Department of Radiology and Psychiatry, National Center Hospital of Mental, Nervous and Muscular Disorders, National Center of Neurology and Psychiatry and , 1 Department of Music, Tokyo National University of Fine Arts and Music, 4-1-1 Ogawa higashi, Kodaira City, Tokyo 187-8551, Japan
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Abstract |
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Introduction |
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Materials and Methods |
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Two groups, comprising right-handed subjects (Edinburgh handedness questionnaire) without history of neurological and psychiatric disorders and with normal audiological status, participated in the present study. The first group (n = 14) consisted of musical students (2027 years old, two males and 12 females, with >12 years of 48 h of training per day) with AP (n = 10) or relative pitch (n = 4). Musicians were recruited from Tokyo National University of Fine Arts and Music. Before the experiment we interviewed musicians to collect information about the number of hours of practice, sight-reading ability, AP ability, the principal instrument and other instruments played, and the age at which musical training began. Absolute pitch ability was verified with an objective pitch identification test and a difficult solfeggio test consisting of atonal melodies and tension codes. The principal instruments of musicians were percussion (11 subjects) and piano (three subjects). All of them began musical training with the piano. Ten out of 12 musicians began their musical practice before 10 years old (mean age 6.2 ± 2.79 years old, range 316 years old). The age- and gender-matched control group (n = 14, 2127 years, two males and 12 females) consisted of undergraduate and graduate students who had never played an instrument and had no formal musical education. Written informed consent was obtained from all subjects in accord with the ethical guidelines laid down by the local ethical committee.
Task
During fMRI, binaural presentation of an instrumental music stimulus (a part of Italian concert BMV 989 by J.S. Bach which was digitally recorded) in and on/off paradigm with 24 s epochs was given. As far as we know, this piece have been never played vocally and all recorded versions were played by keyboard instruments, such as the piano or cembalo. The stimulus was presented by an air-conducting headphone. The same segment of music was played for 24 s at a comfortable listening level during each on period. Subjects were asked to just passively listen to music. They were also asked not to accompany or sing with the listened music. During the off period, no auditory stimulus were given and subjects were discouraged from thinking anything.
Post Hoc Questionnaire
We presented subjects with a post hoc questionnaire after fMRI measurements. The questionnaire was consisted of the following questions:
The questionnaire revealed that 14 out of 17 musicians and all control subjects had never heard this particular piece. Two pianists and one composer played it, so we therefore eliminated these three musicians from the subjects for this study.
fMRI Procedure
Cerebral activation was measured with fMRI using blood oxygen level- dependent contrast (Ogawa et al., 1990). After automatic shimming, a time course series of 75 volumes were obtained using single-shot gradient- refocused echo-planar imaging (TR = 3000 ms, TE = 60 ms, flip angle = 90°, in-plane resolution = 3.44 x 3.44 mm, FOV = 22 cm, contiguous 4 mm slices to cover the entire brain) with a 1.5 T MAGNETOM Vision plus MR scanner (Siemens, Erlangen, Germany) using a standard head coil. Head motion was minimized by placing tight but comfortable foam padding around the subject's head.
Data Analysis
Data were analyzed with Statistical Parametric Mapping software (SPM99, www.fil.ion.ucl.ac.uk/spm). The first five volumes of each fMRI scan were discarded because of the non-steady condition of magnetization, and the remaining 70 volumes were used for the analysis. Scans were realigned and spatially normalized to the standard stereotactic space of Talairach using an EPI template. The parameter for affine and quadratic transformation to the EPI template that was already fitted for Talairach space was estimated by least-squares means. Data were then smoothed in a spatial domain (full width at half-maxim = 8 x 8 x 8 mm) to improve the signal-to-noise ratio. After specifying the appropriate design matrix, delayed box-car function as a reference waveform, the condition, slow hemodynamic fluctuation unrelated to the task, and subject effects were estimated according to the general linear model and temporal smoothness into account. Global normalization was performed using proportional scaling. To test hypotheses about regionally specific condition effects, the estimates were compared by means of linear contrasts of each rest and task period. The resulting set of voxel values for each contrast constituted a statistical parametric map of the t statistic SPM{t}. Previous studies have indicated that the right superior temporal gyrus (STG) must be specialized for processing of music perception (Mazziotta et al., 1982; Liegeois-Chauvel et al., 1998
; Zatorre, 1998
; Tervaniemi et al., 2000
). Therefore, we determine lateralization of STG activation in each subject. The volume of activation in the STG of each hemisphere was determined as numbers of voxels exceeding a significance threshold of a = 0.005. A laterality index (LI) was calculated, corresponding to [left right]/[left + right] x 100. This approach yields values ranging between +100 (strong left hemisphere dominance) and 100 (strong right hemisphere dominance). Furthermore, we applied a random effect model to generalize the inference drawn from multi-subject fMRI data (Friston et al., 1999
). Images of the estimated activation parameter ai were written out as an image. The inter-subject level of analysis proceeds using these subject images as raw data for a one-sample t-test (P = 0.001, uncorrected). The difference between musicians and controls were estimated using these subject images as raw data for a two-sample t-test (P = 0.001, uncorrected). A regression analysis was also done to find where the activation parameter ai responded linearly to the age at which musical training began and scores of the solfeggio test (P = 0.001, uncorrected).
