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Dynamic brain activation during visual infrequent target detection processing
International Congress Series 1232 (2002) 277 – 282
Dynamic brain activation during visual infrequent target detection processing Sunao Iwaki a,*, Naoya Hirata b, Mitsuo Tonoike a a
Life Electronics Laboratory, National Institute of Advanced Industrial Science and Technology, 1-8-31 Midorigaoka, Ikeda, Osaka 563-8577, Japan b Faculty of Engineering Sciences, Kinki University, Higashi Osaka, Osaka 577-8502, Japan
Abstract In this study, we investigated the spatio-temporal characteristics of the neural activities in the human brain related to the detection of visually presented infrequent target stimuli. Neuromagnetic signals were measured during six healthy subjects performing typical visual oddball task. We visualized the multiple brain regions that were activated around 300 ms after the visual stimulus presentation during the infrequent target detection processing using minimum L1-norm method. We observed neural activities in the middle/inferior frontal region (Brodmann’s area (BA) 44, 46), the anterior cingulate cortex (BA24), the left parieto-temporal gyrus (BA40), contralateral occipitotemporal region (BA19), posterior parietal region (BA7), and superior/middle temporal region (BA21, 22) in the latencies around 300 – 400 ms. The temporal characteristics of the estimated neural activities in these regions indicated the involvement of frontal and anterior cingulate cortex in the early P3 component (P3a) and the contribution of the parietal and temporal regions to the later component (P3b). The current results support the hypothesis that multiple regions in the human brain are cooperatively activated during the infrequent target detection in the latencies around 300 ms after the target stimulus presentation. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Visual infrequent target detection; P3; Neuromagnetic measurement; Minimum-norm estimates
1. Introduction Many electrophysiological studies of infrequent target detection have been performed using ‘oddball’ paradigm in which subjects were required to detect and respond to infrequent target events embedded in a series of repetitive (frequent) events. The oddball tasks have been known to elicit prominent component of event-related potentials (ERPs) called P3, *
Corresponding author. Tel.: +81-727-51-8764; fax: +81-727-51-8416. E-mail address: [email protected] (S. Iwaki).
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 1 9 - 1
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S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
which occurs about 300 ms after the infrequent stimulus onset. The P3 is thought to reflect attentional resource allocation when working memory is engaged, and is divided into two components: P3a which is a small positive component of ERP over the frontal lobe, that peaks between 250 and 500 ms, and is considered to reflect the automatic orienting of attention; and P3b which is maximal over the parietal scalp between 300 and 600 ms, and is thought to reflect effortful target detection processing. These components have been widely used to investigate cognitive brain responses, however, the specific brain regions involved in the generation of P3 component were largely unknown. In the present study, to clarify the spatio-temporal characteristics of the neural activities in the human brain related to the detection of visual infrequent target stimuli, neuromagnetic measurements were performed. 2. Methods 2.1. Task Typical visual oddball task was performed in five subjects. Stimuli were presented for 100 ms by light emitting diode (LED), which flashes either in red (infrequent target: 20%) or in green (frequent non-target: 80%) in the randomized order, located in the left visual field and separated with a visual angle of 7.4j from a fixation point in front of the subject. Subjects were instructed to lift their right index finger immediately after detecting the infrequent target stimulus. 2.2. Data acquisition and analysis Neuromagnetic signals were measured with a whole-cortex-type MEG system (Neuromag-122k). The stimulus-related epochs of 700 ms, including a 200-ms pre-stimulus baseline, were recorded with a pass-band of 0.03 – 100 Hz and a sampling rate of 498 Hz. Event-related magnetic fields were independently averaged for more than 50 epochs to correctly identify infrequent target stimuli and frequent non-target stimuli. The averaged data were filtered by the digital band-pass filter with a pass-band of 0.01– 30 Hz. Distributions of neural activities corresponding to the infrequent target stimuli and the frequent non-target stimuli were estimated within a latency range of 100 to 500 ms after the stimulus onset by using the minimum L1-norm current estimation technique [1]. Temporal characteristics of the neural activities in (a) the frontal region, (b) the anterior cingulate region, (c) the posterior superior parietal region, (d) the parieto-temporal region, and (e) the superior temporal region were extracted from the spatio-temporal current distribution estimated in whole cortical regions. These regions were determined from our preliminary study of visual infrequent target detection task in which three subjects were intensively studied with voxel-by-voxel statistical evaluation of the estimated source distribution. 3. Results and discussion Typical MEG waveforms, measured during visual infrequent target detection task, are shown in Fig. 1. Results of the estimation of neural activity distribution in the typical
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
279
Fig. 1. Typical MEG waveforms measured during visual infrequent target detection task.
