Brain, Vol. 123, No. 6, 1203-1215,
June 2000
© 2000 Oxford University Press
Movement-related change of electrocorticographic activity in human supplementary motor area proper
1 Departments of Brain Pathophysiology and 2 Neurosurgery, Kyoto University Graduate School of Medicine, Shogoin, Sakyo-ku, Kyoto, 606–8507 and 3 The National Epilepsy Center, Shizuoka Higashi Hospital, Urushiyama, Shizuoka, 420-0953, Japan
Correspondence to:
Hiroshi Shibasaki, MD, Department of Brain Pathophysiology, Kyoto University Graduate School of Medicine, Shogoin, Sakyo-ku, 606-8507, Japan E-mail: shib{at}kuhp.kyoto-u.ac.jp
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Abstract |
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We investigated movement-related change in the cortical EEG signal by simultaneous recording from the primary sensorimotor area (S1–M1) and the supplementary motor area proper (SMA proper) in four patients with intractable partial epilepsy. By the use of temporal spectral evolution (TSE) analysis, the change in background cortical activity in relation to self-paced finger/wrist extension was compared among the SMA proper, S1 and M1. All three areas showed a decrease in the amount of activity for the frequency range between 10 and 40 Hz before the onset of movement [event- related desynchronization (ERD)]. The SMA proper showed earlier onset of ERD for 18–22 Hz activity (-3.4 ± 0.5 s, mean ± standard deviation) than M1 (-1.7 ± 0.7 s) and S1 (–1.4 ± 0.5 s). The degree of ERD in S1 was greatest for 10–14 Hz and that in M1 for 18–22 Hz, whereas in the SMA proper ERD was observed throughout the frequency bands from 10 to 40 Hz. Neither the degree nor the onset time of ERD in the SMA proper was lateralized to either the ipsilateral or the contralateral side with respect to the movement. A transient increase in activity after movement [event-related synchronization (ERS)] was observed in all three areas. In the SMA proper, two out of four subjects showed ERS for frequency bands below 40 Hz with both ipsilateral and contralateral movements. By contrast, in S1 and M1, ERS was recorded for frequency bands between 20 and 90 Hz, and was predominantly associated with the contralateral movement. The present study suggests that the background cortical activity in the SMA proper has a specific temporal pattern with respect to self-paced movement, and that the SMA proper is involved in motor preparation earlier than S1–M1 in a bilaterally organized manner.
supplementary motor area proper; self-paced hand movements; event-related desynchronization; event-related synchronization; electrocorticography; movement-related cortical potentials
BP = Bereitschaftspotential; SMA = supplementary motor area; ECoG = electrocorticography; ERD = event-related desynchronization; ERS = event-related synchronization; MEG = magnetoencephalography; TSE = temporal spectral evolution; MRCP = movement-related cortical potential
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Introduction |
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The primary sensorimotor cortex (S1–M1) has its own electrical rhythmicity linked to motor function, for example the mu rhythm. Studies using scalp EEG and magnetoencephalography (MEG) have shown reactive changes in rhythmicity in relation to voluntary movement. The amount of rhythmic activity in the EEG and MEG decreases prior to the movement in both ipsilateral and contralateral sensorimotor areas; this is called event-related desynchronization (ERD) (Pfurtscheller and Aranibar, 1977
; Pfurtscheller, 1981; Pfurtscheller and Berghold, 1989; Salmelin and Hari, 1994; Salmelin et al., 1995; Nagamine et al., 1996). This is followed by a transient increase in the rhythm with predominantly contralateral movement, which is termed event-related synchronization (ERS) (Stancak and Pfurtscheller, 1995; Pfurtscheller et al., 1996). Short-lasting 40 Hz oscillations in the scalp EEG (Pfurtscheller et al., 1993, 1996) and MEG (Salenius et al., 1996) were observed around the onset of hand/foot phasic movement in a small number of subjects.
Electrocorticography (ECoG) can record electrical activity without distortion derived from the different electrical conductivities of the scalp, skull, dura mater and cerebrospinal fluid. Thus, ECoG can provide information with higher spatial resolution and a higher signal-to-noise ratio than scalp EEG. Furthermore, ECoG can record high-frequency activity more efficiently than scalp EEG. There have been several ECoG studies during movement tasks that have demonstrated ERD/ERS in S1 and M1 for frequency bands ranging from alpha to gamma (Arroyo et al., 1993; Crone et al., 1993, 1998a, b; Toro et al., 1994). Thus, the question arises of whether cortical activities in different frequency bands have different implications in motor control.
