Perinatally Influenced Autonomic System Fluctuations Drive Infant Vocal Sequences

Abstract

The 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.

Arousal dynamics drive vocal production in marmoset monkeys

“…Considering the relationship between vocal onset and the ongoing phase of the Mayer wave, an indirect consequence of this slow, pervasive autonomic oscillation is to assist in the assembly of vocal behavior. Indeed, vocal developmental data from marmosets suggests that the proper assembly of contact calling occurs postnatally, with an upward shift of the threshold (Zhang and Ghazanfar 2016). Infant marmosets in the undirected context produce vocalizations at almost 10 times the rate of adults, with a range of immature-sounding call types.…”

The autonomic nervous system is the engine for vocal development through social feedback

“…Such transient vocalizations are also evident during song learning by birds [22**]. Unlike Old World nonhuman primates, developing marmosets also produce a babbling-like vocal output [23, 24**, 25], with some vocalizations that sound adult-like (but are produced in the wrong social context) and others that are immature forms of what will ultimately be the contact (“phee”) call used by it during vocal exchanges (Figure 1A) [24**,26**]. …”

“…As it is for human infants [28] and songbirds [22**,29], the babbling output of marmoset infants is very rhythmic [26**]. This rhythmicity suggests that this output is driven by the oscillatory activity of the nervous system.…”

“…This rhythmicity suggests that this output is driven by the oscillatory activity of the nervous system. As in developing songbirds [30], the temporal structure of babbling output by infants is tightly locked to respiration in marmoset monkey infants [26**], with respiration providing the power for generating vocal sounds [31]. Approximately every second, an utterance phase-locked to the respiratory rhythm is produced.…”

“…Approximately every second, an utterance phase-locked to the respiratory rhythm is produced. The time-varying spectral structure of babbling sequences also has a rhythm but at a rate that is an order of magnitude slower: Spectral entropy, a measure of the noisiness of the sound spectrum [24**,32], fluctuates during babbling at a 0.1 Hz frequency [26**]. This is interesting because the autonomic nervous system (ANS) also has a 0.1 Hz rhythm known as the Mayer wave.…”