Language Experience during Infancy Predicts White Matter Myelination at Age 2 Years.

Parental input is considered a key predictor of language achievement during the first years of life, yet relatively few studies have assessed the effects of parental language input and parent-infant interactions on early brain development. We examined the relationship between measures of parent and child language, obtained from naturalistic home recordings at child ages 6, 10, 14, 18, and 24 months, and estimates of white matter myelination, derived from quantitative MRI at age 2 years (mean = 26.30 months, SD = 1.62, N = 22). Analysis of the white matter focused on dorsal pathways associated with expressive language development and long-term language ability, namely, the left arcuate fasciculus (AF) and superior longitudinal fasciculus (SLF). Frequency of parent-infant conversational turns (CT) uniquely predicted myelin density estimates in both the AF and SLF. Moreover, the effect of CT remained significant while controlling for total adult speech and child speech-related utterances, suggesting a specific role for interactive language experience, rather than simply speech exposure or production. An exploratory analysis of 18 additional tracts, including the right AF and SLF, indicated a high degree of anatomic specificity. Longitudinal analyses of parent and child language variables indicated an effect of CT as early as 6 months of age, as well as an ongoing effect over infancy. Together, these results link parent-infant conversational turns to white matter myelination at age 2 years, and suggest that early, interactive experiences with language uniquely contribute to the development of white matter associated with long-term language ability.SIGNIFICANCE STATEMENT Children's earliest experiences with language are thought to have profound and lasting developmental effects. Recent studies suggest that intervention can increase the quality of parental language input and improve children's learning outcomes. However, important questions remain about the optimal timing of intervention, and the relationship between specific aspects of language experience and brain development. We report that parent-infant turn-taking during home language interactions correlates with myelination of language related white matter pathways through age 2 years. Effects were independent of total speech exposure and infant vocalizations and evident starting at 6 months of age, suggesting that structured language interactions throughout infancy may uniquely support the ongoing development of brain systems critical to long-term language ability.

Dual-MEG interbrain synchronization during turn-taking verbal interactions between mothers and children.

Verbal interaction and imitation are essential for language learning and development in young children. However, it is unclear how mother-child dyads synchronize oscillatory neural activity at the cortical level in turn-based speech interactions. Our study investigated interbrain synchrony in mother-child pairs during a turn-taking paradigm of verbal imitation. A dual-MEG (magnetoencephalography) setup was used to measure brain activity from interactive mother-child pairs simultaneously. Interpersonal neural synchronization was compared between socially interactive and noninteractive tasks (passive listening to pure tones). Interbrain networks showed increased synchronization during the socially interactive compared to noninteractive conditions in the theta and alpha bands. Enhanced interpersonal brain synchrony was observed in the right angular gyrus, right triangular, and left opercular parts of the inferior frontal gyrus. Moreover, these parietal and frontal regions appear to be the cortical hubs exhibiting a high number of interbrain connections. These cortical areas could serve as a neural marker for the interactive component in verbal social communication. The present study is the first to investigate mother-child interbrain neural synchronization during verbal social interactions using a dual-MEG setup. Our results advance our understanding of turn-taking during verbal interaction between mother-child dyads and suggest a role for social "gating" in language learning.

Parentese in infancy predicts 5-year language complexity and conversational turns.

Parental input is considered a key predictor of language achievement during the first years of life, yet relatively few studies have assessed its effects on longer-term outcomes. We assess the effects of parental quantity of speech, use of parentese (the acoustically exaggerated, clear, and higher-pitched speech), and turn-taking in infancy, on child language at 5 years. Using a longitudinal dataset of daylong LENA recordings collected with the same group of English-speaking infants (N=44) at 6, 10, 14, 18, 24 months and then again at 5 years, we demonstrate that parents' consistent (defined as stable and high) use of parentese in infancy was a potent predictor of lexical diversity, mean length of utterance, and frequency of conversational turn-taking between children and adults at Kindergarten entry. Together, these findings highlight the potential importance of a high-quality language learning environment in infancy for success at the start of formal schooling.

A comparison of automatic and manual measures of turn-taking in monolingual and bilingual contexts.