The function of the supplementary motor area (SMA) (in the classical terminology) in motor control has been debated, especially with regard to whether it has a supramotor or supplementary motor function in relation to M1, i.e. does the SMA have a hierarchically higher function than M1, or do these two areas operate in parallel (Tanji, 1994)? There have been many experimental and clinical studies supporting both supramotor (Deecke et al., 1969, 1985; Orgogozo and Larsen, 1979; Roland et al., 1980; Eccles, 1982; Tanji and Kurata, 1982; Rao et al., 1993) and supplementary motor (Penfield and Jasper, 1954; Laplane et al., 1977; Fox et al., 1985; Schell et al., 1986; Hyland et al., 1989; Alexander and Crutcher, 1990; Chen et al., 1991; Schmidt et al., 1992; Ikeda et al., 1992; Shibasaki et al., 1993) functions of the classical SMA. To address this issue, however, the supramotor and supplementary motor functions need to be defined precisely. It is necessary to distinguish the two subregions, i.e. the SMA proper and the pre-SMA (Matsuzaka et al., 1992; Luppino et al., 1993; Tanji, 1994), within the classical SMA, if these are indeed present in humans, because the function of the pre-SMA seems to be positioned at a hierarchically higher level than that of the SMA proper (Alexander and Crutcher, 1990; Deiber et al., 1991; Matsuzaka et al., 1992; Halsband et al., 1994; Hikosaka et al., 1996; Shima et al., 1996; Humberstone et al., 1997; Lee et al., 1999).
This is the first study to delineate the temporal change in ECoG signals recorded simultaneously from M1, S1 and the SMA proper during self-paced finger/hand movement in humans.
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Subjects and methods |
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Subjects
We studied four patients (three females and one male, aged 31–52 years) with medically intractable partial epilepsy. All patients underwent chronic implantation of subdural electrodes for the purpose of epilepsy surgery.
The cortical electrical potentials were recorded with subdural electrodes made of platinum (Ad-Tech, Racine, Wis., USA). Each electrode was 3 mm in diameter, and the centre-to-centre inter-electrode distance was 1 cm. The electrodes were placed on the medial and lateral surfaces of the frontal and parietal lobes on the right hemisphere in two subjects (patients 1 and 4) and on the left hemisphere in the other two (patients 2 and 3). This invasive technique was performed to identify the epileptogenic area by recording seizures and to delineate the cortical function at or around the epileptogenic region by cortical electrical stimulation and by recording somatosensory evoked potentials.
Informed consent was obtained from all subjects after the purpose and possible consequences of the studies had been explained according to the Clinical Research Protocol approved by the Committee of Medical Ethics, Graduate School of Medicine, Kyoto University for patients 1 and 2 and of the National Epilepsy Center, Shizuoka for patients 3 and 4. Other neurophysiological findings for patients 1 and 2 have been reported elsewhere (Yazawa et al., 1998, 2000; Ikeda et al., 1999a, b).
Cortical functional mapping
Cortical electrical stimulation was carried out by applying electric current to each electrode. Details of the stimulation method have been described elsewhere (Lüders et al., 1987; Ikeda et al., 1992; Lesser et al., 1992). Cortical regions in which stimulation elicited muscle contraction were defined as `positive motor areas', and areas in which stimulation caused interference with tonic motor activity or with rapid alternating movements were defined as `negative motor areas' (Lüders et al., 1985).
Identification of S1 and M1 on the perirolandic area was based on subjective sensation and positive motor responses, respectively, elicited by cortical electric stimulation. In the mesial cortex, the SMA proper was identified by its unique response to stimulation, consisting predominantly of tonic positive motor responses of the upper and lower limbs, either unilaterally or bilaterally, and of the trunk, neck and face (Ikeda et al., 1992; Lim et al., 1994). When no positive motor responses occurred, the electrodes located posterior to the vertical anterior commissural (VAC) line on the mesial surface of the superior frontal gyrus were judged to be on the SMA proper unless they elicited negative motor responses upon electrical stimulation. The VAC line is regarded as the anatomical border between the pre-SMA and the SMA proper (Wise et al., 1996; Zilles et al., 1996). For electrodes in the SMA proper that caused no positive motor response on electrical stimulation, the somatotopy was determined further by taking movement-related cortical potential (MRCP) findings into account. The somatotopic distribution of MRCP in the SMA proper was consistent with its somatotopic organization as defined by electrical stimulation (Lee et al., 1986; Neshige et al., 1988; Ikeda and Shibasaki, 1992; Ikeda et al., 1992, 1995).
