Neural stability: A reflection of automaticity in reading.

Automaticity, the ability to perform a task rapidly with minimal effort, plays a key role in reading fluency and is indexed by rapid automatized naming (RAN) and processing speed. Yet little is known about automaticity's neurophysiologic underpinnings. The more efficiently sound is encoded, the more automatic sound processing can be. In turn, this automaticity could free up cognitive resources such as attention and working memory to help build an integrative reading network. Therefore, we hypothesized that automaticity and reading fluency correlate with stable neural representation of sounds, given a larger body of literature suggesting the close relationship between neural stability and the integrative function in the central auditory system. To test this hypothesis, we recorded the frequency-following responses (FFR) to speech syllables and administered cognitive and reading measures to school-aged children. We show that the stability of neural responses to speech correlates with RAN and processing speed, but not phonological awareness. Moreover, the link between neural stability and RAN mediates the previously-determined link between neural stability and reading ability. Children with a RAN deficit have especially unstable neural responses. Our neurophysiological approach illuminates a potential neural mechanism specific to RAN, which in turn indicates a relationship between synchronous neural firing in the auditory system and automaticity critical for reading fluency.

Signaling of noncomprehension in communication breakdowns in fragile X syndrome, Down syndrome, and autism spectrum disorder.

The ability to indicate a failure to understand a message is a critical pragmatic (social) language skill for managing communication breakdowns and supporting successful communicative exchanges. The current study examined the ability to signal noncomprehension across different types of confusing message conditions in children and adolescents with fragile X syndrome (FXS), Down syndrome (DS), autism spectrum disorder (ASD), and typical development (TD). Controlling for nonverbal mental age and receptive vocabulary skills, youth with comorbid FXS and ASD and those with DS were less likely than TD controls to signal noncomprehension of confusing messages. Youth with FXS without ASD and those with idiopathic ASD did not differ from controls. No sex differences were detected in any group. Findings contribute to current knowledge of pragmatic profiles in different forms of genetically-based neurodevelopmental disorders associated with intellectual disability, and the role of sex in the expression of such profiles. LEARNING OUTCOMES: Upon completion of this article, readers will have learned about: (1) the social-communicative profiles of youth with FXS, DS, and ASD, (2) the importance of signaling noncomprehension in response to a confusing message, and (3) the similarities and differences in noncomprehension signaling in youth with FXS (with and without ASD), DS, idiopathic ASD, and TD.

Auditory learning through active engagement with sound: biological impact of community music lessons in at-risk children.

The young nervous system is primed for sensory learning, facilitating the acquisition of language and communication skills. Social and linguistic impoverishment can limit these learning opportunities, eventually leading to language-related challenges such as poor reading. Music training offers a promising auditory learning strategy by directing attention to meaningful acoustic elements of the soundscape. In light of evidence that music training improves auditory skills and their neural substrates, there are increasing efforts to enact community-based programs to provide music instruction to at-risk children. Harmony Project is a community foundation that has provided free music instruction to over 1000 children from Los Angeles gang-reduction zones over the past decade. We conducted an independent evaluation of biological effects of participating in Harmony Project by following a cohort of children for 1 year. Here we focus on a comparison between students who actively engaged with sound through instrumental music training vs. students who took music appreciation classes. All children began with an introductory music appreciation class, but midway through the year half of the children transitioned to the instrumental training. After the year of training, the children who actively engaged with sound through instrumental music training had faster and more robust neural processing of speech than the children who stayed in the music appreciation class, observed in neural responses to a speech sound /d/. The neurophysiological measures found to be enhanced in the instrumentally-trained children have been previously linked to reading ability, suggesting a gain in neural processes important for literacy stemming from active auditory learning. Despite intrinsic constraints on our study imposed by a community setting, these findings speak to the potential of active engagement with sound (i.e., music-making) to engender experience-dependent neuroplasticity and may inform the development of strategies for auditory learning.

Music enrichment programs improve the neural encoding of speech in at-risk children.

