Electroreceptors and Mechanosensory Lateral Line Organs Arise from Single Placodes in Axolotls

Abstract

The lateral line system in salamanders consists of mechanoreceptive neuromasts and pit organs, distributed in lines on the head and trunk, and electroreceptive ampullary organs located adjacent to the cephalic lines of mechanoreceptors. Although numerous studies have documented that neuromast and pit organs and the cranial nerves that innervate these receptors arise from a dorsolateral series of placodes, there is no agreement concerning the number of these placodes, the specific groups of receptors that arise from them, or the embryonic origin of ampullary organs. A developmental model was recently proposed (Northcutt et al., 1994) in which all these placodes, except for the most posterior one, elongate to form sensory ridges whose central zones initially form neuromast and pit organ primordia and whose lateral zones subsequently form ampullary primordia. To test this model, individual placodes were unilaterally extirpated, or placodes from pigmented wild-type axolotl embryos were homotopically or heterotopically transplanted into albino hosts. Extirpation resulted in the loss of all three receptor classes, and both homotopic and heterotopic transplants produced pigmented receptors of all three classes in albino hosts. The receptors in the heterotopic transplants still formed lines which occasionally retained their normal orientation despite differentiating in an ectopic environment. These experiments demonstrated that, as previously postulated, specific lines of neuromasts and pit organs do arise from each placode, and ampullary organs also arise from many of the same placodes. The distribution of receptors that develop following incomplete extirpation or heterotopic transplantation also indicates that each placode is patterned regarding receptor classes and orientation prior to sensory ridge formation.

Molecular analysis of neurogenic placode development in a basal ray‐finned fish

“…This result is compatible with, though does not prove, a lateral line placode origin for actinopterygian ampullary organs. If true, this would in turn support a lateral line placode origin for ampullary organs in all bony fish, given that ampullary organs are lateral line placode-derived in sarcopterygians (Northcutt et al, 1995). To prove a lateral line placode origin for paddlefish ampullary organs, however, in vivo fate mapping or labeling studies must be performed during stages of lateral line placode formation and elongation.…”

“…Ampullary organs and the electrosensory hair cells within them were conclusively shown to be derived from lateral line placodes in a tetrapod, the axolotl Ambystoma mexicanum (a urodele amphibian), using fate-mapping and ablation studies (Northcutt et al, 1995). In the shark Scyliorhinus canicula, electrosensory hair cells were proposed to be neural crest-derived owing to their expression of Sox8 and the carbohydrate epitope recognized by the HNK1 antibody (Freitas et al, 2006).…”

“…Shark electrosensory hair cells were recently proposed, on the basis of gene expression alone, to be derived from the neural crest (Freitas et al, 2006). However, in a tetrapod, the axolotl Ambystoma mexicanum (a urodele amphibian), fate-mapping and ablation studies showed that ampullary organs and the electrosensory hair cells within them arise from lateral line placodes (Northcutt et al, 1995). Lateral line placodes (of which primitively there are six pairs: three pre-otic and three post-otic; Northcutt, 1997) give rise to lateral line primordia that elongate or migrate over the head and trunk and deposit characteristic lines of sense organs called neuromasts, which contain mechanosensory hair cells innervated (like electrosensory hair cells) by lateral line placode-derived neurons (reviewed in Baker et al, 2008;Ghysen and Dambly-Chaudière, 2007;Ma and Raible, 2009;Schlosser, 2002).…”

Molecular Conservation and Novelties in Vertebrate Ear Development

“…The literature is filled with suggestions that cell fate commitment occurs after either central or peripheral contacts are established (Gompel et al, 2001;Northcutt et al, 1995). Alternatively, it seems possible that primary sensory neuron cell fate determination starts in the otocyst prior to delamination.…”

Homeobox genes in axolotl lateral line placodes and neuromasts

“…3D, dots) and Dlx-3 (not shown). The electroreceptive ampullary organs of the lateral line form along the margins of the same placodal epithelium from which mechanoreceptors develop (except the posterior placode, which does not produce electroreceptors), starting after most of the primary neuromasts have already erupted, at about stage 42 (Northcutt et al 1995). The ampullary organs show some expression of Msx-2 and Dlx-3, but it is less intense and does not show the same localization within the organ as expression in neuromasts (data not shown).…”