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Romer 2009
Romer 2009
Romer 2009
Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia
a r t i c l e i n f o a b s t r a c t
Article history: Initiation of drug use and other risky behavior in preadolescence is associated with poor developmental
Received 14 November 2008 outcomes. In this research, we examine models that ascribe the trajectory to (a) weak executive cog-
Received in revised form 15 June 2009 nitive function (ECF), (b) early manifestation of externalizing problems, or (c) heightened levels of trait
Accepted 18 June 2009
impulsivity. We test the explanatory power of these factors in a structural equation model with a com-
Available online 26 June 2009
munity sample of 387 preadolescents ages 10–12 years. Participants were tested with a computerized
battery of tasks to assess three facets of ECF (working memory, cognitive control, and reward process-
Keywords:
ing) as well as with an audio assisted computerized self-interview to obtain reports of impulsivity and
Risk behavior
Adolescence
risk behaviors (use of cigarettes and alcohol as well as engaging in fighting and gambling for money)
Impulsivity and a self-administered questionnaire to assess externalizing and internalizing problems. The best fitting
Executive function model explained both early risk taking and externalizing symptoms as the result of individual differences
Working memory in impulsivity. Although no ECF was directly related to risk taking, working memory and one measure
SEM of reward processing performance (reversal learning) were inversely related to impulsivity. The results
Drug use are discussed in regard to theories of early risk taking with particular focus on the potential relation
between ECF and impulsive behavior tendencies and the implications for early intervention to prevent
the dysfunctional trajectory associated with early risk behavior.
© 2009 Elsevier Ltd. All rights reserved.
0028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2009.06.019
D. Romer et al. / Neuropsychologia 47 (2009) 2916–2926 2917
ever, they also note the importance of impulsivity for this trajectory cessing tasks. A study by Finn (2002) found that working memory
(Caspi, Henry, McGee, Moffitt, & Silva, 1995; White et al., 1994). affected the performance of young adults on a task requiring learn-
Despite evidence for a range of behavioral and cognitive deficits ing of cues to reward. In addition, Hinson and colleagues (Hinson,
as the precursors of early drug use and risk taking, the precise nature Jameson, & Whitney, 2002, 2003) as well as Shamosh et al. (2008)
of the deficit has not been isolated (see Zucker, Donovan, Masten, find that reduced working memory capacity increases the ten-
Mattson, & Moss, 2008 and Zucker, 2006, for reviews). Indeed, poor dency to choose smaller immediate rewards over larger but delayed
ECF in preadolescence may not correlate with contemporaneous rewards. Hence, there is some suggestion that weak working mem-
risk behavior. Aytaclar et al. (1999) found that some ECFs at ages ory may interfere with optimal performance on reward processing
10–12 predicted drug use two years later. However, Tarter et al. tasks that involve the need to inhibit responses that previously led
(2003) found that ECF assessed at ages 10–12 did not predict sub- to reward or that currently lead to non-optimal reward.
sequent drug use at age 16 or correlate with risk for drug use based
on parental drug use history, while other indicators, such as exter- 1.1. Role of impulsivity
nalizing behaviors, were much better predictors. It was not until
age 19 that early ECF was a predictor of drug use and SUD. In nei- Another major correlate of risky behavior in adolescents is a set
ther of these studies was drug use assessed at the same time as ECF of relatively stable personality traits under the rubric of impul-
(ages 10–12), and in both cases the samples were drawn to contrast sivity (S.B.G. Eysenck & Eysenck, 1977, 1978; Patton, Stanford, &
high versus lower risk youth rather than more general community Barratt, 1995; Verdejo-Garcia, Lawrence, & Clark, 2008; Whiteside &
populations. Lynam, 2001; Zuckerman, 2006). These traits are regarded as under
Nigg et al. (2004) examined an extensive battery of ECFs in rela- the control of both the prefrontal cortex (PFC) and the subcortical
tion to drug use in boys ages 12–15. The ECFs that were studied did motivational systems to which it is linked (Chambers & Potenza,
not appear to lie on a single dimension, and there was no evidence 2003; Chambers, Taylor, & Potenza, 2003; Cloninger, 1987, 1988;
of relations between early drug use and the various ECF indices. A Zuckerman, 2006). Research in both humans and animals suggests
study of later drug use in the same sample of boys and a smaller that impulsivity is multidimensional (Evenden, 1999; Whiteside &
sample of girls at ages 15–17 revealed a small correlation between Lynam, 2001) and that some of its manifestations grow in strength
performance on a response inhibition task (stop signal reaction during adolescence (Casey, Getz, & Galvan, 2008; Chambers &
time paradigm) and use of alcohol and other drugs (Nigg et al., Potenza, 2003; Chambers et al., 2003; Spear, 2000a). In particular,
2006). However, the sample was drawn primarily from families sensation seeking, the attraction to novel and exciting experiences
with a history of drug abuse, and the ECF-drug use relation did not peaks during adolescence (Romer & Hennessy, 2007; Zuckerman,
emerge until mid adolescence. It is not possible therefore to rule out 2006), likely reflecting enhanced dopamine release to the ventral
the hypothesis that early drug use influences ECF rather than the striatum and prefrontal cortex (Chambers et al., 2003; Spear, 2000a,
other way around. Furthermore, the relation was only observed for 2000b). Based on this increase, one would expect early risk takers
one of many ECF tasks, making it difficult to determine the general- to exhibit higher levels of sensation seeking, a pattern confirmed in
ity of the finding. Hence, little is known about the relation between one study of early drug use initiation (Crawford, Pentz, Chou, Li, &
ECF and risk taking in preadolescent community samples, and what Dwyer, 2003).
