Skip to main content Accessibility help
×
Home

The chromatic and motor effects of neurotransmitter injection in intact and brain-lesioned Octopus

  • P. L. R. Andrews (a1), J. B. Messenger (a2) and E. M. Tansey (a3)

Abstract

Various neurotransmitters were injected into the blood supplying the brain of Octopus vulgaris and the effects, particularly on the chromatophores, were observed. l-glutamate, GABA, dopamine, noradrenaline and octopamine caused expansion of the chromatophores and darkening of the skin; ACh caused retraction of the chromatophores and paling; 5HT caused differential expansion and retraction: mottling. These responses, which are neurally mediated, were particularly well defined for ACh and 5HT and the effects of these drugs were studied in more detail. The paling effect of ACh was mimicked by nicotine but not muscarine and was partially antagonized by tubocurarine. The mottling induced by 5HT was transiently antagonized by methysergide maleate, as was ink-ejection and defaecation. Brain lesions to localize the sites of action of ACh and 5HT suggest that they act at the level of the sub-oesophageal lobes to control the chromatophores, but that 5 HT may act at the level of the optic lobe to control inking and defaecation. These results are related to the pharmacology and histochemistry of the cephalopod brain and to the organization of the chromatophore control system.

Copyright

References

Hide All
Andrews, P. L. R., Messenger, J. B. & Tansey, E. M., 1981. Colour changes in cephalopods after neurotransmitter injection into the cephalic aorta. Proceedings of the Royal Society (B), 213, 93‐99.
Andrews, P. L. R., Packard, A. & Tansey, E. M., 1982. A physiologically discrete population of chromatophores in Octopus vulgaris (Mollusca). Journal of Zoology, 198, 131140.
Andrews, P. L. R. & Tansey, E. M., 1982 a. A technique for central drug administration in Octopus vulgaris. Journal of Neuroscience Methods, 4, 243247.
Andrews, P. L. R. & Tansey, E. M., 1981 b. The effects of some anaesthetic agents in Octopus vulgaris. Comparative Biochemistry and Physiology, 70 C, 241247.
Andrews, P. L. R. & Tansey, E. M., 1983. The digestive tract of Octopus vulgaris: the anatomy, physiology and pharmacology of the upper tract. Journal of the Marine Biological Association of the United Kingdom, 63, 109134.
Bacq, Z. M. & Mazza, F. P., 1935 a. Recherches sur la physiologie et la pharmacologie du système nerveux autonome. XVIII. Isolément de chloro-aurate d'acetylcholine à partir d'un extrait de cellules nerveuses d' Octopus vulgaris. Archives internationales de physiologie et de biochimie, 42, 4346.
Bacq, Z. M. & Mazza, F. P., 1935 b. Identification d'acétylcholine extraite des cellules ganglion-naires d' Octopus. Compte rendu des séances de la Société de biologie, 120, 246247.
Baret, R., Morgue, M., Broc, A. & Charmot, J., 1965. Etude comparative de la désamidination de l’acide γ-guanido-butyrique, et de l'arginine par l'hépatopancréas ou le foie de divers Invertébrés. Compte rendu des séances de la Société de biologie, 159, 24462450.
Barlow, J. J., 1977. Comparative biochemistry of the central nervous system. Symposia of the Zoological Society of London, no. 38, 325346.
Boldyrev, A. A. & Lebedev, A. V. 1972. Precursors of histidine dipeptides in molluscan tissues. Comparative Biochemistry and Physiology, 41 B, 453456.
Bone, Q. & Howarth, J. V., 1980. The role of L-glutamate in neuro-muscular transmission in some molluscs. Journal of the Marine Biological Association of the United Kingdom, 60, 619626.
Bone, Q., Packard, A. & Pulsford, A. L., 1982. Cholinergic innervation of muscle fibres in squid. Journal of the Marine Biological Association of the United Kingdom, 62, 193199.
Boycott, B. B., 1953. The chromatophore system of cephalopods. Proceedings of the Linnean Society of London, 164, 235240.
