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.

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.

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.

From Sensory Perception to Lexical-Semantic Processing: An ERP Study in Non-Verbal Children with Autism.

This study examines electrocortical activity associated with visual and auditory sensory perception and lexical-semantic processing in nonverbal (NV) or minimally-verbal (MV) children with Autism Spectrum Disorder (ASD). Currently, there is no agreement on whether these children comprehend incoming linguistic information and whether their perception is comparable to that of typically developing children. Event-related potentials (ERPs) of 10 NV/MV children with ASD and 10 neurotypical children were recorded during a picture-word matching paradigm. Atypical ERP responses were evident at all levels of processing in children with ASD. Basic perceptual processing was delayed in both visual and auditory domains but overall was similar in amplitude to typically-developing children. However, significant differences between groups were found at the lexical-semantic level, suggesting more atypical higher-order processes. The results suggest that although basic perception is relatively preserved in NV/MV children with ASD, higher levels of processing, including lexical- semantic functions, are impaired. The use of passive ERP paradigms that do not require active participant response shows significant potential for assessment of non-compliant populations such as NV/MV children with ASD.

Auditory discrimination predicts linguistic outcome in Italian infants with and without familial risk for language learning impairment.

Infants' ability to discriminate between auditory stimuli presented in rapid succession and differing in fundamental frequency (Rapid Auditory Processing [RAP] abilities) has been shown to be anomalous in infants at familial risk for Language Learning Impairment (LLI) and to predict later language outcomes. This study represents the first attempt to investigate RAP in Italian infants at risk for LLI (FH+), examining two critical acoustic features: frequency and duration, both embedded in a rapidly-presented acoustic environment. RAP skills of 24 FH+ and 32 control (FH-) Italian 6-month-old infants were characterized via EEG/ERP using a multi-feature oddball paradigm. Outcome measures of expressive vocabulary were collected at 20 months. Group differences favoring FH- infants were identified: in FH+ infants, the latency of the N2* peak was delayed and the mean amplitude of the positive mismatch response was reduced, primarily for frequency discrimination and within the right hemisphere. Moreover, both EEG measures were correlated with language scores at 20 months. Results indicate that RAP abilities are atypical in Italian infants with a first-degree relative affected by LLI and that this impacts later linguistic skills. These findings provide a compelling cross-linguistic comparison with previous research on American infants, supporting the biological unity hypothesis of LLI.

Electrocortical Dynamics in Children with a Language-Learning Impairment Before and After Audiovisual Training.

Detecting and discriminating subtle and rapid sound changes in the speech environment is a fundamental prerequisite of language processing, and deficits in this ability have frequently been observed in individuals with language-learning impairments (LLI). One approach to studying associations between dysfunctional auditory dynamics and LLI, is to implement a training protocol tapping into this potential while quantifying pre- and post-intervention status. Event-related potentials (ERPs) are highly sensitive to the brain correlates of these dynamic changes and are therefore ideally suited for examining hypotheses regarding dysfunctional auditory processes. In this study, ERP measurements to rapid tone sequences (standard and deviant tone pairs) along with behavioral language testing were performed in 6- to 9-year-old LLI children (n = 21) before and after audiovisual training. A non-treatment group of children with typical language development (n = 12) was also assessed twice at a comparable time interval. The results indicated that the LLI group exhibited considerable gains on standardized measures of language. In terms of ERPs, we found evidence of changes in the LLI group specifically at the level of the P2 component, later than 250 ms after the onset of the second stimulus in the deviant tone pair. These changes suggested enhanced discrimination of deviant from standard tone sequences in widespread cortices, in LLI children after training.

Plasticity in developing brain: active auditory exposure impacts prelinguistic acoustic mapping.

A major task across infancy is the creation and tuning of the acoustic maps that allow efficient native language processing. This process crucially depends on ongoing neural plasticity and keen sensitivity to environmental cues. Development of sensory mapping has been widely studied in animal models, demonstrating that cortical representations of the sensory environment are continuously modified by experience. One critical period for optimizing human language mapping is early in the first year; however, the neural processes involved and the influence of passive compared with active experience are as yet incompletely understood. Here we demonstrate that, while both active and passive acoustic experience from 4 to 7 months of age, using temporally modulated nonspeech stimuli, impacts acoustic mapping, active experience confers a significant advantage. Using event-related potentials (ERPs), we show that active experience increases perceptual vigilance/attention to environmental acoustic stimuli (e.g., larger and faster P2 peaks) when compared with passive experience or maturation alone. Faster latencies are also seen for the change discrimination peak (N2*) that has been shown to be a robust infant predictor of later language through age 4 years. Sharpening is evident for both trained and untrained stimuli over and above that seen for maturation alone. Effects were also seen on ERP morphology for the active experience group with development of more complex waveforms more often seen in typically developing 12- to 24-month-old children. The promise of selectively "fine-tuning" acoustic mapping as it emerges has far-reaching implications for the amelioration and/or prevention of developmental language disorders.

