Original
Guillermina Yáñez-Téllez1 Cognitive and executive functions in
Helena Romero-Romero1
Liliana Rivera-García1 ADHD
Belén Prieto-Corona1
Jorge Bernal-Hernández1
Erzsebet Marosi-Holczberger1
Vicente Guerrero-Juárez1
Mario Rodríguez-Camacho1 1
Neuroscience Project
Juan F. Silva-Pereyra1
Facultad de Estudios Superiores Iztacala
Universidad Nacional Autónoma de México
Introduction. Some studies have reported that atten- Funciones cognoscitivas y ejecutivas en el TDAH
tion-deficit/hyperactivity disorder (ADHD) children show
alterations in different cognitive functions. Recently, a de- Introducción. Se han observado alteraciones en diferen-
ficiency in the executive functions (EF) is proposed as the tes funciones cognoscitivas en niños con Trastorno por Déficit
cause underlying all of these symptoms. However discrepan- de Atención con Hiperactividad (TDAH) y recientemente se ha
cies exist about these findings. propuesto que la causa que subyace a toda la sintomatología
es una deficiencia en las funciones ejecutivas (FE), no obstan-
Objective. Assessment of cognitive and executive te, existen muchas discrepancias en los hallazgos.
functions of subjects with both ADHD hyperactive-impulsive
Objetivo. Realizar una evaluación amplia de las funcio-
type and combined type, in order to reveal their
nes cognoscitivas y FE en niños con TDAH tipos hiperactivo-
neuropsychological characteristics and analyze if those impulsivo y combinado (TDAH/HI-C) para conocer sus carac-
functions are related to hyperactive-impulsive behavior. terísticas neuropsicológicas y analizar que funciones pueden
Method. Neuropsychological Battery, Stroop test, Wisconsin relacionarse con su conducta hiperactivo-impulsiva.
Card Sorting test and London Tower test were applied to 51
children between 7 and 12 years old (25 controls and 26 Metodología. Se aplicó una Batería Neuropsicológica y
ADHD). los Test de Stroop, de Clasificación de tarjetas de Wisconsin
(WCST) y Torre de Londres a 51 niños de 7 a12 años de edad
Results. ADHD children showed worst performance in (25 control y 26 con TDAH).
sustained attention, rapid serial naming of figures and
Resultados. El grupo TDAH/HI-C tuvo peor resultado
colors, comprehension of written instructions, word
en atención sostenida, denominación serial rápida de figu-
dictation, number comparison, arithmetical problems, visual ras y colores, comprensión de órdenes escritas, dictado de
working memory, long term memory and the scores of WCST. palabras, comparación de números, problemas aritméticos,
Variables related to hyperactivity-impulsivity were: errors memoria de trabajo visual y de largo plazo y en el WCST. Los
and decreased velocity in rapid serial naming of colors and errores y velocidad en denominación serial rápida de colo-
figures, comprehension of written instructions, arithmetical res y figuras, comprensión de órdenes escritas, problemas
problems and the scores of total errors, perseverating errors aritméticos, y del WCST errores totales, perseverativos y res-
and perseverating responses of WCST. puestas perseverativas, fueron las variables que se relaciona-
ron con la hiperactividad-impulsividad.
Conclusion. ADHD children show a great variety of
cognitive deficiencies and had deficit only in some domains Conclusiones. Los niños con TDAH/HI-C tienen una gran
of executive functions. These deficiencies could explain to variedad de deficiencias cognoscitivas y solamente en algu-
some extent the hyperactive and impulsive behavior. nas áreas de las FE. Estas deficiencias explican en alguna me-
dida el comportamiento hiperactivo-impulsivo.
Key words: ADHD, Cognitive functions, Executive functions, Hyperactivity,
Palabras clave: TDAH, Funciones cognoscitivas, Funciones ejecutivas, Hiperactividad,
Neuropsychology.
