figures 1 and 2 and Table 3).

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522 Journal of Attention Disorders 19(6)

Table 3.  Mean Accuracy Rate (in Percentage) on the Wisconsin Task for Children With ADHD as Compared With Children With
ADHD + RD Before (Test 1) and After (Test 2) Executive Training.

Correct responses (%) T1 Correct responses (%) T2

  ADHD (A) ADHD + RD (B) ADHD (C) ADHD + RD (D)

Trial number M (SD) M (SD) M (SD) M (SD)


First shift 11.72 (7.02) 13.58 (6.27) 8.33 (10.22) 6.66 (6.82)
Second shift 36.11 (10.39) 39.31 (11.44) 37.77 (12.5) 40 (17.52)
Stay-1 59.92 (16.03) 60.25 (17.19) 63.88 (57.22) 57.22 (19.6)
Stay-2 68.65 (12.05) 67.09 (17.19) 73.88 (16.77) 65 (18.71)
Stay-3 67.46 (16.71) 70.08 (16.59) 72.77 (12.68) 72.22 (17.37)
Stay-4 66.66 (19.73) 73.93 (13.10) 72.22 (16.71) 82.33 (13.35)
Stay-last 70.96 (17.76) 74.16 (15.37) 84.48 (12.18) 82.04 (11.32)

Note. M = mean (in percentage).

Table 4.  Mean Reaction Times (ms) for Error Responses on the Wisconsin Task for Children With ADHD as Compared With
Children With ADHD + RD, Before (Test 1) and After (Test 2) an Executive Training Intervention.

Reaction times (ms) T1 Reaction times (m) T2

  ADHD (A) ADHD + RD (B) ADHD (C) ADHD + RD (D)  

Trial number M (SD) M (SD) M (SD) M (SD) t-value Contrasts


First shift 2,902.94 (2,838.49) 3,6663.25 (3,679.39) 1,702.86 (357.62) 1,684.82 (367.87) −.01* B>A
  2.127* A>C
Second shift 6,003.07 (5,564.31) 3,371.97 (1,740.2) 2,304.64 (427.03) 2,308.38 (778.24) −.013** B>A
  2.649* B>D
Stay-1 2,548.77 (1,079.72) 3,112.05 (1,768.99) 2,245.56 (605.27) 1,992.57 (663.31)  
  2.558* B>D
Stay-2 2,928.82 (2,714.95) 2,175.54 (979.3) 2,487.5 (1,389.38) 1,976.58 (884.46) .91* A>B
Stay-3 2,857.12 (1,668.56) 4,265.19 (3,779.29) 2,302.15 (1,203.87) 2,026.85 (808.08) −1.269* B>A
  2.009, p = .084 B>D
Stay-4 1,984.32 (1,013. 3,666.39 (3,762.36) 2,182.81 (773.47) 1,960.15 (907.4) −1.613* B>A
Stay-last 3,129.2 (1,680.28) 3,469.31 (2,595.4) 2,026.18 (1,101.82) 2,192.67 (844.7) 2.938** A>C
  1.958, p = .091 B>D

Note. The results from t-test analyses are presented in the right column.
*p < .05. **p < .01. ***p < .001.

Reaction times.  At baseline (Test 1), results indicate shorter remained the same (a gap of definite value 10; Table 4,
reaction times for errors in children with ADHD + RD in Figures 3 and 4). Paired t-test analyses revealed significant
most stages of the Wisconsin task, except for the last stage, differences in standard deviations (standard deviations
as compared with the ADHD group. After training (Test 2), decreased at Test 2 in both groups) before and after inter-
these differences between the groups disappeared. More- vention, in children with ADHD (p < .05) and in children
over, after training (Test 2), decreased reaction times in the with ADHD + RD (p < .01).
ADHD group were found for the first and last stages,
whereas children in the ADHD + RD group showed
Correlations Between Reading and Executive
decreased reaction times in the second shift, the first time
they were expected to provide a correct response (stay-1), Measures
and a nonsignificant decreased reaction times in the first- The significant correlations between reading measures (see
shift and stay-last stages. Differences were found in the “Behavioral measures” section, reading measures, Variables
slope of the linear regression line between Tests 1 and 2 A-D), and executive function measures (see “Behavioral mea-
within the two groups, though the gap between the groups sures” section, executive function measures, Variables A-E)

