Elysia Poggi Davis
Jacqueline Bruce
Megan R. Gunnar
Institute of Child Development
University of Minnesota
Minneapolis, MN 55455-0345
The Anterior Attention
Network: Associations
With Temperament and
Neuroendocrine Activity
in 6-Year-Old Children
Received 23 October 2000; Accepted 17 April 2001
ABSTRACT: The capacity to effortfully control or regulate behavior is of central importance in
social development. Individual differences in effortful control have been hypothesized to re¯ect
biologically based, temperamental variation among children. Posner and Rothbart (1994, 1998)
have argued that the anterior attention system, which includes areas of the midprefrontal cortex,
underlies effortful control capabilities. Furthermore, components of the anterior attentional system
are believed to be involved in the regulation of reactive, emotion-related system, such as the
hypothalamic±pituitary±adrenocortical system. We assessed 58 six-year-old children's performance on neuropsychological tasks that have been found in functional imaging studies to involve
the anterior brain regions which Posner (1995) describes as comprising the anterior attentional
system. We then related performance on these tasks to delay of grati®cation tasks and parent
report of temperament and behavior problems as well as home and laboratory cortisol levels.
Results provide some support for Posner and Rothbart's model and suggest a relationship between
the anterior attentional system and cortisol regulation. However, these data also illustrate the
multifaceted nature of effortful control and the need for care when attempting to understand the
neural systems involved in the effortful regulation of behavior. ß 2002 John Wiley & Sons, Inc.
Dev Psychobiol 40: 43±56, 2002
Keywords: children; temperament; cortisol; effortful control
Recently, there has been renewed interest in effortful or inhibitory control in research on social and
emotional development. Effortful control is the capacity for active, voluntary inhibition or modulation of
response. It is the ability to purposefully regulate
behavior, to inhibit a prepotent response, or to resist
Correspondence to: E. Poggi Davis
Contract grant sponsor: NIMH
Contract grant number: MH56958
ß 2002 John Wiley & Sons, Inc.
DOI 10.1002/dev.10012
interference (Bjorklund & Kipp, 1996). Young children show marked increases in their capacity for effortful control with development. However, they appear
to maintain fairly stable rank ordering. Thus, children who score lower than peers on effortful control tasks at one age tend to do so again at later ages
(Kochanska, Murray, & Harlan, 2000; Kochanska,
Murray, Jacques, Koenig, & Vandegeest, 1996). Individual differences in effortful control are related
to moral development and social competence among
preschool-aged children (Eisenberg et al., 1996;
Kochanska, Murray, & Coy, 1997; Kochanska et al.,
1996). In sum, effortful control appears to be a
44
Davis, Bruce, and Gunnar
relatively stable characteristic that exhibits developmental change and is related to signi®cant aspects of
development.
Posner and Rothbart (1994)Q3 have attempted to
de®ne the neural systems underlying the capacity for
effortful control. While effortful control is clearly a
heterogeneous construct involving multiple systems,
they argue that a neural system involving areas of the
midprefrontal cortex that includes the anterior cingulate gyrus (ACC) is at the core of the capacity to
effortfully regulate behavior (Posner & Rothbart,
1994, 1998). This system has been labeled the anterior
attention system (Posner, 1995). The anterior attention system is a construct that includes neural systems,
in particular the ACC, that have been proposed to be
involved in modulation of attention and executive
function (Posner & Dehaene, 1994). The ACC plays
an essential role in initiation, motivation, and goaldirected behavior (Casey, Trainor, Giedd et al., 1997).
It is involved in controlling or directing attention and
action by modulating cognitive and affective processing. Lesions to the ACC produce lack of control over
thought and behavior (Posner, 1995).
It has been argued that there are two major
subdivisions of the ACC that subserve distinct
functions (see Bush, Luu, & Posner, 2000 for review).
It has been proposed that the cognitive subdivision is
part of a distributed attentional network that maintains
reciprocal connections with the prefrontal and parietal cortices as well as motor areas. The affective
subdivision maintains connections with various limbic structures and has out¯ow to autonomic, visceromotor, and endocrine systems. It appears to play an
important role in assessing the salience of emotional
and motivational information and the regulation of
emotional responses. There is evidence for a reciprocal relationship between the two subdivisions of the
ACC. Suppression of emotional circuitry, including
components of the limbic system, has been observed
during tasks that activate the cognitive subdivision of
the ACC (Bush et al., 2000; Whalen et al., 1998).
Additionally, the experience of negative emotions has
been found to result not only in limbic activation but
also in simultaneous deactivation of frontal areas
involved in cognitive inhibitory control. It has been
argued both that prefrontal areas involved in attention play a role in regulation of reactive or negative
emotional systems and that limbic areas involved in
reactive emotions may inhibit prefrontal systems
involved in attention (Mayberg et al., 1999). The
close relationship of the ACC to systems involved in
regulation of emotional processing, motor areas, and
memory systems make it well suited to integrate
thought and behavior and to regulate emotional
systems (Rothbart, Ahadi, & Evans, 2000; Rothbart,
Derryberry, & Posner, 1994). Rothbart and colleagues
have argued that individual differences and developmental change in this system are related to individual
differences in the temperament dimension of effortful
control.
To investigate individual differences in effortful
control, some researchers have made use of parent
report measures of this dimension of temperament.
Such a measure can be derived from the Children's
Behavior Questionnaire (CBQ), a parent report instrument developed for children 3 to 8 years of age (Ahadi,
Rothbart, & Ye, 1993). There are scales on the CBQ
that assess parents perceptions of the child's capacity
to inhibit prepotent responses (i.e., play games such as
red light/green light) and maintain and direct their
attention as well as a scale assessing impulsivity (i.e.,
speed of response). When factor analyzed with oblique
rotation, these scales load on two conceptually different higher order factors: Effortful Control, which
consists of Inhibitory Control, Attention Focusing,
Perceptual Sensitivity, Smiling, and Pleasure in Quiet/
Mildly Stimulating Activities; and Surgency/Extroversion, which consists of Impulsivity, Activity Level,
low Shyness, and Pleasure in Highly Stimulating
Activities.
