Attentional modulation of neural sound tracking in children with and without dyslexia.

Auditory selective attention forms an important foundation of children's learning by enabling the prioritisation and encoding of relevant stimuli. It may also influence reading development, which relies on metalinguistic skills including the awareness of the sound structure of spoken language. Reports of attentional impairments and speech perception difficulties in noisy environments in dyslexic readers are also suggestive of the putative contribution of auditory attention to reading development. To date, it is unclear whether non-speech selective attention and its underlying neural mechanisms are impaired in children with dyslexia and to which extent these deficits relate to individual reading and speech perception abilities in suboptimal listening conditions. In this EEG study, we assessed non-speech sustained auditory selective attention in 106 7-to-12-year-old children with and without dyslexia. Children attended to one of two tone streams, detecting occasional sequence repeats in the attended stream, and performed a speech-in-speech perception task. Results show that when children directed their attention to one stream, inter-trial-phase-coherence at the attended rate increased in fronto-central sites; this, in turn, was associated with better target detection. Behavioural and neural indices of attention did not systematically differ as a function of dyslexia diagnosis. However, behavioural indices of attention did explain individual differences in reading fluency and speech-in-speech perception abilities: both these skills were impaired in dyslexic readers. Taken together, our results show that children with dyslexia do not show group-level auditory attention deficits but these deficits may represent a risk for developing reading impairments and problems with speech perception in complex acoustic environments. RESEARCH HIGHLIGHTS: Non-speech sustained auditory selective attention modulates EEG phase coherence in children with/without dyslexia Children with dyslexia show difficulties in speech-in-speech perception Attention relates to dyslexic readers' speech-in-speech perception and reading skills Dyslexia diagnosis is not linked to behavioural/EEG indices of auditory attention.

Slow phase-locked modulations support selective attention to sound.

To make sense of complex soundscapes, listeners must select and attend to task-relevant streams while ignoring uninformative sounds. One possible neural mechanism underlying this process is alignment of endogenous oscillations with the temporal structure of the target sound stream. Such a mechanism has been suggested to mediate attentional modulation of neural phase-locking to the rhythms of attended sounds. However, such modulations are compatible with an alternate framework, where attention acts as a filter that enhances exogenously-driven neural auditory responses. Here we attempted to test several predictions arising from the oscillatory account by playing two tone streams varying across conditions in tone duration and presentation rate; participants attended to one stream or listened passively. Attentional modulation of the evoked waveform was roughly sinusoidal and scaled with rate, while the passive response did not. However, there was only limited evidence for continuation of modulations through the silence between sequences. These results suggest that attentionally-driven changes in phase alignment reflect synchronization of slow endogenous activity with the temporal structure of attended stimuli.

Dimension-selective attention and dimensional salience modulate cortical tracking of acoustic dimensions.

Some theories of auditory categorization suggest that auditory dimensions that are strongly diagnostic for particular categories - for instance voice onset time or fundamental frequency in the case of some spoken consonants - attract attention. However, prior cognitive neuroscience research on auditory selective attention has largely focused on attention to simple auditory objects or streams, and so little is known about the neural mechanisms that underpin dimension-selective attention, or how the relative salience of variations along these dimensions might modulate neural signatures of attention. Here we investigate whether dimensional salience and dimension-selective attention modulate the cortical tracking of acoustic dimensions. In two experiments, participants listened to tone sequences varying in pitch and spectral peak frequency; these two dimensions changed at different rates. Inter-trial phase coherence (ITPC) and amplitude of the EEG signal at the frequencies tagged to pitch and spectral changes provided a measure of cortical tracking of these dimensions. In Experiment 1, tone sequences varied in the size of the pitch intervals, while the size of spectral peak intervals remained constant. Cortical tracking of pitch changes was greater for sequences with larger compared to smaller pitch intervals, with no difference in cortical tracking of spectral peak changes. In Experiment 2, participants selectively attended to either pitch or spectral peak. Cortical tracking was stronger in response to the attended compared to unattended dimension for both pitch and spectral peak. These findings suggest that attention can enhance the cortical tracking of specific acoustic dimensions rather than simply enhancing tracking of the auditory object as a whole.

