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Spatiotemporal distributions of brain oscillation during silent reading
International Congress Series 1232 (2002) 35 – 39
Spatiotemporal distributions of brain oscillation during silent reading Masayuki Hirata, Amami Kato, Hirotomo Ninomiya, Masaaki Taniguchi, Haruhiko Kishima, Toshiki Yoshimine * Department of Neurosurgery, Osaka University Graduate School of Medicine, E6 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan
Abstract The purpose of this study is to demonstrate the spatiotemporal distributions of event-related desynchronization (ERD) and synchronization (ERS) during silent reading. One hundred of threecharacter hiragana semantic words were presented serially on a liquid crystal monitor for 3 s, and with intervals of 3 s. Six healthy right-handed subjects were instructed to read them without phonation. The data were measured using whole-head type magnetometer. The current sources were estimated spatiotemporally by synthetic aperture magnetometry (SAM). Changes in the source power between the active state and the control state were analyzed statistically with Student’s t values. ERD and ERS were distributed multifocally over both hemispheres including classically language-related regions, and lateralized to the left hemisphere. ERSs tended to be distributed serially from the occipital region via the parieto-temporal region to the frontal region. ERDs tended to be distributed multifocally in parallel. Both serial and parallel processings are suggested to be involved in the silent reading. Spatiotemporal distributions and frequency bands of ERD definitely differed from those of ERS. ERS and ERD might reflect the excitation and inhibition of different Hebbian cell assemblies. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Brain oscillation; Desynchronization; Synchronization; Synthetic aperture magnetometry; Language
*
Corresponding author. Tel.: +81-6-6879-3652; fax: +81-6-6879-3659. E-mail addresses: [email protected] (M. Hirata), [email protected] (T. Yoshimine). 0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 7 9 8 - 1
36
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
1. Introduction Event-related desynchronization (ERD) represents an attenuation of the oscillation amplitude of a specific frequency that occurs in relation to specific neural activity [1]. The opposite phenomenon, event-related synchronization (ERS), is an increase in that amplitude [2]. Several previous studies using magnetoencephalography (MEG) demonstrated that brain oscillatory changes in high-frequency bands in the left hemisphere during lexical processing [3– 5]. However, the spatiotemporal distributions of these oscillatory changes have not previously been reported. Thus, we introduced a novel method, synthetic aperture magnetometry (SAM) [9], to investigate the frequency-dependent spatiotemporal distribution of the change of brain oscillation during silent reading on the individual MR images. SAM is one of the statistical spatial filtering methods using an adaptive beamformer, analogous to the technique, which obtains the high spatial selectivity from radio antenna arrays [6– 9].
2. Materials and methods 2.1. Data acquisition Six healthy right-handed male subjects participated in this study. During the experiment, each subject with their eyes open sat in a comfortable chair in a magnetically shielded room. One hundred of three-character Japanese hiragana semantic words were presented serially on a liquid crystal monitor for 3 s with an interval of 3 s. The subjects were instructed to read them only once without phonation immediately after each word was presented. The data were recorded with a 64-channel whole-head MEG system equipped with third-order SQUID gradiometers (Whole-Head SQUID System Model 100, CTF Systems) [10]. MEG signals were digitized at a sampling rate of 625 Hz and filtered with a 200-Hz on-line, low pass filter. Notch filters were used at 60 and 120 Hz to eliminate AC line noise. The data of a 5000-ms duration with a 2500-ms pre-stimulus interval were collected for each of the 100 trials. At the beginning and end of each measurement, the subject’s head position was registered with localization coils placed at the nasion and the bilateral preauricular points. For each subject, magnetic resonance (MR) images were obtained with a 1.0 T MRI system in a T1-weighted sequence of 130 sagittal slices (1.5-mm thickness) with fiducial skin markers at the nasion and bilateral preauricular points. By registration of the head position at these three points, the MEG data can be superimposed on the individual MR images with anatomical accuracy within a few millimeters [6]. 2.2. SAM analysis The MEG data were subjected to each of the following bandpass filters: alpha (8– 13 Hz), beta (13 –25 Hz), low frequency gamma (25 –50 Hz) and high-frequency gamma (50 – 100 Hz). The region of interest (ROI) was set to include the whole brain with a 5mm voxel resolution. The signal power of each voxel was estimated by SAM [7].
