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Nº - 301 - Brocki - 2007 - COMPLEMENTARIO - Ok
Nº - 301 - Brocki - 2007 - COMPLEMENTARIO - Ok
Background: The aim of the present study was to investigate how three different types of inhibitory
control – interference control within task, interference control outside task, and prepotent response
inhibition – and two types of working memory – verbal and spatial – would relate to early symptoms of
attention deficit/hyperactivity disorder (ADHD) and oppositional defiant disorder (ODD), both concur-
rently and longitudinally. Methods: Seventy-two preschoolers, 1/3 who had been identified as being at
risk for developing ADHD and/or ODD, completed neuropsychological tasks designed to measure
inhibitory control and working memory. Behavioral symptoms were measured through parental and
teacher ratings of the DSM-IV criteria for ADHD and ODD. Results: Our results suggest distinct types
of inhibitory control as being good predictors of concurrent and longitudinal symptoms of ADHD, rather
than ODD. However, no associations were obtained between working memory and ADHD or ODD
symptoms either concurrently or longitudinally. Conclusions: This study emphasizes the need to
isolate complex executive processes and break them down into components in order to properly
understand the neuropsychological roots involved in ADHD and ODD. Keywords: ADHD, ODD,
inhibitory control, interference control, prepotent response inhibition, working memory.
on verbal and visuo-spatial working memory in sample including children at risk for developing
relation to ADHD, suggests that impairments may be ADHD and/or ODD. Overall, it was predicted that
stronger for visuo-spatial working memory, but the significant relations would be obtained between the
authors conclude that further studies on the nature inhibitory control measures and concurrent and
and specificity of impairments in ADHD are needed. 2-years-later ADHD and ODD symptoms. It was
Although some studies have reported working further predicted that inhibitory control would relate
memory impairments in children with ODD and/or primarily to ADHD symptoms, irrespective of ODD.
CD (Séguin et al., 1999), there are also studies which The inconsistency in previous findings based on
have come to the opposite conclusion (Oosterlaan, preschool children offered no base for predictions
Scheres, & Sergeant, 2005). with regard to relations between working memory
Compared to the evidence showing impaired and ADHD and ODD symptoms. Further, whether
inhibitory control and working memory in ADHD, the different types of inhibitory control and working
ODD and/or CD in the school-aged years memory would relate to ADHD and ODD, indepen-
(Castellanos et al., 2006; Martinussen et al., 2005; dently of one another, formed an open question.
Oosterlaan et al., 2005, 1998), little is known about
the role of executive processes in the expression of
these disorders in the preschool period. The most
consistent evidence for executive control deficits in Method
association with ADHD symptoms in the preschool Participants and procedures
years holds for impaired inhibitory control (e.g.,
A total of 72 children (60 boys and 12 girls) participated
Berlin & Bohlin, 2002; Sonuga-Barke, Dalen, Daley,
in this study. In order to obtain a sample of children
& Remington, 2002; Byrne, DeWolfe, & Bawden,
scoring across the full range of ADHD symptom sever-
1998). With regard to working memory, findings are ity, 1/3 of the children were recruited from local Child
not as consistent. Some studies do report deficits in Health Care Centers on the basis that the children had
working memory (e.g., Mariani & Barkley, 1997; been identified by child psychologists as being at high
Sonuga-Barke, Dalen, & Remington, 2003; Thorell & risk for primarily developing diagnosable ADHD and/or
Wåhlstedt, 2006), whereas others report no associ- ODD. The sample was supplemented by a group of
ation between working memory and preschool ADHD normal children chosen to be proportional to the risk
symptoms (e.g., Sonuga-Barke et al., 2002). There is sample in terms of boy to girl ratio as well as age. These
a scarcity of empirical studies investigating the children were randomly selected and recruited through
relation between executive control and ODD in pre- the local birth register of Uppsala County, Sweden. No
children in the study were receiving psychostimulant
school, but the few clinical and non-clinical studies
medication for ADHD at the time.