Attentional modulation of neural entrainment to sound streams in children with and without ADHD.

To extract meaningful information from complex auditory scenes like a noisy playground, rock concert, or classroom, children can direct attention to different sound streams. One means of accomplishing this might be to align neural activity with the temporal structure of a target stream, such as a specific talker or melody. However, this may be more difficult for children with ADHD, who can struggle with accurately perceiving and producing temporal intervals. In this EEG study, we found that school-aged children's attention to one of two temporally-interleaved isochronous tone 'melodies' was linked to an increase in phase-locking at the melody's rate, and a shift in neural phase that aligned the neural responses with the attended tone stream. Children's attention task performance and neural phase alignment with the attended melody were linked to performance on temporal production tasks, suggesting that children with more robust control over motor timing were better able to direct attention to the time points associated with the target melody. Finally, we found that although children with ADHD performed less accurately on the tonal attention task than typically developing children, they showed the same degree of attentional modulation of phase locking and neural phase shifts, suggesting that children with ADHD may have difficulty with attentional engagement rather than attentional selection.

Reading ability in children relates to rhythm perception across modalities.

The onset of reading ability is rife with individual differences, with some children termed "early readers" and some falling behind from the very beginning. Reading skill in children has been linked to an ability to remember nonverbal rhythms, specifically in the auditory modality. It has been hypothesized that the link between rhythm skills and reading reflects a shared reliance on the ability to extract temporal structure from sound. Here we tested this hypothesis by investigating whether the link between rhythm memory and reading depends on the modality in which rhythms are presented. We tested 75 primary school-aged children aged 7-11 years on a within-participants battery of reading and rhythm tasks. Participants received a reading efficiency task followed by three rhythm tasks (auditory, visual, and audiovisual). Results showed that children who performed poorly on the reading task also performed poorly on the tasks that required them to remember and repeat back nonverbal rhythms. In addition, these children showed a rhythmic deficit not just in the auditory domain but also in the visual domain. However, auditory rhythm memory explained additional variance in reading ability even after controlling for visual memory. These results suggest that reading ability and rhythm memory rely both on shared modality-general cognitive processes and on the ability to perceive the temporal structure of sound.

Effects of auditory selective attention on neural phase: individual differences and short-term training.

How does the brain follow a sound that is mixed with others in a noisy environment? One possible strategy is to allocate attention to task-relevant time intervals. Prior work has linked auditory selective attention to alignment of neural modulations with stimulus temporal structure. However, since this prior research used relatively easy tasks and focused on analysis of main effects of attention across participants, relatively little is known about the neural foundations of individual differences in auditory selective attention. Here we investigated individual differences in auditory selective attention by asking participants to perform a 1-back task on a target auditory stream while ignoring a distractor auditory stream presented 180° out of phase. Neural entrainment to the attended auditory stream was strongly linked to individual differences in task performance. Some variability in performance was accounted for by degree of musical training, suggesting a link between long-term auditory experience and auditory selective attention. To investigate whether short-term improvements in auditory selective attention are possible, we gave participants 2 â€‹h of auditory selective attention training and found improvements in both task performance and enhancements of the effects of attention on neural phase angle. Our results suggest that although there exist large individual differences in auditory selective attention and attentional modulation of neural phase angle, this skill improves after a small amount of targeted training.

Got Rhythm? Better Inhibitory Control Is Linked with More Consistent Drumming and Enhanced Neural Tracking of the Musical Beat in Adult Percussionists and Nonpercussionists.