In order to determine the anatomical location of the VAC line with respect to electrode position, we used the plain lateral view of a skull X-ray obtained after implantation of subdural electrodes and the sagittal view of T1-weighted MRIs obtained before or after surgery. The X-ray was superimposed on the MRI by using common fiducial landmarks, i.e. nasion and inion (Ikeda et al., 1995, 1996).
Electrodes placed over the hand area of M1, S1 or SMA proper were not placed directly on the structural lesion, which was confirmed by MRI or visual inspection during surgery, in any of the subjects. Furthermore, electrodes that showed frequent interictal spikes or an ictal EEG pattern during monitoring were not used for analysis.
Motor task
The subject lay supine on a bed, comfortably, during recording, with the arm contralateral to the implanted electrodes placed on a pillow, and with the eyes kept open. The subject performed a brisk, voluntary extension of the middle finger (patients 1, 3 and 4) or wrist (patient 2) at a self-paced rate of once per 6–8 s. The subjects were trained so that they could move their finger or wrist briskly with a sufficiently long intertrial interval. The motor performance was continuously monitored by on-line EMG recorded from the extensor digitorum communis muscle for middle finger extension and the extensor carpi radialis muscle for wrist extension. Verbal instruction was given to the subjects whenever their performance was found to be inadequate.
Data acquisition and analysis
Continuous ECoGs were simultaneously recorded from 28–32 subdural electrodes. All subdural electrodes were referenced to a scalp electrode placed on the skin at the mastoid process contralateral to the side of implantation. EMG from the extensor digitorum communis or extensor carpi radialis muscles was recorded by a pair of cup electrodes placed on the skin. The bandpass filter for data acquisition was set to 0.016–330 Hz for both ECoG and EMG. All input signals were digitized at the sampling rate of 1000 Hz and stored on magneto-optical (MO) disks with a digital EEG equipment (EEG2100, Nihon kohden, Tokyo, Japan). Data stored initially on MO disks were digitally bandpass-filtered at 0.03–120 Hz for both ECoG and EMG in two subjects (patients 2 and 3) and at 0.03–120 Hz for ECoG and 5–120 Hz for EMG in the other two (patients 1 and 4). After filtering, all signals were reproduced for further analysis by digital–analogue conversion and were resampled at 500 Hz by the use of other equipment (9000/735, Hewlett Packard, Palo Alto, Calif., USA) and stored on MO disks.
Movement-related cortical potentials
The EMG onset of each finger or wrist movement was determined visually on the continuous data. Trials with artefacts or incomplete relaxation between movements were excluded from further analysis. A total of >80 trials were selected for averaging. After confirming the reproducibility of waveforms in two ensembles of averaged ECoGs, each consisting of >40 trials, a group average ECoG was obtained. The analysis epochs began 3.0 s before EMG onset in one subject (patient 1) and 4.0 s before it in three subjects (patients 2, 3 and 4), and ended 2.0 s after it in all subjects. The onset time of the Bereitschaftspotential (BP) was determined as the time when a slow potential shift started to occur. The amplitude of the BP was measured at the time of EMG onset from the baseline, which was defined as the segment from 2.5 to 3.0 s before EMG onset in patient 1 and from 3.4 to 4.0 s in three other subjects.
