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Hemispheric lateralization in an analysis of speech sounds
Cognitive Brain Research 10 (2000) 119–124 www.elsevier.com / locate / bres
Research report
Hemispheric lateralization in an analysis of speech sounds Left hemisphere dominance replicated in Japanese subjects Sachiko Koyama a , *, Atsuko Gunji a , Hirooki Yabe b , Shoko Oiwa a , Reiko Akahane-Yamada c , d ¨¨ ¨ Ryusuke Kakigi a , Risto Naatanen a
Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki, Aichi, 444 -8585, Japan b Department of Neuropsychiatry, Hirosaki University School of Medicine, Hirosaki, Japan c ATR Human Information Processing Research Laboratories, Kyoto, Japan d Cognitive Brain Research Unit, Department of Psychology, Helsinki University, Helsinki, Finland Accepted 16 May 2000
Abstract ¨¨ ¨ Evoked magnetic responses to speech sounds [R. Naatanen, A. Lehtokoski, M. Lennes, M. Cheour, M. Huotilainen, A. Iivonen, M. Vainio, P. Alku, R.J. Ilmoniemi, A. Luuk, J. Allik, J. Sinkkonen and K. Alho, Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature, 385 (1997) 432–434.] were recorded from 13 Japanese subjects (right-handed). Infrequently presented vowels ([o]) among repetitive vowels ([e]) elicited the magnetic counterpart of mismatch negativity, MMNm (Bilateral, nine subjects; Left hemisphere alone, three subjects; Right hemisphere alone, one subject). The estimated source of the MMNm was stronger in the left than in the right auditory cortex. The sources were located posteriorly in the left than in the right auditory cortex. ¨¨ ¨ These findings are consistent with the results obtained in Finnish [R. Naatanen, A. Lehtokoski, M. Lennes, M. Cheour, M. Huotilainen, A. Iivonen, M.Vainio, P.Alku, R.J. Ilmoniemi, A. Luuk, J. Allik, J. Sinkkonen and K. Alho, Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature, 385 (1997) 432–434.][T. Rinne, K. Alho, P. Alku, M. Holi, J. Sinkkonen, J. ¨¨ ¨ Virtanen, O. Bertrand and R. Naatanen, Analysis of speech sounds is left-hemisphere predominant at 100–150 ms after sound onset. Neuroreport, 10 (1999) 1113–1117.] and English [K. Alho, J.F. Connolly, M. Cheour, A. Lehtokoski, M. Huotilainen, J. Virtanen, R. Aulanko and R.J. Ilmoniemi, Hemispheric lateralization in preattentive processing of speech sounds. Neurosci. Lett., 258 (1998) 9–12.] ¨¨ ¨ subjects. Instead of the P1m observed in Finnish [M. Tervaniemi, A. Kujala, K. Alho, J. Virtanen, R.J. Ilmoniemi and R. Naatanen, Functional specialization of the human auditory cortex in processing phonetic and musical sounds: A magnetoencephalographic (MEG) study. Neuroimage, 9 (1999) 330–336.] and English [K. Alho, J.F. Connolly, M. Cheour, A. Lehtokoski, M. Huotilainen, J. Virtanen, R. Aulanko and R.J. Ilmoniemi, Hemispheric lateralization in preattentive processing of speech sounds. Neurosci. Lett., 258 (1998) 9–12.] subjects, prior to the MMNm, M60, was elicited by both rare and frequent sounds. Both MMNm and M60 sources were posteriorly located in the left than the right hemisphere. 2000 Elsevier Science B.V. All rights reserved. Theme: Sensory systems Topic: Auditory system: central physiology Keywords: Mismatch negativity; Speech; Magnetoencephalography; Auditory cortex; Hemispheric lateralization
1. Introduction Deviant sounds infrequently embedded in a repetitive sequence of auditory stimuli (standard) elicit mismatch negativity (MMN) or its magnetic counterpart (MMNm) *Corresponding author. Tel.: 181-564-557-769; fax: 181-564-527913. E-mail address: [email protected] (S. Koyama).
[1–3,6,8,10,12,15,20,21]. Since MMN or MMNm has been observed even when subjects perform tasks that are completely unrelated to auditory stimuli, they have been regarded as an index of the pre-attentive automatic detection system of auditory stimulus change. Recent studies ¨¨ ¨ by Naatanen and his colleagues showed that MMN or MMNm to speech sounds showed left hemisphere dominance [3,12,15], whereas MMM or MMNm to pure tones [10] and musical cords [20] showed right hemisphere
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dominance. These results indicate that the left hemisphere dominance in speech sounds starts as early as at the pre-attentive processing level. On the other hand, using Japanese subjects, Imaizumi et al. [8] did not find a left hemisphere dominance for MMNm while subjects passively heard a series of speech sounds. When the subjects performed a phoneme detection task, MMNm showed left hemisphere dominance. However, it should be noted that the stimuli were verbs of two syllables not vowels or consonant–vowel syllables which ¨¨ ¨ Naatanen and his colleagues have used [12,15,20]. They used three different forms of the Japanese verb / iku / (to go) which consisted of vowel-consonant–vowel syllables; / itta / (statement, past tense), / itta / ? (question, past tense) and / itte / (demand). / itta / (past tense) had a falling pitch pattern and / itta / ? had a rising pitch pattern. Their stimuli included syntactic factors and were longer in duration than simple vowels or consonant-vowel syllables. The aim of the present study was to examine the laterality of MMNm for simple vowels in Japanese subjects. To make a direct comparison with results reported by ¨¨ ¨ Naatanen et al. [12], the same stimuli, / e / and / o /, were used and most of the experimental parameters were the same., The / e /, / o / prototypes of Japanese are similar in those of Finnish [19].
