Precursors to infant sensorimotor synchronization to speech and non-speech rhythms: A longitudinal study.

Impaired sensorimotor synchronization (SMS) to acoustic rhythm may be a marker of atypical language development. Here, Motion Capture was used to assess gross motor rhythmic movement at six time points between 5- and 11 months of age. Infants were recorded drumming to acoustic stimuli of varying linguistic and temporal complexity: drumbeats, repeated syllables and nursery rhymes. Here we show, for the first time, developmental change in infants' movement timing in response to auditory stimuli over the first year of life. Longitudinal analyses revealed that whilst infants could not yet reliably synchronize their movement to auditory rhythms, infant spontaneous motor tempo became faster with age, and by 11 months, a subset of infants decelerate from their spontaneous motor tempo, which better accords with the incoming tempo. Further, infants became more regular drummers with age, with marked decreases in the variability of spontaneous motor tempo and variability in response to drumbeats. This latter effect was subdued in response to linguistic stimuli. The current work lays the foundation for using individual differences in precursors of SMS in infancy to predict later language outcomes. RESEARCH HIGHLIGHT: We present the first longitudinal investigation of infant rhythmic movement over the first year of life Whilst infants generally move more quickly and with higher regularity over their first year, by 11 months infants begin to counter this pattern when hearing slower infant-directed song Infant movement is more variable to speech than non-speech stimuli In the context of the larger Cambridge UK BabyRhythm Project, we lay the foundation for rhythmic movement in infancy to predict later language outcomes.

Cortical tracking of visual rhythmic speech by 5- and 8-month-old infants: Individual differences in phase angle relate to language outcomes up to 2 years.

It is known that the rhythms of speech are visible on the face, accurately mirroring changes in the vocal tract. These low-frequency visual temporal movements are tightly correlated with speech output, and both visual speech (e.g., mouth motion) and the acoustic speech amplitude envelope entrain neural oscillations. Low-frequency visual temporal information ('visual prosody') is known from behavioural studies to be perceived by infants, but oscillatory studies are currently lacking. Here we measure cortical tracking of low-frequency visual temporal information by 5- and 8-month-old infants using a rhythmic speech paradigm (repetition of the syllable 'ta' at 2 Hz). Eye-tracking data were collected simultaneously with EEG, enabling computation of cortical tracking and phase angle during visual-only speech presentation. Significantly higher power at the stimulus frequency indicated that cortical tracking occurred across both ages. Further, individual differences in preferred phase to visual speech related to subsequent measures of language acquisition. The difference in phase between visual-only speech and the same speech presented as auditory-visual at 6- and 9-months was also examined. These neural data suggest that individual differences in early language acquisition may be related to the phase of entrainment to visual rhythmic input in infancy. RESEARCH HIGHLIGHTS: Infant preferred phase to visual rhythmic speech predicts language outcomes. Significant cortical tracking of visual speech is present at 5 and 8 months. Phase angle to visual speech at 8 months predicted greater receptive and productive vocabulary at 24 months.

Decoding speech information from EEG data with 4-, 7- and 11-month-old infants: Using convolutional neural network, mutual information-based and backward linear models.

BACKGROUND: Computational models that successfully decode neural activity into speech are increasing in the adult literature, with convolutional neural networks (CNNs), backward linear models, and mutual information (MI) models all being applied to neural data in relation to speech input. This is not the case in the infant literature. NEW METHOD: Three different computational models, two novel for infants, were applied to decode low-frequency speech envelope information. Previously-employed backward linear models were compared to novel CNN and MI-based models. Fifty infants provided EEG recordings when aged 4, 7, and 11 months, while listening passively to natural speech (sung or chanted nursery rhymes) presented by video with a female singer. RESULTS: Each model computed speech information for these nursery rhymes in two different low-frequency bands, delta and theta, thought to provide different types of linguistic information. All three models demonstrated significant levels of performance for delta-band neural activity from 4 months of age, with two of three models also showing significant performance for theta-band activity. All models also demonstrated higher accuracy for the delta-band neural responses. None of the models showed developmental (age-related) effects. COMPARISONS WITH EXISTING METHODS: The data demonstrate that the choice of algorithm used to decode speech envelope information from neural activity in the infant brain determines the developmental conclusions that can be drawn. CONCLUSIONS: The modelling shows that better understanding of the strengths and weaknesses of each modelling approach is fundamental to improving our understanding of how the human brain builds a language system.

