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, Japan b Department of Clinical Laboratory, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan c 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 magn etoencep halography (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 somatose nsory Go/No-g o paradigm s, by using magn etoenceph alograph y (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 rebo und in amp litud e was reco rded in the No-g o trials for the ta, alp ha, an d beta acti vity , peak - ing at 600–900 ms. A suppression of amplitud e was recorded in Go and No-go trials for alpha activity, peakin g at 300–600 ms, and in Go and No-go trials for beta activity , peaking at 200–300 ms. Conclusion: The corti cal rhy thmic acti vity clea rly has seve ral disso ciat ed compon ents rela ting to diff eren t motor functions, including response inhibition, execution, and decision-making. Significance: The presen t stud y reve aled the cha racteristi cs of corti cal rhy thmic acti vity 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 respon se inhibito ry processing has been clarified by using scalp electroencephalogra- phy (EEG). EEG has been frequently used to examine the dynamics of synchronized cortical acti vit y, and offe rs a hig h temporal reso lu- tion in the order of milliseconds. Several studies of EEG spectral power have examined the characteristics of cortical oscillation s 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 ban ds decrea ses or incr ease s at 300–900ms after the onset of a No -go stim ulu s. For exam ple, Le oc ani et al. (2 00 1) reported th at the spe ctr al po we r at 10 Hz and 18–22 Hz de cre ase d at 30 0– 60 0 ms after stimulus onset, and th e powe r at 10 Hz and 18– 22 Hz incr ease d at 900 –1200 ms and 600 –90 0 ms, resp ecti vely . Harmony et al. (2009) sho wed a complex spat iote mp ora l pat tern ofspectral 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 re flec t an idlin g co rte x ge nerat ed by a lar ge 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 Mika jima , Toko roza wa, Saita ma 359 -119 2, Japan . Tel. : +81 4 2947 461 4; fax: +81 4 2947 6826. E-mail address: [email protected](H. Nakata). Clinical Neurophysiology 124 (2013) 273–282 Contents lists available at SciVerse ScienceDirect Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
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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-
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.
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
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
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
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
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