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DEVELOPMENTAL NEUROPSYCHOLOGY, 38(5), 281–300 Copyright © 2013 Taylor & Francis Group, LLC ISSN: 8756-5641 print / 1532-6942 online DOI: 10.1080/87565641.2013.799672

The Development of Mismatch Responses to Mandarin Lexical Tones in Early Infancy Ying-Ying Cheng Institute of Neuroscience, National Yang-Ming University, Taipei City, Taiwan

Hsin-Chi Wu Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation, New Taipei City, Taiwan, and School of Medicine, Tzu Chi University, Hualien, Taiwan

Yu-Lin Tzeng Institute of Neuroscience, National Yang-Ming University, Taipei City, Taiwan

Ming-Tao Yang Far Eastern Memorial Hospital, New Taipei City, Taiwan

Lu-Lu Zhao Taipei Tzuchi Hospital, The Buddhist Tzuchi Medical Foundation, New Taipei City, Taiwan

Chia-Ying Lee Institute of Neuroscience, National Yang-Ming University, Taipei City, Taiwan, The Institute of Linguistics, Academia Sinica, Taipei City, Taiwan, and Institute of Cognitive Neuroscience, National Central University, Taoyuan, Taiwan

This study examined how maturation and the size of deviance affect the development of mismatch responses to Mandarin lexical tones by a multi-deviant oddball paradigm with both large deviant T1/T3 and small deviant T2/T3 pairs in newborns and 6-month-olds. The T1/T3 pair elicited a positive mismatch response (P-MMR) at birth but an adult-like mismatch negativity (MMN) at 6 months of age. For the T2/T3 pair, no significant MMR was seen in newborns, whereas a P-MMR was found when infants are 6 months old. Results suggest that the developmental trajectories of MMRs are dependent on the neural maturation and the discriminability of tonal changes.

Correspondence should be addressed to Chia-Ying Lee, The Institute of Linguistics, Academia Sinica, 128, Section 2, Academia Road 115, Taipei, Taiwan, R.O.C. E-mail: [email protected]

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A growing body of studies suggests that the auditory cortical response to acoustic changes recorded by event-related potentials (ERPs) in early infancy may serve as early markers for predicting later language and cognitive development. For example, longitudinal studies reported that newborns’ ERPs to the processing of stop-consonant vowel (CV) syllables predict their pre-reading language skills between 2.5 to 6.5 years of age (Guttorm, Leppänen, Hamalainen, Eklund, & Lyytinen, 2010; Guttorm et al., 2005; Molfese & Molfese, 1985, 1997) and their reading performance at 8 years of age (Molfese, 2000). ERPs to the auditory changes of pure tones in newborns (Leppänen et al., 2010) and of stress patterns in 5-month-olds (Weber, Hahne, Friedrich, & Friederici, 2005) also predict their language outcomes. However, the maturation timetable of auditory change-related cortical responses varies in different sound features, which play different weightings across languages. This study investigated how maturation and acoustic similarity affect the development of mismatch responses (MMRs) to Mandarin lexical tones in adults and infants from birth to 6 months old. The auditory change-related cortical response can be indexed by an ERP component called mismatch negativity (MMN). MMN is typically obtained using an auditory oddball paradigm, in which a deviant in certain aspects of a sound feature occurs infrequently in a sequence of repetitive homogeneous (standard) stimuli (Näätänen, Kujala, & Winkler, 2011; Näätänen, Paavilainen, Rinne, & Alho, 2007). In adults, MMN is a frontal-central distributed negativity peaking between 100 msec and 250 msec by subtracting the ERP to the standard from that to the deviant. The MMN amplitude increases, whereas the peak latency decreases as the discriminability of the standard and the deviant sounds rise. MMN is hypothesized to index change detection based on a sound representation constructed to a repeated auditory input and to reveal whether listeners have formed sufficient and robust representations of automatic pre-attentive discrimination (Näätänen et al., 2007; Winkler, 2007). Cross-linguistic studies have shown that MMN is sensitive to language experiences, even for infants one year old and younger. Cheour and colleagues (1998a) reported that Finnish 12-month-olds showed an enhanced MMN response to their native vowel contrast, as compared with the non-native Estonian vowel contrast, even when the non-native contrast had a more distinct acoustic difference (Cheour et al., 1998a). Infants as young as 4 months of age showed processing advantages to the typical stress pattern in their native language indexed by the presence of mismatch responses (Friederici, Friedrich, & Christophe, 2007). It suggests that, in addition to automatic change detection in short-term memory, MMN is sensitive to the long-term memory trace built on language experience. Most important, the MMN can be elicited, even when a participant does not attend to the stimuli, such as reading a book or watching a silent movie. Thus, the MMN serves as an excellent tool for assessing auditory discrimination, especially for infants and children with limited attention or motivation. Tracing MMN to various speech units might demonstrate how infants allocate attention to processing speech at different ages, and can provide information on whether native language speech perception has become automatized. Although MMN is well established in adults, the polarity and latency of mismatch response in infants are highly inconsistent across studies. Alho, Sainio, Sajaniemi, Reinikainen, and Naatanen (1990) first reported an adult-like MMN, which has mean peak latencies 296 msec at Fz and 270 msec at Cz, for pure tone deviance in quiet sleeping newborns. Cheour et al. found an adult-like MMN peaking at approximately 380 msec to 400 msec in newborns and infants when responding to changes in pure tones (Cheour, Kushnerenko, Ceponiene, Fellman, & Näätänen, 2002; Cheour et al., 2002). Other studies also demonstrated adult-like MMNs in infants for