Emergence of the cortical encoding of phonetic features in the first year of life.

Even prior to producing their first words, infants are developing a sophisticated speech processing system, with robust word recognition present by 4-6 months of age. These emergent linguistic skills, observed with behavioural investigations, are likely to rely on increasingly sophisticated neural underpinnings. The infant brain is known to robustly track the speech envelope, however previous cortical tracking studies were unable to demonstrate the presence of phonetic feature encoding. Here we utilise temporal response functions computed from electrophysiological responses to nursery rhymes to investigate the cortical encoding of phonetic features in a longitudinal cohort of infants when aged 4, 7 and 11 months, as well as adults. The analyses reveal an increasingly detailed and acoustically invariant phonetic encoding emerging over the first year of life, providing neurophysiological evidence that the pre-verbal human cortex learns phonetic categories. By contrast, we found no credible evidence for age-related increases in cortical tracking of the acoustic spectrogram.

Neural phase angle from two months when tracking speech and non-speech rhythm linked to language performance from 12 to 24 months.

Atypical phase alignment of low-frequency neural oscillations to speech rhythm has been implicated in phonological deficits in developmental dyslexia. Atypical phase alignment to rhythm could thus also characterize infants at risk for later language difficulties. Here, we investigate phase-language mechanisms in a neurotypical infant sample. 122 two-, six- and nine-month-old infants were played speech and non-speech rhythms while EEG was recorded in a longitudinal design. The phase of infants' neural oscillations aligned consistently to the stimuli, with group-level convergence towards a common phase. Individual low-frequency phase alignment related to subsequent measures of language acquisition up to 24 months of age. Accordingly, individual differences in language acquisition are related to the phase alignment of cortical tracking of auditory and audiovisual rhythms in infancy, an automatic neural mechanism. Automatic rhythmic phase-language mechanisms could eventually serve as biomarkers, identifying at-risk infants and enabling intervention at the earliest stages of development.

Assessing Sensorimotor Synchronisation in Toddlers Using the Lookit Online Experiment Platform and Automated Movement Extraction.

Adapting gross motor movement to match the tempo of auditory rhythmic stimulation (sensorimotor synchronisation; SMS) is a complex skill with a long developmental trajectory. Drumming tasks have previously been employed with infants and young children to measure the emergence of rhythmic entrainment, and may provide a tool for identification of those with atypical rhythm perception and production. Here we describe a new protocol for measuring infant rhythmic movement that can be employed at scale. In the current study, 50 two-year-olds drummed along with the audiovisual presentation of four steady rhythms, using videos of isochronous drumming at 400, 500, 600, and 700 ms IOI, and provided their spontaneous motor tempo (SMT) by drumming in silence. Toddlers' drumming is observed from video recordings made in participants' own homes, obtained via the Lookit platform for online infant studies. We use OpenPose deep-learning model to generate wireframe estimates of hand and body location for each video. The vertical displacement of the hand was extracted, and the power and frequency of infants' rhythmic entrainment quantified using Fast Fourier Transforms. We find evidence for age-appropriate tempo-flexibility in our sample. Our results demonstrate the feasibility of a fully digital approach to measuring rhythmic entrainment from within the participant's home, from early in development.

Cortical Tracking of Sung Speech in Adults vs Infants: A Developmental Analysis.

