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Comparative 3D microanatomy and histology of the eyes and central nervous systems in coleoid cephalopod hatchlings

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Abstract

Adaptive radiation of an animal group is the evolutionary variation of morphology, physiology, and behavior opening up new habitats and resources. An impressive example of the reciprocal interdependency of form and function is found in the anatomy of cephalopod visual and central nervous systems. Interspecific differences of sensory organs and signal processing structures reflect the eco-functional context, e.g., the species-specific demands emanating from habitat and foraging behavior. To substantiate this, we investigated the eyes and brain neuropils of early post-hatching stages of six coleoid cephalopod species (Sepia officinalis, Rossia macrosoma, Sepietta obscura, Idiosepius notoides, Loligo vulgaris, and Octopus vulgaris), showing different size and inhabiting different ethoecological niches. Comprehensive 3D structure data sets were produced in light microscopic resolution, i.e., semithin section series of the head region (histology presented for I. notoides, R. macrosoma, and S. obscura for the first time) and 3D surface renderings of the neuropils, enabling the display of all components in arbitrary perspectives and combinations, and comparative volumetic anaylsis of homologous lobe neuropils. Differing in absolute size considerably, the visual and central nervous systems of the six species follow the same bauplan in adult-like configuration. The visual sense obviously is of paramount importance already after hatching, but also, equilibrioception and olfaction are well developed. The species-specific shapes of various components show that some plasticity and distinct differences in volumetric ratios are found, subject to their functional relevance and to different demands of the lifestyle on the brachial and swimming motor function, on camouflage, as well as on sensoric and cognitive abilities.

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References

  • Archer, S. N., Djamgoz, M. B. A., Loew, E. R., Partridge, J. C., & Vallerga, S. (1999). Adaptive mechanisms in the ecology of vision (p. 680). Dordrecht: Kluwer Academic Publishers.

    Book  Google Scholar 

  • Boletzky, S. V. (1974). The “larvae” of Cephalopoda: a review. Thalassia Jugoslavica, 10, 45–76.

    Google Scholar 

  • Boletzky, S. V. (2003). Biology of early life stages in cephalopod molluscs. Advances in Marine Biology, 44, 143–203.

    Article  Google Scholar 

  • Boletzky, S. V., & Boletzky, M. V. V. (1973). Observations on the embryonic and early post-embryonic development of Rossia macrosoma (Mollusca, Cephalopoda). Helgolaender Meeresuntersuchungen, 25, 135–161.

    Article  Google Scholar 

  • Boletzky, S. V., Boletzky, M. V. V., Froesch, D., & Gätzi, V. (1971). Laboratory rearing of Sepiolinae (Mollusca, Cephalopoda). Marine Biology, 8, 62–87.

    Google Scholar 

  • Boletzky, S. V., Fioroni, P., & Guerra, A. (1997). Proceedings of the second international symposium on functional morphology of cephalopods. Vie et milieu - Life and environment, 47(2), 187.

    Google Scholar 

  • Bone, Q., & Marshall, N. B. (1985). Biologie der Fische. Stuttgart: Gustav Fischer Verlag.

    Google Scholar 

  • Bonichon, A. (1967). Contribution à l´etude de la neurosécretion et de l´endocrinologie chez les Céphalpodes. I. Octopus vulgaris. Vie et milieu - Life and environment, 18, 27–263.

    Google Scholar 

  • Boycott, B. B. (1961). The functional organization of the brain of the cuttlefish Sepia officinalis. Proceedings of the Royal Society B: Biological Sciences, 153, 503–534.

    Article  Google Scholar 

  • Boycott, B. B., & Young, J. Z. (1955). A memory system in Octopus vulgaris Lamarck. Proceedings of the Royal Society B: Biological Sciences, 153, 503–534.

    Article  Google Scholar 

  • Bozzano, A., Pankhurst, P. M., Moltschaniwskyj, N. A., & Villanueva, R. (2009). Eye development in southern calamary, Sepioteuthis australis, embryos and hatchlings. Marine Biology, 156, 1359–1373.

    Article  Google Scholar 

  • Budelmann, B. U. (1995). The cephalopod nervous system: what evolution has made of the molluscan design. In O. Breidbach & W. Kutsch (Eds.), The nervous system of Invertebrates: an evolutionary and comparative approach (pp. 115–138). Basel: Birkhäuser.

    Chapter  Google Scholar 

  • Budelmann, B. U., Schipp, R., & Boletzky, S. V. (1997). Cephalopoda. In F. W. Harrison & A. J. Kohn (Eds.), Microscopic anatomy of invertebrates (Vol. 6A: Mollusca II, pp. pp. 119–pp. 414). New York: Wiley-Liss.

