Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-23T22:35:41.643Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  16 October 2009

P. L. R. Andrews ,
J. B. Messenger  and
E. M. Tansey
P. L. R. Andrews
Affiliation:
Department of Physiology, Medical School, University of Edinburgh, Teviot Place, Edinburgh, EH8 9AG
J. B. Messenger
Affiliation:
Department of Zoology, University of Sheffield, Western Bank, Sheffield, S10 2TN
E. M. Tansey
Affiliation:
Vision Research Unit, The Rayne Institute, St. Thomas' Hospital, London, SE1 7EH
Get access Rights & Permissions [Opens in a new window]

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.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 63 , Issue 2 , May 1983 , pp. 355 - 370
Copyright
Copyright © Marine Biological Association of the United Kingdom 1983

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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.Google ScholarPubMed
Andrews, P. L. R., Packard, A. & Tansey, E. M., 1982. A physiologically discrete population of chromatophores in Octopus vulgaris (Mollusca). Journal of Zoology, 198, 131–140.CrossRefGoogle Scholar
Andrews, P. L. R. & Tansey, E. M., 1982 a. A technique for central drug administration in Octopus vulgaris. Journal of Neuroscience Methods, 4, 243–247.CrossRefGoogle Scholar
Andrews, P. L. R. & Tansey, E. M., 1981 b. The effects of some anaesthetic agents in Octopus vulgaris. Comparative Biochemistry and Physiology, 70 C, 241–247.Google Scholar
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, 109–134.CrossRefGoogle Scholar
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, 43–46.Google Scholar
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, 246–247.Google Scholar
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, 2446–2450.Google Scholar
Barlow, J. J., 1977. Comparative biochemistry of the central nervous system. Symposia of the Zoological Society of London, no. 38, 325–346.Google Scholar
Boldyrev, A. A. & Lebedev, A. V. 1972. Precursors of histidine dipeptides in molluscan tissues. Comparative Biochemistry and Physiology, 41 B, 453–456.Google Scholar
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, 619–626.CrossRefGoogle Scholar
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, 193–199.CrossRefGoogle Scholar
Boycott, B. B., 1953. The chromatophore system of cephalopods. Proceedings of the Linnean Society of London, 164, 235–240.CrossRefGoogle Scholar
Boycott, B. B., 1961. The functional organisation of the brain of the cuttlefish, Sepia officinalis. Proceedings of the Royal Society (B), 153, 503–534.Google Scholar
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, 273–276.Google Scholar
Cloney, R. A. & Florey, E., 1968. Ultrastructure of cephalopod chromatophore organs. Zeitschrift für Zellforschung und mikroskopische Anatomie, 89, 250–280.CrossRefGoogle ScholarPubMed
Cory, H. T., 1969. Comparative Metabolic Studies in Octopus and Rat Brain. Ph.D. Thesis, University of London.Google Scholar
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, 979–988.CrossRefGoogle ScholarPubMed
Covelli, V., Memo, M., Spano, P. F. & Trabucchi, M., 1981. Characterization of dopamine receptors in various species of invertebrates and vertebrates. Neuroscience, 6, 2077–2079.CrossRefGoogle ScholarPubMed
Dale, H. H., 1954. The beginnings and the prospects of neurohumoral transmission. Pharmacological Reviews, 6, 7–13.Google ScholarPubMed
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, 432–433.Google Scholar
Florey, E., 1966. Nervous control and spontaneous activity of the chromatophores of a cephalopod, Loligo opalescens. Comparative Biochemistry and Physiology, 18, 305–324.CrossRefGoogle ScholarPubMed
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, 98–130.CrossRefGoogle Scholar
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.Google Scholar
Gould, R. M. & Cottrell, G. A., 1974. Putrescine in molluscs: identification and occurrence in neurones and other tissues. Comparative Biochemistry and Physiology, 48 B, 591–597.Google ScholarPubMed
Heilbronn, E., Hause, S. & Lundgren, G., 1971. Chemical identification of acetylcholine in squid-head ganglion. Brain Research, 33, 431–437.CrossRefGoogle ScholarPubMed
Juorio, A. V., 1971. Catecholamines and 5-hydroxytryptamine in nervous tissue of cephalopods. Journal of Physiology, 216, 215–226.CrossRefGoogle ScholarPubMed
Juorio, A. V. & Molinoff, P. B., 1971. Distribution of octopamine in nervous tissues of Octopus vulgaris. British Journal of Pharmacology, 43, 438–439P.Google ScholarPubMed
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, 271–280.CrossRefGoogle ScholarPubMed
Kato, G. & Tattrie, B., 1974. Solubilization of the acetylcholine receptor protein from Loligo Opalescens without detergents. Federation of European Biochemical Societies Letters, 48, 26–31.CrossRefGoogle ScholarPubMed