Inhibitory Control and Attention Focusing are the
scales that seem to most clearly assess behaviors similar to those measured on tasks requiring the anterior
attentional network. However, children's scores on
Inhibitory Control and Impulsivity also are typically
correlated. In other studies, researchers have sometimes focused on these two scales to index effortful
control (see Kochanska et al., 1996). Thus, despite
being conceptually distinct (inhibition of prepotent
responses vs. speed of response), in practice it seems
likely that parent's perceptions of a child's effortful
control ability may be re¯ected in both of these scales,
and perhaps both of the related higher order factors
(Effortful Control and Surgency/Extroversion). Thus,
it might be important to examine both of these scales
and their higher order dimensions in relation to
observations of behavior regulation and neuropsychological tasks assessing neural systems thought to
comprise the anterior attention network.
Links between cognitive assessments of structures
considered to be part of the anterior attentional system
and social behavior and temperament remain tenuous.
To date, there is only one published study that examined such associations in typically developing
children. The results of this study provide some
evidence that children around 3 years of age who are
less affected by spatial con¯ict were rated by their
parents as higher in their ability to control their
The Anterior Attention Network
behavior (effortful control) and had higher scores on
laboratory measures of inhibitory control (GerardiCaulton, 2000). It is the goal of our study to further
elucidate these associations by investigating the
relationship between performance on tasks that have
been shown, to involve the ACC, (Casey, Trainor,
Giedd et al., 1997; Casey, Trainor, Orendi et al., 1997)
and behavioral measures of effortful regulation in a
normative population of children.
Effortful regulation of behavior allows the individual to modulate more reactive emotional systems
(Rothbart et al., 1994). Evidence suggests that the
ability to effortfully control behavior and attention
is related to the reactivity and regulation of stress
systems (Dettling, Parker, Lane, Sebanc, & Gunnar,
2000; Gunnar, Tout, de Haan, Pierce, & Stansbury,
1996). Furthermore, as discussed, the ACC, a key
component of the anterior attentional system, also is
involved in the regulation of emotional behavior.
There is evidence that the emotional subdivision of
the ACC is involved in the regulation of endocrine
systems (Bush et al., 1999). One neuroendocrine
system whose activity may be in¯uenced by activity
of the ACC is the hypothalamic±pituitary±adrenocortical (HPA) system. This system produces the
glucocorticoid (GC) hormone, cortisol. It has been
demonstrated that lesioning the ACC disrupts regulation of the HPA system's response to psychological
stress in rats (Diorio, Viau, & Meaney, 1993).
Evidence suggests that these relations are reciprocal
in nature as GCs also affect the functioning of the
prefrontal cortex, including the ACC (e.g., Karreman,
Moghaddam, 1996; Lowy, 1994). Research involving
experimental administration of exogenous GCs to
adult human and nonhuman primates indicates that
highly elevated levels of GCs interfere with frontal
processes, such as inhibitory control, attention
regulation, and planning (Kopell, Wittner, Lunde,
Warrick, & Edwards, 1970; Lupien, Gillin, & Hauger,
1999; Lyons, Lopez, Yang, & Schatzberg, 2000;
Young, Sahakian, Robbins, & Cowen, 1999). It is this
model, based on administration of high levels of GCs,
that shapes most assumptions regarding the effects of
GCs on cognition. However, it has been well
documented that the effects of GCs on cognition
follow a U-shaped curve (Lupien & McEwen, 1997).
For many cognitive processes, it has been noted that
while high levels of GCs have a detrimental effect on
performance, very low levels also are associated with
impairments. It is moderate levels of GCs that seem to
be associated with optimal performance on many
cognitive tasks.
We examined whether children would show small
elevations in cortisol in response to the challenge of
45
performing dif®cult cognitive tasks. Based on data
indicating that high levels of cortisol impair performance on tasks mediated by the prefrontal cortex, we
hypothesized that poorer performance on the neuropsychological task assessing the anterior attentional
system would be associated with larger increases in
cortisol production. Furthermore, we predicted that the
children showing the greatest elevations in cortisol
would be rated by their parents as being lower in
Effortful ControlÐin particular, lower in Inhibitory
Control and higher in Impulsivity. In fact, there are
data that lend support to this hypothesis. Several
studies have been performed using parent and teacher
reports of temperament. It has been demonstrated
that children who display higher cortisol levels in a
challenging situation are reported by their parents and
teachers, using the CBQ, to be lower in Effortful
Control (Dettling et al., 2000; Gunnar et al., 1996).
While these studies lend support for the predicted
association between HPA activity and Effortful Control, they are far from conclusive. Multiple studies
have failed to ®nd associations between activity of
the HPA system and the Effortful Control temperament
dimension. In fact, these studies frequently demonstrate associations with the Surgency/Extraversion temperament dimension (e.g., Davis, Donzella, Krueger,
& Gunnar, 1999). Of course, it may be that HPA activity is sometimes associated with Effortful Control and
sometimes with Surgency/Extroversion because of the
conceptual overlap between these dimensions that was
noted earlier. Indeed, both the temperament dimensions of Inhibitory Control and Impulsivity have been
found to relate to cortisol levels (Davis et al., 1999;
Dettling, Gunnar, & Donzella, 1999).
It was the goal of this study to investigate whether
performance on neuropsychological tasks that have
been found to involve the ACC and other neural
structures that have been hypothesized to comprise
the anterior attentional system would be related to
measures of Impulsivity, Inhibitory Control, and
Attention Focusing on the CBQ and salivary cortisol
measures of HPA activity. To help examine these
questions, in the following study we had parents of
6-year-olds complete the CBQ temperament questionnaire. We then administered two neuropsychological tasks known to involve structures that have
been proposed to comprise the anterior attention
system to the children (Casey, Trainor, Giedd et al.,
1997; Casey, Trainor, Orendi et al., 1997). The ®rst
taskÐa Go, No-Go taskÐexamines ability to inhibit
a prepotent response (Casey, Trainor, Orendi et al.,
1997). The second task is an attentional control task
assessing ability to prevent attention from being
captured by salient but irrelevant stimuli (Casey,
46
Davis, Bruce, and Gunnar
Trainor, Giedd et al., 1997). These tasks were chosen
because they involve structures that are components
of the anterior attentional system, and individual
differences in performance on these tasks has been
related to individual differences in the ACC in imaging studies (Casey, Trainor, Giedd et al., 1997; Casey,
Trainor, Orendi et al., 1997). These tasks re¯ect
abilities that are at the core of effortful control and
thus can be used as a way of parsing which links
with temperament are re¯ective of the anterior
attentional system. We examined how functioning
on these neuropsychological tasks related to the
CBQ scales of Attention Focusing, Inhibitory
Control, and Impulsivity as well as the superordinate
dimension of Effortful Control and Surgency/Extroversion.