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
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Fig. 1. SAM statistical images of silent reading. Left: ERS in 50 – 100 Hz was demonstrated around the bilateral calcaline sulcus in 50 – 150 ms. Right: ERS in 13 – 25 Hz was demonstrated in left angular gyrus in 400 – 800 ms.
Fig. 2. Temporal profile of silent reading. ERSs tended to be distributed serially from occipital region via parietotemporal region to frontal region. ERDs tended to be distributed multifocally in parallel.
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M. Hirata et al. / International Congress Series 1232 (2002) 35–39
Changes in the signal power for each voxel between the active state (0 to 2500 ms after stimulus) and the control state (2500 to 0 ms before stimulus) were analyzed statistically with Student’s t values. The distribution of t values was displayed on the individual MR images.
3. Results ERD and ERS were distributed multifocally over both hemispheres including classically language-related regions, lateralized to the left hemisphere. The bilateral medial occipital region around calcaline sulcus showed ERD in the 8– 50 Hz and ERS in the 50– 100 Hz (Fig. 1). The left temporo-parieto-occipital region, the left inferior frontal region showed ERD or ERS in the 13 – 50 Hz (Fig. 1). The left middle frontal region showed ERD in the 25 – 50 Hz. Spatiotemporal distributions and frequency bands of ERD and ERS were definitely different with each other (Fig. 2). ERSs tended to be distributed serially from occipital region via parieto-temporal region to frontal region. ERDs tended to be distributed multifocally in parallel.
4. Discussion Gamma-band neuronal activity has been proposed to reflect higher cognitive processes such as attention, perception and language processing [3– 5]. Pulvermu¨ller et al. demonstrated the oscillatory change in the low gamma band in the left hemisphere during the lexical decision task [11]. However, the spatiotemporal distribution of such frequencydependent neuronal activity related to cognitive processes is still unknown. Thus, we introduced a novel method, synthetic aperture magnetometry (SAM) [6]. SAM is one of the statistical spatial filtering methods using an adaptive beamformer, analogous to the technique, which obtains the high spatial selectivity from the radio antenna arrays [6 –9]. Using SAM, we demonstrated the spatiotemporal distribution and frequency bands of the ERD and ERS during the silent reading. ERD and ERS were distributed multifocally over both hemispheres but lateralized to the left hemisphere including the area related to lexical and cognitive processing. The ERS or ERD in the beta and low gamma band was demonstrated in the left middle frontal region, the left inferior frontal region and the left temporo-parieto-occipital region, which may reflect lexical and cognitive processing. The ERS in the high gamma band was demonstrated in the bilateral medial occipital region around calcaline, which may reflect the primary visual processing. The previous study also demonstrated the ERS in the high gamma band in the primary somatosensory area following somatosensory stimulation [12]. Another important finding is temporal distribution of ERS and ERD during the silent reading. ERSs tended to be distributed serially from the occipital region via the parieto-temporal region to the frontal region, whereas ERDs tended to be distributed multifocally in parallel. These results suggest that both serial and parallel processings are involved in silent reading. Spatiotemporal distributions and frequency bands of ERD differ definitely from those of ERS. This difference in the spatiotemporal distributions of ERS and ERD may support our hypothesis that the neural
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
39
mechanisms for ERS and ERD differ, reflecting responses of different cell assemblies related to specific neural functions rather than a frequency shift of the same cell assembly.
Acknowledgements This work was supported in part by a Grant-in-Aid for Scientific Research (11470290) from the Japanese Ministry of Education, Science and Culture.
