A Hierarchy of Autonomous Systems for Vocal Production

Abstract

Vocal production is hierarchical in the time domain. These hierarchies build upon biomechanical and neural dynamics across various timescales. We review studies in marmoset monkeys, songbirds, and other vertebrates. To organize these data in an accessible and across-species framework, we interpret the different timescales of vocal production as belonging to different levels of an autonomous systems hierarchy. The first level accounts for vocal acoustics produced on short timescales; subsequent levels account for longer timescales of vocal output. The hierarchy of autonomous systems that we put forth accounts for vocal patterning, sequence generation, dyadic interactions, and context dependence by sequentially incorporating central pattern generators, intrinsic drives, and sensory signals from the environment. We then show the framework's utility by providing an integrative explanation of infant vocal production learning in which social feedback modulates infant vocal acoustics through the tuning of a drive signal.

Keywords: Mayer wave; biomechanics; birdsong; dynamical system; marmoset monkey; parental feedback; slow oscillations; social reinforcement; timescales; vocalizations.

Figure 1.

Temporal hierarchies of vocalizations, and the corresponding brain structure and vocal apparatus. (A) A segment of infant marmoset monkey vocalization comprised of utterances of different types of calls (contributed by Ghazanfar lab). (B) A segment of Bengalese finch song comprised of fixed and variable syllable sequences (contributed by Yisi Zhang). (C) A segment of midshipman fish grunts (courtesy of Dr. Andrew Bass). (D) Vocal communication system and vocal apparatus of nonhuman primates. Abbreviations: ACC, anterior cingulate cortex; AC, auditory cortex; Am, amygdala; Hy, hypothalamus; PAG, periaqueductal gray; LRF, lateral reticular formation; PB, parabrachial nucleus; MN, motor nuclei; VC, visual cortex (adapted from [125] and [126]). (E) Song system and vocal apparatus of songbirds. Abbreviations: HVC (as a proper name); RA, robust nucleus of the arcopallium; NIf, nucleus interfacialis of the nidopallium; LMAN, lateral magnocellular nucleus of the anterior nidopallium; Area X, striato-palliadal basal ganglia nucleus; DLM, dorsolateral thalamic nucleus; Uva, nucleus uvaeformis; nXIIts, tracheosyringeal part of the hypoglossal motor nucleus (adapted from [127]). (F) Vocal network and vocal apparatus of fish. Abbreviations: POA, preoptic area; AT, anterior tuberal nucleus; VT, ventral tuberal nucleus; PL, paralemniscal midbrain tegmentum; TS, torus semicircularis; VPP, vocal prepacemaker nucleus; VPN, vocal pacemaker nucleus; VMN vocal motor nucleus (adapted from [128]). Solid lines indicate vocal pathways and dotted lines indicate sensory pathways.

Figure 2.

A hierarchical structure of the vocal production system based on time-scales. (A) Two-level system: the vocal biomechanics (lungs and larynx) and two coupled central pattern generators (CPGs). (B) Three-level system: adding a drive signal on top of the CPGs enables the continuous production of various calls. (C) Four-level system: a fourth layer provides the modulation to the drive and allows animals to adjust the vocal output with respect to the environment.

Figure 3.

Vocal development through social feedback. Here we illustrate vocal development through marmoset monkey parent-infant vocal interaction. The parent responds at the transitions where the infant starts producing more mature-sounding vocalizations [117]. As more mature-sounding vocalizations indicate a greater underlying drive signal [53], parental responses occur in the rising phase of the oscillatory drive. The contingent parental calls have a cumulative effect on the infant vocal production towards more high-energy calls, accelerating vocal development on the timescale of days [116]. This process can be a consequence of shaping the drive signal of infant vocal production. The social feedback process described here compactly illustrates its cumulative influence on cumulative changes in the drive signal.