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Results |
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None of the musicians employed as subjects could remember the precise title of the musical stimulus and had never played it; however, most musicians answered that it may have been composed by Bach or Handel. They also had not heard the stimulus before scanning. None of the control subjects had heard the musical stimulus before scanning. However, they recognized that it may be some kind of baroque music.
All musicians answered that they had just listened to the music and had not tred to analyze or memorize it. None of them tried to imagine the score of the presented music or to accompany it.
Cerebral Activation during Passive Music Listening in Musicians and Controls
When compared with the resting baseline, the passive music listening produced significant activation in the bilateral superior and the middle temporal gyri [Brodmann's areas (BA) 21 and 22], known as the auditory association cortex, in both musicians and control subjects. The control subjects demonstrated right dominant temporal cortical activation (BA21 and BA22) during passive music listening (Fig. 1a, Table 1
). Contrary to the control group, musicians showed left dominant temporal cortical activation (BA22, 21) during the same task (Fig. 1b
, Table 1
). t-values of temporal activations were greater on the left side for the musicians and greater on the right for the non-musicians. The laterality index in the STG of the musicians was significantly greater than that of the control group (two-sample t-test; P < 0.01, mean ± SD = 18.3 ± 14.8 in the musicians and 21.4 ± 5.35 in the control group).
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The Correlation between Cerebral Activation and the Age of Inception of Musical Training, Duration of Training and Absolute Pitch Ability
There was a significant negative linear correlation between the age of inception of musical training and the degree of activation in the left PT (BA22) (y = 0.3 0.049x, r = 0.855) (Fig. 2a,b, Table 1
). However, no correlation between the duration of musical training and the degree of cerebral activation was seen in any region. There was a significant positive linear correlation between the AP ability determined by the solfeggio test and the degree of activation in the left posterior DLPFC (BA9) (y = 0.84545 + 0.009471x, r = 0.78) (Fig. 3a,b
, Table 1
) and the left PT (BA22) (y = 2.06 + 0.0228x, r = 0.781) (Fig. 3a,c
, Table 1
).
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Discussion |
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The activation patterns in the musicians can be characterized as follows: (i) stronger activation in the PT than in non-musician controls; (ii) left dominant activation in the secondary auditory area, including the PT; and (iii) co-activation in the left posterior DLPFC (BA9). The results should be seen in the following contexts. First, neuroimaging studies have revealed that the posterior temporal area, including the PT, is involved in various aspects of pitch processing (Mazziotta et al., 1982; Binder et al., 1996
; Griffiths et al., 1998
; Liegeois-Chauvel et al., 1998
; Zatorre, 1998
). Secondly, earlier structural magnetic resonance morphometry has suggested that AP might be associated with an anatomical difference in the left PT (Schlaug et al., 1995
; Zatorre et al., 1998
). Thirdly, a previous PET study indicated that activation in the left posterior DLPFC might represent part of the substrate for AP processing (Zatorre et al., 1998
). Fourthly, behavioral studies have demonstrated a difference in lateralization of musical processing between musicians and non-musicians, with more left-lateralized representation in musicians (Bever and Chiarello, 1974
; Mazzucchi et al., 1981
). Finally, magnetic source imaging studies have revealed increased cortical representation of the somatosensory and auditory areas in skilled musicians (Elbert et al., 1995
; Pantev et al., 1998
). Therefore, our results may suggest that increasing musical sophistication should cause a shift of musical processing, or at least music perception, from the right to the left hemisphere and from the anterior portion of the superior temporal region to the posterior.
