Auditory Rhythm Encoding during the Last Trimester of Human Gestation: From Tracking the Basic Beat to Tracking Hierarchical Nested Temporal Structures

Rhythm perception and synchronization to periodicity hold fundamental neurodevelopmental importance for language acquisition, musical behavior, and social communication. Rhythm is omnipresent in the fetal auditory world and newborns demonstrate sensitivity to auditory rhythmic cues. During the last trimester of gestation, the brain begins to respond to auditory stimulation and to code the auditory environment. When and how during this period do the neural capacities for rhythm processing develop? We conducted a cross-sectional study in 46 neonates (24 male) born between 27 and 35 weeks gestational age (wGA), measuring their neural responses to auditory rhythms with high-density electroencephalography during sleep. We developed measures to evaluate neural synchronization to nested rhythmic periodicities, including the fast isochronous beat and slower metrical (beat grouping) structures. We show that neural synchronization to beat and meter becomes stronger with increasing GA, converging on small phase differences between stimulus and neural responses near term, similar to those observed in adults. Dividing the cohort into subpopulations born before and after 33 wGA revealed that both younger and older groups showed neural synchronization to the fast periodicity related to the isochronous beat, whereas only the older group showed significant neural synchronization to the slower meter frequencies related to beat groupings, suggesting that encoding of nested periodicities arrives during late gestation. Together, our results shed light on the rapid evolution of neural coding of external hierarchical auditory rhythms during the third trimester of gestation, starting from the age when the thalamocortical axons establish the first synapses with the cortical plate.