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.

Early gamma oscillations during rapid auditory processing in children with a language-learning impairment: changes in neural mass activity after training.

Children with language-learning impairment (LLI) have consistently shown difficulty with tasks requiring precise, rapid auditory processing. Remediation based on neural plasticity assumes that the temporal precision of neural coding can be improved by intensive training protocols. Here, we examined the extent to which early oscillatory responses in auditory cortex change after audio-visual training, using combined source modeling and time-frequency analysis of the human electroencephalogram (EEG). Twenty-one elementary school students diagnosed with LLI underwent the intervention for an average of 32 days. Pre- and post-training assessments included standardized language/literacy tests and EEG recordings in response to fast-rate tone doublets. Twelve children with typical language development were also tested twice, with no intervention given. Behaviorally, improvements on measures of language were observed in the LLI group following completion of training. During the first EEG assessment, we found reduced amplitude and phase-locking of early (45-75 ms) oscillations in the gamma-band range (29-52 Hz), specifically in the LLI group, for the second stimulus of the tone doublet. Amplitude reduction for the second tone was no longer evident for the LLI children post-intervention, although these children still exhibited attenuated phase-locking. Our findings suggest that specific aspects of inefficient sensory cortical processing in LLI are ameliorated after training.

Resting frontal gamma power at 16, 24 and 36 months predicts individual differences in language and cognition at 4 and 5 years.

Gamma activity has been linked to a variety of different cognitive processes and exists in both transient and persistent forms. Across studies, different brain regions have been suggested to contribute to gamma activity. Multiple studies have shown that the function of gamma oscillations may be related to temporal binding of early sensory information to relevant top-down processes. Given this hypothesis, we expected gamma oscillations to subserve general brain mechanisms that contribute to the development of cognitive and linguistic systems. The present study aims to examine the predictive relations between resting-state cortical gamma power density at a critical point in language and cognitive acquisition (i.e. 16, 24 and 36 months), and cognitive and language output at ages 4 and 5 years. Our findings show that both 24- and 36-month gamma power are significantly correlated with later language scores, notably Non-Word Repetition. Further, 16-, 24- and 36-month gamma were all significantly correlated with 4-year PLS-3 and CELF-P sentence structure scores. Although associations reported here do not reflect a direct cause and effect of early resting gamma power on later language outcomes, capacity to generate higher power in the gamma range at crucial developmental periods may index better modulation of attention and allow easier access to working memory, thus providing an advantage for overall development, particularly in the linguistic domain. Moreover, measuring abilities at times when these abilities are still emergent may allow better prediction of later outcomes.

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.

Maturation of auditory evoked potentials from 6 to 48 months: prediction to 3 and 4 year language and cognitive abilities.

OBJECTIVE: To investigate the maturation of long-latency auditory evoked potentials (LLAEP) from 6 to 48 months in infants with a family history of language impairment (FH+) and control infants (FH-). METHODS: LLAEPs of seventeen FH+ infants were compared to 28 FH- infants at 6, 9, 12, 16, 24, 36 and 48 months. Participants received a passive oddball paradigm using fast- and slow-rate non-linguistic auditory stimuli and at 36 and 48 months completed a battery of standardized language and cognitive tests. RESULTS: Overall, the morphology of LLAEP responses differed for fast- versus slow-rate stimuli. Significant age-related changes in latency and amplitude were observed. Group differences, favoring FH- infants, in the rate of maturation of LLAEPs were found. Responses to fast-rate stimuli predicted language abilities at 36 and 48 months of age. CONCLUSIONS: The development of LLAEP in FH+ children is modulated by differences in the rate of maturation as well as variations in temporal processing abilities. SIGNIFICANCE: These findings provide evidence for the role of non-linguistic auditory processes in early language development and illustrate the utility of using a perceptual-processing skills model to further our understanding of the precursors of language development and impairment.

