From synaptic input to muscle contraction: Arm muscle cells of Octopus vulgaris show unique neuromuscular junction and excitation-contraction coupling properties

Nir Nesher, Federica Maiole, Tal Shomrat, Benyamin Hochner, Letizia Zullo

Research output: Contribution to journalArticlepeer-review

Abstract

The muscular-hydrostat configuration of octopus arms allows high man-oeuvrability together with the efficient motor performance necessary for its multitasking abilities. To control this flexible and hyper-redundant system the octopus has evolved unique strategies at the various levels of its brain-to-body organization. We focus here on the arm neuromuscular junction (NMJ) and excitation-contraction (E-C) properties of the arm muscle cells. We show that muscle cells are cholinergically innervated at single eye-shaped locations where acetylcholine receptors (AChR) are concentrated, resembling the vertebrate neuromuscular endplates. Na+ and K+ contribute nearly equally to the ACh-activated synaptic current mediating membrane depolarization, thereby activating voltage-dependent L-type Ca2+ channels. We show that cell contraction can be mediated directly by the inward Ca2+ current and also indirectly by calcium-induced calcium release (CICR) from internal stores. Indeed, caffeine-induced cell contraction and immuno-histochemical staining revealed the presence and close association of dihydropyridine (DHPR) and ryanodine (RyR) receptor complexes, which probably mediate the CICR. We suggest that the dynamics of octopus arm contraction can be controlled in two ways; motoneurons with large synaptic inputs activate vigorous contraction via activation of the two routs of Ca2+ induced contraction, while motoneurons with lower-amplitude inputs may regulate a graded contraction through frequency-dependent summation of EPSP trains that recruit the CICR. Our results thus suggest that these motoneuronal pools are likely to be involved in the activation of different E-C coupling modes, thus enabling a dynamics of muscles activation appropriate for various tasks such as stiffening versus motion generation.

Original languageEnglish
Article number1278
JournalProceedings of the Royal Society B: Biological Sciences
Volume286
Issue number1909
DOIs
Publication statusPublished - Jan 1 2019

Keywords

  • ACh receptors
  • Cephalopods
  • CICR
  • Dihydropyridine
  • E-C coupling
  • Neuromuscular junction
  • Ryanodine

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Environmental Science(all)
  • Agricultural and Biological Sciences(all)

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