Musical rhythm engages motor and reward circuitry that is important for cognitive control, and there is evidence for enhanced inhibitory control in musicians. We recently revealed an inhibitory control advantage in percussionists compared with vocalists, highlighting the potential importance of rhythmic expertise in mediating this advantage. Previous research has shown that better inhibitory control is associated with less variable performance in simple sensorimotor synchronization tasks; however, this relationship has not been examined through the lens of rhythmic expertise. We hypothesize that the development of rhythm skills strengthens inhibitory control in two ways: by fine-tuning motor networks through the precise coordination of movements "in time" and by activating reward-based mechanisms, such as predictive processing and conflict monitoring, which are involved in tracking temporal structure in music. Here, we assess adult percussionists and nonpercussionists on inhibitory control, selective attention, basic drumming skills (self-paced, paced, and continuation drumming), and cortical evoked responses to an auditory stimulus presented on versus off the beat of music. Consistent with our hypotheses, we find that better inhibitory control is correlated with more consistent drumming and enhanced neural tracking of the musical beat. Drumming variability and the neural index of beat alignment each contribute unique predictive power to a regression model, explaining 57% of variance in inhibitory control. These outcomes present the first evidence that enhanced inhibitory control in musicians may be mediated by rhythmic expertise and provide a foundation for future research investigating the potential for rhythm-based training to strengthen cognitive function.

Music training alters the course of adolescent auditory development.

Fundamental changes in brain structure and function during adolescence are well-characterized, but the extent to which experience modulates adolescent neurodevelopment is not. Musical experience provides an ideal case for examining this question because the influence of music training begun early in life is well-known. We investigated the effects of in-school music training, previously shown to enhance auditory skills, versus another in-school training program that did not focus on development of auditory skills (active control). We tested adolescents on neural responses to sound and language skills before they entered high school (pretraining) and again 3 y later. Here, we show that in-school music training begun in high school prolongs the stability of subcortical sound processing and accelerates maturation of cortical auditory responses. Although phonological processing improved in both the music training and active control groups, the enhancement was greater in adolescents who underwent music training. Thus, music training initiated as late as adolescence can enhance neural processing of sound and confer benefits for language skills. These results establish the potential for experience-driven brain plasticity during adolescence and demonstrate that in-school programs can engender these changes.

Individual Differences in Rhythm Skills: Links with Neural Consistency and Linguistic Ability.

Durational patterns provide cues to linguistic structure, thus so variations in rhythm skills may have consequences for language development. Understanding individual differences in rhythm skills, therefore, could help explain variability in language abilities across the population. We investigated the neural foundations of rhythmic proficiency and its relation to language skills in young adults. We hypothesized that rhythmic abilities can be characterized by at least two constructs, which are tied to independent language abilities and neural profiles. Specifically, we hypothesized that rhythm skills that require integration of information across time rely upon the consistency of slow, low-frequency auditory processing, which we measured using the evoked cortical response. On the other hand, we hypothesized that rhythm skills that require fine temporal precision rely upon the consistency of fast, higher-frequency auditory processing, which we measured using the frequency-following response. Performance on rhythm tests aligned with two constructs: rhythm sequencing and synchronization. Rhythm sequencing and synchronization were linked to the consistency of slow cortical and fast frequency-following responses, respectively. Furthermore, whereas rhythm sequencing ability was linked to verbal memory and reading, synchronization ability was linked only to nonverbal auditory temporal processing. Thus, rhythm perception at different time scales reflects distinct abilities, which rely on distinct auditory neural resources. In young adults, slow rhythmic processing makes the more extensive contribution to language skills.

Beat synchronization predicts neural speech encoding and reading readiness in preschoolers.

Temporal cues are important for discerning word boundaries and syllable segments in speech; their perception facilitates language acquisition and development. Beat synchronization and neural encoding of speech reflect precision in processing temporal cues and have been linked to reading skills. In poor readers, diminished neural precision may contribute to rhythmic and phonological deficits. Here we establish links between beat synchronization and speech processing in children who have not yet begun to read: preschoolers who can entrain to an external beat have more faithful neural encoding of temporal modulations in speech and score higher on tests of early language skills. In summary, we propose precise neural encoding of temporal modulations as a key mechanism underlying reading acquisition. Because beat synchronization abilities emerge at an early age, these findings may inform strategies for early detection of and intervention for language-based learning disabilities.