Temporal spectral evolution
On the basis of the method originally introduced by Salmelin and Hari (Salmelin and Hari, 1994), temporal spectral evolution (TSE) analysis was used to demonstrate the reactive change of background ECoG activity. ECoG signals were bandpass-filtered by a fast Fourier transform filter with a transition width of 2 Hz through consecutive bandwidths of 4 Hz each, ranging from 6 to 98 Hz. The filtered data were rectified to avoid phase cancellation and were averaged time-locked to EMG onset. The analysis epochs were the same as those used for the MRCP analysis. For each frequency band, the degree of change in the TSE amplitude at each electrode was expressed as a percentage (%ERD) with respect to the absolute value measured during the initial segment of the analysis window, which was the same epoch as that used as the baseline for the MRCP measurement. The method of Nagamine and colleagues was used to characterize the time course (Nagamine et al., 1996). The TSE data were digitally low-pass filtered at 10 Hz. The mean ± 2 SD of the activity during the baseline period was defined as the level of resting activity. The onset of ERD in each channel was determined with the aid of a linear regression line (Fig. 1). The regression line started when the low-pass filtered signal exceeded the range of the resting activity and ended at the peak of ERD. The intersection of the regression line with the baseline was used as the calculated onset with 100 ms accuracy. When the linear regression line did not fit well with the actual waveform, the final determination of the onset was done visually, also with 100 ms accuracy. ERS was defined as a transient increase in TSE amplitude after EMG onset above the mean ± 2 SD of the resting activity. The peak time of ERS was determined visually with 100 ms accuracy. The magnitude of the amplitude increase at the peak of ERS was expressed as the ratio to the absolute value measured during the baseline period (%ERS) at each electrode. When two or more peaks were identified in ERS, the peak showing the largest increase in amplitude was used for further analysis.
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Results |
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Movement-related cortical potentials
Figure 2
shows MRCP waveforms recorded from the hand area of left SMA proper, S1 and M1, together with a schematic illustration of electrode location, in patient 3. A clear BP was recorded in the SMA proper with the finger movement of either side, starting earlier compared with S1 or M1. In the SMA proper, the amplitude at the EMG onset was larger for the contralateral finger movement than for the ipsilateral movement.
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Table 1
shows the onset time and the amplitude of BPs measured on the group average waveform. With the contralateral hand movement, the onset time of BPs in the SMA proper in two subjects (patients 2 and 4) was almost equal to that in either S1 or M1. In the other two subjects (patients 1 and 3), BPs occurred earlier in the SMA proper than in other areas. In terms of amplitude, no consistent tendency was observed among the three areas. Within the SMA proper, the amplitude at the EMG onset was larger with the contralateral hand movement than with the ipsilateral movement in patients 1 and 3, but no significant difference was noted in patients 2 and 4. The onset time of BPs in the SMA proper was earlier with the contralateral hand movement in patient 4 and earlier with the ipsilateral movement in patients 1 and 2, and equal in patient 3.
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ERD
Figure 3
shows the results of TSE analysis in patient 3 for the eight 4-Hz frequency bands from 10 to 94 Hz. Because 60 Hz activity was distorted by line noise, the corresponding band was excluded from analysis. In S1, activity at 10–14 Hz started to decline ~1.5 and 0.8 s before the EMG onset for the contralateral and ipsilateral finger movements, respectively. ERD for 18–22 Hz activity was almost the same as that for 10–14 Hz. In M1, the frequency bands below 40 Hz showed ERD starting earlier for the contralateral finger movement than for the ipsilateral movement. The largest degree of ERD was seen for 18–22 Hz. By contrast, the SMA proper showed ERD for 18–22 Hz starting 4.0 s before the EMG onset almost equally for both movements.
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Table 2
summarizes the onset time of ERD and the greatest percentage reduction with respect to the baseline value for each frequency band in the SMA proper, S1 and M1 for each subject. ERD occurred only rarely in the frequency bands above 40 Hz.
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With regard to the side of S1–M1 in relation to movement, ERD occurred earlier for the contralateral hand movement in all subjects except patient 1. This tendency was most conspicuous for the 18–22 Hz activity. In the SMA proper, however, there was no such tendency for activity in this frequency band. Although two subjects (patients 1 and 3) had an equal onset time, patient 2 showed earlier onset for the ipsilateral movement and patient 4 showed the opposite result. With regard to the degree of ERD, no consistent results were obtained in any area when movements of two sides were compared.
As shown at the bottom of Table 2
, we compared the mean onset time among the SMA proper, M1 and S1 only for the frequency band of 18–22 Hz, because only for this frequency band did the three areas show a clear amplitude reduction in all subjects, with the exception of S1 in patient 4. The 18–22 Hz activity started to decrease earlier in the SMA proper than in S1 or M1 in all subjects, although the time difference between the two areas was variable among the subjects. In summary, the SMA proper was involved earlier than S1–M1, at least for the frequency band of 18–22 Hz.
