Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): I. Neuroanatomy and physiology

Abstract

Molecules present in an animal's environment can indicate the presence of predators, food, or sexual partners and consequently, induce migratory, reproductive, foraging, or escape behaviors. Three sensory systems, the olfactory, gustatory, and solitary chemosensory cell (SCC) systems detect chemical stimuli in vertebrates. While a great deal of research has focused on the olfactory and gustatory system over the years, it is only recently that significant attention has been devoted to the SCC system. The SCCs are microvillous cells that were first discovered on the skin of fish, and later in amphibians, reptiles, and mammals. Lampreys also possess SCCs that are particularly numerous on cutaneous papillae. However, little is known regarding their precise distribution, innervation, and function. Here, we show that sea lampreys (Petromyzon marinus L.) have cutaneous papillae located around the oral disk, nostril, gill pores, and on the dorsal fins and that SCCs are particularly numerous on these papillae. Tract‐tracing experiments demonstrated that the oral and nasal papillae are innervated by the trigeminal nerve, the gill pore papillae are innervated by branchial nerves, and the dorsal fin papillae are innervated by spinal nerves. We also characterized the response profile of gill pore papillae to some chemicals and showed that trout‐derived chemicals, amino acids, and a bile acid produced potent responses. Together with a companion study (Suntres et al., Journal of Comparative Neurology, this issue), our results provide new insights on the function and evolution of the SCC system in vertebrates.

Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): II. Ontogeny and immunocytochemical characterization of solitary chemosensory cells

“…The companion paper to this study has shown that lamprey SCCs on gill pores respond to dead trout water, amino acids and taurocholic acid in electrophysiological recording experiments (Daghfous et al, ). These responses suggest that the gill pore SCCs are useful during feeding.…”

“…planeri . While Baatrup and Døving () and Daghfous et al () have shown neural chemosensory responses in these gill papillae, it is possible that the lamprey SCC activity may also extend to nonneural signaling mechanisms. For example, chemicals emitted by bacteria stimulate a non‐neural antimicrobial innate immune defense response in mammalian SCCs (e.g., Lee et al, 2017).…”

“…planeri ) and the European river lamprey ( Lampetra fluviatilis ), single nerve fibers are positioned adjacent to microvillous epidermal cells on papillae on the mouth, gill pores, dorsal tail fin, male genitalia (Whitear & Lane, ) and nerve fiber recordings have shown chemosensory responses in oral disc papillae (Baatrup & Døving, ). A companion paper on sea lampreys ( Petromyzon marinus L.) in this issue (Daghfous et al, ), showed numerous SCCs on cutaneous papillae located around the oral disc, nostril, gill pores, and on the dorsal fins; that these papillae are innervated by the cranial or spinal nerves, and that gill pore papillae respond to the application of trout‐derived extracts as well as to some amino acids and to taurocholic acid. The immunocytochemical characterization of these SCCs and associated nerve fibers, as well as their abundance during the different life‐stages remain to be determined and are the subject of the present study.…”

“…The present study examined lamprey gill pore SCCs by investigating innervated microvillous epithelial cells located on gill pore papillae and by labeling with antibodies against calretinin and phospholipase C. Abundance during the morphologically distinct phases of the lamprey's life cycle was also examined, as gill ventilation changes from unidirectional to tidal, and feeding takes place during a separate phase from reproduction. A companion study (Daghfous et al, ) examines the neuroanatomy and chemosensory activity of fibers innervating the papillae. These findings contribute to an increasing understanding of the organization and function of the vertebrate solitary chemosensory system.…”

Expression of Urocortin 3 mRNA in the Central Nervous System of the Sea Lamprey Petromyzon marinus

“…A comparison between adults and larvae revealed important developmental changes in Ucn3 expression, with new positive populations appearing in the striatum, torus semicircularis, isthmus and nucleus of the solitary tract after the metamorphosis. Transformation in the sea lamprey is complex, and in the nervous system, it largely affects the visual system including the eye and optic tectum [36][37][38][39][40][41], but also other neural systems such as the medial pallium, cutaneous sensory systems and the olfactory rosette [42][43][44]. Other body organs also suffer important anatomical and physiological changes during transformation to adapt adult lampreys to a new adult life-style (free and ectoparasitic life), which is very different from the blind, burrowing, water-filtering larvae [31].…”