Experience-dependent effects of passive auditory exposure in infants impact theta phase synchrony and predict later language.

The establishment of cortical representations critical for mounting language is supported by both ongoing neural maturation and experience-expectant plasticity as infants increasingly recognize the linguistic events that occur most often in their surrounding environment. Previous research has demonstrated that enhanced efficiency of syllabic representation and discrimination is facilitated by interactive attention-driven, nonspeech auditory experience. However, experience-dependent effects on syllable processing as a function of nonspeech, passive auditory exposure (PAE), remain unclear. As theta band-specific activity has been shown to support syllabic processing, we chose theta inter-trial phase synchrony to examine the experience-dependent effects of PAE on the processing of a syllable contrast. Results demonstrated that infants receiving PAE increased syllabic processing efficiency. Specifically, compared with controls, the group receiving PAE showed more mature, efficient processing, exhibiting less theta phase synchrony for the standard syllable at 9 months, and at 18 months, for the deviant syllable. Furthermore, the PAE modulatory effect on theta phase synchrony at 7 and 9 months was associated with language scores at 12 and 18 months. These findings confirm that supporting emerging perceptual abilities during early sensitive periods impacts syllabic processing efficiency and aligns with literature demonstrating associations between infant auditory perceptual abilities and later language outcomes.

Acoustic-level and language-specific processing of native and non-native phonological sequence onsets in the low gamma and theta-frequency bands.

Acoustic structures associated with native-language phonological sequences are enhanced within auditory pathways for perception, although the underlying mechanisms are not well understood. To elucidate processes that facilitate perception, time-frequency (T-F) analyses of EEGs obtained from native speakers of English and Polish were conducted. Participants listened to same and different nonword pairs within counterbalanced attend and passive conditions. Nonwords contained the onsets /pt/, /pət/, /st/, and /sət/ that occur in both the Polish and English languages with the exception of /pt/, which never occurs in the English language in word onset. Measures of spectral power and inter-trial phase locking (ITPL) in the low gamma (LG) and theta-frequency bands were analyzed from two bilateral, auditory source-level channels, created through source localization modeling. Results revealed significantly larger spectral power in LG for the English listeners to the unfamiliar /pt/ onsets from the right hemisphere at early cortical stages, during the passive condition. Further, ITPL values revealed distinctive responses in high and low-theta to acoustic characteristics of the onsets, which were modulated by language exposure. These findings, language-specific processing in LG and acoustic-level and language-specific processing in theta, support the view that multi scale temporal processing in the LG and theta-frequency bands facilitates speech perception.

Modulation of Theta Phase Synchrony during Syllable Processing as a Function of Interactive Acoustic Experience in Infancy.

Plasticity, a prominent characteristic of the infant brain, supports formation of cortical representations as infants begin to interact with and adapt to environmental sensory events. Enhanced acoustic processing efficiency along with improved allocation of attentional resources at 7 months and establishment of well-defined phonemic maps at 9 months have been shown to be facilitated by early interactive acoustic experience (IAE). In this study, using an oddball paradigm and measures of theta phase synchrony at source level, we examined short- and long-term effects of nonspeech IAE on syllable processing. Results demonstrated that beyond maturation alone, IAE increased the efficiency of syllabic representation and discrimination, an effect that endured well beyond the immediate training period. As compared with naive controls, the IAE-trained group at 7, 9, and 18 months showed less theta phase synchrony for the standard syllable and at 7 and 18 months for the deviant syllable. The decreased theta phase synchrony exhibited by the trained group suggests more mature, efficient, acoustic processing, and thus, better cortical representation and discrimination of syllabic content. Further, the IAE modulatory effect observed on theta phase synchrony in left auditory cortex at 7 and 9 months was differentially associated with receptive and expressive language scores at 12 and 18 months of age.

Retraction Note to: Stability of neuronal avalanches and long-range temporal correlations during the first year of life in human infant.

The authors have retracted this article Jannesari et al. (2019) because an incorrect version of the article was published in error. The manuscript has been republished as Jannesari et al. (2020). All authors agree to this retraction.

Stability of neuronal avalanches and long-range temporal correlations during the first year of life in human infants.

