Skip to main content
Log in

Innervation of chromatophore muscle fibres in the octopus Eledone cirrhosa

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Cephalopod chromatophores are made of a central pigment cell surrounded by 10 to 20 radially arranged muscle fibres under direct nervous control. Innervation of these muscle fibres was studied with anterograde cobalt fills of peripheral nerve bundles and light and electron microscopy. Individual axons branch repeatedly to innervate the muscles of chromatophores scattered over several millimeters. Axons contained in several dermal nerves converge to innervate the same chromatophores. Among the chromaophores, axons were found running either singly or in small bundles, often accompanied by sheath cells. Single chromatophore muscles were innervated by at least one axon running across or along its length. Since nerves terminating on chromatophore muscles are very rare, neuromuscular contact seems to be made “en passant”. Varicosities of the axons apposed to the muscles are thought to be presynaptic sites. However, morphological differentiations of the pre-or post-synaptic membranes were not visible. Two types of innervating processes were found containing either electron-clear or a mixture of electron-clear and dark-core synaptic vesicles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barrantes FJ (1970) The neuromuscular junctions of a pulmonate mollusc. I: Ultra-structural study. Z Zellforsch Mikrosk Anat 104:205–212

    Google Scholar 

  • Benjamin P, Peat A (1968) Myo-neural junctions in the connective tissue sheath of a molluscan ganglion. Nature 219:1371–1372

    Google Scholar 

  • Boyle PR (1981) Methods for the aquarium maintenance of the common octopus of British waters, Eledone cirrhosa. Lab Anim 15:327–331

    Google Scholar 

  • Boyle PR, Froesch D (1979) The peripheral fields of Octopus stellar nerves. Mar Behav Physiol 6:25–31

    Google Scholar 

  • Brocco SL (1977) The ultrastructure of the epidermis, dermis, iridophores, leucophores and chromatophores of Octopus dofleini martini (Cephalopoda Octopoda). Ph.D. Thesis, University of Washington, Seattle

    Google Scholar 

  • Buhler A, Froesch D, Mangold K, Marthy H-H (1975) On the motor projection of the stellate ganglion in Octopus vulgaris. Brain Res 88:69–72

    Google Scholar 

  • Carew TJ, Pinsker HM, Rubinson K, Kandel ER (1974) Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle in Aplysia. J Neurophysiol 37:1020–1040

    Google Scholar 

  • Cloney RA, Florey E (1968) Ultrastructure of cephalopod chromatophore organs. Z Zellforsch Mikrosk Anat 89:250–280

    Google Scholar 

  • Coggeshall RE (1967) A light and electron microscope study of the abdominal ganglion of Aplysia californica. J Neurophysiol 30:1263–1287

    Google Scholar 

  • Cohen JL, Weiss KR, Kupfermann J (1978) Motor control of buccal muscles in Aplysia. J Neurophysiol 41:157–180

    Google Scholar 

  • Dubas F, Boyle PR (1985) Chromatophore motor units in Eledone cirrhosa (Cephalopoda: Octopoda). J Exp Biol 117:415–432

    Google Scholar 

  • Dubas F, Hanlon RT, Ferguson GP, Pinsker HM (1986a) Localization and stimulation of chromatophore motoneurons in the brain of the squid Lolliguncula brevis. J Exp Biol 121:1–26

    Google Scholar 

  • Dubas F, Leonard R, Hanlon RT (1986b) Chromatophore motoneurons in the brain of Lolliguncula brevis: an HRP study. Brain Res 374:21–29

    Google Scholar 

  • Florey E (1966) Nervous control and spontaneous activity of the chromatophores of a cephalopod, Loligo opalescens. Comp Biochem Physiol 18:305–324

    Google Scholar 

  • Florey E, Cahill MA (1982) The innervation pattern of crustacean skeletal muscle. Cell Tissue Res 224:527–541

    Google Scholar 

  • Florey E, Dubas F, Hanlon RT (1985) Evidence for L-glutamate as transmitter substance of motoneurons innervating squid chromatophore muscles. J Comp Biochem Physiol 82C:259–268

    Google Scholar 

  • Florey E, Kriebel ME (1969) Electrical and mechanical responses of chromatophore muscle fibers of the squid Loligo opalescens, to nerve stimulation and drugs. Z Vergl Physiol 65:98–130

    Google Scholar 

  • Froesch D (1973) On the fine structure of the octopus iris. Z Zellforsch Mikrosk Anat 145:119–129

