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 ...

Rutgers University, State University of New Jersey, Newark

University of the Pacific

Stanford University

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.

Oscillatory support for rapid frequency change processing in infants.

To establish reliable procedures and normative values to quantify brainstem encoding of speech sounds.

Brainstem responses to speech syllables.

Afferent auditory processing in the human brainstem is often assumed to be determined by acoustic stimulus features alone and immune to stimulation by other senses or cognitive factors. In contrast, we show that lipreading during speech perception influences early acoustic processing. Event-related brainstem potentials were recorded from ten healthy adults to concordant (acoustic-visual match), conflicting (acoustic-visual mismatch) and unimodal stimuli. Audiovisual (AV) interactions occurred as early as approximately 11 ms post-acoustic stimulation and persisted for the first 30 ms of the response. Furthermore, the magnitude of interaction depended on AV pairings. These findings indicate considerable plasticity in early auditory processing.

Seeing speech affects acoustic information processing in the human brainstem.

Musical training is known to modify cortical organization. Here, we show that such modifications extend to subcortical sensory structures and generalize to processing of speech. Musicians had earlier and larger brainstem responses than nonmusician controls to both speech and music stimuli presented in auditory and audiovisual conditions, evident as early as 10 ms after acoustic onset. Phase-locking to stimulus periodicity, which likely underlies perception of pitch, was enhanced in musicians and strongly correlated with length of musical practice. In addition, viewing videos of speech (lip-reading) and music (instrument being played) enhanced temporal and frequency encoding in the auditory brainstem, particularly in musicians. These findings demonstrate practice-related changes in the early sensory encoding of auditory and audiovisual information.

Musicians have enhanced subcortical auditory and audiovisual processing of speech and music.

Musicians have a variety of perceptual and cortical specializations compared to non-musicians. Recent studies have shown that potentials evoked from primarily brainstem structures are enhanced in musicians, compared to non-musicians. Specifically, musicians have more robust representations of pitch periodicity and faster neural timing to sound onset when listening to sounds or both listening to and viewing a speaker. However, it is not known whether musician-related enhancements at the subcortical level are correlated with specializations in the cortex. Does musical training shape the auditory system in a coordinated manner or in disparate ways at cortical and subcortical levels? To answer this question, we recorded simultaneous brainstem and cortical evoked responses in musician and non-musician subjects. Brainstem response periodicity was related to early cortical response timing across all subjects, and this relationship was stronger in musicians. Peaks of the brainstem response evoked by sound onset and timbre cues were also related to cortical timing. Neurophysiological measures at both levels correlated with musical skill scores across all subjects. In addition, brainstem and cortical measures correlated with the age musicians began their training and the years of musical practice. Taken together, these data imply that neural representations of pitch, timing and timbre cues and cortical response timing are shaped in a coordinated manner, and indicate corticofugal modulation of subcortical afferent circuitry.

Relationships between behavior, brainstem and cortical encoding of seen and heard speech in musicians and non-musicians.

To examine the impact of hearing loss (HL) on audiovisual (AV) processing in the aging population. We hypothesized that age-related HL would have a pervasive effect on sensory processing, extending beyond the auditory domain. Specifically, we predicted that decreased auditory input to the neural system, in the form of HL over time, would have deleterious effects on multisensory mechanisms.

Audiovisual deficits in older adults with hearing loss: biological evidence.

Most auditory events in nature are accompanied by non-auditory signals, such as a view of the speaker's face during face-to-face communication or the vibration of a string during a musical performance. While it is known that accompanying visual and somatosensory signals can benefit auditory perception, often by making the sound seem louder, the specific neural bases for sensory amplification are still debated. In this review, we want to deal with what we regard as confusion on two topics that are crucial to our understanding of multisensory integration mechanisms in auditory cortex: (1) Anatomical Underpinnings (e.g., what circuits underlie multisensory convergence), and (2) Temporal Dynamics (e.g., what time windows of integration are physiologically feasible). The combined evidence on multisensory structure and function in auditory cortex advances the emerging view of the relationship between perception and low level multisensory integration. In fact, it seems that the question is no longer whether low level, putatively unisensory cortex is accessible to multisensory influences, but how.

Neuronal mechanisms, response dynamics and perceptual functions of multisensory interactions in auditory cortex.

Although we have convincing evidence that attention to auditory stimuli modulates neuronal responses at or before the level of primary auditory cortex (A1), the underlying physiological mechanisms are unknown. We found that attending to rhythmic auditory streams resulted in the entrainment of ongoing oscillatory activity reflecting rhythmic excitability fluctuations in A1. Strikingly, although the rhythm of the entrained oscillations in A1 neuronal ensembles reflected the temporal structure of the attended stream, the phase depended on the attended frequency content. Counter-phase entrainment across differently tuned A1 regions resulted in both the amplification and sharpening of responses at attended time points, in essence acting as a spectrotemporal filter mechanism. Our data suggest that selective attention generates a dynamically evolving model of attended auditory stimulus streams in the form of modulatory subthreshold oscillations across tonotopically organized neuronal ensembles in A1 that enhances the representation of attended stimuli.

The spectrotemporal filter mechanism of auditory selective attention.

Studies over several decades have identified many of the neuronal substrates of music perception by pursuing pitch and rhythm perception separately. Here, we address the question of how these mechanisms interact, starting with the observation that the peripheral pathways of the so-called "Core" and "Matrix" thalamocortical system provide the anatomical bases for tone and rhythm channels. We then examine the hypothesis that these specialized inputs integrate acoustic content within rhythm context in auditory cortex using classical types of "driving" and "modulatory" mechanisms. This hypothesis provides a framework for deriving testable predictions about the early stages of music processing. Furthermore, because thalamocortical circuits are shared by speech and music processing, such a model provides concrete implications for how music experience contributes to the development of robust speech encoding mechanisms.

Thalamocortical mechanisms for integrating musical tone and rhythm.

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.

Gabriella Musacchia

Center for Molecular & Behavioral Neuroscience

Rutgers University, State University of New Jersey, Newark

Infant Auditory Processing and Event-related Brain Oscillations

Gabriella Musacchia

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Rutgers University, State University of New Jersey, Newark

Infant Auditory Processing and Event-related Brain Oscillations

Center for Molecular & Behavioral Neuroscience