Getting back on the beat: links between auditory-motor integration and precise auditory processing at fast time scales.

The auditory system is unique in its ability to precisely detect the timing of perceptual events and use this information to update motor plans, a skill that is crucial for language. However, the characteristics of the auditory system that enable this temporal precision are only beginning to be understood. Previous work has shown that participants who can tap consistently to a metronome have neural responses to sound with greater phase coherence from trial to trial. We hypothesized that this relationship is driven by a link between the updating of motor output by auditory feedback and neural precision. Moreover, we hypothesized that neural phase coherence at both fast time scales (reflecting subcortical processing) and slow time scales (reflecting cortical processing) would be linked to auditory-motor timing integration. To test these hypotheses, we asked participants to synchronize to a pacing stimulus, and then changed either the tempo or the timing of the stimulus to assess whether they could rapidly adapt. Participants who could rapidly and accurately resume synchronization had neural responses to sound with greater phase coherence. However, this precise timing was limited to the time scale of 10 ms (100 Hz) or faster; neural phase coherence at slower time scales was unrelated to performance on this task. Auditory-motor adaptation therefore specifically depends upon consistent auditory processing at fast, but not slow, time scales.

Neural entrainment to the rhythmic structure of music.

The neural resonance theory of musical meter explains musical beat tracking as the result of entrainment of neural oscillations to the beat frequency and its higher harmonics. This theory has gained empirical support from experiments using simple, abstract stimuli. However, to date there has been no empirical evidence for a role of neural entrainment in the perception of the beat of ecologically valid music. Here we presented participants with a single pop song with a superimposed bassoon sound. This stimulus was either lined up with the beat of the music or shifted away from the beat by 25% of the average interbeat interval. Both conditions elicited a neural response at the beat frequency. However, although the on-the-beat condition elicited a clear response at the first harmonic of the beat, this frequency was absent in the neural response to the off-the-beat condition. These results support a role for neural entrainment in tracking the metrical structure of real music and show that neural meter tracking can be disrupted by the presentation of contradictory rhythmic cues.

The ability to move to a beat is linked to the consistency of neural responses to sound.

The ability to synchronize movement to a steady beat is a fundamental skill underlying musical performance and has been studied for decades as a model of sensorimotor synchronization. Nevertheless, little is known about the neural correlates of individual differences in the ability to synchronize to a beat. In particular, links between auditory-motor synchronization ability and characteristics of the brain's response to sound have not yet been explored. Given direct connections between the inferior colliculus (IC) and subcortical motor structures, we hypothesized that consistency of the neural response to sound within the IC is linked to the ability to tap consistently to a beat. Here, we show that adolescent humans who demonstrate less variability when tapping to a beat have auditory brainstem responses that are less variable as well. One of the sources of this enhanced consistency in subjects who can steadily tap to a beat may be decreased variability in the timing of the response, as these subjects also show greater between-trial phase-locking in the auditory brainstem response. Thus, musical training with a heavy emphasis on synchronization of movement to musical beats may improve auditory neural synchrony, potentially benefiting children with auditory-based language impairments characterized by excessively variable neural responses.

Resting gamma power is linked to reading ability in adolescents.

Infants who have more power within the gamma frequency range at rest develop better language and cognitive abilities over their first 3 years of life (Benasich et al., 2008). This positive trend may reflect the gradual increase in resting gamma power that peaks at about 4 years (Takano & Ogawa, 1998): infants further along the maturational curve may exhibit both increased resting gamma power and more advanced language and cognitive function. Similar to other neural characteristics such as synaptic density, resting gamma power subsequently decreases with further development into adulthood (Tierney, Strait, O'Connell & Kraus, 2013). If previously reported relationships between resting gamma power and behavioral performance reflect variance in maturation, at least in part, negative correlations between resting gamma and behavior may predominate in later developmental stages, during which resting gamma activity is decreasing. We tested this prediction by examining resting gamma activity and language-dependent behavioral performance, reflected by a variety of reading-related tests, in adolescents between the ages of 14 and 15 years. Consistent with our predictions, resting gamma power inversely related to every aspect of reading assessed (i.e. reading fluency, rapid naming, and basic reading proficiency). Our results suggest that resting gamma power acts as an index of maturational progress in adolescents.

