Developmental change of neurocognitive motor behavior in a continuous performance test with different interstimulus intervals

Developmental change of neurocognitive motor behavior in a continuous performance test with different interstimulus intervals

Clinical Neurophysiology 115 (2004) 1104–1113 www.elsevier.com/locate/clinph Developmental change of neurocognitive motor behavior in a continuous pe...

523KB Sizes 0 Downloads 17 Views

Clinical Neurophysiology 115 (2004) 1104–1113 www.elsevier.com/locate/clinph

Developmental change of neurocognitive motor behavior in a continuous performance test with different interstimulus intervals Shinji Okazakia,*, Miyuki Hosokawab,c, Yuki Kawakubob, Hisaki Ozakid, Hisao Maekawaa, Satoshi Futakamie a

Institute of Disability Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba 305-8572, Japan Doctoral Degree Program of Disability Sciences, University of Tsukuba, Tsukuba 305-8572, Japan c Research Fellow of the Japan Society for the Promotion of Science, Japan d Laboratory of Physiology, Ibaraki University, Mito 310-8512, Japan e Department of Child Rehabilitation, Nippon Telegraph and Telephone East Corporation, Izu Medical Center, Kannami 419-0107, Japan b

Accepted 17 December 2003

Abstract Objective: We investigated the neurocognitive process of motor control using event-related potentials during a cued continuous performance test with different interstimulus intervals in healthy children, and examined their neurocognitive process in motor execution and in motor inhibition. Methods: Twenty-eight children group by age (9 years n ¼ 8, 11 years n ¼ 9, 13 years n ¼ 11) and 10 adults participated. In cued continuous performance test, subjects were asked to press a button when ‘9’ appeared immediately after ‘1.’ To maintain uncertainty in the stimulus series, we used 3 interstimulus intervals between the warning stimulus and subsequent target (800 ms, 1500 ms, 3000 ms). Results: Effects of different interstimulus intervals were observed in the reaction time of hits regardless of the age of the subject. In adults, spatial distribution of the P3 component elicited by targets was centro-parietal maximum that was discriminable from the distribution of Nogo P3, which was characterized by centro-parietal dominant distribution under all interstimulus interval (ISI) conditions. However, in younger children (9 years), the P3 component elicited by No-go distributed to the centro-frontal area, and P2/N2 with a significant anterior negative/posterior positive distribution was observed. As age increased, the dominant distribution of No-go P3 shifted significantly to a more anterior area compared with that of Target P3, and significantly prolonged ISI brought No-go P3 with centro-frontal dominant distribution that might indicate motor inhibition. Conclusions: These results indicated that behavioral change in the developmental course might be concerned with automatization of orientation and evaluation of stimulus relevance. Furthermore, efficient motor control might be enabled by establishment of an inhibitory process in the anterior area, in addition to an executive process in the posterior area. q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. Keywords: Continuous performance test; Neurocognitive development; Motor behavior; Event related potential; Interstimulus interval

1. Introduction Various cerebral structures and neural interconnections contribute to regulating motor behavior, and those cerebral structures might be required to mediate sensory and motor information in visuocognitive motor behavior (Ballard, 2001). Mesulam (1981) suggested contributions of posterior * Corresponding author. Institute of Disability Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba 305-8572, Japan. Tel.: þ 81-29-8536804. E-mail address: [email protected] (S. Okazaki).

parietal cortex to spatial attention, of prefrontal cortex to anticipated motor control, and of brain-stem structures to arousal. Brain imaging studies have demonstrated cerebral activation in those areas while subjects were engaging in cognitive tasks (functional magnetic resonance imaging: Casey et al., 1997; positron emission tomography: Buchsbaum et al., 1990; Pardo et al., 1991; Event-related potential (ERP): Fallgatter et al., 1997; Strik et al., 1998). As an appropriate motor control involves motor activation and motor inhibition, a well-designed experimental paradigm will be needed to elucidate both the covert information processing and overt behavioral control.