During infancy, the human brain rapidly expands in size and complexity as neural networks mature and new information is incorporated at an accelerating pace. Recently, it was shown that single-electrode EEG in preterms at birth exhibits scale-invariant intermittent bursts. Yet, it is currently not known whether the normal infant brain, in particular, the cortex, maintains a distinct dynamical state during development that is characterized by scale-invariant spatial as well as temporal aspects. Here we employ dense-array EEG recordings acquired from the same infants at 6 and 12 months of age to characterize brain activity during an auditory odd-ball task. We show that suprathreshold events organize as spatiotemporal clusters whose size and duration are power-law distributed, the hallmark of neuronal avalanches. Time series of local suprathreshold EEG events display significant long-range temporal correlations (LRTCs). No differences were found between 6 and 12 months, demonstrating stability of avalanche dynamics and LRTCs during the first year after birth. These findings demonstrate that the infant brain is characterized by distinct spatiotemporal dynamical aspects that are in line with expectations of a critical cortical state. We suggest that critical state dynamics, which theory and experiments have shown to be beneficial for numerous aspects of information processing, are maintained by the infant brain to process an increasingly complex environment during development.

Stability of neuronal avalanches and long-range temporal correlations during the first year of life in human infant.

During infancy, the human brain rapidly expands in size and complexity as neural networks mature and new information is incorporated at an accelerating pace. Recently, it was shown that single electrode EEG in preterms at birth exhibits scale-invariant intermittent bursts. Yet, it is currently not known whether the normal infant brain, in particular, the cortex maintains a distinct dynamical state during development that is characterized by scale-invariant spatial as well as temporal aspects. Here we employ dense-array EEG recordings acquired from the same infants at 6 and 12 months of age to characterize brain activity during an auditory oddball task. We show that suprathreshold events organize as spatiotemporal clusters whose size and duration are power-law distributed, the hallmark of neuronal avalanches. Time series of local suprathreshold EEG events display significant long-range temporal correlations (LRTCs). No differences were found between 6 and 12 months, demonstrating stability of avalanche dynamics and LRTCs during the first year after birth. These findings demonstrate that the infant brain is characterized by distinct spatiotemporal dynamical aspects that are in line with expectations of a critical cortical state. We suggest that critical state dynamics, which theory and experiments have shown to be beneficial for numerous aspects of information processing, are maintained by the infant brain to process an increasingly complex environment during development.

Change detection to tone pairs during the first year of life - Predictive longitudinal relationships for EEG-based source and time-frequency measures.

Brain responses related to auditory processing show large changes throughout infancy and childhood with some evidence that the two hemispheres might mature at different rates. Differing rates of hemispheric maturation could be linked to the proposed functional specialization of the hemispheres in which the left auditory cortex engages in analysis of precise timing information whereas the right auditory cortex focuses on analysis of sound frequency. Here the auditory change detection process for rapidly presented tone-pairs was examined in a longitudinal sample of infants at the age of 6 and 12 months using EEG. The ERP response related to change detection of a frequency contrast, its estimated source strength in the auditory areas, as well as time-frequency indices showed developmental effects. ERP amplitudes, source strength, spectral power and inter-trial phase locking decreased across age. A differential lateralization pattern emerged between 6 and 12 months as shown by inter-trial phase locking at 2-3 Hz; specifically, a larger developmental change was observed in the right as compared to the left hemisphere. Predictive relationships for the change in source strength from 6 months to 12 months were found. Six-month predictors were source strength and phase locking values at low frequencies. The results show that the infant change detection response in rapidly presented tone pairs is mainly determined by low frequency power and phase-locking with a larger phase-locking response at 6 months predicting greater change at 12 months. The ability of the auditory system to respond systematically across stimuli is suggested as a marker of maturational change that leads to more automatic and fine-tuned cortical responses.

Reduced left-lateralized pattern of event-related EEG oscillations in infants at familial risk for language and learning impairment.

