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2011 - Response Preparation and Cognitive Control of Highly Intelligent Children
2011 - Response Preparation and Cognitive Control of Highly Intelligent Children
122
T. Liu et al. / Neuroscience 180 (2011) 122–128 123
itations: Firstly, they adopted a simple Go-Nogo paradigm Table 1. Children’s IQ scores and SES characteristics
which contained less conflict situation, and both groups of
children could complete the task well without devoting Gifted Average t-test/
much neural effort to detect the conflict situation. Sec- group group Chi-square
(n⫽20) (n⫽21) test
ondly, their study did not investigate how children’s re-
sponse preparation affected their cognitive control pro- IQ
cesses, so it was also uncertain whether gifted children’s IQ scores 43.2⫾1.7 34.5⫾1.9 P⬍0.001
better inhibition performances were partially attributed to Score range 41–46 30–40
their efficient response preparation processes. Standardized IQ range 120–135 100–115
In order to solve these limitations, current study was SES
aimed at exploring the relationship between response Maternal education
ⱕHigh school 5 4 P⬎0.05
preparation and the subsequent cognitive control pro-
Bachelor’s degree 11 12
cesses in two groups of children with different intellectual Master’s/doctorate 4 5
levels with a revised CPT-ABX experimental task which degree
was more complex and would induce more conflict situa- Parental wealth
tion based on previous studies (Bekker et al., 2004). Two Poor 0 0 P⬎0.05
hypotheses were further proposed: firstly, gifted group Lower than medium 4 5
would have better cognitive control performances due to Medium 14 12
their faster and stronger neural responses of N2 and P3 in Rich 2 4
both conflict monitoring and attentional control processes. IQ difference analysis used t-test, and SES analysis used Chi-
Secondly, gifted children would evoke more efficient square test. Numbers in the SES characteristics were the numbers
cue-P2 and cue-P3 responses for the cue-related re- of participants.
sponse preparation processes than their average peers.
Stimuli and procedure
EXPERIMENTAL PROCEDURES The stimuli were six capital-written Western characters: letter A,
letter B, letter F, letter J, letter T and letter X in black Time New
Participants Roman Regular Font, and they were presented in the center of
light gray screen with the visual angle of 2.9° vertically and 2.7°
Two groups of early adolescents participated in the current study: horizontally.
a group of intellectually gifted children [n⫽20, 11 boys and nine Participants completed 18 trials for practice (3 A, 3 B, 6 X, 2
girls; ages 12.7–13.2 years old (mean age: 12.8 years old); all F, 2 T, 2 J), and the formal experiment consisted of 520 stimulus
right handed] were randomly recruited from the experimental presentations (100 A, 100 B, 200 X, 40 F, 40 T, 40 J) with half the
school that is specifically founded to offer accelerated education number of letter A and half the number of letter B directly followed
for gifted children nationwide, and the curriculum of the gifted by the letter X, which indicated that 50% of the letter X trials (100
education system was mainly focused on the scientific domains trials) need Go processing and the other 50% of the X trials (100
(such as, mathematics, physics, chemistry and biology). The ex- trials) required Nogo processing. All the stimuli were displayed
perimental school enrolls about 30 intellectually gifted children randomly. Participants were instructed to press the left button
from about 2000 candidates nationwide based on multiple criteria when the letter X directly followed the letter A and press the right
and methods each year. Several of the main steps for the enroll- button when the letter X directly followed the letter B as correctly
ment examination and identification are an application, a primary and as quickly as possible, and they were also asked not to
screening test (classical intelligence tests, such as the Wechsler respond to the non-X letters that followed behind the cues. Par-
Preschool and Primary Scale of Intelligence), a retest (focusing on ticipants were informed that some of the letter A and letter B
cognitive abilities [attention, memory, reasoning abilities], creativ- accompanied with the target letter X following behind while some
ity, learning ability, special talents, personality traits [motivation]), did not, and this instruction might induce children’s response
further confirmation (children’s physical conditions) and behav- preparation tendency.