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the duration changes (Brannon, Libertus, Meck, & Woldorff, 2008; Brannon, Roussel, Meck, & Woldorff, 2004) and the changes in speech sounds (Cheour et al., 1998b; Cheour-Luhtanen et al., 1995; Kushnerenko et al., 2001; Martynova, Kirjavainen, & Cheour, 2003). However, such mismatch negativities in newborns and infants usually persist for a longer interval and in a relatively late time window than those typically seen in adult data. Other studies instead reported that mismatch responses in infants are often a positivity between 200 msec and 450 msec, rather than an adult-like negativity (Dehaene-Lambertz & Baillet, 1998; Dehaene-Lambertz & Dehaene, 1994; Friederici, Friedrich, & Weber, 2002; Jing & Benasich, 2006; Leppänen, Eklund, & Lyytinen, 1997; Morr, Shafer, Kreuzer, & Kurtzberg, 2002; Novitski, Huotilainen, Tervaniemi, Näätänen, & Fellman, 2007). For example, Leppänen et al. (1997) observed a positive mismatch response (P-MMR) peaking between 250 msec and 350 msec to the pure tone change in newborns. Dehaene-Lambertz and Dehaene (1994) reported that three-month-old infants showed a P-MMR peaking at approximately 390 msec to initial consonant change (/ba/ vs. /ga/). Friederici et al. (2002) examined the mismatch response to syllables varying in vowel duration (short /ba/ vs. long /ba:/) in 2-month-old infants and found a P-MMR peaking at approximately 400 msec, especially when considering long syllables as the deviance. Generally, the P-MMR was found mainly at a younger age and it can be elicited by various speech and non-speech changes. The characteristics of the P-MMR remain unclear. Some studies have suggested that the polarity of mismatch response depend on maturation factors. For example, Leppänen et al. (2004) reported that the amplitude of mismatch response was positively correlated with physiological maturation in infants. A more mature newborn tends to have a more positive mismatch response. He, Hotson, and Trainor (2007) examined the brain responses of 2- to 4-month-old infants to infrequent pitch changes of piano tones. Their data showed an increase in the left lateralized positive slow wave at 2 and 3 months of age, whereas a faster adult-like MMN was present in 3- to 4-month-old infants. Trainor et al. (2003) reported that the mismatch response turned from positive to negative between 2 and 6 months of age. Kushnerenko, Ceponiene, Balan, Fellman, and Näätänen (2002) longitudinally traced the development of pitch change detection in a group of infants from birth until 12 months of age. Their data showed that the adult-like MMN stabilized between 3 to 6 months of age, although a substantial MMN variability from age to age within the same infant was observed. These findings imply that the adult-like MMN becomes prominent, whereas the P-MMR diminishes as infants age. These observations suggest that the neural maturation may play a role in the developmental changes of mismatch responses. Other studies have suggested that stimulus-related factors, such as short inter-stimulus intervals and smaller magnitude of deviance, decrease the discriminability between standard and deviant, which might be responsible for the polarity transition of mismatch responses. Morr et al. (2002) examined how maturation and the size of deviance affect the polarity of mismatch response in infants and preschoolers. Their data showed that the majority of infants failed to exhibit an adult-like MMN to the small deviance (1,000 Hz vs. 1,200 Hz). The adult-like MMN cannot be elicited reliably by the small deviance until 4 years of age. Conversely, the adult-like MMN presents in most infants and preschoolers to the large deviance (1,000 Hz vs. 2,000 Hz). Maurer, Bucher, Brem, and Brandeis (2003) further examined mismatch responses in adults and 6- to 7-year-old children with substantially smaller frequency (1,000 Hz vs. 1,060 Hz) and phoneme deviance (“ba” vs. “ta” or “da”) with shorter intervals relative to those in most previous studies. Although a typical frontal-central MMN was evident in adults, the positive mismatch

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response remained pertinent in 6- to 7-year-olds (Maurer et al., 2003). These findings suggested that both stimulus-related and biological criteria are required for P-MMR to switch to MMN. Spoken languages vary in phonological structures and speech features, which can be segmental units, such as phonemes, or supra-segmental units, such as word stress and tone. Some features are relatively common across different languages. For example, nearly all languages have at least three phonemic vowels, /i/, /a/, and /u/. However, some features are unique to certain languages, such as vowel duration for Finnish, word stress for German and English, and lexical tone for Thai and Chinese. Accurate speech perception is based on language-specific memory traces of the essential speech units for each language that developed during language acquisition and are represented in long-term memory (Näätänen et al., 2007). Previous studies have established that language experience influences the automatic involuntary processing of speech sounds (Cheour et al., 1998a; Friederici et al., 2007; Naatanen et al., 1997), thus suggesting that MMN can serve as an index of a language-specific memory trace for early identification of children at risk of language deficit (Leppänen et al., 2010; Weber et al., 2005). Lexical tone is an essential feature of Mandarin Chinese. This study aims to uncover the developmental trajectories of mismatch responses to Mandarin lexical tones in early infancy. As mentioned, Mandarin Chinese is a tonal language that exploits variations in pitch at the syllable level to determine different meanings. The four lexical tones can be categorized phonologically into a high-level tone (T1), a high-rising tone (T2), a low-dipping tone (T3), and a high-falling tone (T4). The major sign for discriminating different lexical tones is the contour of fundamental frequency (F0). Studies on speech production showed that, although children master most of the tones by 3 years of age (Hua & Dodd, 2000; Wong, Schwartz, & Jenkins, 2005), each of the lexical tones has a different developmental trajectory. For production, T1 and T4 are mastered earlier than T2 and T3 (Clumeck, 1980; Hua, 2002; Li & Tompson, 1977). Studies on tonal perception also showed a similar developmental trajectory. In a picture-pointing task, 3year-old children showed higher accuracy in perceiving T1, T2, and T4 (90%, 87%, and 89%, respectively) than that for T3 (70%), in which the most frequent error was misidentifying T3 as T2 (Wong et al., 2005). Multidimensional scaling (MDS) analysis is a statistical technique for analyzing proximity data in a set of stimuli to reveal the hidden structure of the data. MDS analysis of tone perception involves constructing dissimilarity matrices based on direct comparisons of tonal pairs. Using MSD analysis, Gandour and his colleagues have reported that pitch contour and pitch height are crucial for characterizing Mandarin tone perception (Gandour, 1983; Gandour & Harshman, 1978). For pitch contour and direction, T2 is acoustically more similar to T3 than T1. Tonal discrimination and identification data confirm that T2 and T3, which are acoustically the most similar, are more often confused with one another, compared to other tonal pairs. Tsao (2008) examined whether acoustic similarity between lexical tones would affect the perceptual discrimination performance of 12-month-old infants by using the head-turn technique, in which infants are taught to turn their heads to a sound or to a change in sound. This technique is ideal for understanding the speech perception capability of infants between 6 and 18 months of age and how such capability changes as a function of language experience and development. Tsao (2008) showed that the distinction accuracy between T1 and T3, which is the most acoustically distinct contrast, is higher than that of the other contrasts (T2 vs. T4 and T2 vs. T3). This suggested that the acoustic similarity affects Mandarin lexical tone discrimination as early as 1 year of age. A few studies concerned mainly with the hemispheric dominance of tonal processing investigated the MMNs for Mandarin lexical tone in adults. A number of studies reported that MMN for lexical tone was larger in the right fronto-central sites than in the left fronto-central sites (Luo