2. Method The subjects were 13 native Japanese (7 females and 6 males; aged 25–40 years, right-handed). Stimuli were binaurally presented through plastic tubes and ear-pieces. The duration of the stimuli was 400 ms including 10 ms rise and fall times. The stimulus-onset asynchrony was 900 ms. Subjects were instructed to watch a silent film and to ignore the auditory stimulation. The total number of trials was 1200 (/ e /, 1020 trials and / o /, 180 trials) and they were presented in a random order. The intensity of / e / was 65 dBL and the loudness of / o / was adjusted to be the same as / e / in each subject before the MEG recording. Magnetic responses were measured with dual 37-channel gradiometers (Magnes, Biomagnetic Technologies Inc., USA). The gradiometers were placed over the left and right temporal sites. The responses were recorded with a 0.1–50 Hz bandpass filter at a sampling rate of 520.8 Hz. The mean value of the signals for 50 ms prior to the stimulus onset was used as the baseline in each channel. Epochs with signal variations of larger than 3.0 pT were excluded from the averaging. Vertical electro-oculograms (EOGs) were recorded simultaneously to monitor eye movements. Epochs with signal variations of larger than 80 mV in the EOG were also excluded from the averaging. The responses to frequent sounds were subtracted from those to the deviant sounds to determine the MMNm. Equivalent current dipoles of the MMNm were analyzed using BESA (version 2.1m) [17,18]. Taking a spatio–
temporal modeling approach, BESA decomposes the recorded responses into a number of discrete neuronal source activities overlapping in time and estimates the strength and timing of each source current over a defined interval. BESA calculates the locations and orientations of dipoles in a spherical head conductor model by an iterative leastsquares fit. The goodness-of-fit (GOF) of the model was expressed as a percentage of the residual variance (%RV) between the observed fields and the theoretical fields generated by the source model. The mean analysis epoch was 65 ms (range: 49–76 ms) in the left hemisphere and 70.6 ms (range: 53–98 ms) in the right. We accepted the source model in which the RV was below 6% with one or two sources. A source in the lower bank of the Sylvian fissure was obtained all the subjects who had MMNm. In addition, half of the subjects (four subjects in the left and seven subjects in the right hemisphere) had a second source located in the cortical area other than the auditory cortex. The location for second sources had actually several possible ‘candidate’. The accuracy of dipole localization depends on the distance between the source and sensor array [4,7,9]. The error increases with increasing a distance between the source and a sensor array. Therefore, the model which had shortest distance between the second source and the center of the sensor array, was selected, when several source models with the RV below 6% for 2 dipoles was obtained. Besides MMNm, a magnetic component peaking at around 60 ms, M60, after the stimulus presentation was observed both for frequent and deviant sounds all the subjects. Source location of M60 was estimated using a single moving dipole model [17] at the peak of M60. Correlation between the theoretical fields generated by the model and the observed fields was used to estimated the goodness of fit of the model and only models whose correlation above 0.97 were accepted. The locations of the estimated sources were described in a head-based coordinate system (see Fig. 2B). The origin of the system was set at the midpoint between preauricular points. The x-axis joins the nasion and the origin. The x-axis thus indicates a coronal plane with positive values in the anterior direction. The y-axis extended from the origin to the left side of the head such that it was perpendicular to the x-axis. The y-axis indicates the sagittal plane with positive values to the left preauricular point. The z-axis indicates the axial plane with positive values directed upward such that it was perpendicular to the x and y axes.
3. Results Fig. 1 shows magnetic responses and estimated sources recorded from one subject. In this subject, the recorded MMNm itself was larger in the right hemisphere than in the left. In the left hemisphere, the zero-level line of the
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Fig. 1. Evoked magnetic responses and their estimated sources in one subject. It should be noted that MMNm (B) were larger for the right than for the left hemisphere. However, the estimated source strength of MMNm (C) was larger for the left than for the right hemisphere. (A) Magnetic responses from 2 sensors to rare [o] and frequent [e] sounds and approximate location of 37 sensors illustrated by circles. (B) Difference in responses to rare sounds and to frequent sounds and the iso-contour maps (step 20 fT) of difference responses. The shadowed area illustrates magnetic flux out of the white area into the skull. Thick line indicates the zero level. (C) The estimated source location and strength.
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iso-contour map is almost straight, indicating that the single dipole source is located under the sensor arrays. In the right hemisphere, the contour pattern suggests that there is a source located somewhat anterior to that in the left hemisphere and that there is another source. Source analysis indicated a single source (latency range of 93.2– 164.0 ms, RV54.8%) in the left auditory cortex and two sources in the right hemisphere (latency range of 81.1– 158.0 ms, RV54.2%): one in the auditory cortex, and the other in the cortex around the posterior part of the Sylvian fissure. The strength of the source in the auditory cortex was larger in the left than in the right hemisphere.