evidence there is suggests that ECF is not strongly related to early Other forms of impulsivity may also correlate with early risk
initiation of risky behavior. behavior. For example, tendencies to act without thinking have
Other research has examined the relation between ECF and risk been studied under the rubric of poor behavioral control (Block,
taking tendencies during childhood and adolescence (Crone & van Block, & Keyes, 1988; Wong et al., 2006) or as part of novelty seek-
der Molen, 2004; Hooper, Luciana, Conklin, & Yarger, 2004; Lamm, ing in Cloninger’s system (1988). This research indicates that early
Zelazo, & Lewis, 2006; Overman et al., 2004). However, this research levels of poor behavioral control foreshadow later drug use, find-
tends to use proxies for risk taking, such as the Iowa Gambling Task ings consistent with models put forth by Cloninger (1988), Tarter et
(IGT) (Bechara, Damasio, Damasio, & Anderson, 1994), rather than al. (2003), and Moffitt (1993). Indeed, early manifestations of poor
actual initiation of drug use or other risky behavior. This task as well behavioral control might reflect the effects of the same mechanisms
as others test the ability to process and keep track of reward con- that underlie sensation seeking. However, less is known about how
tingencies and are often treated as an index of ECF in itself. We refer closely sensation seeking and poor behavioral control correlate dur-
to these tasks as measures of reward processing because they tend ing preadolescence when many risk behaviors first emerge.
to be associated with orbitofrontal functioning (Fellows & Farah, Several theories of cortical and subcortical brain development
2005; Wallis, 2007). However, this research indicates that working focus on the relative imbalance between subcortical reward sys-
memory as well as other aspects of ECF, such as ability to exert cog- tems that mature more rapidly than slowly developing frontal
nitive and behavioral control, is not related to reward processing in control systems, resulting in poor control over impulsive behav-
youth. ior during adolescence (Casey et al., 2008; Nelson et al., 2002;
Research with adults has found that some components of ECF, Steinberg, 2008). These models base their predictions on structural
working memory and reversal learning, are related to performance brain imaging studies showing that dorsal and frontal brain areas
in the IGT (Bechara, Damasio, Tranel, & Anderson, 1998; Bechara exhibit a slower course of pruning and myelination than ventral
& Martin, 2004). However, this relation has only been observed and occipital areas (Gogtay et al., 2004; Sowell et al., 2003). Indeed,
in persons who are drug dependent or who suffered brain lesions these studies indicate that complete maturation of these frontal
that affect decision making. Nevertheless, in commenting on these areas does not occur until the third decade of life. Based on these
findings, Bechara and Martin (2004) noted that “the integrity of models, one would expect that ECF would have only limited ability
decision making seems to be dependent on the intactness of work- to control impulsive behavior tendencies in early adolescence. Nev-
ing memory—that is, the participant’s decision making is affected ertheless, models of neurobehavioral risk for SUD (Moffitt, 1993;
by having an abnormal working memory” (p. 160). In their research, Nigg et al., 2004; Tarter et al., 2003) anticipate that ECF and impul-
Farah and Fellows (2005) found that both working memory capac- sivity will be inversely related. Consistent with this expectation,
ity and reversal learning deficits may underlie performance on this an intervention to improve working memory ability in children
task. ages 7–12 with ADHD found that the resulting improvements in
Other research with normal subjects has found evidence that ECF were accompanied by reductions in parent reports of impulsive
working memory capacity influences performance on reward pro- tendencies (Klingberg et al., 2005).
