View
220
Download
0
Category
Preview:
Citation preview
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 1/10
Cortical rhythm of No-go processing in humans: An MEG study
Hiroki Nakata a,b,c,⇑, Kiwako Sakamoto a,b, Asuka Otsuka b, Masato Yumoto b, Ryusuke Kakigi a
a Department of Integrative Physiology, National Institute for Physiological Sciences, Okazaki, Japanb Department of Clinical Laboratory, Graduate School of Medicine, The University of Tokyo, Tokyo, Japanc Faculty of Sport Sciences, Waseda University, Tokorozawa, Japan
a r t i c l e i n f o
Article history:Accepted 27 June 2012
Available online 3 August 2012
Keywords:
MEG
Response inhibition
Somatosensory
Go/No-go
h i g h l i g h t s
We investigated the characteristics of cortical rhythmic activity in No-go processing during a somato-sensory Go/No-go paradigm, by magnetoencephalography (MEG).
A rebound in amplitude was recorded in the No-go trials for theta, alpha, and beta activity, peaking at
600–900 ms.
The cortical rhythmic activity clearly has several dissociated components relating to different motor
functions, including response inhibition, execution, and decision-making.
a b s t r a c t
Objective: We investigated the characteristics of cortical rhythmic activity in No-go processing during
somatosensory Go/No-go paradigms, by using magnetoencephalography (MEG).
Methods: Twelve normal subjects performed a warning stimulus (S1) – imperative stimulus (S2) task
with Go/No-go paradigms. The recordings were conducted in three conditions. In Condition 1, the Go
stimulus was delivered to the second digit, and the No-go stimulus to the fifth digit. The participants
responded by pushing a button with their right thumb for the Go stimulus. In Condition 2, the Go and
No-go stimuli were reversed. Condition 3 was the resting control.
Results: A rebound in amplitude was recorded in the No-go trials for theta, alpha, and beta activity, peak-ing at 600–900 ms. A suppression of amplitude was recorded in Go and No-go trials for alpha activity,
peaking at 300–600 ms, and in Go and No-go trials for beta activity, peaking at 200–300 ms.
Conclusion: The cortical rhythmic activity clearly has several dissociated components relating to different
motor functions, including response inhibition, execution, and decision-making.
Significance: The present study revealed the characteristics of cortical rhythmic activity in No-go
processing.
Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights
reserved.
1. Introduction
The cortical rhythmic activity relating to response inhibitory
processing has been clarified by using scalp electroencephalogra-phy (EEG). EEG has been frequently used to examine the dynamics
of synchronized cortical activity, and offers a high temporal resolu-
tion in the order of milliseconds. Several studies of EEG spectral
power have examined the characteristics of cortical oscillations
in No-go trials during Go/No-go paradigms (Shibata et al., 1997,
1998, 1999; Leocani et al., 2001; Kamarajan et al., 2004; Kirmizi-
Alsan et al., 2006; Barry, 2009; Harmony et al., 2009). A common
finding is that the power of the theta, alpha, and beta frequency
bands decreases or increases at 300–900 ms after the onset of a
No-go stimulus. For example, Leocani et al. (2001) reported
that the spectral power at 10 Hz and 18–22 Hz decreased at
300–600 ms after stimulus onset, and the power at 10 Hz and18–22 Hz increased at 900–1200 ms and 600–900 ms, respectively.
Harmony et al. (2009) showed a complex spatiotemporal pattern of
spectral power decreases and increases in Go- and No-go condi-
tions. These power changes may be due to a decrease or increase
in synchrony of the underlying neuronal populations. The former
case is called event-related desynchronization (ERD) (i.e. suppres-
sion), and the latter, event-related synchronization (ERS) (i.e. re-
bound) (Pfurtscheller and Lopes da Silva, 1999). There has been
interest in the role of cortical oscillatory activity in sensory, motor
and cognitive processing as a key factor in binding mechanisms
(Farmer, 1998; Alegre et al., 2002). The oscillations have been sug-
gested to reflect an idling cortex generated by a large area of highly
1388-2457/$36.00 Ó 2012 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.http://dx.doi.org/10.1016/j.clinph.2012.06.019
⇑ Corresponding author at: Faculty of Sport Sciences, Waseda University, 2-579-
15 Mikajima, Tokorozawa, Saitama 359-1192, Japan. Tel.: +81 4 2947 4614; fax: +81
4 2947 6826.
E-mail address: nakata@aoni.waseda.jp (H. Nakata).
Clinical Neurophysiology 124 (2013) 273–282
Contents lists available at SciVerse ScienceDirect
Clinical Neurophysiology
j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / c l i n p h
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 2/10
synchronous neuronal firing in the absence of inputs, or alterna-
tively, changes in coherent activity resulting from synchronous in-
puts from other brain regions ( Jurkiewicz et al., 2006). However,
the neurophysiological mechanisms and functional significance
for No-go-related cortical oscillations are not well understood,
although a number of studies have investigated movement-related
cortical oscillations with ERD and ERS (Pfurtscheller and Lopes da
Silva, 1999). We considered that other methodological approaches
were needed to improve understanding of the mechanisms, rather
than the use of EEG or standard Go/No-go paradigms.
Based on these previous studies, the objective of the current
study was to clarify the dynamics of the neuromagnetic cortical
rhythm related to response inhibitory processing in the main fre-
quency components (theta, alpha, and beta), by using magnetoen-
cephalography (MEG). MEG has theoretical advantages over EEG,
because the magnetic fields recorded on the scalp are less affected
by volume currents and anatomical inhomogeneity. MEG also has
a high temporal resolution,permitting neural activityto be differen-
tiated on a time scale of milliseconds (see reviews, Kakigi et al.,
2000; Kaneoke, 2006). Thus, MEG can detect neural activities in
the cerebral cortex directly. To our knowledge, however, no study
has used MEG to investigate the cortical rhythmic activity of re-
sponse inhibitory processing. In the present study, we used Tempo-
ral Spectral Evolution (TSE) to extract the spatiotemporal
characteristics of cortical oscillations, following previous MEG stud-
ies (Salmelin and Hari, 1994; Salmelin et al., 1995; Nagamine et al.,
1996; Salenius et al., 1997; Simoes et al., 2004; Tamura et al., 2005).