3.1. MMNm Clear mismatch fields (MMNm) were bilaterally observed in nine subjects (Left hemisphere alone, three subjects; Right hemisphere alone, one subject). As a result, the sources could be estimated in all the observed MMNm. Fig. 2 shows the strength of MMNm estimated in the auditory cortex (A) and the location of individual MMNm sources in the coronal section (B). A repeated-measure analysis of variance (ANOVA, one-way with a factor of hemisphere) was performed for the data from the 9 subjects who had bilateral MMNm. The analysis revealed that the peak strength of the MMNm source was significantly greater in the left than that in the right hemisphere (F(1, 8)517.88, P,0.01). The mean peak latency of the source was 117.1612.0 ms in the left and 120.8614.8 ms in the right hemisphere. Repeated-measure ANOVAs with a factor of hemisphere were also performed for x, y, z values of the MMNm source location from nine subjects. The difference in x values reached significance (F(1, 8)59.54, P,0.05), indicating that the sources in the left hemisphere were more posteriorly located than those in
the right hemisphere. The difference in y- and z-values (F ,1) was not significant. In the left hemisphere, four subjects had a second source. These sources were located in the cortex around the posterior end of the Sylvian fissure for two subjects and the precentral area for two subjects. The peak amplitude of the source around the posterior end of the Sylvian fissure was 20.2 and 7.8 nAm and the peak latency was 121.7 and 108.4 ms. The peak amplitude of the source in the precentral area was 16.9 and 5.4 nAm and the peak latency was 114.1 and 127.4 ms. In the right hemisphere, seven subjects had a second source as shown in Fig. 1. The sources were located in the cortex around the posterior end of the Sylvian fissure (five subjects), the pre-motor area (two subjects). The peak amplitude of the source around the posterior end of the Sylvian fissure ranged between 4.3 and 24.7 nAm and the peak latency ranged between 95.1 and 142.6 ms. The amplitude of the source in the precentral area was 7.4 and 11.0 nAm and the latency was 108.4 and 150.2 ms.
3.2. M60 Bilateral M60 was observed in 11 subjects for frequent sounds (right alone, two subjects). The mean peak latency was 57.365.2 ms in the left hemisphere and 58.765.5 ms in the right. In the left hemisphere, the source location was successfully estimated in all the 12 subjects who showed M60. The mean source strength was 9.763.5 nAm. In the right hemisphere, the source location was successfully obtained in 11 out of 13 subjects who showed M60. The mean strength was 10.864.2 nAm. The source location for the frequent sounds is shown in Fig. 2B. A repeatedmeasure ANOVA with a factor of hemisphere was performed for the data (source strength and x, y, z values)
Fig. 2. Strength and location of the MMNm source estimated in the auditory cortex. (A) Peak source strength of MMNm. The data from the same subjects are linked with a line (black circle). The data from the subjects who had MMNm in only one hemisphere are shown in gray. The source strength was significantly greater in the left hemisphere than the right. (B) The axial location (x–y plain) of sources for MMNm (dot) and M60 for frequent stimuli (cross).
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from 11 subjects whose M60 source was bilaterally estimated. The difference in x values reached significance (F(1, 9)533.22, P,0.001) indicating that the source in the left hemisphere was more posteriorly located than that in the right hemisphere. The difference in y- (F ,1) and z-values (F ,1) was not significant. The difference in source strength was not significant (F(1, 9)51.62). For deviant sounds, M60 was bilaterally observed for nine subjects (the left hemisphere alone for one subject, the right hemisphere alone for one subject). The mean peak latency was 55.265.7 ms in the left hemisphere and 57.165.6 ms in the right. In the left hemisphere, the source location was successfully estimated in eight out of ten subjects who showed M60. The mean source strength was 11.265.5 nAm. In the right hemisphere, the source location was successfully obtained in six out of ten subjects who showed M60. The mean strength was 14.164.7 nAm. To compare the locations of M60 for frequent sounds and MMNm within each subject, x, y and z values were analyzed with repeated-measure ANOVAs in each hemisphere (11 subjects in the left hemisphere, 10 subjects in the right hemisphere). For x-values in the left hemisphere, the location of the two components was significantly different (F(1, 10)55.80, P,.05), indicating that M60 was more posteriorly located than MMNm. Other differences in the location between the components were not significant.