subject are shown in Fig. 2. The white boxes superimposed on MR images indicate the grid points at which a statistically significant difference ( p<0.0005) in estimated neural activities between the target and the control conditions was observed. Significant enhancement of the neural activity was detected in (a) the middle frontal or inferior frontal region in the latencies between 260 and 310 ms, (b) the anterior cingulate cortex between 280 and 300 ms, (c) left parieto-temporal region between 300 and 320 ms, and (d) the pre-central and post-central gyrus between 290 and 340 ms. Fig. 3 shows the temporal characteristics of the neural activities in (A) the frontal region, (B) the anterior cingulate region, (C) the posterior superior parietal region, (D) the parieto-temporal region, and (E) the superior temporal region were extracted from the spatio-temporal current distribution estimated in whole cortical regions by minimum L1norm current estimates. Activities in parieto-temporal region and posterior superior temporal region were preceded by the activities in frontal and anterior cingulate regions. The temporal characteristics of the estimated neural activities in these regions indicated the involvement of frontal and anterior cingulate cortex in the early P3 component (P3a) and the contribution of the parietal and temporal regions to the later component (P3b). Recent neuroimaging studies have suggested that there were multiple regions involved in the infrequent target detection operations. The activities in the parieto-temporal region are in agreement with the studies showing that lesion to the temporal-parietal cortex abolishes the scalp P3b component measured by EEG [2], and that intracranial P3 signals have been recorded in this region [3]. This region is known to receive pre-processed information
280 S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
Fig. 2. Regions where the statistically significant enhancement of the neural activity was detected in the infrequent target stimulus presentation compared to the frequent stimulus presentation for the typical subject ( p<0.0005).
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
281
Fig. 3. Estimated temporal characteristics of the neural activity during visual infrequent detection task averaged over all subjects.
from multiple modality-specific areas, including vision and audition, and thus thought to be involved in the evaluation, categorization and decision-making operations based on the modality-independent information [4]. Intracranial-evoked potential studies also reported activities, which is analogous to P3 responses, in the widespread area in the frontal lobe including the regions indicated in this study [5]. In addition, the current results indicate the activation in the anterior cingulate cortex, which may be involved in the target detection and the response selection [6] as well as the vigilance attention [7], which slightly preceded the activation in the parieto-temporal region. These results support the hypothesis that the projections from the anterior cingulate may initiate or modulate the activation in the parieto-temporal region [8].
4. Conclusion In this study, we visualized the multiple brain regions that were activated around 300 ms after the visual stimulus presentation during the infrequent target detection processing using minimum L1-norm method. We observed neural activities in the middle/inferior frontal region (Brodmann’s area (BA) 44, 46), the anterior cingulate cortex (BA24), the left supramarginal gyrus (BA40), contralateral occipito-temporal region (BA19), posterior parietal region (BA7), and superior/middle temporal region (BA21, 22) in the latencies around 300– 400 ms. The temporal characteristics of the estimated neural activities in
282
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
these regions indicated the involvement of frontal and anterior cingulate cortex in the early P3 component (P3a) and the contribution of the parietal and temporal regions to the later component (P3b).
References [1] K. Uutela, M. Hamalainen, E. Somersalo, Visualization of magnetoencephalographic data using minimum current estimates, Neuroimage 10 (1999) 173 – 180. [2] R.T. Knight, D. Scabini, D.L. Woods, C.C. Clayworth, Contributions of temporal-parietal junction to the human auditory P3, Brain Res. 502 (1989) 109 – 116. [3] E. Halgren, P. Baudena, J.M. Clarke, G. Heit, C. Liegeois, P. Chauvel, A. Musolino, Intracranial potentials to rare target and distractor auditory and visual stimuli: I. Superior temporal plane and parietal lobe, Electroencephalogr. Clin. Neurophysiol. 94 (1995) 191 – 220. [4] M.M. Mesulam, Large-scale neurocognitive networks and distributed processing for attention, language, and memory, Ann. Neurol. 28 (1990) 597 – 613. [5] P. Baudena, E. Halgren, G. Heit, J.M. Clarke, Intracerebral potentials to rare target and distractor auditory and visual stimuli: III. Frontal cortex, Electroencephalogr. Clin. Neurophysiol. 94 (1995) 251 – 264. [6] O. Devinsky, M.J. Morrell, B.A. Vogt, Contributions of anterior cingulate cortex to behaviour, Brain 118 (1995) 279 – 306. [7] J.V. Pardo, P.T. Fox, M.E. Raichle, Localization of a human system for sustained attention by positron emission tomography, Nature 349 (1991) 61 – 64. [8] V. Menon, J.M. Ford, K.O. Lim, G.H. Glover, A. Pfefferbaum, Combined event-related fMRI and EEG evidence for temporal-parietal cortex activation during target detection, NeuroReport 8 (1997) 3029 – 3037.
