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.

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.

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.

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.

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.

The Carter Neurocognitive Assessment for children with severely compromised expressive language and motor skills.

In this paper, different means of assessing cognitive development in children with severe impairments in both their expressive language and their motor skills are reviewed. A range of techniques are considered, including traditional cognitive tests and behavioral and physiological measures, but these techniques are generally impractical and minimally informative when it comes to assessing children with both motor and speech impairments. Electrophysiological measures show some promise for the future, but are currently inadequate for wide-ranging cognitive assessment. Development of the Carter Neurocognitive Assessment (CNA) is described. The CNA is appropriate for use in clinical and research settings and was designed to minimalize the impact of severely impaired motor skills and expressive language on performance. The CNA is intended to itemize and quantify a range of skills reflecting a cognitive level up to approximately 18 to 24 months in four areas: Social Awareness, Visual Attention, Auditory Comprehension and Vocal Communication. The use of the CNA to assess the performance and developmental growth of eight children with Holoprosencephaly (HPE), a midline developmental brain malformation, is described. The CNA is a useful tool for the assessment of children with severely compromised motor and verbal skills and has provided a more positive view of the cognitive potential of children with severe handicaps, such as the sample of children with HPE, than that presented in the past.