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Horowitz-Kraus 523

in the two groups suggested that increased reading speed Although we saw improvement in speed of processing in
was associated with faster speed of processing (RAS naming both groups and improvement in working memory in the
time: r = −.499, p < .01; naming-letters time: r = −.443, p < ADHD group, we did not see a resulting improvement in
.05) and with better memory skills (digit span: r = .543, p < accuracy on the Wisconsin task following intervention in
.01) in both groups. Also, having slower naming time was either group. We did, however, find decreased reaction
associated with increased errors on the RAS naming task times for both groups after intervention. Even more, in
(RAS naming time: r = −.567, p < .01; RAS naming errors: addition to the general decrease in reaction times, we
r = .478, p < .01; naming-letters time: r = −.52, p < .01). observed a trend of decrease in the variability of the reac-
tion time’s standard deviation within each group. While we
observed differential effects of the training program
Discussion
between groups, each might still contribute to the same gen-
In light of the differences in reading abilities, executive eral effect of decreased variability in reaction times.
functioning and psychological abilities previously found Specifically, we postulate that the ADHD + RD group might
between ADHD and ADHD + RD children, the present benefit from faster speed of processing specifically on the
study aimed to find the differential effect of an executive Wisconsin task, when the participant is asked to screen
functions-based intervention on these measures in these cards and to look for the correct match in a fast and efficient
groups. We also found that these groups differ in their base- way. However, children in the ADHD group might benefit
line reading and executive abilities, and that children with from a combination of faster speed of processing and more
ADHD + RD experience more severe deficits in these efficient working memory, which might help them remem-
realms than do children with ADHD alone, which supports ber the unique rule being applied in each trial of the WCST,
findings from previous research. This trend was observed and thereby respond faster. Further study using EEG and
along all the examined abilities, though some did not reach ERPs methodology would enable us to segment the differ-
statistical significance. The most pronounced significant ent cognitive stages used during the Wisconsin task, to ver-
difference between the groups’ performances on the ify this point (see Horowitz-Kraus, 2012, as a model for this
Wisconsin task was in their reaction times, rather than in suggested design).
what we anticipated, accuracy. We previously demonstrated It is important to consider the total score of a given
that reaction time is actually the result of several subcompo- task, as opposed to overvaluing the absolute number of
nents of the executive system: perception, early attention, correctly answered items. For example, the standard score
working memory, speed of processing and shifting from the symbol search battery is calculated as the total
(Horowitz-Kraus, 2012). Indeed, in the present study we number of correct responses and the subtraction of the
observed significantly slower speed of processing and error responses. When looking only at the standard scores,
working-memory abilities in the ADHD + RD group as no significant effect was found in the ADHD + RD group
compared with the ADHD group. The present findings, following training. However, a significant effect of train-
therefore, support the previously proposed explanation, that ing was found when counting only the number of correct
these executive function deficits might contribute to the responses (the ADHD + RD group showed a greater num-
ADHD + RD group’s significantly slower reaction times. ber of correct responses). A similar effect was observed in
The executive functions are the foundation of proper the digit-symbol subtest, which also represents speed of
reading abilities (Jerman, Reynolds, & Swanson, 2012). processing. This might be due to the low sample size of
Therefore, it is not surprising that this executive functions this present study. It does, however, point to the value in
training program, which resulted in increased speed of pro- examining subcomponents of an overall effect of a certain
cessing and memory abilities in the ADHD group and faster intervention program, to provide a more sensitive obser-
speed of processing and better spatial abilities in the ADHD vation of the effect.
+ RD group, also diminished the gap in reading ability and The present study provided further evidence for differ-
reading comprehension between the two groups. Efficient ences in the executive functioning and academic abilities
speed of processing serves reading ability, as words can be between ADHD + RD and ADHD children, at baseline and
decoded in a more efficient way without overloading one’s following the intervention, thereby supporting the assump-
working memory (Breznitz & Misra, 2003). Then more tion that ADHD + RD is a disability with a unique set of
attention resources are available to comprehend the verbal characteristics (de Jong, Oosterlaan, & Sergeant, 2006;
information. Indeed, speed of processing and working-mem- Rucklidge & Tannock, 2002). We also demonstrated that
ory measures were found to be correlated with reading abil- the foundation of the reading process lies in the executive
ity in both groups. These findings are in line with the findings functions, and especially in speed of processing. Therefore,
of Green et al. (2012), who found an improvement in execu- this study supports the use of executive functions training
tive functions, which was accompanied by an increase in improve immediate measures (i.e., executive functions) as
reading achievements in an ADHD + RD population. well overall reading abilities.