4. Discussion The present study indicates that the MMNm to speech sounds showed left hemisphere dominance in Japanese subjects. This finding was in line with those of previous studies using Finnish [12,15,20] and English subjects [3] that reported a left-hemisphere dominance of MMNm source strength for speech sounds. The latency of MMNm was also comparable to that in Finnish subjects [12,15,20]. Our results thus indicated that regardless of the native language, vowel processing predominantly occurs in the left hemisphere. Since the y-values (lateral location) of the source location did not differ between the hemispheres, hemispheric differences in MMNm source strength were probably not apparent (in source modeling, the deeper the source location, the greater the strength). Four subjects in the left hemisphere and seven subjects in the right hemisphere had second sources. The precentral source (two subjects in both hemispheres) might be comparable to a frontal source reported in event-related brain potential studies [2,6]. The sources located around the posterior end of the Sylvian fissure (two subjects in the left hemisphere and five subjects in the right hemisphere) may be comparable to the parietal source [10]. The peak latency of the second source is similar to that of the primary source in the auditory cortex, the second source is
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possibly a part of MMNm. The validity of second source is not clear thus far and further studies will be required. Contrary to our study, Imaizumi et al. [8] did not find a left-hemisphere dominance of MMNm to speech sounds. Since they used verbs rather than simple vowels, syntactic factors might modulate the hemispheric balance of MMNm. Alternatively, the duration of the stimuli may have an effect. Their stimuli were longer in duration than those of other MMNm studies (360 ms total). A recent MMN study estimated that the temporal window of stimulus integration for temporally close sounds into a unitary event, is about 160–170 ms [21]. The duration of those stimuli was longer than the temporal window and this might affect the MMNm laterality for speech sounds. Another possible explanation is that their stimuli included prosodic changes. Using PET, Zatorre et al. [22] suggested that prosodic aspects of spoken language are processed by the right hemisphere. Pre-attentive prosodic processing might modulate the laterality of MMNm in their study. Another possible reason for the discrepancy between the two studies is dipole analysis. They estimated only one source for MMNm. On the other hand, half of our subjects had two sources in the right hemisphere. As shown in Fig. 1, observed magnetic responses did not show the left hemisphere dominance in most of our subjects. If the single source analysis were applied to our data, MMNm strength might not show the left hemisphere dominance. The multiple-source analysis is thus quite helpful for precise estimation of the MMNm in the auditory cortex, even if the second source obtained here might be a byproduct of subtracting procedure and apparent. The MMNm sources in the auditory cortex were located more posteriorly in the left than in the right hemisphere. The results also replicated the findings obtained in Finnish [15,20] and English subjects [3]. These results are consistent with the finding that aphasic patients with lesion of the posterior temporal lobe in the left hemisphere showed no MMN to a phoneme deviation but had a normal MMN ¨ to frequency change [1]. However, Levanen et al. [10] reported a similar asymmetrical source location for MMNm to pure tones (MMNm elicited by frequency change). Moreover, the left-hemisphere source of M100 for pure tones was found to be more posterior to that in the right hemisphere in Finns [16], Germans [5,16], and Japanese [14]. Such hemispheric asymmetries in source location might thus not be language specific. The M60 was reported in previous studies using pure tones [11,13]. The M60 sources in the auditory cortex were also located posteriorly in the left than those in the right hemisphere. The source of M60 was located posteriorly than that of MMNm in the left hemisphere, but did not differ from that of MMNm in the right hemisphere. In previous studies using Finnish [20] and English [3] subjects, P1m peaking at around 80 ms was observed for both frequent and deviant speech. In Finnish subjects, P1m tended to be located posteriorly than MMNm in both
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hemispheres. We did not observe the P1m equivalent in the present study. Recently Salmelin et al. [16] reported that the source location of N100m to 1 kHz tone differed between Finnish and German male subjects. They suggested that linguistic environments might change functional organization of the auditory cortex. The difference in middle-latency responses might be attributed to the difference in linguistic environments between subjects.
Acknowledgements This study was supported by Grants-in-Aid for Scientific Research, Ministry of Education, Science, and Culture, Japan to S. Koyama (No. 11111230, 12011223) and H. Yabe (09670972, 09710064), R. Kakigi (No. 08878160, 09558102). We are grateful to Doctor Miyauchi for the use of MRI facilities. We thank Doctors M. Matsui and K. Kurakata for their comments and O. Nagata and Y. Takeshima for technical assistance.