available in the literature suggest that impaired
At Time 1 (Age: M ¼ 5 years, 5 months; SD ¼ .69),
executive control should primarily be considered an the children were tested individually at the Department
associate of ADHD rather than of ODD (e.g., Kalff of Psychology, Uppsala University. The 7 tasks being
et al., 2002; Speltz, DeKlyen, Calderon, Greenberg, analyzed in the current paper were part of a larger
& Fisher, 1999; Berlin & Bohlin, 2002; Sonuga- battery designed to tap various executive functions. In
Barke et al., 2002, 2003; Thorell & Wåhlstedt, 2006). an attempt to avoid possible fatigue effects, the tasks
Longitudinally, Berlin, Bohlin, and Rydell (2003) were administered during two sessions over a period of
found for a normal sample that inhibition measured 1 to 2 weeks. The tasks within each session were
at age 5 predicted ratings of hyperactivity and inat- administered in a randomized order. Each session las-
tention at age 81/2. Further, Brophy, Taylor, and ted approximately one hour with a break halfway
through. At the end of each session the children
Hughes (2002) showed that hard-to-manage pre-
received a gift worth approximately $7. At Time 1,
schoolers exhibiting symptoms of ADHD had poorer
questionnaire data from the children’s parents and
inhibitory control than the control group at age 7. teachers were collected for 72 and 68 of the children,
However, to our knowledge no longitudinal studies respectively. Reasons for attrition were that parents did
have, as yet, investigated the extent to which not give consent to contact the teacher (n ¼ 1) and the
preschool executive deficits are specific to sub- teachers were not willing to fill out the questionnaire
sequent ADHD, ODD and/or CD, by controlling for (n ¼ 3). At Time 2 (approximately 2 years after Time 1
comorbidity in the analyses. measurements; Longitudinal gap M ¼ 2 years,
2 months; SD ¼ .28; Age: M ¼ 7 years, 6 months;
SD ¼ .47), questionnaire data from children’s parents
Aim of study and teachers were collected for 66 and 65 children
respectively. Reasons for attrition were that the family
The aim of this study was to investigate how three
had moved out of the area (n ¼ 2) or that the family no
different types of inhibitory control – interference
longer wished to participate (n ¼ 4). Further, parents
control within task, interference control outside did not give consent to contact the teacher (n ¼ 1).
task, and prepotent response inhibition – and two Information about parental educational status (on a
types of working memory – verbal and spatial meas- 5-step scale) was collected as a measure of social
ures – would relate to concurrent and 2-year longi- background and will be taken into account in the
tudinal symptoms of ADHD and ODD in a preschool analyses (see Preliminary analyses).
Ó 2007 The Authors
Journal compilation Ó 2007 Association for Child and Adolescent Mental Health.
Preschool ADHD and ODD symptoms: inhibition and working memory 1035
9. Word Span
Backward
was used as measure of intelligence.
.32**
.33**
.31**
.22
.13
).03
.12
.19
–
Time 1 and 2 measurements
Verbal WM
Ratings of ADHD and ODD symptoms. At both Time
1 and Time 2, parents and teachers completed a ques-
8. Word Span
tionnaire containing items from the DSM-IV criteria for
Forward
.22
.11
.18
.22
.18
).22
.06
ADHD (APA, 1994). This measure has been well vali-
–
dated and is frequently used within ADHD research
Table 1 Inter-correlations between IQ, the Inhibition Measures and the Working Memory Measures, Adjusting for Age and Social Background, N ¼ 66–72
(e.g., DuPaul, Power, Anastopoulos, & Reid, 1998). Nine
items are composed to assess inattention. Six items are
composed to measure hyperactivity, and 3 items are
Spatial WM
composed to assess impulsivity. The questionnaire
7. Pig sty
Note. N ¼ 61–66 for analyses with IQ, WM ¼ working memory. aStandardized and aggregated measure of Stroop-like and Knock and Tap tasks.