The frequency band showing the most damping in S1 was 10–14 Hz in all three subjects in whom the relevant data were available, whereas in M1 it was 18–22 Hz in all subjects except for patient 2, who showed a relatively constant degree of ERD in M1 for the frequency bands from 10 to 40 Hz. The degree of damping in the SMA proper was about two-thirds of that seen in S1–M1. In the SMA proper, there was no consistent frequency band showing the maximum ERD.
With regard to the spatial distribution of ERD, electrodes showing significant ERD were distributed both anterior and posterior to the central sulcus in the lateral frontoparietal area in all subjects (Fig. 4). On the mesial surface, ERD was seen predominantly in the hand area of the SMA proper in all subjects (Fig. 5). No consistent results were obtained for the pre-SMA.
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ERS
In S1–M1, ERS was observed exclusively with the contralateral movement in all subjects. S1 and M1 in patient 3 (Fig. 3
) showed ERS in the frequency bands above 60 Hz, with a peak 0.1–0.3 s after the EMG onset. Summarizing the results for all subjects, both S1 and M1 showed ERS for the frequency bands from 20 to >90 Hz. The peak time of ERS was earlier for the higher frequency bands, i.e. 0.8–0.9 s after the EMG onset for 30–40 Hz and 0.2–0.5 s for 
60 Hz. In addition, ERS of higher than 50 Hz had two peaks (0.5–0.6 and 0.1–0.3 s) in three subjects (patients 1, 2 and 3).
In the SMA proper, significant ERS was observed in patients 1 and 3. Patient 1 showed a relatively large ERS for the frequency bands between 10 and 40 Hz. In patient 3, ERS was seen only for 18–22 Hz activity (Fig. 3). In these two subjects, both contralateral and ipsilateral movements showed ERS. Although the degree of ERS was larger for the contralateral movement than for the ipsilateral movement, the number of subjects was too small to draw a conclusion. The peak time of ERS was ~0.7–1.4 s after the EMG onset. For frequency bands above 50 Hz, no ERS was observed in the SMA proper in any subject.
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Discussion |
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In the present study, we demonstrated movement-related change in cortical rhythmic activity in the SMA proper which was different from that seen in S1 and M1. As we recorded cortical activity simultaneously from M1, S1 and the SMA proper, direct comparison of cortical background activity and slow potential shifts among these three areas was possible. This is the first report to describe the difference among these three areas in the time course and degree of ERD and the characteristics of ERS in humans, based on direct cortical recording.
The temporal pattern of cortical activity in relation to movements, as indicated by ERD and ERS, and its spatial distribution have been reported previously on the basis of studies of scalp EEG, ECoG and MEG (Pfurtscheller 1981; Salmelin and Hari, 1994; Salmelin et al., 1995; Toro et al., 1994; Pfurtscheller et al., 1996; Nagamine et al., 1996; Leocani et al., 1997; Crone et al., 1998a). Taking the results of these studies together, the ERD in EEG/ECoG appears to start ~2.0 s before the movement onset for both alpha- and beta-band activities, while MEG shows an earlier onset of ERD. With regard to the spatial distribution, no consistent results have been obtained among these studies. MEG is more sensitive in detecting the earlier onset of ERD probably because of the different characteristics of the techniques. MEG picks up mainly the tangentially oriented signal, while ECoG can record the electrical activity of the cortical surface just beneath the electrode more easily than that arising from the sulcus (Gloor, 1975). If it is assumed that the generator source of the earlier part of ERD is present in the central sulcus and that of its later part involves both the sulcus and the crown, ECoG is more sensitive to its later part and MEG can pick up both the earlier and the later part. Simultaneous recording of ECoG and MEG, if technically possible, will be able to answer this question.
The onset time of ERD observed here in S1–M1 is consistent with the results of previous reports (Pfurtscheller, 1981; Salmelin and Hari, 1994; Salmelin et al., 1995; Toro et al., 1994; Nagamine et al., 1996; Pfurtscheller et al., 1996; Leocani et al., 1997; Crone et al., 1998a). The new finding in the present study is the earlier onset of ERD in the SMA proper than in S1 and M1. Although the time course of ERD in S1 and M1 was variable among subjects, the earlier onset of ERD in the SMA proper than in S1 and M1 was observed consistently in all subjects. This suggests that the SMA proper is involved in motor preparation earlier than S1 and M1.