To obtain the waveforms of TSE, the signals were firstly filtered
through a passband suggested by a spectral analysis and, subse-
quently, the absolute signal values were averaged with respect to
the event (see a review, Hari et al., 1997). This demonstrates
event-related changes of the average amplitude level of oscillatory
activities in a given passband in thesame unit as theoriginal signals.
The present study used ‘somatosensory Go/No-go paradigms’, in
whichthe second or fifth digit of the left handwas stimulated. Some
event-related potential (ERP) studies found that the amplitude of
theN2 componentwas much smallerfollowingauditory than visualstimuli (Falkenstein et al., 1995, 1999; Kiefer et al. 1998). Falken-
stein et al. (1999) suggested that the inhibitory processing as re-
flected in N2 is modality specific. In a monkey study, Gemba and
Sasaki (1990) also reported that No-go potentials after an auditory
stimulus were observed in the rostral part of the dorsal bank of
the principal sulcus, as opposedto the caudal part of the same bank
after a visual stimulus. Therefore, the present study aimed to inves-
tigate the dynamics of the neuromagnetic cortical rhythm during
‘somatosensory Go/No-go paradigms’. We also designed a target
and non-target stimulus with the same probability to avoid the ef-
fect of stimulus probability and to minimize differences in response
conflictbetween eventtypes(Braveret al.,2001;Nakata et al.,2005).
2. Methods
2.1. Participants
Twelve normal right-handed subjects (three females and nine
males; mean age 31.3 years, range 25–42 years) participated. The
participants had no previous history of neurological or psychiatric
disorders. Informed consent was obtained from all subjects. The
study was approved by the Ethical Committee of the National Insti-
tute for Physiological Sciences.
2.2. Experimental paradigm
The participants performed a warning stimulus (S1) – impera-tive stimulus (S2) task with Go/No-go paradigms. S1 was an
auditory pure tone (60 dB SPL, 50 ms duration), presented binau-
rally through earphones. For S2, we stimulated the second or fifth
digit of the left hand with ring electrodes. The electrical stimuli
were a current constant square-wave pulse 0.2 ms in duration,
and the stimulus intensity was 2.5 times the sensory threshold,
which yielded no pain or unpleasant sensation. The anode was
placed at the distal interphalangeal joint and the cathode at the
proximal interphalangeal joint of the corresponding digit. The
probability of the stimulus for the second and fifth digits was even.
A pair of S1 and S2 stimuli was delivered to the participants at an
interval of 1500 ms. The S1–S1 interval was 5 s.
The recordings were conducted in three conditions. In Condi-
tion 1, the Go stimulus was delivered to the second digit of the left
hand, and the No-go stimulus to the fifth digit of the left hand. The
participants had to respond to it by pushing a button with their
right thumb (contralateral to the stimulated side) as quickly as
possible only after the presentation of a Go stimulus. In Condition
2, the stimulation was reversed, that is, the Go stimulus was deliv-
ered to the fifth digit and the No-go stimulus to the second digit.
The response task was the same as in Condition 1. Condition 3
was the resting control, in which the subjects were asked to relax
and rest quietly with no task. During the recordings, the partici-
pants were instructed to keep their eyes open and look at a small
fixation point positioned in front of them at a distance of approx-
imately 1.5 m. One run comprised 160 epochs of stimulation,
which included 80 epochs for the Go stimuli and 80 for the
No-go stimuli. The order of conditions was randomized for each
participant and counterbalanced across all participants. A practice
session consisting of 20 stimuli preceded the recordings.
2.3. MEG recordings and analysis
Brain activities in Go/No-go paradigms were recorded with a
helmet-shaped 306-channel detector array (Vectorview; ELEKTA
Neuromag Oy, Helsinki, Finland), which comprises 102 identical
triple sensor elements, in a magnetically shielded room. Each sen-
sor element consists of two orthogonal planar gradiometers andone magnetometer coupled to a multi-SQUID (Superconducting
Quantum Interference Device) and thus provides three indepen-
dent measurements of the magnetic fields. In the present study,
we analyzed MEG signals from 204-channel planar-type gradiom-
eters, because the data from magnetometers are usually susceptive
to global magnetic noise including changes in geomagnetic fields
(Hämäläinen et al., 1993) (the noise can be successfully canceled
out in recording with planar sensors). The signals were recorded
with a bandpass filter (0.1–100 Hz) and digitized at 900 Hz. Before
the recordings, four head position indicator (HPI) coils were at-
tached to specific sites on the subject’s head, and then electric cur-
rent was fed to the HPI coils to determine the exact location of the
head with respect to the MEG sensors. The x-axis was fixed with
the preauricular points, pointing to the right, the positive y-axistraversing the nasion, and the positive z -axis pointing up.
From the continuous MEG raw data, epochs from 1000 ms be-
fore the onset of S1 to 1500 ms after the onset of S2 were collected
for the off-line analysis (i.e. 4000 ms in total). The data were fil-
tered at around the theta band (4–8 Hz), alpha band (8–12 Hz),
and beta band (18–22 Hz). The filtered signals were then rectified
and averaged across epochs. The baseline was set from 1000 ms
before S1 onset to S1 onset. The magnetic responses from three re-
gions of 22 channels in each hemisphere (LF = left frontal, LC = left
central, LP = left parietal, RF = right frontal, RC = right central,
RP = right parietal) were averaged, and used for the analyses of
amplitude and latency (Fig. 1). The epochs containing eye motion
artifacts or blinks, which were inspected visually, were excluded
from the off-line analysis using the Graph in Elekta Neuromag soft-ware. In this software to view raw data, the artifacts were
274 H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 3/10
monitored in frontal regions, but detailed scales of the artifacts
could not be represented as a limitation of the system. Thus, we
checked them carefully to average. This method was followed by
previous studies using the same Neuromag system (Nagamine
et al., 1996; Tamura et al., 2005).