.21
).04
).01
).00
.09
).08
further contained 8 items from the DSM-IV criteria for
–
oppositional defiant disorder (APA, 1994). Each item on
the ADHD and ODD scales was scored on a 4-point
scale ranging from 0 (never/seldom occurring) to 3 (very
frequently occurring). The ADHD and ODD rating
6. Go/No-Go
comissions
well as ODD, with coefficients ranging from .87 to .97.
).15
).15
).08
).17
).14
The questions in the ADHD and ODD scales were
–
phrased to represent the child’s current behavior. The
two ADHD symptoms domains (i.e., hyperactivity/
impulsivity and inattention) were highly correlated at
both Time 1 and Time 2 (r ¼ .76 to .84). Further, ADHD
and ODD symptoms were significantly correlated at
both Time 1 and Time 2 (r ¼ .69 to .75). Correlations
between parent and teacher ratings for ADHD and ODD
Interference outside task
.35**
.31**
.32**
and teacher ratings for ADHD at Time 1 as well as for
.20
–
ADHD and ODD at Time 2 were used in the analyses.
However, because of the weak correlation between
parent and teacher ratings for ODD at Time 1, these
particular scales were analyzed separately.
4. Interference
Results
within Taska
.90***
.90***
.35**
Preliminary analyses
–
Interference within task
.31**
2
Measures
Table 2 Descriptive Statistics for Age, IQ, Executive Measures, and Behavioral Ratings, N ¼ 66–72
Table 3 Concurrent and Longitudinal Relations from Inhibition and Working Memory Measures to ADHD and ODD Symptoms,
Adjusted for Age and Social Background. Figures Within Parentheses Represent the Relations Adjusted for Comorbid ODD and
ADHD Symptoms, Respectively N ¼ 62–72
Inhibition
Interference control within task ).41***().27*) ).39***().12) ).48***().41***) ).30**(.10)
Interference control outside task ).53***().46***) ).34***(.09) ).45***().45***) ).21(.22)
Prepotent response inhibition .36***(.23b) .35***(.10) .39**(.27*) .29**(.00)
Working Memory
Spatial working memory ).03().15) .10(.17) ).01(.09) ).09().13)
Verbal working memory (Word span forward) ).13().00) ).12().06) ).15().10) ).11(.00)
Verbal working memory (Word span backward) ).03(.00) ).08().05) ).13().10) ).08(.02)
a
ODD ratings at T1 denote teacher ratings only. No significant correlations were obtained between parent ratings of ODD at T1 and
any of the inhibitory control or working memory measures.bp ¼ .07.
*p < .05, **p < .01, ***p < .001
ratings of ADHD and ODD symptoms were skewed Concurrent relations between inhibition, working
(skewness ranging from ).04 to )1.63, kurtosis from memory, and symptoms of ADHD and ODD
).11 to 2.12), logarithmic transformations were
Table 2 shows descriptive statistics for executive
conducted. Analyses with these more adequately
measures, IQ, and symptoms of ADHD and ODD for
distributed variables did not change the level of
the total sample. The concurrent and longitudinal
significance in any of the analyses. For ease of
relations from inhibition and working memory meas-
interpretation, all results presented below are based
ures to ADHD and ODD symptoms, adjusted for age
on raw scores. Finally, all analyses were performed
and social background, are presented in Table 3.
with ADHD symptoms divided into hyperactivity/
Figures within parentheses in Table 3 represent the
impulsivity and inattention, respectively. The results
relations adjusted for comorbid ODD and ADHD
showed a very similar pattern of findings for the two
symptoms, respectively.
symptom domains, therefore all analyses below are
Interference control within task, interference con-
presented based on the mean score across hyper-
trol outside task, and prepotent response inhibition
activity/impulsivity and inattention (i.e., ADHD
correlated significantly to symptoms of ADHD at Time
symptoms). Attrition for specific measures varied
1. These relations remained significant when con-
between one and five children, due to some children
trolling for teacher ratings of ODD symptoms (pre-
failing to complete a specific task.3
potent response inhibition, p ¼ .07). The inhibitory
measures also correlated significantly with teacher
3
ratings of ODD symptoms at Time 1, but when
Specification of attrition for each task and whether attrition
was for healthy ¼ H, or children at risk ¼ R. N ¼ attrition for:
partialing out the effect of teacher ratings of ADHD,
Stroop-like task (4 R, 1 H); Knock and Tap (2 R, 0 H); Go/no-go these relations no longer remained significant.
