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.

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.

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.

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.

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.

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.

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.

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.

Time course of ERP generators to syllables in infants: a source localization study using age-appropriate brain templates.

Event-related potentials (ERPs) have become an important tool in the quest to understand how infants process perceptual information. Identification of the activation loci of the ERP generators is a technique that provides an opportunity to explore the neural substrates that underlie auditory processing. Nevertheless, as infant brain templates from healthy, non-clinical samples have not been available, the majority of source localization studies in infants have used non-realistic head models, or brain templates derived from older children or adults. Given the dramatic structural changes seen across infancy, all of which profoundly affect the electrical fields measured with EEG, it is important to use individual MRIs or age-appropriate brain templates and parameters to explore the localization and time course of auditory ERP sources. In this study 6-month-old infants were presented with a passive oddball paradigm using consonant-vowel (CV) syllables that differed in voice onset time. Dense-array EEG/ERPs were collected while the infants were awake and alert. In addition, MRIs were acquired during natural non-sedated sleep for a subset of the sample. Discrete dipole and distributed source models were mapped onto individual and averaged infant MRIs. The CV syllables elicited a positive deflection at about 200 ms followed by a negative deflection that peaked around 400 ms. The source models generated placed the dipoles at temporal areas close to auditory cortex for both positive and negative responses. Notably, an additional dipole for the positive peak was localized at the frontal area, at the anterior cingulate cortex (ACC) level. ACC activation has been reported in adults, but has not, to date, been reported in infants during processing of speech-related signals. The frontal ACC activation was earlier but smaller in amplitude than the left and right auditory temporal activations. These results demonstrate that in infancy the ERP generators to CV syllables are localized in cortical areas similar to that reported in adults, but exhibit a notably different temporal course. Specifically, ACC activation in infants significantly precedes auditory temporal activation, whereas in adults ACC activation follows that of temporal cortex. We suggest that these timing differences could be related to current maturational changes, to the ongoing construction of language-specific phonetic maps, and/or to more sensitive attentional switching as a response to speech signals in infancy.

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.

Source localization of event-related potentials to pitch change mapped onto age-appropriate MRIs at 6 months of age.

Auditory event-related potentials (ERPs) have been used to understand how the brain processes auditory input, and to track developmental change in sensory systems. Localizing ERP generators can provide invaluable insights into how and where auditory information is processed. However, age-appropriate infant brain templates have not been available to aid such developmental mapping. In this study, auditory change detection responses of brain ERPs were examined in 6-month-old infants using discrete and distributed source localization methods mapped onto age-appropriate magnetic resonance images. Infants received a passive oddball paradigm using fast-rate non-linguistic auditory stimuli (tone doublets) with the deviant incorporating a pitch change for the second tone. Data was processed using two different high-pass filters. When a 0.5 Hz filter was used, the response to the pitch change was a large frontocentral positive component. When a 3 Hz filter was applied, two temporally consecutive components associated with change detection were seen: one with negative voltage, and another with positive voltage over frontocentral areas. Both components were localized close to the auditory cortex with an additional source near to the anterior cingulate cortex. The sources for the negative response had a more tangential orientation relative to the supratemporal plane compared to the positive response, which showed a more lateral, oblique orientation. The results described here suggest that at 6 months of age infants generate similar response patterns and use analogous cortical areas to that of adults to detect changes in the auditory environment. Moreover, the source locations and orientations, together with waveform topography and morphology provide evidence in infants for feature-specific change detection followed by involuntary switching of attention.

Associations between the size of the amygdala in infancy and language abilities during the preschool years in normally developing children.

Recently, structural MRI studies in children have been used to examine relations between brain volume and behavioral measures. However, most of these studies have been done in children older than 2 years of age. Obtaining volumetric measures in infants is considerably more difficult, as structures are less well defined and largely unmyelinated, making segmentation challenging. Moreover, it is still unclear whether individual anatomic variation across development, in healthy, normally developing infants, is reflected in the configuration and function of the mature brain and, as importantly, whether variation in infant brain structure might be related to later cognitive and linguistic abilities. In this longitudinal study, using T1 structural MRI, we identified links between amygdala volume in normally developing, naturally sleeping, 6-month infants and their subsequent language abilities at 2, 3 and 4 years. The images were processed and manually segmented using Cardviews to extract volumetric measures. Intra-rater reliability for repeated segmentation was 87.73% of common voxel agreement. Standardized language assessments were administered at 6 and 12 months and at 2, 3 and 4 years. Significant and consistent correlations were found between amygdala size and language abilities. Children with larger right amygdalae at 6 months had lower scores on expressive and receptive language measures at 2, 3, and 4 years. Associations between amygdala size and language outcomes have been reported in children with autism. The findings presented here extend this association to normally developing children, supporting the idea that the amygdalae might play an important but as yet unspecified role in mediating language acquisition.

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.

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.

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.

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.

Understanding language and cognitive deficits in very low birth weight children.

Very-low-birth-weight infants are at much higher risk for cognitive and language delays but the nature of such deficits is not clearly understood. Given increasing rates of prematurity and infants born very-low-birth-weight, examination of mechanisms that underlie poorer developmental outcome is essential. We investigated language and cognitive abilities in very-low and normal birth-weight infants to determine whether performance differences were due to poorer global cognitive performance or to deficits in specific processing abilities. Thirty-two very-low and 32 normal birth-weight infants received visual and auditory-visual habituation recognition-memory tasks, and standardized language and cognitive assessments. Very-low-birth-weight infants performed more poorly on visual and auditory-visual habituation tasks and scored lower than controls on cognitive and language measures. These findings suggest that differences in language abilities in very-low-birth-weight children may be part of a global deficit that impacts many areas of cognitive functioning rather than a specific impairment in rapid auditory processing.

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.