Journal of the Neurological Sciences 337 (2014) 201–211
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The modulation of rolandic oscillation induced by digital nerve stimulation and self-paced movement of the finger: A MEG study Rei Enatsu a,1, Takashi Nagamine b,d,⁎, Jun Matsubayashi b, Hitoshi Maezawa b,c, Takayuki Kikuchi a,b, Hidenao Fukuyama b, Nobuhiro Mikuni a,e, Susumu Miyamoto a, Nobuo Hashimoto f a
Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto, Japan Human Brain Research Center, Kyoto University Graduate School of Medicine, Kyoto, Japan Department of Oral and Maxillofacial Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan d Department of Systems Neuroscience, Sapporo Medical University Graduate School of Medicine, Sapporo, Japan e Department of Neurosurgery, Sapporo Medical University Graduate School of Medicine, Sapporo, Japan f National Cerebral and Cardiovascular Center, Suita, Japan b c
a r t i c l e
i n f o
Article history: Received 22 June 2013 Received in revised form 27 November 2013 Accepted 4 December 2013 Available online 12 December 2013 Keywords: Event-related synchronization Event-related desynchronization Rolandic oscillation Temporal spectral evolution Magnetoencephalography Digital nerve
a b s t r a c t Background: The rolandic cortex exhibits spontaneous rhythmic activity. This oscillation can be modulated by somatosensory stimulation and voluntary movement. The purpose of this study is to elucidate the influence of sensory input on the rolandic oscillation in comparison with movement-related oscillation. Methods: Magnetic brain rhythms were recorded in nine healthy subjects in two sessions: electrical stimulation (STIM) of the digital nerve and self-paced movement (SPM) of the right index finger. Thereafter, 10 and 20 Hz oscillatory activities were compared between the two sessions with temporal spectral evolution analysis. Results: Sensory input altered the rolandic oscillations even under no movement conditions. As for 10 Hz ERD in the STIM session, three subjects showed a contralateral dominant pattern, whereas the remaining subjects showed a bilateral pattern. In spite of this individual variability, ERD showed comparable amplitude in both sessions. However, ERSs in the SPM session were larger than that in the STIM session. These findings might reflect the activation of neural networks common to sensory and motor systems followed by the inhibition of the other surrounding cortical areas. Conclusions: Our results suggest that rolandic oscillations may reflect the coordination of sensory and motor systems in the neural networks including both sensory and motor systems. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Gastaut reported that the human rolandic cortex exhibits rhythmic activity similar to the occipital area [1]. This oscillation was termed “rythme en arceau” and now is called mu rhythm owing to its archlike shape. This oscillation can be modulated by somatosensory stimulation and voluntary movement [1,2]. Electroencephalographic and magnetoencephalographic studies have revealed that this activity involves two main frequency bands: alpha bands centered at about 10 Hz and beta bands centered at about 20 Hz [3–8]. The 10 Hz and 20 Hz oscillations have been considered to originate in the postcentral gyrus and the anterior bank of the central sulcus, respectively, on the basis of magnetoencephalography (MEG) recordings [5–7,9,10]. On the other hand, several works have shown that both frequencies are
⁎ Corresponding author at: Department of Systems Neuroscience, School of Medicine, Sapporo Medical University, S1W17, Chuo-ku, Sapporo 060-8556, Japan. Tel.: +81 11 611 2111x2660; fax: +81 11 644 1020. E-mail address: [email protected] (T. Nagamine). 1 Current affiliation: Department of Neurosurgery, Himeji Medical Center, Himeji, Japan. 0022-510X/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jns.2013.12.011
observed in the same sensorimotor area with different modulation patterns [11–13]. These cortical oscillations have been interpreted as a readiness or idling state of the sensorimotor cortex [2,4,5,7,10,14]. Other studies reported that rolandic oscillation is modulated by attention [15–19]. The generator and functional meaning of these oscillations remain controversial. Knowledge of the characteristics of these oscillations can aid to elucidate the complicated system of sensory processing and motor control. Previous magnetoencephalographic studies reported that both 10 Hz and 20 Hz rolandic oscillations over the bilateral hemispheres are modulated by sensory input as well as by movement [6,7,20,21]; however, we should note the content of sensory stimuli in these previous reports. Their studies used electric stimulation of the median nerve with intensities exceeding the motor threshold. It was reported that passive movement induced somatosensory evoked magnetic fields (SEFs) [22] and modulated rolandic oscillation [23,24]. These reports suggest that proprioception could affect rolandic oscillations. In these studies of median nerve stimulation accompanied with movement, the effect of proprioceptive input derived from muscle tension could not be excluded. Although several previous studies tried to avoid this
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Fig. 1. Schematic depiction for temporal spectral evolution. The signals were filtered through a pass-band of interest, followed by rectification. Time-epochs of predetermined lengths (12 s in this paper) were specified taking event of interest (electric stimulation or EMG onset) as a trigger for averaging. Averages were conducted until the reasonable S/N ratio was obtained depending on the paradigm (about 80–100 trials).
effect [12,25], little information is available regarding the difference in contribution between pure sensory input and movement on the responses of rolandic oscillation. The purpose of this study is to elucidate the influence of sensory input and movement on the sensorimotor network. The rolandic oscillation induced by sensory input was compared with movementrelated oscillations, especially focusing on the laterality by using MEG, which has better temporospatial information than electroencephalography (EEG) [20,26]. To exclude the effect of afferent input from the muscle movement, we applied electrical stimulation to the digital nerve for sensory stimulation.
which ranged from 2.7 to 6.0 mA, and 100 stimuli were delivered in total.
2. Materials and methods
Magnetic brain signals were recorded inside a magnetically shielded room using a helmet-shaped whole-head coverage MEG system (VectorView system; Elekta Neuromag Ltd., Helsinki, Finland) [27]. In this study, signals recorded from 204 planar gradiometers were used for analysis because they provided an optimal signal-to-noise ratio for superficial current sources and showed the approximate location of cortical current sources as the largest signals seen immediately above generators. The magnetic field strengths were shown in units of femtotesla per centimeter (fT/cm), and this indication was included in each figure and table accordingly. Four head-position indicator coils were placed on the scalp and their locations with respect to the anatomical fiducial points (nasion, bilateral preauricular points) were determined with a three-dimensional digitizer (Polhemus Ltd., Colchester, VT, USA). Thereafter, the head shape of each subject was measured by checking evenly distributed points covering the whole scalp using a digitizer. In order to find the exact head position with respect to the sensors, a weak electrical current was applied to the coils and the resulting magnetic signals were measured just before each MEG measurement session. During the recording, finger movements were monitored by surface electromyography (EMG) of the bilateral extensor indicis proprius muscles. Electrooculography (EOG) was also recorded. The impedance of all electrodes was kept below 20 kΩ. Continuous data were acquired at a
2.1. Subjects Nine healthy right-handed subjects (aged 26–36 years old, eight men and one woman) were studied (S1-9). The informed consent was obtained before each experiment and all procedures were approved by the ethics committee of Kyoto University Graduate School and Faculty of Medicine. 2.2. Stimulation protocol The subjects sat in a chair in a magnetically shielded room with their forearm on a table. Magnetic brain signals were recorded with a whole head magnetometer under two conditions. 2.2.1. Electrical stimulation (STIM) of the right index finger During electrical stimulation, two ring electrodes were placed around the right index finger, one each on the proximal and distal interphalangeal joints, and stimuli were delivered with 0.3 ms constant current pulses once every 6 s with the proximal ring electrode acting as a cathode. Current strength was set to three times the sensory threshold,
2.2.2. Self-paced movement (SPM) of right index finger The subjects were asked to extend their right index finger for a short duration followed by free return at their own pace once about every 6 s. They continued movements until the number of repetitions reached around 80–100 times in one session. Each session took 8–10 min depending on the subject's weariness. 2.3. Data acquisition
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Fig. 2. Examples of 0.1–100 Hz, 10 Hz and 20 Hz filtered raw data along the left sensorimotor area in two subjects (subject 1 (S1) and subject 6 (S6)). Selected sensor is shown as a filled circle in the sensor array. STIM: electrical stimulation, TRIG: stimulation trigger, SPM: self-paced movement, EMG: electromyography.
sampling rate of 303 Hz for all signals with a band-pass filter of 0.1 to 100 Hz for MEG, EOG and 10 to 100 Hz for EMG.
followed by rectification and averaging over about 80–100 trials with respect to the onset of each STIM or SPM session (Fig. 1). The averaged signal was smoothed with a 10 Hz low-pass filter.