The ability to rapidly discriminate successive auditory stimuli within tens-of-milliseconds is crucial for speech and language development, particularly in the first year of life. This skill, called Rapid Auditory Processing (RAP), is altered in infants at familial risk for language and learning impairment (LLI) and is a robust predictor of later language outcomes. In the present study, we investigate the neural substrates of RAP, i.e., the underlying neural oscillatory patterns, in a group of Italian 6-month-old infants at risk for LLI (FH+, n = 24), compared to control infants with no known family history of LLI (FH-, n = 32). Brain responses to rapid changes in fundamental frequency and duration were recorded via high-density electroencephalogram during a non-speech double oddball paradigm. Sources of event-related potential generators were localized to right and left auditory regions in both FH+ and FH- groups. Time-frequency analyses showed variations in both theta (Ɵ) and gamma (ɣ) ranges across groups. Our results showed that overall RAP stimuli elicited a more left-lateralized pattern of oscillations in FH- infants, whereas FH+ infants demonstrated a more right-lateralized pattern, in both the theta and gamma frequency bands. Interestingly, FH+ infants showed reduced early left gamma power (starting at 50 ms after stimulus onset) during deviant discrimination. Perturbed oscillatory dynamics may well constitute a candidate neural mechanism to explain group differences in RAP. Additional group differences in source location suggest that anatomical variations may underlie differences in oscillatory activity. Regarding the predictive value of early oscillatory measures, we found that the amplitude of the source response and the magnitude of oscillatory power and phase synchrony were predictive of expressive vocabulary at 20 months of age. These results further our understanding of the interplay among neural mechanisms that support typical and atypical rapid auditory processing in infancy.

Minimally-verbal children with autism show deficits in theta and gamma oscillations during processing of semantically-related visual information.

To acquire language, children must build phonemic representations of their native language, learn to associate auditory words to visual objects and assemble a lexicon. It is not clear however, whether the limited linguistic ability seen in minimally-verbal (MV) children with Autism Spectrum Disorder (ASD) relates to deficits in cortical representation of an object and/or in linking an object to its semantic information. This EEG-based study investigated neural mechanisms underlying visual processing of common objects in MV-ASD and control children. Ten MV-ASD children, 4- to 7- years-old and 15 age/gender-matched controls, were presented with a picture-word matching paradigm. Time-frequency analyses were conducted at the sources generating the event-related responses at both early and late visual processing. Permutation testing identified spectral power and phase coherence clusters that significantly differed between the groups. As compared to controls, MV-ASD children exhibited smaller amplitudes and longer source latencies; decreased gamma and theta power with less theta phase coherence in occipital regions, and reduced frontal gamma power. Our results confirm that visual processing is altered in MV-ASD children and suggest that some of the linguistic differences observed in these children arise from impaired object/label cortical representations and reduced allocation of attention, which would impact lexical acquisition.

Early Interactive Acoustic Experience with Non-speech Generalizes to Speech and Confers a Syllabic Processing Advantage at 9 Months.

During early development, the infant brain is highly plastic and sensory experiences modulate emerging cortical maps, enhancing processing efficiency as infants set up key linguistic precursors. Early interactive acoustic experience (IAE) with spectrotemporally-modulated non-speech has been shown to facilitate optimal acoustic processing and generalizes to novel non-speech sounds at 7-months-of-age. Here we demonstrate that effects of non-speech IAE endure well beyond the immediate training period and robustly generalize to speech processing. Infants who received non-speech IAE differed at 9-months-of-age from both naïve controls and those with only passive acoustic exposure, demonstrating broad modulation of oscillatory dynamics. For the standard syllable, increased high-gamma (>70 Hz) power within auditory cortices indicates that IAE fosters native speech processing, facilitating establishment of phonemic representations. The higher left beta power seen may reflect increased linking of sensory information and corresponding articulatory patterns, while bilateral decreases in theta power suggest more mature automatized speech processing, as less neuronal resources were allocated to process syllabic information. For the deviant syllable, left-lateralized gamma (<70 Hz) enhancement suggests IAE promotes phonemic-related discrimination abilities. Theta power increases in right auditory cortex, known for favoring slow-rate decoding, implies IAE facilitates the more demanding processing of the sporadic deviant syllable.

Effects of noise and age on the infant brainstem response to speech.

