The respiratory-vocal system of songbirds

Abstract

This wide-ranging review presents an overview of the respiratory-vocal system in songbirds, which are the only other vertebrate group known to display a degree of respiratory control during song rivalling that of humans during speech; this despite the fact that the peripheral components of both the respiratory and vocal systems differ substantially in the two groups. We first provide a brief description of these peripheral components in songbirds (lungs, air sacs and respiratory muscles, vocal organ (syrinx), upper vocal tract) and then proceed to a review of the organization of central respiratory-related neurons in the spinal cord and brainstem, the latter having an organization fundamentally similar to that of the ventral respiratory group of mammals. The second half of the review describes the nature of the motor commands generated in a specialized “cortical” song control circuit and how these might engage brainstem respiratory networks to shape the temporal structure of song. We also discuss a bilaterally projecting “respiratory-thalamic” pathway that links the respiratory system to “cortical” song control nuclei. This necessary pathway for song originates in the brainstem’s primary inspiratory center and is hypothesized to play a vital role in synchronizing song motor commands both within and across hemispheres.

Discrete Circuits Support Generalized versus Context-Specific Vocal Learning in the Songbird

“…Our results indicate that when it is optimal to generalize modifications across contexts - for example, during initial learning or in response to weakening of musculature or other perturbations that affect control of a syllable regardless of context - consistent biasing signals from the AFP will promote an updating of the core MP representation. In contrast, when context-specificity is appropriate - for example, to modify central commands in a manner that accounts for context-dependent dynamics of the musculoskeletal system (Bouchard and Chang, 2014; Ostry et al, 1996; Schmidt and Wild, 2014; Wohlgemuth et al, 2010) - conflicting biasing signals will interfere with consolidation, and learning will continue to rely on moment-by-moment modulation by the AFP. Such a dependence of consolidation on the coherence of AFP bias may therefore be a natural way for the nervous system to transfer modifications that are generally appropriate to primary motor circuitry, while reserving frontal, “executive” circuitry for dynamically adjusting performance in response to context-specific requirements (Duan et al, 2015; Hilario et al, 2012; Kim and Hikosaka, 2013; Miller and Cohen, 2001; Narayanan and Laubach, 2006).…”

A Distributed Recurrent Network Contributes to Temporally Precise Vocalizations

“…Zebra finches sing highly stereotyped song motifs comprising sequences of single or multi-note syllables, and song timing is precisely reproducible at the note, syllable and motif level – features with timescales that range from milliseconds to seconds (Charlesworth et al, 2011; Chi and Margoliash, 2001; Glaze and Troyer, 2006; Ravbar et al, 2012). Studies in zebra finches and other songbirds have delineated a central circuit for song patterning that includes both forebrain and brainstem elements (Brainard and Doupe, 2013; Mooney, 2009; Schmidt and Wild, 2014), providing a powerful system for identifying the neural mechanisms that contribute to the precise temporal control of vocalization. Do forebrain components of this song circuit effectively commandeer and override brainstem pattern generating networks to enable singing, or do the forebrain and brainstem components interact in a more reciprocal manner?…”

“…An influential idea is that synaptically linked chains of HVC RA cells form a neural clock that controls song timing, which has gained further support from the observation that focal, bilateral manipulation of HVC temperature by a few degrees Celsius slows or accelerates song timing without affecting either frequency or amplitude (Long and Fee, 2008). Nonetheless, the extent to which these timing signals arise from mechanisms local to HVC or from a more distributed brain network has remained controversial (Amador et al, 2013; Andalman et al, 2011; Goldin et al, 2013; Schmidt and Wild, 2014). Notably, song timing can be modulated non-uniformly when HVC is cooled (Andalman et al, 2011), and more extreme cooling of HVC can cause long syllables to break into shorter elements (Goldin et al, 2013), raising the possibility that other brain regions besides HVC are also involved in generating timing signals (Figure 1A).…”

Audition and Hemispheric Specialization in Songbirds and New Evidence from Australian Magpies

“…Furthermore, feedback loops are essential for vocal learning, and these are found only in passerines and parrots (and two species of humming birds), cetaceans and humans. In the former group are the HVC, the robust nucleus of the arcopallium (RA) and the tracheosyringeal component of the hypoglossal nucleus (nXIIts), which are necessary for the acquisition and expression of learned song [50], whilst the latter include Area X and the lateral magnocellular nucleus of the anterior nidopallium (LMAN) [52][53][54]. All of these main nuclei and some important auxiliary nuclei (Figure 1), represented on both sides of the brain, have been tested for lateralized expression.…”