Musicians are often reported to have enhanced neurophysiological functions, especially in the auditory system. Musical training is thought to improve nervous system function by focusing attention on meaningful acoustic cues, and these improvements in auditory processing cascade to language and cognitive skills. Correlational studies have reported musician enhancements in a variety of populations across the life span. In light of these reports, educators are considering the potential for co-curricular music programs to provide auditory-cognitive enrichment to children during critical developmental years. To date, however, no studies have evaluated biological changes following participation in existing, successful music education programs. We used a randomized control design to investigate whether community music participation induces a tangible change in auditory processing. The community music training was a longstanding and successful program that provides free music instruction to children from underserved backgrounds who stand at high risk for learning and social problems. Children who completed 2 years of music training had a stronger neurophysiological distinction of stop consonants, a neural mechanism linked to reading and language skills. One year of training was insufficient to elicit changes in nervous system function; beyond 1 year, however, greater amounts of instrumental music training were associated with larger gains in neural processing. We therefore provide the first direct evidence that community music programs enhance the neural processing of speech in at-risk children, suggesting that active and repeated engagement with sound changes neural function.

Engagement in community music classes sparks neuroplasticity and language development in children from disadvantaged backgrounds.

Children from disadvantaged backgrounds often face impoverished auditory environments, such as greater exposure to ambient noise and fewer opportunities to participate in complex language interactions during development. These circumstances increase their risk for academic failure and dropout. Given the academic and neural benefits associated with musicianship, music training may be one method for providing auditory enrichment to children from disadvantaged backgrounds. We followed a group of primary-school students from gang reduction zones in Los Angeles, CA, USA for 2 years as they participated in Harmony Project. By providing free community music instruction for disadvantaged children, Harmony Project promotes the healthy development of children as learners, the development of children as ambassadors of peace and understanding, and the development of stronger communities. Children who were more engaged in the music program-as defined by better attendance and classroom participation-developed stronger brain encoding of speech after 2 years than their less-engaged peers in the program. Additionally, children who were more engaged in the program showed increases in reading scores, while those less engaged did not show improvements. The neural gains accompanying music engagement were seen in the very measures of neural speech processing that are weaker in children from disadvantaged backgrounds. Our results suggest that community music programs such as Harmony Project provide a form of auditory enrichment that counteracts some of the biological adversities of growing up in poverty, and can further support community-based interventions aimed at improving child health and wellness.

Unstable representation of sound: a biological marker of dyslexia.

Learning to read proceeds smoothly for most children, yet others struggle to translate verbal language into its written form. Poor readers often have a host of auditory, linguistic, and attention deficits, including abnormal neural representation of speech and inconsistent performance on psychoacoustic tasks. We hypothesize that this constellation of deficits associated with reading disorders arises from the human auditory system failing to respond to sound in a consistent manner, and that this inconsistency impinges upon the ability to relate phonology and orthography during reading. In support of this hypothesis, we show that poor readers have significantly more variable auditory brainstem responses to speech than do good readers, independent of resting neurophysiological noise levels. Thus, neural variability may be an underlying biological contributor to well established behavioral and neural deficits found in poor readers.

Speech-evoked auditory brainstem responses reflect familial and cognitive influences.

Cortical function and related cognitive, language, and communication skills are genetically influenced. The auditory brainstem response to speech is linked to language skill, reading ability, cognitive skills, and speech-in-noise perception; however, the impact of shared genetic and environmental factors on the response has not been investigated. We assessed auditory brainstem responses to speech presented in quiet and background noise from (1) 23 pairs of same sex, same learning diagnosis siblings (Siblings), (2) 23 unrelated children matched on age, sex, IQ, and reading ability to one of the siblings (Reading-Matched), and (3) 22 pairs of unrelated children matched on age and sex but not on reading ability to the same sibling (Age/Sex-Matched). By quantifying response similarity as the intersubject response-to-response correlation for sibling pairs, reading-matched pairs, and age- and sex-matched pairs, we found that siblings had more similar responses than age- and sex-matched pairs and reading-matched pairs. Similarity of responses between siblings was as high as the similarity of responses collected from an individual over the course of the recording session. Responses from unrelated children matched on reading were more similar than responses from unrelated children matched only on age and sex, supporting previous data linking variations in auditory brainstem activity with variations in reading ability. These results suggest that auditory brainstem function can be influenced by siblingship and auditory-based communication skills such as reading, motivating the use of speech-evoked auditory brainstem responses for assessing risk of reading and communication impairments in family members.

