The respiratory-vocal system of songbirds: anatomy, physiology, and neural control

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.

Keywords: avian; basal ganglia; brainstem; breathing; medulla; neural; singing; song system; songbirds; sparse code; vocalization.

FIGURE 1

Airflow in the lung and air sacs of a typical passerine bird. (Top) Anatomy of the avian respiratory apparatus. The trachea splits into the left and right primary bronchus (only the left bronchus is shown here) at the level of the syrinx (shaded in orange; grey in the print version). The primary bronchusthen splits further into secondary bronchi which split further into either theparabronchi of the paleopulmo (green; dark grey in the print version) or neopulmo (blue; dark grey in the print version). The bronchi of the lung are directly connected to a system of air sacs. According to their bronchial connections, air sacs are divided into two primary groups, cranial air sacs (cervical, clavicular, and cranial thoracic) and caudal air sacs (caudal thoracic and abdominal). (Bottom) Pattern of airflow during the respiratory cycle. During inspiration (left), oxygenated air (yellow arrows; white in the print version) flows into the caudal air sacs as well as the paleopulmo and neopulmo (not shown). Unoxygenated air (red arrow; dark grey in the print version) flows into the cranial air sacs after having passed through the lungs. During expiration (right), oxygenated air from the caudal air sacs flows into the lung, while unoxygenated air from the cranial air sacs get pushed out the trachea. This system allows for continuous flow of oxygenated air through the lungs during both inspiration and expiration. Airflow in the paleopulmo occurs in the same direction during both inspiration and expiration (large arrow). Airflow in the neopulmo is believed to be bidirectional during both respiratory phases. This figure is adapted from Duncker (1972) and Düring et al. (2013).

FIGURE 2

Modulation of the respiratory pattern and underlying expiratory musculature during singing in songbirds. Amplitude and temporal pattern of respiratory pressure (horizontal line indicates ambient pressure) during vocalization (illustrated as spectrogram in top panel) change markedly from that during normal, silent respiration. A typical zebra finch song bout (shown here) typically consists of one or more motifs preceded by a variable number of introductory notes (intro), with each motif being made up of a stereotyped sequence of syllables. In this example, the song bout contains two motifs and is also preceded by a short distance call (call). Each of the song syllables is associated with a highly stereotyped expiratory pressure pulse (left inset) and expiratory muscle activity (right inset). (Left inset) Air sac pressure measurement for three consecutive syllables measured from three different motifs. (Right inset) EMG recordings from the abdominal expiratory muscles from the same three syllable sequences. This figure was generated based on recordings kindly provided by F. Goller.

FIGURE 3

Anatomy of the songbird syrinx and phonatory mechanism. (A) Ventrolateral external view of a thrasher syrinx depicting syringeal muscles. (B) Cartilage components of the syrinx include three tracheo-bronchial semi-rings (A1–A3) as well as the tympanum (Ty), which contains at its caudal end the pessulus (P), an important attachment site for the medial labium (ML). (C) Schematic ventral view of the songbird syrinx in quiet respiratory (left panel) and phonatory (center and right panels) configurations. During vocalization, the medial (ML) and lateral labia (LL) are set into vibration when they are adducted into the expiratory air stream. In preparation for phonation, the syrinx moves rostral. Contraction of the ipsilateral dorsal syringeal muscles (dS and dTB) rotates the bronchial cartilages into the syringeal lumen, moving the lateral and medial labia into the expiratory air stream where they are set into vibration to produce sound. Phonation may be bilateral (not shown) or unilateral. Unilateral phonation is achieved by closing one side of the syrinx through full adduction of the labium on that side, so that sound (wavy arrows) is only generated on the partially open contralateral right (centre panel) or left (right panel) side. Abbreviations: B, bronchus; ICM, membrane of the interclavicular air sac; T, trachea; M, syringeal muscle; ML, medial labium; LL, lateral labium; MTM, medial tympaniform membrane; P, pessulus; TL, m. tracheolateralis; ST, m. sternotrachealis; vS, m. syringealis ventralis; vTB, m. tracheobronchialis ventralis; dTB, m. tracheobronchialis dorsalis; dS, m. syringealis dorsalis; T, tracheal cartilage; Ty, A1–A3, B, bronchial cartilages; P, pessulus. (A) and (B) Modified from Riede and Goller (2010). Figure legend is modified from Suthers et al. (1999).