The Language ENvironment Analysis system (LENA) records children's language environment and provides an automatic estimate of adult-child conversational turn count (CTC) by automatically identifying adult and child speech in close temporal proximity. To assess the reliability of this measure, we examine correlation and agreement between LENA's CTC estimates and manual measurement of adult-child turn-taking in two corpora collected in the USA: a bilingual corpus of Spanish-English-speaking families with infants between 4 and 22 months (n = 37), and a corpus of monolingual families with English-speaking 5-year-olds (n = 56). In each corpus for each child, 100 30-second segments were extracted from daylong recordings in two ways, yielding a total of 9300 minutes of manually annotated audio. LENA's CTC estimate for the same segments was obtained through the LENA software. The two measures of CTC had low correlations for the segments from the monolingual 5-year-olds sampled in both ways, and somewhat higher correlations for the bilingual samples. LENA substantially overestimated CTC on average, relative to manual measurement, for three out of four analysis conditions, and limits of agreement were wide in all cases. Segment-level analyses demonstrated that accidental contiguity had the largest individual impact on LENA's average CTC error, affecting 12-17% of analyzed segments. Other factors significantly contributing to CTC error were speech from other children, presence of multiple adults, and presence of electronic media. These results indicate wide discrepancies between LENA's CTC estimates and manual CTCs, and call into question the comparability of LENA's CTC measure across participants, conditions, and developmental time points.

Parent coaching from 6 to 18 months improves child language outcomes through 30 months of age.

Interventions focused on the home language environment have been shown to improve a number of child language outcomes in the first years of life. However, data on the longer-term effects of the intervention are still somewhat limited. The current study examines child vocabulary and complex speech outcomes (N = 59) during the year following completion of a parent-coaching intervention, which was previously found to increase the quantity of parent-child conversational turns and to improve child language outcomes through 18 months of age. Measures of parental language input, child speech output, and parent-child conversational turn-taking were manually coded from naturalistic home recordings (Language Environment Analysis System, LENA) at regular 4-month intervals when children were 6- to 24-months old. Child language skills were assessed using the MacArthur-Bates Communicative Development Inventory (CDI) at four time-points following the final intervention session (at 18, 24, 27, and 30 months). Vocabulary size and growth from 18 to 30 months was greater in the intervention group, even after accounting for differences in child language ability during the intervention period. The intervention group also scored higher on measures of speech length and grammatical complexity, and these effects were mediated by 18-month vocabulary. Intervention was associated with increased parent-child conversational turn-taking in home recordings at 14 months, and mediation analysis suggested that 14-month conversational turn-taking accounted for intervention-related differences in subsequent vocabulary. Together, the results suggest enduring, positive effects of parental language intervention and underscore the importance of interactive, conversational language experience during the first 2 years of life. RESEARCH HIGHLIGHTS: Parent coaching was provided as part of a home language intervention when children were 6-18 months of age. Naturalistic home language recordings showed increased parent-child conversational turn-taking in the intervention group at 14 months of age. Measures of productive vocabulary and complex speech indicated more advanced expressive language skills in the intervention group through 30 months of age, a full year after the final intervention session. Conversational turn-taking at 14 months predicted subsequent child vocabulary and accounted for differences in vocabulary size across the intervention and control groups.

Parent coaching increases conversational turns and advances infant language development.

Parental language input is one of the best predictors of children's language achievement. Parentese, a near-universal speaking style distinguished by higher pitch, slower tempo, and exaggerated intonation, has been documented in speech directed toward young children in many countries. Previous research shows that the use of parentese and parent-child turn-taking are both associated with advances in children's language learning. We conducted a randomized controlled trial to determine whether a parent coaching intervention delivered when the infants are 6, 10, and 14 mo of age can enhance parental language input and whether this, in turn, changes the trajectory of child language development between 6 and 18 mo of age. Families of typically developing 6-mo-old infants (n = 71) were randomly assigned to intervention and control groups. Naturalistic first-person audio recordings of the infants' home language environment and vocalizations were recorded when the infants were 6, 10, 14, and 18 mo of age. After the 6-, 10-, and 14-mo recordings, intervention, but not control parents attended individual coaching appointments to receive linguistic feedback, listen to language input in their own recordings, and discuss age-appropriate activities that promote language growth. Intervention significantly enhanced parental use of parentese and parent-child turn-taking between 6 and 18 mo. Increases in both variables were significantly correlated with children's language growth during the same period, and children's language outcomes at 18 mo. Using parentese, a socially and linguistically enhanced speaking style, improves children's social language turn-taking and language skills. Research-based interventions targeting social aspects of parent-child interactions can enhance language outcomes.