ioral observation through equal educational environment (children Participants were seated on a comfortable chair with a
who had excellent performances in the above steps within the top straight visual angle to the center of computer monitor. Each
fifth quantile passed this step). stimulus was presented for 600 ms followed by a blank screen for
A group of intellectually average children [n⫽21, 11 boys and 400 – 600 ms. The usages of left and right hands were balanced
10 girls; age 12.6 –13.4 years old (mean age: 12.9 years old); all within participants. There were four blocks in the formal experi-
right handed] was chosen with the similar gender ratio, ages and ment with 130 stimulus presentations per block, and participants
parental socioeconomic status (SES) as the gifted group. Cattell’s were allowed to have a 2–3 min break after each block.
Culture Fair Test (Child Edition, 46 items, one point/item, scale
range 0 – 46) was used to test children’s general fluid intelligence ERP recording and data analysis
scores, and the gifted group achieved significantly higher intelli-
gence scores than the average group (t⫽7.52, P⬍0.001). SES Electroencephalogram (EEG) was recorded (bandpass filtering
questionnaire included the variables of maternal education and 0.05–100 Hz, sampling rate 1000 Hz, Synamp2 amplifiers) by
parental wealth, and the parental wealth variable was based on using NeuroScan recording system with Ag/AgCl electrodes
parents’ average income per month from the child’s birth. Statis- placed on F3-Fz-F4, FC3-FCz-FC4, C3-Cz-C4, CP3-CPz-CP4,
tical analysis showed that there was no significant difference P3-Pz-P4 and PO3-POz-PO4 according to the 10 –20 interna-
between the two groups in the SES, and the results of psycho- tional system. The reference electrode was attached to the nose
metric testing of IQ and SES are presented in Table 1. All of the reference, and the ground electrode was attached to the forehead.
children had normal or corrected-to-normal visual acuity, and Horizontal electrooculogram (HEOG) was recorded with a pair of
none of them had neurological or psychiatric problems. Informed electrodes placed 10 mm from the outer canthi of two eyes, and
consents were obtained from both their parents and teachers. vertical electrooculogram (VEOG) was recorded with a pair of
124 T. Liu et al. / Neuroscience 180 (2011) 122–128
Fig. 1. Children’s ERP activation of cue-P2 and cue-P3 during response preparation processes in the cue condition and the non-condition.
T. Liu et al. / Neuroscience 180 (2011) 122–128 125
Table 3. Children’s mean and standard deviation of peak amplitudes (V) and latencies (ms) of cue-P2 and cue-P3 during response preparation
processes in the cue condition and the non-cue condition
Groups Preparation condition Cue-P2 latency Cue-P2 amplitude Cue-P3 latency Cue-P3 amplitude
Gifted group Cue condition 195 (39.6) 2.9 (0.5) 354.5 (12.4) 9 (1.5)
Non-cue condition 203 (38.8) 2.6 (0.9) 361 (15.7) 6.5 (2)
Average group Cue condition 204 (40) 4 (1.7) 356 (18) 7.7 (1.1)
Non-cue condition 204 (39.8) 3.8 (1.3) 371 (12.6) 6.2 (1.8)
subjected to repeated measures ANOVAs with Intelligence wed that the gifted children had significantly faster N2
(two levels, gifted group and average group) as between- responses than the average children (F(1,39)⫽5.8, P⬍
subject factor, Cue condition (two levels, cue condition and 0.05), and the Nogo condition induced larger N2 amplitude
non-cue condition) and Electrode sites (three levels, frontal than the Go condition (F(1,39)⫽10.5, P⬍0.01). Go/Nogo
area [F3-Fz-F4], fronto-central area [FC3-FCz-FC4], cen- condition and Electrode sites had significant interaction
tral area [C3-Cz-C4]) as within-subject factors. The gifted effect on N2 amplitude (F(2,39)⫽6.1, P⬍0.05), and further
group had smaller cue-P2 amplitude than the average simple effect analysis showed that the frontal and fronto-
group (F(1,39)⫽7.22, P⬍0.05), and the cue condition in- central areas evoked larger N2 amplitude than the central
duced larger cue-P2 amplitude than the non-cue condition area in the Nogo condition.