1388-2457/$30.00 q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2003.12.021

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

For that purpose, various experimental paradigms have been adopted, i.e. Go/No-go task (Simson et al., 1977), Stroop test (Barkley and Grodzinsky, 1994) and Continuous performance test (CPT; Rosvold et al., 1956). Above all, the CPT has been used widely to assess sustained attention and control of motor response in ADHD and in schizophrenia (Corkum and Siegel, 1993; Cornblatt and Keilp, 1994). The CPT is an attention task in which a series of stimuli (usually letters or digits by visual or auditory modality) are presented individually. This task is roughly divided into CPT-X, CPT-AX, and CPT-Double by target demand. For example, subjects are asked to respond to a target with low probability such as X in CPT-X, while in CPT-AX, subjects are asked to respond to a target within a cue-target sequence such as A-X, i.e. a motor response is required when a designated ‘X’ follows immediately after the specific warning signal ‘A’ (Halperin et al., 1988; Corkum and Siegel, 1993). As expectation released by the warning stimulus might affect motor behavior, CPT-AX is an optimal paradigm for investigating anticipated motor control, including motor inhibition. As for the motor execution, an abundance of information on executive motor processes is provided by behavioral measures (rate of hit, rate of commission, and reaction time). However, as subjects are asked to inhibit their motor response in the non-target trial, the inhibitory process of motor control is difficult to explain by the limited behavioral measures. To extend and supplement the behavioral findings, ERP might provide additional important information regarding the cerebral regulatory process during motor control (Fallgatter et al., 1997; Strik et al., 1998; Okazaki et al., 1999). In normal adult subjects, the mode of motor behavior defines the distribution of ERP, i.e. presentation of the target stimulus after the warning direct the subjects to motor execution and elicits a P3 positivity distributed dominantly in the parietal area. However, nontarget stimuli after the warning direct subjects to inhibit motor activity, resulting in P3 positivity distributed dominantly in the pre-central area. Moreover, these differences in spatial distribution between target stimuli and non-target stimuli have been confirmed in children (Overtoom et al., 1998; van Leeuwen et al., 1998). In many prior studies, CPT-AX with regular interstimulus interval (ISI) was adopted (Corkum and Siegel, 1993). However, a task with a fixed ISI would enable subjects to estimate the occurrence of the following stimulus. Such temporal priming might be unavoidable in CPT-AX with fixed ISI (Posner and Snyder, 1975). As a result, control of motor response in fixed ISI might be easier than that under conditions where temporal timing of the stimulus series was unpredictable. Different ISIs in CPT-AX might show different results (e.g. Conners, 1995; Shelley et al., 1996), and the interval between the warning stimulus and the subsequent target (foreperiod) might also affect motor control. i.e. the foreperiod affects task performance (Alegria, 1975) and the ISI length, as well as ISI regularity,

1105

in CPT-AX affects both performance and ERPs (Shelley et al., 1996). In this study, we recorded ERPs during CPT-AX with different ISIs in healthy children in several age groups, and examined the neurocognitive process during motor execution and that during motor inhibition.

2. Materials and methods 2.1. Subjects Twenty-eight children and 10 adults (male ¼ 7, female ¼ 3, mean age 25.2 years, age range 22.7– 32.2) participated in this study. Children were divided into 3 age groups, a 9-year-old group (male ¼ 4, female ¼ 4, mean age 9.0 years, age range 8.7 – 9.5), an 11-year-old group (male ¼ 7, female ¼ 2, mean age 11.3 years, age range 10.10 – 11.10), and a 13-year-old group (male ¼ 10, female ¼ 1, mean age 13.0 years, age range 12.1– 13.10). All participants were healthy with normal vision. Informed consent was obtained from all participants or from their parents prior to the experiment.

2.2. Task The time sequence of stimulus presentation in CPT-AX is shown in Fig. 1. The stimulus was presented on CRT using STIM software (NeuroScan Inc.). Subjects were asked to press a button when ‘9’ was presented immediately after ‘1’ (warning stimulus). To maintain temporal uncertainty in the stimulus series, we implemented 3 different ISIs between the warning stimulus and the subsequent target (800, 1500 and 3000 ms). The probability of Target (‘9’ after ‘1’) and No-go (a single digit other than ‘9’ after ‘1’) was 5% under each ISI condition. A series of 400 digits was presented per block and two blocks were presented. Between each block, there was a 10 min interval during which subjects were free from the task. It took 40 min for each experiment.

Fig. 1. Time sequence of stimulus presentation.