References [1] G. Pfurtsheller, A. Aranbar, Electroencephalogr. Clin. Neurophysiol. 2 (1977) 817 – 826. [2] G. Pfurtsheller, Electroencephalogr. Clin. Neurophysiol. 83 (1992) 62 – 69. [3] F. Pulvermu¨ller, W. Lutzenberger, H. Preißl, N. Birbaumer, Spectrum responses in the gamma-band: physiological signs of higher cognitive processes? NeuroReport 6 (1995) 2059 – 2064. [4] F. Pulvermu¨ller, C. Eulitz, C. Pantev, B. Mohr, B. Feige, W. Lutzenberger, T. Elbert, N. Birbaumer, Highfrequency cortical responses reflect lexical processing: an MEG study, Electroencephalogr. Clin. Neurophysiol. 98 (1996) 76 – 85. [5] C. Eulitz, B. Maess, C. Pantev, A.D. Friderci, B. Feige, T. Elbert, Oscillatory neuromagnetic activity induced by language and non-language stimuli, Cognit. Brain Res. 4 (1996) 121 – 132. [6] M. Taniguchi, A. Kato, N. Fujita, et al., NeuroImage 12 (2000) 298 – 306. [7] S.E. Robinson, J. Vrba, Functional neuroimaging by synthetic aperture magnetometry (SAM), in: T. Kotani, M. Kotani, S. Kuriki, et al. (Eds.), Recent Advances in Biomagnetism, Tohoku University Press, Sendai, 1999, pp. 302 – 305. [8] R. Ishii, K. Shinosaki, S. Ukai, et al., NeuroReport 10 (1999) 675 – 679. [9] R. Ishii, K. Shinosaki, Y. Ikejiri, et al., NeuroReport 11 (2000) 3283 – 3287. [10] M. Taniguchi, T. Yoshimine, M. Hirata, et al., NeuroReport 9 (1998) 1497 – 1502. [11] F. Pulvermu¨ller, N. Birbaumer, W. Lutzenberger, B. Mohr, High-frequency cortical responses reflect lexical processing: an MEG study, Prog. Neurobiol. 52 (1997) 427 – 445. [12] M. Hirata, A. Kato, M. Taniguchi, H. Ninomiya, D. Cheyne, S.E. Robinson, M. Maruno, E. Kumura, R. Ishii, N. Hirabuki, H. Nakamura, T. Yoshimine, Frequency-dependent spatial distribution of human somatosensory evoked neuromagnetic fields. Neuroscience Letter (in press).
Spatiotemporal distributions of brain oscillation during silent reading Masayuki Hirata, Amami Kato, Hirotomo Ninomiya, Masaaki Taniguchi, Haruhiko Kishima, Toshiki Yoshimine * Department of Neurosurgery, Osaka University Graduate School of Medicine, E6 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan
Abstract The purpose of this study is to demonstrate the spatiotemporal distributions of event-related desynchronization (ERD) and synchronization (ERS) during silent reading. One hundred of threecharacter hiragana semantic words were presented serially on a liquid crystal monitor for 3 s, and with intervals of 3 s. Six healthy right-handed subjects were instructed to read them without phonation. The data were measured using whole-head type magnetometer. The current sources were estimated spatiotemporally by synthetic aperture magnetometry (SAM). Changes in the source power between the active state and the control state were analyzed statistically with Student’s t values. ERD and ERS were distributed multifocally over both hemispheres including classically language-related regions, and lateralized to the left hemisphere. ERSs tended to be distributed serially from the occipital region via the parieto-temporal region to the frontal region. ERDs tended to be distributed multifocally in parallel. Both serial and parallel processings are suggested to be involved in the silent reading. Spatiotemporal distributions and frequency bands of ERD definitely differed from those of ERS. ERS and ERD might reflect the excitation and inhibition of different Hebbian cell assemblies. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Brain oscillation; Desynchronization; Synchronization; Synthetic aperture magnetometry; Language
*
Corresponding author. Tel.: +81-6-6879-3652; fax: +81-6-6879-3659. E-mail addresses: [email protected] (M. Hirata), [email protected] (T. Yoshimine). 0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 7 9 8 - 1
36
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
1. Introduction Event-related desynchronization (ERD) represents an attenuation of the oscillation amplitude of a specific frequency that occurs in relation to specific neural activity [1]. The opposite phenomenon, event-related synchronization (ERS), is an increase in that amplitude [2]. Several previous studies using magnetoencephalography (MEG) demonstrated that brain oscillatory changes in high-frequency bands in the left hemisphere during lexical processing [3– 5]. However, the spatiotemporal distributions of these oscillatory changes have not previously been reported. Thus, we introduced a novel method, synthetic aperture magnetometry (SAM) [9], to investigate the frequency-dependent spatiotemporal distribution of the change of brain oscillation during silent reading on the individual MR images. SAM is one of the statistical spatial filtering methods using an adaptive beamformer, analogous to the technique, which obtains the high spatial selectivity from radio antenna arrays [6– 9].
