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Direct observation of syringeal muscle function in songbirds and a parrot

Ole Næsbye Larsen* and Franz Goller{dagger}

Centre for Sound Communication, Institute of Biology, SDU-Odense University, DK-5230 Odense M, Denmark and Medical Sciences Program, Indiana University, Bloomington, IN 47405, USA
{dagger} Present address: Department of Biology, University of Utah, 257 South, 1400 East, Salt Lake City, UT 84112, USA



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  		Fig. 1. The songbird tracheobronchial syrinx is a complex bipartite structure situated where the connecting tubes to the lungs (the bronchi) join the windpipe (the trachea). (A) Schematic ventro-lateral external view of a songbird syrinx depicting the syringeal muscles. To illustrate the position of the angioscope used for internal views, parts of the trachea have been removed; the yellow colour indicates endoscope light. The external angioscope indicates the viewing angle in Fig. 4. (B) Schematic horizontal section through a songbird syrinx illustrating the two labial sound sources and the approximate position and field of view of the angioscope (yellow light) in Fig. 3. (For the syringeal views in Fig. 2, the angioscope was advanced towards the left side of the syrinx.) BC, bronchial cartilage; 3B, third bronchial cartilage; BL, bronchial lumen; dS, m. syringealis dorsalis; dTB, m. tracheobronchialis dorsalis; ICM, membrane of the interclavicular air sac; LL, lateral labium; M, syringeal muscle; ML, median labium; MTM, median tympaniform membrane; SM, semilunar membrane; ST, m. sternotrachealis; T, trachea; TL, m. tracheolateralis; TY, tympanum (consisting of four closely apposed or fused tracheosyringeal cartilages); vS, m. syringealis ventralis; vTB, m. tracheobronchialis ventralis.

 


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  		Fig. 2. Internal view through the trachea of the left side of the cardinal syrinx illustrating the effect of electrical stimulation of the ipsilateral muscles shown in the insets to the right. (a–d) Simultaneous stimulation of the m. tracheobronchialis dorsalis (dTB) and m. syringealis dorsalis (dS). In the respiratory position (a,d), the medial (ML) and lateral (LL) labia do not protrude far into the bronchial lumen (BL). Upon strong stimulation, they are adducted (move into the BL), but do not touch and close the aperture (b,c). The arrowheads outline the visible portions of the ML (white) and LL (yellow) and indicate labial extension into the bronchial lumen. When stimulation is terminated, the labia move back into the respiratory position. (e,f) Stimulation of the medial portion of the m. syringealis dorsalis (dS) alone mainly affects the ML, which is moved slightly into the lumen. White arrowheads indicate the change from the respiratory (e) to the stimulated (f) position. dS contraction may also result in a rostro-caudal stretching of the ML suggested by a change in the light reflection pattern in the video. (g,h) Stimulation of the left m. tracheobronchialis ventralis (vTB) causes abduction (movement out of the bronchial lumen) of the left LL but does not noticeably affect the position of the ML. In comparison with the opening before stimulation, the aperture of the bronchus is increased by movement of the LL in the caudo-lateral direction (downwards) in h. D, dorsal side; V, ventral side. SM, semilunar membrane.

 


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  		Fig. 3. Electrical stimulation of m. syringealis ventralis (vS), the largest syringeal muscle in songbirds, does not noticeably change the aperture of the bronchus from the respiratory (a) to the stimulated (b) position. However, upon stimulation, a twitching motion of the medial labium is apparent in the video, suggesting that stretching of the medial labium along the rostro-caudal axis may occur (yellow arrowheads). Angioscope position approximately as illustrated in Fig. 1B. D, dorsal side; V, ventral side; BL, bronchial lumen; LL, lateral labium; ML, median labium; SM, semilunar membrane.

 


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  		Fig. 4. Sequence of ventral outside views of the brown thrasher syrinx during the transition from quiet respiration (a), via reconfiguration in preparation for phonation (b), to phonation (c) and return to the starting point (d) induced by electrical brain stimulation. The sequence illustrates the striking rostrad movement during sound production. To illustrate the movement, red arrowheads mark the caudal end of the syringeal midline and blue arrowheads outline the third bronchial cartilage. The movement results in significant stretching of connective tissue in the bronchial section, including the medial tympaniform membranes (the white dotted line outlines the medial edges of the median tympaniform membrane). B, bronchial cartilage; vS, m. syringealis ventralis; vTB, m. tracheobronchialis ventralis.

 


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  		Fig. 5. The cockatiel syrinx is situated at the distal end of the trachea cranial to the bronchi. (A) Schematic external ventral view of the cockatiel syrinx depicting the syringeal muscles and the inserted angioscope. Note the slightly asymmetric m. sternotrachealis (ST). (B) Schematic left-side view illustrating the extent of the paired protrusions (PP). (C) Schematic horizontal section through the cockatiel syrinx with the approximate position and field of view of the angioscope (yellow light) in Figs 6a–f and 7. SP, m. syringealis profundus; SS, m. syringealis superficialis; BC, bronchial cartilage; T, trachea; TL, m. tracheolateralis; TY, tympanum (consisting of four closely apposed or fused tracheosyringeal cartilages); LTM, lateral tympaniform membrane.

 


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  		Fig. 6. Internal view through the trachea (a–f) and external view along the trachea (g–i) of the cockatiel syrinx illustrating the effects of electrical stimulation of the muscles shown in the insets to the right. (a,c,d,f) During quiet respiration, the cranially arching lateral tympaniform membranes (LTMs) of the cockatiel syrinx are positioned in the tracheal lumen, forming a dorso-ventral slot (S). (b) Stimulation of the right m. syringealis superficialis (SS) adducts the ipsilateral LTM (left in picture) into the middle of the tracheal lumen, narrowing S (yellow arrowheads). (e) Stimulation of the left m. syringealis profundus (SP) abducts the ipsilateral LTM (right in picture) from the tracheal lumen, widening S (yellow arrowheads). (g–i) The same situation viewed from the outside caudally along the tracheal axis (see inset). Stimulation of the left SP (h) abducts the ipsilateral member of the paired protrusions (PP) (red arrowheads) as it is drawn cranio-laterad. When stimulation is terminated, the left PP move back into the respiratory position (i). D, dorsal side; V, ventral side.

 


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  		Fig. 7. Electrical stimulation at high intensity of the cockatiel’s right tracheosyringeal nerve cranial to the common anastomosis produces a vigorous bilateral abduction of the lateral tympaniform membranes (LTM) (yellow arrowheads). (a) Quiet breathing. (b) Nerve stimulation. Note the four tracheosyringeal cartilages (TC) below the LTM extending towards the bronchial divide. (c) Return to quiet breathing. D, dorsal side; V, ventral side; S, dorso-ventral slot; SP, m. syringealis profundus.

 

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© The Company of Biologists Ltd 2002