2918 D. Romer et al. / Neuropsychologia 47 (2009) 2916–2926
Impulsivity may also play a role in the manifestation of vari- The sample was predominantly non-Hispanic white (63%) and African Amer-
ous types of externalizing problems that have also been associated ican (27%) with nearly equal representation of boys (49%) and girls (51%). Mean
age was 11.4 (SD = .9), at enrollment, with 10% in grade 4, 49% in grade 5, 26% in
with drug use and other risky behaviors in childhood and ado-
grade 6, and the rest (15%) in grade 7. Sixty-six percent of participants lived in
lescence. Indeed, sensation seeking and poor behavioral control households with married parents. Average household size was 4 individuals. Median
are major characteristics of externalizing behaviors (Caspi et al., years of parental education were 14. Hollingshead’s Two-Factor Index of Social Status
1995; White et al., 1994). In addition, externalizing problems tend (reversed scored) (Hollingshead & Redlich, 1958, 2007) was 47.0 ± 15.8 correspond-
to correlate moderately with internalizing symptoms in children ing to the lower range of middle-class.
2.3. Neurocognitive battery digits on the card (e.g., three “4’s” goes into the 3 pile). The Stroop Effect is the reac-
tion time difference between the congruent and incongruent conditions. This task
Using a battery of neurocognitive tasks, we assessed the following three has the advantage over the classical color-naming Stroop in that it does not depend
prefrontally mediated executive cognitive functions: Working Memory, Cognitive on skilled automatic reading (since poor readers will do paradoxically better on the
Control, and Reward Processing. Although these three functions are sufficiently dis- classic Stroop). Functional neuroimaging studies have shown that for both Color and
tinct in their functions to merit the label “system,” and can be assessed by separate Counting Stroop, the incongruent condition activates the ACC relative to the congru-
sets of tasks, it is also true that they operate in concert (Duncan & Owen, 2000). ent condition (Bush et al., 1998). For the Stroop task, the reaction time difference
Accordingly, the tasks included here were intended to place disproportionately score (reaction time difference between incongruent and congruent conditions) was
heavy demands on a particular system, not to cleanly isolate that system (Huizinga, the dependent measure used in our analyses.
Dolan, & van der Molen, 2006; Miyake et al., 2000, 2001). All but one, the Digit Span
subtest from the Wechsler Intelligence Scale for Children-IV, (Wechsler, 2003) were
administered using laptop computers. 2.3.2.2. Flanker task. In this task, developed by Eriksen and Eriksen (1974), subjects
are asked to press a left-hand or right-hand response key depending on the direction
2.3.1. Working memory indicated by a central arrow. The task is made challenging by flanking the central
Working memory plays an essential role in many activities that are not tests arrow with rows of other arrows, which can point in either the same direction (con-
of memory per se. The ability to hold the present context or goals of a complex gruent) as the central arrow or in the opposite direction (incongruent condition)
task in mind requires working memory (Cohen, Cohen, & Ayache, 1992; Kimberg (Eriksen & Eriksen, 1974). The dependent measures in this task are the reaction
& Farah, 1993). More specifically, working memory is an underlying component of time differences between congruent and incongruent trials. Opposite flankers cause
psychological self-regulation, which has been found to be deficient in children at response conflict and thus require cognitive control, the degree of which is corre-
risk for drug use (Tarter, Kirisci, Habeych, Reynolds, & Vanyukov, 2004). Working lated with activation of the ACC (Casey et al., 2000). For the flanker task, the final
memory is most reliably associated with dorsolateral PFC (Mehta et al., 2000). We reaction time score (reaction time difference between incongruent and congruent
administered four tasks to assess this important function. conditions) was the dependent measure used for analyses.