We added two additional assessments to our procedures to help ground this study and relate it to previous ®ndings. Additionally, these measures allowed
for comparison with the study reported by Gerardi
Caulton (2000), in which associations between delay
of grati®cation tasks and performance on a spatial
con¯ict task, thought to involve structures comprising the anterior attention system, were reported.
First, we examined associations with behavioral
measures of delay of grati®cation. Delay of grati®cation tasks have a long history in research on social
development and socialization (Block & Block,
1980). These tasks are expected to re¯ect the effortful control of behavior. Kochanska and colleagues
have developed a series of laboratory tasks to assess
inhibitory control. Among these tasks, she includes
measures of delay of grati®cation. Kochanska's
inhibitory control battery has high internal consistency and correlates signi®cantly with parent reports
of Inhibitory Control and Impulsivity using the CBQ
(Kochanska et al., 1996).
Finally, because effortful regulation of behavior
is believed to be critically involved in socialization,
and because children who exhibit de®cits on frontal
lobe tasks, such as the one we are using, frequently
exhibit externalizing behavior problems (Toupin,
Dery, Pauze, Mercier, & Fortin, 2000), we also had
parents complete the Social Skills Rating System
(SSRS; Flanagan, Alfonso, Primavera, Povall, &
Higgins, 1996). This instrument yields scores for
internalizing and externalizing behavior problems.
Thus, in addition to examining the interrelations
among neuropsychological measures of inhibitory
control, parent reports of effortful control, and
measures of HPA system activity, we also grounded
this study by determining whether these measures
helped explain variance in parent reports of children's
behavior problems. Six-year-olds participated in the
following study as children of this age were the
youngest studied in the imaging environment by
Casey and were within the age range appropriate for
the use of the CBQ, the SSRS, and the Kochanska
delay of grati®cation tasks.
METHODS
Participants
Sixty-one kindergarten children (31 girls, 30 boys;
range 5 years 11 months±6 years 6 months) were
recruited from a list of families who indicated at the
birth of their child that they were interested in participating in research. Subjects were 95% Caucasian
and came primarily from middle- to upper-middleclass families.1
Procedure
Families agreeing to participate came to the University of Minnesota at 4 p.m. for one laboratory
session that lasted approximately 1 hr. Two female
graduate students served as the experimenters. Each
experimenter tested half of the boys and half of the
girls. Children participated in two neuropsychological
tasks of inhibitory control and two delay of grati®cation tasks. Tasks were presented in the following
order: Go, No-Go, attentional control, dinky toys, and
gift. The delay of grati®cation tasks were always last
because they were presented in the context of giving
the child a prize for participation in the study. Four
saliva samples were collected at 20 min intervals
throughout the session. In addition, families collected
samples on two typical school days in the morning
when the child woke up, between 4 and 5 p.m., and
between 8 and 9 p.m.
Measures
Parent Report Measures. While the children were
being tested, the parent who accompanied the child
(97% mothers) completed two questionnaires, the
SSRS and the CBQ, in a nearby room.
The SSRS is designed to assess behavior problems
in a normal and a clinical population and yields a
summary measure of behavior problems. This scale
assesses the frequency of externalizing behaviors, internalizing behaviors, and hyperactivity in elementary
school children. The mean score for behavior problems
in this sample was 10.7 for girls and 13.2 for boys,
1
Three participants (2 girls) were recruited as pilot subjects
and thus were not included in analyses.
The Anterior Attention Network
which is within half of a standard deviation of the
mean based on the national standardized population of
1,009 children reported by Gresham and Elliot (10.9
and 13.8, respectively; Gresham & Elliot, 1990).
The CBQ is a measure designed to assess temperament for children between the ages of 3 and 8
(Ahadi et al., 1993). The parent of 1 boy did not
complete the CBQ. The CBQ is a 195-item questionnaire that yields three higher order dimensions,
two of which were examined in this report. These
dimensions, the scales comprising them, and their
reliabilities are as follows. Effortful Control was computed as the summed and averaged standardized
scales of Inhibitory Control (a ˆ .88), Attention Focusing (a ˆ .67), Smiling (a ˆ .84), Low Intensity Pleasure (a ˆ .75), and Perceptual Sensitivity (a ˆ .82).
Surgency/Extroversion was computed as the summed and averaged standardized scales of High Pleasure (a ˆ .80), Impulsivity (a ˆ .82), Activity Level
(a ˆ .79), and Shyness (reversed scored; a ˆ .93).
Laboratory Tasks
Neuropsychological Tasks of Inhibitory Control.
These tasks were drawn from a battery developed by
Casey and colleagues. Children completed two tasks
measuring different aspects of inhibitory control. The
®rst was a Go, No-Go task measuring ability to inhibit
a prepotent motor response by selectively attending
and responding to the target stimuli while ignoring
or inhibiting responses to equally salient nontarget
stimuli (Casey, Trainor, Orendi et al., 1997). The
second was an attentional control task that required
subjects to process multiple stimulus attributes and
to inhibit attention to irrelevant attributes (Casey,
Trainor, Giedd et al., 1997). Both tasks were presented
on a Macintosh Quadra 660 AV computer.2
In the Go, No-Go task, the participants responded
to every letter (target stimuli) except ``X'' (nontarget
stimuli). This task contained two conditions: (a) a
control or ``Go'' condition of 42 trials which contained 100% targets (i.e., not Xs) and (b) a response
inhibition or ``No-Go'' condition of 42 trials containing 50% targets (i.e., not Xs) and 50% nontargets
(i.e., Xs). In both conditions, stimuli were presented
for 500 ms with an interstimulus interval of 1,500 ms.