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et al., 2006; Ren, Yang, & Li, 2009; Xi, Zhang, Shu, Zhang, & Li, 2010). Luo et al. (2006) conducted a dipole analysis to localize the neural generator of MMN for lexical tone. They reported that the dipole was significantly stronger in the right hemisphere than in the left hemisphere, and that the hemispheric lateralization of MMN for consonant deviance has a reverse pattern. However, other studies failed to find a significant right lateralization of MMNs for lexical tone (Chandrasekaran, Krishnan, & Gandour, 2007a,b, 2009). Furthermore, Xi et al. (2010) examined the categorical perception of Mandarin lexical tone by MMN for within- and across-category deviance selected from a 10-interval continuum between T2 and T4. Their data showed that MMN for cross-category deviance was larger than that for within-category deviance only in the left-distributed sites. The contradiction on scalp distribution suggested that MMN reflected both acoustical and phonological processing of tonal changes. Regarding how the size of deviance affects MMNs for Mandarin lexical tone, Chandrasekaran et al. (2007a) compared MMNs for different tonal pairs. Their data showed that the acoustically distinct T1/T3 pair elicited larger MMN with earlier peak latency than the acoustically similar T2/T3 pair. However, the acoustical similarity effect on MMN was observed only in the native Chinese group, but not in the native English group (Chandrasekaran et al., 2007a). Their following studies supported that MMN could index the experience-dependent neural plasticity to the acoustic features of lexical tones (Chandrasekaran, Gandour, & Krishnan, 2007b; Chandrasekaran et al., 2009). Although the adult data showed that deviance size affects MMNs for Mandarin lexical tones, the developmental trajectory of this effect remains unclear. Meng et al. (2005) addressed whether dyslexic children have neural deficits in auditory processing. In a part of their experiments, they examined the MMNs to lexical tone by subtracting ERPs to the standard “ba1” (T1) from ERPs to the deviant “ba2” (T2) in 8- to 13-year-old children with and without dyslexia. Their data suggested that no difference exists in mismatch responses to lexical tone between dyslexic and normal children. However, they did not examine if a significant mismatch response (the difference between the ERPs elicited by standard and that elicited by the deviant) exists in each group. In other words, whether the dyslexic group and their matched control showed significant MMN to the T1/T2 contrast is unclear. A more discreet data analysis is required to investigate the mismatch response to lexical tone in early childhood. Lexical tone awareness has been shown to be strongly associated with Chinese reading (McBride-Chang et al., 2008), suggesting that supra-segmental perception is particularly essential in exploring Chinese reading development and impairment. The current study used MMN, which has been used to index an automatic pre-attentive discrimination of speech sounds, for investigating the development of lexical tone perception in early infancy. In addition, whether the size of deviance affects the mismatch response to lexical tones remains unclear, especially in developmental populations. Tsao (2008) showed that acoustic similarity affects perceptual discrimination performance in infants as young as one year of age. Thus, this study examined how both biological maturation and deviance size affect the mismatch responses to Mandarin lexical tone in infants at birth and at 6 months of age. The size-of-deviance effect on mismatch responses, both the acoustically distinct T1/T3 and the acoustically similar T2/T3 contrasts were used with a multi-deviant oddball paradigm (Näätänen, Pakarinen, Rinne, & Takegata, 2004). Two experiments were conducted: Experiment 1 involved determining whether typical MMN and the size-of-deviance effect can be demonstrated in the mature brain. The results of this experiment shall be able to replicate those of Chandrasekaran et al. (2007a) by showing that a larger deviance (T1/T3 pair) elicits larger and earlier MMN than does a smaller deviance (T2/T3 pair) in adult native Mandarin Chinese speakers. Then, the same paradigm was used

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in Experiment 2 to explore the developmental trajectories of mismatch responses from birth to 6 months of age and to determine how the difficulty of lexical tone discriminability affects the maturation on mismatch responses. Previous studies have shown that mismatch responses could switch from positive to negative with growth in younger age (He et al., 2007; Morr et al., 2002). The transition from a P-MMR to adult-like MMN is expected in mismatch responses to lexical tones in early infancy, especially for the acoustically distinct T1/T3 contrast.