2.3.1.1. Corsi Block Tapping. This task is a non-verbal variant of the Digit Span task 2.3.3. Reward processing
(Milner, 1971). The participant views a set of identical blocks that are spatially dis- An important aspect of executive function is the ability to resist the pull of reward
persed on the screen. The blocks are individually lit up in a random sequence. The stimuli, especially when they may lead to losses. This general concept has been oper-
participant is asked to tap each box in the reverse order of the sequence of lit boxes. ationalized in different laboratory tasks that pit the pull of a reward stimulus against
This task is considered a task of spatial working memory as the sequence must the need to withhold or delay a response to avoid loss. Deficits in reward processing
be maintained and reversed in working memory in order to guide the subject’s have been linked to impulse disorders in adolescents that are predisposing for drug
response. Performance on this task is dependent on right prefrontal brain regions abuse (Ernst et al., 2003) or to adults suffering from lesions to orbitofrontal regions
(Banich, 2004). The Corsi Block Tapping total correct score was used as the dependent (Fellows & Farah, 2005). We administered two tasks to assess reward processing.
variable in analyses.
WM is working memory; CC is cognitive control; RP is reward processing; E1 is Eysenck1, the absence of thinking when acting; E2 is Eysenck2, reports of problems associated with acting without thinking; SS is sensation seeking;
0.03
0.17
RB4
2.5. Analysis
Descriptive analyses were conducted using SPSS. Because we used multiple mea-
sures to assess ECFs and impulsivity, it was important to identify underlying factors
.097
0.29
0.45
RB3
for each set of indicators (Huizinga et al., 2006) Hence, we used structural equation
modeling to identify the factors and to test relations between them. In particular,
we tested models in which measures of the three types of ECF and the two measures
.133
.312
of impulsivity predicted risk taking as assessed by a variety of behaviors. We antici-
0.38
0.69
RB2
pated that risk behaviors would form a single factor but that impulsivity might form
two factors, one for sensation seeking and another for poor behavior control (lack
of planning or thinking and problems associated with those tendencies) assessed
.323
.209
.122
0.50
0.21
RB1
by the Eysenck scale. Assessment of externalizing behavior tends to reveal correla-
tion between externalizing and internalizing problems (Krueger, Chentsova-Dutton,
Markon, Goldberg, & Ormel, 2003; Youngstrom, Findling, & Calabrese, 2003). Hence,
.280
.237
.378
.318
we expected to find the same pattern in our data.
PB2
9.0
7.0
We used the program EQS to test alternative measurement models and relations
between factors (Bentler, 2004). The program allows for the simultaneous estimation
.606
.104
.162
.127
.186
of direct and mediating effects on latent variables. It also provides the ability to
12.3
8.2
PB1
impute missing values, which in this dataset were primarily observed for a measure
of working memory using the digit-span test. Due to an administration error, scores
for this test were not available for approximately 16% of the sample. Additionally, EQS
.096
.208
.337
.251
.166
.213
offers robust statistics, which adjust for the effects of departures from multivariate
11.4
3.1
normality due to skewness and kurtosis. All coefficients shown in the results have
SS
probabilities evaluated with robust standard errors.
We assessed goodness of fit using three criteria. First, a Chi-square test (2 ) was
.400
.336
.280
.209
.205
.222
.312
0.32
0.30
used to compare the predicted covariance matrix with the observed matrix. We used
E2
the Yuan-Bentler scaled 2 which is provided for models with robust standard errors
(Yuan & Bentler, 1998). A non-significant value for this measure indicates that the
predicted model accounts for the covariation between measures. Chi-square tests,
.204
.455
.356
.382
.303
.487
.257
.271
0.32
0.40
however, are very sensitive to sample size, and significant values do not necessarily
E1
indicate a poor fit with large samples. For this reason, we augment this measure with
additional indices that are not as sensitive to sample size and represent a graded
index of fit (Hu & Bentler, 1995): the Comparative Fit Index (CFI) and Root Mean
−.105 −.009
.049
.045
.038
.058
−.101 −.020
−.030
−.144 −.154
−.103 −.021
Square Error of Approximation (RMSEA).
24.6
11.3
RP2
CFI is a comparison of two fit functions: one from the covariance matrix esti-
mated from the fitted model and one from a model that assumes no association
.098
.008
.023
−.030
.016
−.113
between the observed variables. Higher values reflect the relative advantage of the
RP1
1060
357
proposed model over a model with no association. Values greater than .90 are con-
sidered acceptable (Hu & Bentler, 1995).The RMSEA measures the mean residuals
between the observed and predicted covariance matrix. Departures from zero rep-
resent poorer fit. RMSEA values less than or equal to .05 are considered acceptable
.008
.062
−.082
.054
.030
−.033
−.162
−.107
−.101
−.015
−.113
0.28
0.23
CC2
(Kaplan, 2000).