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524 Journal of Attention Disorders 19(6)

To conclude, the present study adds validity to the litera- was different from the effect on those with only ADHD. A
ture examining the Wisconsin task as an evaluation of execu- future study should enroll an additional group of children
tive functions. The results of the present study show that even with only RD, as well as a nonclinical group of children, to
while looking at two closely related disorders, this task makes better understand if ADHD + RD involves a separate etiol-
it possible to determine differences in specific areas of execu- ogy than RD and how ADHD + RD and ADHD differ from
tive functioning. The use of the WCST here also helps in sup- a nonclinical group. Studies using imaging data (EEG and
porting the effectiveness of our 8-week executive functions ERPs methodology), which have the ability to map cogni-
intervention program (smaller standard deviation scores were tive functioning to a certain stage in a given task, will be
achieved following intervention). An executive functions able to better explain which cognitive improvement con-
training program might be the right approach for children tributed to a better performance on the WCST. Last but not
with ADHD, who suffer primarily from an executive impair- the least, while researchers and practitioners would proba-
ment (Biederman et al., 2004), and it has demonstrated effec- bly be delighted by the prospect of an effective cognitive
tiveness for children with ADHD + RD. intervention for ADHD, they recognize that the weight of
However, the ADHD and ADHD + RD groups benefit- the existing evidence favors pharmacological interventions
ted differently from the same intervention, and the differen- for treatment of the core symptoms of ADHD. Whether
tial effect should be taken into consideration by clinicians promising cognitive training approaches can serve as a
and educators when determining the appropriate interven- substitute for pharmacological intervention or are better
tions for a child. Each child’s unique cognitive abilities and conceived as an adjunct approach is an unresolved ques-
challenges should be taken into account, and our results tion that demands more intensive research, including ade-
here can improve a clinician’s ability to factor a child’s indi- quate group sizes, and spanning years representative of a
vidual situation into treatment options and decisions. range of developmental stages.
Overall, this work strongly supports our hypothesis that
ADHD and ADHD + RD are unique diagnoses, and that Acknowledgments
researchers and clinicians should be careful not to combine The author would like to thank Professor Zvia Breznitz, PhD, for
individuals from these two groups into one. Early identifi- her mentorship and her help in designing the present study.
cation of ADHD and/or ADHD + RD is an important future
direction for research and clinical implication as well, as Declaration of Conflicting Interests
intervention programs like the WCST can be started early in
The author(s) declared no potential conflicts of interest with
life, to establish a solid foundation for reading abilities that respect to the research, authorship, and/or publication of this
affect the futures and lives of such children (Diamond & article.
Lee, 2011).
These conclusions should be taken into account with the Funding
present study’s limitations. First, we worked with a rela-
The author(s) disclosed receipt of the following financial support
tively small sample size. This small sample size prevented for the research, authorship, and/or publication of this article: The
us from achieving differential significance when conduct- present study was supported by the Edmond J. Safra Foundation.
ing a Group × Test Repeated Measures Analysis of Variance,
as we originally did, and limited us to a main effect of inter- References
vention (data not shown). Also, the inclusion of only two American Psychiatric Association. (1994). Diagnostic and statisti-
females in the ADHD + RD group, which was not an equal cal manual of mental disorders (4th ed.). Washington, DC:
number to the males, is a drawback. This study did not use Author.
any technique (e.g., ERPs) that enabled us to conclude Antigas-Pallares, J. (2009). Pharmacological treatment of dys-
which improved executive abilities affected the change in lexia. Revista de Neuroligia, 48, 585-591.
reaction times on the WCST. Finally, because the focus of Barcelo, F. (2003). The Madrid card sorting test (MCST): A task
the present study was to look at the differences between the switching paradigm to study executive attention with event-
ADHD + RD and the ADHD groups, we did not include a related potentials. Brain Research Protocols, 11, 27-37.
group of children only experiencing reading difficulties or Beck, S. J., Hanson, C. A., Puffenberger, S. S., Berninger, K.
even a nonclinical group of children. L., & Berninger, W. B. (2010). A controlled trial of work-
ing memory training for children and adolescents with
Therefore, we are unable to conclude whether either
ADHD. Journal of Child and Adolescents Psychiatry, 39,
group showed significant impairment relative to a norma- 825-836.
tive group for any measure. We did, however, use normal- Biederman, J., Monuteaux, M. C., Doyle, A. E., Seidman, L. J.,
ized tests in this study, to be able to describe the performance Wilens, T. E., Ferrero, F., . . .Faraone, S. V. (2004). Impact of
of each group in relation to generalized normative data. executive function deficits and attention-deficit/hyperactivity
The present study’s results allow us to conclude that the disorder (ADHD) on academic outcomes in children. Journal
effect of the intervention on children with ADHD + RD of Consulting and Clinical Psychology, 72, 757-766.