(F(1,39)⫽6.18, P⬍0.05). Cue condition and Electrode sites The mean peak amplitudes and latencies of P3 (300 –
had significant interaction effect on cue-P2 amplitude 500 ms, at the electrodes of F3-Fz-F4, FC3-FCz-FC4,
(F(2,39)⫽7.01, P⬍0.05), and further simple effect contrast C3-Cz-C4, P3-Pz-P4, PO3-POz-PO4) are presented in
analysis showed that the cue condition evoked larger cue-P2 Table 4 and subjected to repeated measures ANOVAs
amplitude in the frontal and fronto-central areas than the with Intelligence (two levels, gifted group and average
non-cue condition. group) as between-subject factor, Go/Nogo condition (two
The mean peak amplitudes and latencies of cue-P3 levels, Go condition and Nogo condition) and Electrode
(250 – 450 ms, at the electrodes of F3-Fz-F4, FC3-FCz- sites (five levels, frontal area [F3-Fz-F4], fronto-central
FC4, C3-Cz-C4, P3-Pz-P4) are presented in Table 3 and area [FC3-FCz-FC4], central area [C3-Cz-C4], parietal
subjected to repeated measures ANOVAs with Intelligence area [P3-Pz-P4], parietal-occipital area [PO3-POz-PO4])
(two levels, gifted group and average group) as between- as within-subject factors. The Nogo condition induced sig-
subject factor, Cue condition (two levels, cue condition and nificantly later P3 response than the Go condition
non-cue condition) and Electrode sites (four levels, frontal (F(1,39)⫽16.4, P⬍0.005). Intelligence and Go/Nogo con-
area [F3-Fz-F4], fronto-central area [FC3-FCz-FC4], cen- dition had significant interaction effect on P3 latency
tral area [C3-Cz-C4], parietal area [P3-Pz-P4]) as within- (F(1,39)⫽5.3, P⬍0.05), and further simple effect contrast
subject factors. The cue condition induced larger and ear- analysis showed that the gifted children had significantly
lier cue-P3 response than the non-cue condition (ampli- earlier P3 response in the Nogo condition than the average
tude: F(1,39)⫽18.7, P⬍0.001; latency: F(1,39)⫽5.9, P⬍ children did. Furthermore, the gifted children elicited sig-
0.05), and the parietal area had larger and earlier cue-P3 nificantly larger P3 amplitude than the average children
activation than the other areas (amplitude: F(3,39)⫽23.71, (F(1,39)⫽20.2, P⬍0.001), and the parietal area had larger
P⬍0.001; latency: F(3,39)⫽11.5, P⬍0.01). Intelligence P3 amplitude than the other areas (F(4,39)⫽15.9, P⬍
and Electrode sites had significant interaction effect on 0.005). Intelligence and Go/Nogo condition had significant
cue-P3 amplitude (F(3,39)⫽10.1, P⬍0.01), and further interaction effect on P3 amplitude (F(1,39)⫽14.5, P⬍
simple effect analysis showed that the gifted children had 0.005), and further simple effect contrast analysis showed
larger cue-P3 amplitude than the average children in the that the average children induced smaller P3 amplitude in
fronto-central, central and parietal areas but not in the the Nogo condition than that in the Go condition. Go/Nogo
frontal area. condition and Electrode sites had significant interaction
effect on P3 amplitude (F(4,39)⫽15.7, P⬍0.005), and fur-
ERP results of Go-Nogo cognitive control processes
ther simple effect contrast analysis showed that the Nogo
Fig. 2 showed two groups’ neural activation of N2 and P3 condition induced larger P3 amplitude than the Go condition
responses for cognitive control processes, and the mean in the frontal and fronto-central areas, while the Go condition
peak amplitudes and latencies of N2 (200 –350 ms, at the elicited larger P3 amplitude than the Nogo condition in the
electrodes of F3-Fz-F4, FC3-FCz-FC4, C3-Cz-C4) are central, parietal and parietal-occipital areas.
