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. 2008 Jul 25;30(5):1568–1579. doi: 10.1002/hbm.20624

Movement gating of beta/gamma oscillations involved in the N30 somatosensory evoked potential

Ana Maria Cebolla 1, Caty De Saedeleer 1, Ana Bengoetxea 1, Françoise Leurs 1, Costantino Balestra 2, Pablo d'Alcantara 1, Ernesto Palmero‐Soler 1, Bernard Dan 3, Guy Cheron 1,4,✉
PMCID: PMC6870656  PMID: 18661507

Abstract

Evoked potential modulation allows the study of dynamic brain processing. The mechanism of movement gating of the frontal N30 component of somatosensory evoked potentials (SEP) produced by the stimulation of the median nerve at wrist remains to be elucidated. At rest, a power enhancement and a significant phase‐locking of the electroencephalographic (EEG) oscillation in the beta/gamma range (25–35 Hz) are related to the emergence of the N30. The latter was also perfectly identified in presence of pure phase‐locking situation. Here, we investigated the contribution of these rhythmic activities to the specific gating of the N30 component during movement. We demonstrated that concomitant execution of finger movement of the stimulated hand impinges such temporal concentration of the ongoing beta/gamma EEG oscillations and abolishes the N30 component throughout their large topographical extent on the scalp. This also proves that the phase‐locking phenomenon is one of the main actors for the N30 generation. These findings could be explained by the involvement of neuronal populations of the sensorimotor cortex and other related areas, which are unable to respond to the phasic sensory activation and to phase‐lock their firing discharges to the external sensory input during the movement. This new insight into the contribution of phase‐locked oscillation in the emergence of the N30 and in its gating behavior calls for a reappraisal of fundamental and clinical interpretation of the frontal N30 component. Hum Brain Mapp 2009. © 2008 Wiley‐Liss, Inc.

Keywords: evoked potential, somatosensorysystem, beta gamma oscillation, N30 component, phase locking

INTRODUCTION

Dynamic gating is a key aspect of neural processing allowing to select and enhance integration of stimuli and events that are most relevant to keep the focus on specific goals in the face of numerous environmental distractions [O'Reilly, 2006]. For example, it was recently demonstrated that sensory integration during reaching movement is a dynamic process driven by the task computational demands [Sober and Sabes, 2005]. It is generally accepted that gating mechanisms involve multiple parallel circuits including loops between the cortex, the basal ganglia, and the thalamus. Disinhibition and dopamine modulation play central roles in these neural networks [Durstewitz et al., 2000].

A possible way for noninvasive investigation of these processes in human resides in the analysis of the spectral content of neuronal oscillatory activity recorded in electroencephalographic (EEG) signals. This provides brain‐state measure reflecting thalamo‐cortical and cortico‐cortical functioning [Buzsáki and Draguhn, 2004; Steriade, 2001]. As subcortical nuclei such as the thalamus are involved in the active gating of different sensory influx [Steriade et al., 1997] and contribute to change in EEG rhythms, the electrical median nerve stimulation provides a convenient and easily quantified sensory input for the study of the gating process.

Recent technological advances allow concomitant analysis of spontaneous ongoing EEG activity and evoked potentials [Delorme and Makeig, 2004; Makeig et al., 2002; Saunseng et al., 2007]. Relevant measures include the quantification of power changes in different frequency bands of the EEG signals with respect to stimulation. Among them, event‐related spectral perturbation (ERSP) measure corresponds either to a narrow‐band of event‐related synchronization (power increase) or desynchronization (power decrease) of ongoing EEG activity. Another relevant measurement evaluates the level of phase‐locking in different frequency bands of the ongoing EEG with respect to stimulation. This phase‐locking factor [Tallon‐Baudry et al., 1996] is here quantified by an intertrial coherence (ITC) measure. ERSP and ITC thus reflect physiological modifications of neural activity induced by external stimulation. This approach has led to a more comprehensive understanding of the origin of evoked potentials [Makeig et al., 2002; Sauseng et al., 2007 for a review].