EXPERIMENT 1: MMNS FOR MANDARIN LEXICAL TONES IN ADULTS Methods Participants. Eighteen native speakers of Mandarin Chinese (2 women, age range = 18–29) with normal hearing were paid to participate in this study. All the participants are college or graduate students without a history of neurological or psychological issues. The current study was approved by the Human Subject Research Ethics Committee/IRB. Written consent forms were obtained from all participants. Stimuli. The stimuli consisted of three Mandarin syllables with different lexical tones: yi1, “clothing” (T1), yi2 “aunt” (T2), and yi3 “chair” (T3), which share the same vowel /i/, but carry different tonal contours. The T3 was assigned as the standard, with T1 and T2 as deviants. The T1/T3 pair represents the larger deviant contrast, and the T2/T3 pair represents the smaller deviant contrast. All the stimuli are meaningful syllables in Mandarin Chinese. These stimuli were pronounced by a native female speaker of Mandarin and were recorded at 16 bits, with a sampling rate of 44 kHz. Intensity and duration of the stimuli were normalized to 70 dB and 250 msec, respectively, with Sony Sound Forge 9.0 software. Procedure. Participants were seated in a soundproof and electrically shielded room. They were instructed to play a puzzle computer game called “super-box” silently while listen passively to auditory stimuli. The stimuli were presented at a sound pressure level (SPL) of 70 dB through a set of loudspeakers located approximately 75 cm in front of the participants. The experimental session started with 20 trials of standard, followed by 1,000 trials with 80% standard and 20% deviants (10% for each deviant). To establish a memory trace for the standard trial before each deviant, the pseudo-randomized sequence with at least two successive standards between deviants was adopted. Such a design has been widely used in MMN studies for both adults and infants (Cheour et al., 2002; He et al., 2007; Kushnerenko et al., 2007; Shestakova, Huotilainen, Ceponiene, & Cheour, 2003). In each trial, the stimuli lasted 250 msec, with 500 msec of inter-stimulus interval. EEG recording and data analysis. The electroencephalogram (EEG) signals were ampli® fied by SYNAMPS2 (Neuroscan, Inc.) in DC mode, low-pass 100 Hz, and digitized at a sampling rate of 500 Hz. EEG data were recorded from 64 Ag/AgCl electrodes (QuickCap, Neuromedical Supplies, Sterling, USA), arranged according to the international 10–20 system, including a reference electrode located between Cz and CPz and a ground electrode located between Fpz and Fz. Six additional electrodes were attached over the left and right mastoids, supra- and infra-orbital ridges of left eye (VEOG), and outer canthi of both eyes (HEOG).


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For offline analysis, the EEG data were re-referenced to the average of the left and right mastoids. Continuous EEG was segmented into epochs from 100 msec prior to the onset of the stimulus to 700 msec after onset, and the pre-stimulus interval was used for baseline correction. A 1 Hz to 30 Hz (zero phase shifting, 12 dB/oct) band-pass filter was applied before artifact rejection. The first 20 trials and epochs with artifacts exceeding ±100 µV were rejected. To ensure that the ERP to standard does not detect any change-detection response, the post deviant standards are usually excluded from the standard averages (see Ahmmed, Clarke, & Adams, 2008; Cheour et al., 2002; He et al., 2007). To ensure further that the numbers of trials between the standard and deviant were comparable, only the standard trials that were preceded by at least three successive standards were included for analyses. For each participant, at least 45 accepted deviants were required to be included in further analyses. The mean number of accepted deviants was 76.56, and that of accepted standards was 173.5. The grand averaged ERPs for standard, small deviant, and large deviant were computed for each participant and each electrode. To evaluate the spatial-temporal ERP differences between standard and each deviant, repeated measures ANOVAs with conditions (standard, large deviant, and small deviant) and electrode sites (F3, FZ, F4, FC3, FCZ, FC4, C3, CZ, and C4) as within-subject factors were conducted in a mean amplitude of six successive epochs of 50 msec each, from 50 msec to 350 msec. This procedure allowed for identification of the temporal courses at which the mismatch effect appeared. The planned comparisons were conducted between the large deviant and standard (T1/T3), and between the small deviant and the standard (T2/T3), to determine whether both types of deviants elicited significant MMRs. In all ANOVAs, the Greenhouse-Geisser adjustment to the degrees of freedom was applied to correct violations of sphericity associated with repeated measures. Accordingly, the corrected p-value for all the F tests with more than one degree of freedom in the numerator is reported. Only the effects or interactions showing significant differences (p < .05) in at least two consecutive time windows were considered meaningful and reported. To evaluate further the precise moments of MMRs for both T1/T3 and T2/T3 contrasts, MMN peak latencies obtained from each difference wave for each participant between 100 to 300 msec were submitted to a repeated measures ANOVA under particular conditions (T1/T3 and T2/T3) and electrode sites (F3, FZ, F4, FC3, FCZ, FC4, C3, CZ, and C4) as within-subject factors.

Results MMN data were derived by subtracting the standard from each deviant, resulting in individual MMNs for T1/T3 and T2/T3. The grand average of MMNs was fronto-to-central-distributed between 100 msec and 300 msec after the onset of stimuli (Figure 1). The main effect of the condition was significant in four consecutive time windows: 100–150 msec (F(2,34) = 30.56, p < .0001), 150–200 msec (F(2,34) = 54.52, p < .0001), 200–250 msec (F(2,34) = 16.75, p < .0001), and 250–300 msec (F(2,34) = 26.79, p < .0001). Interactions between conditions and sites were significant in two consecutive time windows: 100–150 msec (F(16,272) = 3.52, p < .005) and 150–200 msec (F(16,272) = 4.05, p < .005). Post hoc analysis revealed that the condition effect was significant in all selected sites for both time windows (F(2,272) = 100.38–527.07, ps < .0001). It revealed the difference among standard and two deviants was significant in intervals from 100 to 300 msec. Planned comparison revealed that MMN for T1/T3 was significant in the intervals of 100–150 msec (F(1,34) = 48.67, p < .0001) and 150–200 msec ((F(1,34) = 96.26,

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FIGURE 1 Mismatch negativities for the T1/T3 contrast (solid lines) and the T2/T3 contrast (dotted lines) in adults (n = 18).

p < .0001), and MMN for T2/T3 was significant in the intervals of 200–250 msec (F(1,34) = 18.01, p < .0001) and 250–300 msec (F(1,34) = 20.91, p < .0001). In summarizing successive time window analyses, T1/T3 elicited MMN from 100 to 200 msec, and T2/T3 elicited MMN in later periods from 200 to 300 msec. To compare the T1/T3 with T2/T3 contrasts, MMN peak latencies were obtained from each difference wave for each participant from 100 to 300 msec. In addition, the MMN amplitude was measured as the mean amplitude of a 100-msec period centered on the peak. The MMN peak latency and amplitude were analyzed using repeated measures ANOVAs with contrast (T1/T3 and T2/T3) and electrode sites (F3, FZ, F4, FC3, FCZ, FC4, C3, CZ, and C4) as withinsubject factors. For the peak latency, the main effect of contrast was significant (F(1,17) = 169, p < .0001). The MMN latency for T1/T3 (mean = 166.27 msec) was significantly earlier than that for T2/T3 (mean = 247.28 msec). Regarding the MMN amplitude, a significant main effect of contrast (F(1,17) = 6.62, p < .05) revealed that the MMN amplitude for T1/T3 (mean = – 2.45 µV) was larger than that for T2/T3 (mean = –1.91 µV). Neither the peak latency nor the amplitude analysis showed significant interaction between contrast and electrode sites. Discussion This experiment demonstrated the typical MMN for both T1/T3 and T2/T3 pairs in adult native Mandarin Chinese speakers. Congruent with Chandrasekaran et al. (2007a), the acoustically