Assistive listening devices drive neuroplasticity in children with dyslexia.

Children with dyslexia often exhibit increased variability in sensory and cognitive aspects of hearing relative to typically developing peers. Assistive listening devices (classroom FM systems) may reduce auditory processing variability by enhancing acoustic clarity and attention. We assessed the impact of classroom FM system use for 1 year on auditory neurophysiology and reading skills in children with dyslexia. FM system use reduced the variability of subcortical responses to sound, and this improvement was linked to concomitant increases in reading and phonological awareness. Moreover, response consistency before FM system use predicted gains in phonological awareness. A matched control group of children with dyslexia attending the same schools who did not use the FM system did not show these effects. Assistive listening devices can improve the neural representation of speech and impact reading-related skills by enhancing acoustic clarity and attention, reducing variability in auditory processing.

Subcortical representation of speech fine structure relates to reading ability.

Impaired perception of consonants by poor readers is reflected in poor subcortical encoding of speech timing and harmonics. We assessed auditory brainstem representation of higher harmonics within a consonant-vowel formant transition to identify relationships between speech fine structure and reading. Responses were analyzed in three ways: a single stimulus polarity, adding responses to inverted polarities (emphasizing low harmonics), and subtracting responses to inverted polarities (emphasizing high harmonics). Poor readers had a reduced representation of higher speech harmonics for subtracted polarities and a single polarity. No group differences were found for the fundamental frequency. These findings strengthen the evidence of subcortical encoding deficits in poor readers for speech fine structure and delineate effective strategies for capturing these neural impairments in humans.

Test-retest consistency of speech-evoked auditory brainstem responses in typically-developing children.

The click-evoked auditory brainstem response (ABR) is widely used in clinical settings, partly due to its predictability and high test-retest consistency. More recently, the speech-evoked ABR has been used to evaluate subcortical processing of complex signals, allowing for the objective assessment of biological processes underlying auditory function and auditory processing deficits not revealed by responses to clicks. Test-retest reliability of some components of speech-evoked ABRs has been shown for adults and children over the course of months. However, a systematic study of the consistency of the speech-evoked brainstem response in school-age children has not been conducted. In the present study, speech-evoked ABRs were collected from 26 typically-developing children (ages 8-13) at two time points separated by one year. ABRs were collected for /da/ presented in quiet and in a 6-talker babble background noise. Test-retest consistency of response timing, spectral encoding, and signal-to-noise ratio was assessed. Response timing and spectral encoding were highly replicable over the course of one year. The consistency of response timing and spectral encoding found for the speech-evoked ABRs of typically-developing children suggests that the speech-evoked ABR may be a unique tool for research and clinical assessment of auditory function, particularly with respect to auditory-based communication skills.

Subcortical processing of speech regularities underlies reading and music aptitude in children.

BACKGROUND: Neural sensitivity to acoustic regularities supports fundamental human behaviors such as hearing in noise and reading. Although the failure to encode acoustic regularities in ongoing speech has been associated with language and literacy deficits, how auditory expertise, such as the expertise that is associated with musical skill, relates to the brainstem processing of speech regularities is unknown. An association between musical skill and neural sensitivity to acoustic regularities would not be surprising given the importance of repetition and regularity in music. Here, we aimed to define relationships between the subcortical processing of speech regularities, music aptitude, and reading abilities in children with and without reading impairment. We hypothesized that, in combination with auditory cognitive abilities, neural sensitivity to regularities in ongoing speech provides a common biological mechanism underlying the development of music and reading abilities. METHODS: We assessed auditory working memory and attention, music aptitude, reading ability, and neural sensitivity to acoustic regularities in 42 school-aged children with a wide range of reading ability. Neural sensitivity to acoustic regularities was assessed by recording brainstem responses to the same speech sound presented in predictable and variable speech streams. RESULTS: Through correlation analyses and structural equation modeling, we reveal that music aptitude and literacy both relate to the extent of subcortical adaptation to regularities in ongoing speech as well as with auditory working memory and attention. Relationships between music and speech processing are specifically driven by performance on a musical rhythm task, underscoring the importance of rhythmic regularity for both language and music. CONCLUSIONS: These data indicate common brain mechanisms underlying reading and music abilities that relate to how the nervous system responds to regularities in auditory input. Definition of common biological underpinnings for music and reading supports the usefulness of music for promoting child literacy, with the potential to improve reading remediation.