The frontal or precentral N30 component of somatosensory evoked potentials (SEP) is known to be highly sensitive to interference or gating from concomitant involvement of the brain in sensory, motor, and mental activities [Cheron and Borenstein, 1987, 1991, 1992; Rossini et al., 1999; Rushton et al., 1981]. The amplitude of the frontal N30 significantly decreases when the stimulated hand performs an actual movement or during movement imagery [Cheron and Borenstein, 1991, 1992; Cheron et al., 2000]. Conversely, the observation of the same motor act by the subject at rest increases N30 amplitude [Rossi et al., 2002]. This wave is specifically modulated by electrical stimulation of the internal part of the globus pallidus or the subthalamus nuclei of Parkinsonian patients [Pierantozzi et al., 1999], suggesting that it may represent a reliable physiological index of the dopaminergic motor pathways [Cheron et al., 1994; Cheron, 1999]. Investigation of the frontal N30 component has increasingly been used in a host of clinical conditions [Fukuda et al., 2003; Murase et al., 2000; Pierantozzi et al., 1999; Tinazzi et al., 2004].

Recently, we have demonstrated that the N30 SEP component was accompanied by an increase of the power spectrum of beta/gamma rhythm peaking at 30 Hz and by a concomitant increase of the intertrials coherence at this frequency band [Cheron et al., 2007]. Pure phase‐locking of the beta/gamma rhythm was found in a large percentage of the trials. We also demonstrated that a reorganization of the spontaneous phase of the ongoing beta rhythm contributed to the production of N30 component.

Here, we investigated the behavior of this pure phase‐locking during the gating produced by movement of the stimulated hand. A major hypothesis of the present study is that the decrement in N30 amplitude during movement gating was mainly due to an alteration in the beta/gamma phase‐locking mechanism.

METHODS

Subjects and Conditions

The data were collected from 14 normal volunteers (seven females and seven males, mean age: 26 ± 3.2 years). They were in good health and free from neurological disease. The procedures were approved by the local ethics committee of the University and conformed to the Declaration of Helsinki.

Somatosensory evoked potentials (SEP) were recorded at rest with the eyes closed and during a movement interference task. During this task the subjects were asked to flex and extend four fingers of the stimulated hand (not the thumb) together. Finger movements were unrelated to the stimulation.

SEP Stimulation and Recording Parameters

The stimuli were 0.2 ms square electrical pulses delivered through a pair of Ag–AgCl electrodes cup to the left median nerve at the wrist. The intensity was adjusted for eliciting visible small thumb twitches. Random stimuli intervals (0.5–2 s range) were used throughout the experiment. In the first group of seven subjects, the standard electrode positions corresponded to F3, F4, a contralateral, and an ipsilateral parietal site situated 70 mm from the midline and 30 mm behind C4–C3 [these loci correspond to the site where the N20 component was maximally recorded when the contralateral wrist was stimulated [Desmedt and Cheron, 1980]; all electrodes were referred to the contralateral earlobe. The on‐line SEP averaging was performed using a four‐channel NihonKohden averager (Neuropack, MEB‐9100). The overall band‐pass was 0.5 Hz–1.5 kHz and the analysis time was 100 ms with a sampling rate of 5 kHz. Scalp electrodes impedances were kept below 5 kΩ. Two series of 500 potentials were checked for reproducibility. After ocular artefact reduction, any remaining artefacts were rejected by visual inspection. As the averager used does not permit the spectral analysis of the single sweep data and to independently analyze the ongoing rhythmic EEG activity from the evoked response, the raw (unaveraged) EEG data were transferred in parallel to a Pentium III personal computer with analog‐to‐digital converter boards (Digidata Axoscope). This analysis was only performed on the F4 channel. Off‐line analysis and illustrations were then performed using the EEGLAB software [Delorme and Makeig, 2004].

To perform topographical analysis of SEP gating, SEPs were recorded using 128 channels EEG recorder (ANT system, The Netherlands) in a second group of seven subjects. This system uses full‐band DC amplifier including active‐noise cancellation process, worked at a sampling frequency of 2,048 Hz, and with a resolution of 22 bit (71.5 nV per bit). An active‐shield cap using 128 Ag–AgCl sintered ring electrodes and shielded coaxial cables (5–10 electrode system placement) was comfortably adjusted to subject head.