1106

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

2.3. EEG recordings Using Ag/AgCl electrodes (Electrocap), EEGs were recorded from 15 locations on the scalp according to the 10 –20 system with linked earlobes as a common reference. Vertical EOG was also monitored. EEG was filtered with a bandpass of 0.05– 30 Hz and digitized at 500 Hz. Sweeps with artifacts more than 80 mV were excluded from further analysis. Sweeps with response failure and those with false alarms were also excluded. ERPs were separately averaged for Target and for No-go after warnings under each ISI condition. 2.4. Data analysis Percentage of correct response to target (rate of hits) and mean reaction time with correct response (mean RT of hits) was collected for each subject. Percentage of incorrect responses to nontargets (rate of false alarms; FA) was also collected. Total numbers of FA were classified into 4 subtypes (1-not-9 error, 1-only error, 9-only error, and random error; Halperin et al., 1991). Rate of 1-not-9 errors (erroneous response to No-go) and rate of 1-only errors (erroneous response to warning) were examined in this study. Rate of hits, FA, and RT were compared statistically using analysis of variance (ANOVA, repeated-measure) within factors of the subject group (9 years, 11 years, 13 years and adults) and of ISI conditions (Short, Medium, Long). Contrast tests were performed to compare measurement between groups (Fisher’s PLSD, P , 0:05). To examine the time course of brain electric field, global field power (GFP), global dissimilarity and Centroid locations (positive and negative) were computed using an average reference (Lehmann and Skrandies, 1980; Wakkermann et al., 1993). Computing spatial standard deviations of over all voltages in each map, a single numerical figure was obtained as GFP. Dissimilarity indicates the amount of topographic difference between the current electric field and the adjacent area. Referring to the maximal point in the dissimilarity curve and to the minimal point in the GFP curve, a temporal boundary between different microstates was determined (Brandeis et al., 1998). ERPs were statistically compared using ANOVA (repeated-measure), and tested for significant effects per subject group (9 years, 11 years, 13 years and adults), per stimulus condition (Target or No-go) and per ISI condition (Short, Medium, Long). Contrast tests were performed to compare measurement between groups (Fisher’s PLSD, P , 0:05). 3. Results 3.1. Performance of CPT-AX Mean hit rate and RT in each age group are shown in Fig. 2. Hit rate increased significantly with age (ANOVA;

Fig. 2. Mean rate and RT of hits in each group.

Fð3; 68Þ ¼ 9:713, P , 0:0001), i.e. the hit rate in the 11-year-old group increased significantly compared to that in the 9-year-old group (P , 0:05). In the 9-year-old group, hit rate with Short ISI was significantly higher than that with Long ISI (P , 0:05). In the remaining subject groups, significant difference was not observed among hit rates in each ISI condition. The mean RT differed significantly among subject groups (Fð3; 68Þ ¼ 6:003, P , 0:01), and a significant difference was observed between RT in the 9-year-old group and that in the 13-year-old group (P , 0:05). In every subject of the 11-year-old, 13-year-old and adult groups, RT with Short ISI was significantly longer than that with Long ISI (P , 0:01). The main effect of subject group on rates of FA subtypes was observed (Fð3; 136Þ ¼ 3:710, P , 0:05, Table 1), i.e. the rate of 1-not-9 error was significantly larger than that of 1-only error in every subject group for each ISI condition (Fð1; 136Þ ¼ 29:730, P , 0:0001). Significant differences were observed between rate of 1-not-9 errors in the 11-yearold group and that in adults (P , 0:05). There was no significant difference among FA of 1-only error in each subject group. A main effect of ISI was observed (Fð2; 136Þ ¼ 22:590, P , 0:0001), and interaction with FA subtypes and ISI condition was also observed (Fð2; 136Þ ¼ 24:098, P , 0:0001). With prolongation of ISI, 1-not-9 errors increased significantly in the 9-year-old and 11-year-old groups (P , 0:05). In the 13-year-old

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

1107

Table 1 Mean rate of 1-not-9 error and 1-only error under each ISI condition Group