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distinct T1/T3 pair elicited an earlier and larger MMN than the acoustically similar T2/T3 did. This corresponds with the findings of behavioral studies on lexical tone perception (Huang & Johnson, 2010; Tsao, 2008; Wong et al., 2005) and suggests that MMN is sensitive to the difficulty of lexical tone discrimination. MMN has been shown to be influenced by long-term experience (Näätänen et al., 2007). Recent studies have suggested that the lexical properties may also contribute to the MMN effect (Pulvermuller, Shtyrov, Kujala, & Naatanen, 2004). When listeners were presented with word and pseudo-word deviants among pseudo-word standards, the MMN elicited by word deviants were more pronounced than those elicited by acoustically matched pseudo-word deviants. This MMN enhancement could be caused by the activation of cortical memory traces for words. Considering that every Mandarin syllable also corresponds to at least one Chinese character, it is crucial to clarify whether the greater difficulty for T2/T3 than that for T1/T3 is solely because of acoustic similarity, or may confound with other lexical factors, such as lexical frequency. For lexical frequency, all three stimuli yi1 (T1), yi2 (T2), and yi3 (T3) used in this study are meaningful Mandarin syllables. They are matched according to their type frequency; meaning that each can be written according to 9 to 12 frequently used Chinese homophones, based on the top 50% of the frequency ranking of Chinese characters. However, regarding the token frequency (the sum of character frequency of homophones), yi2 (T2) has a lower token frequency (34,886 per 10 millions) than do yi1 (T1) and yi3 (T3) (155,866 and 111,184 per 10 million, respectively). However, previous studies have suggested that lexical frequency is actually a relatively insignificant factor causing MMN enhancement, as compared to the lexical status of the stimuli (Pulvermuller, et al., 2001, 2004). Most important, Chandrasekaran and colleagues (2007a) showed that the peak latency of the T2/T3 condition is shifted later when compared to the T1/T3 condition in both English and Chinese groups. Because the lexical frequency is meaningful only for Chinese group, the possible confounding factor from the lexical frequency seems untenable. However, in future studies, controlling the various acoustic and lexical parameters in the speech stimuli that potentially contribute to the mismatch response might be more favorable. In summary, our adult data demonstrated the typical MMN for both T1/T3 and T2/T3 pairs and suggests that the current experimental design is feasible to elicit MMN. Lee et al. (2012) used the same paradigm in 4- to 6-year-old preschoolers and showed that all of the groups exhibited adult-like MMN to the T1/T3 contrast, but elicited P-MMR to the T2/T3 pair (Lee et al., 2012). Whether adult-like MMN can be found in early infancy remains to be seen.

EXPERIMENT 2: MISMATCH RESPONSE TO MANDARIN LEXICAL TONES IN INFANTS This experiment investigates the mismatch responses to Mandarin lexical tones in infants from birth to 6 months of age, and examines how the deviance size effect shapes the maturation of mismatch responses. Previous studies have reported that infants showed either a P-MMR or an adult-like MMN for speech sounds, but the effects of maturation and deviance size on the transition of polarity have never been examined simultaneously. Therefore, we collected mismatch responses by using the multi-deviant oddball paradigm several days after birth of the infants and at 6 months of age. The maturation effect could be examined by comparing the property of mismatch response in two age groups. Furthermore, the deviance size effect on the emergence and

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polarity of mismatch responses could be examined by inspecting the independent response to T1/T3 and T2/T3. Methods Participants. Thirty-one full-term infants whose parents were native speakers of Mandarin Chinese participated in this study. The study protocols were approved by the Human Subject Research Ethics Committee/IRB and written consent forms were obtained from the parents for their infants’ participation. All the participants had a gestational age (GA) in the range of 37 to 41 weeks and a birth weight in the range of 2,200 to 3,760 grams, and their 1- and 5min Apgar scores were higher than 8. All the participants passed the acoustic emission test for hearing screening. For newborns, ERP data were collected within 13 days after birth while they were asleep. The data of 6 newborns among all the participants (n = 31) were excluded from analysis because of setting errors or their failing to fall asleep. Thereafter, data from 25 (10 female) newborns were included for final analysis. It was required that all the 31 participants return for their second stage of ERP recording when they were 6 months old (within 15 days). At this stage, eight infants dropped out because they are incapable of staying quiet during data collection. Accordingly, the final analysis included data from 23 6-month-olds, in which 13 (3 female) infants were sleeping, and the remaining 10 (7 female) infants were awake during the ERP recording. Their cognitive outcomes were assessed by using the Bayley Scales of Infant Development-Mental Developmental Index (MDI) before the 6-month-old ERP recording. All of the participants had a MDI within normal limits (ranging from 85 to 114), except two infants in the waking group. The follow-up assessments showed that the two sub-average infants had a MDI within normal limits when at 12 or 18 months of age. Stimuli and procedures. The stimuli and the multi-deviant oddball task were the same as those in Experiment 1. During data recording, sleeping infants were either lying on a bed or held by their caregivers. The waking infants were seated comfortably on their caregivers’ laps. In following similar procedures that have been used in other infant MMN studies (Morr et al., 2002; Shafer, Yu, & Datta, 2011), silent movies or cartoons were played on a monitor in front of the waking infants to engage them and minimize their movement. An experimenter entertained the infants with quiet toys whenever they lost interest in the videos. EEG recording and data analysis. Infants’ EEG signals were amplified by NuAmps (Neuroscan, Inc.) in DC mode, with 100 Hz low-pass and 60 Hz notch filters, and digitized online at a rate of 500 Hz. For newborns, Ag/AgCl electrodes were attached to eight scalp sites: FPz, F3, Fz, F4, C3, C4, O1, O2, and left and right mastoids according to the international 10–20 system. The FPz was considered the ground electrode, and the EEG was referenced online to Fz. Eye movement was monitored with two electrodes: one at the supra-outer canthus of the left eye, and the other at the infra-outer canthus of the right eye. The setting for 6-month-old infants was the same as that for neonates, except that all the electrodes were held with an elastic cap. The procedure for EEG data processing and artifact reject was the same as that used in Experiment 1. The repeated measures ANOVAs with conditions (standard, large deviant, and small deviant) and electrode sites (F3, F4, C3, and C4) as within-subject factors were conducted in a mean amplitude of nine consecutive 50 msec time intervals, from 50 msec to 500 msec