−.042
−.045
.042
−.028
−.032
−.029
.053
−.080
−.109
−.012
.019
−.014
40.4
31.3
CC1
3. Results
−.099
.003
.342
.007
−.039
.047
−.057
.037
−.127
−.072
.074
−.016
WM4
Note: Significant coefficients at p < .05 are in bold and at p < .01 are italicized and shaded.
sures analyzed in this study as well as their relations with male
30.7
19.3
Intercorrelations between gender, age, ECFs, impulsivity, problem and risk behaviors.
gender and age. For each measure, means and standard deviations
are listed in the last rows of the table. Male youth tended to exhibit
better cognitive control on the Flanker task but not on the Stroop,
.003
.066
−.332
−.063
−.063
−.043
.059
−.028
−.024
−.103
−.146
.015
.015
−.116
WM3
3.1
16.0
.004
−.288
.064
.085
.002
.002
−.252
.243
−.039
−.120
−.189
−.013
.014
110.7
13.8
.049
.236
−.060
WM1
−.054
.028
−.022
.054
−.058
−.083
−.001
−.277
.079
.156
.013
.116
.009
.068
.054
.082
.053
.120
−.166
.231
.169
−.156
.146
.123
−.015
.116
.114
−.113
.099
−.084
.069
.243
.028
.080
.001
.093
−.120
−.047
.134
.146
−.031
.071
−.012
.119
Male
0.49
0.50
RB2 Gambling
Characteristic
RB4 Smoking
RP1 Reversal
PB2 External
RB3 fighting
PB1 Internal
RB1 Alcohol
CC1 Flanker
WM1 Corsi
CC2 Stroop
RP2 BART
Mean
also highly correlated and related to risk behaviors. Finally, the four
Age
SD
SS
a single factor, the externalizing score had a stronger loading than Problem behaviors
the internalizing score. Internalizing .643 –
Externalizing .943 <.001
Examination of residuals between predicted and observed cor-
*
relations revealed that boys were more likely to exhibit fighting Note: To identify the model, one variable on each factor was fixed to an unstan-
than girls, that girls were more likely to exhibit internalizing prob- dardized value of 1. These variables do not have significance tests.
lems than boys, and that internalizing problems declined with age.
Because these deviations from the measurement model were not
relevant to our tests of relations between ECF and risk behaviors, revealed that none of the ECFs directly predicted risk behavior or
we included them as additional correlates in the model. This result- problems apart from their relations with impulsivity. Hence, we
ing model provided a good fit to the data, 2 (110) = 174.8, p < .001; dropped those paths as well as insignificant correlations between
CFI = .93, RMSEA = .038 (90% CI = .026, .048). exogenous predictors to produce the final model shown in Fig. 1.
This model fit the data well, 2 (130) = 191.6, p < .001; CFI = .93,
RMSEA = .034 (90% CI = .022, .044). Significant paths in the model
3.2. Testing relations between factors indicated that age was positively related while working memory
and reversal learning were negatively related to impulsivity. In
Having defined an appropriate measurement model, we pro- addition, impulsivity was positively and strongly related to both
ceeded to assess how well each of the ECFs predicted impulsivity, risk and problem behaviors. However, problem behaviors were no
risk behavior, and externalizing problem behaviors. This analysis longer related to risk behavior after controlling for impulsivity. That
Fig. 1. Standardized path coefficients for SEM predicting risk behavior. Indicators for each factor are in Table 2. Significant path coefficients (p < .05) are in bold. Unexplained
variation in each factor (1–R2 ) is indicated by open circles and associated coefficients.