2.4. Temporal spectral evolution analysis 2.5. Data analysis Signals were analyzed off-line to obtain precise trigger timing for averaging from the rectified EMG. From continuous MEG raw data, epochs from 6 s before stimulation onset to 6 s after onset were collected for the STIM sessions. Epochs from 6 s before EMG onset to 6 s after onset were collected for the SPM sessions. Signals were reviewed visually, and epochs including eye movement artifacts, ambiguous EMG bursts, or other artifacts were omitted from the averaging. Temporal spectral evolution (TSE) analysis [6,7] was adopted to calculate the average amplitude level of 10 and 20 Hz activities related to a certain event as a function time. This method demonstrates eventrelated but not necessarily phase-locked changes of the averaged amplitude level of oscillatory activities in a given pass-band. In our study, the signals were filtered through a pass-band around 10 Hz and 20 Hz
In our study, the signals were filtered through a pass-band of 8–13 Hz for 10 Hz signal and of 18–23 Hz for 20 Hz signal. Considering that the signals from planar gradiometers are strongest when the sensors are located just above local cerebral sources, we used the data from the most reactive sensor that showed the largest amplitude difference between maximum suppression and maximum enhancement in each hemisphere to quantify the modulation of the rolandic rhythms. Event-related desynchronization (ERD) and event-related synchronization (ERS) were defined as a time-locked decrease and increase in amplitude of ongoing rhythmic activities from the baseline period, respectively [4,28]. TSE amplitudes of 10 Hz and 20 Hz activities in these sessions were analyzed using the mean value of the period
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between −10 ms and +10 ms to the time of maximal suppression and enhancement. For statistical analysis, the percentages of the decrement (Dmax) and increment (Imax) of the TSE amplitude at these two time points were evaluated with respect to that during the baseline period. Their latencies were defined as when minimum (Dmax latency) and maximum (Imax latency) values were reached, respectively [9,10]. The prestimulus 200 ms (from −200 to 0 ms) and 200 ms periods 3 s preceding movement onset (−3100 ms to −2900 ms) were adopted as the baseline period for STIM sessions and SPM sessions, respectively. Maximum suppression and enhancement with changes larger than 2 times standard deviation (2 S.D.) of baseline period were accepted for further analysis in this study. For comparison of the percentage change (left vs right, STIM session vs SPM session), the Wilcoxon signed rank test was used. For statistical analysis, PASW (PASW statistics 17.0; SPSS Inc., Chicago) was used and P b 0.05 was regarded as significant. 3. Results 3.1. Oscillatory changes in STIM session As seen in the examples of non-filtered raw data taken from the left sensorimotor area in two subjects (S1 and S6), amplitude fluctuation of oscillatory activity was observed in both the STIM and SPM sessions. They were more clearly manifested by application of a bandpass frequency filter of 10 Hz (8–13 Hz) and 20 Hz (18–23 Hz) (Fig. 2). In the STIM session of one subject (S6), TSE analysis identified one focal reactive area in each hemisphere in both 10 Hz and 20 Hz components (Fig. 3). In the left hemisphere, the amplitude of the 10 Hz component started to decrease after electrical stimulation and reached maximum suppression 330 ms after onset; thereafter, the amplitude increased and reached the maximum enhancement at 1480 ms. In the right hemisphere, the amplitude of the 10 Hz component slightly
decreased by 15% from the baseline level at 190 ms after stimulation. The amplitude increased up to the maximum at 580 ms. In the 20 Hz component, the amplitude started to decrease after stimulus onset over the bilateral hemispheres and increased amplitude followed in the same areas as those of the 10 Hz component. In the left hemisphere, the amplitude decreased by 20% from the baseline level at 250 ms; thereafter, it started to increase and reached maximum enhancement 480 ms after stimulation. Over the right hemisphere, the decrease of amplitude was 8% from the baseline level and the maximum suppression was seen 270 ms after stimulation. The amplitude increased to the maximum enhancement at 600 ms. All of the subjects showed two focal reactive areas for the 10 Hz component, one in each hemisphere (Fig. 4). These time-locked amplitude decrements of ongoing rhythmic activity were accepted as ERD. Two subjects (S1, S3) did not show any traceable amplitude decrease larger than 2 S.D. from the baseline in the left and right hemispheres, and they showed an amplitude increase immediately after stimulus onset; therefore, we excluded these subjects from the statistical analysis of 10 Hz maximum suppression. The time-locked amplitude increases of ongoing rhythm were accepted as ERS. With respect to 20 Hz, two focal reactive areas were identified in all subjects and each hemisphere had one reactive area similar to that at 10 Hz (Fig. 5). In three hemispheres of three subjects, since the amplitude decrease was smaller than 2 S.D. from the baseline and ERS was observed immediately after stimulus onset without showing ERD (left side in S1 and S2, right side in S5), we excluded these three hemispheres from the statistical analysis of 20 Hz maximum suppression. 3.2. STIM session With respect to 10 Hz oscillatory change, Dmax ranged 2–62% (median: 9%) and 3–18% (median: 8%) in left and right sensorimotor
Fig. 3. TSE analysis of STIM session in one subject (S6). Clear responses were observed in both the 10 Hz and 20 Hz frequency ranges, and were found to concentrate around the bilateral sensorimotor area. Single plus: maximum suppression, double plus: maximum enhancement. Lt: left, Rt: right.