Downloaded from jad.sagepub.com at UNIV NEBRASKA LIBRARIES on October 9, 2015


Horowitz-Kraus 525

Breznitz, Z. (1997). Enhancing the reading of dyslexic children Jacobson, L. A., Ryan, M., Martin, R. B., Ewen, J., Mostofsky,
by reading acceleration and auditory masking. Journal of S. H., Denckla, M. B., & Mahone, E. M. (2011). Working
Educational Psychology, 89, 103-113. memory influences processing speed and reading fluency in
Breznitz, Z., & Misra, M. (2003). Speed of processing of the ADHD. Child Neuropsychology, 17, 209-224.
visual–orthographic and auditory-phonological systems in Jerman, O., Reynolds, C., & Swanson, H. L. (2012). Does growth
adult dyslexics: The contribution of “asynchrony” to word in working memory span or executive processes predict
recognition deficits. Brain and Language, 85, 486-502. growth in reading and math in children with reading disabili-
CogniFit Ltd. (2008). CogniFit Personal Coach (CPC) training ties? Learning Disability Quarterly, 35, 144-157.
program and database. Yokneam, Israel: Author. Kail, R. (1991). Developmental changes in speed of processing
Conners, C. K. (1989). Conners Rating Scales’ manual. North during childhood and adolescence. Psychological Bulletin,
Tonawanda, NY: Multi-Health System. 109, 490-501.
de Jong, C. G. W., Oosterlaan, J., & Sergeant, J. A. (2006). The Katz, L. J., Brown, F. C., Roth, R. M., & Beers, S. R. (2011).
role of double dissociation studies in the search for candi- Processing speed and working memory performance in those
date endophenotypes for the comorbidity of attention deficit with both ADHD and a reading disorder compared with those
hyperactivity disorder and reading disability. International with ADHD alone. Archives of Clinical Neuropsychology, 26,
Journal of Disability, Development and Education, 53, 425-433.
177-193. Kimberg, D. Y., D’Esposito, M., & Farah, M. J. (1997). Frontal
Denckla, M. B., & Rudel, R. G. (1976). Rapid automatized nam- lobes: Neuropsychological aspects. In T. E. Feinberg & M.
ing (RAN): Dyslexia differentiated from other learning dis- J. Farah (Eds.), Behavioral neurology and neuropsychology
abilities. Neuropsychologia, 14, 471-479. (pp. 409-418). New York, NY: McGraw-Hill.
Diamond, A., & Lee, K. (2011). Interventions shown to aid execu- Lezak, M. D. (1995). Neuropsychological assessment. New York,
tive function development in children 4 to 12 years old. NY: Oxford University Press.
Science, 19(vol. 333): 959-964. Mannuzza, S., Klein, R. G., Bessler, A., Malloy, P., & LaPadula,
Donnelly, M., Haby, M. M., Carter, R., Andrews, G., & Vos, T. M. (1993). Adult outcome of hyperactive boys. Educational
(2004). Cost-effectiveness of dexamphetamine and meth- achievement, occupational rank, and psychiatric status.
ylphenidate for the treatment of childhood attention deficit Archives in Genetic Psychiatry, 50, 565-576.
hyperactive disorder. Australian and New Zealand Journal of Mattison, R. E., & Mayes, S. D. (2012). Relationships between learn-
Psychiatry, 38, 592-601. ing disabilities, executive function, and psychopathology in chil-
Faraone, S. V., Sergeant, J., Gillberg, C., & Biederman, J. (2003). dren with ADHD. Journal of Attention Disorders, 16, 138-146.
The worldwide prevalence of ADHD: Is it an American con- Milner, B. (1963). Effects of different brain lesions on card sort-
dition? World Psychiatry, 2, 104-113. ing. Archives of Neurology, 9, 100-110.
Gray, S. A., Chaban, P., Martinussed, R., Goldberg, R., Gotlieb, Norton, E. S., & Wolf, M. (2012). Rapid Automatized Naming
H., Kronitz, R., . . .Tannock, R. (2012). Effects of computer- (RAN) and reading fluency: Implications for understand-
ized working memory training program on working memory, ing and treatment of reading disabilities. Annual Review of
attention, and academics in adolescents with severe LD and Psychology, 63, 427-452.
comorbid ADHD: A randomized controlled trial. Journal of Purvis, K. L., & Tannock, R. (2000). Phonological processing,
Child Psychology and Psychiatry, 53, 1277-1284. not inhibitory control, differentiates ADHD and reading dis-
Green, C. T., Long, D. L., Green, D., Iosif, A., Dixon, J. F., Miller, ability. Journal of American Academy of Child & Adolescent
M. R., . . .Schweitzer, J. B. (2012). Will working memory train- Psychiatry, 39, 485-494.
ing generalize to improve off-task behavior in children with Raven, J. C. (1969). Guide to the standard progressive matrices.
attention-deficit/hyperactive disorder? Neurotherapeutics, 9, London, England: H. K. Lewis.
639-648. doi:10.1007/s13311-012-0124-y Rucklidge, J. J., & Tannock, R. (2002). Neuropsychological pro-
Greven, C. U., Rijsdijk, F. V., Asherson, P., & Plomin, R. (2012). files of adolescents with ADHD: Effects of reading difficul-
A longitudinal twin study on the association between ADHD ties and gender. Journal of Child Psychological Psychiatry,
symptoms and reading. Journal of Child Psychological 43, 988-1003.
Psychiatry, 53, 234-242. Sexton, C. C., Gelhorn, H., Bell, J., & Classi, P. (2011). The co-
Hodgson, K., Hutchinson, A. D., & Denson, L. (2012). occurrence of reading disorder and ADHD: Epidemiology,
Nonpharmacological treatments for ADHD: A meta-analytic treatment, psychosocial impact, and economic burden.
review. Journal of Attention Disorders. Advance online pub- Journal of Learning Disabilities, 45, 1-28.
lication. doi:10.1177/1087054712444732 Shany, M., Lachman, D., Shalem, Z., Bahat, A., & Zeiger, T.
Horowitz-Kraus, T. (2012). Pinpointing the deficit in executive (2006). Aleph-Taph: A test for the diagnosis of reading and
functions in teenage dyslexic readers: An ERP study using the writing disabilities, based on national Israeli norms. Tel Aviv,
Wisconsin Card Sorting Test. Journal of Learning Disabilities. Israel: Yesod.
Advance online publication. doi:10.1177/0022219412453084 Shatil, E., Nevo, B., & Breznitz, Z. (2008). Elull learning dis-
Horowitz-Kraus, T. (2013). Can the error monitoring system abilities diagnostic test: The reading sub-Test. Haifa, Israel:
differentiate ADHD from ADHD with reading disability? University of Haifa.
Reading and executive dysfunction as reflected in error moni- Skounti, M., Philalithis, A., & Galanakis, E. (2007). Variations in
toring. Journal of Attention Disorders. Advance online publi- prevalence of attention deficit hyperactivity disorder world-
cation. doi:10.1177/1087054713488440 wide. European Journal of Pediatrics, 166, 117-123.