We suggest that activations in the PT and left DLPFC should be associated with AP processing and use-dependent functional reorganization caused by early engagement of musical training. Before the fMRI experiment, musicians were interviewed to determine the age at which their musical training had begun and tested AP ability by using a difficult solfeggio test. There was a significant negative linear correlation between the age of inception of musical training and the degree of activation in the left PT (BA22). The data suggest that the degree of the use-dependent functional reorganization could depend on the age at which musical training began. This finding is similar to those reported in previous studies, which examined somatosensory representation of fingering digits in string players and cortical representation for piano tones in musicians (Elbert et al., 1995; Pantev et al., 1998
). Although it is possible that such a functional reorganization could be dependent on the duration of training, we could not find any correlation between the duration of training and the degree of cerebral activation. In addition to the results of previous studies (Elbert et al., 1995
; Pantev et al., 1998
), our data suggest that functional reorganization of the left PT in musicians could be caused by the early commencement of training rather than long-term training. The left dominant PT activation for music perception that we observed in musicians corresponds to the result of an earlier MR study: a structural enlargement of the left PT in musicians (Schlaug et al., 1995
; Zatorre et al., 1998
). Our data therefore associate the use-dependent functional property with cortical architectonics and raise the possibility that musical experience during childhood may influence structural development of PT.
One possible alternative interpretation of the results here is that the different activation pattern only reflects a different strategy of musical perception that calls on the left hemispheric function (Mazziotta et al., 1982). A previous PET study reported that left dominant temporo-parietal activation was found when subjects used highly organized analytical approaches during a tonal memory task. In that study, greater activation of the right side than of the left auditory areas during the same task was found when subjects did not use a specific strategy (using visual imagery) (Mazziotta et al., 1982
). However, we asked our musicians to listen to the music passively. Indeed, the post hoc questionnaire revealed that they did not employ any specific analytic approach, especially visual imagery, during the fMRI measurements. Although they did not use any specific strategy consciously, it is still possible that the musicians have developed a different way of listening to music, which is inherently more analytical. There is a possibility that musical training not only changes the regions involved in musical perception, but may also change how the music is perceived.
The left PT is known as Wernicke's area, which is related to language comprehension. The human PT is a roughly triangular region of the superior temporal plane located posterior to the primary auditory field. It is, on average, larger in the left hemisphere, suggesting that it may play a specialized role in language and language lateralization (Steinmetz et al., 1991). Why is the left PT involved in music perception in trained musicians? Do they employ a common strategy in music perception and language comprehension? We consider that the stronger PT activation in musicians than in controls could be related to AP processing. There was a significant positive linear correlation between the AP ability determined by the solfeggio test and the degree of activation in the left posterior DLPFC (BA9) and PT (BA22) (Fig. 3
, Table 1
). Because note labeling is obligatory for AP processors even when passively listening, these activations should represent part of the substrate for AP ability (Marin and Perry, 1999
). Although a previous PET study indicated that the PT did not contribute to AP ability (Zatorre et al., 1998
), morphometric measures of the PT have suggested that AP may be associated with a structural difference in the left PT (Schlaug et al., 1995
; Zatorre et al., 1998
). Taken together, AP ability may arise from a qualitatively different neural process within the left PT. The left posterior DLPFC is also thought to be a part of the substrate for AP (Zatorre et al., 1998
). Our data also indicated that the left posterior DLPFC should be associated with AP ability. Functional neuroimaging studies of the human prefrontal cortex have revealed that it is associated with a broad range of different cognitive demands, such as perception, response selection, working memory and problem solving (Duncan and Owen, 2000
). The posterior DLPFC has been shown to be important for conditional-associative learning of sensory stimuli (Petrides, 1985
, 1990
). Therefore, AP may be characterized as the ability to retrieve an association between a stimulus attribute (the pitch of sound) and a verbal label of the note name, such as A, D-flat, etc. Furthermore, the PT contains an auditory association area that projects directly to the most posterior portion of the DLPFC (Petrides and Pandya, 1988
). We assume that AP ability may result from at least two neural mechanisms. One such possible mechanism is a form of conditional-associative learning (verbaltonal association), which results from an interaction between computations in the PT and the left DLPFC. Another is the different initial stage of perceptual analysis processed in the left PT.
In conclusion, there is a distinct cerebral activity pattern in the auditory association areas and prefrontal cortex of trained musicians. Such activity could be associated with AP ability and the use-dependent functional reorganization produced by longterm training.
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Notes |
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Address correspondence to Takashi Ohnishi, Department of Radiology and Psychiatry, National Center Hospital of Mental, Nervous and Muscular Disorders, National Center of Neurology and Psychiatry, 4-1-1 Ogawa higashi, Kodaira City, Tokyo 187-8551, Japan. Email: tohnishi{at}hotmail.com.
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