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Fig. 4. 10 Hz TSE analysis of STIM session in bilateral sensorimotor areas of all subjects. The prestimulus 200 ms (from −200 to 0) was adopted as the baseline for STIM session. The percentage decrement and increment of TSE amplitude from the mean amplitude of the baseline periods were used for %decrease of maximum suppression (%dec) and %increase of maximum enhancement (%inc), respectively. Single plus: maximum suppression, double plus: maximum enhancement.
areas, respectively. Imax ranged 7–42% (median: 17%) and 7–38% (median: 20%) in left and right sensorimotor areas, respectively (Fig. 6). Dmax latencies ranged 270–460 ms (median: 340 ms) and 90–540 ms (median: 340 ms), in the left and right hemispheres, respectively (Fig. 7). Imax latencies of left and right hemispheres ranged 160–2080 ms (median: 1190 ms) and 340–1750 ms (median: 1080 ms), respectively. With respect to the 20 Hz component, Dmax ranged 9–30% (median: 17%) and 2–20% (median: 12%) in left and right sensorimotor areas, respectively. 20 Hz Imax ranged 9–56% (median: 27%) and 7–48% (median: 27%) in left and right sensorimotor areas, respectively (Fig. 6). Dmax latencies of left and right hemispheres ranged 230–680 ms (median: 310 ms) and 60–440 ms (median: 300 ms), respectively (Fig. 7). Imax latencies of left and
right hemispheres ranged 480–1910 ms (median: 750 ms) and 520–1720 ms (median: 710 ms), respectively. The comparison of 10 Hz ERD between the sides showed wide individual variability in the contra–ipsi patterns. In three subjects (S6, 7, 8), 10 Hz ERDs showed apparent laterality, manifested as Dmax greater over the left hemisphere exceeding 30% (Fig. 6). In another four subjects (S2, 4, 5, 9), bilateral 10 Hz ERDs were comparable in size and Dmax was smaller than 30%. The differences in Dmax between left and right ranged 27–54% in the former three subjects and 3–9% in the remaining subjects. As for statistical analysis of 10 Hz Dmax between sides using all 7 subjects, there was no significant difference as a group. On the other hand, with respect to 10 Hz ERS, the amplitude differences between left and right were not prominent, even in subjects with prominent left 10 Hz ERD. Imax was not statistically different between the
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Fig. 5. 20 Hz TSE analysis of STIM session in bilateral sensorimotor areas of all subjects. The prestimulus 200 ms (−200 to 0) was adopted as the baseline for electrical stimulation session. Single plus: maximum suppression, double plus: maximum enhancement.
sides. With respect to the 20 Hz component, none of the subjects showed clear laterality of oscillatory change in both ERD and ERS, even in the three subjects showing prominent left 10 Hz ERD (Fig. 6). In 20 Hz components, there was no statistically significant difference between left and right sides in both Dmax and Imax. With respect to Dmax latencies and Imax latencies, there was no significant difference between left and right sides in both 10 and 20 Hz frequency ranges (Fig. 7). 3.3. SPM session With respect to the 10 Hz component in the SPM session, each hemisphere had one focal reactive area around the sensorimotor, similarly to the STIM session (Fig. 8). Dmax ranged 7–62% (median: 22%) and 7–51% (median: 22%) in left and right sensorimotor areas,
respectively (Fig. 8, 10a). Imax ranged 15–75% (median: 22%) and 11–138% (median: 28%) in left and right sensorimotor areas, respectively. Dmax latencies ranged from −372 to 633 ms (median: 57 ms) in the left hemisphere and from − 299 to 538 ms (median: 292 ms) in the right hemispheres. Imax latencies of left and right hemispheres ranged 137–2779 ms (median: 1576 ms) and 217–2838 ms (median: 1037 ms), respectively. Similarly, in the 20 Hz component, each hemisphere had one focal reactive area around the sensorimotor area in the SPM session (Fig. 9). All of the subjects showed both ERD and ERS of 20 Hz in bilateral sensorimotor areas except for ERD in the right hemisphere of one subject (S5). With respect to the 20 Hz component, Dmax ranged 3–51% (median: 28%) and 7–24% (median: 17%) in left and right sensorimotor areas, respectively (Figs. 9, 11a). 20 Hz Imax ranged 6–116% (median: 61%) and 8–117% (median: 44%) in left and right
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3.4. Comparison between STIM and SPM
Fig. 6. Percentage change of TSE amplitudes of maximum suppression and enhancement from the baseline period in 10 and 20 Hz frequency ranges in STIM session. Gray marks and lines show the group in which left prominent ERDs were observed (S6, 7, 8).
sensorimotor areas, respectively. Dmax latencies of left and right hemispheres ranged from − 249 to 317 ms (median: 130 ms) and from − 152 to 580 ms (median: 301 ms), respectively. Imax latencies of left and right hemispheres ranged 486–2528 ms (median: 1255 ms) and 186–2061 ms (median: 936 ms), respectively. As for laterality of 10 Hz Dmax, only one subject (S6) showed clear laterality with a difference between left and right hemispheres larger than 20%. This difference was not significant in the statistical analysis of all subjects as a whole (Fig. 10a). In the comparison of 10 Hz Imax between left and right, three subjects showed differences larger than 20%. However, since two subjects (S5, S9) demonstrated right dominance (26%, 84%) and the other subject (S3) showed left dominance pattern (35%), no consistent tendency was observed. With respect to 20 Hz Dmax, the left side was larger than the right with the difference larger than 20% in three subjects (S4, 6, 8) (Fig. 11a). However this difference was not statistically significant. With respect to 20 Hz Imax in the SPM session, consistent laterality was not observed and there was no significant difference between sides.
As seen in Fig. 10b, in the comparison of left 10 Hz Dmax between STIM and SPM sessions, there was no significant difference between the sessions. This tendency of no significant difference was also applicable to the three subjects (S6, 7, 8) whose ERD was prominent in the STIM session. The left 10 Hz Imax was larger in the SPM session in seven (S1, 3, 4, 5, 6, 8, 9) of nine subjects than in the STIM session and this difference was significant as a group (n = 9, P = 0.02) (Fig. 10b). Right 10 Hz Dmax was larger in the SPM session than in the STIM session in six (S2, 4, 5, 6, 7, 8) of seven subjects; however, this difference was not statistically significant. Right 10 Hz Imax was larger in the SPM session than in the STIM session in eight subjects (S1, 2, 3, 4, 5, 6, 8, 9) and this difference was statistically significant (n = 9, P = 0.03). In the comparison of left 20 Hz Dmax between STIM and SPM sessions, it was larger in the SPM session than in the STIM session in five (S3, 4, 6, 8, 9) of seven subjects (Fig. 11b). However, this difference was not statistically significant as a group. Left 20 Hz Imax was larger in the SPM session than in the STIM session in seven subjects (S2, 3, 4, 5, 6, 8, 9) and smaller in two subjects (S1, 7), and statistical analysis showed that it was significantly larger in the SPM session as a group (n = 9, P = 0.02) (Fig. 11b). Right 20 Hz Dmax was larger in the SPM session than in the STIM session in six (S1, 2, 3, 6, 7, 9) of eight subjects and smaller in two subjects (S4, 8). Right 20 Hz Imax was larger in the SPM session than in the STIM session in six (S3, 4, 5, 6, 8, 9) of nine subjects. These %changes over the right hemisphere did not show any significant differences between the two sessions. In the three subjects (S6, 7, 8) with prominent left 10 Hz ERD in both STIM and SPM sessions, 20 Hz ERDs did not display this prominent change in either STIM or SPM sessions (Figs. 10, 11).
4. Discussion We found that sensory input accompanying no movement can modulate rolandic oscillations in both 10 Hz and 20 Hz frequency ranges over the bilateral hemispheres. This finding is consistent with previous studies [12,13]. Although there was no significant laterality as a whole for both ERD and ERS in 10 Hz and 20 Hz in the STIM session, 10 Hz
Fig. 7. The latency of maximum suppression and enhancement in 10 and 20 Hz frequency ranges in STIM session. Max Sup: maximum suppression, Max Enh: maximum enhancement.
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Fig. 8. 10 Hz TSE analysis of SPM session in bilateral sensorimotor areas of all subjects. The 200 ms periods 3 s preceding movement onset (−3100 ms to −2900 ms) was adopted as the baseline period for self-paced movement session. Single plus: maximum suppression, double plus: maximum enhancement.
