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. Author manuscript; available in PMC: 2020 Nov 1.
Published in final edited form as: Ear Hear. 2019 Nov-Dec;40(6):1376–1390. doi: 10.1097/AUD.0000000000000726

Neural Indices of Vowel Discrimination in Monolingual and Bilingual Infants and Children

Yan H Yu 1, Carol Tessel 2, Xiaoxu Han 3, Luca Campanelli 4, Nancy Vidal 5, Jennifer Gerometta 5, Karen Garrido-Nag 6, Hia Datta 7, Valerie L Shafer 4
PMCID: PMC6814506  NIHMSID: NIHMS1522420  PMID: 31033699

Abstract

OBJECTIVES

To examine maturation of neural discriminative responses to an English vowel contrast from infancy to four years of age and to determine how biological factors (age, sex) and an experiential factor (amount of Spanish versus English input) modulate neural discrimination of speech.

DESIGN

Event-related potential (ERP) Mismatch responses (MMRs) were used as indices of discrimination of the American English vowels [ε] versus [I] in infants and children between three months and 47 months of age. A total of 168 longitudinal and cross-sectional data sets were collected from 98 children (Bilingual Spanish-English: 47 male and 31 female sessions; Monolingual English: 48 male and 42 female sessions). Language exposure and other language measures were collected. Event-related potential responses were examined in an early time window (160–360 ms; early MMR) and late time window (400–600ms; late MMR).

RESULTS

The early MMR became more negative with increasing age. Language experience and sex also influenced the amplitude of the early MMR. Specifically, bilingual children, especially bilingual females, showed more negative early MMR compared to monolingual children and to males. However, the subset of bilingual children with more exposure to English than Spanish compared to those with more exposure to Spanish than English (as reported by caretakers) showed similar amplitude of the early MMR to their monolingual peers. Age was the only factor that influenced the amplitude of the late MMR. More negative late MMR was observed in older children with no difference found between bilingual and monolingual groups.

CONCLUSIONS

Consistent with previous studies, our findings revealed that biological factors (age and sex) and language experience modulated the amplitude of the early MMR in young children. The early negative MMR is likely to be the mismatch negativity (MMN) found in older children and adults. In contrast, the late MMR amplitude was influenced only by age and may be equivalent to the Nc in infants and to the late negativity (LN) observed in some auditory passive oddball designs.

Keywords: speech development, bilingual, event-related potentials, mismatch negativity, mismatch response, late negativity, infants

Introduction

Considerable research has tracked the time course of first-language speech perception development and has revealed that experience with a language influences how an infant categorizes speech from birth (and even in the womb) through early childhood, typically measured via behavioral preference and novelty tasks (Best, et al., 1982; DeCasper et al., 1994; Kuhl et al., 1992, Kuhl 2004). By one year of age, children have learned which phonological patterns are contrastive (phonemes) in their native language and they have already shown sensitivity to language-specific phonological information (e.g., Werker & Tees, 1983; Jusczyk, et al., 1994). However, phonological development is incomplete well into the grade-school years (Nittrouer & Miller, 1997). For example, one-year olds will fail to discriminate difficult phoneme contrasts (e.g., /ba/ and /da/ in more challenging tasks such as lexical learning) until 18 months of age, even though they demonstrate discrimination in a simpler task (e.g., Werker, et al., 2002).

Both experience and auditory cortical maturation are likely to be necessary to attain an adult-like phonological system. Studies of speech perception development have largely focused on the former variable. More recent models have acknowledged the importance of considering the developmental level of a child when interpreting speech perception results (Werker & Curtin, 2005; Curtin, et al., 2011). The goal of the current study is to examine both experience and maturation in the development of speech discrimination.

Studies of neural maturation of the auditory system have revealed considerable cortical immaturity before six months of age (e.g., Kostović & Jovanov-Milosević, 2006; Moore & Linthicum, 2007). Considerable structural maturation (e.g., number of axon collaterals, amount of myelination) and functional maturation (e.g., latency and topography of obligatory, auditory components) occurs during the first year of life, with the rate of maturation slowing down through the preschool and into the grade-school years (Moore & Lithicum, 2007). Thus internal, biological factors constrain the rate of auditory cortical maturation in neonates and young infants (Leppänen et al., 2004; Kostović & Jovanov-Milosević, 2006; Moore & Lithicum, 2007). Studies of children with congenital deafness followed by cochlear implant indicate that early input also plays a role in maturation of the auditory system (Sharma, et al., 2002). What is less clear is the degree to which the characteristics of the input (e.g., monolingual versus bilingual speech input) modulate auditory development.

An additional source of evidence for biological factors constraining maturation comes from studies of sex differences. Sex differences during prenatal and early infancy periods have been observed (Basic sensory difference: see Alexander & Wilcox, 2012 for a review; Oral-motor function: Miller et al., 2006; Nagy et al., 2007). Male and female infants show different rates of cortical maturation driven by differing levels of sex hormones (e.g., Shucard et al.,1981; Shucard & Shucard, 1990; Friederici et al., 2008). In particular, female infants initially showed more rapid maturation of electrophysiological responses to tones over left compared to right hemisphere sites and male infants showed the opposite pattern (Shucard & Shucard, 1990); furthermore, one study found that female infants generally showed more linguistic rule-based learning than male infants (Mueller et al., 2012). Irrespective of the exact underlying sources of these sex differences related to cortical maturation, variations in cortical maturation can be inferred from these findings of sex differences.

Cross linguistic studies of speech perception have shown that listeners often have difficulty discriminating and categorizing non-native phonological contrasts not found in their first language (e.g., Werker & Tees, 1984; Best, 1985). In the case of second-language (L2) learning, late learners of an L2 (after approximately 11 years of age) may show poor L2 speech perception (e.g., Strange, 2011). In contrast, early learning of an L2 results in better behavioral perception of L2 phonological contrasts (e.g., Flege, 1995; Sundara & Polka, 2008; Gonzales & Lotto, 2013). Some studies, however, suggest that even early learning of an L2 (before five years of age) may result in less robust brain discrimination of L2 speech contrasts, as compared to monolingual listeners for some (e.g., Hisagi, et al., 2014), but not all early bilinguals (Datta, et al., 2019). Understanding the factors that influence L2 speech perception in adult bilinguals who had learned the L2 early in life is a challenging task. Previous studies have shown that amount of input in the first language (L1) versus the second language (L2) is likely to be a major factor (Flege, 1995; Flege & Mackay, 2004). Thus, examining L2 speech perception in the time period when amount of input can be better evaluated is desirable (Datta, et al., 2019).

Behavioral studies of bilingual language development in infants have shown that speech processing in one or both of a bilingual’s languages can be delayed if the two languages are difficult to separate (e.g., prosodically-similar languages such as Spanish and Catalan) (Bosch & Sebastián-Gallés, 2003; Sebastián-Gallés & Bosch, 2009). In cases that the languages (e.g., English and French) are easier to separate, the time course of speech perception development for both languages appears to be somewhat similar for bilinguals and monolinguals (Sundara, et al., 2008). However, in a previous event-related potential (ERP) study we found a small but significant effect of bilingual exposure on vowel speech processing in children between 3 months and 36 months for two languages (Spanish and English) that should be relatively easy to separate (Shafer, et al., 2011; 2012). Therefore, the relationship between language similarity and bilingual development may be less straightforward.

