Cortical rhythm of No-go processing in humans: An MEG study
Highlights
► We investigated the characteristics of cortical rhythmic activity in No-go processing during a somatosensory 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.
Introduction
The cortical rhythmic activity relating to response inhibitory processing has been clarified by using scalp electroencephalography (EEG). EEG has been frequently used to examine the dynamics of synchronized cortical activity, and offers a high temporal resolution 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, Shibata et al., 1998, Shibata et al., 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 and 18–22 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 conditions. 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. suppression), and the latter, event-related synchronization (ERS) (i.e. rebound) (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 suggested to reflect an idling cortex generated by a large area of highly synchronous neuronal firing in the absence of inputs, or alternatively, changes in coherent activity resulting from synchronous inputs 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 frequency components (theta, alpha, and beta), by using magnetoencephalography (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 activity to be differentiated 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 response inhibitory processing. In the present study, we used Temporal Spectral Evolution (TSE) to extract the spatiotemporal characteristics of cortical oscillations, following previous MEG studies (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, subsequently, 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 the same unit as the original signals.
The present study used ‘somatosensory Go/No-go paradigms’, in which the second or fifth digit of the left hand was stimulated. Some event-related potential (ERP) studies found that the amplitude of the N2 component was much smaller following auditory than visual stimuli (Falkenstein et al., 1995, Falkenstein et al., 1999, Kiefer et al., 1998). Falkenstein et al. (1999) suggested that the inhibitory processing as reflected 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 opposed to the caudal part of the same bank after a visual stimulus. Therefore, the present study aimed to investigate 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 effect of stimulus probability and to minimize differences in response conflict between event types (Braver et al., 2001, Nakata et al., 2005).
Section snippets
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 Institute for Physiological Sciences.
Experimental paradigm
The participants performed a warning stimulus (S1) – imperative stimulus (S2) task with Go/No-go paradigms. S1 was an auditory pure tone (60 dB SPL,
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
Discussion
In the present study, we investigated the characteristics of cortical rhythmic activity in No-go processing, by using whole-head MEG. Our data demonstrated a rebound in amplitude in No-go trials for theta, alpha, and beta bands, peaking at 600–900 ms. Suppression 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 cortical oscillations,
Acknowledgements
We are very grateful to Mr. O. Nagata and Mr. Y. Takeshima for technical help during this study.
References (57)
- et al.
Beta EEG changes during passive movements: sensory afferences contribute to the beta event-related desynchronization in humans
Neurosci Lett
(2002) Evoked activity and EEG phase resetting in the genesis of auditory Go/Nogo ERPs
Biol Psychol
(2009)Movement and stimulus preceding negativity
Biol Psychol
(1988)- et al.
Time and frequency domain event-related electrical activity associated with response control in schizophrenia
Clin Neurophysiol
(2010) - et al.
Late ERP components in visual and auditory Go/Nogo tasks
Electroencephalogr Clin Neurophysiol
(1995) - et al.
ERP components in Go/Nogo tasks and their relation to inhibition
Acta Psychol
(1999) - et al.
Uncoupling of contingent negative variation and alpha band event-related desynchronization in a Go/No-go task
Clin Neurophysiol
(2001) - et al.
Potential related to No-go reaction in Go/No-go hand movement with discrimination between tone stimuli of different frequencies in the monkey
Brain Res
(1990) - et al.
Magnetoencephalographic cortical rhythms
Int J Psychophysiol
(1997) - et al.
Time–frequency-topographic analysis of induced power and synchrony of EEG signals during a Go/No-go task
Int J Psychophysiol
(2009)