    Google Scholar 

  • Gerschenfeld HM (1963) Observations on the ultrastructure of synapses of some pulmonate molluscs. Z Zellforsch Mikrosk Anat 60:258–275

    Google Scholar 

  • Heyer CB, Kater SB, Karlsson VL (1973) Neuromuscular systems in molluscs. Am Zool 13:247–270

    Google Scholar 

  • Hill RB, Sanger JW (1974) Anatomy of the innervation and neuromuscular junctions of the radular protractor muscle of the whelk Busycon canaliculatum. Biol Bull 147:369–385

    Google Scholar 

  • Hofmann FB (1907) Histologische Untersuchungen über die Innervation der glatten und der ihr verwandten Muskulatur der Wirbeltiere und Mollusken. Arch Mikr Anat 70:361–413

    Google Scholar 

  • Hofmann FB (1910) Gibt es in der Muskulatur der Mollusken periphere, kontinuierlich leitende Nervennetze bei Abwesenheit von Ganglienzellen? II: Weitere Untersuchungen an den Chromatophoren der Kephalopoden. Pflugers Arch 132:43–81

    Google Scholar 

  • McKenna OC, Rosenbluth J (1973) Myoneuronal and intermuscular junctions in a molluscan smooth muscle. J Ultrastruct Res 42:434–450

    Google Scholar 

  • Mirow S (1972) Skin colour in squids: 1. Chromatophores. Z Zellforsch Mikrosk Anat 125:143–175

    Google Scholar 

  • Onodera K, Takeuchi A (1980) Distribution and pharmacological properties of synaptic and extrasynaptic glutamate receptors on crayfish muscle. J Physiol 306:233–250

    Google Scholar 

  • Palmgren A (1948) A rapid method for selective silver staining of nerve fibers and nerve endings in mounted paraffin sections. Acta Zool (Stockholm) 29:377–392

    Google Scholar 

  • Pantin CFA (1969) Notes on microscopical techniques for zoologists. Cambridge Univ Press, London

    Google Scholar 

  • Prosser CL, Young JZ (1937) Responses of muscles of the squid to repetitive stimulation of the giant nerve fibers. Biol Bull 73:237–241

    Google Scholar 

  • Pumphrey RJ (1938) The double innervation of muscles in the clam (Mya arenarid). J Exp Biol 15:500–505

    Google Scholar 

  • Ramsay JA (1940) A nerve-muscle preparation from the snail. J Exp Biol 17:96–115

    Google Scholar 

  • Rowell CH (1963) Excitatory and inhibitory pathways in the arm of Octopus. J Exp Biol 40:257–270

    Google Scholar 

  • Salpeter MM, Faeder IR (1974) The role of sheath cells in glutamate uptake by insect nerve-muscle preparations. In: Prog Brain Research 34:103–115

    Google Scholar 

  • Sato M, Tamasige M, Ozeki M (1960) Electrical activity of the retractor pharynx muscle of the snail. Japan J Physiol 10:85–98

    Google Scholar 

  • Stephens PS (1971) Histological methods. In: The anatomy of the nervous system of Octopus vulgaris. Young JZ, Clarendon Press Oxford

    Google Scholar 

  • Taraskevich PS, Gibbs D, Schmued L, Orkand RK (1977) Excitatory effects of cholinergic adrenergic and glutaminergic agonists on a buccal muscle of Aplysia. J Neurobiol 8:325–335

    Google Scholar 

  • Ten Cate J (1928) Contribution à la question de l'innervation des chromatophores chez Octopus vulgaris. Arch Neerl Physiol 12:568–599

    Google Scholar 

  • Tyrer NM, Altman JS (1974) Motor and sensory flight neurones in a locust demonstrated using cobalt chloride. J Comp Neurol 157:117–138

    Google Scholar 

  • Weber W (1968) Multiple Innervation der Chromatophorenmuskelzellen von Loligo vulgaris. Z Zellforsch Mikrosk Anat 108:446–456

    Google Scholar 

  • Wilson DM (1960) Nervous control of movement in cephalopods. J Exp Biol 37:57–72

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by a postgraduate award from the University of Aberdeen (GB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dubas, F. Innervation of chromatophore muscle fibres in the octopus Eledone cirrhosa . Cell Tissue Res. 248, 675–682 (1987). https://doi.org/10.1007/BF00216498

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00216498

Key words

Navigation