In addition to language similarity, the amount of language exposure in each language also affects speech and language development in young children (Hoff, et al., 2012; Conboy & Mills, 2006). Hoff and colleagues reported that the rate of development of each language in bilingual children is a function of their relative amount of language exposure (Hoff et al., 2012). Conboy and Mills also found a large effect of language experience on electrophysiological measures to words in the dominant versus non-dominant languages of Spanish-English toddlers (e.g., Conboy & Mills, 2006). Recently, Cattani and colleagues reported that 60% or more English exposure will lead to monolingual-like performance on English language tests in bilingual 2;6-year-olds (Cattani et al., 2014).

There has been an increased interest in examining the neurodevelopment of speech processing in bilingual children in the past 15 years (e.g., Rivera-Gaxiola et al., 2005; Shafer et al., 2010, 2012, 2015; Ferjan Ramirez et al., 2016; Garcia-Sierra et al., 2016; Rinker et al., 2017). Most studies have used an auditory oddball paradigm, in which a frontocentral neural response called Mismatch Negativity (MMN) is used to measure auditory processing (Näätänen, et al., 1997). The mature MMN is a negative peak between 100–250 ms post stimulus onset. Children older than approximately four years of age show somewhat similar neural measures of sound discrimination to adults, but sometimes at later latencies (Gomes, et al. 1999; Shafer, et al., 2000; Shafer et al., 2010). For example, Shafer et al. (2010) observed an MMN in four- to seven-year-old children to a speech sound contrast; this MMN peaked between 200 and 400 ms in the children, rather than between 100 and 250 ms, as expected for adults. The MMN shifts earlier in latency with increasing age, but does not reach adult latencies for more difficult sound contrasts until past puberty for some auditory and speech contrasts (Ponton, et al., 2000; Shafer, et al., 2000, Shafer et al., 2010).

Infants typically show a slow positive mismatch response (pMMR) in a passive oddball paradigm (Dehaene-Lambertz & Dehaene, 1994; Dehaene-Lambertz & Baillet, 1998; Trainor et al., 2001; Kushnerenko et al., 2002; Morr, et al., 2002; Leppänen et al., 2004; Friederici et al, 2007; Lee et al., 2012; Shafer et al., 2012; Partanen, et al., 2013a; Partanen, et al., 2013b). However, a few studies have observed a negative MMR (nMMR) rather than a pMMR (e.g., Cheour, et al., 1998; Trainor et al., 2001; Kushnerenko et al., 2002; He et al., 2007, 2009). With increasing age, the pMMR declines in amplitude and the nMMR emerges, peaking between 100 and 400 ms. The pMMR and nMMR may co-occur and partially overlap in infants and young children (e.g., Leppänen et al., 1997; Morr et al., 2002). It is likely that the timeframe for the emergence of the nMMR is dependent on the degree of acoustic or phonetic difference for the stimulus contrasts. For example, the nMMR emerges after three years of age to the subtle vowel contrast /I/ versus /ε/ (Shafer, et al., 2010), but to a large acoustic difference, such as 1000 versus 2000 Hz, the nMMR is observed in infants under one year of age (Morr, et al., 2002; see Kushnerenko, et al., 2013, for review). The pMMR continues to be observed (preceding the nMMR, if it co-occurs) to somewhat more difficult contrasts into the grade-school ages (Shafer, et al., 2010; Lee et al. 2012; Liu et al., 2014).

The nMMR may be equivalent to the MMN observed in adults and older children. The MMN indicates a mismatch between a stimulus or stimulus pattern (deviant) and the predictions generated by the prior context (standards) (Kushnerenko, et al., 2013). The nature of pMMR is less clear. Some studies have suggested that the pMMR is an analogue of adult P3a, indexing involuntary attention switch to stimulus change (Alho et al, 1990; Trainor et al., 2001; Kushnerenko et al., 2002). Others suggest that it reflects “an automatic categorization of the stimulus” (Friedrich et al., 2004), or an index of a general process as a result of neural adaptation (He, et al., 2009). Recent studies have found larger pMMR to more difficult than to easier stimulus contrasts (e.g., Lee, et al., 2012); these findings are more consistent with one of the latter two explanations for the pMMR. There is also evidence that a much later positive component (PC) peaking later than 300 ms and observed to novel sounds is the precursor of the adult P3a response, rather than the earlier occurring pMMR (Kushnerenko, et al., 2013).

Infants, children and adults may also show a second negative discriminative peak at superior anterior scalp sites. In an early study with adults, this response was called the re-orienting negativity (RON) (Schroger & Wolff, 1998); in studies with children, a similar response has been called the late discriminative negativity (LDN)(e.g., Cheour et al., 2001), the late MMN, the MMN2 (Korpilati, et al., 2001), or the late negativity (LN) (Datta et al., 2019; Shafer, et al., 2005; Yu et al., 2017; Yu et al., 2018). The Nc in infants may be comparable to this late negativity in children and adults. The Nc is found in a fairly late time interval (500–600 ms; Kurtzberg et al., 1984; Courschesne, 1990; Kushnerenko, et al., 2013).

Differences in the LN timing and topography, as well as different findings across studies, currently limit our understanding of what the LN reflects. Some studies suggest that the LN is modulated by phonological or lexical aspects of processing. For example, Korpilati and colleagues (2001) reported that a late MMN was significantly larger for deviant words than deviant tones, and suggested that it was related to automatic detection of lexical difference. Yu et al. (2017) found that the LN amplitude to lexical tone contrast was larger in native Mandarin listeners than monolingual English listeners when presented at a relatively long interstimulus interval (at the rate of approximately 3 second). In other studies, the LN was related to language status (language-impaired versus typically-developing) (Bishop et al. 2010; Datta et al., 2010). Alternatively, the LN may reflect enhanced auditory attention, considering that it is also observed to non-speech auditory stimuli and is modulated by novelty (Kushnerenko, et al., 2013). We observed positive responses in infants and younger children in the LN time window, and this positive response gradually became more negative. We therefore use the term “late MMR” to refer to the responses in the later time window for the remainder of the article. We refer to the MMR in the time window of 160–360 ms as “early MMR.” (eMMR). Depending on age and language background, this eMMR may be positive or negative. Other studies have used the term eMMN to refer to early Mismatch Negativity in this time window (e.g., Choudhury, Parascando & Benasisch, 2015).

The present study examines ERP correlates of processing the American English vowel contrast [ɛ]versus [ɪ] in monolingually-exposed and bilingually-exposed infants and children between three and 47 months of age. The goals of the current study were: 1) to examine how level of maturity modulates the neurodevelopment of speech processing throughout the period in which the child is mastering language (infancy to four years of age); and 2) how age, sex, and language experience modulate event-related potentials (ERPs) associated with speech-sound discrimination. We hypothesized that even a minimal amount of experience with an L2 would influence speech processing in a young child. We also expected to find age-related modulation of the ERPs. In particular, we expected to see increased negativity in both early and late MMR amplitude with increasing age (Shafer, et al., 2010). Finally, we predicted that sex would influence the early and late MMRs but more so during the first year of life than at later ages.

