Innervation of the syrinx of the zebra finch (Taeniopygia guttata)

Abstract

In songbirds, the learning and maintenance of song is dependent on auditory feedback, but little is known about the presence or role of other forms of sensory feedback. Here, we studied the innervation of the avian vocal organ, the syrinx, in the zebra finch. Using a combination of immunohistochemistry, immunofluorescence and neural tracing with subunit B of cholera toxin (CTB), we analysed the peripheral and central endings of the branch of the hypoglossal nerve that supplies the syrinx, the tracheosyringeal nerve. In the syringeal muscles, we show the presence of numerous choline acetyl transferase-like immunoreactive en plaque motor endplates and substance P-like immunoreactive, thin and varicose free nerve endings. Substance P-like immunoreactive free nerve endings were also present in the luminal syringeal tissues, especially in the luminal epithelium of the trachea and pessulus. Also, by a combination of immunofluorescence and transganglionic tracing following injections of CTB in the tracheosyringeal nerve, we identified as central targets of the syringeal receptors the caudolateral part of the interpolaris subnucleus of the descending trigeminal tract, a caudolateral region of the nucleus tractus solitarius, and a lateral band of the principal sensory trigeminal nucleus. Further studies are required to determine the sensory modalities of these receptors and the connections of their specific synaptic targets.

The ascending projections of the nuclei of the descending trigeminal tract (nTTD) in the zebra finch (Taeniopygia guttata)

“…For instance, injections limited to dorsomedial regions of nTTD caudalis, i.e., the mandibular nerve‐recipient region of caudalis (Faunes & Wild, ), labeled medial parts of the trigeminal column and PrV (Figure a–e); whereas injections centered ventrolaterally in nTTD oralis labeled ventrolateral parts of the trigeminal column and PrV (Figure a”–e”). Similarly, an injection in the hypoglossal‐recipient dorsolateral region of nTTD interpolaris and oralis (injection N° 5 in Figure e,f) produced labeling in the other hypoglossal‐recipient regions of the trigeminal column (Wild, ; Faunes et al, ): a cytoarchitectonically distinct oval dorsolateral region of PrV, the lateral nTTD interpolaris and caudalis, and the medial cervical dorsal horn.…”

“…During singing, movements and adoption of different positions of the beak, upper vocal tract, and tongue act to filter the sound produced at the syrinx (Hoese, Podos, Boetticher, & Nowicki, ; Riede, Suthers, Fletcher, & Blevins, ; Ohms, Beckers, Ten Cate, & Suthers, ; Riede, Schilling, & Goller, ; Suthers, Rothgerber, & Jensen, ). In addition, the syrinx itself has sensory receptors that are innervated by fibers that project to the sensory trigeminal nuclei (Bottjer & Arnold, , Faunes et al, ), although the nature of these receptors is not known specifically. Nevertheless, it seems likely that trigeminal sensory feedback could be involved in the control of singing (Bottjer & To, ).…”

The sensory trigeminal complex and the organization of its primary afferents in the zebra finch (Taeniopygia guttata)

“…To visualize the hypoglossal projection to the trigeminal nuclei, we injected the lingual branch of the hypoglossal nerve (XIIl). As shown in an accompanying article (Faunes et al, ), the projection of the tracheosyringeal branch of the hypoglossal nerve to the sensory trigeminal complex is relatively small; it includes a dorsolateral portion of caudal nTTDi and a thin lateral band of the dorsolateral PrV.…”

“…While most of nTTDi has small cells of similar coronal section diameter as nTTDc (Figure b, c), the lateral part of nTTDi has clusters of cells that are intermingled with the fibers of TTD, and appear to be larger in the coronal plane (black arrowheads in Figure d, e), as reflected by differences in the mean coronal cell diameters (Figure c, d; 8.918 ± 2.1 µm in the medial region vs. 12.01 ± 3.227 µm in the lateral region, ANOVA with Tukey's multiple comparisons, p < .05). In the caudo‐lateral part of nTTDi there are patches of substance P‐like immunoreactive fiber endings (white arrowheads in Figure d”), that originate from syringeal receptors (Faunes et al, ).…”

“…Studies addressing the cytoarchitecture and organization of afferent input to the sensory trigeminal complex, including both PrV and nTTD, have been performed only in pigeons and ducks (Dubbeldam & Karten, ; Dubbeldam, ; Arends & Dubbeldam, ; Wild & Zeigler, ). In the present work, we extended this analysis to the zebra finch, to contribute to a comparative view of this system among avian species, and to set the grounds for analyzing the ascending connections of the nTTD (Faunes & Wild, ) and of the central projections of the sensory component of the tracheosyringeal nerve (Faunes et al, ). The overall organization of the sensory trigeminal nuclei of the zebra finch is similar to that found in other avian species.…”