ERD showed wide individual variability of laterality in the STIM session. ERDs in the STIM session, including these 10 Hz components, were comparable in amplitude to that in the SPM session. However, ERSs in the SPM session were larger than that in the STIM session. As for bilateral distribution, previous MEG studies have dealt with this using sensory evoked field (SEF) [29,30] and rolandic oscillations [6,7,9,10,20,21,26]. A previous MEG study in humans reported that SEF produced by median nerve stimulation was enhanced by cutaneous information given to the other hand [31]. Regarding this bilateral influence from the periphery, although transcallosal connections between the two hemispheres were previously reported in human [32,33] as well as nonhuman primates [34], uncrossed projections from body parts to the sensory cortex have not been identified either in human or non-human primates [35]. Therefore, it is reasonable to estimate that the bilateral
distribution of oscillatory change in our results was conveyed through the transcallosal communication between the two hemispheres. However, Dmax latencies and Imax latencies ranged 90–540 ms and 160–2080 ms, respectively and these latencies were too late for direct afferent input. Furthermore, latencies for Imax/Dmax in the left side were not always earlier than those for the right side. All these findings cannot be explained by the direct input to primary somatosensory cortex (SI). Therefore, it might reflect the indirect secondary processing. In addition to this documentation for alternation of SI activities, it has been also reported that both alpha and beta frequency oscillatory activities are altered in the bilateral secondary somatosensory cortex (SII) by electrical stimulations [36]. Della Penna et al. applied an inverse operator to the raw field distribution over the helmet and estimated waveforms originating from SI and SII [36]. By this way, they were
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Fig. 9. 20 Hz TSE analysis of SPM session in bilateral sensorimotor areas of all subjects. The 200 ms periods 3 s preceding movement onset (−3100 ms to −2900 ms) was adopted as the baseline period for self-paced movement session. Single plus: maximum suppression, double plus: maximum enhancement.
able to separate activities between SI and SII. With respect to their estimated SII oscillation, the latencies of maximum ERD and ERS were observed at approximately 430 ms and 1140 ms after the stimuli respectively. These latencies of maximum ERD and ERS coincided with our results, hence the bilateral oscillatory changes in our study might also be associated with bilateral SII activity as well as SI activity. In our results in the STIM session, 10 Hz ERD showed the wide individual variability in the contra–ipsi patterns; 10 Hz ERD was predominant on the contralateral side in three subjects and showed a similar amplitude in the remaining subjects. Previous studies speculated that ERD is likely to correspond to cortical activation [11,15,16]. Taking these previous reports into account, the wide range of 10 Hz ERD observed in the present results might reflect various extent of cortical
activation induced by sensory input, which varies depending on individual. This study has not elucidated the functional significance of 10 Hz ERD on sensory processing and motor control. This could be elucidated if we could specify the difference related to sensory processing or motor control in groups with and without prominent left 10 Hz ERD. It would be an interesting consideration for the future studies. In the comparison of oscillatory changes between STIM and SPM sessions, ERS was significantly larger in the SPM session than in the STIM session except for right 20 Hz ERS. This contrast is consistent with previous reports [6,7,20,21,25]. Houdayer et al. suggest that the magnitude of ERS depends on the type of afferent inputs [25]. Therefore, this difference in our data as for ERS magnitude can be explained by the inference that only cutaneous nerves are stimulated in the STIM session, whereas
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Fig. 10. %Change of 10 Hz frequency range in each subject (a) %increase of 10 Hz maximum enhancement and %decrease of 10 Hz maximum suppression in left and right sensorimotor areas in SPM sessions, (b) left %increase of 10 Hz maximum enhancement and %decrease of 10 Hz maximum suppression in both STIM and SPM sessions. Gray marks and lines show the group in which left prominent ERDs were observed in STIM session (S6, 7, 8).
both cutaneous and proprioceptive nerves are stimulated in the SPM session. ERS is considered to reflect the shift from an activated state to a deactivated state or inhibited cortical network [11,16]. Our results suggest that inhibition of the cortical network depends on the type of afferent inputs. On the other hand, with respect to ERD, there was no significant difference between the STIM and SPM sessions. The %change of 10 Hz ERD in the SPM session was comparable to that in the STIM session irrespective of the existence of left prominent 10 Hz ERD. The comparable ERD between two sessions suggests that sensory input induced cortical activation to the same extent as movement. We speculate that this same extent of ERD suggests the activation of neural networks common to
sensory and motor systems. As for the difference between ERD and ERS, Neuper and Pfurtscheller hypothesized that antagonistic ERD/ERS patterns, called ‘focal ERD/surround ERS’, may reflect a thalamocortical mechanism to enhance focal cortical activation by simultaneous inhibition of other cortical areas [16]. Our results that sensory inputs affected ERD and ERS differently can be explained by their hypothesis that ERD and ERS might correspond to the different physiological processes conducted in different cortical areas. ERD and ERS might reflect the activation of sensorimotor networks and the inhibition of the surrounding cortical areas, respectively. Gaetz et al. reported in their MEG study that neural networks in the primary motor cortex common to sensory and motor systems are activated during tactile stimulation [12]. They speculated based on this fact that sensorimotor cortical rhythms reflect higher order sensory control of movement. The presence of neural networks including both sensory and motor systems is supported by a previous stereoelectroencephalographic study which detected cortical rhythm in the primary somatosensory area in addition to that in the motor cortex during self-paced hand movement [11]. Our results also suggest that cortical rhythms are associated with the neural networks including both sensory and motor systems, and these rhythms may reflect the coordination of sensory and motor systems. In the present study, as the magnetic field decays rapidly over distance [37], the distance between the gradiometer and the brain sources could affect the detectability of MEG. Therefore, our record cannot exclude the possibility that the asymmetric distances to the gradiometer could affect the laterality of 10 Hz ERD among subjects. Other recording modalities which are not affected by distance, such as intracranial recording, would be useful for future analysis. Another issue is the stimulation intensity of digital nerve. To minimize the effect of proprioceptive sensation of the muscle tendon and the finger joint, we applied electrical stimulation to the digital nerve accompanying no movement. However, the current strength was set to three times the sensory threshold in this study. It might have also stimulated proprioceptive nerves of fingers to some extent and we cannot exclude the possibility that this activation of proprioceptive nerves affects the results. In conclusion, pure sensory input modulated bilateral rolandic oscillations at both 10 Hz and 20 Hz frequencies as well as self-paced movement. The new finding is that 10 Hz ERD showed the individual variability in the contra–ipsi patterns. ERDs in the STIM session, including these 10 Hz components, were comparable in amplitude to that in the SPM session. However, ERSs in the SPM session were larger than that in the STIM session. These findings might reflect the activation of neural networks common to sensory and motor systems followed by the inhibition of the surrounding cortical areas. Our results suggest that rolandic oscillations may reflect the coordination of sensory and motor systems in the neural networks including both sensory and motor systems. Conflict of interest None of the authors has any conflicts of interest in relation to this work. Acknowledgments We confirm that we have read the journal's position on issues involved in ethical publication and confirm that this report is consistent with those guidelines. This study was supported by a Grant-in-Aid for Scientific Research (C) 22500373 to TN.
Fig. 11. %Change of 20 Hz frequency range in each subject (a) %increase of 20 Hz maximum enhancement and %decrease of 20 Hz maximum suppression in left and right sensorimotor areas in SPM sessions, (b) left %increase of 20 Hz maximum enhancement and %decrease of 20 Hz maximum suppression in both STIM and SPM sessions. Gray marks and lines show the group in which left prominent ERDs were observed in STIM session (S6, 7, 8).