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[8] S. Imaizumi, K. Mori, S. Kiritani, H. Hosoi, M. Tonoike, Taskdependent laterality for cue decoding during spoken language processing, Neuroreport 9 (1998) 899–903. [9] S. Kuriki, M. Murase, F. Takeuchi, Locating accuracy of a current source of neuromagnetic responses: simulation study for a single current dipole in a spherical conductor, Electroencephalogr. Clin. Neurophysiol. 73 (1989) 499–506. ¨ [10] S. Levanen, A. Ahonen, R. Hari, L. McEvoy, M. Sams, Deviant auditory stimuli activate human left and right auditory cortex differently, Cerebral Cortex 6 (1996) 288–296. ¨ ¨ M. Hamalainen, ¨ ¨¨ [11] J.P. Makela, R. Hari, L. McEvoy, Whole-head mapping of middle-latency auditory evoked magnetic fields, Electroencephalogr. Clin. Neurophysiol. 92 (1994) 414–421. ¨¨ ¨ [12] R. Naatanen, A. Lehtokoski, M. Lennes, M. Cheour, M. Huotilainen, A. Iivonen, M. Vainio, P. Alku, R.J. Ilmoniemi, A. Luuk, J. Allik, J. Sinkkonen, K. Alho, Language-specific phoneme representations revealed by electric and magnetic brain responses, Nature 385 (1997) 432–434. [13] D. Naka, R. Kakigi, M. Hoshiyama, H. Yamasaki, T. Okusa, S. Koyama, Structure of the auditory evoked magnetic fields during sleep, Neuroscience 93 (1999) 573–583. [14] N. Nakasato, S. Fujita, K. Seki, T. Kawamura, A. Matani, I. Tamura, S. Fujiwara, T. Yashimoto, Functional localization of bilateral auditory cortices using an MRI-linked whole head magnetoencephalography (MEG) system, Electroencephalogr. Clin. Neurophysiol. 94 (1995) 183–190. [15] T. Rinne, K. Alho, P. Alku, M. Holi, J. Sinkkonen, J. Virtanen, O. ¨¨ ¨ Bertrand, R. Naatanen, Analysis of speech sounds is left-hemisphere predominant at 100–150 ms after sound onset, Neuroreport 10 (1999) 1113–1117. [16] R. Salmelin, A. Schnitzler, L. Parkkonen, K. Biermann, P. Helenius, K. Kiviniemi, K. Kuukka, F. Schmitz, H. Freund, Native language, gender, and functional organization of the auditory cortex, Proc. Natl. Acad. Sci. USA 96 (1999) 10460–10465. [17] J. Sarvas, Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem, Phys. Med. Biol. 32 (1987) 11–22. [18] M. Scherg, Functional imaging and localization of electromagnetic brain activity, Brain Topogr. 5 (1992) 103–111. [19] K. Shimizu, Transfer effects in the production of English vowels by Japanese learners, in: Proceedings of the 14th International Congress of Phonetic Sciences (ICPhS), 1999, pp. 1463–1465. [20] M. Tervaniemi, A. Kujala, K. Alho, J. Virtanen, R.J. Ilmoniemi, R. ¨¨ ¨ Naatanen, Functional specialization of the human auditory cortex in processing phonetic and musical sounds: A magnetoencephalographic (MEG) study, Neuroimage 9 (1999) 330–336. [21] H. Yabe, M. Tervaniemi, J. Sinkkonen, M. Huotilainen, R.J. ¨¨ ¨ Ilmoniemi, R. Naatanen, Temporal window of integration of auditory information in the human brain, Psychophysiology 35 (1998) 615–619. [22] R.J. Zatorre, A.C. Evans, E. Meyer, Neural mechanisms underlying melodic perception and memory for pitch, J. Neurosci. 14 (1994) 1908–1919.
Research report
Hemispheric lateralization in an analysis of speech sounds Left hemisphere dominance replicated in Japanese subjects Sachiko Koyama a , *, Atsuko Gunji a , Hirooki Yabe b , Shoko Oiwa a , Reiko Akahane-Yamada c , d ¨¨ ¨ Ryusuke Kakigi a , Risto Naatanen a
Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki, Aichi, 444 -8585, Japan b Department of Neuropsychiatry, Hirosaki University School of Medicine, Hirosaki, Japan c ATR Human Information Processing Research Laboratories, Kyoto, Japan d Cognitive Brain Research Unit, Department of Psychology, Helsinki University, Helsinki, Finland Accepted 16 May 2000
Abstract ¨¨ ¨ Evoked magnetic responses to speech sounds [R. Naatanen, A. Lehtokoski, M. Lennes, M. Cheour, M. Huotilainen, A. Iivonen, M. Vainio, P. Alku, R.J. Ilmoniemi, A. Luuk, J. Allik, J. Sinkkonen and K. Alho, Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature, 385 (1997) 432–434.] were recorded from 13 Japanese subjects (right-handed). Infrequently presented vowels ([o]) among repetitive vowels ([e]) elicited the magnetic counterpart of mismatch negativity, MMNm (Bilateral, nine subjects; Left hemisphere alone, three subjects; Right hemisphere alone, one subject). The estimated source of the MMNm was stronger in the left than in the right auditory cortex. The sources were located posteriorly in the left than in the right auditory cortex. ¨¨ ¨ These findings are consistent with the results obtained in Finnish [R. Naatanen, A. Lehtokoski, M. Lennes, M. Cheour, M. Huotilainen, A. Iivonen, M.Vainio, P.Alku, R.J. Ilmoniemi, A. Luuk, J. Allik, J. Sinkkonen and K. Alho, Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature, 385 (1997) 432–434.][T. Rinne, K. Alho, P. Alku, M. Holi, J. Sinkkonen, J. ¨¨ ¨ Virtanen, O. Bertrand and R. Naatanen, Analysis of speech sounds is left-hemisphere predominant at 100–150 ms after sound onset. Neuroreport, 10 (1999) 1113–1117.] and English [K. Alho, J.F. Connolly, M. Cheour, A. Lehtokoski, M. Huotilainen, J. Virtanen, R. Aulanko and R.J. Ilmoniemi, Hemispheric lateralization in preattentive processing of speech sounds. Neurosci. Lett., 258 (1998) 9–12.] ¨¨ ¨ subjects. Instead of the P1m observed in Finnish [M. Tervaniemi, A. Kujala, K. Alho, J. Virtanen, R.J. Ilmoniemi and R. Naatanen, Functional specialization of the human auditory cortex in processing phonetic and musical sounds: A magnetoencephalographic (MEG) study. Neuroimage, 9 (1999) 330–336.] and English [K. Alho, J.F. Connolly, M. Cheour, A. Lehtokoski, M. Huotilainen, J. Virtanen, R. Aulanko and R.J. Ilmoniemi, Hemispheric lateralization in preattentive processing of speech sounds. Neurosci. Lett., 258 (1998) 9–12.] subjects, prior to the MMNm, M60, was elicited by both rare and frequent sounds. Both MMNm and M60 sources were posteriorly located in the left than the right hemisphere. 2000 Elsevier Science B.V. All rights reserved. Theme: Sensory systems Topic: Auditory system: central physiology Keywords: Mismatch negativity; Speech; Magnetoencephalography; Auditory cortex; Hemispheric lateralization
1. Introduction Deviant sounds infrequently embedded in a repetitive sequence of auditory stimuli (standard) elicit mismatch negativity (MMN) or its magnetic counterpart (MMNm) *Corresponding author. Tel.: 181-564-557-769; fax: 181-564-527913. E-mail address: [email protected] (S. Koyama).