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after stimulus onset, for examining the time course of the condition effects across electrodes. The planned comparisons between the large deviant and standard (T1/T3) and between the small deviant and the standard (T2/T3) were also conducted in each electrode. Only effects or interactions showing significant differences (p < .05) in at least two consecutive time windows were considered meaningful and reported. Results Newborn infants. ERPs did not show N1-P2 deflection for auditory stimuli (Figure 2A). Two-way ANOVA revealed significant main effects of the condition in two separate time windows: the 200–250 msec (F(2,48) = 7.41, p = .0018) and the 350–400 msec (F(2,48) = 3.64, p = .0394). The interaction between conditions and electrodes was marginally significant in two consecutive time windows: 250–300 msec (F(6,144) = 2.17, p = .0858) and 300–350 msec (F(6,144) = 2.19, p = .084). MMRs could be inspected from the difference waves derived by subtracting the standard from each deviant (Figure 2B). Planned comparisons showed that T1 was significantly more positive than T3 in four consecutive time windows on F3: 300–350 msec (F(1,24) = 7.62, p = .0082), 350–400 msec (F(1,24) = 5.98, p = .0182), 400–450 msec (F(1,24) = 5.57, p = .0224), and 450–500 msec (F(1,24) = 4.61, p = .0369). The difference between T2 and T3 was significant in the 200 msec to 250 msec time window on all electrodes (F(1,24) = 5.91 (F3), 5.40 (C3), 5.55 (F4) and 8.08 (C4), ps < .05), although it did not fulfill the criterion of two consecutive time windows. In summary, the newborns showed a P-MMR to T1/T3 in 300 msec to 500 msec on the left frontal electrode (F3), but did not show a significant mismatch response to T2/T3. 6-month-old infants. ERPs in 6-month-old infants were subdivided into sleeping (n = 13) and waking groups (n = 10). ERPs showed typical N1-P2 deflection for auditory stimuli in both subgroups. For the waking group, the two-way ANOVA showed significant main effects of condition in two consecutive time windows: 150–200 msec (F(2,18) = 6.17, p = .0144) and 200–250 msec (F(2,18) = 4.23, p = .0331). The interaction between conditions and electrodes was significant in three consecutive time windows: 250–300 msec (F(6,54) = 3.62, p = .0177), 300–350 msec (F(6,54) = 3.79, p = .0257) and 350–400 msec (F(6,54) = 3.00, p = .0395). As shown in Figure 3B, the T1/T3 difference showed negativity followed by positivity, but the T2/T3 difference showed only positivity. For the T1/T3 pair, planned comparisons showed significant mismatch negativity in two consecutive time windows on F3 and F4: 150–200 msec (F(1,18) = 7.83 (F3) and 11.37 (F4), ps < .05) and 200–250 msec (F(1,18) = 8.08 (F3) and 4.94 (F4), ps < .05), and a significant mismatch positivity in three consecutive time windows on C3: 300-350 msec (F(1,18) = 7.02, p = .0163), 350–400 msec (F(1,18) = 15.56, p = .0009) and 400–450 msec (F(1,18) = 11.92, p = .0028). For the T2/T3 pair, planned comparisons showed a significant mismatch positivity in two consecutive time windows on C3: 300–350 msec (F(1,18) = 5.61, p = .0293) and 350–400 msec (F(1,18) = 5.04, p = .0375). A summary of the significance of planned comparisons is shown in Table 1. For the sleeping group, no significant condition effect was found. In summary, waking 6-month-old infants showed an adult-like MMN for T1/T3 in 150 msec to 250 msec on the frontal electrodes (F3 and F4), and a P-MMR to both T1/T3 and T2/T3 in 300 msec to 450 msec on the left central electrodes (C3).

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A F3

F4

C3

C4

T3 T1 T2

−2µV

−100

100

B

300

500

700 ms

F3

F4

C3

C4

−2µV

−100

T1−T3 T2−T3 100

300

500

700 ms

FIGURE 2 (A) The event-related potentials (ERPs) in newborns (n = 25) to T3 (solid lines), T1 (dash lines), and T2 (dotted lines). (B) The mismatch response to the T1/T3 contrast (solid lines) and the T2/T3 contrast (dash lines).


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A Sleeping

Awake

F3

F4

F3

F4

C3

C4

C3

C4

−8µV

−100

B

100

300

500

T3 T1 T2

700 ms

Sleeping

Awake

F3

F4

F3

F4

C3

C4

C3

C4

−4µV

T1−T3 T2−T3 −100

100

300

500

700 ms

FIGURE 3 (A) The event-related potentials (ERPs) in 6-month-old infants to T3 (solid lines), T1 (dash lines), and T2 (dotted lines). (B) The mismatch response to the T1/T3 contrast (solid lines) and the T2/T3 contrast (dash lines). Data from sleeping and awake subgroups are depicted in the left and right panels, respectively.