Neuropsicología
Actas Esp Psiquiatr 2012;40(6):293-8
INTRODUCTION
Correspondence:
Dra. Guillermina Yáñez Téllez
Av de los Barrios No. 1, Los Reyes Iztacala, Tlanepantla, Estado de México, México In accordance with the Diagnostic and Statistical
CP 54090 Manual of Mental Disorders, fourth edition revised,1
Fax. 52 55 5390 7604
E-mail: [email protected] Attention Deficit Hyperactivity Disorder (ADHD) has three
Actas Esp Psiquiatr 2012;40(6):293-8 293
Guillermina Yáñez-Téllez, et al. Cognitive and executive functions in ADHD
principal groups of symptoms: inattention, hyperactivity in mind that they will need to guide their subsequent actions
and impulsivity. According to the greater or lesser and disorganized in their thinking, to the point of losing
prevalence of these symptoms, ADHD is classified into the sight of the objective of their activities. Miranda-Casas et
subgroups of predominately inattention, predominantly al.16 observed that the performance of children with ADHD
hyperactivity-impulsivity and combined, the latter with on a temporo-visuospatial WM task was worse during a
symptoms of inattention and hyperactivity-impulsivity. memory delay for inverse digits compared to NC children,
This disorder very frequently occurs in the school aged although the same was not found in temporal-visuospatial
population, with an estimated prevalence of 3 to 7%.1 WM without delay and digits in direct order.
Characterization of ADHD from the neuropsychological Regarding reading in children with ADHD, some
point of view has been a widely debated subject. Barkley2 authors have not detected differences between normal
proposed the hypothesis of an underlying deficiency in control and ADHD children,17 while others have observed
executive functions (EF), specifically in behavior inhibition, clear deficiencies in some aspects such as reading of
for the hyperactive-impulsive and combined subtypes. pseudowords.18-20 Regarding calculation, deficiencies have
Contradictory findings have been found in empirical works been found in children with ADHD in oral, and written
conducted to test the hypothesis of EF deficiencies. Cantrill3 calculation and math problems,15 although the latter
observed that the ADHD group had deficient performance finding has not been consistent.16
in inhibition and sense of time, but not in working memory
As has been mentioned, different investigations have
(WM). On their part, Stevens et al.4 observed that children
shown that the cognitive deficiencies in ADHD children are
with ADHD had deficits in inhibitory control, WM and
quite varied, although these results have not been
short-term memory. In this sense, Shallice5 studied the EFs
consistent. These studies were conducted using samples
of children with ADHD based on reaction time, sustained
chosen with different criteria according to the different
attention, vigilance, completing statements, knowledge of
generations of the manuals of the American Psychiatric
spatial rules, fluency, stop type tasks and WM. They found Association.1 In general, the subtypes were not differentiated
that these children were more deficient than a control in the earliest works and the cognitive functions studies
group in all the tasks, except for the fluency task. On the were not always the same in the different works. For these
contrary to the previous findings, when Scheres et al.6 reasons, it is likely that the characterization of ADHD from
compared children with ADHD with normal controls (NC), the neuropsychological point of view is still a controversial
from the beginning they observed deficits in control of subject.
interference, inhibition, planning and letter fluency. After
controlling for age and IQ, none of the deficits were Consequently, studies are needed that jointly approach
maintained. Equally, Geurts et al.7 did not find support for those functions in which deficiencies may exist in children
the deficit hypothesis in the EFs of children with combined with ADHD using more homogeneous samples based on
ADHD and in a meta-analysis, Schwartz and Verhaeghen clear criteria such as those presented in the DSM-IV-TR.1
also did not detect any deficiencies in control of This could make it possible to determine if any or some of
interferences8. the possible cognitive deficiencies of the children with
ADHD could explain the behavioral symptoms or their
One of the principal symptoms of ADHD is sustained severity.
attention deficit. Nonetheless, its verification by objective
methods has also been inconsistent. Some findings in the This study aimed to describe the cognitive functioning
application of the continuous task execution (CTE) to of children with hyperactive-impulsive and combined type
evaluate sustained attention have been greater rate of ADHD. In this study, most of the functions studied in the
omission and commission errors in children with ADHD literature in a single population were evaluated and it was
compared to normal controls (NC).9 However, other studies attempted to determine the possible deficiencies that
have not observed this pattern.10 could be related with the behavioral symptoms and their
severity.