[1–3,6,8,10,12,15,20,21]. Since MMN or MMNm has been observed even when subjects perform tasks that are completely unrelated to auditory stimuli, they have been regarded as an index of the pre-attentive automatic detection system of auditory stimulus change. Recent studies ¨¨ ¨ by Naatanen and his colleagues showed that MMN or MMNm to speech sounds showed left hemisphere dominance [3,12,15], whereas MMM or MMNm to pure tones [10] and musical cords [20] showed right hemisphere
0926-6410 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S0926-6410( 00 )00034-3
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dominance. These results indicate that the left hemisphere dominance in speech sounds starts as early as at the pre-attentive processing level. On the other hand, using Japanese subjects, Imaizumi et al. [8] did not find a left hemisphere dominance for MMNm while subjects passively heard a series of speech sounds. When the subjects performed a phoneme detection task, MMNm showed left hemisphere dominance. However, it should be noted that the stimuli were verbs of two syllables not vowels or consonant–vowel syllables which ¨¨ ¨ Naatanen and his colleagues have used [12,15,20]. They used three different forms of the Japanese verb / iku / (to go) which consisted of vowel-consonant–vowel syllables; / itta / (statement, past tense), / itta / ? (question, past tense) and / itte / (demand). / itta / (past tense) had a falling pitch pattern and / itta / ? had a rising pitch pattern. Their stimuli included syntactic factors and were longer in duration than simple vowels or consonant-vowel syllables. The aim of the present study was to examine the laterality of MMNm for simple vowels in Japanese subjects. To make a direct comparison with results reported by ¨¨ ¨ Naatanen et al. [12], the same stimuli, / e / and / o /, were used and most of the experimental parameters were the same., The / e /, / o / prototypes of Japanese are similar in those of Finnish [19].
2. Method The subjects were 13 native Japanese (7 females and 6 males; aged 25–40 years, right-handed). Stimuli were binaurally presented through plastic tubes and ear-pieces. The duration of the stimuli was 400 ms including 10 ms rise and fall times. The stimulus-onset asynchrony was 900 ms. Subjects were instructed to watch a silent film and to ignore the auditory stimulation. The total number of trials was 1200 (/ e /, 1020 trials and / o /, 180 trials) and they were presented in a random order. The intensity of / e / was 65 dBL and the loudness of / o / was adjusted to be the same as / e / in each subject before the MEG recording. Magnetic responses were measured with dual 37-channel gradiometers (Magnes, Biomagnetic Technologies Inc., USA). The gradiometers were placed over the left and right temporal sites. The responses were recorded with a 0.1–50 Hz bandpass filter at a sampling rate of 520.8 Hz. The mean value of the signals for 50 ms prior to the stimulus onset was used as the baseline in each channel. Epochs with signal variations of larger than 3.0 pT were excluded from the averaging. Vertical electro-oculograms (EOGs) were recorded simultaneously to monitor eye movements. Epochs with signal variations of larger than 80 mV in the EOG were also excluded from the averaging. The responses to frequent sounds were subtracted from those to the deviant sounds to determine the MMNm. Equivalent current dipoles of the MMNm were analyzed using BESA (version 2.1m) [17,18]. Taking a spatio–
temporal modeling approach, BESA decomposes the recorded responses into a number of discrete neuronal source activities overlapping in time and estimates the strength and timing of each source current over a defined interval. BESA calculates the locations and orientations of dipoles in a spherical head conductor model by an iterative leastsquares fit. The goodness-of-fit (GOF) of the model was expressed as a percentage of the residual variance (%RV) between the observed fields and the theoretical fields generated by the source model. The mean analysis epoch was 65 ms (range: 49–76 ms) in the left hemisphere and 70.6 ms (range: 53–98 ms) in the right. We accepted the source model in which the RV was below 6% with one or two sources. A source in the lower bank of the Sylvian fissure was obtained all the subjects who had MMNm. In addition, half of the subjects (four subjects in the left and seven subjects in the right hemisphere) had a second source located in the cortical area other than the auditory cortex. The location for second sources had actually several possible ‘candidate’. The accuracy of dipole localization depends on the distance between the source and sensor array [4,7,9]. The error increases with increasing a distance between the source and a sensor array. Therefore, the model which had shortest distance between the second source and the center of the sensor array, was selected, when several source models with the RV below 6% for 2 dipoles was obtained. Besides MMNm, a magnetic component peaking at around 60 ms, M60, after the stimulus presentation was observed both for frequent and deviant sounds all the subjects. Source location of M60 was estimated using a single moving dipole model [17] at the peak of M60. Correlation between the theoretical fields generated by the model and the observed fields was used to estimated the goodness of fit of the model and only models whose correlation above 0.97 were accepted. The locations of the estimated sources were described in a head-based coordinate system (see Fig. 2B). The origin of the system was set at the midpoint between preauricular points. The x-axis joins the nasion and the origin. The x-axis thus indicates a coronal plane with positive values in the anterior direction. The y-axis extended from the origin to the left side of the head such that it was perpendicular to the x-axis. The y-axis indicates the sagittal plane with positive values to the left preauricular point. The z-axis indicates the axial plane with positive values directed upward such that it was perpendicular to the x and y axes.
