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.

Primate auditory prototype in the evolution of the arcuate fasciculus

“…Our observations fit with the notion that language adaptations may have arisen from primate auditory pathways 17 . We speculate that this dorsal auditory pathway is involved in not just spatial processing in the classical sense but also sound and vocal patterning in the time domain 18 , which is supported by evidence implicating inferior frontal cortex in sound sequence patterning in macaques and humans 19 and vocalization sound processing and production in macaques, marmosets and humans 20 . Whereas auditory processes in monkeys may have previously been assumed to involve ventral pathways, the current results in macaques indicate that a dorsal auditory pathway should not be dismissed.…”

A novel reticular oscillator in the brainstem synchronizes neonatal crying with breathing

“…Its proximity to the cNA is consistent with a previous hypothesis that a central pattern generator for vocalization resides in the medullary reticular formation ( 6 ). A simple model predicts that patterning of laryngeal and breathing motor groups is sufficient to control vocalizations ( 7 ). Furthermore, it is anticipated that such a patterning system would also encode the tempo of syllables within vocalizations.…”

“…The innate vocalization motor program is initiated by brainstem projections from the midbrain periaqueductal gray ( 5 ); however, the neural circuitry required to fully orchestrate these vocalizations remains poorly understood ( 6 , 7 ). Moreover, because mammalian vocalizations are produced by the concerted activity of articulator (laryngeal and tongue) and breathing (diaphragm and intercostal) muscles ( 8 ), they must be seamlessly integrated with the breathing rhythm.…”

Echolocation reverses information flow in a cortical vocalization network

“…Vocal production is a crucial behaviour that underlies the evolutionary success of various animal species. Several cortical and subcortical structures in the mammalian brain support vocalization (Jurgens, 2009), their activities related to vocal control (Gavrilov et al, 2017;Okobi et al, 2019;Zhang and Ghazanfar, 2020), motor preparation (Okobi et al, 2019;Schulz et al, 2005;Tschida et al, 2019), and feedback correction of vocal outputs (Eliades and Tsunada, 2018;Eliades and Wang, 2008). However, the precise neural dynamics that underpin vocal production within these regions, and the nature of long-distance interactions in large-scale neural networks related to vocal utterance, remain poorly understood.…”