Involuntary switching of attention mediates differences in event-related responses to complex tones between early and late Spanish-English bilinguals.

Most research with bilinguals has used speech stimuli to demonstrate differences in auditory processing abilities. Two main factors have been identified as modulators of such differences: proficiency and age of acquisition of the second language (L2). However, whether the bilingual brain differs from the monolingual in the efficient processing of non-verbal auditory events (known to be critical to the acoustic analysis of the speech stream) remains unclear. In this EEG/ERP study, using the mismatch negativity (MMN), P3a, and late negativity (LN), we examined differences in discrimination, involuntary switching of attention and reorienting of attention between monolinguals and bilinguals as they processed complex tones. Further, we examined the role that age of acquisition plays in modulating such responses. A group of English monolinguals and a group of proficient Spanish-English bilinguals were presented with a multiple-deviant oddball paradigm with four deviant conditions (duration, frequency, silent gap, and frequency modulation). Late bilinguals, who learned English after age 10, exhibited larger MMN and P3a responses than early bilinguals, across all deviant conditions. Significant associations were found between amplitude of the responses and both age of L2 acquisition and years of L2 experience. Individuals who acquired English at later ages and had fewer years of L2 experience had larger MMN, P3a, and LN responses than those who learned it earlier. These findings demonstrate that age of L2 acquisition is an important modulator of auditory responses in bilinguals even when processing non-speech signals. Involuntary attention switching is suggested as the main factor driving these differences.

Early cognitive and language skills are linked to resting frontal gamma power across the first 3 years.

High-frequency cortical activity in humans and animals has been linked to a wide variety of higher cognitive processes. This research suggests that specific changes in neuronal synchrony occur during cognitive processing, distinguished by emergence of fast oscillations in the gamma frequency range. To determine whether the development of high-frequency brain oscillations can be related to the development of cognitive abilities, we studied the power spectra of resting EEG in children 16, 24 and 36 months of age. Individual differences in the distribution of frontal gamma power during rest were highly correlated with concurrent language and cognitive skills at all ages. Gamma power was also associated with attention measures; children who were observed as having better inhibitory control and more mature attention shifting abilities had higher gamma power density functions. We included a group of children with a family history of language impairment (FH+) and thus at higher risk for language disorders. FH+ children, as a group, showed consistently lower gamma over frontal regions than the well-matched FH- controls with no such family history (FH-). We suggest that the emergence of high-frequency neural synchrony may be critical for cognitive and linguistic development, and that children at risk for language impairments may lag in this process.

Infant information processing and family history of specific language impairment: converging evidence for RAP deficits from two paradigms.

An infant's ability to process auditory signals presented in rapid succession (i.e. rapid auditory processing abilities [RAP]) has been shown to predict differences in language outcomes in toddlers and preschool children. Early deficits in RAP abilities may serve as a behavioral marker for language-based learning disabilities. The purpose of this study is to determine if performance on infant information processing measures designed to tap RAP and global processing skills differ as a function of family history of specific language impairment (SLI) and/or the particular demand characteristics of the paradigm used. Seventeen 6- to 9-month-old infants from families with a history of specific language impairment (FH+) and 29 control infants (FH-) participated in this study. Infants' performance on two different RAP paradigms (head-turn procedure [HT] and auditory-visual habituation/recognition memory [AVH/RM]) and on a global processing task (visual habituation/recognition memory [VH/RM]) was assessed at 6 and 9 months. Toddler language and cognitive skills were evaluated at 12 and 16 months. A number of significant group differences were seen: FH+ infants showed significantly poorer discrimination of fast rate stimuli on both RAP tasks, took longer to habituate on both habituation/recognition memory measures, and had lower novelty preference scores on the visual habituation/recognition memory task. Infants' performance on the two RAP measures provided independent but converging contributions to outcome. Thus, different mechanisms appear to underlie performance on operantly conditioned tasks as compared to habituation/recognition memory paradigms. Further, infant RAP processing abilities predicted to 12- and 16-month language scores above and beyond family history of SLI. The results of this study provide additional support for the validity of infant RAP abilities as a behavioral marker for later language outcome. Finally, this is the first study to use a battery of infant tasks to demonstrate multi-modal processing deficits in infants at risk for SLI.

Links between abnormal brain structure and cognition in holoprosencephaly.