Materials and Methods

The experiment reported here was approved by The Graduate Center, CUNY Institutional Review Board, and was conducted in compliance with the Declaration of Helsinki. Parental consent was obtained from the parent/legal guardian(s) for each participant.

Participants

Fifty-nine bilingual Spanish-English children and 59 monolingual English children were recruited. Ten children from the bilingual group were not included in this study for the following reasons: five refused to be tested (no data), two had too few trials, two had corrupt data, and one had missing data files. Of the remaining 49 bilingually exposed children, 30 were male and 19 were female. Seventy-eight data sessions were collected with 16 (nine males, seven females) of these bilingually-exposed children being tested two to five times at different ages in a longitudinal design. Ten children from the monolingual English group were not included for the following reasons: three were tested in a different paradigm, three refused to be tested, two showed indications of language impairment, and two had missing or corrupt data files. Of the remaining 49 monolingual children, 26 were male and 23 were female. Ninety data sessions were collected with 20 (10 males, 10 females) of the monolingually-exposed children being tested two to six times at different ages in a longitudinal design.

A total of 168 data sets were collected from the 98 children (Bilingual: 47 male and 31 female sessions; Monolingual: 48 male and 42 female sessions; Age: 3–5, 6–12, 13–24, and 25–47 months old). Table 1 presents a summary of the number of ERP sessions in terms of participant age, sex, and language for the cross-sectional and longitudinal data combined. There was no session number difference in terms of the language or sex factor (Chi Square test: X2 = 0.558, p = 0.46). An additional eleven bilingual sessions and seventeen monolingual sessions are included here compared to our previous report (Shafer, et al., 2011). In addition, the previous report did not include the standardized language measures, or the subtypes of bilingual exposure (more English versus less English), and it examined maturation in a cross-sectional design. Shafer et al. (2012) focused exclusively on a comparison of the bilingual and monolingual 6–8 month-old infants.

Table 1.

A total of 168 sessions from cross-sectional and longitudinal sessions combined by age (in month) and sex (M = male, F = female). Among a total of 98 children, 20 monolingual and 16 bilingual children were tested two to six times between three and 47 months of age. The sessions from the longitudinal and cross-sectional children are in parentheses.

Age (months) 3–5 6–12 13–24 25–47 Grand Total
Monolingual 3M,7F 16M,17F 16M,10F 13M,8F 48M,42F
Longitudinal (3M,4F) (10M,12F) (12M,9F) (7M,5F) (32M,30F)
Cross-sectional (0M,3F) (6M,5F) (4M,1F) (6M,3F) (18M,12F)
Bilingual 9M,1F 15M,16F 12M,7F 11M,7F 47M,31F
Longitudinal (4M,0F) (7M,9F) (9M,4F) (7M,4F) (27M,17F)
Cross-sectional (5M,1F) (8M,7F) (3M,3F) (4M,3F) (20M,14F)

Language input was estimated from a language background questionnaire (LBQ) filled out by the principal caretaker, using a seven-point scale for rating input across multiple persons (e.g., father, mother, babysitter, siblings) and situations (e.g., home, playground), with 3 indicating all Spanish (labeled on the questionnaire as “Spanish all the time”), −3 indicating all English (labeled on the questionnaire as “English all the time”), and 0 indicating equal Spanish and English input (labeled on the questionnaire as “equal English and Spanish”). Note that on the questionnaire the values 1 to 7 were used and were then transformed to a scale of −3 to 3 for ease of interpretation. None of the bilingual children had a language background score of 3 (indicating all Spanish exposure), or −3 (indicating all English exposure). Twenty-eight out of 49 children had relatively-balanced English-Spanish exposure with an LBQ score between the values of −1 and 1. In one descriptive analysis and one mixed model regression analysis, we divided the bilingual children into two subcategories based upon LBQ scores (see Table 2). A total of 20 (8 females) children were categorized as Spanish-dominant with an LBQ score of 0 to 2.9 and a mean of 0.62 ((SD= 0.80), and the remainder (N=29, 11 females) were categorized as English-dominant with an LBQ score between −0.1 and −2.9, mean −1.47 (SD = 0.76). The mean LBQ score for all the bilingual children was −0.62 (SD = 1.3).

Table 2.

Bilingual sessions were further divided into more English (BME) and less English (BLE) subgroups in some analyses.

3–5 mos 6–12 mos 13–24 mos 25–47 mos Total
BME 3M,0F 5M,5F 4M,4F 6M,3F 30
BLE 6M,1F 10M,11F 8M,3F 5M,4F 48

Language measures were obtained using the Preschool Language Scale-4 (PLS-4) in English and, for bilinguals, in both English and Spanish. Three-year-old children also received the English Peabody Picture Vocabulary Test-3 (PPVT-3) (Dunn & Dunn, 1997) and, for bilinguals, the Spanish Test de Vocabulario en Imagenes Peabody (TVIP) (Dunn and Dunn, 1986). Table 3 shows standard language scores on the PLS-4 (Zimmerman et al., 2002) by language group (monolingual and bilingual, Spanish dominant versus English dominant bilinguals). All children had language measures on the English tests; Spanish measures were available for 16 of the 20 Spanish-dominant children and for 19 of the 29 English-dominant bilingual children. Note that for children under 12 months of age, the test items on the PLS-4 reflected general communication development (until first words are reported), and thus we did not collect measures for both the English and Spanish versions of the PLS at this age. The only difference in these two tests on early development is whether the question to the caretaker is asked in English or Spanish. Of the bilingual children lacking Spanish scores, only four of these children were older than nine months of age. In these cases, absence of Spanish scores was due to failure to complete the Spanish testing due to fatigue.

Table 3.

Mean (SD) language scores for monolinguals and bilinguals. Subgroups of bilinguals were included. PLS-A = Auditory Comprehension and PLS–E = Expressive skills. English Lang-all is the mean of the PLS-4 scores and the PPVT-3 (for older children). Bilingual-English (Bil-Eng) children had mean exposure scores on the LBQ between −0.6 and −2.9, whereas Bilingual-Spanish (Bil-Span) children had scores between −0.59 and 2.9.

Group English Lang-all English PLS_A English PLS_E Spanish PLS_A Spanish PLS_E
Monolingual 100(12) 98(16) 100(12) NA NA
Bilingual total 100(14) 100(16) 102(14) 101(20) 96(15)
 Bil-Eng 100(16) 100(19) 103(16) 94(22) 94(16)
 Bil-Span 100(11) 98(15) 101(12) 105(12) 103(12)

In the main statistical analyses, we used language as a categorical measure (monolingual versus bilingual; monolingual, balanced bilingual versus Spanish-dominant bilingual) because 1) the amount of English exposure does not follow a linear distribution since all monolingual children have 100% of English; 2) the monolingual and two bilingual groups of children did not significantly differ on the English language tests for any pairwise comparison between monolinguals and bilinguals in the longitudinal and cross-sectional groups, or between English- versus Spanish-dominant groups (t-tests, p-values > 0.20). The only differences were between English-dominant versus Spanish-dominant groups on the Spanish language tests. Unsurprisingly, bilingually-exposed children with relatively greater exposure to Spanish (0 to 2.9 on the LBQ) showed significantly higher receptive Spanish language standard scores than those with less Spanish exposure (−0.1 to – 2.9; p = 0.05 for receptive language, and p = 0.11 for expressive language).