Discussion Experiment 2 entailed investigating the development of mismatch responses to Mandarin tonal changes in early infancy and how deviance size affects these responses. The same set of stimuli and paradigm, which have successfully educed typical MMNs to both large (T1/T3 pair) and small (T2/T3 pair) deviants in adults, were applied in a longitudinal study of infants at birth and at 6 months of age. The infant data showed that the more discriminable T1/T3 pair elicited a left frontal-distributed P-MMR in 300 msec to 500 msec at birth, whereas it elicited an adultlike MMN bilaterally preceding a left-central P-MMR in 300 to 450 msec at 6 months of age. This suggests that MMRs to the T1/T3 pair transit from P-MMR to MMN before 6 months of

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age, which is consistent with the developmental trajectory of MMRs to pure tone (Kushnerenko et al., 2002). The transition of polarity between newborns and 6-month-olds demonstrated the maturation effect on the polarity of the infants’ mismatch response to pitch contour change in linguistic context. The MMRs to T2/T3 pair, however, had a developmental trajectory that was different from the MMRs for T1/T3. The T2/T3 pair elicited no significant MMRs in newborns and a left central-distributed P-MMR in 6-month-old infants. Congruent with Lee et al. (2012), the data of infants at 6 months of age demonstrated the co-existence of MMN and P-MMR and suggested that the developmental trajectory of MMR polarity transition can be explained not only by citing the maturational factor, but also by referring to the stimuli-related factors (such as the discriminability of contrast and the size of deviance). Studies using non-speech pitch change have suggested that the polarity of mismatch response is dependent on both maturation and stimulus-related factors (He, Hotson, & Trainor, 2009a, 2009b). The younger infants would show P-MMR to the changes of lexical tones (especially for the small deviant T2/T3) because of the insufficiently detailed representations to support automatic, pre-attentive discrimination. With increasing age, the negative MMR (presumably the emerging MMN) are expected because more children will have developed robust representations. This is especially true for the larger deviant (T1/T3) with relatively high discriminability. The larger deviant elicited P-MMR in newborns, and the adult-like MMN became apparent in awake infants at 6 months of age. However, the P-MMR remains stable at a time window of approximately 300 msec to 450 msec, from birth to 6 months of age. For the small deviant (T2/T3), the MMR was not presented until 6-months of age. A P-MMR was found in the left central site in 6month-old infants while they were awake. The transition from P-MMR to MMR seems not only to be affected by maturation, but also by the deviance size. Furthermore, a stable mismatch response resembling adult’s MMN is already present early in the development for the larger change in lexical tone. The presence of MMN implies that the developed phonological representations in the brain support an automatic, pre-attentive discrimination. Earlier maturation of discrimination for T1/T3 than that for T2/T3 mirrors the observations of speech acquisition (Tsao, 2008; Wong et al., 2005). The absence of MMN in newborns was expected because previous studies showed more positive responses to the deviant stimuli, especially in infants under one year of age (He et al., 2007; Kushnerenko et al., 2002; Leppänen et al., 1997; Trainor, Samuel, Desjardins, & Sonnadara, 2001; Trainor et al., 2003). For example, Leppänen et al. (1997) observed a P-MMR peaking between 250 msec to 350 msec to the pure tonal change in newborns. The studies series by He et al. demonstrated that MMN became robust in 4-month-old infants, whereas only a broad positive mismatch response was present in 2-month-olds (He et al., 2007, 2009a, 2009b). The present findings show that the large deviant T1/T3 elicited P-MMR in sleeping newborns, and the transition from P-MMR to adult-like MMN was evident in waking infants at 6 months of age. These results are in agreement with the findings by Moore and colleagues (Moore, 2002; Moore & Linthicum, 2007), which suggest that the neural regions (cortical layers) that are the likely sources of the adult MMN are insufficiently mature before 3 months of age. The immature auditory cortices are considered the source of infant MMRs for perinatal infants. Not only age but also the stimuli-related factors (such as the discriminability of contrast) affect when and how the transition from P-MMR to MMN occurs. For example, our data showed that the smaller deviant did not elicit any MMR in newborns but a P-MMR in infants at 6 months of age. This suggested that MMN could not be found consistently to fine-grained differences in

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T2/T3

P∗ P∗∗∗ P∗∗

N∗ N∗

T1/T3

P∗ P∗

T2/T3

6-month-olds (awake)

–– ––

N∗∗∗

N∗∗∗ N∗∗∗

–– ––

N∗∗∗ N∗∗∗

–– ––

N∗∗∗ N∗∗∗ N∗∗∗

T2/T3

–– ––

N∗∗∗ N∗∗∗

T1/T3

adults

C3

F3

50–100 100–150 150–200 200–250 250–300 300–350 350–400 400–450 450–500

50–100 100–150 150–200 200–250 250–300 300–350 350–400 400–450 450–500

Time windows

C4

F4

T1/T3

T2/T3

newborns

N∗∗ N∗

T1/T3

T2/T3

6-month-olds (awake)

–– ––

N∗∗∗ N∗∗∗

–– ––

N∗∗∗ N∗∗∗

–– ––

N∗∗∗ N∗∗∗ N∗∗∗

–– ––

N∗∗∗ N∗∗∗ N∗∗∗

T2/T3

adults T1/T3

Note. “P” denotes that the deviance is significantly more positive than the standard, whereas “N” denotes the deviance is more negative than the standard. ∗ p < .05. ∗∗ p < .005. ∗∗∗ p < .001.

P∗ P∗ P∗ P∗

T1/T3

newborns

TABLE 1 Summary of Planned Comparisons in Each Time Window at Electrodes F3, F4, C3, and C4, Independently