When analyzing the data, we investigated the neuromagnetic
cortical rhythm in Go (Condition 1), No-go (Condition 2), and Con-
trol (Condition 3) for the second digit stimulation, and Go (Condi-
tion 2), No-go (Condition 1), and Control (Condition 3) for the fifthdigit stimulation. If visible differences in the activity of ‘Go’ and/or
‘No-go’ were observed for each region, the peak latency was sub-
jected to an analysis of variance (ANOVA) with repeated measures
using within-subject factors. The peak latency of the suppression
and rebound was defined for each individual as the time when
the maximum deflection of the oscillation was observed in the text
data. In addition, the mean TSE amplitudes were calculated from
300 to 1200 ms after the onset of S2 in each band, which included
peak amplitudes of both maximal suppression and rebound. The
mean amplitudes in preparatory periods were analyzed from
500 ms to 1500 ms after the onset of S1. The data on mean ampli-
tude was subjected to ANOVAs with Digit (Second vs. Fifth), Condi-
tion (Go, No-go, and Control), Region (Frontal, Central and Parietal),
and Hemisphere (Left vs. Right) as within-subjects factors. Thebehavioral data on the mean reaction time (RT), the standard devi-
ation (SD) of RT, commission error, and omission error were sub-
jected to repeated measures ANOVAs with Condition (Condition
1 vs. Condition 2) as a factor. For all repeated measures factors with
more than two levels, it was tested whether Mauchly’s sphericity
assumption was violated. If the test result was significant and
the assumption of sphericity was violated, the Greenhouse–Geisser
adjustment was used to correct the sphericity by altering the de-
grees of freedom using a correction coefficient epsilon. When sig-
nificant effects were identified, the Bonferroni post hoc multiple
comparison was used to identify specific differences. Statistical
tests were performed using computer software (SPSS for windows
ver. 16.0, SPSS). Statistical significance was set atp
< 0.05.
3. Results
3.1. Behavioral performance
Table 1 shows the mean RT, SD of RT, commission error rate,
and omission error rate in Conditions 1 and 2. For the mean RT, a
significant main effect of Condition was found (F(1,11) = 24.509,
p < 0.001), indicating that the responses were faster for the second
digit than for the fifth digit. In addition, a significant main effect of
Condition was observed for the commission error rate
(F(1,11) = 11.312, p < 0.01), showing that the commission error
rate was significantly larger in Condition 2 than Condition 1. There
were no significant differences between conditions in the SD of RTor omission error rate.
3.2. Theta band
Fig. 2A displays the grand-averaged waveforms of theta bands
in the three conditions across all participants for the second digit
stimulation. Judging from the morphology, a rebound in amplitude
was recorded in No-go trials after the onset of S2. No remarkable
suppression or rebound was evident during Go and Control trials.
A rebound similar to that in the No-go trials was found for the fifth
digit stimulation (Fig. 2B). The latency in the No-go trials peaked at
around 800 ms (Table 2 and Supplementary Table S1). ANOVAs
with Hemisphere and Region as factors did not show any signifi-
cant main effects or interactions.ANOVAs for the mean amplitude of theta bands revealed main
effects of Condition (F(2,22) = 9.699, p < 0.01) and Digit
(F(1,11) = 6.015, p < 0.05), Digit–Region interaction (F(2, 22) =
7.357, p < 0.01), and Condition–Region interaction (Greenhouse–
Geisser correction: F(2.432, 26.751) = 4.303, e = 0.608, p < 0.05)
(Table 3 and Supplementary Table S2). Furthermore, three-way
ANOVAs with Digit, Condition, and Hemisphere showed a signifi-
cant main effect of Condition in the frontal region (F(2, 22) =
3.531, p < 0.05), significant main effects of Digit (F(1,11) = 8.182,
p < 0.05) and Condition (F(2, 22) = 11.123, p < 0.001) in the tempo-
ral region, and significant main effects of Digit (F(1,11) = 6.091,
p < 0.05) and Condition (F(2, 22) = 7.819, p < 0.001) in the parietal
region.
A post hoc analysis revealed that mean amplitude was signifi-cantly more positive in No-go than Go and Control in the temporal
region ( p < 0.001, and p < 0.01, respectively), and in No-go than Go
and Control in the parietal region ( p < 0.01, and p < 0.05,
respectively).
3.3. Alpha band
Fig. 3A represents the grand-averaged waveforms of alpha
bands in each condition for the second digit. The rebound in No-go
trials was recorded in all regions, peaking at around 700–800 ms
for the second digit stimulation. The rebound was confirmed in
the central and parietal regions for the fifth digit stimulation
(Fig. 3B). ANOVAs for the peak latency in the second and fifth digit
stimulation did not show any significant main effects or interac-tions. Suppression for the second digit was recorded only in Go
Fig. 1. Location of sensors in the regions of interest. LF = left frontal, LC = left
central, LP= left parietal, RF = right frontal, RC = right central, RP = right parietal.
Table 1
The mean reaction time and error rates in the two movement conditions.
RT (ms) SD of RT (ms) Com (%) Omi (%)
Con. 1 248.8 (17.8) 56.1 (6.9) 1.0 (0.3) 0.8 (0.6)
Con. 2 271.0 (18.3) 64.3 (6.7) 4.0 (0.9) 1.1 (0.6)
Con.: Condition; Com: commission error; Omi: omission error. Values in paren-theses are the standard error (SE).
H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282 275
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 4/10
trials at LC, LP, RC, and RP, peaking at 400–600 ms (Table 2). Sup-
pression for the fifth digit was obtained in Go and No-go trials at
LP and RP, peaking at 300–400 ms (Supplementary Table S2). AN-
OVAs with Condition and Hemisphere demonstrated a significant
main effect of Condition (F(1,11) = 7.217, p < 0.05), indicating that
the peak latency of the suppression was earlier in No-go than Go.
ANOVAs for the mean amplitude of alpha bands revealed a main
effect of Condition (F(2,22) = 14.996, p < 0.001), Digit–Hemisphere
interaction (F(1, 11) = 9.297, p < 0.05), and Condition–Region inter-
action (Greenhouse–Geisser correction: F(2.012,22.128) = 6.656,e = 0.503, p < 0.01) (Table 3 and Supplementary Table S2). In
addition, three-way ANOVAs with Digit, Condition, and Hemi-
sphere demonstrated significant main effects of Condition in the
frontal region (F(2,22) = 13.762, p < 0.05), in the temporal region
(F(2,22) = 17.724, p < 0.001), and in the parietal region
(F(2,22) = 10.442, p < 0.01).