Participants were asked to respond as quickly as
possible without making mistakes. Responses were
2
A third task, which required participants to press one of
four buttons with the four ®ngers on their right hand in
response to viewing the numbers 1, 2, 3, or 4, was not
included in analyses a priori because children lacked the
motor coordination to perform this task.
47
made by pressing the keyboard space bar. The percent correct, number of false alarms (responding to a
nontarget), number of omissions (failing to respond
to the target stimuli), and average reaction time
was determined for the response inhibition and
control conditions on this task. The square root of
the reaction time was taken because the distribution
was asymmetrical.
The Attentional Control task involved inhibiting
or directing attention to different sensory stimuli.
Participants were given a forced-choice, visual discrimination task. In this paradigm, three stimuli were
presented in a row on a computer screen. The stimuli
varied in shape (circles or squares) and in color (black
or white). The participants were asked to determine
which of the three stimuli was different from the other
two. Participants were not told which features would
be different. Stimuli remained on the computer screen
until the participant responded by pressing one of
three marked keys to indicate which of the three
stimuli were different. Participants were asked to
make a response as quickly as possible. Targets appeared equally often in each of the three locations in a
random order.
This task contained two conditions: (a) a control
condition involving automatic processing and (b) a
response inhibition condition involving controlled
attentional processes. There were four blocks in this
task (two in each condition). The ®rst and third blocks
involved a predominantly automatic response. In
these blocks, the attribute that the participant used to
determine uniqueness was the same for a block of
trials (always color or always shape). Such stimulus
detection tasks involving only variation of one feature
seem to be relatively automatic (Treisman, 1986 as
cited in Casey, Trainor, Orendi et al., 1997). In Blocks
2 and 4, the stimulus attribute that determined uniqueness changed from trial to trial. Tasks that require
shifts in attentional set from trial to trial are thought
to involve attentional resources or control processes
(Shiffrin & Schneider, 1977 as cited in Casey, Trainor,
Orendi et al., 1997). The subjects were presented with
49 trials per block. Percent correct and average
reaction time was determined for each of the four
blocks. The square root of the reaction time was taken
because the distribution was asymmetrical. Two children were unable to complete this task; their scores
were dropped from this task, but included in all other
measures. One child had an attentional control reaction time that was over three standard deviations
above the mean. This child was assigned the next
highest value to prevent her score from skewing future
analyses. Performance on the two control and two
response inhibition conditions were combined,
48
Davis, Bruce, and Gunnar
creating a reaction time and an accuracy score for
each condition.
Delay of Grati®cation Tasks. These tasks were
drawn from the battery of tasks developed by
Kochanska and colleagues (Kochanska et al., 1997).
Children's performance on these tasks was coded
from videotape by two coders. Twenty percent of the
videotapes were reviewed by both coders to calculate
interrater reliability. Reliability kappa was greater
than .85 for each task. In the ®rst task, dinky toys,
children were allowed to choose a prize from a plastic
box. They were instructed to keep their hands in their
lap and to make their choice without touching or
pointing. The coding ranged from 0 to 3 (0 ˆ grabbed
the prize, 1 ˆ touched the prize, 2 ˆ pointed to the
prize, and 3 ˆ did not remove hands from lap). The
reliability kappa was .88. The time until children
touched or pointed also was measured. Coders were
found to be within 50 ms of each other 100% of
the time. Children who did not touch or point
were assigned a score equal to the longest time. The
square root of the reaction time was taken because
the distribution was asymmetrical. These two scores
were standardized and averaged to create a score for
the dinky toys task.
In the gift task, the children were told that they
would get a prize, but that the experimenter had to
wrap it ®rst. The children sat in a chair with their
backs to the experimenter and were instructed not to
peek. The experimenter noisily wrapped the prize for
1 min and then left the room for 2 min ``to go get a
ribbon.'' The children were reminded not to peek
while the experimenter was gone. The children's
behavior was coded during the time while the
experimenter was wrapping the prize and the time
while the children were in the room alone (0 ˆ turned
to look at the prize, 1 ˆ peeked over their shoulder,
2 ˆ subtle movement in an attempt to peek, and
3 ˆ never moved). The kappa for reliability was .92.
These two gift scores were standardized and averaged
to create a score for the gift task.
Cortisol Sampling. In the laboratory, four samples
of saliva were obtained for cortisol determination. The
®rst sample was taken upon arrival at the laboratory,
at 4 p.m. Subsequent samples were taken at 20 min
intervals, as is typical in research on this neuroendocrine system (Kirschbaum, Pirke, & Hellhammer,
1993). To collect saliva, the child was given Trident
Original gum to stimulate salivation. The child then
spit through a straw into a small plastic vial. In
addition, parents were asked to collect saliva samples
at home on 2 normal school days in the morning when
the child woke up, between 4 and 5 p.m. (to correspond with the lab samples), and between 8 and 9 p.m.
School days were chosen for two reasons. First,
children's daily routines (i.e., sleep, wake, and mealtimes) have been found to be much more regular on
school as compared to weekend days (Davis et al.,
1999). Second, children always came into the lab on
school days and thus, the 4 p.m. sample time at home
and in the lab were more comparable. Families stored
collected saliva samples in their refrigerator until
sampling was completed. Parents then mailed the
sample to the laboratory, where they were stored in
a freezer at ÿ20 C until assayed. Mailing has not
been found to affect cortisol concentrations (Clements
& Parker, 1998). Fifty-three participants completed
the home saliva-collection portion of the study.
Samples were assayed in 50 ml aliquots using a modi®cation of the Ciba Corning Magic cortisol assay kit
(Kirschbaum, Strasburger, Jammers, & Hellhammer,
1989). The use of Trident Original gum to stimulate
salivation has been shown to have little effect on
cortisol levels using this assay (Schwartz, Granger,
Sussman, & Gunnar, 1998). All samples from each
participant were included in the same batch to eliminate within subject interassay variance. Samples were
assayed in duplicate and averaged. Duplicate varying
by more than 20% were reassayed. The interassay and
intraassay coef®cients of variation were 9.43 and 6.30,
respectively.