(0); Statue (2 R, 2 H); Pig sty (1 R, 0 H); Word span forward (1 R, Further, no significant correlations were obtained
0 H); Word span backward (3 R, 0 H). between parent ratings of ODD at Time 1 and any of
Ó 2007 The Authors
Journal compilation Ó 2007 Association for Child and Adolescent Mental Health.
1038 Karin C. Brocki et al.
the inhibitory control measures, regardless of control we made a difference variable (ADHDT2 – ADHDT1)
for ADHD symptoms. where scores below zero, reflecting decreases in
No significant correlations between the two types ADHD symptoms over time, were set to zero. First,
of working memory and symptoms of ADHD and Pearson correlation analyses were performed
ODD were obtained at Time 1. between the neuropsychological measures and the
change variable. Interference control, prepotent
response inhibition, and verbal working memory
Longitudinal relations between inhibition, working
were found to be at least near-significant predictors
memory, and symptoms of ADHD and ODD
of increase in ADHD symptoms (p ¼ .03 to .09).
Similarly to the concurrent relations, the three types Second, a multiple regression analysis with these
of inhibitory control correlated significantly with three variables as predictors and the variable
ADHD symptoms at Time 2 (see Table 3). These reflecting increase in ADHD symptoms as outcome
correlations remained significant when controlling was performed. The results showed that only
for ODD symptoms. Interference control within task prepotent response inhibition contributed uniquely
and prepotent response inhibition also correlated to the prediction of an increase in ADHD symptoms
significantly with ratings of ODD symptoms at Time over time, ß ¼ .25, p ¼ .05.
2, but when partialing out the effect of ADHD
symptoms, these relations no longer remained sig-
nificant. Again, no significant relations were ob- Intelligence
tained between the working memory measures and
IQ was significantly related to combined parent and
symptoms of ADHD or ODD at Time 2.
teacher ratings of ADHD symptoms at Time 1 and
To investigate whether the three types of inhibitory
Time 2, r ¼ ).44, p < .0001, r ¼ ).32, p < .01. IQ
control contributed with common or independent
was also significantly correlated with parent ratings
variance in explaining ADHD symptoms at Time 2,
of ODD at Time 1, r ¼ ).31, p < .01, and combined
these measures were simultaneously entered into a
parent and teacher ratings of ODD symptoms at
multiple linear regression analysis, with the inhibi-
Time 2, r ¼ ).26, p < .01, but not with teacher rat-
tion measures as predictor variables and the ADHD
ings of ODD at Time 1, r ¼ ).09, p > .05. With regard
symptom score as the outcome variable. The
to correlations among IQ and the inhibitory control
regression model was significant, F (5, 56) ¼ 7.28,
and working memory measures (presented in
p < . 0001, R2 ¼ .39, with all three types of inhibitory
Table 1), significant correlations were obtained
control predicting ratings of ADHD at Time 2
between IQ, the Stroop-like task, Knock and Tap as
independently of one another, (ßInterfer.Within.Task ¼
well as with interference control within task (i.e.,
).34, p < .01, ßInterfer.Outside.Task ¼ ).27, p < .05,
composite across the Stroop-like task and Knock
ßPrepot.resp.inhib. ¼ .26, p < .05). Together, interfer-
and Tap), interference control outside task (i.e.,
ence control within task, interference control outside
Statue) and verbal working memory (i.e., Word span
task, and prepotent response inhibition explained
backwards). Controlling for IQ when predicting
34% of the variance in ADHD symptoms. When
ADHD and ODD symptoms from measures of
conducting the same multiple regression analysis
inhibitory control and working memory did not
with control for ODD symptoms, the two types of
change the level of significance of contributing vari-
interference control still made independent contri-
ables.
butions, although the effect of prepotent response
inhibition was only marginally significant (p < .09)
and the explained variance was reduced to 19%.
