Anatomy and Ontogeny of a Novel Hemodynamic Organ in Zebrafish

Abstract

The zebrafish maxillary barbel can protract and retract in response to stimuli, and appears connected to a prominent blood sinus on the lateral aspect of the maxillary bone. However, the mechanism of barbel movement is not described. Using whole-mount phalloidin staining of the sinus region, we observed long filamentous actin cables, suggesting highly organized vascular smooth muscle cells, surrounding an endothelial chamber. Although the chamber is variably filled by erythrocytes in vivo, cardiac injection of fluorescent dextrans shows that it consistently contains plasma. Full-thickness confocal imaging of dextran-injected adults containing EGFP+ endothelial cells revealed a vascular complex with three compartments, here named the distal bulb, central chamber, and accessory chamber. The early ontogeny of all three compartments was confirmed in a whole-mount series of Tg(fli1a:EGFP) juveniles. In wild type adults, the fine structure of each chamber was studied using paraffin- and plastic-section histochemistry and transmission electron microscopy. The distal bulb and central chamber have smooth muscle coats with luminally-elongated septa, forming semi-detached blood-filled lacunae. The central chamber walls and septa are extensively innervated by small, unmyelinated axons, as confirmed by immunohistochemical detection of acetylated tubulin, a component of axonal cytoplasm. The accessory chamber appears neither innervated nor muscularized, but is an endothelial cul-de-sac with a thickened elastic adventitia, suggesting an extensible fluid reservoir. We propose that we have identified a new organ in zebrafish, the maxillary barbel blood sinus, whose neurovascular specializations may contribute to zebrafish sensory biology and appendage control.