Kleinschuster, S. J. & Morris, J. E., 1972. Glutamine synthetase, an enzyme characteristic of vertebrate systems in invertebrate tissues. Experientia, 28, 1157–1158.CrossRefGoogle ScholarPubMed
Laverack, M. S., 1980. Electrophysiology of the isolated central nervous system of the northern octopus Eledone cirrhosa. Marine Behaviour and Physiology, 7, 155–169.CrossRefGoogle Scholar
Leake, L. & Walker, R. J., 1980. Invertebrate Neuropharmacology. 358 pp. London: Blackie.Google Scholar
Lewis, P. R., 1952. The free amino acids of invertebrate nerve. Biochemical Journal, 52, 330–338.CrossRefGoogle ScholarPubMed
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, 509–522.CrossRefGoogle ScholarPubMed
Mann, E. & Enna, S. J., 1980. Phylogenetic distribution of bicuculline-sensitive γ-amino-butyric acid (GABA) receptor binding. Brain Research, 184, 367–373.CrossRefGoogle ScholarPubMed
Martin, R., Froesch, D., Weber, E. & Voigt, K. H., 1979. Metenkephalin-like immunoreactivity in a cephalopod neurohemal organ. Neuroscience Letters, 15, 253–257.CrossRefGoogle Scholar
Matus, A. I., 1973. Histochemical localization of biogenic monoamines in the cephalic ganglia of Octopus vulgaris. Tissue and Cell, 5, 591–601.CrossRefGoogle ScholarPubMed
Messenger, J. B., 1967. The peduncle lobe: a visuo-motor centre in Octopus. Proceedings of the Royal Society (B), 167, 225–251.Google Scholar
Messenger, J. B., 1979. The eyes and skin of Octopus: compensating for sensory deficiencies. Endeavour, 3, 92–98.CrossRefGoogle Scholar
Miledi, R., 1972. Synaptic potentials in nerve cells of the stellate ganglion in the squid. Journal of Physiology, 225, 501–514.CrossRefGoogle ScholarPubMed
Mislin, H., 1955. Die rhythmischer Spontanentladungen in Zentralnervensystem der Tintenfische. Acta medica scandinavica Supplementum, 307, 152–158.Google Scholar
Nachmansohn, D. & Weiss, M. S., 1948. Studies on choline acetylase. IV. Effect of citric acid. Journal of Biological Chemistry, 173, 677–687.CrossRefGoogle Scholar
Osborne, N. N., 1971. Occurrence of GABA and taurine in the nervous systems of dogfish and some invertebrates. Comparative and General Pharmacology, 2, 433–438.CrossRefGoogle ScholarPubMed
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, 579–585.Google ScholarPubMed
Packard, A., 1972. Cephalopods and fish: the limits of convergence. Biological Reviews, 47, 241–307.CrossRefGoogle Scholar
Packard, A., 1974. Chromatophore fields in the skin of the octopus. Journal of Physiology, 238, 38–40P.Google ScholarPubMed
Packard, A. & Hochberg, F. G., 1977. Skin patterning in Octopus and other genera. Symposia of the Zoological Society of London, no. 38, 191–231.Google Scholar
Packard, A. & Sanders, G. D., 1971. Body patterns of Octopus vulgaris and maturation of the response to disturbance. Animal Behaviour, 19, 780–790.CrossRefGoogle Scholar
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, 23–31.CrossRefGoogle Scholar
Roberts, E., 1964. Comparative aspects of ninhydrin-reactive constituents in nervous tissue. In Comparative Neurochemistry (ed. Richter, D.), pp. 167–178. Pergamon Press.CrossRefGoogle Scholar
Rose, S. P. R. & Cory, H. T., 1970. Glutamate metabolism in octopus brain in vivo: absence of a Waelsch effect. Journal of Neurochemistry, 17, 817–820.CrossRefGoogle ScholarPubMed
Rowell, C. H. F., 1963. Excitatory and inhibitory pathways in the arm of Octopus. Journal of Experimental Biology, 40, 257–270.CrossRefGoogle Scholar
Sanders, F. K. & Young, J. Z., 1940. Learning and other functions of the higher nervous centres of Sepia. Journal of Neurophysiology, 3, 501–526.CrossRefGoogle Scholar
Simpson, J. W., Allen, K. & Awapara, J., 1959. Free amino acids in some aquatic invertebrates. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 117, 371–381.CrossRefGoogle Scholar
Tansey, E. M., 1978. A Histochemical Study of the Cephalopod Brain. Ph.D. Thesis, University of Sheffield.Google Scholar
Tansey, E. M., 1979. Neurotransmitters in the cephalopod brain – a review. Comparative Biochemistry and Physiology, 64 C, 173–182.Google Scholar
Tansey, E. M., 1980. Aminergic fluorescence in the cephalopod brain. Philosophical Transactions of the Royal Society (B), 291, 127–145.Google Scholar
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. 179–183. Pergamon Press.CrossRefGoogle Scholar
Villegas, J., 1975. Characterization of acetylcholine receptors in the Schwann cell membrane of the squid nerve fibre. journal of physiology, 249, 679–689.CrossRefGoogle ScholarPubMed
Voight, K. H., Kiehling, C., Froesch, D., Schieke, M. & Martin, R., 1981. Enkephaline-related peptides: direct action on the Octopus heart. Neuroscience Letters, 27, 25–30.CrossRefGoogle Scholar
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, 467–482.CrossRefGoogle Scholar
Young, J. Z., 1971. The Anatomy of the Nervous System of Octopus vulgaris. xxi, 690 pp. Oxford: Clarendon Press.Google Scholar