3. Results Fig. 1 shows magnetic responses and estimated sources recorded from one subject. In this subject, the recorded MMNm itself was larger in the right hemisphere than in the left. In the left hemisphere, the zero-level line of the
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Fig. 1. Evoked magnetic responses and their estimated sources in one subject. It should be noted that MMNm (B) were larger for the right than for the left hemisphere. However, the estimated source strength of MMNm (C) was larger for the left than for the right hemisphere. (A) Magnetic responses from 2 sensors to rare [o] and frequent [e] sounds and approximate location of 37 sensors illustrated by circles. (B) Difference in responses to rare sounds and to frequent sounds and the iso-contour maps (step 20 fT) of difference responses. The shadowed area illustrates magnetic flux out of the white area into the skull. Thick line indicates the zero level. (C) The estimated source location and strength.
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iso-contour map is almost straight, indicating that the single dipole source is located under the sensor arrays. In the right hemisphere, the contour pattern suggests that there is a source located somewhat anterior to that in the left hemisphere and that there is another source. Source analysis indicated a single source (latency range of 93.2– 164.0 ms, RV54.8%) in the left auditory cortex and two sources in the right hemisphere (latency range of 81.1– 158.0 ms, RV54.2%): one in the auditory cortex, and the other in the cortex around the posterior part of the Sylvian fissure. The strength of the source in the auditory cortex was larger in the left than in the right hemisphere.
3.1. MMNm Clear mismatch fields (MMNm) were bilaterally observed in nine subjects (Left hemisphere alone, three subjects; Right hemisphere alone, one subject). As a result, the sources could be estimated in all the observed MMNm. Fig. 2 shows the strength of MMNm estimated in the auditory cortex (A) and the location of individual MMNm sources in the coronal section (B). A repeated-measure analysis of variance (ANOVA, one-way with a factor of hemisphere) was performed for the data from the 9 subjects who had bilateral MMNm. The analysis revealed that the peak strength of the MMNm source was significantly greater in the left than that in the right hemisphere (F(1, 8)517.88, P,0.01). The mean peak latency of the source was 117.1612.0 ms in the left and 120.8614.8 ms in the right hemisphere. Repeated-measure ANOVAs with a factor of hemisphere were also performed for x, y, z values of the MMNm source location from nine subjects. The difference in x values reached significance (F(1, 8)59.54, P,0.05), indicating that the sources in the left hemisphere were more posteriorly located than those in
the right hemisphere. The difference in y- and z-values (F ,1) was not significant. In the left hemisphere, four subjects had a second source. These sources were located in the cortex around the posterior end of the Sylvian fissure for two subjects and the precentral area for two subjects. The peak amplitude of the source around the posterior end of the Sylvian fissure was 20.2 and 7.8 nAm and the peak latency was 121.7 and 108.4 ms. The peak amplitude of the source in the precentral area was 16.9 and 5.4 nAm and the peak latency was 114.1 and 127.4 ms. In the right hemisphere, seven subjects had a second source as shown in Fig. 1. The sources were located in the cortex around the posterior end of the Sylvian fissure (five subjects), the pre-motor area (two subjects). The peak amplitude of the source around the posterior end of the Sylvian fissure ranged between 4.3 and 24.7 nAm and the peak latency ranged between 95.1 and 142.6 ms. The amplitude of the source in the precentral area was 7.4 and 11.0 nAm and the latency was 108.4 and 150.2 ms.
3.2. M60 Bilateral M60 was observed in 11 subjects for frequent sounds (right alone, two subjects). The mean peak latency was 57.365.2 ms in the left hemisphere and 58.765.5 ms in the right. In the left hemisphere, the source location was successfully estimated in all the 12 subjects who showed M60. The mean source strength was 9.763.5 nAm. In the right hemisphere, the source location was successfully obtained in 11 out of 13 subjects who showed M60. The mean strength was 10.864.2 nAm. The source location for the frequent sounds is shown in Fig. 2B. A repeatedmeasure ANOVA with a factor of hemisphere was performed for the data (source strength and x, y, z values)
Fig. 2. Strength and location of the MMNm source estimated in the auditory cortex. (A) Peak source strength of MMNm. The data from the same subjects are linked with a line (black circle). The data from the subjects who had MMNm in only one hemisphere are shown in gray. The source strength was significantly greater in the left hemisphere than the right. (B) The axial location (x–y plain) of sources for MMNm (dot) and M60 for frequent stimuli (cross).