Cortisol levels follow a circadian rhythm and are
affected by food intake and sleep patterns. For each
sampling day, parents completed a diary noting the
time of each sample, when the child woke up, went to
bed, time of meals, use of medication, and general
health. These data were examined to determine that
sampling times were listed as occurring before
breakfast in the morning and that the child did not
have a fever on sampling days and was not taking
medication. One child's cortisol data was excluded
from analyses due to the daily use of an asthma
inhaler. The cortisol values were log transformed to
normalize the distribution of the data. Home cortisol
levels were averaged within time of day to yield
a more stable estimate of baseline cortisol levels
(see Table 1 for descriptive information on time of
sampling).
RESULTS
Data Management and Analyses
Preliminary analyses were performed using analysis of variance to investigate sex differences and
The Anterior Attention Network
Table 1. Descriptive Statistics for Time of Saliva
Sampling
Cortisol Samples
Home Samples (n ˆ 52)
Morning
Afternoon
Evening
Laboratory Samples (n ˆ 57)
Sample 1
Sample 2
Sample 3
Sample 4
M
SD
7:45
16:28
20:32
43 min
41 min
44 min
16:06
16:22
16:43
17:02
14
15
16
16
min
min
min
min
differences in condition or time of measurement
where applicable. First, the two neuropsychological
tasks were examined for sex differences and differences in speed and accuracy on the control and response inhibition conditions. Parent report measures
(CBQ and SSRS) and the two delay of grati®cation
measures were then examined to determine if sex
differences existed. Next, cortisol measures were
examined to determine whether cortisol levels were
affected by time (morning, afternoon, and evening),
day (home afternoon vs. lab afternoon) of measurement, or sex. Intercorrelations within task groups were
examined, and data were reduced to yield one score
for each of the following: speed and accuracy on the
neuropsychological tasks, delay of grati®cation, home
cortisol levels, lab cortisol levels, and lab cortisol
slope.
The next set of analyses used Pearson product
correlations to examine the relations among these
summary variables. We began by examining whether
either parent report measure of Inhibitory Control,
Attention Focusing, and Impulsivity or behavioral
measures of effortful control (delay of grati®cation)
were associated with accuracy or reaction time on
the neuropsychological tasks assessing the anterior
attentional system. Next, we examined whether the
superordinate dimensions of Effortful Control and
Table 2.
Surgency/Extroversion were related to performance
on the neuropsychological tasks. Additionally, we
sought to determine whether we could replicate relations previously reported by Kochanska and colleagues (1996) between delay of grati®cation and parent
report of Inhibitory Control and Impulsivity on the
CBQ. Then, we examined whether cortisol levels at
home or in the laboratory were related to the
neuropsychological measures of the anterior attentional system and temperament. Finally, we examined
whether any of the measures of frontal functioning,
temperament, or behavior regulation were related to
parent reports of children's behavior problems.
Preliminary Analyses and Data Reduction
Neuropsychological Inhibitory Control Tasks. For
each task, comparisons were made between children's
performance on control and response inhibition
conditions for both speed and accuracy. The descriptive data for these two tasks is shown in Table 2.
To assess accuracy on the Go, No-Go task, a 2 2
(Sex Condition) ANOVA with repeated measures on
the last factor was computed. There was no sex
difference in accuracy, F(1, 56) ˆ 1.56, n.s. There
was, however, a main effect of condition for accuracy,
F(1, 56) ˆ 158.25, p ˆ .001. Participants were more
accurate in the control condition than in the response
inhibition condition. There are two ways that children
could make mistakes on this task leading to a decrease
in accuracy: by failing to respond to a target (response omission) or by responding to a nontarget (false
alarms). In fact, children's errors consisted primarily
of false alarms (M ˆ 6.03, SD ˆ 3.02) rather than
response omissions (M ˆ 1.93, SD ˆ 2.25). For this
reason, and because we were mainly interested in
failures of response inhibition, the remaining analyses
used false alarms as the accuracy measure. For reaction time, a 2 2 (Sex Condition) ANOVA with
repeated measures on the last factor was computed.
Descriptive Data for the Neuropsychological Tasks of Inhibitory Control
Control Condition
Tasks
Go, No-Go (n ˆ 58)
Reaction Time
Accuracy
Attentional Control (n ˆ 56)
Reaction Time
Accuracy
49
Response Inhibition Condition
M
SD
M
SD
416.10
96.28
90.91
4.48
505.10
81.05
88.44
9.17
1562.44
96.65
302.12
3.42
1579.94
96.56
320.67
4.15
50
Davis, Bruce, and Gunnar
There was no sex difference in reaction time,
F(1, 56) ˆ .24, n.s. There was a main effect of condition for reaction time, F(1, 56) ˆ 79.74, p ˆ .0001.
The children had faster reaction times in the control
condition than the response inhibition condition.
To determine if there was a difference in accuracy
between the control and the response inhibition condition on the Attentional Control task, a 2 2 (Sex Condition) ANOVA with repeated measures on the
last factor was computed. Neither the main effect of
sex, F(1, 54) ˆ .86, n.s., nor condition, F(1, 54) ˆ .08,
n.s., was signi®cant. Differences in reaction time also
were examined in a 2 2 (Sex Condition) ANOVA
with repeated measures on the last factor. There
were no main effect of sex, F(1, 54) ˆ 1.38, or
condition, F(1, 54) ˆ 1.02, n.s. While group means
were not different between control and response
inhibition conditions, variability in task performance
allowed for exploration of associations with other
measures.
Table 3. Descriptive Statistics for Parent Report
Measures
Data Reduction for Neuropsychological Tasks. The
four variables of interest were reaction time and
accuracy in the response inhibition condition for the
Go, No-Go and attentional control tasks. Previous
research found that fast reaction times and high
accuracy were related to the ACC (Casey, Trainor,
Giedd et al., 1997; Casey, Trainor, Orendi et al.,
1997). To reduce the number of variables used in
subsequent analyses, we created two summary scores:
``speed'' and ``accuracy.'' Speed was created by
standardizing and summing the reaction time measures, such that a high score re¯ected fast reaction
times. The speed measures on the two tasks were
correlated, r(56) ˆ .38, p ˆ .004, and the resulting
averaged score (M ˆ .03, SD ˆ .84) was normally
distributed. Accuracy was created by standardizing
and summing the accuracy measures, such that a high
score re¯ected a large number of correct responses.