9-year-old 11-year-old 13-year-old Adult

1-not-9 error

AVG SD AVG SD AVG SD AVG SD

1-only error

Short

Medium

Long

Short

Medium

Long

0.3125 0.88388 0.27778 0.83333 0.22727 0.75378 0 0

0.9375 1.86006 1.94444 3.25427 1.81818 2.52262 0 0

1.5625 1.86006 2.22222 2.3199 1.13636 1.71888 0.75 1.20761

0 0 0 0 0 0 0 0

0.3125 0.88388 0.41667 0.88388 0 0 0 0

0.46875 0.64694 0.27778 0.5512 0.22727 0.50565 0 0

group, 1-not-9 errors under Medium ISI were significantly increased compared with those under Long ISI conditions (P , 0:05). However, there was no significant difference observed in 1-only error under each ISI condition. 3.2. Spatio-temporal electric fields for Target/No-go stimuli in CPT-AX The grand mean ERP in the 9-year-old group (Target, Medium ISI) was segmented using GFP, global dissimilarities, Centroid, and ERP map series (Fig. 3). The maximal time point in the dissimilarity curve coincided with the minimal in the GFP curve, was designated as a boundary

(dotted line) between different microstates. This approach yielded 4 different successive segments under each ISI condition, i.e. temporo-occipital positivity around 130 ms (P1), temporo-occipital negativity around 180 ms (N1), posterior-positivity/anterior-negativity around 300 ms (P2/N2), and central-parietal dominant positivity (P3). These segments of ERP were stable regardless of subject group or stimulus condition (Target or No-go). Further analysis focused on each segment within the same time window between 100 and 500 ms. Temporal sequences of those spatial parameters were displayed under each stimulus condition (Fig. 4). ERP maps at GFP peak times of each component are also shown in Fig. 5.

Fig. 3. Adaptive segmentation of grand mean ERP (9-year-old) and ERP map series elicited by Target in Medium ISI.

1108

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

Fig. 4. Global field power (GFP), global dissimilarities (Diss.), and Centroid trajectories (Cent., anterior-posterior, A-P) under 3 ISI conditions for Target and No-go in each group.

3.2.1. N1 component Whether the stimulus condition was Target or No-go in all age groups, the boundary between P1 and N1 segments appeared around 150 ms after stimulation under Long ISI

conditions (Fig. 4). Statistical comparison of boundary latency by ANOVA demonstrated the main effect of ISI, i.e. prolongation of boundary latency between P1 and N1 segments according to the reduction of ISI

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

1109

Fig. 5. ERP peak map of each component elicited by peak of GFP under Target (A) and No-go (B) condition for each ISI.

(Fð3; 136Þ ¼ 3:069, P , 0:05). Also, further contrast tests demonstrated a significant difference between boundary latencies under different ISI conditions in both the 13-year-old and adult groups (P , 0:05). The peak latency of N1 significantly decreased with age (Fð3; 136Þ ¼ 28:687, P , 0:0001), and a significant difference in N1 latency was observed between the 13-year-old and adult groups (P , 0:05). The peak amplitudes of N1 were also increased significantly in the right-temporal electrode with the prolongation of ISI regardless of

whether the stimulus was Target or No-go (T4; Fð3; 136Þ ¼ 8:427, P , 0:05) in all subject groups (P , 0:05). 3.2.2. P2/N2 component In each year group, spatial features after the second segment boundary around 230 ms (N1 and P2/N2; Fig. 4) were characterized by posterior positive/anterior-negative brain electric field under every ISI condition. There were no significant differences between the latency of the second

