Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter

Abstract

The ability to extract rhythmic structure is important for the development of language, music and social communication. Although previous studies show infants’ brains entrain to the periodicities of auditory rhythms and even different metrical interpretations (e.g., groups of two vs. three beats) of ambiguous rhythms, whether the premature brain tracks beat and meter frequencies had not been explored previously. We used high-resolution electroencephalography, while premature infants (n = 19, five male, mean age 32 ± 2.59 wGA) heard two auditory rhythms in the incubators. We observed selective enhancement of the neural response at both beat and meter-related frequencies. Further, neural oscillations at the beat and duple (groups of 2) meter were phase aligned with the envelope of the auditory rhythmic stimuli. Comparing the relative power at beat and meter frequencies across stimuli and frequency revealed evidence for selective enhancement of duple meter. This suggests that even at this early stage of development, neural mechanisms for processing auditory rhythms beyond simple sensory coding are present. Our results add to a few recent neuroimaging studies demonstrating discriminative auditory abilities of premature neural networks. Specifically, our results demonstrate the early capacities of the immature neural circuits and networks to code both simple beat and beat grouping (i.e., hierarchical meter) regularities of auditory sequences. Considering the importance of rhythm processing for acquiring language and music, our findings indicate that even before birth, the premature brain is already learning this important aspect of the auditory world in a sophisticated and abstract way.Significant Statement:Processing auditory rhythm is of great neurodevelopmental importance. In an electroencephalography experiment in premature newborns, we found converging evidence that when presented with auditory rhythms the premature brain encodes multiple periodicities corresponding to beat and beat grouping (meter) frequencies, and even selectively enhances the neural response to meter compared to beat, as in human adults. We also found that the phase of low frequency neural oscillations align to the envelope of the auditory rhythms, and that this phenomenon becomes less precise at lower frequencies. These findings demonstrate the initial capacities of the developing brain to code auditory rhythm, and the importance of special care to the auditory environment of this vulnerable population during a highly dynamic period of neural development.

Pushing the boundaries of MEG based on optically pumped magnetometers towards early human life

“…The existence of significant peaks in the power spectrum SNR at the oddball frequency and its first harmonic is a frequency tagging analog of the auditory mismatch negativity (MMN), which reflects automatic change detection (33). In the frequency tagging approach, these peaks can also reveal rhythm perception and, more generally extraction of structural patterns (30)(31)(32), as the trains of stimuli are presented periodically. Interestingly, the magnetic topographies suggest right-lateralized cortical sources for these oddball responses, echoing previous observations in 2-month-olds (34).…”

“…In the second paradigm, we demonstrated the possibility of using our OPM-MEG system to perform frequency tagging paradigms with newborns, which have been shown to be very fruitful with young participants [27,33]. While frequency tagging paradigms related to the one applied in this study were carried out with EEG in adults [34] and infants [35][36][37], steady-state responses have not yet been studied in infants with MEG, nor with tone frequency changes. The power spectrum SNR exhibited significant peaks at the base frequency, at the oddball frequency and at its first harmonic.…”

“…The last two are a frequency tagging analog of the auditory mismatch negativity (MMN), reflecting automatic change detection [38]. In the frequency tagging approach, these peaks can also reveal rhythm perception and, more generally extraction of structural patterns [35][36][37], as the trains of stimuli are presented periodically. It is worth noting that observing an SNR peak in the spectrum at 0.75 Hz is a nontrivial feat of our system, as the OPM signal is known to be very noisy at such low frequencies due to movement and ambient field drifts [14].…”

Early social communication through music: State of the art and future perspectives

“…EEG studies show that infants' brains track beat and meter frequencies of auditory patterns (Cirelli, Spinelli, et al, 2016;Winkler et al, 2009) as well as ID songs (T. Nguyen et al, 2023) and nursery rhymes (Attaheri et al, 2022). Remarkably, even premature infants at 30-33 weeks' gestation track both beat and meter frequencies in auditory patterns (Edalati et al, 2023). Infants can also be primed to perceive a metrically ambiguous patternthat is, a pattern that could be perceived to have a duple or a triple meter in one meter or the other by bouncing them on either every second or every third beat (Phillips-Silver & Trainor, 2005).…”

Social interaction links active musical rhythm engagement and expressive communication in autistic toddlers

“…When considering specific components of music engagement that may link to social and communication behaviors, there is increasing attention to the role of rhythm processing. Rhythm perception, including the ability to perceive a steady, underlying beat, emerges very early in typical development, as evidenced both by behavioral (Ilari, 2015; Zentner & Eerola, 2010) and neural measures (Edalati et al, 2023; Háden et al, 2015; Honing et al, 2009; Winkler et al, 2009). Rhythm skills are associated with social connection (Marsh et al, 2009), interpersonal coordination (Keller et al, 2014; Lang et al, 2016), and individuals' capacities for linguistic communication (Nayak et al, 2022; Nitin et al, 2023) in nonautistic children and adults.…”