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Measurements of brain magnetic fields associated with apparent self-motion
International Congress Series 1232 (2002) 367 – 371
Measurements of brain magnetic fields associated with apparent self-motion Seiji Nakagawa a,*, S. Nishiike b, M. Tonoike a, N. Takeda c, T. Kubo b a
Life Electronics Laboratory, National Institute of Advanced Industrial Science and Technology, 1-8-31 Midorigaoka, Ikeda, Osaka 563-8577, Japan b Department of Otolaryngology and Sensory Organ Surgery, Osaka University Graduate School of Medicine, Osaka, Japan c Department of Otolaryngology, Tokushima University School of Medicine, Tokushima, Japan
Abstract We investigated the cortical sites that process sensations of apparent self-motion (vection) using magnetoencephalography (MEG). Expanding rectangles were presented on the black screen continuously to make the subjects feel as if they go through a tunnel. Seven healthy volunteers were carefully selected and previously trained to experience vections. For both the vection and the control stimuli, the activation of post-central gyrus, infero-posterior temporal lobe, lingual/fusiform gyrus were found. On the other hand, activations in posterior, posterior operculum, parietal lobule, precentral gyrus, superior temporal gyrus were observed only for vection stimulus. These areas may be human analogs of vestibular cortex identified by former studies in monkey. The results also suggest that these areas integrate multi-modal information. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Linear vection; Magnetoencephalography; Vestibular cortex; Posterior insula
1. Introduction Our abilities to move in space depend a great amount on the vestibular system—a sensor of head acceleration. Electrophysiological studies in monkeys identified regions of cerebral cortex that receive vestibular inputs including the posterior part of the insula and operculum (posteroinsular vestibular cortex: PIVC) [1,2], portions of the intraparietal cortex (area 2v) [3], the superior temporal gyrus [4], and the central sulcus (area 3aV, area 4) [5,6]. In humans, vestibular inputs to intra-parietal sulcus and superior temporal gyrus *
Corresponding author. Tel.: +81-727-51-8785; fax: +81-727-51-8416. E-mail address: [email protected] (S. Nakagawa).
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 0 - 7
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S. Nakagawa et al. / International Congress Series 1232 (2002) 367–371
were reported from case studies of patients with focal lesions, as well as electric stimulation studies [7,8]. In functional imaging studies using caloric stimulation [9,10], activation of posterior insula was reported. These studies demonstrated that information about processing of body rotation is received by semicircular canals. On the other hand, the information of linear acceleration is received by otolith receptor. In human imaging experiments, however, stimulation to otolith receptor had not been used due to its difficulty. Since the vestibular system cannot detect self-motion at constant velocity, perception of self-motion during constant velocity movement is dependent on visual information. An apparent visually induced self-motion (vection) can be perceived while gazing at moving clouds, or moving adjacent trains. Activities of PIVC, area 2v, were observed during circular vection [11]. In this study, we used apparent linear self-motion (linear vection) to stimulate otolith receptor. Brain activation during linear vection was observed using magnetoencephalography (MEG).
2. Methods 2.1. Stimuli The following white expanding stimuli were presented on the black screen continuously to make the subjects feel as if they go through a tunnel: (a) a rectangle expanding at 5.3 deg/s, 71.4%, (b: vection stimulus) a rectangle expanding at 26.5 deg/s, 14.3%, (c: control stimuli) a circle expanding at 5.3 deg/s, 14.3% (Fig. 1). All subjects reported that they experienced vections for stimulus (b).
Fig. 1. Visual stimuli presented to the subjects. An expanding rectangle appeared in the center of the screen one after the other.
S. Nakagawa et al. / International Congress Series 1232 (2002) 367–371
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2.2. Subjects Seven healthy volunteers (6 males, 22 –34 years old, right-handed) took part in this experiment. They were carefully selected and previously trained to experience vections for the stimulus. During recordings, they sat on a chair in the magnetically shielded room, and were requested to gaze at a fixation point on the center of the screen. 2.3. Recordings and source analyses Recordings of event-related magnetic fields were carried out in a magnetically shielded room using a 122-channel whole-head neuromagnetometer (Neuromag-122k, Neuromag, Finland). The vertical electrooculogram (EOG) was recorded with infra- and supraorbital electrodes to monitor artifacts from eye blinks and eye movements. The magnetic data
Fig. 2. A number of ECD clusters estimated in four cortical regions.
