Neural oscillations suggest periodicity encoding during auditory beat processing in the premature brain

Abstract

When exposed to rhythmic patterns with temporal regularity, adults exhibit an inherent ability to extract and anticipate an underlying sequence of regularly spaced beats, which is internally constructed, as beats are experienced even when no events occur at beat positions (e.g., in the case of rests). Perception of rhythm and synchronization to periodicity is indispensable for development of cognitive functions, social interaction, and adaptive behavior. We evaluated neural oscillatory activity in premature newborns (n = 19, mean age, 32 ± 2.59 weeks gestational age) during exposure to an auditory rhythmic sequence, aiming to identify early traces of periodicity encoding and rhythm processing through entrainment of neural oscillations at this stage of neurodevelopment. The rhythmic sequence elicited a systematic modulation of alpha power, synchronized to expected beat locations coinciding with both tones and rests, and independent of whether the beat was preceded by tone or rest. In addition, the periodic alpha-band fluctuations reached maximal power slightly before the corresponding beat onset times. Together, our results show neural encoding of periodicity in the premature brain involving neural oscillations in the alpha range that are much faster than the beat tempo, through alignment of alpha power to the beat tempo, consistent with observations in adults on predictive processing of temporal regularities in auditory rhythms. RESEARCH HIGHLIGHTS: In response to the presented rhythmic pattern, systematic modulations of alpha power showed that the premature brain extracted the temporal regularity of the underlying beat. In contrast to evoked potentials, which are greatly reduced when there is no sounds event, the modulation of alpha power occurred for beats coinciding with both tones and rests in a predictive way. The findings provide the first evidence for the neural coding of periodicity in auditory rhythm perception before the age of term.

Keywords: EEG; alpha oscillations; music; neurodevelopment; phase amplitude coupling; rhythm.