Here we duplicate a neural tracking paradigm, previously published with infants (aged 4 to 11 months), with adult participants, in order to explore potential developmental similarities and differences in entrainment. Adults listened and watched passively as nursery rhymes were sung or chanted in infant-directed speech. Whole-head EEG (128 channels) was recorded, and cortical tracking of the sung speech in the delta (0.5-4 Hz), theta (4-8 Hz) and alpha (8-12 Hz) frequency bands was computed using linear decoders (multivariate Temporal Response Function models, mTRFs). Phase-amplitude coupling (PAC) was also computed to assess whether delta and theta phases temporally organize higher-frequency amplitudes for adults in the same pattern as found in the infant brain. Similar to previous infant participants, the adults showed significant cortical tracking of the sung speech in both delta and theta bands. However, the frequencies associated with peaks in stimulus-induced spectral power (PSD) in the two populations were different. PAC was also different in the adults compared to the infants. PAC was stronger for theta- versus delta- driven coupling in adults but was equal for delta- versus theta-driven coupling in infants. Adults also showed a stimulus-induced increase in low alpha power that was absent in infants. This may suggest adult recruitment of other cognitive processes, possibly related to comprehension or attention. The comparative data suggest that while infant and adult brains utilize essentially the same cortical mechanisms to track linguistic input, the operation of and interplay between these mechanisms may change with age and language experience.

Neural detection of changes in amplitude rise time in infancy.

Amplitude rise times play a crucial role in the perception of rhythm in speech, and reduced perceptual sensitivity to differences in rise time is related to developmental language difficulties. Amplitude rise times also play a mechanistic role in neural entrainment to the speech amplitude envelope. Using an ERP paradigm, here we examined for the first time whether infants at the ages of seven and eleven months exhibit an auditory mismatch response to changes in the rise times of simple repeating auditory stimuli. We found that infants exhibited a mismatch response (MMR) to all of the oddball rise times used for the study. The MMR was more positive at seven than eleven months of age. At eleven months, there was a shift to a mismatch negativity (MMN) that was more pronounced over left fronto-central electrodes. The MMR over right fronto-central electrodes was sensitive to the size of the difference in rise time. The results indicate that neural processing of changes in rise time is present at seven months, supporting the possibility that early speech processing is facilitated by neural sensitivity to these important acoustic cues.

Delta- and theta-band cortical tracking and phase-amplitude coupling to sung speech by infants.

The amplitude envelope of speech carries crucial low-frequency acoustic information that assists linguistic decoding at multiple time scales. Neurophysiological signals are known to track the amplitude envelope of adult-directed speech (ADS), particularly in the theta-band. Acoustic analysis of infant-directed speech (IDS) has revealed significantly greater modulation energy than ADS in an amplitude-modulation (AM) band centred on ∼2 Hz. Accordingly, cortical tracking of IDS by delta-band neural signals may be key to language acquisition. Speech also contains acoustic information within its higher-frequency bands (beta, gamma). Adult EEG and MEG studies reveal an oscillatory hierarchy, whereby low-frequency (delta, theta) neural phase dynamics temporally organize the amplitude of high-frequency signals (phase amplitude coupling, PAC). Whilst consensus is growing around the role of PAC in the matured adult brain, its role in the development of speech processing is unexplored. Here, we examined the presence and maturation of low-frequency (<12 Hz) cortical speech tracking in infants by recording EEG longitudinally from 60 participants when aged 4-, 7- and 11- months as they listened to nursery rhymes. After establishing stimulus-related neural signals in delta and theta, cortical tracking at each age was assessed in the delta, theta and alpha [control] bands using a multivariate temporal response function (mTRF) method. Delta-beta, delta-gamma, theta-beta and theta-gamma phase-amplitude coupling (PAC) was also assessed. Significant delta and theta but not alpha tracking was found. Significant PAC was present at all ages, with both delta and theta -driven coupling observed.

Rate of infant carrying impacts infant spontaneous motor tempo.