Post hoc testing showed that the mean amplitude was signifi-
cantly more positive in No-go than Go and Control in the frontal re-
gion ( p < 0.001, and p < 0.01, respectively), more positive in No-go
than Go and Control in the central region ( p < 0.001, and p < 0.01,
respectively), more positive in No-go than Go in the parietal region( p < 0.001).
Fig. 2. (A) (B) Grand-averaged waveforms of theta bands in the frontal, central, and parietal regions for the second and fifth digit stimulation. Left and right hemispheric data
were collapsed. Blue, red, and green lines indicate waveforms for Go, No-go, and Control, respectively. Thick and thin gray zones indicate periods analyzed for the mean
amplitudes, involving the preparatory period and the rebound, respectively. Red arrows demonstrate the peak in the rebound for No-go.
Table 2
Peak latency of suppression and rebound in theta, alpha, and beta bands for the second digit stimulation.
(ms) LF LC LP RF RC RP
Theta
No-go Rebound 789 (33) 825 (32) 758 (44) 797 (33) 774 (39) 758 (37)
Alpha
No-go Rebound 733 (77) 727 (64) 712 (61) 766 (74) 754 (60) 805 (67)
Go Suppression 556 (60) 498 (39) 595 (73) 424 (79)
Beta
No-go Rebound 654 (61) 743 (58) 715 (51) 623 (50) 713 (55) 666 (54)
No-go Suppression 230 (22) 195 (25)
Go Suppression 330 (38) 255 (45)
LF = left frontal, LC = left central, LP = left parietal, RF = right frontal, RC = right central, RP = right parietal. Values in parentheses are the standard error (SE).
276 H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 5/10
3.4. Beta band
Fig. 4A displays the grand-averaged waveforms of beta bands
in each condition for the second digit stimulation. The rebound
in No-go was recorded in all regions, peaking at around
700 ms, and a similar rebound was recorded in the fifth digit
stimulation (Fig. 4B). The suppressions for the second and fifth
digits were recorded in Go and No-go trials at LC and RC,
Table 3
Mean amplitude of theta, alpha, and beta bands in three conditions for the second digit stimulation.
(fT/cm) LF LC LP RF RC RP
Theta
Go À0.5 (1.7) 0.6 (2.3) 0.7 (2.1) À0.6 (1.8) À3.1 (2.3) À0.1 (2.7)
No-go 5.1 (2.3) 10.6 (3.4) 11.3 (4.7) 2.2 (1.5) 8.0 (2.9) 10.3 (3.7)
Control À1.0 (1.5) 1.4 (1.8) 1.2 (1.7) À0.8 (1.7) 1.0 (2.1) 1.9 (3.0)
Alpha
Go 2.2 (2.1) 0.3 (3.9) À3.0 (4.4) À0.9 (2.4) À7.6 (5.1) À2.9 (7.1)
No-go 8.9 (3.2) 17.0 (7.1) 19.4 (9.6) 4.5 (2.5) 11.5 (6.1) 11.7 (7.0)
Control 2.0 (1.6) 4.4 (3.4) 9.5 (6.3) 0.5 (1.3) 2.7 (3.9) 6.6 (5.5)
Beta
Go 5.1 (1.8) 0.0 (1.6) À0.3 (1.1) 2.2 (0.9) À0.5 (2.0) 0.2 (1.7)
No-go 8.4 (2.4) 11.6 (3.3) 7.6 (3.4) 5.6 (1.4) 11.1 (2.1) 8.6 (1.8)
Control 4.6 (1.5) 7.8 (2.3) 4.1 (1.6) 3.1 (1.3) 9.5 (2.9) 7.5 (2.2)
Values in parentheses are the standard error (SE).
Fig. 3. (A) (B) Grand-averaged waveforms of alpha bands in the frontal, central, andparietal regions for the second andfifth digit stimulation. Left and right hemispheric data
were collapsed. Blue, red, and green lines indicate waveforms for Go, No-go, and Control, respectively. Thick and thin gray zones indicate periods analyzed for the mean
amplitudes, involving the preparatory period and the rebound, respectively. Red arrows directed downward show the peak of the rebound. Red and blue arrows directed
upward indicate the peak of the suppression.
H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282 277
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 6/10
peaking at around 200 ms (Table 2 and Supplementary Table S1),
and ANOVAs with Condition (Go vs. No-go), Digit, and Hemi-
sphere as factors demonstrated no significant main effect or
interaction.
ANOVAs for the mean amplitude of beta bands revealed main
effects of Condition (F(2,22) = 14.476, p < 0.001) and Digit
(F(1,11) = 6.826, p < 0.05), and Condition–Digit interaction
(F(2,22) = 4.160, p < 0.05), Condition–Region interaction (Green-house–Geisser correction: F(2.334, 25.669) = 8.389, e = 0.583,
p < 0.001), Hemisphere–Region interaction (F(2,22) = 8.647,
p < 0.01), and Digit–Hemisphere–Region interaction (F(2,22) =
5.654, p < 0.05) (Table 3 and Supplementary Table S2). Further-
more, one-way ANOVAs showed significant main effects of Condi-
tion in the frontal region (F(2,22) = 8.002, p < 0.01), in the temporal
region (F(2,22) = 17.859, p < 0.001), and in the parietal region
(F(2,22) = 7.606, p < 0.01), and significant main effects of Digit in
No-go trials (F(1,11) = 9.076, p < 0.05) and Control (F(1,11) =
8.112, p < 0.05).
Post hoc testing showed that the mean amplitude was signifi-
cantly more positive in No-go than Go and Control in the frontal re-
gion ( p < 0.05, and p < 0.01, respectively), more positive in No-go
than Go in the central region ( p < 0.001), more positive in No-gothan Go in the parietal region ( p < 0.01).
3.5. Preparatory periods
The characteristics of the preparatory period differed among
bands: that is, the amplitudes of the theta and alpha bands did
not change in any regions, but the amplitude of the beta bands
showed a gradual decrease over time before the onset of S2 (Fig. 4).