OBJECTIVE: Background noise makes hearing speech difficult for people of all ages. This difficulty can be exacerbated by co-occurring developmental deficits that often emerge in childhood. Sentence-type speech-in-noise (SIN) tests are available clinically but cannot be administered to very young individuals. Our objective was to examine the use of an electrophysiological test of SIN, suitable for infants, to track developmental trajectories. METHODS: Speech-evoked brainstem potentials were recorded from 30 typically-developing infants in quiet and +10 dB SNR background noise. Infants were divided into two age groups (7-12 and 18-24 months) and examined across development. Spectral power of the frequency following response (FFR) was computed using a fast Fourier Transform. Cross-correlations between quiet and noise responses were computed to measure encoding resistance to noise. RESULTS: Older infants had more robust FFR encoding in noise and had higher quiet-noise correlations than their younger counterparts. No group differences were observed in the quiet condition. CONCLUSIONS: By two years of age, infants show less vulnerability to the disruptive effects of background noise, compared to infants under 12 months. SIGNIFICANCE: Speech-in-noise electrophysiology can be easily recorded across infancy and provides unique insights into developmental differences that tests conducted in quiet may miss.

A Modulatory Effect of Brief Passive Exposure to Non-linguistic Sounds on Intrinsic Functional Connectivity: Relevance to Cognitive Performance.

A growing literature on resting-state fMRI (R-fMRI) has explored the impact of preceding sensory experience on intrinsic functional connectivity (iFC). However, it remains largely unknown how passive exposure to irrelevant auditory stimuli, which is a constant in everyday life, reconfigures iFC. Here, we directly compared pre- and post-exposure R-fMRI scans to examine: 1) modulatory effects of brief passive exposure to repeating non-linguistic sounds on subsequent iFC, and 2) associations between iFC modulations and cognitive abilities. We used an exploratory regional homogeneity (ReHo) approach that indexes local iFC, and performed a linear mixed-effects modeling analysis. A modulatory effect (increase) in ReHo was observed in the right superior parietal lobule (R.SPL) within the parietal attention network. Post hoc seed-based correlation analyses provided further evidence for increased parietal iFC (e.g., R.SPL with the right inferior parietal lobule). Notably, less iFC modulation was associated with better cognitive performance (e.g., word reading). These results suggest that: 1) the parietal attention network dynamically reconfigures its iFC in response to passive (thus irrelevant) non-linguistic sounds, but also 2) minimization of iFC modulation in the same network characterizes better cognitive performance. Our findings may open up new avenues for investigating cognitive disorders that involve impaired sensory processing.

Active auditory experience in infancy promotes brain plasticity in Theta and Gamma oscillations.

Language acquisition in infants is driven by on-going neural plasticity that is acutely sensitive to environmental acoustic cues. Recent studies showed that attention-based experience with non-linguistic, temporally-modulated auditory stimuli sharpens cortical responses. A previous ERP study from this laboratory showed that interactive auditory experience via behavior-based feedback (AEx), over a 6-week period from 4- to 7-months-of-age, confers a processing advantage, compared to passive auditory exposure (PEx) or maturation alone (Naïve Control, NC). Here, we provide a follow-up investigation of the underlying neural oscillatory patterns in these three groups. In AEx infants, Standard stimuli with invariant frequency (STD) elicited greater Theta-band (4-6Hz) activity in Right Auditory Cortex (RAC), as compared to NC infants, and Deviant stimuli with rapid frequency change (DEV) elicited larger responses in Left Auditory Cortex (LAC). PEx and NC counterparts showed less-mature bilateral patterns. AEx infants also displayed stronger Gamma (33-37Hz) activity in the LAC during DEV discrimination, compared to NCs, while NC and PEx groups demonstrated bilateral activity in this band, if at all. This suggests that interactive acoustic experience with non-linguistic stimuli can promote a distinct, robust and precise cortical pattern during rapid auditory processing, perhaps reflecting mechanisms that support fine-tuning of early acoustic mapping.

Oscillatory Dynamics Underlying Perceptual Narrowing of Native Phoneme Mapping from 6 to 12 Months of Age.