Auditory brainstem measures predict reading and speech-in-noise perception in school-aged children.

Reading and speech-in-noise perception, fundamental aspects of human communication, have been linked to neural indices of auditory brainstem function. However, how these factors interact is currently unclear. Multivariate analysis methods (structural equation modeling) were employed to delineate and quantify the relationships among factors that relate to successful reading and speech in noise perception in children. Neural measures of subcortical speech encoding that reflect the utilization of stimulus regularities, differentiation of stop consonants, and robustness of neural synchrony predicted 73% of the variance in reading scores. A different combination of neural measures, specifically, utilization of stimulus regularities, strength of encoding of lower harmonics, and the extent of noise-induced timing delays uniquely predicted 56% of the variance in speech-in-noise perception measures. The neural measures relating to reading and speech-in-noise perception were substantially non-overlapping and resulted in poor fitting models when substituted for each other, thereby suggesting distinct neural signatures for the two skills. When phonological processing and working memory measures were added to the models, brainstem measures still uniquely predicted variance in reading ability and speech-in-noise perception, highlighting the robustness of the relationship between subcortical auditory function and these skills. The current study suggests that objective neural markers may prove valuable in the assessment of reading or speech-in-noise abilities in children.

Biological changes in auditory function following training in children with autism spectrum disorders.

BACKGROUND: Children with pervasive developmental disorders (PDD), such as children with autism spectrum disorders (ASD), often show auditory processing deficits related to their overarching language impairment. Auditory training programs such as Fast ForWord Language may potentially alleviate these deficits through training-induced improvements in auditory processing. METHODS: To assess the impact of auditory training on auditory function in children with ASD, brainstem and cortical responses to speech sounds presented in quiet and noise were collected from five children with ASD who completed Fast ForWord training. RESULTS: Relative to six control children with ASD who did not complete Fast ForWord, training-related changes were found in brainstem response timing (three children) and pitch-tracking (one child), and cortical response timing (all five children) after Fast ForWord use. CONCLUSIONS: These results provide an objective indication of the benefit of training on auditory function for some children with ASD.

Context-dependent encoding in the human auditory brainstem relates to hearing speech in noise: implications for developmental dyslexia.

We examined context-dependent encoding of speech in children with and without developmental dyslexia by measuring auditory brainstem responses to a speech syllable presented in a repetitive or variable context. Typically developing children showed enhanced brainstem representation of features related to voice pitch in the repetitive context, relative to the variable context. In contrast, children with developmental dyslexia exhibited impairment in their ability to modify representation in predictable contexts. From a functional perspective, we found that the extent of context-dependent encoding in the auditory brainstem correlated positively with behavioral indices of speech perception in noise. The ability to sharpen representation of repeating elements is crucial to speech perception in noise, since it allows superior "tagging" of voice pitch, an important cue for segregating sound streams in background noise. The disruption of this mechanism contributes to a critical deficit in noise-exclusion, a hallmark symptom in developmental dyslexia.

Subcortical differentiation of stop consonants relates to reading and speech-in-noise perception.