Rhythm production is a critical component of human interaction, not least forming the basis of our musicality. Infants demonstrate a spontaneous motor tempo (SMT), or natural rate of rhythmic movement. Here, we ask whether infant SMT is influenced by the rate of locomotion infants experience when being carried. Ten-month-old, non-walking infants were tested using a free drumming procedure before and after 10 min of being carried by an experimenter walking at a slower (98 BPM) or faster (138 BPM) than average tempo. We find that infant SMT is differentially impacted by carrying experience dependent on the tempo at which they were carried: infants in the slow-walked group exhibited a slower SMT from pre-test to post-test, while infants in the fast-walked group showed a faster SMT from pre-test to post-test. Heart rate data suggest that this effect is not due to a general change in the state of arousal. We argue that being carried during caregiver locomotion is a predominant experience for infants throughout the first years of life, and as a source of regular, vestibular, information, may at least partially form the basis of their sense of rhythm.

Machine learning accurately classifies neural responses to rhythmic speech vs. non-speech from 8-week-old infant EEG.

Currently there are no reliable means of identifying infants at-risk for later language disorders. Infant neural responses to rhythmic stimuli may offer a solution, as neural tracking of rhythm is atypical in children with developmental language disorders. However, infant brain recordings are noisy. As a first step to developing accurate neural biomarkers, we investigate whether infant brain responses to rhythmic stimuli can be classified reliably using EEG from 95 eight-week-old infants listening to natural stimuli (repeated syllables or drumbeats). Both Convolutional Neural Network (CNN) and Support Vector Machine (SVM) approaches were employed. Applied to one infant at a time, the CNN discriminated syllables from drumbeats with a mean AUC of 0.87, against two levels of noise. The SVM classified with AUC 0.95 and 0.86 respectively, showing reduced performance as noise increased. Our proof-of-concept modelling opens the way to the development of clinical biomarkers for language disorders related to rhythmic entrainment.

Infant Spontaneous Motor Tempo.

Spontaneous Motor Tempo (SMT) is influenced by individual differences in age and body size. We present the first data documenting the SMT of infants from 5 to 37 months of age using a simple drumming task. As in late childhood and adulthood, we predicted that infant SMT would slow across the first years of life. However, we find that older infants drum more quickly than younger infants. Furthermore, studies of adults suggest larger bodies prefer slower rhythms. This relationship may be the product of biomechanical resonance, or effects may be driven by rhythmic experience, such as of locomotion. We used infants, whose body size is dissociated from their predominant experience of locomotion as their parent often carries them, to test this argument. We reveal that infant SMT is predicted by parent, but not own, body size, supporting a passive experience-based argument, and propose that early rhythm may be set by repetitive vestibular stimulation when carried by the caregiver.

Embodiment and the origin of interval timing: kinematic and electromyographic data.

Recent evidence suggests that interval timing (the judgment of durations lasting from approximately 500 ms. to a few minutes) is closely coupled to the action control system. We used surface electromyography (EMG) and motion capture technology to explore the emergence of this coupling in 4-, 6-, and 8-month-olds. We engaged infants in an active and socially relevant arm-raising task with seven cycles and response period. In one condition, cycles were slow (every 4 s); in another, they were fast (every 2 s). In the slow condition, we found evidence of time-locked sub-threshold EMG activity even in the absence of any observed overt motor responses at all three ages. This study shows that EMGs can be a more sensitive measure of interval timing in early development than overt behavior.

Mapping the origins of time: scalar errors in infant time estimation.

Time is central to any understanding of the world. In adults, estimation errors grow linearly with the length of the interval, much faster than would be expected of a clock-like mechanism. Here we present the first direct demonstration that this is also true in human infants. Using an eye-tracking paradigm, we examined 4-, 6-, 10-, and 14-month-olds' responses to the omission of a recurring target, on either a 3- or 5-s cycle. At all ages (a) both fixation and pupil dilation measures were time locked to the periodicity of the test interval, and (b) estimation errors grew linearly with the length of the interval, suggesting that trademark interval timing is in place from 4 months.