Speech versus song: multiple pitch-sensitive areas revealed by a naturally occurring musical illusion.

It is normally obvious to listeners whether a human vocalization is intended to be heard as speech or song. However, the 2 signals are remarkably similar acoustically. A naturally occurring boundary case between speech and song has been discovered where a spoken phrase sounds as if it were sung when isolated and repeated. In the present study, an extensive search of audiobooks uncovered additional similar examples, which were contrasted with samples from the same corpus that do not sound like song, despite containing clear prosodic pitch contours. Using functional magnetic resonance imaging, we show that hearing these 2 closely matched stimuli is not associated with differences in response of early auditory areas. Rather, we find that a network of 8 regions, including the anterior superior temporal gyrus (STG) just anterior to Heschl's gyrus and the right midposterior STG, respond more strongly to speech perceived as song than to mere speech. This network overlaps a number of areas previously associated with pitch extraction and song production, confirming that phrases originally intended to be heard as speech can, under certain circumstances, be heard as song. Our results suggest that song processing compared with speech processing makes increased demands on pitch processing and auditory-motor integration.

The motor origins of human and avian song structure.

Human song exhibits great structural diversity, yet certain aspects of melodic shape (how pitch is patterned over time) are widespread. These include a predominance of arch-shaped and descending melodic contours in musical phrases, a tendency for phrase-final notes to be relatively long, and a bias toward small pitch movements between adjacent notes in a melody [Huron D (2006) Sweet Anticipation: Music and the Psychology of Expectation (MIT Press, Cambridge, MA)]. What is the origin of these features? We hypothesize that they stem from motor constraints on song production (i.e., the energetic efficiency of their underlying motor actions) rather than being innately specified. One prediction of this hypothesis is that any animals subject to similar motor constraints on song will exhibit similar melodic shapes, no matter how distantly related those animals are to humans. Conversely, animals who do not share similar motor constraints on song will not exhibit convergent melodic shapes. Birds provide an ideal case for testing these predictions, because their peripheral mechanisms of song production have both notable similarities and differences from human vocal mechanisms [Riede T, Goller F (2010) Brain Lang 115:69-80]. We use these similarities and differences to make specific predictions about shared and distinct features of human and avian song structure and find that these predictions are confirmed by empirical analysis of diverse human and avian song samples.

Voice actors show enhanced neural tracking of pitch, prosody perception, and music perception.

Experiences with sound that make strong demands on the precision of perception, such as musical training and experience speaking a tone language, can enhance auditory neural encoding. Are high demands on the precision of perception necessary for training to drive auditory neural plasticity? Voice actors are an ideal subject population for answering this question. Voice acting requires exaggerating prosodic cues to convey emotion, character, and linguistic structure, drawing upon attention to sound, memory for sound features, and accurate sound production, but not fine perceptual precision. Here we assessed neural encoding of pitch using the frequency-following response (FFR), as well as prosody, music, and sound perception, in voice actors and a matched group of non-actors. We find that the consistency of neural sound encoding, prosody perception, and musical phrase perception are all enhanced in voice actors, suggesting that a range of neural and behavioural auditory processing enhancements can result from training which lacks fine perceptual precision. However, fine discrimination was not enhanced in voice actors but was linked to degree of musical experience, suggesting that low-level auditory processing can only be enhanced by demanding perceptual training. These findings suggest that training which taxes attention, memory, and production but is not perceptually taxing may be a way to boost neural encoding of sound and auditory pattern detection in individuals with poor auditory skills.