Event‐Related Spectral Perturbation

The EEGLAB software enables the analysis of the event‐related average dynamics changes in amplitude of the broad band EEG frequency spectrum and to decipher the ongoing EEG processes that may be partially time‐ and phase‐locked to experimental events [Delorme and Makeig, 2004]. The event‐related spectral perturbation measure (ERSP) may correspond to a narrow‐band of event‐related desynchronization (ERD) or synchronization (ERS). Briefly, for this calculation, EEGLAB computes the power spectrum over a sliding latency window on each epoch and normalizes each of them by its respective mean baseline spectra and then performs averaging across data trials. Each trial consists of samples from −400 ms before up to 400 ms after the stimulus. The size of the sliding window was of 512 data points. ERSP image provides a color code where each template pixel indicates the power (in dB) at a preset frequency f and latency t relative to the stimulation onset. Typically, for n trials, if Fk(f, t) is the spectral estimate of trial k at frequency f and time t,

equation image (1)

To compute Fk(f, t), EEGLAB uses the short‐time Fourier transform that provides a fixed time and frequency resolution.

Intertrial Coherence

Intertrial coherence (ITC) is a frequency‐domain measure of the partial or exact synchronization of activity at a particular latency and frequency to a set of experimental events to which EEG data trials are time‐locked. This measure corresponds to the “phase‐locking factor” [Tallon‐Baudry et al., 1996]. The term ITC refers here to its interpretation as the event‐related phase coherence (ITPC), which is defined by

equation image (2)

where |·| represents the complex norm. The ITC measure takes values between 0 and 1. A value of 0 represents absence of synchronization between EEG data and the time‐locking events; a value of 1 indicates their perfect synchronization.

The significance levels of the ITC and ERSP were fixed at 0.001 and assessed using surrogate data by randomly shuffling the single‐trial spectral estimates from different latency windows during the baseline period (EEGlab bootstrap method).

Selection of Trials With Pure Phase Resetting

The single sweep selection aims to conserve only the trials for which the EEG amplitude of the filtered signal (e.g. 25–35 Hz) measured around the N30 latency remained similar compared to the prestimulus amplitude. For this, we compared in each filtered single‐sweep the root‐mean‐square (RMS) amplitude of the pre‐ and post‐stimulus periods ([−200, 0 ms] and [0, +60 ms], respectively) according to the following equation:

equation image (3)

where Max Ampl, the maximal amplitude of the filtered single sweep signal, is measured for the period ([−200, 0 ms]). Then, we selected only the trials for which the following criterion was respected:

equation image (4)

where ΔRMSdata was compared to ΔRMSstim‐free for two periods free of stimulus ([−350, −150 ms] and [−150, −90 ms]). After that, it was verified that the selected ΔRMSdata distribution was included inside the ΔRMSstim‐free distribution. This means that no significant amplitude enhancement or decrement were present in these selected trials.

Phase Histogram Analysis

The degree of synchronization of the ongoing EEG oscillation was assessed by means of histograms of the instantaneous phase of the components across an ensemble of the selected trials [Jansen et al., 2003]. Phase histograms of the components found in the beta (25–35 Hz) band in the selected trials were generated every 5 ms, starting 60 ms before stimulus up to 150 ms after stimulus. The Kuiper statistic κ coefficient, expressed as a ln, was used to evaluate differences in empirical distribution functions [Press et al., 1992] and to quantify the degree with which the phase histograms resembled a uniform density function. κ is defined as

equation image (5)

with

equation image (6)

where F 0(xi) and SN(xi) are the mean pre‐stimulus reference period [−60, −5 ms] and the actually observed cumulative distribution function, respectively; N is the effective number of data points, L the number of bins in the histogram and xi the upper bound of bin i.

The more the observed SN(xi) is different from the reference F 0(xi), the more κ will be negative. Z‐score of κ was used to provide further evidence of reliability of the effect across subjects. As the Z scores are defined through individual subject mean and SD, it results in different statistical levels at rest and during movement gating.

Data were analyzed using a one‐way ANOVA test and Bonferroni's post‐hoc test after assessing their normality by a Kolmogorov–Smirnov test (Statistica 7.1, Statsoft). Differences were considered significant at P < 0.05. Results are expressed as means ± SD.

RESULTS

To highlight the extent of movement gating on the frontal N30 component, we performed topographical studies by mean of a 128 channels recording (ANT system) in seven subjects. Figure 1 illustrates topographical differences for each subject, at rest (Fig. 1A) and during movement gating (Fig. 1B). Response amplitude changes between both conditions were compared by means of MANOVA test (P ≤ 0.05) for the 128 channels in the seven subjects (Fig. 1C).

Figure 1.