2. Materials and methods 2.1. Data acquisition Six healthy right-handed male subjects participated in this study. During the experiment, each subject with their eyes open sat in a comfortable chair in a magnetically shielded room. One hundred of three-character Japanese hiragana semantic words were presented serially on a liquid crystal monitor for 3 s with an interval of 3 s. The subjects were instructed to read them only once without phonation immediately after each word was presented. The data were recorded with a 64-channel whole-head MEG system equipped with third-order SQUID gradiometers (Whole-Head SQUID System Model 100, CTF Systems) [10]. MEG signals were digitized at a sampling rate of 625 Hz and filtered with a 200-Hz on-line, low pass filter. Notch filters were used at 60 and 120 Hz to eliminate AC line noise. The data of a 5000-ms duration with a 2500-ms pre-stimulus interval were collected for each of the 100 trials. At the beginning and end of each measurement, the subject’s head position was registered with localization coils placed at the nasion and the bilateral preauricular points. For each subject, magnetic resonance (MR) images were obtained with a 1.0 T MRI system in a T1-weighted sequence of 130 sagittal slices (1.5-mm thickness) with fiducial skin markers at the nasion and bilateral preauricular points. By registration of the head position at these three points, the MEG data can be superimposed on the individual MR images with anatomical accuracy within a few millimeters [6]. 2.2. SAM analysis The MEG data were subjected to each of the following bandpass filters: alpha (8– 13 Hz), beta (13 –25 Hz), low frequency gamma (25 –50 Hz) and high-frequency gamma (50 – 100 Hz). The region of interest (ROI) was set to include the whole brain with a 5mm voxel resolution. The signal power of each voxel was estimated by SAM [7].
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
37
Fig. 1. SAM statistical images of silent reading. Left: ERS in 50 – 100 Hz was demonstrated around the bilateral calcaline sulcus in 50 – 150 ms. Right: ERS in 13 – 25 Hz was demonstrated in left angular gyrus in 400 – 800 ms.
Fig. 2. Temporal profile of silent reading. ERSs tended to be distributed serially from occipital region via parietotemporal region to frontal region. ERDs tended to be distributed multifocally in parallel.
38
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
Changes in the signal power for each voxel between the active state (0 to 2500 ms after stimulus) and the control state (2500 to 0 ms before stimulus) were analyzed statistically with Student’s t values. The distribution of t values was displayed on the individual MR images.
3. Results ERD and ERS were distributed multifocally over both hemispheres including classically language-related regions, lateralized to the left hemisphere. The bilateral medial occipital region around calcaline sulcus showed ERD in the 8– 50 Hz and ERS in the 50– 100 Hz (Fig. 1). The left temporo-parieto-occipital region, the left inferior frontal region showed ERD or ERS in the 13 – 50 Hz (Fig. 1). The left middle frontal region showed ERD in the 25 – 50 Hz. Spatiotemporal distributions and frequency bands of ERD and ERS were definitely different with each other (Fig. 2). ERSs tended to be distributed serially from occipital region via parieto-temporal region to frontal region. ERDs tended to be distributed multifocally in parallel.