2922 D. Romer et al. / Neuropsychologia 47 (2009) 2916–2926
is, the path from problem to risk behavior was not significant, p = .14. in the small amount of variation explained in impulsivity, their
Although Stroop performance (cognitive control) was highly related relations with impulsivity were not strong. Performance on the
to working memory performance, none of the other ECF tasks was cognitive control Stroop task was highly related to working mem-
significantly related to impulsivity. ory performance; however, it was not related to either impulsivity
The model indicates that impulsivity mediates the effects of age or risk behaviors apart from working memory. Hence, the findings
and ECF on both risk and problem behavior. We further tested the only support an indirect role for ECF in the emergence of early risk
possibility that impulsivity explains both risk taking and external- taking.
izing problems by restricting the path from problems to risk taking The central role of impulsive tendencies in the emergence of
to zero. This produced only a slightly less adequate fit to the data, early risk behaviors is consistent with findings observed by others
2 (1) = 1.11, p > .15. Hence, there was support for only one path lead- (Block et al., 1988; Crawford et al., 2003; Wong et al., 2006). It is also
ing to risk taking in this sample of preadolescents. Furthermore, the consistent with the theorizing of Chambers et al. (2003) and Spear
model accounted for nearly 70% of the variation in the risk behavior (2000a, 2000b), who suggest that adolescence is the period when
factor and slightly over 50% of the variation in problem behaviors. the rise in activity of the dopamine system encourages experimen-
This indicates that impulsivity can account for a large share of the tation with novel and exciting behaviors. Our finding that age was
variation in both of these outcomes. Nevertheless, the amount of positively related to impulsivity and that impulsivity mediated the
variation explained by ECFs, age, and gender was quite small (about relation between age and risk behavior is also consistent with this
8%). This indicates that impulsivity was largely influenced by factors explanation.
outside the model. The finding that impulsivity was highly related to externaliz-
We examined residual correlations between the predicted and ing behaviors was expected since such problems are characterized
observed correlation matrix to identify unexplained relations. Only by deficits in impulse control (Gottfredson & Hirschi, 1990;
one stood out: performance on the two-back task (working mem- Waschbusch, 2002; Waschbusch et al., 2002). We were surprised
ory) was negatively related to fighting, r = −.20, p < .01. Apparently however to find that externalizing behaviors did not correlate with
this relation was unique to this measure of working memory and risk behavior once impulsivity was controlled. Tarter’s neurobe-
to fighting as none of the other risk behaviors was correlated with havioral disinhibition model explicitly predicts such an association
any of the working memory scores apart from what was explained (Tarter et al., 2004, 2003). Furthermore, longitudinal studies find
in the model. that early evidence of conduct disorder and other externalizing
behaviors is related to later drug use and fighting (Zucker, 2006).
However, impulsivity may be the central predisposing condition
3.3. An alternative model
underlying both early manifestations of conduct disorder and later
health-risk behavior. Studies that examine very early temperamen-
Although we found strong support for the model in Fig. 1, it
tal factors find that behaviors symptomatic of poor behavior control
is always possible that an alternative model might account for
predict later externalizing problems (Caspi et al., 1995; White et
the data equally well. We tested one such model by reversing the
al., 1994), suggesting that impulsivity is an important factor in the
roles of impulsivity and problem behaviors. That is, we placed
development of such outcomes. Our results support this conclusion,
externalizing problems as the more proximal correlate of ECFs
although a potential additional link between externalizing behavior
and demographics with impulsivity acting as a potential media-
and risk behavior cannot be ruled out given the presence of some,
tor of the relation between problems and risk behavior. This model
albeit statistically non-significant, relation that remains.
also fit the data: 2 (130) = 197.3, p < .001; CFI = .92, RMSEA = .035
The finding that working memory capacity was indirectly
(90% CI = .024, .045). However, although externalizing behavior was
related to risk behavior initiation by virtue of its relation with
strongly related to impulsivity (.733, p < .001), it was not directly
impulsivity has not to our knowledge been previously observed.
related to risk behavior (.223, p = .16). On the other hand, impulsiv-
This finding suggests that youth with greater ability to manip-
ity was strongly related to risk behavior (.641, p < .001). Hence, this
ulate information in working memory have greater control over
model produced essentially the same result as the favored model:
sensation seeking and other impulsive drives. The finding is also
impulsivity is strongly related to externalizing behavior as well as
consistent with research linking working memory performance
risk behavior but externalizing behavior is only weakly related to
with proxies for risky decision making, such as the IGT (Bechara
risk behavior apart from impulsivity.
et al., 1998, 2001; Fellows & Farah, 2003, 2005). It is also consistent
with interventions that find that improved working memory in chil-
4. Discussion dren leads to reduced symptoms of impulsive behavior (Klingberg
et al., 2005). The importance of working memory to the overall
This study of a community sample of pre-adolescent youth iden- ability of PFC to exert control over behavior has often been noted
tified early initiators of several risk behaviors described by a single (Fuster, 1997; Miller & Cohen, 2001) and is consistent with theo-
factor, confirming the existence of a general risk-taking tendency ries of PFC function that place particular emphasis on this ability.