There have been many debates about whether the SMA is involved in higher-order function compared with M1. Ikeda and colleagues, by recording MRCP with subdural electrodes, observed simultaneous activation of the SMA (SMA proper) and M1 (Ikeda et al., 1992). In the present study, the onset time of MRCP was almost equal in S1–M1 and the SMA proper in two subjects. By contrast, the onset time of ERD was earlier in the SMA proper than in S1–M1 in all subjects. This discrepancy may be based on the different generator mechanisms of ERD and MRCP, as discussed by Toro and colleagues (Toro et al., 1994). These authors showed that ERD responses and MRCPs differed in their temporal sequence of magnitude and spatial distribution, although these two EEG phenomena shared several common features. Although the precise mechanism of ERD/ERS has not been elucidated until now, the present electrophysiological study is the first report to show clearly that the SMA proper is involved earlier than S1 and M1 in motor preparation.
The recently introduced technique of functional MRI (fMRI) combined with event-related or cross-correlation analysis provided us with information that has much better time resolution than the conventional fMRI method. Several studies have shown the earlier involvement of SMA than of M1, at least in certain motor tasks (Richter et al., 1997; Wildgruber et al., 1997; Kansaku et al., 1998). However, since the two subregions within the SMA were not differentiated in those studies, it is possible that activation of the pre-SMA contributed to these findings. The notion that the pre-SMA responds in more complicated contexts than the SMA proper, especially in the motor preparatory phase or motor selection, is suggested by recent experimental and neuroimaging studies (Alexander and Crutcher, 1990; Matsuzaka et al., 1992; Luppino et al., 1993; Halsband et al., 1994; Shima et al., 1996; Ikeda et al., 1999b; Lee et al., 1999). These results suggest strongly that the pre-SMA plays a more important role in the so-called supramotor function than the SMA proper. Since we did not analyse the EEG activity of the pre-SMA in the present study, because of the lack of common findings among different subjects with respect to the behaviour of ERD/ERS, the difference between the SMA proper and the pre-SMA remains to be clarified further.
In the present study, the frequency band showing the most damping was lower in S1 (10–15 Hz) than in M1 (~20 Hz), which conforms with the previous reports (Salmelin and Hari, 1994; Salmelin et al., 1995; Pfurtscheller et al., 1996). In the SMA proper, the magnitude of ERD was relatively small, and the frequency band showing the largest ERD was not consistent among the subjects. Thus, in S1 and M1, activity at 10 and 20 Hz, respectively, might be predominant, whereas in the SMA proper activities in a wider frequency range may be involved. In addition, the ERD response in the SMA proper, like MRCPs, showed a similar pattern with respect to the movement of the contralateral and ipsilateral hands. This may be explained by the anatomical characteristics of the SMA proper, such as the strong transcallosal connection between the bilateral SMAs (McGuire et al., 1991; Rouiller et al., 1994), the bilateral corticospinal innervation (Luppino et al., 1991; Galea and Darian-Smith, 1994; Dum and Strick, 1996) and the bilateral subcortical projections (Künzle, 1978; Wiesendanger et al., 1996).
Gamma-band activity, especially of ~40 Hz, seems to show a unique type of behaviour. In scalp EEG studies employing phasic finger movement, a transient increase in 40 Hz activity was observed by Pfurtscheller and colleagues around the time of movement onset, with clear somatotopy (Pfurtscheller and Neaper, 1992; Pfurtscheller et al., 1993, 1996). These authors suggested that the ERS can be seen as a correlate of activated neural structures and is probably related to sensorimotor integration immediately before or during the activation of pyramidal neurons in the motor cortex. They further suggested that this phenomenon might reflect motor planning. A recent ECoG study by Crone and colleagues demonstrated low and high gamma ERS in a visual–motor decision task (Crone et al., 1998b). These authors suggested that low gamma (35–50 Hz) ERS might reflect motor output, sustained attention to the motor output and/or continued motor programming, whereas high gamma (75–100 Hz) ERS might be specifically associated with the planning or initiation of the motor response rather than its continuous execution. They also showed that the topography of gamma ERS was more consistent with the traditional maps of sensorimotor functional anatomy than with alpha and beta band activities.