The correlation among the two accuracy measures
was r(56) ˆ .24, p ˆ .07. The resulting averaged score
(M ˆ .03, SD ˆ .78) also was normally distributed.
The expected speed±accuracy trade-off was seen in
performance, r(58) ˆ ÿ.44, p ˆ .001.
variance was computed to examine sex differences on
the Problem Behavior scale of the SSRS. There was a
nonsigni®cant trend for boys to exhibit higher levels
of problem behaviors, F(1, 56) ˆ 3.35, p ˆ .073. As
mentioned previously, the Problem Behavior scale
is comprised of three subscales, two of which assess
externalizing behaviors, Externalizing Problems and
Hyperactivity, and one of which assesses internalizing
behaviors, Internalizing Problems. As the two externalizing subscales were highly correlated, r(58) ˆ .67,
p ˆ .0001, we averaged these two scales to create one
measure of externalizing behavior problems.
Delay of Grati®cation Tasks. Sex differences were
examined for these behavioral measures using a
multivariate analysis of variance. There was no signi®cant effect of sex, F(2, 55) ˆ 1.34, n.s. The two delay
of grati®cation scores (gift and dinky toys) were
correlated, r(58) ˆ .24, p ˆ .065. To reduce the number of measures used, the scores for these tasks were
standardized and averaged to create an overall delay
of grati®cation score with a mean of zero and the
standard deviation of .67.
Parent Report. The descriptive data on the higher
order factors of the CBQ and SSRS are shown in
Table 3. A 2 2 (Sex Temperament) multivariate
analysis of variance was computed to examine sex
differences for CBQ temperament factors. There was
no signi®cant effect of sex, Hotellings F(2, 54) ˆ 1.80,
n.s. As expected based on previous data, Inhibitory
Control and Impulsivity were highly correlated in
our sample, r(57) ˆ ÿ.62, p ˆ .0001. An analysis of
Cortisol Levels. Descriptive data on the laboratory
and home cortisol levels are shown in Table 4. For
the home baseline measures, a 2 3 (Sex Time
of Cortisol Measurement) ANOVA was computed
with repeated measures on the last factor using
Greenhouse±Geisser adjustment as required. The
main effect of sex, F(1, 50) ˆ 1.0 n.s., was not signi®cant. However, consistent with the daily rhythm
in cortisol, the effect of time-of-day was highly
Temperament Scales (n ˆ 57)
M
SD
Effortful Control
Attention Focusing
Inhibitory Control
Low Pleasure
Perceptual Sensitivity
Smiling/Laughter
Surgency/Extroversion
Activity Level
High Pleasure
Impulsivity
Shyness
Problem Behaviors
Externalizing/Hyperactivity
Internalizing
.01
5.01
5.11
5.73
5.17
5.89
0
4.74
4.90
4.29
3.54
11.95
4.26
3.42
.74
.74
.87
.55
.75
.60
.74
.76
.82
.80
1.15
5.49
2.28
1.59
Note : Higher order temperament dimensions were computed as
the mean of the standardized subscales.
The Anterior Attention Network
Table 4. Descriptive Statistics for Cortisol Measures
in mg/dl
Cortisol Samples
Home Samples (n ˆ 52)
Morning
Afternoon
Evening
Laboratory Samples (n ˆ 57)
Sample 1
Sample 2
Sample 3
Sample 4
M
SD
.71
.25
.12
.30
.12
.10
.26
.26
.22
.18
.14
.11
.09
.07
signi®cant, F(1.6, 78.7) ˆ 234.0, p ˆ .0001. Morning
cortisol levels were signi®cantly correlated with
afternoon and evening levels r(52) ˆ .39, p ˆ .004
and r(52) ˆ .28, p ˆ .04. Afternoon and evening
levels were not signi®cantly associated, r(52) ˆ .08,
n.s. To reduce the number of analyses performed, the
baseline morning, afternoon, and evening cortisol
values were standardized and averaged, creating one
home baseline cortisol measure with a mean of zero
and a standard deviation of .71. This home cortisol
measure was normally distributed.
We predicted that children would display a slight
increase in cortisol in response to the mildly stressful
cognitive tasks they were asked to perform in the lab.
Thus, we expected that cortisol levels would elevate
across the time that children were in the lab and that
their cortisol levels in the lab would be higher than
their cortisol levels at home at the same time of day. A
2 4 (Sex Time of Cortisol Measurement) repeated
measures ANOVA using Greenhouse±Geisser adjustments as required on the laboratory cortisol measures
indicated, in contrast to our predictions, a signi®cant
decrease in cortisol levels over the testing period in
the laboratory, F(2.4, 132.2) ˆ 45.47, p ˆ .0001.
There was no signi®cant effect of sex, F(1, 58) ˆ 0,
n.s. To test the prediction that children who displayed
greater elevations in cortisol across the time that they
were in the laboratory would show poorer performance on tasks assessing prefrontal function, we
computed a slope measure of these four laboratory
cortisol values for each child. Cortisol values were
regressed on the sampling times, and the resulting
slope value was retained. For the cortisol slope measure, higher values re¯ect sharper increases in cortisol
levels across the time in the laboratory. The correlations among the laboratory measures ranged from .68
to .87. To reduce the number of variables examined,
one measure of laboratory cortisol was obtained that
re¯ected the standardized and averaged laboratory
51
measures. The resulting score had a mean of zero
and a standard deviation of .92 and was normally
distributed. The summary lab cortisol and home baseline cortisol measures were correlated, r(52) ˆ .46,
p ˆ .001. The laboratory cortisol values and the
afternoon home cortisol values (taken at the same
time of day) were not signi®cantly different,
t(51) ˆ .81, n.s., suggesting that on average children
did not show a cortisol response to coming into
the lab.