at this early age. We also found evidence for a general tendency It is quite likely that youth who have limited ability to consider
toward impulsive behavior defined by both sensation seeking and multiple and potentially conflicting goals are less likely to think
lack of thinking and planning when acting. Furthermore, consistent before acting and to temper their interest in novel and exciting
with our expectations concerning the importance of impulsivity as experiences. This would lead them to develop a relatively stable
a precursor to early risk behavior, impulsivity was strongly related style of behavior that is observed in trait measures of impulsivity.
to risk behavior initiation. In addition, differences in externalizing Working memory capacity is also strongly related to general cogni-
and correlated internalizing problem behaviors were highly related tive ability as assessed in intelligence tests (Colom, Abad, Quiroga,
to impulsivity, but these behaviors were not strongly related to risk Shih, & Flores-Mendoza, 2008; Shamosh et al., 2008). It is possi-
taking once impulsivity was controlled. This finding suggests that ble therefore that working memory capacity is responsible for the
impulsivity plays a large role in the emergence of both externaliz- small but persistent correlation that has been observed between IQ
ing and health-risk behaviors. Both working memory performance and youth engagement in multiple risk behaviors (Henry & Moffitt,
and reversal learning (reward processing) were inversely related 1997; Lynam, Moffitt, & Stouthamer-Loeber, 1993).
to impulsivity. However, none of the ECFs was directly related to The finding that reversal learning performance (reward process-
risk behavior apart from relations with impulsivity, and as reflected ing) was inversely related to impulsivity has also to our knowledge
D. Romer et al. / Neuropsychologia 47 (2009) 2916–2926 2923
not been observed. This finding suggests that youth with deficits in why these measures of ECF correlate with drug use more strongly
the ability to adjust to new reinforcement contingencies are more in adults (Bechara & Martin, 2004) or youth with more serious sub-
likely to exhibit impulsive tendencies. The finding is consistent stance use disorders (Tarter et al., 2003). One possibility is that as
with studies of adults who suffered lesions to orbitofrontal brain youth experience increased drug use, ECFs become compromised
regions and who also exhibit impulsive decision making (Fellows so that their performance deteriorates. There is evidence that heavy
& Farah, 2003; Rolls, Hornak, Wade, & McGrath, 1994). Youth with use of potentially addictive drugs alters brain function produc-
such deficits may well develop impulsive styles of behavior that ing deficits in working memory and inhibitory control (Jentsch &
fail to recognize changes in reward contingencies. Furthermore, Taylor, 1999). Over time, these effects could introduce correlations
youth who exhibit weak performance on both working memory and between ECFs and drug use. For example, the finding that ECF did
reversal tasks would be expected to develop even greater impul- not correlate with drug use at ages 12–15 (Nigg et al., 2004) but did
sive behavior styles. Indeed, working memory and reversal learning at ages 15–17 (Nigg et al., 2006) is consistent with such an account.
performance were largely unrelated, consistent with the different Another possible explanation for the absence of direct relations
brain regions to which they have been associated (dorsolateral for between ECFs and drug use in adolescents is that youth with poor
working memory and orbitofrontal for reversal learning). working memory are more susceptible to the interfering effects of
Despite the directionality in our SEM, the relations between drugs on their behavior (Finn, Justus, Mazas, & Steinmetz, 1999).
impulsivity and either working memory or reversal learning perfor- As a result, they are more susceptible to developing dysfunctional
mance are purely correlational and subsequent waves of our study trajectories of drug use. Thus, deficits in working memory and other
may help to determine whether development of ECF in general and ECFs might not correlate with drug use and SUD until later in life
working memory or reversal learning in particular predict declines after the deleterious effects of working memory limitations have
in impulsivity. It is possible for example that impulsivity interferes had their effect. This explanation is consistent with the findings of
with working memory performance by challenging the system with Tarter et al. (2003) that early ECF did not predict drug use at age 16
task irrelevant response tendencies that are difficult to control. This but did predict SUD at age 19.
may lead to poorer performance on working memory tasks. It is also
possible that impulsivity reduces attention to changes in reward
4.2. Age related changes in risk behavior and ECF
contingencies. If either of these were the case, then developmental
changes in impulsivity would predict changes in working memory
One finding that stands out in the pattern of age related differ-
or reversal learning rather than the other way around.