Figure 1

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Topographical extent of the movement gating of the N30 component. Potential scalp distribution for seven subjects with 128 channels, at rest (A) and during gating (B) of the N30 component. (C) Response amplitude changes between both conditions calculated by MANOVA test (P ≤ 0.05) on the 128 channels for the seven subjects: red circles represent electrodes with significant values of change in amplitude. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

At rest, the negativity at 30 ms spreads mainly on the whole frontal and central areas with more extension toward ipsilateral parietal area, as classically described. A concomitant positivity was present on the contralateral parietal area. During movement gating, the frontal negativity is significantly decreased on the whole extent of the frontal and central areas (Fig. 1C).

ERSP and ITC Analysis in Grand Averaged Data

Figure 2 illustrates the movement gating in a grand average display representing the relationship between the frontal N30 component and the related ERSP and ITC at rest (Fig. 2A–C) (3,000 trials, n = 7 subjects, F4 channel, NihonKhoden system) and during the movement gating (Fig. 2D–F) (3,039 trials, n = 7 subjects). At rest, a significant phase‐locking in the beta/gamma band oscillation (mean frequency: 33.1 ± 1.3 Hz) peaking at a latency of 34.9 ± 5.2 ms and expressed by a maximal ITC value of 0.53 ± 0.17 is accompanied by an ERSP cluster (peaking at 35.2 ± 6.3 ms) with a maximal value of 2.4 ± 1.5 dB. Concerning alpha rhythm, cluster with smaller ITC maximal value (0.29 ± 0.10) at the latency of 54.8 ± 40.5 ms was not accompanied by significant ERSP cluster value. Faster rhythms than 30 Hz were not systematically present in all the subjects; there are not on the scope of the present study.

Figure 2.

Figure 2

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Grand average analysis of N30 component at rest and during movement gating. (A, D) Grand average of the frontal N30 component recorded from F4 during median nerve stimulation at the wrist at rest and during movement gating conditions, respectively. Little open triangle peaking at P14. (B, C, E, F) Grand average of time/frequency template from ERSP and ITC analysis, for both conditions. Note that the peak of ERSP and ITC value in the beta range (25–35 Hz) coincided with the N30 latency peak at rest. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

The conservation of the same amount of the afferent drive during the movement gating was demonstrated by the absence of significant modification of the amplitude of the subcortical P14 far‐field (1.1 ± 0.5 μV at rest vs. 0.84 ± 0.5 μV during movement, P = 0.34) and of the parietal N20 component reflecting the first cortical activation (1.8 ± 0.7 μV at rest vs. 1.7 ± 0.6 μV during movement). The main effect of the movement gating was a very strong reduction in N30 amplitude [4.8.± 1.8 μV at rest (Fig. 2A), vs. 0.7 ± 0.5 μV during the movement gating (Fig. 2D)], while the amplitude of the following N60 component remained unchanged. The gating of the N30 amplitude was accompanied by a significant reduction of the ITC cluster value at 30 Hz (0.53 ± 0.17 at rest vs. 0.26 ± 0.07 during movement P < 0.001) (Fig. 2F). In this condition, the diffuse alpha ITC cluster and the beta/gamma ITC cluster were also shifted toward longer latency (112.0 ± 35.3 ms and 56.2 ± 14.6 ms for alpha and beta/gamma and rhythms, respectively). The ERSP plot also showed the disappearance of beta ERSP cluster for all the poststimulus period analyzed (Fig. 2E). This disorganization of the beta/gamma oscillation phase‐locking by the movement gating is illustrated by the comparison of the superimposition of the filtered (25–35 Hz) EEG trials at rest (Fig. 3A) and during the gating movement (Fig. 3B). At rest, spontaneous beta oscillations were reorganized in relation to the stimulus. In this case, the negative part of single beta oscillation peaked at the latency of the N30 component. Conversely, during the movement gating such temporal reorganization was absent and beta waves were not phase‐locked to the median nerve stimulation.

Figure 3.

Figure 3

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Superimposition of single‐filtered (25–35 Hz) EEG trials with respect to median nerve stimulation at rest (A) and during movement gating (B). For each condition, 10 (upper traces group) and 100 (lower traces group) trials are superimposed. Note that at rest the phase rearrangement involves concentration of negative wave at the latency of the N30 component.