4. Discussion Gamma-band neuronal activity has been proposed to reflect higher cognitive processes such as attention, perception and language processing [3– 5]. Pulvermu¨ller et al. demonstrated the oscillatory change in the low gamma band in the left hemisphere during the lexical decision task [11]. However, the spatiotemporal distribution of such frequencydependent neuronal activity related to cognitive processes is still unknown. Thus, we introduced a novel method, synthetic aperture magnetometry (SAM) [6]. SAM is one of the statistical spatial filtering methods using an adaptive beamformer, analogous to the technique, which obtains the high spatial selectivity from the radio antenna arrays [6 –9]. Using SAM, we demonstrated the spatiotemporal distribution and frequency bands of the ERD and ERS during the silent reading. ERD and ERS were distributed multifocally over both hemispheres but lateralized to the left hemisphere including the area related to lexical and cognitive processing. The ERS or ERD in the beta and low gamma band was demonstrated in the left middle frontal region, the left inferior frontal region and the left temporo-parieto-occipital region, which may reflect lexical and cognitive processing. The ERS in the high gamma band was demonstrated in the bilateral medial occipital region around calcaline, which may reflect the primary visual processing. The previous study also demonstrated the ERS in the high gamma band in the primary somatosensory area following somatosensory stimulation [12]. Another important finding is temporal distribution of ERS and ERD during the silent reading. ERSs tended to be distributed serially from the occipital region via the parieto-temporal region to the frontal region, whereas ERDs tended to be distributed multifocally in parallel. These results suggest that both serial and parallel processings are involved in silent reading. Spatiotemporal distributions and frequency bands of ERD differ definitely from those of ERS. This difference in the spatiotemporal distributions of ERS and ERD may support our hypothesis that the neural
M. Hirata et al. / International Congress Series 1232 (2002) 35–39
39
mechanisms for ERS and ERD differ, reflecting responses of different cell assemblies related to specific neural functions rather than a frequency shift of the same cell assembly.
Acknowledgements This work was supported in part by a Grant-in-Aid for Scientific Research (11470290) from the Japanese Ministry of Education, Science and Culture.
References [1] G. Pfurtsheller, A. Aranbar, Electroencephalogr. Clin. Neurophysiol. 2 (1977) 817 – 826. [2] G. Pfurtsheller, Electroencephalogr. Clin. Neurophysiol. 83 (1992) 62 – 69. [3] F. Pulvermu¨ller, W. Lutzenberger, H. Preißl, N. Birbaumer, Spectrum responses in the gamma-band: physiological signs of higher cognitive processes? NeuroReport 6 (1995) 2059 – 2064. [4] F. Pulvermu¨ller, C. Eulitz, C. Pantev, B. Mohr, B. Feige, W. Lutzenberger, T. Elbert, N. Birbaumer, Highfrequency cortical responses reflect lexical processing: an MEG study, Electroencephalogr. Clin. Neurophysiol. 98 (1996) 76 – 85. [5] C. Eulitz, B. Maess, C. Pantev, A.D. Friderci, B. Feige, T. Elbert, Oscillatory neuromagnetic activity induced by language and non-language stimuli, Cognit. Brain Res. 4 (1996) 121 – 132. [6] M. Taniguchi, A. Kato, N. Fujita, et al., NeuroImage 12 (2000) 298 – 306. [7] S.E. Robinson, J. Vrba, Functional neuroimaging by synthetic aperture magnetometry (SAM), in: T. Kotani, M. Kotani, S. Kuriki, et al. (Eds.), Recent Advances in Biomagnetism, Tohoku University Press, Sendai, 1999, pp. 302 – 305. [8] R. Ishii, K. Shinosaki, S. Ukai, et al., NeuroReport 10 (1999) 675 – 679. [9] R. Ishii, K. Shinosaki, Y. Ikejiri, et al., NeuroReport 11 (2000) 3283 – 3287. [10] M. Taniguchi, T. Yoshimine, M. Hirata, et al., NeuroReport 9 (1998) 1497 – 1502. [11] F. Pulvermu¨ller, N. Birbaumer, W. Lutzenberger, B. Mohr, High-frequency cortical responses reflect lexical processing: an MEG study, Prog. Neurobiol. 52 (1997) 427 – 445. [12] M. Hirata, A. Kato, M. Taniguchi, H. Ninomiya, D. Cheyne, S.E. Robinson, M. Maruno, E. Kumura, R. Ishii, N. Hirabuki, H. Nakamura, T. Yoshimine, Frequency-dependent spatial distribution of human somatosensory evoked neuromagnetic fields. Neuroscience Letter (in press).