Children with reading impairments have deficits in phonological awareness, phonemic categorization, speech-in-noise perception, and psychophysical tasks such as frequency and temporal discrimination. Many of these children also exhibit abnormal encoding of speech stimuli in the auditory brainstem, even though responses to click stimuli are normal. In typically developing children the auditory brainstem response reflects acoustic differences between contrastive stop consonants. The current study investigated whether this subcortical differentiation of stop consonants was related to reading ability and speech-in-noise performance. Across a group of children with a wide range of reading ability, the subcortical differentiation of 3 speech stimuli ([ba], [da], [ga]) was found to be correlated with phonological awareness, reading, and speech-in-noise perception, with better performers exhibiting greater differences among responses to the 3 syllables. When subjects were categorized into terciles based on phonological awareness and speech-in-noise performance, the top-performing third in each grouping had greater subcortical differentiation than the bottom third. These results are consistent with the view that the neural processes underlying phonological awareness and speech-in-noise perception depend on reciprocal interactions between cognitive and perceptual processes.

Reading and subcortical auditory function.

Although it is largely agreed that phonological processing deficits are a major cause of poor reading, the neural origins of phonological processing are not well understood. We now show, for the first time, that phonological decoding, measured with a test of single-nonword reading, is significantly correlated with the timing of subcortical auditory processing and also, to a lesser extent, with the robustness of subcortical representation of the harmonic content of speech, but not with pitch encoding. The relationships we observe between reading and subcortical processing fall along a continuum, with poor readers at one end and good readers at the other. These data suggest that reading skill may depend on the integrity of subcortical auditory mechanisms and are consistent with the idea that subcortical representation of the acoustic features of speech may play a role in normal reading as well as in the development of reading disorders. These data establish a significant link between subcortical auditory function and reading, thereby contributing to the understanding of the biological bases of reading. At a more general level, these findings are among the first to establish a direct relationship between subcortical sensory function and a specific cognitive skill (reading). We argue that this relationship between cortical and subcortical function could be shaped during development by the corticofugal pathway and that this cortical-subcortical link could contribute to the phonological processing deficits experienced by poor readers.

Subcortical laterality of speech encoding.

It is well established that in the majority of the population language processing is lateralized to the left hemisphere. Evidence suggests that lateralization is also present in the brainstem. In the current study, the syllable /da/ was presented monaurally to the right and left ears and electrophysiological responses from the brainstem were recorded in adults with symmetrical interaural click-evoked responses. Responses to the right-ear presentation occurred earlier than those to left-ear presentation in two peaks of the frequency following response (FFR) and approached significance for the third peak of the FFR and the offset peak. Interestingly, there were no differences in interpeak latencies indicating the response to right-ear presentation simply occurred earlier over this region. Analyses also showed more robust frequency encoding when stimuli were presented to the right ear than the left ear. The effect was found for the harmonics of the fundamental that correspond to the first formant of the stimulus, but was not seen in the fundamental frequency range. The results suggest that left lateralization of processing acoustic elements important for discriminating speech extends to the auditory brainstem and that these effects are speech specific.

Neural correlates of orthographic and phonological consistency effects in children.

The objective of this study was to examine the neural correlates of phonological inconsistency (relationship of spelling to sound) and orthographic inconsistency (relationship of sound to spelling) in visual word processing using functional magnetic resonance imaging (fMRI). Children (9- to 15-year-old) performed a rhyming and spelling task in which two words were presented sequentially in the visual modality. Consistent with previous studies in adults, higher phonological inconsistency was associated with greater activation in several regions including left inferior frontal gyrus and medial frontal gyrus/anterior cingulate cortex. We additionally demonstrated an effect of orthographic inconsistency in these same areas, suggesting that these regions are involved in the integration of orthographic and phonological information and, with respect to the medial frontal/anterior cingulate, greater demands on executive function. Higher phonological and orthographic consistency was associated with greater activation in precuneus/posterior cingulate cortex, the putative steady state system active during resting, suggesting lower demands on cognitive resources for consistent items. Both consistency effects were larger for the rhyming compared with the spelling task suggesting greater demands of integrating spelling and sound in the former task. Finally, accuracy on the rhyming task was negatively correlated with the consistency effect in left fusiform gyrus. In particular, this region showed insensitivity to consistency in low performers, sensitivity to inconsistency (higher activity) in moderate performers, and sensitivity to inconsistency (high activation) and to consistency (deactivation). In general, these results show that the influence of spelling-sound (and sound-spelling) correspondences on processing in fusiform gyrus develops as a function of skill.