As identification of phase resetting of spontaneous EEG activities in certain frequency bands requires the demonstration of the presence of these EEG oscillations in the absence of stimulus, we measured the power spectrum of the spontaneous beta oscillation in each single trial excluding the periods of evoked activity both in rest and movement conditions. For all the recorded trials, the mean of the beta/gamma power spectrum represented a value of 17.1 ± 4.9 dB at rest and 17.2 ± 2.5 during movement gating. For comparison, the mean power spectrum of the dominant α‐mu rhythm (∼10 Hz) during the same period was 26.4 ± 5.3 dB at rest and 26.5 ± 3.3 during movement gating. This suggests that the beta/gamma oscillation (representing about 65% of the alpha rhythm power both at rest and during movement gating) may be involved in a phase‐locking process in both conditions.

As it was demonstrated that in case of phase‐locking with enhancement, which corresponds to the present situation at rest, it was impossible to distinguish the possible contribution of EEG phase‐resetting from phasic activity [Shah et al., 2004; Yeung et al., 2004], we restricted our analysis on the trials of individual subjects for which the power spectrum remained unchanged after the stimulation.

For each of the seven subjects, we identified at rest a large percentage of trials (62 ± 16%) for which the power spectrum remained unchanged (pure phase‐locking situation) within the whole frequency range spanning 1–50 Hz. Figure 4 illustrates results of this selection in one subject. When all the recorded trials were taken into account, a clear ERSP cluster appeared in the beta/gamma band (Fig. 4A) concomitantly accompanied by a significant ITC cluster in the same frequency band (Fig. 4B). After the selection, although no more ERSP cluster could be found (Fig. 4D), a significant ITC cluster in the beta/gamma band was still present (Fig. 4E). A decrease of power in a large frequency band occurred around 100 ms meaning that it may thus not participate in the N30 generation. The maximal ITC value (0.51 before vs. 0.55 after selection), peak latency (42 ms before vs. 41.4 ms after), and frequency band (19–44 Hz before vs. 23–44 Hz after) of the ITC cluster were not significantly changed by the trial selection (Fig. 4B–E). Conversely, the N30 amplitude was significantly reduced by the selection [mean amplitude of 4.5 ± 1.7 vs. 3.6 ± 1.2 μV, P < 0.02 (Fig. 4C, F)]. In spite of this amplitude reduction, the N30 component conserved its initial morphology and peaked at the same latency (mean value 31.3 ± 0.9 ms before selection vs. 31.1 ± 0.9 ms after). After the selection procedure the relative percentage of the 30 Hz power, in the period excluding the stimulation, remained the same (66.6%).

Figure 4.

Figure 4

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Selection of pure phase‐locking and movement gating effect illustrated for one subject. (A–C) ERSP, ITC, and N30 evoked potentials, respectively, recorded when all the trials were taken into account. Note that this situation corresponds to phase‐locking with amplitude enhancement, where the N30 component was accompanied by significant ERSP (A) and ITC (B) cluster in the β‐gamma frequency range. (D–F) ERSP, ITC, and N30 evoked potentials, respectively, recorded when only the trials for which no amplitude enhancement were taken into account. This situation corresponds to pure phase‐locking where the N30 component was only accompanied by the ITC cluster in the β‐gamma range. Note the reduction of the N30 amplitude in the pure phase‐locking situation (F). (G–I) ERSP, ITC, and N30 evoked potentials, respectively, recorded during movement gating. Note the absence of ERSP and ITC clusters at the N30 latency and the major reduction of this evoked component. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

For comparison, the same subject is illustrated during the movement gating (Fig. 4G–I). In this case, no significant ERSP change was observed after the stimulation (Fig. 4G) and the pure phase‐locking selection procedure was thus not necessary. During movement gating, the ITC cluster in the beta range around 30 ms was dramatically decreased and diluted (from 0.51 to 0.24 ITC max value).The ITC surface in the beta band is centered in this case at 68.5 ms (Fig. 4H). The mean latency of the beta/gamma ITC peak was 34.9 ± 5.2 ms at rest versus 56.25 ± 14.66 ms during the gating. As shown in the illustrated subject, this new ITC picture accompanied the important reduction of the N30 amplitude from 4.2 to 1.12 μV (Fig. 4I).