Downloaded from jad.sagepub.com at UNIV NEBRASKA LIBRARIES on October 9, 2015


526 Journal of Attention Disorders 19(6)

Vakil, E., Blachstein, H., Wertman-Elad, R., & Greenstein, Y. comparison of the cognitive deficits in reading disability and
(2011). Verbal learning and memory as measured by the Rey- attention-deficit/hyperactivity disorder. Journal of Abnormal
Auditory Verbal Learning Test: ADHD with and without Psychology, 110, 157-172.
learning disabilities. Child Neuropsychology, 18, 449-466. Wolf, M., Bally, H., & Morris, R. (1986). Automaticity, retrieval
Wechsler, D. (1997). Wechsler Adult Intelligence Scale–Third processes, and reading: A longitudinal study in average and
Edition (WAIS-III). New York, NY: The Psychological impaired readers. Child Development, 57, 988-1000.
Corporation.
Willcutt, E. G., Doyle, A. E., Nigg, J. T., Faraone, S. V., & Author Biography
Pennington, B. F. (2005). Validity of the executive function Tzipi Horowitz-Kraus is the program director of the Reading and
theory of attention-deficit/hyperactivity disorder: A meta- Literacy Discovery Center in Cincinnati Children's Hospital,
analytic review. Biological Psychiatry, 57, 1336-1346. Ohio, USA. Dr. Horowitz- Kraus is a neuroscientist and clinician
Willcutt, E. G., Pennington, B. F., Boada, R., Ogline, J. S., who combines these specialties and implements it into a transla-
Tunick, R. A., Chhabildas, N. A., & Olson, R. K. (2001). A tional research in the field.

Downloaded from jad.sagepub.com at UNIV NEBRASKA LIBRARIES on October 9, 2015

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