Musical experience is linked to enhanced dimension-selective attention to pitch and increased primary weighting during suprasegmental categorization.

Speech perception requires the integration of evidence from acoustic cues across multiple dimensions. Individuals differ in their cue weighting strategies, that is, the weight they assign to different dimensions during speech categorization. In two experiments, we investigate musical training as one potential predictor of individual differences in prosodic cue weighting strategies. Attentional theories of speech categorization suggest that prior experience with the task-relevance of a particular dimension leads that dimension to attract attention. Experiment 1 tested whether musicians and nonmusicians differed in their ability to selectively attend to pitch and loudness in speech. Compared to nonmusicians, musicians showed enhanced dimension-selective attention to pitch but not loudness. Experiment 2 tested the hypothesis that musicians would show greater pitch weighting during prosodic categorization due to prior experience with the task-relevance of pitch cues in music. Listeners categorized phrases that varied in the extent to which pitch and duration signaled the location of linguistic focus and phrase boundaries. During linguistic focus categorization, musicians upweighted pitch compared to nonmusicians. During phrase boundary categorization, musicians upweighted duration relative to nonmusicians. These results suggest that musical experience is linked with domain-general enhancements in the ability to selectively attend to certain acoustic dimensions in speech. As a result, musicians may place greater perceptual weight on a single primary dimension during prosodic categorization, while nonmusicians may be more likely to choose a perceptual strategy that integrates across multiple dimensions. These findings support attentional theories of cue weighting, which suggest attention influences listeners' perceptual weighting of acoustic dimensions during categorization. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Salient sounds distort time perception and production.

The auditory world is often cacophonous, with some sounds capturing attention and distracting us from our goals. Despite the universality of this experience, many questions remain about how and why sound captures attention, how rapidly behavior is disrupted, and how long this interference lasts. Here, we use a novel measure of behavioral disruption to test predictions made by models of auditory salience. Models predict that goal-directed behavior is disrupted immediately after points in time that feature a high degree of spectrotemporal change. We find that behavioral disruption is precisely time-locked to the onset of distracting sound events: Participants who tap to a metronome temporarily increase their tapping speed 750 ms after the onset of distractors. Moreover, this response is greater for more salient sounds (larger amplitude) and sound changes (greater pitch shift). We find that the time course of behavioral disruption is highly similar after acoustically disparate sound events: Both sound onsets and pitch shifts of continuous background sounds speed responses at 750 ms, with these effects dying out by 1,750 ms. These temporal distortions can be observed using only data from the first trial across participants. A potential mechanism underlying these results is that arousal increases after distracting sound events, leading to an expansion of time perception, and causing participants to misjudge when their next movement should begin.

Weighting of cues to categorization of song versus speech in tone-language and non-tone-language speakers.

One of the most important auditory categorization tasks a listener faces is determining a sound's domain, a process which is a prerequisite for successful within-domain categorization tasks such as recognizing different speech sounds or musical tones. Speech and song are universal in human cultures: how do listeners categorize a sequence of words as belonging to one or the other of these domains? There is growing interest in the acoustic cues that distinguish speech and song, but it remains unclear whether there are cross-cultural differences in the evidence upon which listeners rely when making this fundamental perceptual categorization. Here we use the speech-to-song illusion, in which some spoken phrases perceptually transform into song when repeated, to investigate cues to this domain-level categorization in native speakers of tone languages (Mandarin and Cantonese speakers residing in the United Kingdom and China) and in native speakers of a non-tone language (English). We find that native tone-language and non-tone-language listeners largely agree on which spoken phrases sound like song after repetition, and we also find that the strength of this transformation is not significantly different across language backgrounds or countries of residence. Furthermore, we find a striking similarity in the cues upon which listeners rely when perceiving word sequences as singing versus speech, including small pitch intervals, flat within-syllable pitch contours, and steady beats. These findings support the view that there are certain widespread cross-cultural similarities in the mechanisms by which listeners judge if a word sequence is spoken or sung.