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The modulation of rolandic oscillation induced by digital nerve stimulation and self-paced movement of the finger: A MEG study Rei Enatsu a,1, Takashi Nagamine b,d,⁎, Jun Matsubayashi b, Hitoshi Maezawa b,c, Takayuki Kikuchi a,b, Hidenao Fukuyama b, Nobuhiro Mikuni a,e, Susumu Miyamoto a, Nobuo Hashimoto f a
Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto, Japan Human Brain Research Center, Kyoto University Graduate School of Medicine, Kyoto, Japan Department of Oral and Maxillofacial Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan d Department of Systems Neuroscience, Sapporo Medical University Graduate School of Medicine, Sapporo, Japan e Department of Neurosurgery, Sapporo Medical University Graduate School of Medicine, Sapporo, Japan f National Cerebral and Cardiovascular Center, Suita, Japan b c
a r t i c l e
i n f o
Article history: Received 22 June 2013 Received in revised form 27 November 2013 Accepted 4 December 2013 Available online 12 December 2013 Keywords: Event-related synchronization Event-related desynchronization Rolandic oscillation Temporal spectral evolution Magnetoencephalography Digital nerve
a b s t r a c t Background: The rolandic cortex exhibits spontaneous rhythmic activity. This oscillation can be modulated by somatosensory stimulation and voluntary movement. The purpose of this study is to elucidate the influence of sensory input on the rolandic oscillation in comparison with movement-related oscillation. Methods: Magnetic brain rhythms were recorded in nine healthy subjects in two sessions: electrical stimulation (STIM) of the digital nerve and self-paced movement (SPM) of the right index finger. Thereafter, 10 and 20 Hz oscillatory activities were compared between the two sessions with temporal spectral evolution analysis. Results: Sensory input altered the rolandic oscillations even under no movement conditions. As for 10 Hz ERD in the STIM session, three subjects showed a contralateral dominant pattern, whereas the remaining subjects showed a bilateral pattern. In spite of this individual variability, ERD showed comparable amplitude in both sessions. However, ERSs in the SPM session were larger than that in the STIM session. These findings might reflect the activation of neural networks common to sensory and motor systems followed by the inhibition of the other surrounding cortical areas. Conclusions: Our results suggest that rolandic oscillations may reflect the coordination of sensory and motor systems in the neural networks including both sensory and motor systems. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Gastaut reported that the human rolandic cortex exhibits rhythmic activity similar to the occipital area [1]. This oscillation was termed “rythme en arceau” and now is called mu rhythm owing to its archlike shape. This oscillation can be modulated by somatosensory stimulation and voluntary movement [1,2]. Electroencephalographic and magnetoencephalographic studies have revealed that this activity involves two main frequency bands: alpha bands centered at about 10 Hz and beta bands centered at about 20 Hz [3–8]. The 10 Hz and 20 Hz oscillations have been considered to originate in the postcentral gyrus and the anterior bank of the central sulcus, respectively, on the basis of magnetoencephalography (MEG) recordings [5–7,9,10]. On the other hand, several works have shown that both frequencies are
⁎ Corresponding author at: Department of Systems Neuroscience, School of Medicine, Sapporo Medical University, S1W17, Chuo-ku, Sapporo 060-8556, Japan. Tel.: +81 11 611 2111x2660; fax: +81 11 644 1020. E-mail address: [email protected] (T. Nagamine). 1 Current affiliation: Department of Neurosurgery, Himeji Medical Center, Himeji, Japan. 0022-510X/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jns.2013.12.011
observed in the same sensorimotor area with different modulation patterns [11–13]. These cortical oscillations have been interpreted as a readiness or idling state of the sensorimotor cortex [2,4,5,7,10,14]. Other studies reported that rolandic oscillation is modulated by attention [15–19]. The generator and functional meaning of these oscillations remain controversial. Knowledge of the characteristics of these oscillations can aid to elucidate the complicated system of sensory processing and motor control. Previous magnetoencephalographic studies reported that both 10 Hz and 20 Hz rolandic oscillations over the bilateral hemispheres are modulated by sensory input as well as by movement [6,7,20,21]; however, we should note the content of sensory stimuli in these previous reports. Their studies used electric stimulation of the median nerve with intensities exceeding the motor threshold. It was reported that passive movement induced somatosensory evoked magnetic fields (SEFs) [22] and modulated rolandic oscillation [23,24]. These reports suggest that proprioception could affect rolandic oscillations. In these studies of median nerve stimulation accompanied with movement, the effect of proprioceptive input derived from muscle tension could not be excluded. Although several previous studies tried to avoid this
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Fig. 1. Schematic depiction for temporal spectral evolution. The signals were filtered through a pass-band of interest, followed by rectification. Time-epochs of predetermined lengths (12 s in this paper) were specified taking event of interest (electric stimulation or EMG onset) as a trigger for averaging. Averages were conducted until the reasonable S/N ratio was obtained depending on the paradigm (about 80–100 trials).
effect [12,25], little information is available regarding the difference in contribution between pure sensory input and movement on the responses of rolandic oscillation. The purpose of this study is to elucidate the influence of sensory input and movement on the sensorimotor network. The rolandic oscillation induced by sensory input was compared with movementrelated oscillations, especially focusing on the laterality by using MEG, which has better temporospatial information than electroencephalography (EEG) [20,26]. To exclude the effect of afferent input from the muscle movement, we applied electrical stimulation to the digital nerve for sensory stimulation.
which ranged from 2.7 to 6.0 mA, and 100 stimuli were delivered in total.
2. Materials and methods
Magnetic brain signals were recorded inside a magnetically shielded room using a helmet-shaped whole-head coverage MEG system (VectorView system; Elekta Neuromag Ltd., Helsinki, Finland) [27]. In this study, signals recorded from 204 planar gradiometers were used for analysis because they provided an optimal signal-to-noise ratio for superficial current sources and showed the approximate location of cortical current sources as the largest signals seen immediately above generators. The magnetic field strengths were shown in units of femtotesla per centimeter (fT/cm), and this indication was included in each figure and table accordingly. Four head-position indicator coils were placed on the scalp and their locations with respect to the anatomical fiducial points (nasion, bilateral preauricular points) were determined with a three-dimensional digitizer (Polhemus Ltd., Colchester, VT, USA). Thereafter, the head shape of each subject was measured by checking evenly distributed points covering the whole scalp using a digitizer. In order to find the exact head position with respect to the sensors, a weak electrical current was applied to the coils and the resulting magnetic signals were measured just before each MEG measurement session. During the recording, finger movements were monitored by surface electromyography (EMG) of the bilateral extensor indicis proprius muscles. Electrooculography (EOG) was also recorded. The impedance of all electrodes was kept below 20 kΩ. Continuous data were acquired at a
2.1. Subjects Nine healthy right-handed subjects (aged 26–36 years old, eight men and one woman) were studied (S1-9). The informed consent was obtained before each experiment and all procedures were approved by the ethics committee of Kyoto University Graduate School and Faculty of Medicine. 2.2. Stimulation protocol The subjects sat in a chair in a magnetically shielded room with their forearm on a table. Magnetic brain signals were recorded with a whole head magnetometer under two conditions. 2.2.1. Electrical stimulation (STIM) of the right index finger During electrical stimulation, two ring electrodes were placed around the right index finger, one each on the proximal and distal interphalangeal joints, and stimuli were delivered with 0.3 ms constant current pulses once every 6 s with the proximal ring electrode acting as a cathode. Current strength was set to three times the sensory threshold,
2.2.2. Self-paced movement (SPM) of right index finger The subjects were asked to extend their right index finger for a short duration followed by free return at their own pace once about every 6 s. They continued movements until the number of repetitions reached around 80–100 times in one session. Each session took 8–10 min depending on the subject's weariness. 2.3. Data acquisition
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Fig. 2. Examples of 0.1–100 Hz, 10 Hz and 20 Hz filtered raw data along the left sensorimotor area in two subjects (subject 1 (S1) and subject 6 (S6)). Selected sensor is shown as a filled circle in the sensor array. STIM: electrical stimulation, TRIG: stimulation trigger, SPM: self-paced movement, EMG: electromyography.
sampling rate of 303 Hz for all signals with a band-pass filter of 0.1 to 100 Hz for MEG, EOG and 10 to 100 Hz for EMG.
followed by rectification and averaging over about 80–100 trials with respect to the onset of each STIM or SPM session (Fig. 1). The averaged signal was smoothed with a 10 Hz low-pass filter.