Neuropsychological Inhibitory Control
Tasks: Associations With Delay of
Grati®cation and Parent-Reported
Temperament
Since accuracy on the neuropsychological tasks has
been shown to involve prefrontal systems including
the ACC, we expected that accuracy would be related
to three key subscales of the CBQ: Inhibitory Control, Attention Focusing, and Impulsivity. We also
expected associations with the laboratory measure of
delay of grati®cation. We found the expected associaions with the Inhibitory Control and Impulsivity
scales. Surprisingly, neither Attention Focusing nor
performance on the delay grati®cation tasks were
signi®cantly related to accuracy on the neuropsychological tasks. Furthermore, when the higher order
dimensions of Effortful Control and Surgency/Extroversion were examined, while there was the trend for
Effortful Control to be related to accuracy, only
Surgency/Extroversion was signi®cantly related to
the accuracy measure (Table 5). Because of the speed
accuracy trade-off in performance on this task, it was
possible that surgent, impulsive children were less
accurate because they were more motivated to ``go
fast.'' Speed was positively correlated with Surgency/
Extroversion and its subscales (range .21±.42). However, even after removing the variance due to speed,
Surgency/Extroversion remained signi®cantly related
to this residualized accuracy score, r(57) ˆ ÿ.42,
p ˆ .001. Thus, surgent children had lower accuracy
scores on this task even after accounting for their
faster speed.
Delay of Grati®cation: Associations With
Parent Reports of Child Temperament
The associations between Inhibitory Control, Attention Focusing, and Impulsivity from the CBQ and
performance on the delay of grati®cation tasks were
examined. Only Inhibitory Control was signi®cantly related to the delay of grati®cation measure,
52
Davis, Bruce, and Gunnar
Table 5. Correlations Between Neuropsychological Tasks and Temperament, Delay of
Grati®cation Tasks, Cortisol, and Behavior Problems
Neuropsychological Tasks
Effortful Control
Attention Focusing
Inhibitory Control
Surgency/Extroversion
Impulsivity
Delay of Grati®cation Tasks
Mean of Home Cortisol
Slope of Laboratory Cortisol
Mean of Laboratory Cortisol
Externalizing Problems
df
Accuracy
Reaction Time
57
57
57
57
57
58
52
57
57
58
.25y
.12
.30*
ÿ.53**
ÿ.36**
0
.38*
ÿ.03
.32*
ÿ.33*
ÿ.18
ÿ.05
ÿ.26*
.42**
.36**
.25y
ÿ.14
.01
ÿ.16
.22
y p < :01., *p < :05., **p < :01.
r(57) ˆ .28, p ˆ .035. Furthermore, the higher order
dimensions of Effortful Control, r(57) ˆ .29, p ˆ .027,
but not Surgency/Extroversion, r(57) < .1, n.s., was
correlated with the delay of grati®cation score. These
data replicate previous ®ndings of modest correlation
between Inhibitory Control, as assessed using the
CBQ, and performance on laboratory tasks of inhibitory control (Kochanska et al., 1996).
Associations With Cortisol
We predicted that children who scored lower on
neuropsychological measures of the anterior attentional system would show an increase in cortisol
production across the time that they were in the lab
and would have higher baseline and lab cortisol levels.
Cortisol slope across the time that children were in
the laboratory was not associated with performance
on the frontal tasks (ps > .1). However, mean cortisol
levels at home and at the lab were related to
neuropsychological task performance. Surprisingly,
children who were more accurate on the prefrontal
tasks had higher average home baseline cortisol,
r(52) ˆ .38, p ˆ .006, and higher average cortisol in
the lab while they were performing these tasks,
r(57) ˆ .32, p ˆ .014. Associations between cortisol
and performance on the neuropsychological tasks
were strongest for morning levels, r(52) ˆ .36, p ˆ .01.
However, the association was in the same direction for
afternoon and evening measures, r(52) ˆ .22, p ˆ .13,
and r(52) ˆ .23, p ˆ .10 respectively. Neither the
delay of grati®cation tasks nor Effortful Control was
related to home or laboratory cortisol (rs ranged
from ÿ.03 to ÿ.18). There was a trend for Surgency/
Extroversion to be negatively related to laboratory,
but not home cortisol, r(56) ˆ ÿ.22, p ˆ .10, and
r(52) ˆ ÿ.09, n.s., respectively.
Behavior Problems, Temperament, and
Frontal Functioning
We predicted that children who were reported by their
parents to have more externalizing behavior problems
would display less accurate performance on the neuropsychological tasks and poorer ability to delay grati®cation. In addition, we expected that these children
would be rated by their parents as being higher in
Surgency/Extroversion and lower in Effortful Control.
The results support our predictions. Accuracy on the
neuropsychological tasks, r(58) ˆ ÿ.33, p ˆ .012, performance on the delay grati®cation tasks, r(58) ˆ .24,
p ˆ .067, and parent report of temperament, Surgency/
Extroversion: r(57) ˆ .48, p ˆ .0001; Effortful Control: r(57) ˆ ÿ.46, p ˆ .0001, were related to parent
report of externalizing problem behaviors. To determine whether these associations were speci®c to externalizing problems, similar correlations were computed
using the Internalizing scale from the SSRS. The
results showed that only Effortful Control was signi®cantly related to internalizing behavior problems,
r(57) ˆ ÿ.37, p ˆ .004.
DISCUSSION
Based on what is known about the neural structures
proposed to comprise the anterior attentional system,
we expected that performance on the neuropsychological tasks would be correlated with the CBQ
The Anterior Attention Network
subscales of Inhibitory Control, Attention Focusing,
and Impulsivity. In accordance with our predictions,
performance on the neuropsychological tasks were
positively correlated with parent reports of Inhibitory
Control and negatively correlated with their reports
of children's Impulsivity. Based on the model proposed by Posner and Rothbart, in addition, we
expected that the neuropsychological measures which
we predicted, based on previous imaging studies, to be
subserved by structures Posner (1995) describes as
comprising the anterior attentional system would
correlate with the higher order CBQ dimension of
Effortful Control. This is the dimension on which the
scales of Inhibitory and Attention Focusing load. The
results only partially supported this prediction. While
there was a trend for Effortful Control to be related
to accuracy, it was the higher order dimension of
Surgency/Extroversion that was more clearly related
to performance on the neuropsychological tasks.
Impulsivity loaded on this dimension, thus we might
expect that the association was due to more highly
surgent children responding faster and making more
errors. However, the number of false alarms was
associated with scores on the Surgency/Extroversion
dimension even after removing the variance due to
speed of responding. It is important to note that the
correlations between Surgency and performance on
these tasks were modest and other factors, such as
motivation, clearly come into play.
