One-to-one innervation of vocal muscles allows precise control of birdsong

Iris Adam, Alyssa Maxwell, Helen Rößler, Emil B Hansen, Michiel Vellema, Jonathan Brewer, Coen P H Elemans*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

The motor control resolution of any animal behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of motor units (MUs) and muscle-specific force. Birdsong is an excellent model system for understanding acquisition and maintenance of complex fine motor skills, but we know surprisingly little about how the motor pool controlling the syrinx is organized and how MU recruitment drives changes in vocal output. Here we developed an experimental paradigm to measure MU size distribution using spatiotemporal imaging of intracellular calcium concentration in cross-sections of living intact syrinx muscles. We combined these measurements with muscle stress and an in vitro syrinx preparation to determine the control resolution of fundamental frequency (fo), a key vocal parameter, in zebra finches. We show that syringeal muscles have extremely small MUs, with 40%-50% innervating ≤3 and 13%-17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm2) known to skeletal vertebrate muscle, small force steps by the major fo controlling muscle provide control of 50-mHz to 7.3-Hz steps per MU. We show that the song system has the highest motor control resolution possible in the vertebrate nervous system and suggest this evolved due to strong selection on fine gradation of vocal output. Furthermore, we propose that high-resolution motor control was a key feature contributing to the radiation of songbirds that allowed diversification of song and speciation by vocal space expansion.

Original languageEnglish
JournalCurrent Biology
Volume31
Issue number14
Pages (from-to)3115-3124
ISSN0960-9822
DOIs
Publication statusPublished - 26. Jul 2021

Bibliographical note

Preprint published January 11, 2020

Keywords

  • birdsong
  • motor control
  • motor unit
  • songbird
  • sound production
  • vocal communication
  • voice

Fingerprint

Dive into the research topics of 'One-to-one innervation of vocal muscles allows precise control of birdsong'. Together they form a unique fingerprint.

Cite this