Development of infants' neural speech processing and its relation to later language skills: A MEG study.

The 'sensitive period' for phonetic learning (∼6-12 months) is one of the earliest milestones in language acquisition where infants start to become specialized in processing speech sounds in their native language. In the last decade, advancements in neuroimaging technologies for infants are starting to shed light on the underlying neural mechanisms supporting this important learning period. The current study reports on a large longitudinal dataset with the aim to replicate and extend on two important questions: 1) what are the developmental changes during the 'sensitive period' for native and nonnative speech processing? 2) how does native and nonnative speech processing in infants predict later language outcomes? Fifty-four infants were recruited at 7 months of age and their neural processing of speech was measured using Magnetoencephalography (MEG). Specifically, the neural sensitivity to a native and a nonnative speech contrast was indexed by the mismatch response (MMR). They repeated the measurement again at 11 months of age and their language development was further tracked from 12 months to 30 months of age using the MacArthur-Bates Communicative Development Inventory (CDI). Using an a priori Region-of-Interest (ROI) approach, we observed significant increases for the Native MMR in the left inferior frontal region (IF) and superior temporal region (ST) from 7 to 11 months, but not for the Nonnative MMR. Complementary whole brain comparison revealed more widespread developmental changes for both contrasts. However, only individual differences in the left IF and ST for the Nonnative MMR at 11 months of age were significant predictors of individual vocabulary growth up to 30 months of age. An exploratory machine-learning based analysis further revealed that whole brain time series for both Native and Nonnative contrasts can robustly predict later outcomes, but with very different underlying spatial-temporal patterns. The current study extends our current knowledge and suggests that native and nonnative speech processing may follow different developmental trajectories and utilize different mechanisms that are relevant for later language skills.

Brain myelination at 7 months of age predicts later language development.

Between 6 and 12 months of age there are dramatic changes in infants' processing of language. The neurostructural underpinnings of these changes are virtually unknown. The objectives of this study were to (1) examine changes in brain myelination during this developmental period and (2) examine the relationship between myelination during this period and later language development. Macromolecular proton fraction (MPF) was used as a marker of myelination. Whole-brain MPF maps were obtained with 1.25 mm3 isotropic spatial resolution from typically developing children at 7 and 11 months of age. Effective myelin density was calculated from MPF based on a linear relationship known from the literature. Voxel-based analyses were used to identify longitudinal changes in myelin density and to calculate correlations between myelin density at these ages and later language development. Increases in myelin density were more predominant in white matter than in gray matter. A strong predictive relationship was found between myelin density at 7 months of age, language production at 24 and 30 months of age, and rate of language growth. No relationships were found between myelin density at 11 months, or change in myelin density between 7 and 11 months of age, and later language measures. Our findings suggest that critical changes in brain structure may precede periods of pronounced change in early language skills.

Infant brain imaging using magnetoencephalography: Challenges, solutions, and best practices.

The excellent temporal resolution and advanced spatial resolution of magnetoencephalography (MEG) makes it an excellent tool to study the neural dynamics underlying cognitive processes in the developing brain. Nonetheless, a number of challenges exist when using MEG to image infant populations. There is a persistent belief that collecting MEG data with infants presents a number of limitations and challenges that are difficult to overcome. Due to this notion, many researchers either avoid conducting infant MEG research or believe that, in order to collect high-quality data, they must impose limiting restrictions on the infant or the experimental paradigm. In this article, we discuss the various challenges unique to imaging awake infants and young children with MEG, and share general best-practice guidelines and recommendations for data collection, acquisition, preprocessing, and analysis. The current article is focused on methodology that allows investigators to test the sensory, perceptual, and cognitive capacities of awake and moving infants. We believe that such methodology opens the pathway for using MEG to provide mechanistic explanations for the complex behavior observed in awake, sentient, and dynamically interacting infants, thus addressing core topics in developmental cognitive neuroscience.