Surgency/Extroversion is characterized by approach to novelty, exuberance, sensation seeking,
and impulsivity. While these can be viewed as
positive characteristics, this temperament dimension
also has been associated with behavior problems,
such as disruptive classroom behavior and risk
taking. Research suggests that impulsivity, a major
component of this temperament dimension, is related
to development of neural systems in the prefrontal
cortex that comprise the construct of the anterior
attentional system (Carter, Krener, Chaderjian,
Northcutt, & Wolfe, 1995). Thus, it is not surprising
that performance on these neuropsychological tasks
would be related to Surgency/Extroversion. Furthermore, children who were rated as more surgent by
their parents also were rated as exhibiting more
externalizing behavior problems. Thus, in a normative sample, in addition to exhibiting a larger number
of externalizing problems, more surgent children
exhibited mild de®cits on tasks dependent on frontal
circuitry, and their problems were not merely due to
their propensity to perform these tasks quickly. It is
not known whether Surgency/Extroversion is a function of poor/slower frontal lobe development or if
children with this temperament spend less time in
53
activities that might support development of attention/inhibitory control abilities.
As in previous studies, we found that the CBQ
scale of Inhibitory Control was positively correlated
with behavioral tasks assessing delay of grati®cation.
Interestingly, however, scores on the delay of grati®cation tasks failed to correlate with the performance
on the neuropsychological tasks. These results are in
contrast to previously reported ®ndings of associations between performance on delay of grati®cation
tasks and a spatial con¯ict task thought to involve
frontal regions, including the ACC (Gerardi-Caulton,
2000). However, in that study, which tested three age
groups of children between 24 and 36 months of age,
only one age group displayed this association. The
cause of this inconsistency in associations between
delay of grati®cation tasks and neuropsychological
assessments of the structures involved in the anterior
attentional system is unclear. The multifaceted nature
of inhibitory control and the potential in¯uence of
motivational factors may be involved (Rothbart et al.,
2000). Furthermore, these data illustrate a dif®culty
with developmental research. Delay of grati®cation
tasks used with toddlers are too easy for older children
and would not challenge their inhibitory control
abilities suf®ciently. Thus, different tasks must be
used with different ages. At the same time, by changing the tasks one runs the risk of assessing different
facets of child functioning.
More striking in our results was the ®nding that
greater accuracy on the neuropsychological tasks
assessing structures presumably involved in the anterior attentional system was associated with higher, not
lower, cortisol concentrations both at home and in the
lab. However, this result may not be as surprising as
it initially seemed. As mentioned previously, there
is a well-documented, inverted U-shaped relationship between cortisol and many cognitive functions
(Lupien & McEwen, 1997). There are many possible
reasons for this, including the effects of increased
cortisol levels on metabolism, cardiac functioning,
and catecholamines (de Kloet, Oitzl, & Joels, 1999).
Indeed, decrements in cognitive functions are typically only seen at very high levels of cortisol production. While higher cortisol at home and in the lab
was associated with greater accuracy on the neuropsychological tasks, cortisol levels were clearly well
within normal range for baseline cortisol levels in this
population. Thus, it is likely that even children
displaying the highest levels of cortisol in this sample
were not at levels that have been shown to impair
cognitive processes. Furthermore, children did not
display elevated cortisol in response to coming into
the lab. Thus, we do not have a measure of children's
54
Davis, Bruce, and Gunnar
cortisol response to stress. Perhaps, had we presented
children with a stressor capable of activating the HPA
system, we would have seen the predicted association
of lower cortisol levels in children who performed
better on these attentional tasks.
Given that the observed cortisol levels were within
the normal range for baseline levels, associations
between higher cortisol and better performance may
be in accord with theory suggesting optimal performance with moderate levels of cortisol. Indeed, one
recent study showed that a decrease in cortisol in
response to a stressor was related to poor performance
on tasks assessing structures presumably involved in
the anterior attentional network (Vedhara, Hyde,
Gilchrist, Tytherleigh, & Plummer, 2000). Further
research is clearly necessary to improve our understanding of the relationship between baseline levels of
cortisol and cognitive functioning as well as the
mechanism underlying this association.
These ®ndings lend support to the notion that
prefrontal functioning is related to the functioning of
the HPA system. Of course, neither the direction of
effect nor even the causal basis of these correlations
can be determined with the present data. In particular,
it is important to note the possibility that it is the
temperament of the child that is responsible for
the associations seen between cortisol and performance on the cognitive tasks. Six-year-olds who are
high in Surgency are unlikely to be anxious over the
accuracy of their performance in a lab situation, and it
might be for this reason that they had fast latencies,
made more errors, and had lower cortisol. While
we cannot identify the cause, it is noteworthy that a
signi®cant association was found between cortisol
levels and performance on these neuropsychological
tasks.
Finally, because de®cits in frontal lobe function
often have been of concern in studies of children with
clinically signi®cant behavior problems (Bush et al.,
1999; Carter et al., 1995), we also examined parent
reports of behavior problems in this normative
sample. As expected, the children scored in the nonclinical range for both internalizing and externalizing
problems. However, even in this nonclinical range, the
predicted association between measures of the frontal
attentional network and externalizing problems was
obtained. This lends support to the importance of
understanding the neural basis of normative variations
in temperament in research on both behavior regulation and behavior problems. Overall, these data are
consistent with Posner and Rothbart's theory that
the anterior attention network underlies aspects of
children's temperament and social behavior. However,
these results also underscore the noted complexity and
multifaceted nature of self-regulatory competence
(Kochanska, 1993).
NOTES
This research was supported by National Institute of
Mental Health Grant MH56958 to Megan R. Gunnar.
Portions of this data were presented at the 1999
biennial meeting of the Society for Research in Child
Development. The authors wish to express their gratitude to the families who helped with this research.
Thanks also are expressed to Sarah Warner and
Lindsey McDougall for their assistance with data
collection and to Mary Fowler and Linda Bailey of the
Endocrine Laboratory at that University of Minnesota
for their careful analysis of the salivary cortisol data.
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