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awake infants and are absent in sleeping newborns. This is supported by Morr et al. (2002), who reported a P-MMR to the pitch change between 1,000 Hz and 1,200 Hz but an adult-like MMN for the change between 1,000 Hz and 2,000 Hz in infants within 1 year of age. The P-MMR remained in older children when fine-grained deviances were used. Maurer et al. (2003) reported P-MMR to a substantially smaller frequency deviance (100 Hz vs. 1,060 Hz or 1,030 Hz) and phoneme deviance (/ba/ vs. /ta/ or /da/) in 6- to 7-year-old children. The present findings of adult-like MMN for T1/T3 and P-MMR to T2/T3 in 6-month-old infants supported that the degree of deviance on lexical tone could modulate the polarity of MMRs. The T2/T3 contrast does not suffice in salience for 6-month-old infants to elicit an MMN for automatic change detection. This is also congruent with the behavioral observation that showed the difficulty in discriminating between T2 and T3 remaining, even at three years of age (Wong et al., 2005). Further studies are required to follow the developmental trajectory of the polarity transition in MMRs to T2/T3. Data from awake 6-month-old infants revealed the coexistence of MMN and P-MMR. However, the adult-like MMN and P-MMR have distinct scalp distributions. The adult-like MMN in 6-month-old infants were bilaterally significant in the frontal electrodes, whereas the P-MMRs in newborns and 6-month-old infants were significant only in left electrodes. These findings suggest that the adult-like MMN and P-MMR may reflect different characteristics of processing. Because the MMN usually indexes the automaticity of auditory change detection, the presence of P-MMR seemingly reflects an immature brain response to auditory changes if it is more likely to be observed in children or infants at a younger age and in response to small deviance, which is difficult to discriminate. However, the functional significance of P-MMR remains unclear. A number of studies suggest that the P-MMR might be an analogue of adults’ P3a response, which reflects an involuntary attention switching to a task-irrelevant novel sound (He, Hotson, & Trainor, 2008; Kushnerenko et al., 2002; Shestakova et al., 2003). However, Kushnerenko et al. (2007) examined whether the P3a-like positivity in newborns could be attributed to novelty as such, or to acoustic characteristics of novel sounds by using various types of novel sounds, such as novel environmental sounds, white-noise segments, or harmonic tones with a higher pitch or with higher intensity. They found that newborns are most sensitive to the spectral width of sounds because the largest and most reliable P3a was found in response to infrequent white noise segments than to other novel stimuli. This phenomenon was not found in adults, and suggested that the P3a-like positivity in infants might be attributed to the spectral richness rather than in response to novelty as such. Thus, the P-MMR of infants may not be identified with the P3a response seen in adults. A number of studies have suggested that P3a elicitation is dependent on adequate change detection, which was indexed by the preceding MMN (Escera, Alho, Winkler, & Näätänen, 1998; Friedman, Cycowicz, & Gaeta, 2001). However, no preceding MMN was found in the P-MMRs elicited by T1/T3 in newborns or by T2/T3 in 6-month-old infants. This is in line with the study conducted by Shafer et al. (2011), which reported a P-MMR to English vowel contrasts without preceding MMN from 6 to 18 months of age. The P-MMR may not merely reflect the involuntary attention shifting as the P3a, but also indexes a preliminary change detection mechanism in infancy. Our newborn data showed a P-MMR to large deviant (T1/T3), but no significant MMR to small deviant (T2/T3). When infants turned into 6-month-old, the MMRs could be detected only when they were awake, but no MMRs could be detected when they were sleeping. The data imply that alertness affects the presence of MMRs in early infancy. However, it is unclear why


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MMRs could be detected in sleeping newborns but not in 6-month-old infants when they were also sleeping. One possible reason is that the MMN-generating system may be affected in differently in newborns and in infants of 6-month-olds during sleep. Many studies have successfully demonstrated MMN in sleeping newborns (Cheour et al., 2002; Leppänen et al., 2004; Martynova et al., 2003). However, for adults and older infants, MMN has been detected mainly in states of wakefulness (Atienza, Cantero, & Dominguez-Marin, 2002; Friederici et al., 2002). Studies have roughly divided the sleep state into different stages (such as REM (rapid eye movement) and non-REM (NREM) sleep) and demonstrated the adult MMN during REM sleep but not in NREM sleep (Atienza et al., 2002; Nashida et al., 2000). However, the MMN amplitude obtained in REM sleep is considerably more attenuated as compared with that obtained during wakefulness (Atienza et al., 2002). By contrast, MMN in newborns can be recorded during wakefulness, and quiet (equivalent to NREM sleep in adults) and active (equivalent to REM sleep in adults) sleep, and its amplitude does not vary across these states (Cheour, Leppänen, & Kraus, 2000; Martynova et al., 2003). This implies that active (REM) and quiet (NREM) sleep in newborns may serve different functional processes as compared with the respective sleep stages in adults. The maturation of the neural structure, as indicated by fewer neurons, sparser dendritic branching, fewer axon collaterals, and incomplete myelination of axons in primary and secondary cortical regions, may also contribute to the morphological difference between developmental groups. Previous studies have suggested that neonates are not capable of blocking or inhibiting afferent or efferent systems during sleep because of an immature thalamic inhibitory system in infants (Winkler, 2007). The thalamus is incapable of efficiently inhibiting information during sleeping before the second or third month of life. Therefore, it is reasonable to expect MMRs are elicited in different states of infant sleep, indicating that newborns are able to process and learn auditory input while sleeping (Weber, Hahne, Friedrich, & Friederici, 2004). It would be much more relevant to use MMRs to determine whether infants can develop sufficient ability to discriminate a set of speech units at certain ages, than to examine the morphological differences (such as MMR latency and amplitude) across different age groups.

CONCLUSION This study demonstrated how maturation and stimulus-dependent factors affect the mismatch responses to the Mandarin lexical tone in adults and early infancy. In adults, typical MMN were obtained for both the T1/T3 pair and the T2/T3 pair. The acoustically distinct T1/T3 pair elicited an earlier and larger MMN than the acoustically similar T2/T3 did. In the infants, T1/T3 pair elicited a left frontal-distributed P-MMR in the newborns, whereas it elicited an adult-like MMN in the 6-month-old infants. However, the T2/T3 did not elicit any MMRs in the newborns but elicited a P-MMR in the 6-month-old infants only when they were awake. Apparently, the PMMR surfaced in newborns when the change sufficed in salience. The P-MMR switched to the adult-like MMN with infants’ growth, but the trajectory of the polarity transition depended on the degree of deviance. The coexistence of P-MMR and adult-like MMN suggested that the change detection mechanism in 6-month-old infants may not be as automatic as those in adults. Additional studies are required to determine when the automatic change detection indexed by adult-like MMN for T2/T3 discrimination can be shown in later ages. In addition, more detailed

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study of how responses to different sound features develop across ages in normal developing children would be crucial for early identification of children with language impairments.

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