presented in Table 4 and subjected to repeated measures
ANOVAs with Intelligence (two levels, gifted group and
DISCUSSION
average group) as between-subject factor, Go/Nogo con-
dition (two levels, Go condition and Nogo condition) and Current study was devoted to investigate the neural corre-
Electrode sites (three levels, frontal area [F3-Fz-F4], lation among response preparation, cognitive control and
fronto-central area [FC3-FCz-FC4], central area [C3-Cz- human intelligence, and the behavioral results indicated
C4]) as within-subject factors. The statistical results sho- that gifted children could execute Go responses with in-
126 T. Liu et al. / Neuroscience 180 (2011) 122–128
Fig. 2. Children’s ERP activation of N2 and P3 during conflict monitoring and cognitive control processes in the Go condition and the Nogo condition.
creased accuracies and inhibit improper responses (Nogo al., 2007; Johnson et al., 2003). The electrophysiological
response) with less commission error rate than intellectu- results further demonstrated how response preparation
ally average children, which illustrated that gifted children affected cognitive control processes between two groups
had better cognitive control abilities (Arffa, 2007; Calero et of children.
Table 4. Children’s mean and standard deviation of peak amplitudes (V) and latencies (ms) of N2 and P3 during conflict monitoring and cognitive
control processes in the Go condition and the Nogo condition
Gifted group Go condition 217 (20.6) ⫺0.2 (0.02) 337 (18) 12 (2.8)
Nogo condition 244 (20.5) ⫺1.5 (0.05) 358.4 (16.5) 11.3 (2.8)
Average group Go condition 220 (21.6) 1 (0.04) 336 (17.6) 10.6 (2.6)
Nogo condition 254 (21.5) ⫺1.1 (0.04) 384 (18.6) 7.5 (2.1)
T. Liu et al. / Neuroscience 180 (2011) 122–128 127
Response preparation 2006; Jonkman, 2006; Smith et al., 2008). Present study
achieved that N2 component was strongly elicited under
The current waveform morphology was similar with previous
the Nogo condition and mainly distributed across frontal
studies that reported cue-related fronto-central P2 and cen-
and fronto-central areas but not over central area, which
tro-parietal P3 could be significantly induced by the cue stim-
supported the previous source location analysis that re-
uli for the response preparation processes in the cue-related
garded Nogo-N2 was generated in ACC and dorsolateral
Go/Nogo paradigms (Banaschewski et al., 2003; Bekker et
frontal lobe (Falkenstein, 2006; Smith et al., 2008; van
al., 2004; Jonkman, 2006). Children’s cue-P2 and cue-P3
Veen and Carter, 2002) and related to conflict monitoring
responses under the cue condition and non-cue condition
processing (Botvinick et al., 2004). Moreover, it was ob-
were compared to analyze the differences in neural activation
served that gifted children induced faster N2 response
during cue-related response preparation processes. The re-
than their average peers, which suggested that they could
sults achieved that the cue condition elicited larger cue-P2
efficiently detect conflict situation with faster neural pro-
activation than the non-cue condition, which supported that
cessing speed, and gifted children’s better conflict moni-
cue-P2 activation reflected early cue-related automatic sen-
toring processing might rely on their mature frontal function
sory processing (Banaschewski et al., 2003). Interestingly,
in solving conflict and complex problems (Jonkman, 2006;
present study found that gifted children induced smaller
Segalowitz and Davies, 2004; Shaw et al., 2006). These
cue-P2 responses than their average peers, and this result
findings were different from Duan et al. (2009)’s study
was out of our expectation and might illustrate that gifted
which did not find any differences in neural activation
individuals could complete cue-related automatic sensory
between gifted children and average children during con-
processing by devoting less neural effort, which might be due
flict monitoring processing. One possible reason was that
to their efficient pre-attention processing (Liu et al., 2007). In
their experimental paradigm was too simple and only con-
addition, this finding was in line with previous studies which
tained two stimuli (digit one and nine), one for Go condition
reported that brighter individuals produced less cortical acti-
and the other for Nogo condition, and both groups of
vation (more neural efficiency) when accomplishing cognitive
children could complete the task successfully without de-
operations (Neubauer and Fink, 2003; Neubauer et al.,
voting much neural effort and resource to detect the con-
2004), so the current finding could also support the neural
flict situation. While, the current CPT-ABX paradigm com-
efficiency hypothesis of intelligence which emphasized that
prised more conflict (Bekker et al., 2004) and made aver-
gifted individuals had more efficient neural functions and
age children devote more neural effort to complete the
could use fewer neurons and specific neuronal circuits to
task, and further led to their slower neural response speed
complete cognitive tasks than intellectually average individu-
in conflict detection processing.