We used age as a continuous variable for the main statistical analyses. We also used age as a categorical variable in the t-tests, figures and some tables for easy summary of participant characteristics. In some analyses, we divided children into the following age groups: 3–5 months, 6–12 months, 13–24 months, and 25–47 months. Our rationale for these four groups was derived from literature on early brain development and behavioral speech discrimination development. Moore and Linthicum (2007) divide early brain development into five distinct stages: transitioning to perinatal (27 to 29 fetal weeks), perinatal (third trimester to sixth postnatal month), transition to childhood (six months to 12 months), early childhood (2 to 5 years of age) and later childhood (6 to 12 years of age). Up to 6 months of age, the auditory cortex is still quite immature. Behavioral studies indicate that by six months of age, monolingual infants already show language-specific modulation of vowel discrimination (Eilers et al, 1979; Kuhl et al., 1992). Between six month and 1 years of age, there is a marked reduction of axons in the marginal layer, and filament-filled axons become visible in the auditory radiations in the core of the temporal lobe and the deeper layers of the cortex. Behavioral studies indicate language specific discrimination effects of more fine-grained speech information (Werker & Tees, 1984; Polka & Werker, 1994) and differences between monolinguals and bilinguals in vowel perception emerge during this period (Bosch & Sebastián-Gallés, 2003). Thirteen-24 months is a time of rapid lexical growth, whereas from 24–48 months, children are expected to acquire the grammatical patterns of language (Werker & Yeung, 2005).

The Bayley Scales of Infant and Toddler Development (Bayley, 1993) was used as a measure of general cognitive development. A t-test showed no group differences (monolingual mean = 103, SD = 15; bilingual mean = 98, SD = 17, p = 0.14). All infants were full-term, and had a normal birth history with no history of cognitive, neurological, speech, language, or hearing deficits in immediate family members. All had passed a newborn hearing screening according to parental report, and most passed a Transient Evoked Otoacoustic Emissions (TOAE) hearing screening in the laboratory. We did not have records of TOAE for several children due to incomplete behavioral testing or participant lack of compliance. All infants in the analyses showed a clearly-defined P1 obligatory auditory evoked potential (AEP) at frontocentral sites, indicating encoding of the auditory sound (Sharma, et al., 2009). Socio-economic status (SES) information was collected for all children using the Hollingshead Four-Factor Index of Socioeconomic Status (Hollingshead, 1975). Most of the children came from families with a middle-class or higher SES, but the monolingual group had a higher average SES than the bilingual group (Monolingual: mean = 50.7, SD = 12.1; Bilingual: mean = 39.5, SD = 16.9, p < 0.001).

Stimuli

Two, 250-ms re-synthesized vowels [ε] as in “bet” and [I] as in “bit” that differed in F1 and F2 formant frequencies (F1, 650 Hz and 500 Hz, F2: 1980 Hz and 2160 Hz, respectively) were used (See Figure 1). These stimuli were from a continuum of nine stimuli (deviant [I]: step 3, standard [ε]: step 9 of the continuum) used in previous studies with four- to ten-year old children with and without language impairment (Datta, et al., 2010; Shafer et al., 2010; Rinker, et al., 2017). Previous studies in our laboratory using all nine stimuli (step 1 to 9) showed that the categorical perception crossover point was at step 6 for both adults and children; thus, step 3 and step 9 were equal step distances from the crossover point. Moreover, step 3 was consistently identified as [I], and step 9 as [ε] by both adults and children as reported in our previous studies (Shafer, et al., 2007; Datta et al., 2010). In addition, other studies indicated poor categorization and neural responses MMN to these vowels by late adult learners of English with Spanish as a first language (Hisagi et al., 2014), and poor categorization of these vowels in children with specific language impairment (e.g., Datta, et al., 2010). The stimuli were presented at 86.5 dB SPL in sound field over two speakers, located 1 m in front of and 1 m slightly above and behind the child’s head.

Figure 1.

Figure 1.

The waveforms and spectrograms of the standard [ε] (left) and deviant [I] (right) stimuli.

Electrophysiological Design and Procedures

The electroencephalogram (EEG) was recorded from a 63-site Geodesic net using Net Station amplifiers and Net Station 4.1 software at a 250 Hz sampling rate and 0.1 to 30 Hz bandpass. The EEG was timelocked to the onset of the vowel stimuli. The stimuli were delivered via Eprime software (Psychology Software Tools, Pittsburgh, PA, United States) in sequences of 10 stimuli with an ISI of 400 ms between stimuli in the sequence, and 1500 ms between each sequence of 10. Three train types were randomly presented (see Table 4). The deviant stimulus occurred in the 4th and 8th position for 100 trains, in the 5th and 10th position for 50 trains, and in the 6th and 10th position for 50 trains, for a total of 1600 standards [ε] (80%) and 400 deviants [I] (20%). This is the same paradigm that was used in Shafer, et al. (2010; 2011 & 2012). We did not reverse the standard and deviant because the study time would be too long and our goal was to compare group effects.

Table 4.

Experimental paradigm: Ten stimulus per train, and three types of stimulus trains were randomly presented with a stimulus onset asynchrony of 650 ms, and inter-train-interval of 1500 ms.

train type 1 2 3 4 5 6 7 8 9 10
1 [ε] [ε] [ε] [I] [ε] [ε] [ε] [ε] [I] [ε]
2 [ε] [ε] [ε] [ε] [I] [ε] [ε] [ε] [ε] [I]
3 [ε] [ε] [ε] [ε] [ε] [I] [ε] [ε] [ε] [I]

The procedures were explained to the caretakers, who then read and signed informed consent. The electrode net was first soaked in a saline solution and then excess solution was removed. The nets were placed on the participant’s scalp while the participant was entertained by a laboratory assistant. The impedances of electrodes were maintained at or below 50 kOhms, which is sufficient for high input impedance amplifiers (200 Megaohms). During the experiment, older children sat in a chair, whereas infants sat on the caretaker’s lap while watching a video (e.g., Elmo, Baby Einstein) with the sound muted. Caretakers wore headphones playing music so that they would not orient to the vowel changes. Up to 200 sequences of ten stimuli were delivered (1600 standards, 400 deviants) in an approximately 40-minute session (28 minutes of stimulus delivery plus preparation time). Sessions were ended if a child became fussy and could not be calmed by changing the distracting task (e.g., by a researcher blowing bubbles or showing silent toys).

The continuous EEG was re-filtered offline using a low pass filter of 20 Hz, and was segmented with a pre-stimulus duration of 200 ms and 800 ms post-stimulus onset and baseline corrected using the pre-stimulus 100 ms amplitude. Any epochs with electrical activity exceeding +/− 140 μV at any electrode site were rejected, and bad channels (on 20% of segmented trials) were replaced by spline interpolation algorithm from surrounding channels. Over 90% of the children had more than 100 trials for the deviant stimulus after artifact rejection. The mean number of trials for the standard and deviant ERPs after artifact reject did not differ significantly between the monolingual and bilingual groups although there was a trend towards fewer trials obtained for the bilingual groups (p-values > .07, Standards: Monolingual Mean = 601, SD = 217, Bilingual Mean = 540, SD = 224; Deviants: Monolingual Mean = 241, SD = 88, Bilingual Mean = 216, SD = 91). Segments (−200 to 800 ms) were averaged for type (standard, deviant).