Discussion
A similar multiple regression analysis was con-
ducted with ODD symptoms at Time 2 as the outcome Motivated by the mounting need to identify early
variable and the inhibitory control measures as neuropsychological risk factors in developmental
predictor variables. The regression model was syndromes, this study investigated the influence of
significant, F (5, 56) ¼ 2.90, p < . 05, R2 ¼ .21, with different types of inhibitory control and working
none of the inhibitory control measures contributing memory processes on concurrent and 2-year lon-
with independent variance. Together the three types gitudinal symptoms of ADHD and ODD in a sample
of inhibitory control explained 11% of the variance of preschool children. Overall, the findings showed
in ODD symptoms at Time 2. A similar pattern of that three distinct inhibitory processes, interference
results was obtained when conducting the same control within task, interference control outside
multiple regression analysis with control for ADHD task, and prepotent response inhibition, made
symptoms, with none of the inhibitory control meas- independent contributions to concurrent and
ures making independent contributions and the 2-year longitudinal symptoms of ADHD. Con-
explained variance in ODD symptoms being reduced versely, relations between measures of inhibitory
to 1%. control and ODD were eliminated upon adjusting
To investigate whether early neuropsychological for ADHD symptoms. Further, variations in work-
function could predict increase in ADHD symptoms, ing memory did not contribute to the explained
Ó 2007 The Authors
Journal compilation Ó 2007 Association for Child and Adolescent Mental Health.
Preschool ADHD and ODD symptoms: inhibition and working memory 1039
variance of ADHD or ODD symptoms in this age of ADHD has not been addressed in previous stud-
period. ies. Thus, this study takes the role of inhibitory
control as a potential neuropsychological marker
for ADHD a step further, by suggesting potentially
Concurrent and 2-year longitudinal relations
distinct inhibitory pathways between risk and
between inhibitory control and symptoms
later-developing ADHD. Indeed, the results showed
of ADHD and ODD
that interference control within task, interference
Regarding the concurrent relations between inhibit- control outside task, and prepotent response inhi-
ory control and ADHD symptoms, similar findings bition predicted independent parts of the variance in
have been reported in the very few previous studies ADHD symptoms two years later. These results
of preschoolers that have controlled for comorbidity contrast with Barkley’s (1997) proposition and the
(Berlin & Bohlin, 2002; Sonuga-Barke et al., 2002, previous empirical findings of, for example, Leung
2003; Thorell & Wåhlstedt, 2006). Together, these and Connolly (1996) that it is interference within
results extend findings on elementary school-aged task rather than interference outside the task that
children to preschool children, in terms of inhibitory seems most important in relation to ADHD. These
control being primarily related to ADHD, whereas the inconsistencies could be a result of the different
relation to ODD is caused by the large overlap be- developmental levels of the samples studied (pre-
tween ADHD and ODD (e.g., see Oosterlaan et al., school vs. school age). In other words, it could be
2005; Waschbusch, 2002 for reviews). It should, speculated that the relative importance of different
however, be noted that some studies of school-aged types of inhibitory control in relation to ADHD dif-
children have concluded that inhibitory control is fers as a function of age. This is an issue that awaits
not specifically related to ADHD, but is also a neuro- empirical testing and should be of interest in future
psychological correlate of ODD and CD (e.g., Oos- studies examining ADHD from a developmental
terlaan et al., 1998; Sergeant, Geurtz, & Oosterlaan, perspective.