2.4. Temporal spectral evolution analysis 2.5. Data analysis Signals were analyzed off-line to obtain precise trigger timing for averaging from the rectified EMG. From continuous MEG raw data, epochs from 6 s before stimulation onset to 6 s after onset were collected for the STIM sessions. Epochs from 6 s before EMG onset to 6 s after onset were collected for the SPM sessions. Signals were reviewed visually, and epochs including eye movement artifacts, ambiguous EMG bursts, or other artifacts were omitted from the averaging. Temporal spectral evolution (TSE) analysis [6,7] was adopted to calculate the average amplitude level of 10 and 20 Hz activities related to a certain event as a function time. This method demonstrates eventrelated but not necessarily phase-locked changes of the averaged amplitude level of oscillatory activities in a given pass-band. In our study, the signals were filtered through a pass-band around 10 Hz and 20 Hz
In our study, the signals were filtered through a pass-band of 8–13 Hz for 10 Hz signal and of 18–23 Hz for 20 Hz signal. Considering that the signals from planar gradiometers are strongest when the sensors are located just above local cerebral sources, we used the data from the most reactive sensor that showed the largest amplitude difference between maximum suppression and maximum enhancement in each hemisphere to quantify the modulation of the rolandic rhythms. Event-related desynchronization (ERD) and event-related synchronization (ERS) were defined as a time-locked decrease and increase in amplitude of ongoing rhythmic activities from the baseline period, respectively [4,28]. TSE amplitudes of 10 Hz and 20 Hz activities in these sessions were analyzed using the mean value of the period
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between −10 ms and +10 ms to the time of maximal suppression and enhancement. For statistical analysis, the percentages of the decrement (Dmax) and increment (Imax) of the TSE amplitude at these two time points were evaluated with respect to that during the baseline period. Their latencies were defined as when minimum (Dmax latency) and maximum (Imax latency) values were reached, respectively [9,10]. The prestimulus 200 ms (from −200 to 0 ms) and 200 ms periods 3 s preceding movement onset (−3100 ms to −2900 ms) were adopted as the baseline period for STIM sessions and SPM sessions, respectively. Maximum suppression and enhancement with changes larger than 2 times standard deviation (2 S.D.) of baseline period were accepted for further analysis in this study. For comparison of the percentage change (left vs right, STIM session vs SPM session), the Wilcoxon signed rank test was used. For statistical analysis, PASW (PASW statistics 17.0; SPSS Inc., Chicago) was used and P b 0.05 was regarded as significant. 3. Results 3.1. Oscillatory changes in STIM session As seen in the examples of non-filtered raw data taken from the left sensorimotor area in two subjects (S1 and S6), amplitude fluctuation of oscillatory activity was observed in both the STIM and SPM sessions. They were more clearly manifested by application of a bandpass frequency filter of 10 Hz (8–13 Hz) and 20 Hz (18–23 Hz) (Fig. 2). In the STIM session of one subject (S6), TSE analysis identified one focal reactive area in each hemisphere in both 10 Hz and 20 Hz components (Fig. 3). In the left hemisphere, the amplitude of the 10 Hz component started to decrease after electrical stimulation and reached maximum suppression 330 ms after onset; thereafter, the amplitude increased and reached the maximum enhancement at 1480 ms. In the right hemisphere, the amplitude of the 10 Hz component slightly
decreased by 15% from the baseline level at 190 ms after stimulation. The amplitude increased up to the maximum at 580 ms. In the 20 Hz component, the amplitude started to decrease after stimulus onset over the bilateral hemispheres and increased amplitude followed in the same areas as those of the 10 Hz component. In the left hemisphere, the amplitude decreased by 20% from the baseline level at 250 ms; thereafter, it started to increase and reached maximum enhancement 480 ms after stimulation. Over the right hemisphere, the decrease of amplitude was 8% from the baseline level and the maximum suppression was seen 270 ms after stimulation. The amplitude increased to the maximum enhancement at 600 ms. All of the subjects showed two focal reactive areas for the 10 Hz component, one in each hemisphere (Fig. 4). These time-locked amplitude decrements of ongoing rhythmic activity were accepted as ERD. Two subjects (S1, S3) did not show any traceable amplitude decrease larger than 2 S.D. from the baseline in the left and right hemispheres, and they showed an amplitude increase immediately after stimulus onset; therefore, we excluded these subjects from the statistical analysis of 10 Hz maximum suppression. The time-locked amplitude increases of ongoing rhythm were accepted as ERS. With respect to 20 Hz, two focal reactive areas were identified in all subjects and each hemisphere had one reactive area similar to that at 10 Hz (Fig. 5). In three hemispheres of three subjects, since the amplitude decrease was smaller than 2 S.D. from the baseline and ERS was observed immediately after stimulus onset without showing ERD (left side in S1 and S2, right side in S5), we excluded these three hemispheres from the statistical analysis of 20 Hz maximum suppression. 3.2. STIM session With respect to 10 Hz oscillatory change, Dmax ranged 2–62% (median: 9%) and 3–18% (median: 8%) in left and right sensorimotor
Fig. 3. TSE analysis of STIM session in one subject (S6). Clear responses were observed in both the 10 Hz and 20 Hz frequency ranges, and were found to concentrate around the bilateral sensorimotor area. Single plus: maximum suppression, double plus: maximum enhancement. Lt: left, Rt: right.