ANOVAs for the amplitude of the theta bands revealed no signif-
icant main effect or interaction.ANOVAs for the amplitude of the alpha bands showed a signif-
icant main effect of Hemisphere (F(1,11) = 5.733, p < 0.05), and Di-
git–Hemisphere interaction (F(1, 11) = 10.876, p < 0.01). ANOVAs
for the amplitude of the beta bands revealed a significant Condi-
tion–Digit–Region interaction (F(1.916,21.076) = 4.094, e = 0.479,
p < 0.05). Post-hoc testing collapsing the effect of Hemisphere
demonstrated that the amplitudes for the second digit were signif-
icantly more negative in Go than Control in the central region
( p < 0.05), but there were no significant differences in the ampli-
tudes for the fifth digit.
3.6. The event-related magnetic field
Fig. 5 shows the event-related magnetic field waveforms in arepresentative subject to compare the difference in waveforms
Fig. 4. (A) (B) Grand-averaged waveforms of beta bands in the frontal, central, and parietal regions for the second and fifth digit stimulation. Left and right hemispheric data
were collapsed. Blue, red, and green lines indicate waveforms for Go, No-go, and Control, respectively. Thick and thin gray zones indicate periods analyzed for the mean
amplitudes, involving the preparatory period and the rebound, respectively. Red arrows directed downward demonstrate the peak of the rebound. Red and blue arrows
directed upward show the peak of the suppression.
278 H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 7/10
from band-related activity. The specific neural activity related to
No-go processing was recorded after the onset of S2 in both
hemispheres. A detailed analysis using an equivalent current
dipole model was performed in our previous study (Nakata et al.,
2005).
4. Discussion
In the present study, we investigated the characteristics of cor-
tical rhythmic activity in No-go processing, by using whole-headMEG. Our data demonstrated a rebound in amplitude in No-go
trials for theta, alpha, and beta bands, peaking at 600–900 ms. Sup-
pression was recorded in both Go and No-go trials for alpha bands,
peaking at 300–600 ms, and in both Go and No-go trials for beta
bands, peaking at 200–300 ms.
TSE with MEG has been used to clarify the characteristics of cor-
tical oscillations, especially for voluntary movement-related corti-
cal activity (Salmelin and Hari, 1994; Salmelin et al., 1995;
Nagamine et al., 1996; Salenius et al., 1997; Simoes et al., 2004;
Tamura et al., 2005). To our knowledge, however, this is the first
MEG study to examine the response inhibitory processing in a
Go/No-go paradigm, though the suppression (ERD) and rebound
Fig. 5. (Top)The event-related magnetic field waveforms over 204 planarcoils from the topof the head in a representative subject. (Bottom) An enlarged waveformrecorded
from four regions. Blue, red, and green lines indicate waveforms for Go, No-go, and Control, respectively. The arrows show the peak of the specific activity related to No-go
processing after the onset of S2. All data were digitally filtered (0.1–40 Hz bandpass) for display purposes.
H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282 279
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 8/10
(ERS) phenomena have been found not only with EEG but also with
MEG.
4.1. Behavioral performance
The mean RT was significantly faster in Condition 1 than Condi-
tion 2, and the commission error rate was significantly larger in
Condition 2 than Condition 1. These results indicate that the stim-
ulus site in somatosensory Go/No-go paradigms is related to the
difficulty of each task. Indeed, it seems difficult to interpret these
results, because our previous findings did not reveal a significant
difference (Nakata et al., 2005), but other data showed that the re-
sponses were faster for the second digit than fifth digit in the same
Go/No-go paradigms (Nakata et al., 2006a). We hypothesized that
the RT tended to be faster for the second digit than fifth digit.
The second and fifth digits are anatomically dominated by the
median nerve and ulnar nerve, respectively (Kimura, 2001), but
conduction time from the digit to primary somatosensory cortex
(SI) is almost the same (Huttunen et al., 2006). One possibility is
that the information processing in the SI and activation of the pri-
mary motor cortex (MI) necessary to cause sequential reaction are
more important following stimulation of the second digit than fifth
digit, since the somatosensory evoked magnetic fields ascending
through the second digit would be greater (Hari et al., 1993).
4.2. The rebound in Go/No-go paradigms
The strong rebound in amplitude of theta bands was recorded
only in No-go trials for the second digit stimulation (Fig. 2A), and
a similar weak rebound was also found in the waveforms for the
fifth digit stimulation (Fig. 2B). The latency peaked at around
800 ms. A rebound in amplitude of the alpha and beta bands was
also observed in No-go trials, peaking at around 700–800 ms (Figs.
3 and 4). The suppression/rebound (ERD/ERS) are generally
thought to reflect activation-based changes in functionally-related
groups of cortical neurons (see a review, Pfurtscheller and Lopes da
Silva, 1999), and considerable evidence for changes of amplitude inalpha and beta bands has been accumulated. The rebound ob-
served after movement has been often interpreted as an indicator
of idling in the cortex (Pfurtscheller et al., 1996), aswell as the con-
sequence of processes related to the end of the movement (Alegre
et al., 2002). Within this framework, our current results indicate
the specific neural activity related to No-go processing. A No-go-
specific enhancement of power has been reported in previous
EEG studies using auditory and visual Go/No-go paradigms (Shiba-
ta et al., 1997, 1998, 1999; Leocani et al., 2001; Kamarajan et al.,
2004; Kirmizi-Alsan et al., 2006; Barry, 2009; Harmony et al.,
2009). Consequently, the rebound in amplitude for No-go trials
would be common to the visual, auditory, and somatosensory
modalities.
It was of particular interest that the rebound in No-go trials wasfound in the bilateral frontal, central, and parietal regions. Human
neuroimaging has revealed that the neural networks for inhibitory
processing include the dorsolateral (DLPFC) and ventrolateral
(VLPFC) prefrontal cortices, supplementary motor area (SMA),
anterior cingulate cortex (ACC), and temporal and parietal lobes
(Kawashima et al., 1996; Konishi et al., 1999; Garavan et al.,
1999; Chikazoe et al., 2007; Nakata et al., 2008a,b). The present
study did not clarify which regions were responsible for the re-
bound in the No-go trials, suggesting that this rebound arises from
widespread generators.