In relation to language, it has been proposed that
children with ADHD have problems with phonological Knowing the cognitive functioning of children with
tasks,11, 12 morphosyntactic skills,12 semantic processing,13 ADHD may be very useful in the planning of adequate
naming speed for colors and figures14 and for letters and intervention strategies for this population. Currently, the
colors15. intervention models are basically pharmacological and
some are based on the application of behavior modification
Regarding memory, Barkley2 stated that persons with techniques.21 In spite of the utility of these techniques,
ADHD have problems with WM so that they are described as neuropsychological intervention is advisable to favor the
forgetful, incapable of maintaining important information longer-term cognitive changes.
294 Actas Esp Psiquiatr 2012;40(6):293-8
Guillermina Yáñez-Téllez, et al. Cognitive and executive functions in ADHD
METHODOLOGY and long term memory. It has rules for children 7 to 12
year of age and all the tests have an internal consistency
Subjects reliability of >0.70.
2. Tower of London.24 This fundamentally evaluates
Two groups of children were studied, one with planning and problem solving capacity.
hyperactive-impulsive and combined subtypes of ADHD 3. The Stroop Color Word test.25 One of its objectives is the
(ADHD/HI-C), without drug or psychological treatment, and evaluation of one of the aspects of executive functions:
a group of normal control children (NC). control of interference.
4. Wisconsin Card Sorting Test (WCST).26 This evaluates
The ADHD/HI-C group was made up of 26 male children, abstract reasoning and cognitive flexibility.
7 to 12 years of age, mean age of 8.6 years, from the Regular
School of the City of Mexico Service Support Units. These
units are made up of specialist groups that provide support Procedure
within the public schools to children with different learning
problems or problems of integration into a regular group. An informed consent was obtained from the parents for
DSM-IV-TR criteria for hyperactive-impulsive and combined all the children. After, a structured interview was administered
subtypes1 and the Conners Scale-Revised22 were used for to the parents to obtain the clinical history data. Those
their selection. The scale was answered by both the parents children who had repeated any academic course or were
and teachers. The requirement was that they would reach reported to have learning problems at school did not go on
the cutoff in one or some of the two subtypes mentioned in to the next phases.
both evaluation. Only children with normal IQ who did not
have learning problems, who had not repeated any course During a second session, the WISC-R was applied and a
during their schooling and who did not have any other neurological evaluation was made. Those children with
neurological complication, were included. normal IQ, without neurological disorders, whose parents
and teachers answered the Conners Scale-Revised,22 remained
The control group was made up of 25 males with normal in the study. The NBC and executive function tests were
IQ, with similar ages to the ADHD group (mean 9 years) and applied in two consecutive days.
from the same schools as the children of the study group,
without learning or behavior disorders and rule scores on
the Conners Scale -Revised22 did not surpass the cutoffs, in Analysis
addition to having a normal neurological evaluation.
Using the scores derived from each one of the subtests
as dependent variables, a T test was conducted among the
Instruments NC groups and the ADHD/HI-C. After, a multiple linear
regression analysis with the backward method was applied
For the selection of the subjects: in regards to those variables that showed differences
between groups in order to obtain the best combination of
1. Structured interview.
2. Wechsler Intelligence Scale for Children -Revised variables that would predict hyperactivity-impulsivity
(WISC-R). symptoms as evaluated with the behavioral scales.
3. Conners Scale- Revised, Farré-Riba and Narbona
version.22 This scale contains 20 items, 5 of which
RESULTS
correspond to hyperactivity-impulsivity, 5 others to
inattention and 10 to behavior disorders.