2002). This inconsistency in findings could be a
result of having only studied group differences, not
Concurrent and 2-year longitudinal relations
taking into consideration that children with ODD
between working memory and behavioral
often have elevated levels of ADHD symptoms. These
problem symptoms
symptoms at the sub-clinical level can be related to
neuropsychological deficits and need to be controlled In contrast to inhibitory control, working memory
for dimensionally by using ADHD and/or ODD did not correlate with concurrent or longitudinal
symptoms as a covariate (e.g., Nigg, Hinshaw, Carte, symptoms of either ADHD or ODD. These results are
& Treuting, 1998). in line with findings from the preschool study by
The fact that our results showed very similar pat- Sonuga-Barke and colleagues (2002), whereas most
terns of associations between the neuropsycholo- studies of older children have found associations
gical measures and the two ADHD symptom between working memory and ADHD symptoms
domains should be commented on. These results (e.g., Martinussen et al., 2005, Martinussen & Tan-
may be taken to contrast with findings on school- nock, 2006; Willcutt et al., 2005). Although the
aged children suggesting that impaired executive current study does not specifically address neuro-
control is most strongly associated with inattention psychological correlates of ADHD as a function of
symptoms (e.g., Chhabildas, Pennington, & Willcutt, age, a developmental explanation for this inconsist-
2001; Willcutt, Doyle, Nigg, Faraone, & Pennington, ency seems plausible, given the fact that working
2005). The apparent contrast may, however, be memory processes are not sufficiently developed at
understood by referring to the results reported by preschool age (Gathercole, Pickering, Ambridge, &
Brocki and Bohlin (2006). They showed reciprocal Wearing, 2004). In line with this developmental
associations between the two ADHD symptom reasoning, Barkley (1997), in elaborating his hybrid
domains and executive deficits in the late preschool model of ADHD, suggested that inhibitory control is
and early school-age years, whereas executive dys- the ‘first’ impaired neuropsychological component in
function was related only to inattention in older ADHD, which in turn ‘sets the stage’ for impairments
school-aged children. in later-developing, more complex executive func-
tions, such as working memory and planning.
Corroborating Barkley’s hypothesis about develop-
Relations between different types of inhibitory
mental change in ADHD are findings by Brocki and
control and ADHD symptoms
Bohlin (2006) demonstrating that poor inhibition
While our overall results give support to existing was most clearly associated with ADHD symptoms
data suggesting a strong link between preschool for children in late preschool and early school age,
ADHD symptoms and inhibitory control (Sonuga- whereas poor functioning with regard to later-
Barke et al., 2002; Berlin & Bohlin, 2002), the developing and more complex executive functions
question of independent contributions of different such as working memory was associated only with
types of inhibitory control to the explained variance inattention symptoms for older school aged children.
Ó 2007 The Authors
Journal compilation Ó 2007 Association for Child and Adolescent Mental Health.
1040 Karin C. Brocki et al.
It should be noted, however, that some preschool developmental disorder with deficits in underlying
studies do report relations between working memory neuropsychological components possibly varying
and ADHD (Mariani & Barkley, 1997; Sonuga-Barke with child age.
et al., 2003; Thorell & Wåhlstedt, 2006). Discrep-
ancies in results for working memory and ADHD in
preschool children are not easily explained, but may Acknowledgement
be attributable to variations in samples and type of
This study was supported by a grant from The Bank
measures used. Relating to the possibility of results
of Sweden Tercentenary Foundation.
being task-specific, it should be acknowledged that
the working memory measures used in the current
study may not have been optimal. This explanation
Correspondence to
especially relates to the spatial working memory
measure primarily tapping into the storage compon- Karin C. Brocki, Department of Psychology, Uppsala
ent (i.e., short-term memory) of the working memory University, P.O. Box 1225, SE-751 42 Uppsala,
system. However, this explanation is less relevant for Sweden; Tel: +46 18 471 22 24; Fax: +46 18 471 21 23;
the lack of relation between backward word span Email: Karin.Brocki@psyk.uu.se
(commonly thought to be a working memory mea-
sure) and ADHD symptoms. It is currently unclear
both empirically and theoretically whether short- References
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Ó 2007 The Authors
Journal compilation Ó 2007 Association for Child and Adolescent Mental Health.
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