As for the timing of occurrence in response inhibition, transcra-
nial magnetic stimulation (TMS) also has been used to investigate
both excitatory and inhibitory effects on the cerebral cortex during
the performance of Go/No-go paradigms (Hoshiyama et al., 1996,1997; Leocani et al., 2000; Waldvogel et al., 2000; Sohn et al.,
2002; Yamanaka et al., 2002; Nakata et al., 2006b). Common find-
ings of these studies were a decrease in the amplitude of motor
evoked potentials (MEPs) at 100–200 ms after No-go stimuli, and
an increase after Go stimuli. In addition, Waldvogel et al. reported
that inhibitionof the amplitude of MEPs lasted for 500 ms after No-
go stimuli. There has been no study showing how long the No-go
processing of the corticospinal tract lasted, but our TSE findings
may indicate the duration of neural activity in response inhibitory
processing.
4.3. The suppression in Go/No-go paradigms
The suppression in amplitude of alpha bands for the second di-
git stimulation was recorded in Gotrials at LC, LP, RC, and RP, peak-
ing at 400–600 ms (Fig. 3A). Nagamine et al. (1996) using TSE with
MEG provided evidence that alpha activity showed maximum sup-
pression about 300 ms after the onset of electromyography (EMG)
in both hemispheres. In the present study, the mean RT was about
250 ms in Condition 1 and 270 ms in Condition 2 (Table 1), sug-
gesting that the onset of EMG occurred approximately 220–
240 ms after the onset of S2. Subsequently, by adding 300 ms to
the onset of EMG, the peak in suppression of alpha bands in our
findings becomes consistent with the results of Nagamine et al.
Therefore, the suppression of alpha activity may be related directly
to motor response execution (Go) processing. However, since the
suppression for the fifth digit stimulation was found in both Go
and No-go trials at LP and RP (Fig. 3B), motor processing and other
neural mechanisms would be related to the suppression of alpha
activity.
The suppression of beta activity was found in both Go and No-
go trials at LC and RC for the second and fifth digit stimulation,
peaking at around 200 ms (Fig. 4). These findings suggested that
the suppression was associated with stimulus discrimination and
decision-making processing, rather than response execution and
inhibition processing. In our past studies using functional magnetic
resonance imaging (fMRI) during somatosensory Go/No-go para-
digms, areas of the brain related to Go trials were located in theDLPFC, VLPFC, SMA and premotor area (PM), primary somato-mo-
tor area (SMI), inferior parietal lobule (IPL), insula, superior tempo-
ral gyrus (STG), temporoparietal junction (TPJ), posterior parietal
cortex (PPC), and ACC (Nakata et al., 2008b). Brain activities related
to the No-go trials were located in the DLPFC, VLPFC, pre-SMA/
middle frontal gyrus (MFG), primary somatosensory area (SI), IPL,
insula, TPJ, and ACC (Nakata et al., 2008a). We did not perform a
conjunction analysis for the regions activated during both Go and
No-go trials, but judging from each specific activity, DLPFC, VLPFC,
SMA, IPL, insula, TPJ, and ACC would be related to the overlapping
regions in Go and No-go trials, indicating the neural networks for
response selective and decision-making processing.
4.4. Cortical oscillations in the preparatory period
Our neuromagnetic data for cortical oscillations in the prepara-
tory period showed that the amplitudes of the theta and alpha
bands changed little, but the amplitude of the beta bands gradually
decreased. Alegre et al. (2004) utilizing auditory Go/No-go para-
digms reported no changes in amplitude for alpha bands between
S1 and S2 stimuli, which was in line with our finding. However,
they did not show suppression in beta bands during the prepara-
tory period. It seems difficult to interpret this finding, but in gen-
eral, the beta pattern consists of a suppressive phase that begins
at least 1.5 s before the movement starts (Stancak and Pfurtschel-
ler, 1995, 1996), and the suppression has long been known to re-
flect movement preparation.
The amplitudes in preparatory periods were relatively similarbetween Go and No-go trials. In our S1–S2 paradigms, S1 delivered
280 H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 9/10
the warning and set up the response and S2 indicated the Go/No-
go information (i.e. S2-centered-paradigm). By contrast, some
studies have used a S1–S2 paradigm in which S1 delivered Go/
No-go information and S2 merely showed the timing of the re-
sponse after the Go-S1 stimulus (i.e. S1-centered-paradigm), show-
ing the difference between Go and No-go activity during
preparatory periods (Filipovic et al., 2001; Alegre et al., 2004). Tak-
ing our paradigms into consideration, our results are logical since
participants should focus on both Go and No-go stimuli for S2.
In the control condition, there were slow modulations of the
oscillatory activity in the alpha band before the onset of S2, indi-
cating that subjects might have paid some attention to the stimuli
although they were instructed to relax. In a CNV paradigm without
a motor task in response to an imperative stimulus (S2), well-pro-
nounced negativity was recorded prior to S2 (Ruchkin et al., 1986;
van Boxtel and Brunia, 1994). CNV has been associated with both
motor preparation and cognitive processing including expectancy,
motivation, attention, and arousal (Brunia, 1988; van Boxtel and
Brunia, 1994; Ikeda et al., 1996). Therefore, we inferred that the
slow modulation in alpha activity reflected expectancy and atten-
tion to the S2.
In conclusion, here we found that a rebound in amplitude was
recorded in No-go trials for theta, alpha, and beta bands, peaking
at 600–900 ms. The suppression in amplitude was recorded in both
Go and No-go trials for alpha and beta bands, peaking at 200–
600 ms. These results in normal healthy subjects suggest that cor-
tical rhythmic activity clearly has several dissociated components
relating to different motor functions, including response inhibition,
execution, and decision-making. Furthermore, our findings might
guide future studies of the neurophysiological changes in patients,
and help to interpret the error profiles seen in patients during No-
go trials. Indeed, several studies have shown differences in wave-
forms of ERPs and oscillation during No-go trials between normal
subjects and patients (Weisbrod et al., 2000; Wiersema et al.,
2006; Doege et al., 2010).
The present study revealed the neuromagnetic activity of corti-
cal rhythm in No-go processing.