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Fig. 4. 10 Hz TSE analysis of STIM session in bilateral sensorimotor areas of all subjects. The prestimulus 200 ms (from −200 to 0) was adopted as the baseline for STIM session. The percentage decrement and increment of TSE amplitude from the mean amplitude of the baseline periods were used for %decrease of maximum suppression (%dec) and %increase of maximum enhancement (%inc), respectively. Single plus: maximum suppression, double plus: maximum enhancement.
areas, respectively. Imax ranged 7–42% (median: 17%) and 7–38% (median: 20%) in left and right sensorimotor areas, respectively (Fig. 6). Dmax latencies ranged 270–460 ms (median: 340 ms) and 90–540 ms (median: 340 ms), in the left and right hemispheres, respectively (Fig. 7). Imax latencies of left and right hemispheres ranged 160–2080 ms (median: 1190 ms) and 340–1750 ms (median: 1080 ms), respectively. With respect to the 20 Hz component, Dmax ranged 9–30% (median: 17%) and 2–20% (median: 12%) in left and right sensorimotor areas, respectively. 20 Hz Imax ranged 9–56% (median: 27%) and 7–48% (median: 27%) in left and right sensorimotor areas, respectively (Fig. 6). Dmax latencies of left and right hemispheres ranged 230–680 ms (median: 310 ms) and 60–440 ms (median: 300 ms), respectively (Fig. 7). Imax latencies of left and
right hemispheres ranged 480–1910 ms (median: 750 ms) and 520–1720 ms (median: 710 ms), respectively. The comparison of 10 Hz ERD between the sides showed wide individual variability in the contra–ipsi patterns. In three subjects (S6, 7, 8), 10 Hz ERDs showed apparent laterality, manifested as Dmax greater over the left hemisphere exceeding 30% (Fig. 6). In another four subjects (S2, 4, 5, 9), bilateral 10 Hz ERDs were comparable in size and Dmax was smaller than 30%. The differences in Dmax between left and right ranged 27–54% in the former three subjects and 3–9% in the remaining subjects. As for statistical analysis of 10 Hz Dmax between sides using all 7 subjects, there was no significant difference as a group. On the other hand, with respect to 10 Hz ERS, the amplitude differences between left and right were not prominent, even in subjects with prominent left 10 Hz ERD. Imax was not statistically different between the
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Fig. 5. 20 Hz TSE analysis of STIM session in bilateral sensorimotor areas of all subjects. The prestimulus 200 ms (−200 to 0) was adopted as the baseline for electrical stimulation session. Single plus: maximum suppression, double plus: maximum enhancement.
sides. With respect to the 20 Hz component, none of the subjects showed clear laterality of oscillatory change in both ERD and ERS, even in the three subjects showing prominent left 10 Hz ERD (Fig. 6). In 20 Hz components, there was no statistically significant difference between left and right sides in both Dmax and Imax. With respect to Dmax latencies and Imax latencies, there was no significant difference between left and right sides in both 10 and 20 Hz frequency ranges (Fig. 7). 3.3. SPM session With respect to the 10 Hz component in the SPM session, each hemisphere had one focal reactive area around the sensorimotor, similarly to the STIM session (Fig. 8). Dmax ranged 7–62% (median: 22%) and 7–51% (median: 22%) in left and right sensorimotor areas,
respectively (Fig. 8, 10a). Imax ranged 15–75% (median: 22%) and 11–138% (median: 28%) in left and right sensorimotor areas, respectively. Dmax latencies ranged from −372 to 633 ms (median: 57 ms) in the left hemisphere and from − 299 to 538 ms (median: 292 ms) in the right hemispheres. Imax latencies of left and right hemispheres ranged 137–2779 ms (median: 1576 ms) and 217–2838 ms (median: 1037 ms), respectively. Similarly, in the 20 Hz component, each hemisphere had one focal reactive area around the sensorimotor area in the SPM session (Fig. 9). All of the subjects showed both ERD and ERS of 20 Hz in bilateral sensorimotor areas except for ERD in the right hemisphere of one subject (S5). With respect to the 20 Hz component, Dmax ranged 3–51% (median: 28%) and 7–24% (median: 17%) in left and right sensorimotor areas, respectively (Figs. 9, 11a). 20 Hz Imax ranged 6–116% (median: 61%) and 8–117% (median: 44%) in left and right
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3.4. Comparison between STIM and SPM
Fig. 6. Percentage change of TSE amplitudes of maximum suppression and enhancement from the baseline period in 10 and 20 Hz frequency ranges in STIM session. Gray marks and lines show the group in which left prominent ERDs were observed (S6, 7, 8).
sensorimotor areas, respectively. Dmax latencies of left and right hemispheres ranged from − 249 to 317 ms (median: 130 ms) and from − 152 to 580 ms (median: 301 ms), respectively. Imax latencies of left and right hemispheres ranged 486–2528 ms (median: 1255 ms) and 186–2061 ms (median: 936 ms), respectively. As for laterality of 10 Hz Dmax, only one subject (S6) showed clear laterality with a difference between left and right hemispheres larger than 20%. This difference was not significant in the statistical analysis of all subjects as a whole (Fig. 10a). In the comparison of 10 Hz Imax between left and right, three subjects showed differences larger than 20%. However, since two subjects (S5, S9) demonstrated right dominance (26%, 84%) and the other subject (S3) showed left dominance pattern (35%), no consistent tendency was observed. With respect to 20 Hz Dmax, the left side was larger than the right with the difference larger than 20% in three subjects (S4, 6, 8) (Fig. 11a). However this difference was not statistically significant. With respect to 20 Hz Imax in the SPM session, consistent laterality was not observed and there was no significant difference between sides.
As seen in Fig. 10b, in the comparison of left 10 Hz Dmax between STIM and SPM sessions, there was no significant difference between the sessions. This tendency of no significant difference was also applicable to the three subjects (S6, 7, 8) whose ERD was prominent in the STIM session. The left 10 Hz Imax was larger in the SPM session in seven (S1, 3, 4, 5, 6, 8, 9) of nine subjects than in the STIM session and this difference was significant as a group (n = 9, P = 0.02) (Fig. 10b). Right 10 Hz Dmax was larger in the SPM session than in the STIM session in six (S2, 4, 5, 6, 7, 8) of seven subjects; however, this difference was not statistically significant. Right 10 Hz Imax was larger in the SPM session than in the STIM session in eight subjects (S1, 2, 3, 4, 5, 6, 8, 9) and this difference was statistically significant (n = 9, P = 0.03). In the comparison of left 20 Hz Dmax between STIM and SPM sessions, it was larger in the SPM session than in the STIM session in five (S3, 4, 6, 8, 9) of seven subjects (Fig. 11b). However, this difference was not statistically significant as a group. Left 20 Hz Imax was larger in the SPM session than in the STIM session in seven subjects (S2, 3, 4, 5, 6, 8, 9) and smaller in two subjects (S1, 7), and statistical analysis showed that it was significantly larger in the SPM session as a group (n = 9, P = 0.02) (Fig. 11b). Right 20 Hz Dmax was larger in the SPM session than in the STIM session in six (S1, 2, 3, 6, 7, 9) of eight subjects and smaller in two subjects (S4, 8). Right 20 Hz Imax was larger in the SPM session than in the STIM session in six (S3, 4, 5, 6, 8, 9) of nine subjects. These %changes over the right hemisphere did not show any significant differences between the two sessions. In the three subjects (S6, 7, 8) with prominent left 10 Hz ERD in both STIM and SPM sessions, 20 Hz ERDs did not display this prominent change in either STIM or SPM sessions (Figs. 10, 11).
4. Discussion We found that sensory input accompanying no movement can modulate rolandic oscillations in both 10 Hz and 20 Hz frequency ranges over the bilateral hemispheres. This finding is consistent with previous studies [12,13]. Although there was no significant laterality as a whole for both ERD and ERS in 10 Hz and 20 Hz in the STIM session, 10 Hz
Fig. 7. The latency of maximum suppression and enhancement in 10 and 20 Hz frequency ranges in STIM session. Max Sup: maximum suppression, Max Enh: maximum enhancement.
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Fig. 8. 10 Hz TSE analysis of SPM session in bilateral sensorimotor areas of all subjects. The 200 ms periods 3 s preceding movement onset (−3100 ms to −2900 ms) was adopted as the baseline period for self-paced movement session. Single plus: maximum suppression, double plus: maximum enhancement.