During the first months of life, human infants process phonemic elements from all languages similarly. However, by 12 months of age, as language-specific phonemic maps are established, infants respond preferentially to their native language. This process, known as perceptual narrowing, supports neural representation and thus efficient processing of the distinctive phonemes within the sound environment. Although oscillatory mechanisms underlying processing of native and non-native phonemic contrasts were recently delineated in 6-month-old infants, the maturational trajectory of these mechanisms remained unclear. A group of typically developing infants born into monolingual English families, were followed from 6 to 12 months and presented with English and Spanish syllable contrasts varying in voice-onset time. Brain responses were recorded with high-density electroencephalogram, and sources of event-related potential generators identified at right and left auditory cortices at 6 and 12 months and also at frontal cortex at 6 months. Time-frequency analyses conducted at source level found variations in both θ and γ ranges across age. Compared with 6-month-olds, 12-month-olds' responses to native phonemes showed smaller and faster phase synchronization and less spectral power in the θ range, and increases in left phase synchrony as well as induced high-γ activity in both frontal and left auditory sources. These results demonstrate that infants become more automatized and efficient in processing their native language as they approach 12 months of age via the interplay between θ and γ oscillations. We suggest that, while θ oscillations support syllable processing, γ oscillations underlie phonemic perceptual narrowing, progressively favoring mapping of native over non-native language across the first year of life. SIGNIFICANCE STATEMENT: During early language acquisition, typically developing infants gradually construct phonemic maps of their native language in auditory cortex. It is well known that, by 12 months of age, human infants move from universal discrimination of most linguistic phonemic contrasts to phonemic expertise in their native language. This perceptual narrowing occurs at the expense of the ability to process non-native phonemes. However, the neural mechanisms underlying this process are still poorly understood. Here we demonstrate that perceptual narrowing is, at least in part, accomplished by decreasing power and phase coherence in the θ range while increasing activity in high-γ in left auditory cortex. Understanding the normative neural mechanisms that support early language acquisition is crucial to understanding and perhaps ameliorating developmental language disorders.

High-resolution EEG source imaging of one-year-old children.

Recently we described an iterative skull conductivity and source location estimation (SCALE) algorithm for simultaneously estimating head tissue conductivities and brain source locations. SCALE uses a realistic FEM forward problem head model and scalp maps of 10 or more near-dipolar sources identified by independent component analysis (ICA) decomposition of sufficient high-density EEG data. In this study, we applied SCALE to 20 minutes of 64-channel EEG data and magnetic resonance (MR) head images from four twelve-months-of-age infants. For each child, we selected 15-16 near-dipolar independent components from multiple-model adaptive mixture ICA (AMICA) decomposition of their EEG data. SCALE converged to brain-to-skull conductivity ratio (BSCR) estimates in the 10-12 range and mostly compact gyral or sulcal cortical distributions for the IC sources.

Infant Auditory Processing and Event-related Brain Oscillations.

Rapid auditory processing and acoustic change detection abilities play a critical role in allowing human infants to efficiently process the fine spectral and temporal changes that are characteristic of human language. These abilities lay the foundation for effective language acquisition; allowing infants to hone in on the sounds of their native language. Invasive procedures in animals and scalp-recorded potentials from human adults suggest that simultaneous, rhythmic activity (oscillations) between and within brain regions are fundamental to sensory development; determining the resolution with which incoming stimuli are parsed. At this time, little is known about oscillatory dynamics in human infant development. However, animal neurophysiology and adult EEG data provide the basis for a strong hypothesis that rapid auditory processing in infants is mediated by oscillatory synchrony in discrete frequency bands. In order to investigate this, 128-channel, high-density EEG responses of 4-month old infants to frequency change in tone pairs, presented in two rate conditions (Rapid: 70 msec ISI and Control: 300 msec ISI) were examined. To determine the frequency band and magnitude of activity, auditory evoked response averages were first co-registered with age-appropriate brain templates. Next, the principal components of the response were identified and localized using a two-dipole model of brain activity. Single-trial analysis of oscillatory power showed a robust index of frequency change processing in bursts of Theta band (3 - 8 Hz) activity in both right and left auditory cortices, with left activation more prominent in the Rapid condition. These methods have produced data that are not only some of the first reported evoked oscillations analyses in infants, but are also, importantly, the product of a well-established method of recording and analyzing clean, meticulously collected, infant EEG and ERPs. In this article, we describe our method for infant EEG net application, recording, dynamic brain response analysis, and representative results.

Enhancement of gamma oscillations indicates preferential processing of native over foreign phonemic contrasts in infants.