Table 1 describes the demographic and I.Q characteristics
For the neuropsychological evaluation: of the children of the control group and those with ADHD/
HI-C. There were no significant differences between the
1. Neuropsychological battery for children (NBC).23 It groups in any of the variables mentioned. (Table 1)
contains tests to evaluate different functions: 1)
Attention (CTE); 2) Language: phonological processing,
(analysis and synthesis tasks), rapid serial naming (RSN) Neuropsychology Battery
(digits, letters, colors, figures), repetition, understanding
or orders, vocabulary (receptive and expressive); 3) Attention
Reading words, lexical decision and understanding of
instructions; 4) Writing of words; 5) Arithmetic (oral In the paper and pencil continuous task execution (CTE),
calculation, written calculation, comparison of numbers the ADHD/HI-C group showed a lower rate of detection of
and arithmetic problems), 6) short term memory, WM the white stimulus than the control group [t(49)=2.78,
Actas Esp Psiquiatr 2012;40(6):293-8 295
Guillermina Yáñez-Téllez, et al. Cognitive and executive functions in ADHD
Table 1 Demographic characteristics and in- *
70 Control
Control
telligence quotient of the control and
ADHD
ADHD/HI-C groups 60
TDAH
Mean (SD) 50
segundos
seconds
Control ADHD 40
N 25 26 30
Age in years 9.0 (1.7) 8.6 (1.7)
20
Verbal Intelligence Quotient 109.6(12.6) 106.8 (12.4)
10
Executive Intelligence Quotient 108 (15.5) 104.5 (11.8)
0
Total Intelligent quotient 109.8 (14.3) 106.4 (12) Digits
Dígitos Letters
Letras Colors
Colores Figures
Figuras
p=0.008], with means of 32.5 and 44.2, respectively. There
Figure 1 Comparison of the control and ADHD/
were no significant differences in the errors.
HI-C groups in the rapid serial naming
task for different categories of stimuli
Language
Significant differences were only obtained in the rapid
serial naming task for figures [t(49)= -3.09, p=0.003] and colors [t(49)=2.26, p=0.028] and memories with clues [t(49)=2.042,
[t(49)=-2.69, p=0.01], where the ADHD/HI-C group took longer p=0.047]. In every case, there was less performance for the
to carry out the tasks (Fig. 1). There were also statistically ADHD/HI-C.
significant differences in the total amount of errors on the
rapid serial naming (RSN) with a greater amount for the
ADHD/HI-C group [t(49)=-3.05, p=0.004]. (Figure 1) Executive functions tests
No statistically significant differences were observed
Reading and writing between groups with the Tower of London and Stroop Tests.
In the WCST, the ADHD group showed a greater amount of
There were no significant differences in reading of total errors, perseverative errors and perseverative responses
words speed and accuracy or in a lexical decision task. as well as a lower number of answers on the conceptual level
Significant differences were only observed in the compared to the CN group (Table 2).
understanding of written instructions [t(49)=2.37, p=0.02],
with less performance for the ADHD /HI-C group. In the
dictation of frequent words, a significant difference was Relation between cognitive deficits and
observed, with more correct answers for the NC group hyperactive-impulsive behavior
[t(49)=2.57, p=0.013].
In a multiple linear regression analysis with the backward
Arithmetic method, it was observed that the combination of variables
that best predicted severity of the hyperactivity-impulsivity
A significant difference was found in the comparison of symptoms evaluated with the Conners Scale22 were: errors in
numbers [t(49)=2.22, p=0.031] and arithmetic problems rapid serial naming (RSN) and speed in naming colors and
[t(49)=2.06, p=0.045]. There was better performance for the figures (RSN), understanding of written instruction (RSN),
arithmetic problems (RSN), perseverative errors (WCST), total
NC group in both cases. There were no significant differences
errors (WCST) and perseverative responses (WCST) R2=0.69 [F
in oral calculation, written calculation and number naming.
(8,27)=7.38; p=0.000] with an elevated level of statistical
significance.