1110

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

microstates in each age group regardless of whether the stimulus was Target or No-go (Fig. 4). The main effect on durations of P2/N2 segment was obtained in each subject group (Fð3; 136Þ ¼ 14:509, P , 0:0001), and the duration of P2/N2 segment in adults was significantly reduced compared to those in the remaining subject groups (P , 0:05). In every child group, the electric fields of P2/N2 were characterized by persistent anterior negativity/posterior positivity with greater intensity. The P2/N2 component was also observed in the adult group. However, the intensity of this component was not as prominent as those in the child groups (Fig. 5). 3.2.3. P3 component The transition from P2/N2 segment to P3 was ambiguous in the 9-year-old group (Target: Fig. 4A, No-go: Fig. 4B). In the remaining subject groups, however, the P2/N2 segment switched to the P3 segment more abruptly with prolongation of ISI. The main effect of ISI was obtained in the latency of the boundary between the P2/N2 and P3 segments (Fð3; 68Þ ¼ 9:624, P , 0:0001), and the onset of segment boundaries in adults was significantly faster than that in the 13-year-old group under all ISI conditions (P , 0:05). The latency of the P3 peak decreased with age (Fð3; 136Þ ¼ 20:569, P , 0:0001), and P3 latency differed significantly among all groups (P , 0:05). The main effect of subject (Fð3; 68Þ ¼ 9:5419, P , 0:0001) was obtained for positive Centroid in the y direction (anterior-posterior axis), i.e. Centroid location of P3 peak in the 9-year-old group distributed significantly more posterior than that in the other groups regardless of Target or No-go stimulus. The main effect of stimulus condition was also significant (Fð1; 68Þ ¼ 30:347, P , 0:0001), showing the No-go P3 was more anterior than Target P3 in the 11-year-old, 13-year-old, and adult groups. In these groups, the P3 component by Target was characterized as a centro-parietal dominancy (Fig. 5A), and that by No-go was characterized as a centro-frontal dominancy (Fig. 5B). Moreover, the main effect of ISI condition (Fð2; 67Þ ¼ 5:0166, P , 0:01) indicated that Nogo P3 under Long ISI condition distributed more anterior than that under Short ISI condition. In Short ISI, spatial distribution of P3 component under No-go conditions was similar to that under Target condition in the 9-year-old and 11-year-old groups. As for the 13-year-old and adult groups, a transition to No-go P3 segment abruptly occurred around 350 ms in Centroid trajectories (Fig. 4B), and anterior dominant P3 in adults was observed on the brain electric map (Fig. 5B). In Medium ISI, anterior P3 was also observed in the 11-year-old group, as well as in the 13-year-old and adult groups. However, P3 in the 9-year-old group was distributed in the centro-parietal area even under this ISI condition. Positive Centroid location of P3 in the 9-year-old group moved in the anterior direction with Long ISI.

4. Discussion 4.1. Behavioral performance on CPT-AX under different ISI conditions Behavioral measure (rate of hits, RT of hits, and rate of FA) might provide important information about motor behavior. Under the condition of stimulus presentation with random ISI, choice RT is affected by the length of the foreperiod, i.e. the target response is prolonged in short intervals (see for review Niemi and Na¨a¨ta¨nen, 1981). ISI in CPT-AX paradigm is also a crucial factor for the evaluation of response control even in normal adult subjects (Okazaki et al., 1999) or schizophrenic patients (Shelley et al., 1996). As well as the development of sustained attention, the developmental change in motor control in children has been studied using reaction time tasks (Williams et al., 1999) and using CPT (Greenberg and Waldman, 1993). However, developmental change under different ISI in CPT-AX has not yet been reported. In this study, we adopted CPT-AX with a fixed ISI except for the intervals between warning signal and subsequent target where 3 different ISIs were implemented. As to the RT under various ISI conditions, Los et al. (2001) has reported a delay of RT at short ISI. Results of Short ISI in our study corresponded with these prior studies; these prolongations of RT in shorter ISI might occur regardless of age. Moreover, shorter RT was observed in Long ISI, and the number of FAs was increased with ISI length regardless of 1-not-9 error or 1-only error. These results might reflect that the non-semantic priming performance contributed by the automatic activation process (Posner and Snyder, 1975). Therefore, ISI between warning and subsequent target might affect motor behavior in children. However, the obtained data on the rate of hits indicate that execution of an anticipated response might not be affected by different intervals. Especially, the rate of hits in the 11-year-old group and beyond indicated clear ceiling effects. These ceiling effects around 11 years were also observed in a prior study using CPT (Lin et al., 1999); there might be little influence in that different ISI conditions affect rate of hits. That is, even in the 9-year-old group, children were able to execute an appropriate motor behavior as long as the ISI cue-target was longer than 800 ms and shorter than 3000 ms. However, RT of hits and rate of FA subtype were remarkably affected by the length of foreperiod, i.e. RT under the Short ISI condition was prolonged and the FA response under the Long ISI condition was increased in each age group. As far as choice reaction time task is concerned, there was no FA observed in adult subjects (Olivier and Rival, 2002). The increased FA with prolonged ISI in this study suggests that inhibition of motor response was seriously affected by a longer foreperiod. Furthermore, FA under prolonged ISI even in adults indicates higher task demand in CPT-AX than that in choice reaction time task,