Dynamic brain activation during visual infrequent target detection processing Sunao Iwaki a,*, Naoya Hirata b, Mitsuo Tonoike a a
Life Electronics Laboratory, National Institute of Advanced Industrial Science and Technology, 1-8-31 Midorigaoka, Ikeda, Osaka 563-8577, Japan b Faculty of Engineering Sciences, Kinki University, Higashi Osaka, Osaka 577-8502, Japan
Abstract In this study, we investigated the spatio-temporal characteristics of the neural activities in the human brain related to the detection of visually presented infrequent target stimuli. Neuromagnetic signals were measured during six healthy subjects performing typical visual oddball task. We visualized the multiple brain regions that were activated around 300 ms after the visual stimulus presentation during the infrequent target detection processing using minimum L1-norm method. We observed neural activities in the middle/inferior frontal region (Brodmann’s area (BA) 44, 46), the anterior cingulate cortex (BA24), the left parieto-temporal gyrus (BA40), contralateral occipitotemporal region (BA19), posterior parietal region (BA7), and superior/middle temporal region (BA21, 22) in the latencies around 300 – 400 ms. The temporal characteristics of the estimated neural activities in these regions indicated the involvement of frontal and anterior cingulate cortex in the early P3 component (P3a) and the contribution of the parietal and temporal regions to the later component (P3b). The current results support the hypothesis that multiple regions in the human brain are cooperatively activated during the infrequent target detection in the latencies around 300 ms after the target stimulus presentation. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Visual infrequent target detection; P3; Neuromagnetic measurement; Minimum-norm estimates
1. Introduction Many electrophysiological studies of infrequent target detection have been performed using ‘oddball’ paradigm in which subjects were required to detect and respond to infrequent target events embedded in a series of repetitive (frequent) events. The oddball tasks have been known to elicit prominent component of event-related potentials (ERPs) called P3, *
Corresponding author. Tel.: +81-727-51-8764; fax: +81-727-51-8416. E-mail address: [email protected] (S. Iwaki).
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 1 9 - 1
278
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
which occurs about 300 ms after the infrequent stimulus onset. The P3 is thought to reflect attentional resource allocation when working memory is engaged, and is divided into two components: P3a which is a small positive component of ERP over the frontal lobe, that peaks between 250 and 500 ms, and is considered to reflect the automatic orienting of attention; and P3b which is maximal over the parietal scalp between 300 and 600 ms, and is thought to reflect effortful target detection processing. These components have been widely used to investigate cognitive brain responses, however, the specific brain regions involved in the generation of P3 component were largely unknown. In the present study, to clarify the spatio-temporal characteristics of the neural activities in the human brain related to the detection of visual infrequent target stimuli, neuromagnetic measurements were performed. 2. Methods 2.1. Task Typical visual oddball task was performed in five subjects. Stimuli were presented for 100 ms by light emitting diode (LED), which flashes either in red (infrequent target: 20%) or in green (frequent non-target: 80%) in the randomized order, located in the left visual field and separated with a visual angle of 7.4j from a fixation point in front of the subject. Subjects were instructed to lift their right index finger immediately after detecting the infrequent target stimulus. 2.2. Data acquisition and analysis Neuromagnetic signals were measured with a whole-cortex-type MEG system (Neuromag-122k). The stimulus-related epochs of 700 ms, including a 200-ms pre-stimulus baseline, were recorded with a pass-band of 0.03 – 100 Hz and a sampling rate of 498 Hz. Event-related magnetic fields were independently averaged for more than 50 epochs to correctly identify infrequent target stimuli and frequent non-target stimuli. The averaged data were filtered by the digital band-pass filter with a pass-band of 0.01– 30 Hz. Distributions of neural activities corresponding to the infrequent target stimuli and the frequent non-target stimuli were estimated within a latency range of 100 to 500 ms after the stimulus onset by using the minimum L1-norm current estimation technique [1]. Temporal characteristics of the neural activities in (a) the frontal region, (b) the anterior cingulate region, (c) the posterior superior parietal region, (d) the parieto-temporal region, and (e) the superior temporal region were extracted from the spatio-temporal current distribution estimated in whole cortical regions. These regions were determined from our preliminary study of visual infrequent target detection task in which three subjects were intensively studied with voxel-by-voxel statistical evaluation of the estimated source distribution. 3. Results and discussion Typical MEG waveforms, measured during visual infrequent target detection task, are shown in Fig. 1. Results of the estimation of neural activity distribution in the typical
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
279
Fig. 1. Typical MEG waveforms measured during visual infrequent target detection task.