Phase‐Locking Analysis

To compare the temporal reorganization of beta oscillations following median nerve stimulation in the resting and movement gating conditions, the instantaneous phase of each selected trial recorded in each condition was calculated along time for each subject. Figure 5 shows relative cumulative histograms of instantaneous phase of the selected trials of all the subjects at rest (n = 1,739) (upper part black colored histograms) and during gating (lower part grey colored histograms). Before the stimulus, both at rest and during gating condition, the histogram of phase distribution corresponds to uniform density function (Fig. 5A). In the resting condition, a phase alignment occurred after the stimulus and the phase distribution became gradually more peaked so that the distribution presents a maximum of trials with an instantaneous phase value of 0 radian at the latency of the N30 component (upper part of Fig. 5E). The comparison between the mean histogram calculated for the prestimulus reference period (Fig. 5A) and the 30 ms poststimulus time (Fig. 5E) showed a clear distinction between uniform and peaked distribution at 0 radian, in the resting condition. In contrast, during the movement gating, the phase distribution remained practically the same and no clear peaked distribution emerges at the latency of the N30 component.

Figure 5.

Figure 5

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Reorganization of the spontaneous phase of beta oscillation at rest and during movement gating. Cumulative histograms of the spontaneous phase of single trials beta band oscillation (25–35 Hz) recorded in all the subjects (pooled as a single set) and selected with respect to the pure phase‐locking criteria. Upper black colored histograms and Lower gray colored histograms correspond, respectively, to the data recorded at rest and during the movement gating. Horizontal phase axis ranges from −π to π. Vertical axis corresponds to the relative number of trials. (A) Histograms for the prestimulus reference period ([−60 ms, −5 ms]). (B–H) Histograms from 0 to 60 ms with respect to the stimulation time (illustrated at every 10 ms). Note the progressive reorganization of phase distribution peaking at 0 radian at 30 ms at rest and the absence of reorganization during the movement gating.

Figure 6 illustrates in both resting and gating conditions the mean Z score of the Kuiper's statistic κ. The phase distribution difference between the prestimulus reference period ([−60 ms, −5 ms]) and the poststimulus times was significant (P < 0.05) below a Z score value of 0.68 and 0.047 for both conditions, respectively. In the resting condition, significant threshold was reached for each analyzed time after the stimulus and became highly significant around the N30 latency, reaching a value of −1.44 ± 0.28. In contrast, the mean Z score did not reach significant value around 30 ms during movement gating. The most significant Z score value (−0.85) in this condition corresponded to the least peaked distribution observed at 60 ms in Figure 5H.

Figure 6.

Figure 6

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Statistical analysis of the beta phase distribution at rest and during movement gating. Evolution of the Z score (mean and SD) of the Kuiper's statistic κ. Z score is significant (P < 0.05) below 0.68 and 0.047, and the highest significant values are reached around a poststimulus time of 30 and 60 ms, for the resting and gating conditions, respectively.

DISCUSSION

Our findings demonstrate that the N30 component results from two different mechanisms. One is related to a phasic process that produces by its inherent properties (stimulus locked) an evoked potential accompanied by a β‐gamma power increase. The other is related to a pure phase‐locking mechanism. As the gating produces a complete and specific suppression of both β‐gamma ERSP increase and ITC occurring at the N30 latency, we may propose that the gating interference affects both the phasic and the oscillating generator mechanisms. Nevertheless, it is only when the ITC is suppressed that the N30 is gated. In this context, the relative functional independence of an oscillating generator mechanism with respect to a phasic generator mechanism plays in favor of a dual nature of the N30 component. This physiological characteristic may be supported by more than one single generator model. It is interesting to note that phase‐locking phenomenon is often supported by long range neuronal synchronization implicating communication between distinct areas [Singer, 1999 for a review]. This could corroborate the findings of Kanovsky et al. [2003] describing separate generators within the frontal cortex (BA6 and BA8). These intracortical N30 recordings performed in epileptic patients also reproduced the gating protocols [Cheron and Borenstein, 1987, 1992]. In particular, the mental movement paradigm inducing a blood flow increase in the SMA (BA6) [Roland et al., 1980] produced a specific gating of the N30 without affecting the postcentral components [Cheron and Borenstein, 1992]. This N30 suppression was reproduced by intracortical SMA recordings [Kanovsky et al., 2003] indicating that this region at least could be a source of the N30 component. The current debate concerning the interpretation of the intracortical N30 recording comes from the difficulties to record polarity‐reversal potentials in the frontal lobe [see Barba et al., 2001, 2003, 2005; Barba and Valeriani, 2004]. Taking into account the convolutional anatomic conformation of the cortex, the polarity‐reversal recording may be highly difficult if not impossible. Nevertheless, in addition to the gating approach a large set of evidence has been accumulated in favor of a frontal origin of the N30, namely (1) the N30 amplitude depends on motor cortex excitability [Rossini et al., 1991], (2) apomorphine injection or electrical stimulation of the basal ganglia induced selective increase of N30 amplitude in Parkinsonian patients [Cheron et al., 1994; Pierantozzi et al., 1999; Rossini et al., 1995], (3) transcranial magnetic stimulation (TMS) of the premotor cortex at very low frequency rate produced a specific N30 amplitude increase [Urushihara et al., 2006]. These latter authors hypothesized that this effect may be due to an increase in premotor cortex inhibition. As we demonstrate here that N30 is supported by β‐gamma oscillation, the inhibition‐timing hypothesis [Klimesch et al., 2007] may explain a N30 amplitude increase in presence of increasing inhibition produced by TMS and conversely a N30 decrease in presence of increasing excitation of premotor and motor areas produced by movement execution.