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

and subjects require more resources to actuate their motor control in CPT-AX. Developmental change was also observed both in RT of hits and in the rate of FA subtype. Olivier and Rival (2002) examined the choice reaction time in children (age 6, 8, and 10 years old) under conditions with different ISIs (500, 1000, and 2000 ms). They reported prolonged reaction time with more errors in children compared with adults. They also pointed out an ISI effect on motor behavior in each age group. In this study where the age window of the subjects was expanded to adulthood, we also obtained prolonged reaction time in children and similar ISI effects on motor behavior. Therefore, anticipated motor control seems to develop progressively throughout childhood until adolescence, although the length of the foreperiod significantly influenced their motor action. These findings were not determined without adapting the CPT-AX with different ISIs. Due to multiplicity of CPT-AX used in this study, CPT-AX might be a powerful tool to investigate the developmental process of motor regulation. To disclose further details of the regulatory process of motor action, we will discuss the neurocognitive data that provide objective evidence of biological phenomena. 4.2. Cerebral process and its development during execution for anticipated motor response As the development of motor controls might be deeply rooted in the neurophysiological background, a neurocognitive approach will complement and extend the findings derived from behavioral data. The obvious deflection in the primary ERP component might be N1, and the onset time of this component was delayed and the amplitude decreased due to a reduction in the stimulus interval after cue signal. A similar finding has also been reported on auditory modality (Teder et al., 1993). These findings imply that sensory processing at an early stage might be affected by whether related neural elements have recovered from information capture of previous stimulus. Therefore, the behavioral response with extended RT under Short ISI conditions might cause a delay due to insufficient recovery state at an early stage of sensory processing (Los et al., 2001). The subsequent obvious component following N1 might be P2/N2 with an anterior negative/posterior positive distribution, and this component has been regarded as being concerned with the engagement of attention as described by Posner and Petersen (1990). Using adaptive segmentation procedures, Brandeis et al. (1998) detected P2/N2 component distributed in the anterior-negative/ posterior-positive electric field during the Go/STOP task, and they concluded that P2/N2 was a component relevant to resource allocation. The amplitude of the P2/N2 component, in this study, decreased with development, and was characterized by a short segment duration with lower intensity in adults. However, this component was not

1111

affected by the ISI condition. Therefore, this component might be concerned with orienting attention to distinguish the relevancy of stimuli. A significant P2/N2 component in children might indicate insufficient (unelaborated) anticipated motor control and such an unelaborated motor control might become automatic with further development. Posterior P3 elicited by Target has already been reported in children (Overtoom et al., 1998; van Leeuwen et al., 1998). However, latency of the posterior P3 reported by these prior studies was approximately 300 ms, while the posterior P3 in our study followed P2/N2 with the latency of P3 being about 400 ms. That difference might be caused by increased demand of attentional orientation in changing stimulus ISI, and these results indicated that the CPT-AX paradigm in this study demands subject execution or inhibition of motor action at each experimental trial. Although high cognitive demand is involved in the experimental paradigm in this study, the posterior P3 was clearly observed under each ISI condition regardless of age. Therefore, the cerebral process concerned with motor execution has already been established at least by the age of 9. However, the time course of P3 significantly differed according to the age of the subjects. Such a delayed onset of P3 in the younger age group might indicate the prolixity of motor execution in children compared with that in adults. 4.3. Cerebral process and its development of inhibitory control on anticipated motor response As the No-go task demands that subjects not release their motor action, it is difficult to examine how subjects inhibit an anticipated motor action except when an erroneous response occurred as FA. However, it is possible to assess their neurocognitive process from the neuroelectric signal. Characteristics of the N1 component elicited by a No-go signal were comparable to that elicited by Target under different ISI conditions in each subject group. Regardless of the stimulus, the cerebral process of the perceptive stage of the visual signal is similarly affected according to the length of the stimulus ISI. P2/N2 component was also observed in each age group in children following the No-go signal. The intensity of P2/N2 decreased with age, and was unclear in adults. These results suggest that P2/N2 reflects the cognitive process of attentional orientation and of allocating resources regardless of stimulus relevance. In adults, however, spatial distribution of P3 component by Target was discriminable from that by No-go, i.e. Target P3 was characterized by centro-parietal dominant distribution, and No-go P3 was characterized by centro-frontal dominant distribution in all ISI conditions. The anteriorization of the No-go P3 was reported in many prior studies (Simson et al., 1977; Roberts et al., 1994; Fallgatter et al., 1997; Strik et al., 1998), and our results extend these findings, showing that the anteriorization of the No-go P3 might also occur with different ISI. The spatial distribution of Target P3 was not affected by the stimulus interval at any