ences in risk behavior is that although our sample of preadolescents
Another possibility regarding the relation between ECF and
tends to exhibit increasing risk behavior with development, they
impulsivity is that as adolescents mature, their ability to control
also exhibit increasing development of working memory. This pat-
impulsivity increases and is more readily observable across differ-
tern suggests that engaging in risk behavior is related to cognitive
ent facets of ECF. Research on the development of ECF suggests that
maturation and that exploring these risks is part of the natural
cognitive control ability is not fully mature until age 15 and that
development of adolescents. The finding that better working mem-
working memory and reward processing continues to mature into
ory and reversal learning are related to less impulsivity suggests
young adulthood (Huizinga et al., 2006; Luciana, Conklin, Hooper,
that the continued development of these capabilities may even-
& Yarger, 2005). Perhaps these functions, especially cognitive con-
tually overcome the adverse influences of impulsive tendencies,
trol, are not sufficiently developed until mid-adolescence to slow
perhaps leading to their decline.
down the increase in impulsivity that characterizes adolescence.
Our results indicate that age was positively related to working
memory and to Stroop performance. Although these functions were 4.3. Implications for intervention
not strong enough to inhibit age related increases in impulsivity,
they may gain in strength as the PFC matures. This may explain why Depending on the ultimate relations we observe between impul-
the research program by Nigg et al. (2006) finds a relation between sivity, ECF, and risk behavior, we will draw different conclusions
impulse control and drug use at ages 15–17 but not at ages 12–15 about appropriate interventions to reduce the risk of excessive
(Nigg et al., 2006). engagement in potentially addictive and harmful behaviors. If ECF
The finding that measures of cognitive control (Stroop and eventually matures to the point where it begins to control heavy use
flanker tasks) and reward processing (BART) were not related to of drugs, then efforts to improve ECF should be a focus. However,
impulsivity, risk behaviors, or externalizing symptoms was some- if impulsivity is the major contributor to excessive drug use, then
what surprising given the central roles that they are assumed to other strategies may be needed. There is evidence that training of
play in these outcomes. It is important to keep in mind however life skills can reduce drug use (Botvin & Schenke, 1997), but less is
that one measure of cognitive control (Stroop) was highly related known about how well these skills can control drug use for those
to working memory and hence may not have contributed predic- with high levels of impulsivity. Future research may need to focus
tion beyond what it shared with that ability. Nevertheless, other on this question, especially if ECF proves not to be critical to drug
research has also failed to find any relations between ECFs and early use prevention.
use of drugs (Nigg et al., 2004; Tarter et al., 2003), and research If drug use during adolescence retards the development of ECF
using proxies for risk taking such as the IGT also fail to find strong and this enhances the risk for emergence of SUD and other disor-
relations with ECFs in adolescents (Crone & van der Molen, 2004; ders, then efforts to prevent early drug use itself will be a major
Hooper et al., 2004). Results of the BART have to our knowledge focus of attention. Indeed, national campaigns to prevent drug
only been correlated with drug use in small and older adolescent use emphasize this trajectory. This explanation is consistent with
samples (Aklin et al., 2005; Lejuez et al., 2003b). considerable research indicating that drug abusers exhibit deficits
in reward processing (Bechara, 2004; Bechara & Martin, 2004;
4.1. Discrepancies between adult and early adolescent Goudriaan, Grekin, & Sher, 2007). It is also possible, however, that
relationships early impulsive and disruptive behavior leads to the use of drugs
that then interferes with the normal development of age appropri-
Given the absence of relations between several ECFs with early ate ECF. From the perspective of this explanation, early intervention
risk behaviors and the weak relation of working memory and rever- to treat impulsive and disruptive behavior should reduce the like-
sal learning in comparison with impulsivity, it is important to ask lihood of progressing on the dysfunctional trajectory.
2924 D. Romer et al. / Neuropsychologia 47 (2009) 2916–2926
In addition to these two explanations, it is also possible that early expectancy with functional magnetic resonance imaging. Proceedings of the
manifestations of risk for SUD and conduct disorder are mere mark- National Academy of Sciences, 97(15), 8728–8733.
Caspi, A., Henry, B., McGee, R. O., Moffitt, T. E., & Silva, P. A. (1995). Temperamental
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