Analysis

ERP data reduction

The first step in the analysis was to reduce the ERP data using a combination of an objective metric and the existing literature. F3, Fz, and F4 are the most often reported sites to represent the left, central, and right frontal areas of MMN responses in the current literature. We selected two other neighboring sites that were highly correlated (Pearson’s r > 0.6, df = 248) with each of these three sites respectively building the three models. That is, we used the average of responses from Geodesic sites 8, 9, and 13, which are located near F3 for the left frontal model, sites 5, 55, and 4, which are located between Cz and Fz for the frontocentral model, and sites 3, 58, and 62, which are located near F4 for the right frontal hemisphere model (Figure 2) (see Shafer et al., 2012 for a similar approach). This method of data reduction reduces independent noise measured at each electrode for participants, and thus increases signal/noise ratio. Five intervals of 40 ms from 160–360 ms were selected to reflect the time interval where MMN emerges. Five later time intervals of 40 ms between 400 ms and 600 ms were selected to examine the late response where late MMR was expected. The subtraction waveforms (waveforms of deviant minus standard) were used for statistical analysis.

Figure 2.

Figure 2.

The sensor net and sites used for analysis. Left front model: the average waveforms from site 8, 9 and F3; the fronto-central model: site 5, 55 and Fz; the right front model: site 3, 58 and F4.

t-test to determine the presence of early and late MMRs

In the first step, Welch’s Paired Sample (two-tailed) t-tests were calculated for monolingual and bilingual language groups within each time interval of 40 ms (between 160 ms and 360 ms for early MMR, and 400 and 600 ms for late MMR) to determine the presence of significant early and late MMRs in four age groups (3–5 months, 6–12 months, 13–24 months, and 25–47 months of age). For simplicity, we pooled the left, central and right hemisphere responses. Note that our previous paper showed a significant positive MMR from approximately 200 to 360 ms in monolingual children (Shafer, et al., 2011), and significant negativity in six-month-olds from 560–600 ms (Shafer, et al., 2012). Thus, these t-tests were expected to replicate the previous findings.

Linear mixed-effects modeling analyses in the earlier and later time window

We hypothesized that MMR amplitude was modulated by both intrinsic factors (such as age and sex) and extrinsic factors (such as language exposure during early childhood). We also expected hemispheric differences based on our earlier findings (e.g., Shafer et al., 2010). To examine whether such factors were predictive of the early and late MMR amplitude measures, linear mixed-effects models were developed using R (R Core Team, 2014) and the lmer package (version 3.1–132) (Pinheiro et al., 2017). We chose a linear mixed-effects model approach because it allowed us to combine the longitudinal data and cross-sectional data together; linear mixed-effect modeling does not require the assumption of data-point independence. It also allowed us to use age as a continuous variable. The amplitude of the subtraction waveform (deviant minus standard) was modeled as a function of age (in months), language background (first: monolingual versus bilingual, then: monolingual, bilingual-more English and bilingual-more Spanish), hemisphere (left, central, right), and time bins (five intervals between 160 and 360 ms for the earlier time interval, and five intervals between 400 and 600 ms for the later time interval, respectively). To account for within-subject variability, a random intercept and a random slope of time and hemisphere for each participant were included in the model. Two sets of mixed-effects modeling were performed separately, one between 160 and 360 ms and the other between 400 and 600 ms. The effects of age (in months), hemisphere, sex, and language exposure were then tested following a bottom-up theory-guided approach, starting with level one predictors, then progressively adding subject level independent variables and interaction terms. The Bayesian information criterion (BIC) was used to compare the fit of the competing models (Burnham & Anderson, 2004). Partial effect sizes for specific model parameters were reported using semi-partial R-squared (Rβ2) (Edwards, et al., 2008). To facilitate the interpretation of the results, we reported Type III Analysis of Variance Table; p values were obtained using the Satterthwaite approximation for degrees of freedom (lmerTest version 2.0–36; Kuznetsova, et al., 2017).

All models included maximal random effects structure (Barr, et al., 2013), that is, random intercept for subject and random slopes for the within-subject independent variables were included. Random slopes were excluded only in those cases in which maximal models failed to converge. Within- and between-subject outliers were trimmed following a 2-stage procedure: first, we excluded values more than 3 SD below or above the mean; second, level one and level two standardized residuals were examined and we re-fitted the models without observations with residual values more than 3 SD below or above the mean. No more than 0.3% of the data were excluded for any of the models. Outliers were also excluded from group averages (Table 5).

Table 5.

The average amplitudes (SD) of the subtraction waveforms (deviant minus standard) for monolinguals and bilinguals between 3 months and 47 months of age for mismatch responses (160–360 ms) and late negativity (400–600 ms). Responses from hemispheres (left, central and right) were pooled. Significant p-values are in bold.

Age (months) Language df 160–200 200–240 240–280 280–320 320–360 400–440 440–480 480–520 520–560 560–600
3–5 Monolingual 29 0.43 (2.55) 0.95 a (2.33) 0.65 a (2.81) 0.93a (2.43) 0.82 (2.39) 0.91 a (2.45) 0.85 (2.48) 0.87 (2.48) 0.43 (2.12) 0.34 (1.78)
Bilingual 26 0.17 (2.03) 0.43 (2.53) 0.69 (3.13) 1 (2.95) 0.83 (2.72) 0.72 (2.54) 0.72 (2.51) 1.04a (2.77) 0.76 (3.01) 0.32 (3.03)

6–12 Monolingual 95 0.38a (1.73) 0.65b (2) 1.01c (2.15) 1.05c (2.07) 0.87c (2.1) 0.21 (2.3) 0.34 (2.46) 0.54 (2.62) 0.69b (2.65) 0.61a (2.67)
Bilingual 92 −0.06 (1.79) 0.28 (1.98) 0.79c (2.08) 0.72b (2.51) 0.46 (2.5) 0.31 (2.48) 0.35 (2.7) 0.47 (2.62) 0.73b (2.66) 0.53a (2.63)

13–24 Monolingual 83 0.05 (1.4) 0.21 (1.61) 0.64c (1.43) 0.84c (1.5) 0.51b (1.66) −0.04 (1.82) 0.04 (1.97) −0.23 (1.99) −0.50 a (1.87) −0.67b (2.1)
Bilingual 59 −0.43a (1.57) −0.11 (1.67) 0.15 (1.71) −0.11 (1.69) −0.5a (1.66) −0.32 (1.58) −0.15 (1.83) −0.46 (2.06) −0.5 (2.05) −0.61a (2.05)

25–47 Monolingual 59 0.18 (1.2) 0.32 (1.32) 0.66c (1.48) 0.44 (1.88) −0.15 (1.79) −0.17 1.76) −0.23 (2.06) −0.25 (2.14) −0.59 (2.42) −0.8a (2.65)
Bilingual 26 −0.2 (1.48) 0.14 (1.34) 0.39 (1.29) 0.47b (1.30) −0.08 (1.37) −0.27 (1.91) −0.29 (2) −0.47 (2.25) −0.78a (2.24) −1.00b (2.26)

Superscript

“a”

means p < 0.05

“b”

means p < 0.01

“c”

means p < 0.001.