ERD showed wide individual variability of laterality in the STIM session. ERDs in the STIM session, including these 10 Hz components, were comparable in amplitude to that in the SPM session. However, ERSs in the SPM session were larger than that in the STIM session. As for bilateral distribution, previous MEG studies have dealt with this using sensory evoked field (SEF) [29,30] and rolandic oscillations [6,7,9,10,20,21,26]. A previous MEG study in humans reported that SEF produced by median nerve stimulation was enhanced by cutaneous information given to the other hand [31]. Regarding this bilateral influence from the periphery, although transcallosal connections between the two hemispheres were previously reported in human [32,33] as well as nonhuman primates [34], uncrossed projections from body parts to the sensory cortex have not been identified either in human or non-human primates [35]. Therefore, it is reasonable to estimate that the bilateral
distribution of oscillatory change in our results was conveyed through the transcallosal communication between the two hemispheres. However, Dmax latencies and Imax latencies ranged 90–540 ms and 160–2080 ms, respectively and these latencies were too late for direct afferent input. Furthermore, latencies for Imax/Dmax in the left side were not always earlier than those for the right side. All these findings cannot be explained by the direct input to primary somatosensory cortex (SI). Therefore, it might reflect the indirect secondary processing. In addition to this documentation for alternation of SI activities, it has been also reported that both alpha and beta frequency oscillatory activities are altered in the bilateral secondary somatosensory cortex (SII) by electrical stimulations [36]. Della Penna et al. applied an inverse operator to the raw field distribution over the helmet and estimated waveforms originating from SI and SII [36]. By this way, they were
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Fig. 9. 20 Hz TSE analysis of SPM session in bilateral sensorimotor areas of all subjects. The 200 ms periods 3 s preceding movement onset (−3100 ms to −2900 ms) was adopted as the baseline period for self-paced movement session. Single plus: maximum suppression, double plus: maximum enhancement.
able to separate activities between SI and SII. With respect to their estimated SII oscillation, the latencies of maximum ERD and ERS were observed at approximately 430 ms and 1140 ms after the stimuli respectively. These latencies of maximum ERD and ERS coincided with our results, hence the bilateral oscillatory changes in our study might also be associated with bilateral SII activity as well as SI activity. In our results in the STIM session, 10 Hz ERD showed the wide individual variability in the contra–ipsi patterns; 10 Hz ERD was predominant on the contralateral side in three subjects and showed a similar amplitude in the remaining subjects. Previous studies speculated that ERD is likely to correspond to cortical activation [11,15,16]. Taking these previous reports into account, the wide range of 10 Hz ERD observed in the present results might reflect various extent of cortical
activation induced by sensory input, which varies depending on individual. This study has not elucidated the functional significance of 10 Hz ERD on sensory processing and motor control. This could be elucidated if we could specify the difference related to sensory processing or motor control in groups with and without prominent left 10 Hz ERD. It would be an interesting consideration for the future studies. In the comparison of oscillatory changes between STIM and SPM sessions, ERS was significantly larger in the SPM session than in the STIM session except for right 20 Hz ERS. This contrast is consistent with previous reports [6,7,20,21,25]. Houdayer et al. suggest that the magnitude of ERS depends on the type of afferent inputs [25]. Therefore, this difference in our data as for ERS magnitude can be explained by the inference that only cutaneous nerves are stimulated in the STIM session, whereas
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Fig. 10. %Change of 10 Hz frequency range in each subject (a) %increase of 10 Hz maximum enhancement and %decrease of 10 Hz maximum suppression in left and right sensorimotor areas in SPM sessions, (b) left %increase of 10 Hz maximum enhancement and %decrease of 10 Hz maximum suppression in both STIM and SPM sessions. Gray marks and lines show the group in which left prominent ERDs were observed in STIM session (S6, 7, 8).
both cutaneous and proprioceptive nerves are stimulated in the SPM session. ERS is considered to reflect the shift from an activated state to a deactivated state or inhibited cortical network [11,16]. Our results suggest that inhibition of the cortical network depends on the type of afferent inputs. On the other hand, with respect to ERD, there was no significant difference between the STIM and SPM sessions. The %change of 10 Hz ERD in the SPM session was comparable to that in the STIM session irrespective of the existence of left prominent 10 Hz ERD. The comparable ERD between two sessions suggests that sensory input induced cortical activation to the same extent as movement. We speculate that this same extent of ERD suggests the activation of neural networks common to
sensory and motor systems. As for the difference between ERD and ERS, Neuper and Pfurtscheller hypothesized that antagonistic ERD/ERS patterns, called ‘focal ERD/surround ERS’, may reflect a thalamocortical mechanism to enhance focal cortical activation by simultaneous inhibition of other cortical areas [16]. Our results that sensory inputs affected ERD and ERS differently can be explained by their hypothesis that ERD and ERS might correspond to the different physiological processes conducted in different cortical areas. ERD and ERS might reflect the activation of sensorimotor networks and the inhibition of the surrounding cortical areas, respectively. Gaetz et al. reported in their MEG study that neural networks in the primary motor cortex common to sensory and motor systems are activated during tactile stimulation [12]. They speculated based on this fact that sensorimotor cortical rhythms reflect higher order sensory control of movement. The presence of neural networks including both sensory and motor systems is supported by a previous stereoelectroencephalographic study which detected cortical rhythm in the primary somatosensory area in addition to that in the motor cortex during self-paced hand movement [11]. Our results also suggest that cortical rhythms are associated with the neural networks including both sensory and motor systems, and these rhythms may reflect the coordination of sensory and motor systems. In the present study, as the magnetic field decays rapidly over distance [37], the distance between the gradiometer and the brain sources could affect the detectability of MEG. Therefore, our record cannot exclude the possibility that the asymmetric distances to the gradiometer could affect the laterality of 10 Hz ERD among subjects. Other recording modalities which are not affected by distance, such as intracranial recording, would be useful for future analysis. Another issue is the stimulation intensity of digital nerve. To minimize the effect of proprioceptive sensation of the muscle tendon and the finger joint, we applied electrical stimulation to the digital nerve accompanying no movement. However, the current strength was set to three times the sensory threshold in this study. It might have also stimulated proprioceptive nerves of fingers to some extent and we cannot exclude the possibility that this activation of proprioceptive nerves affects the results. In conclusion, pure sensory input modulated bilateral rolandic oscillations at both 10 Hz and 20 Hz frequencies as well as self-paced movement. The new finding is that 10 Hz ERD showed the individual variability in the contra–ipsi patterns. ERDs in the STIM session, including these 10 Hz components, were comparable in amplitude to that in the SPM session. However, ERSs in the SPM session were larger than that in the STIM session. These findings might reflect the activation of neural networks common to sensory and motor systems followed by the inhibition of the surrounding cortical areas. Our results suggest that rolandic oscillations may reflect the coordination of sensory and motor systems in the neural networks including both sensory and motor systems. Conflict of interest None of the authors has any conflicts of interest in relation to this work. Acknowledgments We confirm that we have read the journal's position on issues involved in ethical publication and confirm that this report is consistent with those guidelines. This study was supported by a Grant-in-Aid for Scientific Research (C) 22500373 to TN.
Fig. 11. %Change of 20 Hz frequency range in each subject (a) %increase of 20 Hz maximum enhancement and %decrease of 20 Hz maximum suppression in left and right sensorimotor areas in SPM sessions, (b) left %increase of 20 Hz maximum enhancement and %decrease of 20 Hz maximum suppression in both STIM and SPM sessions. Gray marks and lines show the group in which left prominent ERDs were observed in STIM session (S6, 7, 8).
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