Development of executive function-relevant skills is related to both neural structure and function in infants.

The development of skills related to executive function (EF) in infancy, including their emergence, underlying neural mechanisms, and interconnections to other cognitive skills, is an area of increasing research interest. Here, we report on findings from a multidimensional dataset demonstrating that infants' behavioral performance on a flexible learning task improved across development and that the task performance is highly correlated with both neural structure and neural function. The flexible learning task probed infants' ability to learn two different associations, concurrently, over 16 trials, requiring multiple skills relevant to EF. We examined infants' neural structure by measuring myelin density in the brain, using a novel macromolecular proton fraction (MPF) mapping method. We further examined an important neural function of speech processing by characterizing the mismatch response (MMR) to speech contrasts using magnetoencephalography (MEG). All measurements were performed longitudinally in monolingual English-learning infants at 7- and 11-months of age. At the group level, 11-month-olds, but not 7-month-olds, demonstrated evidence of learning both associations in the behavioral task. Myelin density in the prefrontal region at 7 months of age was found to be highly predictive of behavioral task performance at 11 months of age, suggesting that myelination may support the development of these skills. Furthermore, a machine-learning regression analysis revealed that individual differences in the behavioral task are predicted by concurrent neural speech processing at both ages, suggesting that these skills do not develop in isolation. Together, these cross-modality results revealed novel insights into EF-related skills. HIGHLIGHT: Monolingual infants demonstrated flexible learning on a task requiring executive function skills at 11 months, but not at 7 months. Infants' myelin density at 7 months is highly predictive of their behavioral performance in the flexible learning task at 11 months of age. Individual differences in the flexible learning task performance are also correlated with concurrent neural processing of speech at both ages.

Reduced Glx and GABA Inductions in the Anterior Cingulate Cortex and Caudate Nucleus Are Related to Impaired Control of Attention in Attention-Deficit/Hyperactivity Disorder.

Attention-deficit/hyperactivity disorder (ADHD) is a neurodevelopmental disorder that impairs the control of attention and behavioral inhibition in affected individuals. Recent genome-wide association findings have revealed an association between glutamate and GABA gene sets and ADHD symptoms. Consistently, people with ADHD show altered glutamate and GABA content in the brain circuitry that is important for attention control function. Yet, it remains unknown how glutamate and GABA content in the attention control circuitry change when people are controlling their attention, and whether these changes can predict impaired attention control in people with ADHD. To study these questions, we recruited 18 adults with ADHD (31-51 years) and 16 adults without ADHD (28-54 years). We studied glutamate + glutamine (Glx) and GABA content in the fronto-striatal circuitry while participants performed attention control tasks. We found that Glx and GABA concentrations at rest did not differ between participants with ADHD or without ADHD. However, while participants were performing the attention control tasks, participants with ADHD showed smaller Glx and GABA increases than participants without ADHD. Notably, smaller GABA increases in participants with ADHD significantly predicted their poor task performance. Together, these findings provide the first demonstration showing that attention control deficits in people with ADHD may be related to insufficient responses of the GABAergic system in the fronto-striatal circuitry.

Myelin development in cerebral gray and white matter during adolescence and late childhood.

Myelin development during adolescence is becoming an area of growing interest in view of its potential relationship to cognition, behavior, and learning. While recent investigations suggest that both white matter (WM) and gray matter (GM) undergo protracted myelination during adolescence, quantitative relations between myelin development in WM and GM have not been previously studied. We quantitatively characterized the dependence of cortical GM, WM, and subcortical myelin density across the brain on age, gender, and puberty status during adolescence with the use of a novel macromolecular proton fraction (MPF) mapping method. Whole-brain MPF maps from a cross-sectional sample of 146 adolescents (age range 9-17 years) were collected. Myelin density was calculated from MPF values in GM and WM of all brain lobes, as well as in subcortical structures. In general, myelination of cortical GM was widespread and more significantly correlated with age than that of WM. Myelination of GM in the parietal lobe was found to have a significantly stronger age dependence than that of GM in the frontal, occipital, temporal and insular lobes. Myelination of WM in the temporal lobe had the strongest association with age as compared to WM in other lobes. Myelin density was found to be higher in males as compared to females when averaged across all cortical lobes, as well as in a bilateral subcortical region. Puberty stage was significantly correlated with myelin density in several cortical areas and in the subcortical GM. These findings point to significant differences in the trajectories of myelination of GM and WM across brain regions and suggest that cortical GM myelination plays a dominant role during adolescent development.