Converging information on medical issues, motor ability, and cognitive outcomes is essential when addressing long-term clinical management in children with holoprosencephaly. This study considered whether adding more informative structural indices to classic holoprosencephaly categories would increase prediction of cognitive outcomes. Forty-two children with holoprosencephaly were examined to determine the association of deep gray nuclei abnormalities with cognitive abilities and the effect of motor skill deficits on cognitive performance. Additionally, a cognitive profile was described using the Carter Neurocognitive Assessment, an experimental diagnostic instrument designed specifically for young children with severe neurodevelopmental dysfunction. Findings indicated that nonseparation of the deep gray nuclei was significantly associated with the cognitive construct of vocal communication, but not with the cognitive constructs of social awareness, visual attention, or auditory comprehension. Importantly, motor skill deficits did not significantly affect performance on the Carter Neurocognitive Assessment. This study is the first investigation to provide a descriptive overview of specific cognitive skills in this group of children. The results also strongly suggest that this feature of the brain's structure does not predict all aspects of neurodevelopmental function. These findings contribute a critical component to the growing body of knowledge regarding the medical and clinical outcomes of children with holoprosencephaly.

Auditory event-related responses in children with semi-lobar holoprosencephaly.

The purpose of this study was to evaluate auditory sensory and discrimination responses in children with semi-lobar holoprosencephaly (HPE). Event-related potential (ERP) signals were recorded to tone pair stimuli at 62 electrode sites from the scalp using an oddball paradigm (a two-block design, inter-stimulus interval=70 or 300 ms; frequency of tone pair=100 vs. 100 Hz for the frequent and 100 vs. 300 Hz for the infrequent). Latencies and amplitudes of P150, N250, and mismatch negativity (MMN)-like components were compared between children with HPE and controls. Our results revealed less organized ERP waveforms to both stimuli in children with HPE, with diminished P150 and N250 components across brain area. Robust and delayed MMN-like responses were elicited from the children with HPE, with decreased MMN amplitudes in the central, parietal, occipital, and posterior temporal areas. Our results suggest that while brain sensory responses to auditory tones may be impaired in children with semi-lobar HPE, subcomponents of auditory discrimination processes remain functional.

Brain responses to tonal changes in the first two years of life.

Maturation of auditory perceptual and discrimination process within the first two years of life is investigated in healthy infants by examining event-related potentials (ERPs). High-density EEG signals were recorded from the scalp monthly between 3 and 24 months of age. Two types of stimuli (100 vs. 100 Hz for standard stimuli; 100 vs. 300 Hz for deviant stimuli; occurrence rate: 85:15%) were presented using an oddball paradigm. Latencies and amplitudes were compared across development. The results showed that latencies of P150, N250, P350, and N450 components gradually decreased with increasing age. Amplitudes of the N250 and P350 components gradually increased and reached the maximum at 9 months, and then gradually decreased with the increase of age. Mismatch negativity was not obvious at 3 months of age, but was seen at 4-5 months and became robust after 6 months. Robust late positivity was recorded at all ages. These mismatch responses were noticeable in the frontal, central, and parietal areas, and the maximal MMN amplitude distribution gradually moved from the parietal area to the frontal area across the age range. Two important periods--one around 6 months and the other around 9 months are suggested in the maturation of auditory central system. Dynamical changes in the underlying source strengths and orientations may be principal contributors to ERP morphological changes in infants within the first 24 months.

Timing errors in auditory event-related potentials.

Electronic problems of electroencephalographic (EEG) system may occur in even the best-managed laboratories. Timing error may happen in the coupling of computers from various manufactures, resulting in the misalignment of event markers that signal the onset of stimuli. In one system, an impedance check desynchronized a computer and thus caused misalignment of events in EEG signals. Thus, the aim of this study was to develop a method to identify and correct such timing errors that contaminated 114 raw data of EEG/auditory event-related potentials (ERPs) recorded in one of our longitudinal studies. A two-step procedure was introduced in the correction of timing errors. First, the time delay was roughly estimated by identifying a P150 component in two ERP blocks. Second, a small phase-locked positive wave was identified for fine estimation. Reliability within and among evaluators was examined using ERP data with simulated timing errors. Concordant results were obtained in 104 (91.2%) of the 114 raw EEG/ERP data sets. Our results showed that the method presented here is reliable and can be used for correcting timing errors without introduction of experimenter bias.