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S. Nakagawa et al. / International Congress Series 1232 (2002) 367–371
were sampled at 0.4 kHz after band-pass-filtering between 0.03 and 100 Hz. Any epoch coinciding with magnetic signals exceeding 3000 fT/cm and/or a vertical EOG deflections beyond 150 AV were rejected for further analysis. The average of more than 100 epochs were digitally band-pass-filtered between 0.1 and 30 Hz. The average of 200-ms prestimulus period served as the baseline. N1m equivalent current dipoles (ECDs) were estimated in the both hemispheres, for each kind of stimuli, at the N1m peak latencies. The localization of single equivalent current dipoles (ECDs) was estimated using 34 sets of locally selected channels, each covering a part of the head, assuming the single dipole in a spherical head model. Only the ECDs that satisfied the following conditions, GOF—80% and 95%-confidence volume—2000 mm3, were selected. They were accepted when such ECDs were found in a time series of 10 ms or more. The resulting time series of stable ECDs is called an ECD cluster.
3. Results and discussions Large magnetic deflections were observed for the vection stimuli in the temporoparietal region. For both the vection and the control stimuli, ECD clusters were estimated in the post-central gyrus (100 –200 ms), infero-posterior temporal lobe (300 – 500 ms), lingual/fusiform gyrus (300 – 500 ms). On the other hand, activations in posterior insula (300 – 400 ms), posterior operculum (400 – 500 ms), parietal lobule (300 – 500 ms), precentral gyrus (300 – 400 ms), superior temporal gyrus (400 –500 ms) were observed for only vection stimulus. Fig. 2 shows a number of clusters estimated in the four cortical regions. More clusters were observed for the vection stimuli than for the control stimuli. These regions may be the human analogs of vestibular cortex identified by former studies in monkey. The results suggest that vestibular cortices were activated even by apparent linear self-motion, and information of linear acceleration is processed in the same region as rotational acceleration. It is also suggested that vestibular cortex not only receive inputs from the peripheral vestibular apparatus, but also processes the equilibrium sensation from multi-modal information.
References [1] O.J. Gru¨sser, M. Pause, U. Schreiter, Localization and responses of neurons in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis), J. Physiol. 430 (1990) 537 – 557. [2] O.J. Gru¨sser, M. Pause, U. Schreiter, Vestibular neurons in the parieto-insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses, J. Physiol. 430 (1990) 537 – 557. [3] D.F.M. Schwarz, J. Fredrickson, Rhesus monkey vestibular cortex: a bimodal primary projection field, Science 172 (1971) 280 – 281. [4] P. Their, R.G. Erickson, Vestibular input to visual-tracking neurons in area MST of awake rhesus monkeys, Ann. N. Y. Acad. Sci. 656 (1992) 960 – 963. [5] L. Leinonen, J. Hyva¨rinen, A.R.A. Sovija¨rvvi, Functional properties of neurons in the temporoparietal association cortex of awake monkey, Exp. Brain Res. 39 (1980) 203 – 215. [6] S. Faugier-Grimaud, J. Ventre, Anatomic connections of inferior parietal cortex (area 7) with subcortical structures related to vestibulo-ocular function in a monkey (Macaca fascicularis), J. Comp. Neurol. 280 (1989) 1 – 14.
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[7] W. Penfield, Vestibular sensation and the cerebral cortex, Ann. Otol., Rhinol., Laryngol. 66 (1957) 691 – 698. [8] W. Penfield, T. Rasmussen, The Cerebral Cortex of Man—A Clinical Study of Localization of Function, Macmillan, New York, 1950. [9] L. Friberg, T.S. Olsen, P.E. Roland, O.B. Paulson, N.A. Lassen, Focal increase of blood flow in the cerebral cortex of man during vestibular stimulation, Brain 108 (1985) 609 – 623. [10] G. Bottini, R. Sterzi, E. Paulesu, G. Vallar, S.F. Cappa, F. Erminio, R.E. Passingham, C.D. Frith, R.S. Frackowiak, Identification of the central vestibular projections in man: a positron emission tomography activation study, Exp. Brain Res. 99 (1994) 164 – 169. [11] W.O. Guldin, O.J. Gru¨sser, Is there a vestibular cortex? Trends Neurosci. 21 (1998) 254 – 259.