In the present study, the onset and peak of gamma band ERS in S1 and M1 were earlier for the higher frequency band than for the lower ones, suggesting that ERS of >50 Hz is more likely to be related to the initiation of movement. This result is consistent with the report mentioned above (Crone et al., 1998b). In contrast to S1–M1, the SMA proper showed no change in gamma band activity of >50 Hz, although two subjects (patients 1 and 3) showed ERS in the lower frequency bands in the movement of either side. Thus, the high-frequency oscillation above 50 Hz seems to be seen preferentially in S1–M1 and not in the SMA proper. Of course, we cannot exclude the possibility that that these activities were not detected because of technical limitations. Even in S1–M1, the absolute value of high-frequency activity was about one tenth of alpha-band activity and the distribution was smaller compared with lower frequency components (not shown). Furthermore, the number of electrodes placed on the mesial frontal area was smaller than the number placed on S1–M1. This might explain why we could not detect any high-frequency components in the SMA proper. On the basis of a somatosensory discrimination study, Menon and colleagues proposed that subdural electrode arrays for cortical recording would need spacing of <5 mm to detect gamma-band oscillation underlying perceptual categorization (Menon et al., 1996). Further investigations are needed before we can conclude that ERS of >50 Hz does not exist in the SMA proper.
Several investigators have been interested in gamma-band oscillation (up to 80 Hz) of unit discharges and field potentials in animals and humans in relation to different kinds of brain function, such as olfactory (Freeman, 1978), visual (Eckhorn et al., 1988; Gray et al., 1989), auditory (Pantev et al., 1991) and sensorimotor (Sanes and Donoghue, 1993; Murthy and Fetz, 1996; Donoghue et al., 1998). Results of studies in the motor cortex in monkeys (Sanes and Donoghue, 1993; Murthy and Fetz, 1996; Donoghue et al., 1998) have shown that high-frequency oscillations (20–80 Hz) of local field potentials in the motor cortex are abundant in the preparatory phase and diminish during motor execution. Donoghue and colleagues postulated that the oscillations might reflect a more global, ongoing process in the neocortex rather than specific details of the upcoming motor action, because of their variability with respect to behaviour (Donoghue et al., 1998). They also argued that oscillations could reflect attempts to couple with other cortical areas related to movement preparation, such as the premotor cortices. In these experiments, unlike in the present study, the oscillations were not subdivided into different frequency bands. Thus, the results of these studies in monkeys are not directly comparable with the results reported here. Furthermore, it is unknown which frequency range activity in the human motor cortex corresponds to the oscillations observed in the motor cortex of the monkey. The clear ERD pattern of the alpha- and beta-range activities reported here is in good agreement with the findings of the monkey studies. The behaviour of the gamma-band ERS, however, is not consistent with that of oscillations in the monkey studies in several respects: gamma-band ERS in the present study was time-locked to the onset of movement and appeared only during the short period around movement onset.
The effect of applying filters to transient signals should be taken into account. In this study, we used the fast Fourier transform filter to extract activity in particular frequency bands. Since this filter is not ideally suited to the analysis of transient signals, possible distortion of the transient activity concerning ERS should not be ignored. In patient 1, for example, MRCPs in both M1 and S1 had some transient peaks after the EMG onset. However, only the contralateral movement showed significant ERS in S1 for the frequency bands above 50 Hz. If ERS was a ghost product produced by this filtering, all electrodes should have shown a similar ERS pattern. Therefore, the majority of features demonstrated here can be regarded as real phenomena.
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Acknowledgments |
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The authors wish to thank Dr M. Hämäläinen and Mr M. Kajola for help in data analysis. This study was supported by Grants-in-Aid for Scientific Research (A) 09308031, (A) 08558083, on Priority Areas 08279106, (C) 10670583 and (C) 1167621 from Japan Ministry of Education, Science, Sports and Culture, Research for the Future Program from the Japan Society for the Promotion of Science JSPS-RFTF97L00201.
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Received July 19, 1999. Revised January 12, 2000. Accepted January 20, 2000.
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