FIGURE 4

Example of a song from the brown thrasher illustrating the switching between left and right syrinx showing syllables with two-voice and single-voice components. Contributions from the right syrinx are shown in blue; not distinguishable in print, those from the left syrinx in green, and inspiratory minibreaths are shaded in grey. Airflow measurements are measured by placing a thermistor probe in the primary bronchus. This figure is modified from figure 4 in Suthers et al. (1994).

FIGURE 5

Nuclei and some of the interconnections of the respiratory-vocal system in a songbird. Abbreviations from top down: RA, robust nucleus of the arcopallium; Uva, nucleus uvaeformis; DM, dorsomedial nucleus of the intercollicular complex; PBvl, ventrolateral part of the parabrachial nucleus; IOS, nucleus infra-olivarus superior; RVL, ventrolateral nucleus of the rostral medulla; PAm, nucleus parambigualis; nTS, nucleus of the solitary tract; nA, nucleus ambiguus; RAm, nucleus retroambigualis; XIIts, tracheosyringeal part of the hypoglossal nucleus; ts, tracheosyringeal nerve; NX, cranial nerve X (vagus); Insp, inspiratory motoneurons at the level of spinal cord segment 14 (lower brachial); Exp, expiratory motoneurons at the level of spinal cord segment 19 (lower thoracic). Expiratory and inspiratory motoneurons receive predominantly contralateral projections from RAm and PAm, respectively—indicated by solid lines. Dots represent cell bodies and inverted arrowheads terminations. The two sides are symmetrical, of course, but for clarity the projections of RA and DM to all the nuclei of the ventrolateral pons and medulla, as well as to XIIts, are shown on the right, and the cascade of descending projections is shown on the left, as are the ascending recurrent pathways from RAm and Pam, these being predominantly ipsilateral. Note the sensory input from the lungs, air sacs and syrinx that reaches nTS, and hence PAm and Uva. The specific origin/type of syringeal afferents (illustrated by the asterisk) is presently unknown. Figure modified from Wild (2008).

FIGURE 6

Summary of cell types and their spatial localization in PAm. The left most panel shows the phase histograms of PAm respiratory-related neurons aligned vertically. Respiratory cycles are aligned to the onset of the inspiratory phase (red; 0° (light grey in the print version)) to show the respective contribution of different cell types throughout the respiratory cycle. The time of occurrence of the transition from inspiration to expiration (blue; grey in the print version) could vary within the respiratory cycle. (i) Pre-I phase histogram. (ii) Early-I phase histogram. (iii) I-Augment phase histogram. (iv) Late-I phase histogram. (v) Post-I phase histogram. (vi) E-Augment phase histogram. The schematic on the right illustrates the ventral respiratory column and other brainstem nuclei together with the rostrocaudal distribution of recorded respiratory-related cells with respect to the obex. The rostrocaudal location and cell type is schematically represented in an enlargement of the portion of the VRC spanning the obex (red V) (dark grey in print) on the right. VII, facial nucleus; VIII, vestibulocochlear nuclei; X, nucleus ambiguus; XII, hypoglossal nucleus; nTS, nucleus of the Tractus solitarius. Modified from figure 7 in Mclean et al. (2013).

FIGURE 7

Schematic representation of the avian song system and its relationship to the respiratory system. This figure highlights the bilateral nature of the projections from PAm to Uva and HVC. Details of several important circuits necessary in song learning and perception (e.g., the anterior forebrain pathway (AFP) and the ascending auditory pathway) have been omitted for simplicity.

FIGURE 8

A sparse motor code for song. Example recording from a neuron in RA during the production of a song motif. Top trace represents the spectrogram of a song motif with syllables labeled A–E. Middle and bottom traces show respectively a single unit recording while the bird is singing the motif and a raster plot showing spike timing during seven renditions of the motif. Notice the near perfect alignment of spikes across multiple renditions (1 through 7) of the song motif. This figure is based on data generously provided to the authors by Kyler J. Brown and Dan Margoliash.

FIGURE 9

Spontaneous activity of nonrespiratory bursting (NRB) neurons in PAm is correlated with bursting in the contralateral HVC. A, Simultaneous recordings of two single units in the left PAm while maintaining the same unit in the contralateral HVC. For the top pair, the recording electrode was placed closer to a site showing the characteristic nonrespiratory bursting pattern. Bursts in these neurons occur at approximately the same time as bursts (and subsequent pauses) in HVC. In the bottom pair, a respiratory neuron recorded several minutes after the unit on the left shows a complete lack of correlated activity with the same HVC neuron.