Measurements of brain magnetic fields associated with apparent self-motion Seiji Nakagawa a,*, S. Nishiike b, M. Tonoike a, N. Takeda c, T. Kubo b a
Life Electronics Laboratory, National Institute of Advanced Industrial Science and Technology, 1-8-31 Midorigaoka, Ikeda, Osaka 563-8577, Japan b Department of Otolaryngology and Sensory Organ Surgery, Osaka University Graduate School of Medicine, Osaka, Japan c Department of Otolaryngology, Tokushima University School of Medicine, Tokushima, Japan
Abstract We investigated the cortical sites that process sensations of apparent self-motion (vection) using magnetoencephalography (MEG). Expanding rectangles were presented on the black screen continuously to make the subjects feel as if they go through a tunnel. Seven healthy volunteers were carefully selected and previously trained to experience vections. For both the vection and the control stimuli, the activation of post-central gyrus, infero-posterior temporal lobe, lingual/fusiform gyrus were found. On the other hand, activations in posterior, posterior operculum, parietal lobule, precentral gyrus, superior temporal gyrus were observed only for vection stimulus. These areas may be human analogs of vestibular cortex identified by former studies in monkey. The results also suggest that these areas integrate multi-modal information. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Linear vection; Magnetoencephalography; Vestibular cortex; Posterior insula
1. Introduction Our abilities to move in space depend a great amount on the vestibular system—a sensor of head acceleration. Electrophysiological studies in monkeys identified regions of cerebral cortex that receive vestibular inputs including the posterior part of the insula and operculum (posteroinsular vestibular cortex: PIVC) [1,2], portions of the intraparietal cortex (area 2v) [3], the superior temporal gyrus [4], and the central sulcus (area 3aV, area 4) [5,6]. In humans, vestibular inputs to intra-parietal sulcus and superior temporal gyrus *
Corresponding author. Tel.: +81-727-51-8785; fax: +81-727-51-8416. E-mail address: [email protected] (S. Nakagawa).
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 0 - 7
368
S. Nakagawa et al. / International Congress Series 1232 (2002) 367–371
were reported from case studies of patients with focal lesions, as well as electric stimulation studies [7,8]. In functional imaging studies using caloric stimulation [9,10], activation of posterior insula was reported. These studies demonstrated that information about processing of body rotation is received by semicircular canals. On the other hand, the information of linear acceleration is received by otolith receptor. In human imaging experiments, however, stimulation to otolith receptor had not been used due to its difficulty. Since the vestibular system cannot detect self-motion at constant velocity, perception of self-motion during constant velocity movement is dependent on visual information. An apparent visually induced self-motion (vection) can be perceived while gazing at moving clouds, or moving adjacent trains. Activities of PIVC, area 2v, were observed during circular vection [11]. In this study, we used apparent linear self-motion (linear vection) to stimulate otolith receptor. Brain activation during linear vection was observed using magnetoencephalography (MEG).
2. Methods 2.1. Stimuli The following white expanding stimuli were presented on the black screen continuously to make the subjects feel as if they go through a tunnel: (a) a rectangle expanding at 5.3 deg/s, 71.4%, (b: vection stimulus) a rectangle expanding at 26.5 deg/s, 14.3%, (c: control stimuli) a circle expanding at 5.3 deg/s, 14.3% (Fig. 1). All subjects reported that they experienced vections for stimulus (b).
Fig. 1. Visual stimuli presented to the subjects. An expanding rectangle appeared in the center of the screen one after the other.
S. Nakagawa et al. / International Congress Series 1232 (2002) 367–371
369
2.2. Subjects Seven healthy volunteers (6 males, 22 –34 years old, right-handed) took part in this experiment. They were carefully selected and previously trained to experience vections for the stimulus. During recordings, they sat on a chair in the magnetically shielded room, and were requested to gaze at a fixation point on the center of the screen. 2.3. Recordings and source analyses Recordings of event-related magnetic fields were carried out in a magnetically shielded room using a 122-channel whole-head neuromagnetometer (Neuromag-122k, Neuromag, Finland). The vertical electrooculogram (EOG) was recorded with infra- and supraorbital electrodes to monitor artifacts from eye blinks and eye movements. The magnetic data
Fig. 2. A number of ECD clusters estimated in four cortical regions.