Memory
No significant differences were found in short-term
CONCLUSION
memory tasks. In WM, there were significant differences
This work has aimed to discover the cognitive functioning of
[t(49)=2.002, p=0.05] only in the visual modality. Significant
children with ADHD/HI-C and then to try to determine which
differences were found in the free long-term memory
296 Actas Esp Psiquiatr 2012;40(6):293-8
Guillermina Yáñez-Téllez, et al. Cognitive and executive functions in ADHD
Table 2 Comparison between the control group and the ADHD/HI-C on the Wisconsin Card Sorting Test
Groups
Percentiles Control ADHD t p
Control Control
Mean (SD) Mean (SD)
Total errors 51.86 (20.8) 32.42 (23.1) 2.932 .005
Perseverative responses 48.43 (23.1) 29.76 (23.0) 2.688 .01
Perseverative errors 49.56 (23.0) 31.04 (22.3) 2.703 .01
Non-perseverative errors 58.65 (23.0) 49.57 (29.0) 1.156 .25
Percentage of responses on the conceptual level 44.43 (18.2) 30.90 (21.4) 2.260 .02
alterations can explain the behavioral symptoms and their calculation. Thus, it can be concluded that the problem that
severity. In accordance with the results, the characteristics that children with ADHD/HI-C have is not one of calculation per se,
distinguish ADHD/HI-C children with normal I.Q. from NC children but rather that this deficiency could be secondary to attention
are lower performance on sustained attention tasks, greater and working memory problems.
number of errors and more time to perform rapid serial naming
tasks of figures and colors as well as more errors in the As referred to in the literature,16 significant differences were
understanding of written instructions and in word dictation. not observed in short-term memory tasks. In WM, which according
Furthermore, they had deficiencies in arithmetic tasks of to the hypothesis of Barkley2 would be one of the most altered
comparison of numbers and problem solving. Regarding memory, functions, we only detected lower performance in the ADHD/HI-C
problems were observed in visual WM and long-term memory. On group in the visual modality, similar to that observed in another
the other hand, they had more total and perseverative errors on study.16
the WCST, that is, these children had less cognitive flexibility than
For the free long-term memory, for which we do not know
the control children.
the previous data, a deficit of the ADHD/HI-C children was
The RSN variables that predict hyperactivity-impulsivity observed in the coding of visual information and of maintaining
grade are: errors in rapid serial naming, speed to name figures it in the long-term memory.
and colors and understanding of written instructions. From the
Despite this pattern of results, we also observed some
WCST, the variables are perseverative errors, total errors and
important inconsistencies regarding the already published data.
perseverative responses.
It has been postulated that one of the principal alterations
Our results agree with some of the works published. Although underlying ADHD/HI-C is a deficit in the executive functions (EF).2
there is controversy in determining if there are alterations in In this study, three of the tests that are prototypical of the
sustained attention in ADHD/HI-C children, in our study these functioning of different areas of EF were applied, and significant
children had a lower number of correct answers on continuous differences were only obtained in the cognitive flexibility test.
task execution (CTE), these results coinciding with those obtained Thus, overall, it cannot be said that the EF deficiencies are those
by Losier et al.10 that determine the impulsivity and hyperactivity problems in
these children. These seem to be confined to deficiencies in
One finding that can be directly related with an inattention abstract reasoning and cognitive flexibility.
symptom in children with ADHD/HI-C, which is referred to in the
DSM-IV TR1 as that “they do not to listen when spoken to and do We consider that the cognitive deficiencies in ADHD found
not follow instructions,” is lower performance in understanding in different studies are probably due to the comorbidity that
or orders tasks, both orally and written, although only the latter occurs with the learning disorders and when they are not
was significant. adequately ruled out, they may contribute to the differences
observed. We think that more studies that analyze the altered
Coinciding with other studies14, 15 in the rapid serial naming skills jointly in these children need to be conducted in order to
of colors and figures task, children with ADHD/HI-C were slower determine the neuropsychological profile of this population more
and had more errors than the normal control group children. consistently.
As we have previously observed,15 children with ADHD/HI-C The study of the cognitive functions of children with ADHD/
had lower performance in arithmetic problem solving. However, HI-C may be useful to begin to establish a fixed neuropsychological
we did not observe significant differences in oral and written battery to perform a standardized evaluation of this population.
Actas Esp Psiquiatr 2012;40(6):293-8 297
Guillermina Yáñez-Téllez, et al. Cognitive and executive functions in ADHD
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IN307311-3 13. Idiazábal A, Guerrero-Gallo D, Sánchez-Bisbal MM. Déficit en el
procesamiento semántico. Rev Neurol. 2006;42:S29-36.
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