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

Abstract

Our knowledge of the avian sensory trigeminal system has been largely restricted to the principal trigeminal nucleus (PrV) and its ascending projections to the forebrain. Studies addressing the cytoarchitecture and organization of afferent input to the sensory trigeminal complex, which includes both the PrV and the nuclei of the descending trigeminal tract (nTTD), have only been performed in pigeons and ducks. Here we extend such an analysis to a songbird, the zebra finch (Taeniopygia guttata). We describe the cytoarchitecture of the sensory trigeminal complex, the patterns of calbindin-like and substance P-like immunoreactivity, and the organization of afferents from the three branches of the trigeminal nerve and from the lingual branch of the hypoglossal nerve. On the basis of cytoarchitecture and immunohistochemistry, the sensory trigeminal column can be subdivided from caudal to rostral, as in other species, into cervical dorsal horn, subnucleus caudalis, subnucleus interpolaris, subnucleus oralis, and nucleus principalis. The relative positions of the terminal fields of the three trigeminal branches move from medial to lateral in the dorsal horn to dorsomedial to ventrolateral in nTTD, whereas in PrV there is considerable overlap of mandibular and ophthalmic terminal fields, with only a small maxillary input ventrally. The hypoglossal afferents, which terminate medially in the dorsal horn and dorsolaterally in nTTD, terminate in specific cell groups in the dorsolateral nTTDo and in PrV. This work sets the grounds for further analyses of the ascending connections of the nTTD and the afferents from the syrinx to the trigeminal sensory column.

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

“…Primary afferent terminals were transganglionically labeled in the ipsilateral sensory trigeminal nuclei (nTTD and principal nucleus [PrV]), and in the nucleus of the solitary tract (nTS). Labeling in the trigeminal complex was consistent across cases: in the nTTD, labeled terminals were located in the caudolateral part of the interpolaris subdivision (nTTDi, Faunes & Wild, ), and in the principal trigeminal nucleus, it was restricted to a thin band on its lateral aspect (Figures and ), which lies just lateral to the terminal fields of the lingual branch of the hypoglossal (XII) nerve (Bottjer & Arnold, ; Faunes & Wild, ; Wild, ). Labeling in the nucleus of the solitary tract was more variable.…”

“…The central projections of the tracheosyringeal receptors described here represent a small portion of the previously described hypoglossal terminal fields, most of which derive from lingual mechanoreceptors, and include a continuous rostro‐caudal column spanning the brainstem from the medial cervical dorsal column to the lateral half of PrV (Bottjer & Arnold, ; Faunes & Wild, ; Wild, ). A hypoglossal projection to the lateral region of the nTS has also been described for the lingual nerve by Wild (), but not by Bottjer & Arnold ().…”

“…The syringeal motoneurons send their axons to the syrinx through the tracheosyringeal hypoglossal nerve (ts nerve). Through this nerve also travel afferent fibers of cell bodies located in the jugular vagal ganglion, the central projections of which project to the trigeminal sensory complex together with lingual hypoglossal afferents (Bottjer & Arnold, ; Faunes & Wild, ; Wild, ). However, the sensory endings of the syringeal receptors have not yet been described, and their specific trigeminal targets have not been distinguished from the lingual afferent terminal fields.…”

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

“…The cytoarchitecture of nTTD of the zebra finch is described in an accompanying article (Faunes & Wild, ). The nTTD can be subdivided, following the nomenclature used in mammals (Olszewski, ), into three subnuclei along the rostro‐caudal axis: caudalis, interpolaris, and oralis.…”

“…At the dorsolateral side of oralis there is a group of cells that receives lingual hypoglossal afferents (Wild, ). Oralis extends rostrally up to the caudoventral aspect of the entrance of Vs (Faunes & Wild, ).…”