Young infants discriminate phonetically relevant speech contrasts in a universal manner, that is, similarly across languages. This ability fades by 12 months of age as the brain builds language-specific phonemic maps and increasingly responds preferentially to the infant's native language. However, the neural mechanisms that underlie the development of infant preference for native over non-native phonemes remain unclear. Since gamma-band power is known to signal infants' preference for native language rhythm, we hypothesized that it might also indicate preference for native phonemes. Using high-density electroencephalogram/event-related potential (EEG/ERP) recordings and source-localization techniques to identify and locate the ERP generators, we examined changes in brain oscillations while 6-month-old human infants from monolingual English settings listened to English and Spanish syllable contrasts. Neural dynamics were investigated via single-trial analysis of the temporal-spectral composition of brain responses at source level. Increases in 4-6 Hz (theta) power and in phase synchronization at 2-4 Hz (delta/theta) were found to characterize infants' evoked responses to discrimination of native/non-native syllable contrasts mostly in the left auditory source. However, selective enhancement of induced gamma oscillations in the area of anterior cingulate cortex was seen only during native contrast discrimination. These results suggest that gamma oscillations support syllable discrimination in the earliest stages of language acquisition, particularly during the period in which infants begin to develop preferential processing for linguistically relevant phonemic features in their environment. Our results also suggest that by 6 months of age, infants already treat native phonemic contrasts differently from non-native, implying that perceptual specialization and establishment of enduring phonemic memory representations have been initiated.

Oscillatory support for rapid frequency change processing in infants.

Rapid auditory processing and auditory change detection abilities are crucial aspects of speech and language development, particularly in the first year of life. Animal models and adult studies suggest that oscillatory synchrony, and in particular low-frequency oscillations play key roles in this process. We hypothesize that infant perception of rapid pitch and timing changes is mediated, at least in part, by oscillatory mechanisms. Using event-related potentials (ERPs), source localization and time-frequency analysis of event-related oscillations (EROs), we examined the neural substrates of rapid auditory processing in 4-month-olds. During a standard oddball paradigm, infants listened to tone pairs with invariant standard (STD, 800-800 Hz) and variant deviant (DEV, 800-1200 Hz) pitch. STD and DEV tone pairs were first presented in a block with a short inter-stimulus interval (ISI) (Rapid Rate: 70 ms ISI), followed by a block of stimuli with a longer ISI (Control Rate: 300 ms ISI). Results showed greater ERP peak amplitude in response to the DEV tone in both conditions and later and larger peaks during Rapid Rate presentation, compared to the Control condition. Sources of neural activity, localized to right and left auditory regions, showed larger and faster activation in the right hemisphere for both rate conditions. Time-frequency analysis of the source activity revealed clusters of theta band enhancement to the DEV tone in right auditory cortex for both conditions. Left auditory activity was enhanced only during Rapid Rate presentation. These data suggest that local low-frequency oscillatory synchrony underlies rapid processing and can robustly index auditory perception in young infants. Furthermore, left hemisphere recruitment during rapid frequency change discrimination suggests a difference in the spectral and temporal resolution of right and left hemispheres at a very young age.

Regional infant brain development: an MRI-based morphometric analysis in 3 to 13 month olds.

Elucidation of infant brain development is a critically important goal given the enduring impact of these early processes on various domains including later cognition and language. Although infants' whole-brain growth rates have long been available, regional growth rates have not been reported systematically. Accordingly, relatively less is known about the dynamics and organization of typically developing infant brains. Here we report global and regional volumetric growth of cerebrum, cerebellum, and brainstem with gender dimorphism, in 33 cross-sectional scans, over 3 to 13 months, using T1-weighted 3-dimensional spoiled gradient echo images and detailed semi-automated brain segmentation. Except for the midbrain and lateral ventricles, all absolute volumes of brain regions showed significant growth, with 6 different patterns of volumetric change. When normalized to the whole brain, the regional increase was characterized by 5 differential patterns. The putamen, cerebellar hemispheres, and total cerebellum were the only regions that showed positive growth in the normalized brain. Our results show region-specific patterns of volumetric change and contribute to the systematic understanding of infant brain development. This study greatly expands our knowledge of normal development and in future may provide a basis for identifying early deviation above and beyond normative variation that might signal higher risk for neurological disorders.