Molecular Basis of Chemotactile Sensation in Octopus

Cell. 2020 Oct 29;183(3):594-604.e14. doi: 10.1016/j.cell.2020.09.008.

Abstract

Animals display wide-ranging evolutionary adaptations based on their ecological niche. Octopuses explore the seafloor with their flexible arms using a specialized "taste by touch" system to locally sense and respond to prey-derived chemicals and movement. How the peripherally distributed octopus nervous system mediates relatively autonomous arm behavior is unknown. Here, we report that octopus arms use a family of cephalopod-specific chemotactile receptors (CRs) to detect poorly soluble natural products, thereby defining a form of contact-dependent, aquatic chemosensation. CRs form discrete ion channel complexes that mediate the detection of diverse stimuli and transduction of specific ionic signals. Furthermore, distinct chemo- and mechanosensory cells exhibit specific receptor expression and electrical activities to support peripheral information coding and complex chemotactile behaviors. These findings demonstrate that the peripherally distributed octopus nervous system is a key site for signal processing and highlight how molecular and anatomical features synergistically evolve to suit an animal's environmental context.

Keywords: chemosensation; evolution; ion channels; neuroethology; neuroscience; octopus; sensory physiology; signal transduction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Amino Acid Sequence
  • Animals
  • Behavior, Animal
  • Chemoreceptor Cells / metabolism*
  • Female
  • HEK293 Cells
  • Humans
  • Octopodiformes / anatomy & histology
  • Octopodiformes / genetics
  • Octopodiformes / physiology*
  • Receptors, Cell Surface / chemistry
  • Receptors, Cell Surface / metabolism
  • Receptors, Cholinergic / metabolism
  • Signal Transduction
  • Touch / physiology*

Substances

  • Receptors, Cell Surface
  • Receptors, Cholinergic
  • Acetylcholine