1112

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113

age. However, the spatial distribution of No-go P3 was seriously affected by stimulus conditions and also by subjects. That is, even in the 13-year-old group, P3 by No-go under Short ISI characterized by centro-parietal dominant distribution also characterizes P3 by Target and might indicate motor execution. However, even in the 11-year-old group, No-go stimulus under Long ISI brought P3 with centro-frontal dominant distribution that might indicate motor inhibition. Strik et al. (1998) adopted source localization for No-Go anteriorization of P3 from healthy adults, and reported that right frontal sources are responsible for the No-Go P3. van Leeuwen et al. (1998) reported that an early CNV/P3 corresponding to P2/N2 and P3 in this study was observed only for cue and stimulus after cue in 11-year-old children with attention deficit and control children, and concluded that these reflected attentional orientation and response preparation. In our study, anterior P3 was ambiguous in the 9-year-old group. However, spatial distributions of the No-go P3 in the 11-year-old group and later were clearly shifted to a more anterior area. These results are consistent with those of van Leeuwen et al. (1998), and demonstrated an initial anteriorization of the No-Go P3 in children under 13 years old. Although the number of participants per age group in this study was rather small, our results corresponded with those of the prior study. Therefore, developmental processes of attention and motor control throughout childhood might involve the different maturational time course of the anterior and parietal cerebral cortices as proposed by Luria (1973). Moreover, in the 11-year-old group and thereafter, No-go P3 shifted more anteriorly with prolonged ISI, which might indicate that the long intervals specifically increase demands on the inhibitory processes as well as behavioral data. These results indicate that cerebral motor inhibition is achievable in children at 11 years or older if the warning signal is followed by non-target stimulus with an optimal interval. In conclusion, behavioral and neurocognitive approaches using CPT-AX with different ISI might be suitable to demonstrate efficient motor control by the interaction of the anterior and posterior brain areas.

References Alegria J. Sequential effects of foreperiod duration: some strategical factors in tasks involving time uncertainty. In: Rabbitt PMA, Dornic S, editors. Attention and performance, vol. V. London: Academic Press; 1975. p. 1 –10. Ballard JC. Assessing attention: comparison of response-inhibition and traditional continuous performance test. J Clin Exp Neuropsychol 2001; 23:331–50. Barkley RA, Grodzinsky G. Are neuropsychological tests of frontal lobe functions useful in the diagnosis of attention deficit disorders? Clin Neuropsychol 1994;8:121–39. Brandeis D, van Leeuwen TH, Rubia K, Vitacco D, Steger J, PascualMarqui RD, Steinhausen HC. Neuroelectric mapping reveals precursor