Comparing Automatic and Manual Measures of Parent-Infant Conversational Turns: A Word of Caution.

The Language ENvironment Analysis system (LENA) records children's language environment and provides an automatic estimate of adult-child conversational turn count (CTC). The present study compares LENA's CTC estimate to manually coded CTC on a sample of 70 English-speaking infants recorded longitudinally at 6, 10, 14, 18, and 24 months of age. At each age, LENA's CTC was significantly higher than manually coded CTC (all ps < .001, Cohen's ds: 0.9-2.05), with the largest discrepancies between the two methods observed at younger ages. The Limits of Agreement Analyses confirm wide disagreements between the two methods, highlighting potential problems with automatic measurement of parent-infant verbal interaction. These findings suggest that future studies should validate LENA's CTC estimates with manual coding.

Linguistic effect on speech perception observed at the brainstem.

Linguistic experience affects speech perception from early infancy, as previously evidenced by behavioral and brain measures. Current research focuses on whether linguistic effects on speech perception can be observed at an earlier stage in the neural processing of speech (i.e., auditory brainstem). Brainstem responses reflect rapid, automatic, and preattentive encoding of sounds. Positive experiential effects have been reported by examining the frequency-following response (FFR) component of the complex auditory brainstem response (cABR) in response to sustained high-energy periodic portions of speech sounds (vowels and lexical tones). The current study expands the existing literature by examining the cABR onset component in response to transient and low-energy portions of speech (consonants), employing simultaneous magnetoencephalography (MEG) in addition to electroencephalography (EEG), which provide complementary source information on cABR. Utilizing a cross-cultural design, we behaviorally measured perceptual responses to consonants in native Spanish- and English-speaking adults, in addition to cABR. Brain and behavioral relations were examined. Results replicated previous behavioral differences between language groups and further showed that individual consonant perception is strongly associated with EEG-cABR onset peak latency. MEG-cABR source analysis of the onset peaks complimented the EEG-cABR results by demonstrating subcortical sources for both peaks, with no group differences in peak locations. Current results demonstrate a brainstem-perception relation and show that the effects of linguistic experience on speech perception can be observed at the brainstem level.

Two are better than one: Infant language learning from video improves in the presence of peers.

Studies show that young children learn new phonemes and words from humans significantly better than from machines. However, it is not clear why learning from video is ineffective or what might be done to improve learning from a screen. The present study, conducted with 9-month-old infants, utilized a manipulation-touch screen video-which allowed infants to control presentations of foreign-language video clips. We tested the hypothesis that infant learning from a screen would be enhanced in the presence of a peer, as opposed to learning alone. Brain measures of phonetic learning and detailed analyses of interaction during learning confirm the hypothesis that social partners enhance learning, even from screens.

Parent coaching at 6 and 10 months improves language outcomes at 14 months: A randomized controlled trial.

Previous studies reveal an association between particular features of parental language input and advances in children's language learning. However, it is not known whether parent coaching aimed to enhance specific input components would (a) successfully increase these components in parents' language input and (b) result in concurrent increases in children's language development. The present randomized controlled trial assigned families of typically developing 6-month-old infants to Intervention (parent coaching) and Control (no coaching) groups. Families were equivalent on socioeconomic status, infants' gender, and infants' age. Parent coaching took place when infants were 6 and 10 months of age, and included quantitative and qualitative linguistic feedback on the amount of child-directed speech, back-and-forth interactions, and parentese speech style. These variables were derived from each family's first-person LENA recordings at home. Input variables and infant language were measured at 6, 10, and 14 months. Parent coaching significantly enhanced language input as measured by two social interaction variables: percentage of speech directed to the child and percentage of parentese speech. These two variables were correlated, and were both related to growth in infant babbling between 6 and 14 months. Intervention infants showed greater growth in babbling than Control infants. Furthermore, at 14 months, Intervention infants produced significantly more words than Control infants, as indicated by LENA recordings and parent report via the MacArthur-Bates Communicative Developmental Inventory. Together, these results indicate that parent coaching can enrich specific aspects of parental language input, and can immediately and positively impact child language outcomes. A video abstract of this article can be viewed at: https://youtu.be/7wqR28gPiwo.

