Perinatally Influenced Autonomic System Fluctuations Drive Infant Vocal Sequences

• Like human infants, marmoset monkey infants produce babbling-like vocal sequences
• Different vocal elements were dependent upon unique patterns of respiration
• Fluctuations of the autonomic nervous system drove patterns of respiration
• Perinatal experience influenced the physiology underlying vocal sequences

SummaryThe variable vocal behavior of human infants is the scaffolding upon which speech and social interactions develop. It is important to know what factors drive this developmentally critical behavioral output. Using marmoset monkeys as a model system, we first addressed whether the initial conditions for vocal output and its sequential structure are perinatally influenced. Using dizygotic twins and Markov analyses of their vocal sequences, we found that in the first postnatal week, twins had more similar vocal sequences to each other than to their non-twin siblings. Moreover, both twins and their siblings had more vocal sequence similarity with each other than with non-sibling infants. Using electromyography, we then investigated the physiological basis of vocal sequence structure by measuring respiration and arousal levels (via changes in heart rate). We tested the hypothesis that early-life influences on vocal output are via fluctuations of the autonomic nervous system (ANS) mediated by vocal biomechanics. We found that arousal levels fluctuate at ∼0.1 Hz (the Mayer wave) and that this slow oscillation modulates the amplitude of the faster, ∼1.0 Hz respiratory rhythm. The systematic changes in respiratory amplitude result in the different vocalizations that comprise infant vocal sequences. Among twins, the temporal structure of arousal level changes was similar and therefore indicates why their vocal sequences were similar. Our study shows that vocal sequences are tightly linked to respiratory patterns that are modulated by ANS fluctuations and that the temporal structure of ANS fluctuations is perinatally influenced.