subject are shown in Fig. 2. The white boxes superimposed on MR images indicate the grid points at which a statistically significant difference ( p<0.0005) in estimated neural activities between the target and the control conditions was observed. Significant enhancement of the neural activity was detected in (a) the middle frontal or inferior frontal region in the latencies between 260 and 310 ms, (b) the anterior cingulate cortex between 280 and 300 ms, (c) left parieto-temporal region between 300 and 320 ms, and (d) the pre-central and post-central gyrus between 290 and 340 ms. Fig. 3 shows the temporal characteristics of the neural activities in (A) the frontal region, (B) the anterior cingulate region, (C) the posterior superior parietal region, (D) the parieto-temporal region, and (E) the superior temporal region were extracted from the spatio-temporal current distribution estimated in whole cortical regions by minimum L1norm current estimates. Activities in parieto-temporal region and posterior superior temporal region were preceded by the activities in frontal and anterior cingulate regions. The temporal characteristics of the estimated neural activities in these regions indicated the involvement of frontal and anterior cingulate cortex in the early P3 component (P3a) and the contribution of the parietal and temporal regions to the later component (P3b). Recent neuroimaging studies have suggested that there were multiple regions involved in the infrequent target detection operations. The activities in the parieto-temporal region are in agreement with the studies showing that lesion to the temporal-parietal cortex abolishes the scalp P3b component measured by EEG [2], and that intracranial P3 signals have been recorded in this region [3]. This region is known to receive pre-processed information
280 S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
Fig. 2. Regions where the statistically significant enhancement of the neural activity was detected in the infrequent target stimulus presentation compared to the frequent stimulus presentation for the typical subject ( p<0.0005).
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
281
Fig. 3. Estimated temporal characteristics of the neural activity during visual infrequent detection task averaged over all subjects.
from multiple modality-specific areas, including vision and audition, and thus thought to be involved in the evaluation, categorization and decision-making operations based on the modality-independent information [4]. Intracranial-evoked potential studies also reported activities, which is analogous to P3 responses, in the widespread area in the frontal lobe including the regions indicated in this study [5]. In addition, the current results indicate the activation in the anterior cingulate cortex, which may be involved in the target detection and the response selection [6] as well as the vigilance attention [7], which slightly preceded the activation in the parieto-temporal region. These results support the hypothesis that the projections from the anterior cingulate may initiate or modulate the activation in the parieto-temporal region [8].
4. Conclusion In this study, we visualized the multiple brain regions that were activated around 300 ms after the visual stimulus presentation during the infrequent target detection processing using minimum L1-norm method. We observed neural activities in the middle/inferior frontal region (Brodmann’s area (BA) 44, 46), the anterior cingulate cortex (BA24), the left supramarginal gyrus (BA40), contralateral occipito-temporal region (BA19), posterior parietal region (BA7), and superior/middle temporal region (BA21, 22) in the latencies around 300– 400 ms. The temporal characteristics of the estimated neural activities in
282
S. Iwaki et al. / International Congress Series 1232 (2002) 277–282
these regions indicated the involvement of frontal and anterior cingulate cortex in the early P3 component (P3a) and the contribution of the parietal and temporal regions to the later component (P3b).
References [1] K. Uutela, M. Hamalainen, E. Somersalo, Visualization of magnetoencephalographic data using minimum current estimates, Neuroimage 10 (1999) 173 – 180. [2] R.T. Knight, D. Scabini, D.L. Woods, C.C. Clayworth, Contributions of temporal-parietal junction to the human auditory P3, Brain Res. 502 (1989) 109 – 116. [3] E. Halgren, P. Baudena, J.M. Clarke, G. Heit, C. Liegeois, P. Chauvel, A. Musolino, Intracranial potentials to rare target and distractor auditory and visual stimuli: I. Superior temporal plane and parietal lobe, Electroencephalogr. Clin. Neurophysiol. 94 (1995) 191 – 220. [4] M.M. Mesulam, Large-scale neurocognitive networks and distributed processing for attention, language, and memory, Ann. Neurol. 28 (1990) 597 – 613. [5] P. Baudena, E. Halgren, G. Heit, J.M. Clarke, Intracerebral potentials to rare target and distractor auditory and visual stimuli: III. Frontal cortex, Electroencephalogr. Clin. Neurophysiol. 94 (1995) 251 – 264. [6] O. Devinsky, M.J. Morrell, B.A. Vogt, Contributions of anterior cingulate cortex to behaviour, Brain 118 (1995) 279 – 306. [7] J.V. Pardo, P.T. Fox, M.E. Raichle, Localization of a human system for sustained attention by positron emission tomography, Nature 349 (1991) 61 – 64. [8] V. Menon, J.M. Ford, K.O. Lim, G.H. Glover, A. Pfefferbaum, Combined event-related fMRI and EEG evidence for temporal-parietal cortex activation during target detection, NeuroReport 8 (1997) 3029 – 3037.