als (Neubauer and Fink, 2009).
During attentional control processing, current study
Furthermore, current study also observed that the cue
achieved that participants had larger and faster Go-P3
condition induced larger and faster cue-P3 response than the
response comparing with Nogo-P3, and Nogo-P3 was
non-cue condition, which confirmed that cue-P3 activation
strongly activated over frontal and fronto-central areas for
reflected cue evaluation and expectation to the occurrence of
motor inhibition, while Go-P3 reflected executive control
Go stimuli (Bekker et al., 2004), and it supported that cue-P3
and was mainly generated across central and parietal
activation was generated from parietal area (Banaschewski
areas (Bokura et al., 2001; Smith et al., 2008). Further-
et al., 2003; Bekker et al., 2004; Jonkman, 2006). Moreover,
more, gifted children induced faster P3 response in the
it was also achieved that gifted children induced larger
Nogo condition, which was consistent with Duan et al.’s
cue-P3 response over fronto-central and parietal areas, while
findings, and it was demonstrated that gifted children could
average children activated frontal area for cue-P3 activation,
withhold the improper responses with faster neural pro-
and this finding might indicate that gifted children saved some
cessing speed. Current study also observed that gifted
frontal resource for the following cognitive control processes
children elicited larger P3 activation and without significant
which strongly required frontal function (Bokura et al., 2001;
differences between their Go-P3 and Nogo-P3 responses,
Botvinick et al., 2004) and their efficient cue evaluation pro-
but average children induced smaller Nogo-P3 than Go-P3
cessing could make better neuropsychological preparation
activation. Previous studies have stated that frontal-pari-
for the subsequent neural processes (Freitas et al., 2007;
etal network closely related to cognitive control processes
Jonkman, 2006). Therefore, the different neural reaction pat-
(Brass et al., 2005; Bunge et al., 2002), and current results
terns between these two groups further demonstrated that
of P3 activation further demonstrated that gifted children
gifted children had more efficient neural function for cue-
might have developed more mature frontal-parietal neural
target response preparation processes (Liu et al., 2007; Neu-
network for both inhibition control and execution control
bauer and Fink, 2009; Segalowitz et al., 1992).
processes comparing with their average peers (Duncan,
2003; Gray et al., 2003; Neubauer and Fink, 2009). More-
Conflict monitoring and inhibition control
over, inhibition control was one of the most important
Consistent with previous CPT-AX studies, our present components of self-regulation abilities, and the current
study achieved similar waveform morphology of frontal N2 findings also provided the electrophysiological proof for
for conflict monitoring and P3 for inhibition control pro- gifted children’s better self-regulation abilities and strate-
cesses (Bekker et al., 2004; Bokura et al., 2001; Bruin et gies (Calero et al., 2007). Taken together the electro-
al., 2001; Donkers and van Boxtel, 2004; Falkenstein, physiological findings in both conflict monitoring and
128 T. Liu et al. / Neuroscience 180 (2011) 122–128
cognitive control processes, it further supported that Bruin KJ, Wijers AA, van Staveren AS (2001) Response priming in a
gifted children had more efficient and mature neural go/nogo task: do we have to explain the go/nogo N2 effect in terms
function in accomplishing complex cognitive processes of response activation instead of inhibition? Clin Neurophysiol
112:1660 –1671.