Boycott, B. B., 1961. The functional organisation of the brain of the cuttlefish, Sepia officinalis. Proceedings of the Royal Society (B), 153, 503534.
Chichery, R. & Chanelet, J., 1972. Action de l'acétylcholine et de diverses substances curarisantes surle systmènerveux de la seiche. Compte rendu des séances de la Société de biologie, 166, 273276.
Cloney, R. A. & Florey, E., 1968. Ultrastructure of cephalopod chromatophore organs. Zeitschrift für Zellforschung und mikroskopische Anatomie, 89, 250280.
Cory, H. T., 1969. Comparative Metabolic Studies in Octopus and Rat Brain. Ph.D. Thesis, University of London.
Cory, H. T. & Rose, S. P. R., 1969. Glucose and amino acid metabolism in octopus optic and vertical lobes in vitro. Journal of Neurochemistry, 16, 979988.
Covelli, V., Memo, M., Spano, P. F. & Trabucchi, M., 1981. Characterization of dopamine receptors in various species of invertebrates and vertebrates. Neuroscience, 6, 20772079.
Dale, H. H., 1954. The beginnings and the prospects of neurohumoral transmission. Pharmacological Reviews, 6, 713.
Feldman, J. L. & Dowdall, M. J., 1973. 5-hydroxytryptamine: an uptake mechanism in synaptosomes from the optic lobe of squid (Loligo pealeii). Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 145, 432433.
Florey, E., 1966. Nervous control and spontaneous activity of the chromatophores of a cephalopod, Loligo opalescens. Comparative Biochemistry and Physiology, 18, 305324.
Florey, E. & Kriebel, M. E., 1969. Electrical and mechanical responses of chromatophore muscle fibres of the squid, Loligo opalescens, to nerve stimulation and drugs. Zeitschrift für vergleichende Physiologie, 65, 98130.
Goodman, L. S., Gilman, A. G. & Gilman, A. (eds.), 1980. Goodman and Gilman's The Pharmacological Basis of Therapeutics, 6th ed.1843 pp. New York: Macmillan.
Gould, R. M. & Cottrell, G. A., 1974. Putrescine in molluscs: identification and occurrence in neurones and other tissues. Comparative Biochemistry and Physiology, 48 B, 591597.
Heilbronn, E., Hause, S. & Lundgren, G., 1971. Chemical identification of acetylcholine in squid-head ganglion. Brain Research, 33, 431437.
Juorio, A. V., 1971. Catecholamines and 5-hydroxytryptamine in nervous tissue of cephalopods. Journal of Physiology, 216, 215226.
Juorio, A. V. & Molinoff, P. B., 1971. Distribution of octopamine in nervous tissues of Octopus vulgaris. British Journal of Pharmacology, 43, 438439P.
Juorio, A. V. & Molinoff, P. B., 1974. The normal occurrence of octopamine in neural tissues of the Octopus and other cephalopods. Journal of Neurochemistry, 22, 271280.
Kato, G. & Tattrie, B., 1974. Solubilization of the acetylcholine receptor protein from Loligo Opalescens without detergents. Federation of European Biochemical Societies Letters, 48, 2631.
Kleinschuster, S. J. & Morris, J. E., 1972. Glutamine synthetase, an enzyme characteristic of vertebrate systems in invertebrate tissues. Experientia, 28, 11571158.
Laverack, M. S., 1980. Electrophysiology of the isolated central nervous system of the northern octopus Eledone cirrhosa. Marine Behaviour and Physiology, 7, 155169.
Leake, L. & Walker, R. J., 1980. Invertebrate Neuropharmacology. 358 pp. London: Blackie.
Lewis, P. R., 1952. The free amino acids of invertebrate nerve. Biochemical Journal, 52, 330338.
Loe, P. R. & Florey, E., 1966. The distribution of acetylcholine and cholinesterase in the nervous system and in innervated organs of Octopus dofleini. Comparative Biochemistry and Physiology, 17, 509522.
Mann, E. & Enna, S. J., 1980. Phylogenetic distribution of bicuculline-sensitive γ-amino-butyric acid (GABA) receptor binding. Brain Research, 184, 367373.
Martin, R., Froesch, D., Weber, E. & Voigt, K. H., 1979. Metenkephalin-like immunoreactivity in a cephalopod neurohemal organ. Neuroscience Letters, 15, 253257.
Matus, A. I., 1973. Histochemical localization of biogenic monoamines in the cephalic ganglia of Octopus vulgaris. Tissue and Cell, 5, 591601.