Results

Presence of MMRs in the early time windows and MMRs in the later time windows

Figure 3 displays the grand average responses at the superior frontocentral site (Fz) for the standard and deviant conditions for monolingual and bilingual children, respectively. Each language group was divided into four subgroups according to age. In general, in the early time window (160–360 ms), positive MMR appeared in all four age groups for monolinguals; in contrast, for bilingual children a positive MMR was significant in all but those between 13–24 months of age. In the later time window (400–600 ms), the amplitudes of the difference waves were significantly positive for both monolinguals and bilinguals under 12 months of age, and significantly negative for all age/language groups older than 12 months of age (Table 5).

Figure 3.

Figure 3.

The waveforms for the standard [ε] and deviant [I] at the fronto-central sites for monolinguals and bilinguals between 3 months and 47 months of age.

Figure 4 presents the early MMR and late MMR (deviant minus standard) for each of the language/age subgroups at the left (near F3), midline (near FCz), and right (near F4) regions. Table 5 reports the results from the t-tests regarding the presence/absence of significant MMRs in the early and later time windows. Table 6 reports the Proportions of children with negative eMMR (160–360 ms) and negative late MMR (400–600 ms).

Figure 4.

Figure 4.

The subtraction waveforms (deviant minus standard) for the left, central and right frontal regions for monolinguals and bilinguals. The dashed boxes indicate time windows of analysis. Early MMR: 160–360 ms, late MMR: 400–600 ms.

Table 6.

Proportions of children with negative eMMR (160–360 ms) and negative late MMR (400–600 ms).

Monolingual Bilingual
eMMR late MMR eMMR late MMR
3–5 mos 0.23 0.34 0.29 0.25
6–12 mos 0.26 0.39 0.28 0.34
12–24 mos 0.3 0.49 0.49 0.51
25–47 mos 0.27 0.44 0.33 0.45

Mixed-effects modeling in the early time window (160–360 ms)

In the early time window (160–360 ms), linear mixed-effects regression analysis revealed that sex [F(1,168) = 5.000, p = 0.03, Rβ2 = 0.03], age [F(1,168) = 5.586, p = 0.02, Rβ2 = 0.03], language [F(1,168) = 5.699, p = 0.02, Rβ2 = 0.03], time [F(4, 212) = 16.2, p < 0.001, Rβ2 = 0.23], and a sex by age interaction [F(1,168) = 5.01, p = 0.03, Rβ2 = 0.03] were significant predictors of MMR amplitude, while hemisphere was not a significant predictor of MMR amplitude. It appears that more negative MMRs were observed in female than male infants, especially at a younger age (Figure 5).

Figure 5.

Figure 5.

Topomaps of the subtraction waveforms for early mismatch responses.

We further divided bilingual children into more English versus less English experience, as quantified on the LBQ, and repeated the analysis procedure using language as a ternary variable (English monolingual, bilingual-more-English, and bilingual-less-English exposure). The same main effects and interaction were observed as in the model above in which language was used as a binary variable (Language: F(2,168.2) = 3.185, p = 0.04; sex: F(1,168.2) = 4.904, p = 0.03; age: F(1,168.2) = 5.669, p = 0.02; Sex by age interaction: F(1,168.2) = 4.903, p = 0.03]. Post hoc tests revealed that the only difference between the two models was that when language was used as a ternary variable, there was a difference between monolingual children and bilingual children with less English exposure (p = 0.01), but the difference between monolingual and bilingual children with more English exposure was not significant (p = 0.22).

MMRs in the later time window 400–600 ms

The final mixed-effects model revealed that only age and time had significant predictive effects [Age: F(1,168) = 7.557, p = 0.007, Rβ2 = 0.04; Time: F(4,214) = 2.643, p = 0.03, Rβ2 = 0.05). The effects of sex, hemisphere, and language exposure were not statistically significant, and more negative MMR amplitude was associated with older age.

In summary, t-tests confirmed significant differences between the standard and deviant responses in the early and the late time windows, which indicated stimulus discrimination. The results from the mixed-effects modeling revealed language background, sex, age, and a sex-by-age interaction are significant predictors of MMR amplitude between 160 and 360 ms. In the late time window of 400–600 ms, only age is a significant predictor of MMR amplitude.

Discussion

This study examined the modulation of MMRs to English vowels in three-month to 47-month-old children by the factors of age, sex, hemisphere, and language experience. The current analysis showed that age, sex, and language experience influenced the amplitude of MMR in the early time window of 160–360 ms. In contrast, age was the only factor that influenced the amplitude of the late MMR in the time window of 400–600 ms. The new findings that we contribute to the current literature include: 1) Relative amount of bilingual exposure in English versus Spanish modulated the amplitude of the early MMR, but not the late MMR. Specifically, bilingual children with relatively-balanced English and Spanish exposure or more English than Spanish had similar MMR amplitude to their monolingual peers in the early time window (i.e., eMMR). However, bilingual children with Spanish-dominant exposure showed a difference in MMR amplitude from English monolinguals in the early interval. 2) Both the early and late MMRs to the vowel contrast shifted gradually from robust positivity to negativity from infancy as age increased. 3) No language exposure or sex effects were observed for the amplitude of the MMR in the late time window between 400 and 600 ms (i.e., late MMR). Below, we discuss our findings in greater detail in relation to the general literature.

Maturational Factors for the early MMR

Age was a significant predictor of the amplitudes of the early MMR (eMMR). The amplitudes of eMMR for this vowel contrast became less positive (or more negative) between three months and 47 months of age. This pattern was independent of language exposure and sex. This result is consistent with the majority of previous developmental studies (e.g., Morr, et al., 2002; He et al., 2009). He and colleagues (2009) found that in response to musical tone differences (specifically, a large fundamental frequency pattern contrast), four-month old infants showed a robust negative MMR, but two-month-old infants showed a positive MMR. However, the pattern of findings is quite complicated in young infants and appears to be dependent on stimulus factors, as well as age. For example, Leppänen and colleagues (2004) found that in neonates, a larger positive MMR amplitude is associated with longer gestational age and more mature heart period (HP) at F3 and C3. The studies by Shafer and colleagues (Morr, et al., 2002; Shafer, et al., 2000) and Kushnerenko and colleagues (2002) showed a positive MMR to tone contrasts (20% and 50% frequency (F0) change) in infants that was largest between 3 and 8 months of age and decreased in positivity and was largely absent at two years of age, with emerging negativity between three and four years of age. The findings of the current study using these vowel contrasts are highly consistent with this pattern. Future studies will be needed to explore how degree of stimulus difference, as well as stimulus quality (speech versus non-speech) influence this pattern of development. The study by Kusherenko, et al. (2007) has begun this task, revealing differences in neural discrimination of broadband white noise and narrower pitch differences.