(Jaušovec and Jaušovec, 2000; Shaw et al., 2006).
Bunge SA, Dudukovic NM, Thomason ME, Vaidya CJ, Gabrieli JDE
(2002) Immature frontal lobe contributions to cognitive control in
CONCLUSION children: evidence from fMRI. Neuron 33:301–311.
Calero MD, García-Martín MB, Jiménez MI, Kazén M, Araque A (2007)
This study confirmed the significant correlations among
Self-regulation advantage for high-IQ children: findings from a
response preparation, cognitive control and intelligence in research study. Learn Individ Differ 17:328 –343.
early adolescents. The intellectually gifted group exhibited Donkers FC, van Boxtel GJ (2004) The N2 in go/no-go tasks reflects
better execution and inhibition control performances than conflict monitoring not response inhibition. Brain Cogn 56:165–176.
the average group. In response preparation processes Duan X, Shi J, Wu J, Mou Y, Cui H, Wang G (2009) Electrophysio-
gifted children had efficient cue-related automatic sensory logical correlates for response inhibition in intellectually gifted chil-
dren: a go/nogo study. Neurosci Lett 457:45– 48.
processing (smaller cue-P2) and stronger neural activation
Duncan J (2003) Intelligence tests predict brain response to demand-
for cue evaluation processing (larger cue-P3), and during ing task events. Nat Neurosci 6:207–208.
cognitive control processes they could detect conflict situ- Falkenstein M (2006) Inhibition, conflict and the nogo-N2. Clin Neuro-
ation by eliciting faster N2 response over frontal and cen- physiol 117:1638 –1640.
tral areas and induce faster and stronger P3 activation for Freitas AL, Azizian A, Leung HC, Squires NK (2007) Resisting recently
attentional control processes than their average peers. acted-on cues: compatibility of go/nogo responses to response
The current findings further supported the neural efficiency history modulates (frontal P3) event-related potentials. Psycho-
physiology 44:2–10.
hypothesis of intelligence and made valuable contribution
Gray JR, Chabris CF, Braver TS (2003) Neural mechanisms of general
to the understanding of the developmental trajectory of fluid intelligence. Nat Neurosci 6:316 –322.
general intelligence and cognitive control. Green DM, Swets JA (1966) Signal detection theory and psychophys-
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Ackowledgments—This research was supported by Natural Sci- Jaušovec N, Jaušovec K (2000) Correlations between ERP parame-
ence Foundation for the Youth of China (Grant No. 31000468), ters and intelligence: a reconsideration. Biol Psychol 50:137–154.
Outstanding Doctoral Dissertation and President Award Scientific Johnson J, Im-Bolter N, Pascual-Leone J (2003) Development of
Research Foundation of Chinese Academy of Sciences, and Sci- mental attention in gifted and mainstream children: the role of
entific Research Foundation for the Youth of Institute of Psychol- mental capacity, inhibition, and speed of processing. Child Dev 74:
ogy, Chinese Academy of Sciences. We express our warmest 1594 –1641.
thanks to all of the children for their participation. The helpful Jonkman LM (2006) The development of preparation, conflict moni-
comments of the anonymous reviewers are gratefully acknowl- toring and inhibition from early childhood to young adulthood: a
go/nogo ERP study. Brain Res 1097:181–193.
edged.
Liu T, Shi J, Zhang Q, Zhao D, Yang J (2007) Neural mechanisms of
auditory sensory processing in children with high intelligence. Neu-
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