Acknowledgements
We are very grateful to Mr. O. Nagata and Mr. Y. Takeshima for
technical help during this study.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.clinph.2012.
06.019.
References
Alegre M, Labarga A, Gurtubay IG, Iriarte J, Malanda A, Artieda J. Beta EEG changes
during passive movements: sensory afferences contribute to the beta event-
related desynchronization in humans. Neurosci Lett 2002;331:29–32.
Alegre M, Gurtubay IG, Labarga A, Iriarte J, Valencia M, Artieda J. Frontal and central
oscillatory changes related to different aspects of the motor process: a study in
Go/No-go paradigms. Exp Brain Res 2004;159:14–22.
Barry RJ. Evoked activity and EEG phase resetting in the genesis of auditory Go/
Nogo ERPs. Biol Psychol 2009;80:292–9.
Braver TS, Barch DM, Gray JR, Molfese DL, Snyder A. Anterior cingulate cortex and
response conflict: effects of frequency, inhibition and errors. Cereb Cortex
2001;11:825–36.
Brunia CHM. Movement and stimulus preceding negativity. Biol Psychol
1988;26:165–78.
Chikazoe J, Konishi S, Asari T, Jimura K, Miyashita Y. Activation of right inferior
frontal gyrus during response inhibition across response modalities. J Cogn
Neurosci 2007;19:69–80.
Doege K, Kumar M, Bates AT, DasD, Boks MP, LiddlePF. Time andfrequency domain
event-related electrical activity associated with response control inschizophrenia. Clin Neurophysiol 2010;121:1760–71.
Falkenstein M, Koshlykova NA, Kiroi VN, Hoormann J, Hohnsbein J. Late ERP
components in visual and auditory Go/Nogo tasks. Electroencephalogr Clin
Neurophysiol 1995;96:36–43.
Falkenstein M, Hoormann J, Hohnsbein J. ERP components in Go/Nogo tasks and
their relation to inhibition. Acta Psychol 1999;101:267–91.
Farmer SF. Phythmicity, synchronization and binding in human and primate motor
systems. J Physiol 1998;509:3–14.
Filipovic SR, Jahanshahi M, Rothwell JC. Uncoupling of contingent negative variation
and alpha band event-related desynchronization in a Go/No-go task. Clin
Neurophysiol 2001;112:1307–15.
Garavan H, Ross TJ, Stein EA. Right hemispheric dominance of inhibitory control: anevent-related functional MRI study. Proc Natl Acad Sci USA 1999;96:8301–6.
Gemba H, SasakiK. Potential related to No-goreactionin Go/No-go hand movement
with discrimination between tone stimuli of different frequencies in the
monkey. Brain Res 1990;537:340–4.
Hämäläinen M, Hari R, Ilmoniemi RJ, Knuutila J, Lounasmaa OV.
Magnetoencephalography-theory, instrumentation, and applications to
noninvasive studies of the working human brain. Rev Mod Phys
1993;65:413–97.
Hari R, Salmelin R, Mäkelä JP, Salenius S, Helle M. Magnetoencephalographic
cortical rhythms. Int J Psychophysiol 1997;26:51–62.
Hari R, Karhu J, Hämäläinen M, Knuutila J, Salonen O, Sama M, et al. Functional
organization of the human first and second somatosensory cortices: a
neuromagnetic study. Eur J Neurosci 1993;5:724–34.
Harmony T, Alba A, Marroquín JL, González-Frankenberger B. Time–frequency-
topographic analysis of induced power and synchrony of EEG signals during a
Go/No-go task. Int J Psychophysiol 2009;71:9–16.
Hoshiyama M, Koyama S, Kitamura Y, Shimojo M, Watanabe S, Kakigi R. Effects of
judgement process on motor evoked potentials in Go/No-go hand movement
task. Neurosci Res 1996;24:427–30.
Hoshiyama M, Kakigi R, Koyama S, Takeshima Y, Watanabe S, Shimojo M. Temporal
changes of pyramidal tract activities after decision of movement: a study using
transcranial magnetic stimulation of the motor cortex in humans.
Electroencephalogr Clin Neurophysiol 1997;105:255–61.
Huttunen J, Komssi S, Lauronen L. Spatial dynamics of population activities at S1
after median and ulnar nerve stimulation revisited: an MEG study. NeuroImage
2006;32:1024–31.
Ikeda A, Lüders HO, Collura TF, Burgess RC, Morris HH, Hamano T, et al. Subdural
potentials at orbitofrontal and mesial prefrontal areas accompanying
anticipation and decision making in humans: a comparison with Bereitschafts
potential. Electroencephalogr Clin Neurophysiol 1996;98:206–12.
Jurkiewicz MT, Gaetz WC, Bostan AC, Cheyne D. Post-movement beta rebound is
generated in motor cortex: evidence from neuromagnetic recordings.
NeuroImage 2006;32:1281–9.
Kakigi R, Hoshiyama M, Shimojo M, Naka D, Yamasaki H, Watanabe S, et al.
The somatosensory evoked magnetic fields. Progr Neurobiol 2000;61:495–
523.
KamarajanC, Porjesz B, Jones KA, Choi K, ChorlianDB, Padmanabhapillai A, et al.Therole of brain oscillations as functional correlates of cognitive systems: a study of
frontal inhibitory control in alcoholism. Int J Psychophysiol 2004;51:155–80.
Kaneoke Y. Magnetoencephalography: in search of neural processes for visual
motion information. Progr Neurobiol 2006;80:219–40.
Kawashima R, Satoh K, Itoh H, Ono S, Furumoto S, Gotoh R, et al. Functional
anatomy of Go/No-go discrimination and response selection–a PET study in
man. Brain Res 1996;728:79–89.
Kiefer M, Marzinzik F, Wetsbrod M, Scherg M, Spitzer M. The time course of brain
activations during response inhibition: evidence from event-related potentials
in a go/no go task. NeuroReport 1998;9:765–70.
Kimura H. Assessment of individual nerves. In: kimura J, editor. Electrodiagnosis in
diseases of nerve and muscle: principles and practice. 3rd
ed. Philadelphia: Davis Company; 2001. p. 130–77.
Kirmizi-Alsan E, Bayraktaroglu Z, Gurvit H, Keskin YH, Emre M, Demiralp T.