Although, gating during active movement may be due to a combination of both central and peripheral factors, in agreement with earlier gating studies [Cheron and Borenstein, 1987, 1991; Cohen and Starr, 1987; Jones et al., 1989], the present study showed no gating of the SEP wave at subcortical levels below the thalamus [indexed by the conservation of the far‐field P14, originating in the median lemniscus [Desmedt and Cheron, 1981] and between the thalamus and the first parietal activation [indexed by the conservation of the parietal N20, generated by a tangentially oriented dipole located in area 3b of the posterior bank of the central sulcus [Allison et al., 1989]. However, there are some controversies concerning the gating of the parietal N20. A small but significant decrease has been found during vibration interference [Ibanez et al., 1989], passive and active movements [Huttunen and Hömberg, 1991]. A similar N20 gating has been described by Gobbelé et al. [2003], where they also studied the high‐frequency oscillation (HFO ∼ 600 Hz) of very low voltage (<500 nV) accompanying the low frequency N20 component [Curio et al., 1997]. Interestingly, the reported N20 gating was accompanied by attenuation of the late HFO, while the early HFO remained unaffected. Although HFO are generated by different mechanisms than the low frequency component of the N20 [Gobbelé et al., 2004; Urasaki et al., 2006], the comparison with the present β‐gamma oscillation sustaining the N30 is difficult because of major methodological differences. In addition to the major difference in frequency band, HFO have been observed and analyzed after the averaging of digitally band‐pass filtering (450–750 Hz) of the EEG, and no ERSP and ITC analysis have been performed yet on single trials. In addition, HFO remains temporally limited between the N20 onset and fades before the parietal P27 peak (mean duration of 7 ms) [Nakano and Hashimoto, 1999] and thus occurs early before the more widespread N30 component.

The plausible physiological contribution of β‐gamma oscillation phase‐locking to the N30 component is reinforced by intracerebral recordings of spontaneous beta rhythm in the pre‐ and postcentral gyrus and in the frontal medial cortex of humans [Szurhaj et al., 2003, 2005]. Magnetoencephalographic (MEG) studies of the hand sensorimotor areas have showed that finger stimulation induced increment of beta (20–32 Hz) and gamma (36–46 Hz) synchronization. Tecchio et al. [2003, 2004] and Palva et al. [2005] have demonstrated that as early as 30 ms after electrical stimulus given on the finger tip, neural activity phase‐locked more strongly and persistently to the consciously perceived stimuli than to the unperceived stimuli. In particular, they reported a phase‐locking of the beta (14–28 Hz) and low‐gamma (28–40 Hz) oscillation in the contralateral sensori‐motor region. Beta EEG oscillations (14–35 Hz) have also been reported in the hand sensory motor area 1 s after termination of a self‐paced voluntary movement [Pfurtscheller et al., 1997]. It was previously shown that median nerve stimulation was able to trigger an increase in the power of the 10 and 20 Hz oscillations [Pfurtscheller et al., 1997], but only after a delay of 300 ms, which is ten times later than the occurrence of the present beta oscillation. The same type of stimulation evoked an increase in the power of beta oscillation peaking around 500 ms with a latency onset of 300 ms [Pfurtscheller et al., 2002]. These authors showed a decrease in beta oscillation during hand manipulation whereas the amplitude of P140/N200 SEP components was increased. However, the behavior of early SEP components was not the focus of these studies. In monkeys, field‐potential oscillations in the 20–30 Hz range have been reported [Baker et al., 1999] and were supported by synchronous oscillatory activity in a large number of cortical neurons [Murthy and Fetz, 1992] providing synchronization of neuronal firing between somatosensory and motor areas [Wheaton et al., 2005].