Studies of brain maturation indicate that cortical auditory regions are highly immature in the newborn infant (Kostović & Jovanov-Milosević, 2006; Moore & Linthicum, 2007). Moore and Linthicum (2007) pointed out that intense sounds with large spectral differences are necessary to drive neural firing for encoding and discrimination at this young age. By six months of age, neural assemblies that receive auditory input have matured sufficiently to allow for encoding and discrimination of finer stimulus differences (Shafer et al., 2015). Kushnerenko et al. (2013) suggested that resolution of pitch information improves between 2 and 4 months of age. Fine-grained frequency resolution is essential for discriminating spectral differences between the vowels used in this study. The presence of a positive MMR indicates that the auditory cortex is sufficiently mature to resolve the spectral difference between vowels. However, we suggest that this pattern does not indicate the predictive detection that is signaled by MMN. Rather, the emerging negative MMR reflects this process. Future studies will need to examine how behavioral correlates of perception relate to the positive versus negative eMMR in this early time interval.

As we predicted, we did observe a sex difference that appears to suggest more rapid maturation of female than male infants. Female children had significantly less positive eMMR (i.e., more negative eMMR responses). In particular, none of the male infants under approximately four months of age showed negative eMMRs to the vowel difference. In addition, 15 of the 41 female infants under 12 months of age did showed negative eMMRs. Evidence that negative eMMR is an index of more mature processing comes from a study in which infants who demonstrated neural discrimination of complex higher order patterns (e.g., rapid learning of a linguistic rule), were the same as those who showed a negative eMMR to a pitch change (Mueller et al. 2012). Thus, we hypothesize that the more negative eMMR in female than male infants in the current study reflects faster maturation of the speech perception system, or more broadly, faster maturation of the auditory cortex, as reported in earlier studies (Shucard et al., 1981; Shucard, & Shucard, 1990; Shafer, et al., 1999; Friederici et al., 2008).

In the current study, hemisphere was not a significant predictor of eMMR amplitude. We evaluated a larger age range (3- to 47-month) than some studies that have reported a sex and hemispheric interaction in infancy (e.g., Shucard et al., 1977). For example, Friederici et al (2008) reported that at four weeks of age among infants with low testosterone levels, female infants showed more bilateral discriminative responses while male infants showed more left lateralized responses. More rapid maturation of the left hemisphere has been observed in three-month-old females and of the right hemisphere for three-month-old males (Shucard et al., 1981; Shafer, et al., 1999). Lack of a hemispheric effect or sex-hemisphere interaction in a larger age range suggests that the left and right hemispheric difference is less robust or disappears in males versus females, as infants grow older.

Development of Automaticity as indexed by MMR

We had previously suggested that automaticity of speech perception is not present to the fine, phonetic contrast examined in the current study until around four years of age (Shafer, et al., 2010; Shafer, et al., 2011). Specifically, children are not initially automatic with discriminating this contrast because it takes time and experience to establish robust, selective perceptual routines (SPRs) for native-language phonological categories (Strange, 2011). It is possible that larger acoustic-phonetic differences, for example between [i] and [ɑ], would allow for automaticity of discrimination because these are sufficiently salient. Crick & Koch (1990) argued that highly salient distinctions can be processed (discriminated or identified) with fewer attentional resources than less salient information. However, they also pointed out that less salient information can be made more salient through over-learning. Lack of robust negative MMR (or the presence of positive MMR) in the early time window suggests that “over-learning” of these subtle differences is not yet achieved in young children. Some studies have reported the pMMR to nMMR polarity shift for auditory contrasts at younger ages (e.g., at 4 months for piano tone in He et al., 2007; at 6 months for lexical tone in Cheng et al., 2013). Cheng and colleagues (2015) found the pMMR in neonates shifted into nMMR for a large deviant /du/-/da/ contrast, but remained positive for smaller deviant /di/-/da/ contrast in 6-month-olds. Some of our 6-month-olds also showed nMMR rather than pMMR. However, at the group level, we did not observe nMMR in children under 12 months of age.

An alternative explanation for the absence of an nMMR is that filtering of the data at 0.3-Hz high-pass does not attenuate a large-slow positivity, and this positivity overlaps with the faster-rate nMMR. Some studies reporting group level MMN (i.e., negativity) used a high-pass filter of 1 Hz, which would attenuate slow activity with a time constant greater than 1 second (Cheng et al., 2013, Cheng et al. 2015, Garcia-Sierra et al., 2016). However, it is important to recognize that this filtering choice of 1-Hz high-pass would also attenuate a slow negativity, such as the late MMR/Nc. Note also that a faster eMMR (or 5–10 Hz) would still be discernable when riding on a slow positivity, but this pattern is not apparent in Figure 4.

Monolingual versus bilingual experience on MMR

We observed a sex by language interaction in our earlier, cross-sectional study on the 6-month-old monolingual versus bilingual infants (e.g., Shafer et al., 2012). In the current study, we examined a wider age range, and bilingual children, rather than female infants showed a more negative eMMR. Part of the reason for the difference between studies may be related to the increased n, but also the wider age range. In the current study, a larger proportion of bilingual (41% in children > 12 months) than monolingual children (29% in children > 12 months) showed nMMR. Thus, this result indicated that bilingual experience was associated with more negative MMR.

This result challenges the interpretation that negative MMR is more adult-like, or is associated with more developed processing of speech contrasts, as reported in some studies (e.g., Cheng et al., 2015). Specifically, bilingual infants/children had less experience with this English vowel contrast than did monolingual infants/children. In Shafer et al., (2012), we reported evidence that regardless of language experience, infants showed more negative MMR to a deviant that occurred in the final position compared to the mid position of sequences of 10 stimuli. A longer ISI of 1500 ms separated the final position from the onset of the next sequence of 10. We suggested that the final position drew more attention, and took as evidence an increase in positivity to a standard stimulus in this 10th position. Based on this finding, we speculate that more negative MMR in bilinguals in the current study is due to more attention allocation by the bilingual children than the monolingual children. Behavioral studies have reported attention differences between monolingual and bilingual infants (e.g., Lewkowicz & Hansen-Tift, 2012; Pons et al., 2015). Interestingly, in our recent study using short versions of these vowels comparing monolingual and bilingual adults and 8–11 year old children, we found differences in attention-related neural measures, but not in the MMN (Datta, et al., 2019). A study of infants is needed that directly manipulates attention to and away from the speech stimuli to test this hypothesis that the difference in MMR amplitude between the language groups is related to attention.

Amount of English versus Spanish Input

We had predicted that the amount of language input would modulate development of neural discrimination of this English vowel contrast. Our LBQ allowed us to divide the bilingual children into two subgroups. The bilinguals with more English exposure (BME) had similar MMR amplitude to the monolingual group, whereas the bilingual children with less English exposure (BLE) differed from BME and their monolingual peers, showing less positive MMR amplitudes in the early time range. Interestingly, Garcia-Sierra and colleagues (2016) reported that monolingual children with low language input had similar amplitude MMR to bilingual children, specifically showing more positive MMR than observed for monolinguals with high language input. For bilingual children, they found that more language input was positively correlated with the amplitude of pMMR to a contrast from that language. These findings suggest a complex relationship between MMR amplitude and language input. Specifically, less positivity in infants can indicate poorer discrimination or less positivity can indicate the emergence of an overlapping negative MMR (namely, the MMN). Specifically, with increasing age, the MMN moves earlier in latency as shown in our study with 4- to 7-year-old children using the same stimuli (Shafer, et al., 2010). As a result, the MMN can overlap with and reduce the amplitude of the positive MMR (Morr, et al., 2002; Shafer, et al., 2010).

