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

J Comp Neurol. 2020 Mar 1;528(4):664-686. doi: 10.1002/cne.24787. Epub 2019 Oct 21.

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.

Keywords: Merkel cells; lamprey; microvilli; papillae; solitary chemosensory cells; taste.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Epidermis / anatomy & histology*
  • Epidermis / chemistry
  • Epidermis / physiology*
  • Epithelium / anatomy & histology
  • Epithelium / chemistry
  • Epithelium / physiology
  • Female
  • Male
  • Petromyzon / anatomy & histology*
  • Petromyzon / physiology*
  • Sensory Receptor Cells / chemistry
  • Sensory Receptor Cells / physiology*
  • Skin / anatomy & histology
  • Skin / chemistry
  • Skin / ultrastructure

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