It is important to emphasize that the presence of pure phase‐locking in resting condition does not exclude that evoked phasic activity occurs when all the trials were taken into account. Indeed, when the trials presenting power enhancement were rejected, we found that the N30 amplitude was significantly decreased. As ITC values remained the same, this amplitude reduction indicates the contribution of phasic activation to the N30 amplitude. As proposed in the case of many ERP components [Basar, 1980], in addition to this phase‐resetting effect, the rest of the evoked component may be generated by coherent phasic activation of pyramidal neurons via thalamo‐cortical input, as predicted by the additive model.

Resonance in the basal ganglionic‐thalamo‐cortical loop could be implicated in EEG oscillation triggered by sensory stimulation. Neuronal activity in the 30–80 Hz band is associated with motor function in the presence of normal dopaminergic drive [Brown et al., 2001, 2002; Cassidy et al., 2002; MacKay, 1997] and acts as pacemaker for sensorimotor integration [Humphries et al., 2006]. Although their precise functional role remains an open question, it may provide a temporal window for the processing of sensory information [MacKay, 1997]. This rhythmic activity is replaced by slower oscillations in the off‐state of Parkinsonian patients [Brown et al., 2001], and could be related to the N30 alteration in the Parkinsonian off‐state [Cheron et al., 1994; Rossini et al., 1993]. Recently, Kühn et al. [2006] suggested that the 30 Hz oscillation in the subthalamic nucleus that is suppressed during finger actual movement or mental imagery in Parkinsonian patients could be physiological and present in normal subjects. In this theoretical framework, the present time frequency behavior of the N30 component could be viewed as resulting from the phase‐locking of the basal ganglionic‐thalamo‐cortical loop activity resonating around 30 Hz. In the absence of movement, this loop may be activated by the sensory stimulation triggering the phase alignment of the 30 Hz EEG oscillation. Conversely, during active movement the loop is involved in movement control and unable to response to the external stimulation.

As described for the auditory 40 Hz oscillation [Ribary et al., 1991], the N30 related beta/gamma rhythm may be viewed as a more global mechanism working in parallel to the stimuli processing of the somatosensory pathway. The phase‐locking of this rhythm allows the placement of the sensory signal in the temporal context taking into account the intrinsic functional state of the brain at the arrival time of the stimulus.

Phase resetting of both local field potential and single‐unit activity representative of the ongoing motor cortical beta (15–30 Hz) rhythms has been demonstrated in pyramidal tract stimulation in monkeys [Jackson et al., 2002]. This view is also supported by in vitro and in vivo physiological studies [Hughes et al., 2004] showing enhanced oscillation when neurons fire in‐phase with the oscillation field. This could explain at a cellular level how the depolarization induced by the sensory stimulus is able to reset the oscillating phase and bring the system into a synchronous attractor basin at the latency of the N30 component. In contrast, during the finger movement the neuronal populations of the sensory motor cortex and other related areas are involved in the ongoing motor cortical beta rhythms assuming the cortico‐muscular coherence and the action goals [Baker et al., 1999]. In this active context, it is likely that these neuronal populations could be not responsive to the phasic sensory activation and unable to phase‐lock their firing discharges to the external sensory input. Further experimental works will be necessary to dissociate the rhythmic activities linked to motor action from those involved in sensory integration and help to resolve the complex behavior of the N30 component.

CONCLUSION

The important reduction of the frontal N30 occurring throughout its wide topographical extension on the scalp was mainly due to disorganization of the phase‐locking of the beta/gamma EEG oscillations, which normally occurred when the sensory input was not in competition with movement production.

Acknowledgements

The authors would like to thank Arnaud Delorme and Scott Makeig for their generous gift of software. We wish to thank P. Demaret, M. Dufief, and E. Hortmanns for expert technical assistance.

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