An important question is how much English language exposure is necessary for a bilingual toddler to achieve a similar language profile to his/her monolingual peers. Cattani and colleagues (2014) reported that the proportion of English exposure is the main predictor of bilingual Spanish-English toddlers’ language performance, and bilingual toddlers who hear 60% or more English have matching language skills to their monolingual peers. Our study provided neural evidence that is consistent with the findings of Cattani and colleagues (2014). Our BME subgroup consisted of children who hear more than 50% of English in the ambient environment. These results have important clinical implications in that the amount of input can help decide whether an apparent language delay in a bilingual child is possibly due to insufficient input rather than to a true language disorder. However, it is important to recognize that even these higher levels of English input in children who are bilingual may still result in language differences from monolingual children, including lower-level English skills (Hoff, 2013).

One caveat in the current study was that SES was not matched across groups. Monolingual children from different SES backgrounds can have a language input difference between low and high SES with as large as 30 million words during their first three years of life (Hart & Risely, 2003), and SES affects language production growth measures (Hoff, 2013). In the current study, the BLE (less English) subgroup had similar SES scores (mean = 46.6, SD = 14.8) to the monolingual group (mean = 50.7, SD = 12.1), whereas the BME subgroup had lower SES scores (mean = 30.8, SD = 15.5) than the other two groups. The subgroup with similar amounts of English exposure (BME), rather than the subgroup with similar SES (BLE), however, showed similar-amplitude MMR responses to the monolingual children. Thus, differences in SES appeared to be less important than amount of English exposure in the current study. It will be necessary to have a larger number of bilingual children, varying SES, proportion of English/Spanish input and a more fine-grained measure of amount of input to allow a fuller exploration of how SES and amount of input interact to impact MMR amplitude.

The second limitation to generalizing our result broadly across all bilinguals is that Spanish and English are prosodically quite different. These prosodic differences may have aided the children in keeping the input from the two languages separate. In contrast, prosodically-similar languages such as Spanish and Catalan might result in a significantly different pattern of neural responses, as suggested by the different behavioral trajectory for Catalan monolingual and Spanish-Catalan bilingual infants (Bosch & Sebastián-Gallés, 2003). Thus, research examining other language pairs will be essential to fully understand the development of speech processing in bilingual children.

The late MMR

We compared the amplitude of the MMR in the late time window in monolingual and bilingual children, and found that age is the only factor that influences this response. The emerging negativity in older children may be equivalent to the LN found in grade school children or, alternatively, it may be the emerging MMN. Recall that researchers have used various names to refer to this late MMR, including LN (Kushnerenko, et al., 2013). In infants, the presence of positivity in this window could be equivalent to the P3a. However, it is difficult to interpret these responses in isolation. The studies of Kushnerenko and colleagues (2007) examined MMRs to different stimulus types in different contexts and observed a late negativity to novelty sounds and not to an infrequent deviant (that was always the same stimulus). These novelty sounds, which changed on each trial, are more likely to draw attention. Our previous study also suggested that attention is necessary to elicit a late MMR, at least in 6-month old infants (Shafer, et al., 2012). In addition, this late MMR is consistent with the Nc observed to novel events in infants (e.g., Courchesne, 1990). In the current study, after 12 months of age, both monolinguals and bilinguals showed significant late negative MMR. The lack of language exposure effects for the late MMR was similar to the findings of Garcia-Sierra and colleagues (2016). Specifically, they found increased negativity to the deviant between 350 and 550 ms, and that amount of language input did not affect MMR amplitude in the late time window in either monolingual or bilingual toddlers. These findings, however, contrasted with other studies that showed an effect of language on the late MMR, specifically in older children with language impairment (e.g., Bishop et al. 2010; Datta, et al., 2010) or typically developing children who were learning a second language (Shestakova et al., 2003).

Our results cannot fully address the mechanisms indexed by late MMR because we only used one contrast. Putkinen and colleagues (2012) examined multiple deviant types (e.g., duration, intensity, frequency, silent gap) with large, medium, or small magnitudes of acoustic differences. They obtained a robust late negativity (which we will call LN) for all deviant types in toddlers between 2 and 3 years of age. The authors argued that the fact that the smallest frequency contrast can elicit robust LN is inconsistent with the hypothesis that LN reflects reorienting of attention after a distracting stimuli (Shestakova et al., 2003; Horvath et al., 2009). If this was the case, then LN should be larger to greater stimulus difference. In our recent study with 8–11 year old and adult bilinguals, LN was larger for bilingual than monolingual adults but did not differ between monolingual and bilingual children (Datta, et al., 2019). The stimuli in Datta et al. were 50-ms versions of the [ε] versus [I] vowels used in the current study, and, thus, more difficult to discriminate (cf. Shafer, et al., 2005 and Datta, et al., 2010). However, Datta et al. also included conditions focusing attention to the auditory modality. Thus, whether the mechanism indexed by the LN reflects reorienting has not been definitively decided. While the nature and functional role of the late MMR and LN needs to be further examined, the developmental changes of the late MMR found in the current study together with other studies suggest that this late response has the potential of being used to evaluate the development of speech processing in toddlers. This is important because the MMR in the earlier time frame (150–400 ms) is often not significant to the subtle speech contrasts that are of particular interest in studies of language development.

Conclusion

Our findings demonstrate that neural indices of speech processing during the first few years of life undergo considerable development. Both maturational factors (age, sex) and experiential factors (language experience) modulate the infant/child MMRs. These developmental changes cannot be inferred from behavior. The considerable changes in neural discrimination (e.g., from a positive to a negative MMR dominating the response) provide clues indicating that the mechanisms for encoding and discriminating auditory information differ greatly from those used by older children and adults. Specifically, we found that immaturity in neural discrimination was indexed by a positive MMR prior to 350 ms to the English [ε] versus [I] speech contrast. Increased maturity, in terms of age, was indexed by increased negativity of the MMR in this early time frame. In addition, female infants showed increased negativity of the MMR, consistent with more rapid maturation than male infants. The finding that language experience modulated the MMR in the early time frame, provides further evidence for the importance of early speech experience in auditory-speech development. We hypothesize that this increasing negativity reflects increasing automaticity of discriminating the target contrast. We also suggested that the different pattern found for bilinguals could be the result of increased attention to the speech signal. Future studies need to further explore language-specific experience using other language pairs to fully understand the development of neural measures of speech processing.

Acknowledgments

This research was supported by NIH HD46193 to V. L. Shafer. We would like to thank A. Barias and M. Wroblewski for helping with data collection, B. Tagliaferri for technical support and W. Strange and R. G. Schwartz for advice on the design.

Financial Disclosures/Conflicts of Interest:

This research was funded by the National Institute of Health. NIH HD 46193 to Valerie Shafer

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