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from 11 subjects whose M60 source was bilaterally estimated. The difference in x values reached significance (F(1, 9)533.22, P,0.001) indicating that the source in the left hemisphere was more posteriorly located than that in the right hemisphere. The difference in y- (F ,1) and z-values (F ,1) was not significant. The difference in source strength was not significant (F(1, 9)51.62). For deviant sounds, M60 was bilaterally observed for nine subjects (the left hemisphere alone for one subject, the right hemisphere alone for one subject). The mean peak latency was 55.265.7 ms in the left hemisphere and 57.165.6 ms in the right. In the left hemisphere, the source location was successfully estimated in eight out of ten subjects who showed M60. The mean source strength was 11.265.5 nAm. In the right hemisphere, the source location was successfully obtained in six out of ten subjects who showed M60. The mean strength was 14.164.7 nAm. To compare the locations of M60 for frequent sounds and MMNm within each subject, x, y and z values were analyzed with repeated-measure ANOVAs in each hemisphere (11 subjects in the left hemisphere, 10 subjects in the right hemisphere). For x-values in the left hemisphere, the location of the two components was significantly different (F(1, 10)55.80, P,.05), indicating that M60 was more posteriorly located than MMNm. Other differences in the location between the components were not significant.
4. Discussion The present study indicates that the MMNm to speech sounds showed left hemisphere dominance in Japanese subjects. This finding was in line with those of previous studies using Finnish [12,15,20] and English subjects [3] that reported a left-hemisphere dominance of MMNm source strength for speech sounds. The latency of MMNm was also comparable to that in Finnish subjects [12,15,20]. Our results thus indicated that regardless of the native language, vowel processing predominantly occurs in the left hemisphere. Since the y-values (lateral location) of the source location did not differ between the hemispheres, hemispheric differences in MMNm source strength were probably not apparent (in source modeling, the deeper the source location, the greater the strength). Four subjects in the left hemisphere and seven subjects in the right hemisphere had second sources. The precentral source (two subjects in both hemispheres) might be comparable to a frontal source reported in event-related brain potential studies [2,6]. The sources located around the posterior end of the Sylvian fissure (two subjects in the left hemisphere and five subjects in the right hemisphere) may be comparable to the parietal source [10]. The peak latency of the second source is similar to that of the primary source in the auditory cortex, the second source is
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possibly a part of MMNm. The validity of second source is not clear thus far and further studies will be required. Contrary to our study, Imaizumi et al. [8] did not find a left-hemisphere dominance of MMNm to speech sounds. Since they used verbs rather than simple vowels, syntactic factors might modulate the hemispheric balance of MMNm. Alternatively, the duration of the stimuli may have an effect. Their stimuli were longer in duration than those of other MMNm studies (360 ms total). A recent MMN study estimated that the temporal window of stimulus integration for temporally close sounds into a unitary event, is about 160–170 ms [21]. The duration of those stimuli was longer than the temporal window and this might affect the MMNm laterality for speech sounds. Another possible explanation is that their stimuli included prosodic changes. Using PET, Zatorre et al. [22] suggested that prosodic aspects of spoken language are processed by the right hemisphere. Pre-attentive prosodic processing might modulate the laterality of MMNm in their study. Another possible reason for the discrepancy between the two studies is dipole analysis. They estimated only one source for MMNm. On the other hand, half of our subjects had two sources in the right hemisphere. As shown in Fig. 1, observed magnetic responses did not show the left hemisphere dominance in most of our subjects. If the single source analysis were applied to our data, MMNm strength might not show the left hemisphere dominance. The multiple-source analysis is thus quite helpful for precise estimation of the MMNm in the auditory cortex, even if the second source obtained here might be a byproduct of subtracting procedure and apparent. The MMNm sources in the auditory cortex were located more posteriorly in the left than in the right hemisphere. The results also replicated the findings obtained in Finnish [15,20] and English subjects [3]. These results are consistent with the finding that aphasic patients with lesion of the posterior temporal lobe in the left hemisphere showed no MMN to a phoneme deviation but had a normal MMN ¨ to frequency change [1]. However, Levanen et al. [10] reported a similar asymmetrical source location for MMNm to pure tones (MMNm elicited by frequency change). Moreover, the left-hemisphere source of M100 for pure tones was found to be more posterior to that in the right hemisphere in Finns [16], Germans [5,16], and Japanese [14]. Such hemispheric asymmetries in source location might thus not be language specific. The M60 was reported in previous studies using pure tones [11,13]. The M60 sources in the auditory cortex were also located posteriorly in the left than those in the right hemisphere. The source of M60 was located posteriorly than that of MMNm in the left hemisphere, but did not differ from that of MMNm in the right hemisphere. In previous studies using Finnish [20] and English [3] subjects, P1m peaking at around 80 ms was observed for both frequent and deviant speech. In Finnish subjects, P1m tended to be located posteriorly than MMNm in both
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hemispheres. We did not observe the P1m equivalent in the present study. Recently Salmelin et al. [16] reported that the source location of N100m to 1 kHz tone differed between Finnish and German male subjects. They suggested that linguistic environments might change functional organization of the auditory cortex. The difference in middle-latency responses might be attributed to the difference in linguistic environments between subjects.
Acknowledgements This study was supported by Grants-in-Aid for Scientific Research, Ministry of Education, Science, and Culture, Japan to S. Koyama (No. 11111230, 12011223) and H. Yabe (09670972, 09710064), R. Kakigi (No. 08878160, 09558102). We are grateful to Doctor Miyauchi for the use of MRI facilities. We thank Doctors M. Matsui and K. Kurakata for their comments and O. Nagata and Y. Takeshima for technical assistance.
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