of stop failures in children with attention deficits. Behav Brain Res 1998;(94):111 –25. Buchsbaum MS, Nuechterlein KH, Haier RJ, Wu J, Sicotte N, Hazlett E, Asarnow W, Potkin S, Guich S. Glucose metabolic rate in normals and schizophrenics during the Continuous Performance Test assessed by positron emission tomography. Br J Psychiatry 1990;(156):216–27. Casey BJ, Castellanos FX, Giedd JN, Marsh WL, Hamburger SD, Schubert AB, Vauss YC, Vaituzis AC, Dickstein DP, Sarfatti SE, Rapoport JL. Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 1997;36:374–83. Conners CK. The Conners Continuous Performance Test. Toronto: MultiHealth Systems; 1995. Corkum PV, Siegel LS. Is the continuous performance task a valuable research tool for use with children with attention-deficit hyperactivity disorder? J Child Psychol Psychiatry 1993;34:1217–39. Cornblatt BA, Keilp JG. Impaired attention, genetics, and pathophysiology of schizophrenia. Schizophr Bull 1994;20:31 –46. Fallgatter AJ, Brandeis D, Strik WK. Robust assessment of the no-go anteriorisation of P300 microstates in a cued continuous performance test. Brain Topogr 1997;(9):295– 302. Greenberg LM, Waldman ID. Developmental normative data on the test of variables of attention (T.O.V.A.). J Child Psychol Psychiatry 1993;34: 1019–30. Halperin JM, Wolf LE, Pascualvaca DM, Newcorn JH, Healey JM, O’Brien JD, Morganstein A, Young JG. Differential assessment of attention and impulsivity in children. J Am Acad Child Adolesc Psychiatry 1988;27: 326 –9. Halperin JM, Sharma V, Greenblatt E, Schwartz ST. Assessment of the continuous performance test: Reliability and validity in a nonreferred sample. Psychological assessment. J Consult Clin Psychol 1991;3: 603 –8. Lehmann D, Skrandies W. Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroenceph clin Neurophysiol 1980;48:609–21. Lin CCH, Hsiao CK, Chen WJ. Development of sustained attention assessed using the Continuous Performance Test among children 6–15 years of age. J Abnorm Child Psychol 1999;27:403–12. Los SA, Knol DL, Boers RM. The foreperiod effect revisited: conditioning as a basis for nonspecific preparation. Acta Psychol 2001;106:121–45. Luria AR. The working brain: an introduction to neuropsychology. New York: Basic Books; 1973. Mesulam M-M. A cortical network for directed attention and unilateral neglect. Ann Neurol 1981;10:309–25. Niemi P, Na¨a¨ta¨nen R. Foreperiod and simple reaction time. Psychol Bull 1981;89:133–62. Okazaki S, Ozaki H, Maekawa H. Event-related potentials in motor response execution and inhibition during a cued continuous performance test with various interstimulus interval. Jpn J Electroenceph Clin Neurophysiol 1999;27:393–403. Olivier I, Rival C. Foreperiod duration and motor preparation during childhood. Neurosci Lett 2002;319:125– 8. Overtoom CCE, Verbaten MN, Kemner C, Kenemans JL, van Engeland H, Buitelaar JK, Camfferman G, Koelega HS. Associations between event-related potentials and measures of attention and inhibition in the continuous performance task in children with ADHD and normal controls. J Am Acad Child Adolesc Psychiatry 1998;37: 977 –85. Pardo JV, Fox PT, Raichle ME. Localization of a human system for sustained attention by positron emission tomography. Nature 1991;349: 61 –4. Posner MI, Petersen SE. The attention system of the human brain. Annu Rev Neurosci 1990;13:25– 42. Posner MI, Snyder CRR. Attention and cognitive control. In: Solso RL, editor. Information processing and cognition. Hillsdale, NJ: Erlbaum; 1975. p. 55– 85.

S. Okazaki et al. / Clinical Neurophysiology 115 (2004) 1104–1113 Roberts LE, Rau H, Lutzenberger W, Birbaumer N. Mapping P300 waves onto inhibition: Go/no-go discrimination. Electroenceph clin Neurophysiol 1994;92:44–55. Rosvold HE, Mirsky AF, Sarason I, Bransome Jr ED, Beck LH. A continuous performance test of brain damage. J Consult Psychol 1956; 20:343–50. Shelley AM, Grochowski S, Lieberman JA, Javitt DC. Premature disinhibition of P3 generation in schizophrenia. Biol Psychiatry 1996; 39:714–9. Simson R, Vaughan Jr HG, Ritter W. The scalp topography of potentials in auditory and visual go/no-go tasks. Electroenceph clin Neuropsysiol 1977;43:864 –75. Strik WK, Fallgatter AJ, Brandeis D, Pascual-Marqui RD. Threedimensional tomography of event-related potentials during response inhibition: evidence for phasic frontal lobe activation. Electroenceph clin Neurophysiol 1998;108:406– 13.

1113

Teder W, Alho K, Reinikainen K, Na¨a¨ta¨nen R. Interstimulus interval and the selective-attention effect on auditory ERPs: ‘N1 enhancement’ versus processing negativity. Psychophysiology 1993;30: 71– 81. van Leeuwen TH, Steinhausen H-C, Overtoom CCE, Pascual-Marqui RD, van’t Klooster B, Rothenberger A, Sergeant JA, Brandeis D. The continuous performance test revisited with neuroelectric mapping: impaired orienting in children with attention deficits. Behav Brain Res 1998;94:97–110. Wakkermann J, Lehmann D, Michel CM, Strik WK. Adaptive segmentation of spontaneous EEG map series into spatially defined microstates. Int J Psychophysiol 1993;14:269– 83. Williams BR, Ponesse JS, Schachar RJ, Logan GD, Tannock R. Development of inhibitory control across the life span. Dev Psychol 1999;35:205–13.