370
S. Nakagawa et al. / International Congress Series 1232 (2002) 367–371
were sampled at 0.4 kHz after band-pass-filtering between 0.03 and 100 Hz. Any epoch coinciding with magnetic signals exceeding 3000 fT/cm and/or a vertical EOG deflections beyond 150 AV were rejected for further analysis. The average of more than 100 epochs were digitally band-pass-filtered between 0.1 and 30 Hz. The average of 200-ms prestimulus period served as the baseline. N1m equivalent current dipoles (ECDs) were estimated in the both hemispheres, for each kind of stimuli, at the N1m peak latencies. The localization of single equivalent current dipoles (ECDs) was estimated using 34 sets of locally selected channels, each covering a part of the head, assuming the single dipole in a spherical head model. Only the ECDs that satisfied the following conditions, GOF—80% and 95%-confidence volume—2000 mm3, were selected. They were accepted when such ECDs were found in a time series of 10 ms or more. The resulting time series of stable ECDs is called an ECD cluster.
3. Results and discussions Large magnetic deflections were observed for the vection stimuli in the temporoparietal region. For both the vection and the control stimuli, ECD clusters were estimated in the post-central gyrus (100 –200 ms), infero-posterior temporal lobe (300 – 500 ms), lingual/fusiform gyrus (300 – 500 ms). On the other hand, activations in posterior insula (300 – 400 ms), posterior operculum (400 – 500 ms), parietal lobule (300 – 500 ms), precentral gyrus (300 – 400 ms), superior temporal gyrus (400 –500 ms) were observed for only vection stimulus. Fig. 2 shows a number of clusters estimated in the four cortical regions. More clusters were observed for the vection stimuli than for the control stimuli. These regions may be the human analogs of vestibular cortex identified by former studies in monkey. The results suggest that vestibular cortices were activated even by apparent linear self-motion, and information of linear acceleration is processed in the same region as rotational acceleration. It is also suggested that vestibular cortex not only receive inputs from the peripheral vestibular apparatus, but also processes the equilibrium sensation from multi-modal information.
References [1] O.J. Gru¨sser, M. Pause, U. Schreiter, Localization and responses of neurons in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis), J. Physiol. 430 (1990) 537 – 557. [2] O.J. Gru¨sser, M. Pause, U. Schreiter, Vestibular neurons in the parieto-insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses, J. Physiol. 430 (1990) 537 – 557. [3] D.F.M. Schwarz, J. Fredrickson, Rhesus monkey vestibular cortex: a bimodal primary projection field, Science 172 (1971) 280 – 281. [4] P. Their, R.G. Erickson, Vestibular input to visual-tracking neurons in area MST of awake rhesus monkeys, Ann. N. Y. Acad. Sci. 656 (1992) 960 – 963. [5] L. Leinonen, J. Hyva¨rinen, A.R.A. Sovija¨rvvi, Functional properties of neurons in the temporoparietal association cortex of awake monkey, Exp. Brain Res. 39 (1980) 203 – 215. [6] S. Faugier-Grimaud, J. Ventre, Anatomic connections of inferior parietal cortex (area 7) with subcortical structures related to vestibulo-ocular function in a monkey (Macaca fascicularis), J. Comp. Neurol. 280 (1989) 1 – 14.
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[7] W. Penfield, Vestibular sensation and the cerebral cortex, Ann. Otol., Rhinol., Laryngol. 66 (1957) 691 – 698. [8] W. Penfield, T. Rasmussen, The Cerebral Cortex of Man—A Clinical Study of Localization of Function, Macmillan, New York, 1950. [9] L. Friberg, T.S. Olsen, P.E. Roland, O.B. Paulson, N.A. Lassen, Focal increase of blood flow in the cerebral cortex of man during vestibular stimulation, Brain 108 (1985) 609 – 623. [10] G. Bottini, R. Sterzi, E. Paulesu, G. Vallar, S.F. Cappa, F. Erminio, R.E. Passingham, C.D. Frith, R.S. Frackowiak, Identification of the central vestibular projections in man: a positron emission tomography activation study, Exp. Brain Res. 99 (1994) 164 – 169. [11] W.O. Guldin, O.J. Gru¨sser, Is there a vestibular cortex? Trends Neurosci. 21 (1998) 254 – 259.