Comparative analysis of event-related potentials during Go/Nogo and CPT:
decomposition of electrophysiological markers of response inhibition and
sustained attention. Brain Res 2006;1104:114–28.
Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y. Common
inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 1999;122:981–91.
Leocani L, Cohen LG, Wassermann EM, Ikoma K, Hallett M. Human corticospinal
excitability evaluated with transcranial magnetic stimulation during different
reaction time paradigms. Brain 2000;123:1161–73.
Leocani L, Toro C, Zhuang P, Gerloff C, Hallett M. Eventrelated desynchronization in
reaction time paradigms: a comparison with event-related potentials and
corticospinal excitability. Clin Neurophysiol 2001;112:923–30.
Nakata H, Inui K, Wasaka T, Akatsuka K, Kakigi R. Somato-motor inhibitory
processing in humans: a study with MEG and ERP. Eur J Neurosci
2005;22:1784–92.
Nakata H, Inui K, Wasaka T, Tamura Y, Kida T, Kakigi R. The characteristics of the
nogo-N140 component in somatosensory Go/Nogo tasks. Neurosci Lett
2006a;397:318–22.
Nakata H, Inui K, Wasaka T, Tamura Y, Akatsuka K, Kida T, et al. Higher anticipated
force required a stronger inhibitory process in Go/Nogotasks. Clin Neurophysiol
2006b;117:1669–76.
Nakata H, Sakamoto K, Ferretti A, Perrucci GM, Del Gratta C, Kakigi R, et al. Somato-
motor inhibitory processing in humans: an event-related functional MRI study.NeuroImage 2008a;39:1858–66.
H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282 281
7/28/2019 Nakata Et Al, 2013
http://slidepdf.com/reader/full/nakata-et-al-2013 10/10
Nakata H, Sakamoto K, Ferretti A, Perrucci GM, Del Gratta C, Kakigi R, et al.
Executive functions with different motor outputs in somatosensory Go/Nogo
tasks: an event-related functional MRI study. BrainRes Bull 2008b;77:197–205.
Nagamine T, Kajola M, Salmelin R, Shibasaki H, Hari R. Movement-related slow
cortical magnetic fields and changes of spontaneous MEG- and EEG-brain
rhythms. Electroencephalogr Clin Neurophysiol 1996;99:274–86.
Pfurtscheller G, Stancak A, Neuper C. Post-movement beta synchronization. A
correlate of an idling motor area? Electroencephalogr Clin Neurophysiol
1996;98:281–93.
Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and
desynchronization: basic principles. Clin Neurophysiol 1999;110:1842–57.Ruchkin DS, Sutton S, Mahaffev D, Glaser J. Terminal CNV in the absence of motor
response. Electroencephalogr Clin Neurophysiol 1986;63:445–63.
Salenius S, Schnitzler A, Salmelin R, Jousmäki V, Hari R. Modulation of human
cortical rolandic rhythms during natural sensorimotor tasks. NeuroImage
1997;5:221–8.
Salmelin R, Hari R. Spatiotemporal characteristics of sensorimotor neuromagnetic
rhythms related to thumb movement. Neuroscience 1994;60:537–50.
Salmelin R, Haämaälaäinen M, Kajola M, Hari R. Functional segregation of
movement-related rhythmic activity in the human brain. NeuroImage
1995;2:237–43.
Stancak A, Pfurtscheller G. Desynchronization and recovery of beta rhythms during
brisk and slow self-paced finger movements in man. Neurosci Lett
1995;196:21–4.
Stancak A, Pfurtscheller G. Event-related desynchronisation of central beta-rhythms
during brisk and slow selfpaced finger movements of dominant and
nondominant hand. Brain Res Cogn Brain Res 1996;4:171–83.
Shibata T, Shimoyama I, Ito T, Abla D, Iwasa H, Koseki K, et al. The time course of
interhemispheric EEG coherence during a Go:Nogo task in humans. Neurosci
Lett 1997;233:117–20.
Shibata T, Shimoyama I, Ito T, Abla D, Iwasa H, Koseki K, et al. The synchronization
between brain areas under motor inhibition process in humans estimated by
event-related EEG coherence. Neurosci Res 1998;31:265–71.
Shibata T, Shimoyama I, Ito T, Abla D, Iwasa H, Koseki K, et al. Event-related
dynamics of the gamma-band oscillation in the human brain: information
processing during a Go:Nogo hand movement task. Neurosci Res
1999;33:215–22.
Simoes C, Salenius S, Curio G. Short-term (approximately 600 ms) prediction of
perturbation dynamics for 10- and 20-Hz MEG rhythms in human primary
sensorimotor hand cortices. NeuroImage 2004;22:387–93.
Sohn YH, Wiltz K, Hallett M. Effect of volitional inhibition on cortical inhibitorymechanisms. J Neurophysiol 2002;88:333–8.
Tamura Y, Hoshiyama M, Nakata H, Hiroe N, Inui K, Kaneoke Y, et al. Functional
relationship between human rolandic oscillations and motor cortical
excitability: an MEG study. Eur J Neurosci 2005;21:2555–62.
van Boxtel GJ, Brunia CH. Motor and non-motor aspects of slow brain potentials.
Biol Psychol 1994;38:37–51.
Waldvogel D, van Gelderen P, Muellbacher W, Ziemann U, Immisch I, Hallett M. The
relative metabolic demand of inhibition and excitation. Nature
2000;406:995–8.
Weisbrod M, Kiefer M, Marzinzik F, Spitzer M. Executive control is disturbed in
schizophrenia: evidence from event-related potentials in a Go/Nogo task. Biol
Psychiatry 2000;47:51–60.
Wiersema R, van der Meere J, Roeyers H, Van Coster R, Baeyens D. Event rate and
event-related potentials in ADHD. J Child Psychol Psychiatry 2006;47:560–7.
Yamanaka K, Kimura T, Miyazaki M, Kawashima N, Nozaki D, Nakazawa K, et al.
Human cortical activities during Go/Nogo tasks with opposite motor control
paradigms. Exp Brain Res 2002;142:301–7.
282 H. Nakata et al. / Clinical Neurophysiology 124 (2013) 273–282
Recommended