Neuroplasticity, bilingualism, and mental mathematics: A behavior-MEG study.

Bilingual experience alters brain structure and enhances certain cognitive functions. Bilingualism can also affect mathematical processing. Reduced accuracy is commonly reported when arithmetic problems are presented in bilinguals' second (L2) vs. first (L1) language. We used MEG brain imaging during mental addition to characterize spatiotemporal dynamics during mental addition in bilingual adults. Numbers were presented auditorally and sequentially in bilinguals' L1 and L2, and brain and behavioral data were collected simultaneously. Behaviorally, bilinguals showed lower accuracy for two-digit addition in L2 compared to L1. Brain data showed stronger response magnitude in L2 versus L1 prior to calculation, especially when two-digit numbers were involved. Brain and behavioral data were significantly correlated. Taken together, our results suggest that differences between languages emerge prior to mathematical calculation, with implications for the role of language in mathematics.

Musical intervention enhances infants' neural processing of temporal structure in music and speech.

Individuals with music training in early childhood show enhanced processing of musical sounds, an effect that generalizes to speech processing. However, the conclusions drawn from previous studies are limited due to the possible confounds of predisposition and other factors affecting musicians and nonmusicians. We used a randomized design to test the effects of a laboratory-controlled music intervention on young infants' neural processing of music and speech. Nine-month-old infants were randomly assigned to music (intervention) or play (control) activities for 12 sessions. The intervention targeted temporal structure learning using triple meter in music (e.g., waltz), which is difficult for infants, and it incorporated key characteristics of typical infant music classes to maximize learning (e.g., multimodal, social, and repetitive experiences). Controls had similar multimodal, social, repetitive play, but without music. Upon completion, infants' neural processing of temporal structure was tested in both music (tones in triple meter) and speech (foreign syllable structure). Infants' neural processing was quantified by the mismatch response (MMR) measured with a traditional oddball paradigm using magnetoencephalography (MEG). The intervention group exhibited significantly larger MMRs in response to music temporal structure violations in both auditory and prefrontal cortical regions. Identical results were obtained for temporal structure changes in speech. The intervention thus enhanced temporal structure processing not only in music, but also in speech, at 9 mo of age. We argue that the intervention enhanced infants' ability to extract temporal structure information and to predict future events in time, a skill affecting both music and speech processing.

Brain white matter structure and COMT gene are linked to second-language learning in adults.

Adult human brains retain the capacity to undergo tissue reorganization during second-language learning. Brain-imaging studies show a relationship between neuroanatomical properties and learning for adults exposed to a second language. However, the role of genetic factors in this relationship has not been investigated. The goal of the current study was twofold: (i) to characterize the relationship between brain white matter fiber-tract properties and second-language immersion using diffusion tensor imaging, and (ii) to determine whether polymorphisms in the catechol-O-methyltransferase (COMT) gene affect the relationship. We recruited incoming Chinese students enrolled in the University of Washington and scanned their brains one time. We measured the diffusion properties of the white matter fiber tracts and correlated them with the number of days each student had been in the immersion program at the time of the brain scan. We found that higher numbers of days in the English immersion program correlated with higher fractional anisotropy and lower radial diffusivity in the right superior longitudinal fasciculus. We show that fractional anisotropy declined once the subjects finished the immersion program. The relationship between brain white matter fiber-tract properties and immersion varied in subjects with different COMT genotypes. Subjects with the Methionine (Met)/Valine (Val) and Val/Val genotypes showed higher fractional anisotropy and lower radial diffusivity during immersion, which reversed immediately after immersion ended, whereas those with the Met/Met genotype did not show these relationships. Statistical modeling revealed that subjects' grades in the language immersion program were best predicted by fractional anisotropy and COMT genotype.