Messenger, J. B., 1967. The peduncle lobe: a visuo-motor centre in Octopus. Proceedings of the Royal Society (B), 167, 225251.
Messenger, J. B., 1979. The eyes and skin of Octopus: compensating for sensory deficiencies. Endeavour, 3, 9298.
Miledi, R., 1972. Synaptic potentials in nerve cells of the stellate ganglion in the squid. Journal of Physiology, 225, 501514.
Mislin, H., 1955. Die rhythmischer Spontanentladungen in Zentralnervensystem der Tintenfische. Acta medica scandinavica Supplementum, 307, 152158.
Nachmansohn, D. & Weiss, M. S., 1948. Studies on choline acetylase. IV. Effect of citric acid. Journal of Biological Chemistry, 173, 677687.
Osborne, N. N., 1971. Occurrence of GABA and taurine in the nervous systems of dogfish and some invertebrates. Comparative and General Pharmacology, 2, 433438.
Osborne, N. N., 1972. Occurrence of glycine and glutamic acid in the nervous system of two fish species and some invertebrates. Comparative Biochemistry and Physiology, 43 B, 579585.
Packard, A., 1972. Cephalopods and fish: the limits of convergence. Biological Reviews, 47, 241307.
Packard, A., 1974. Chromatophore fields in the skin of the octopus. Journal of Physiology, 238, 3840P.
Packard, A. & Hochberg, F. G., 1977. Skin patterning in Octopus and other genera. Symposia of the Zoological Society of London, no. 38, 191231.
Packard, A. & Sanders, G. D., 1971. Body patterns of Octopus vulgaris and maturation of the response to disturbance. Animal Behaviour, 19, 780790.
Pollard, H. B., Barker, J. L., Bohr, W. A. & Dowdall, M. J., 1975. Chlorpromazine: specific inhibition of L-noradrenaline and 5-hydroxytryptamine uptake in synaptosomes from squid brain. Brain Research, 85, 2331.
Roberts, E., 1964. Comparative aspects of ninhydrin-reactive constituents in nervous tissue. In Comparative Neurochemistry (ed. Richter, D.), pp. 167178. Pergamon Press.
Rose, S. P. R. & Cory, H. T., 1970. Glutamate metabolism in octopus brain in vivo: absence of a Waelsch effect. Journal of Neurochemistry, 17, 817820.
Rowell, C. H. F., 1963. Excitatory and inhibitory pathways in the arm of Octopus. Journal of Experimental Biology, 40, 257270.
Sanders, F. K. & Young, J. Z., 1940. Learning and other functions of the higher nervous centres of Sepia. Journal of Neurophysiology, 3, 501526.
Simpson, J. W., Allen, K. & Awapara, J., 1959. Free amino acids in some aquatic invertebrates. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 117, 371381.
Tansey, E. M., 1978. A Histochemical Study of the Cephalopod Brain. Ph.D. Thesis, University of Sheffield.
Tansey, E. M., 1979. Neurotransmitters in the cephalopod brain – a review. Comparative Biochemistry and Physiology, 64 C, 173182.
Tansey, E. M., 1980. Aminergic fluorescence in the cephalopod brain. Philosophical Transactions of the Royal Society (B), 291, 127145.
Tsukada, Y., Uemara, K., Hirano, S. & Nagata, Y., 1964. Distribution of amino acids in the brain in different species. In Comparative Neurochemistry (ed. Richter, D.), pp. 179183. Pergamon Press.
Villegas, J., 1975. Characterization of acetylcholine receptors in the Schwann cell membrane of the squid nerve fibre. journal of physiology, 249, 679689.
Voight, K. H., Kiehling, C., Froesch, D., Schieke, M. & Martin, R., 1981. Enkephaline-related peptides: direct action on the Octopus heart. Neuroscience Letters, 27, 2530.
Welsch, F. & Dettbarn, W.-D., 1972. The subcellular distribution of acetylcholine, acetyl-cholinesterases and choline acetyltransferase in the optic lobes of the squid Loligo pealeii. Brain Research, 39, 467482.
Young, J. Z., 1971. The Anatomy of the Nervous System of Octopus vulgaris. xxi, 690 pp. Oxford: Clarendon Press.

The chromatic and motor effects of neurotransmitter injection in intact and brain-lesioned Octopus

  • P. L. R. Andrews (a1), J. B. Messenger (a2) and E. M. Tansey (a3)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed