Myogenic activity and serotonergic inhibition in the chromatophore network of the squid Dosidicus gigas (family Ommastrephidae) and Doryteuthis opalescens (family Loliginidae)

J Exp Biol. 2017 Dec 15;220(Pt 24):4669-4680. doi: 10.1242/jeb.164160. Epub 2017 Oct 23.

Abstract

Seemingly chaotic waves of spontaneous chromatophore activity occur in the ommastrephid squid Dosidicus gigas in the living state and immediately after surgical disruption of all known inputs from the central nervous system. Similar activity is apparent in the loliginid Doryteuthis opalescens, but only after chronic denervation of chromatophores for 5-7 days. Electrically stimulated, neurally driven activity in intact individuals of both species is blocked by tetrodotoxin (TTX), but TTX has no effect on spontaneous wave activity in either D. gigas or denervated D. opalescens Spontaneous TTX-resistant activity of this sort is therefore likely myogenic, and such activity is eliminated in both preparations by serotonin (5-HT), a known inhibitor of chromatophore activity. Immunohistochemical techniques reveal that individual axons containing L-glutamate or 5-HT (and possibly both in a minority of processes) are associated with radial muscle fibers of chromatophores in intact individuals of both species, although the area of contact between both types of axons and muscle fibers is much smaller in D. gigas Glutamatergic and serotonergic axons degenerate completely following denervation in D. opalescens Spontaneous waves of chromatophore activity in both species are thus associated with reduced (or no) serotonergic input in comparison to the situation in intact D. opalescens Such differences in the level of serotonergic inhibition are consistent with natural chromogenic behaviors in these species. Our findings also suggest that such activity might propagate via the branching distal ends of radial muscle fibers.

Keywords: Chromatophore; Denervation; Excitability; Ommastrephid; Serotonin; Squid.

MeSH terms

  • Animals
  • Axons / ultrastructure
  • Chromatophores / metabolism*
  • Chromatophores / physiology
  • Chromatophores / ultrastructure
  • Decapodiformes / metabolism
  • Decapodiformes / physiology*
  • Decapodiformes / ultrastructure
  • Electric Stimulation
  • Image Processing, Computer-Assisted
  • Immunohistochemistry
  • In Vitro Techniques
  • Muscles / innervation
  • Muscles / physiology
  • Muscles / ultrastructure