    Google Scholar 

  • Claes, M. F. (1996). Functional morphology of the white bodies of the cephalopod mollusc Sepia officinalis. Acta Zoologica (Stockholm), 77, 173–190.

    Article  Google Scholar 

  • Collewijn, H. (1970). Oculomotor reactions in the cuttlefish, Sepia officinalis. The Journal of Experimental Biology, 52(2), 369–384.

    Google Scholar 

  • Collin, S. P., & Partridge, J. C. (1996). Fish vision: retinal specializations in the eyes of deep-sea teleosts. Journal of Fish Biology, 49, 157–174.

    Article  Google Scholar 

  • Di Cristo, C., Van Minnen, J., & Di Cosmo, A. (2005). The presence of APGWamide in Octopus vulgaris: a possible role in the reproductive behavior. Peptides, 26(1), 53–62.

    Article  PubMed  Google Scholar 

  • Di Cristo, C., De Lisa, E., & Di Cosmo, A. (2009). Control of GnRH expression in the olfactory lobe of Octopus vulgaris. Peptides, 30(3), 538–544.

    Article  PubMed  Google Scholar 

  • Dietl, M. J. (1878). Untersuchungen über die Organisation des Gehirns wirbelloser Thiere (Cephalopoden, Tethys). Sitzungsberichte der Akademie der Wissenschaften in Wien, 77, 481–533.

    Google Scholar 

  • Fishelson, L., Ayalon, G., Zverdling, A., & Holzman, R. (2004). Comparative morphology of the eye (with particular attention to the retina) in various species of cardinal fish (Apogonidae, Teleostei). The Anatomical Record.Part A. Discoveries in Molecular, Cellular, and Evolutionary Biology, 277(2), 249–261.

    Article  PubMed  Google Scholar 

  • Frösch, D. (1971). Quantitative Untersuchungen am Zentralnervensystem der Schlüpfstadien von zehn mediterranen Cephalopodenarten. Revue Suisse de Zoologie, 57, 1069–1122.

    Google Scholar 

  • Frösch, D. (1974). The subpedunculate lobe of the octopus brain: evidence for dual function. Brain Research, 75(2), 277–285.

    Article  Google Scholar 

  • Gilbert, D. L., Adelman, W. J., & Arnold, J. M. (1990). Squid as experimental animals (p. 548). New York: Plenum Press.

    Book  Google Scholar 

  • Graziadei, P. (1971). The nervous system of the arms. In J. Z. Young (Ed.), The anatomy of the nervous system of Octopus vulgaris (pp. 45–61). Oxford: Claredon Press.

    Google Scholar 

  • Groeger, G., Cotton, P. A., & Williamson, R. (2005). Ontogenetic changes in the visual acuity of Sepia officinalis measured using the optomotor response. Canadian Journal of Zoology, 83(2), 274–279.

    Article  Google Scholar 

  • Groeger, G., Chrachri, A., & Williamson, R. (2006). Changes in cuttlefish retinal sensitivity during growth. Vie et Milieu, 56(2), 167–173.

    Google Scholar 

  • Hanlon, R. T., & Messenger, J. B. (1988). Adaptive coloration in young cuttlefish (Sepia officinalis L.): the morphology and development of body patterns and their relation to behaviour. Philosophical Transactions of the Royal Society, B: Biological Sciences, 320, 437–487.

    Article  Google Scholar 

  • Hanlon, R. T., & Messenger, J. B. (1996). Cephalopod behaviour (p. 232). Cambridge: Cambridge University Press.

    Google Scholar 

  • Hao, Z.-L., Zhang, X.-M., Kudo, H., & Kaeriyama, M. (2010). Development of the retina in the cuttlefish Sepia esculenta. Journal of Shellfish Research, 29(2), 463–470.

    Article  Google Scholar 

  • Heß, M. (2007). Semi-automated mapping of cell nuclei in 3D-stacks from optical-sectioning microscopy. In P. Perner & O. Salvetti (Eds.), Advances in mass data analysis of signals and images in medicine, biotechnology and chemistry (Lecture Notes in Computer Science (Vol. 4826, pp. pp. 156–pp. 164). Berlin: Springer.

    Chapter  Google Scholar 

  • Hillig, R. (1912). Das Nervensystem von Sepia officinalis L. Zeitschrift für Wissenschaftliche Zoologie, 101, 736–800.

    Google Scholar 

  • Jereb, P., & Roper, C. F. E. (2005). Cephalopods of the world: an annotated and illustrated catalogue of cephalopod species known to date. Volume 1. Chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae) (Vol. 4(1), FAO species catalogue for fishery purposes). Rome: FAO. 262 p.

  • Jereb, P., & Roper, C. F. E. (2010). Cephalopods of the world: an annotated and illustrated catalogue of cephalopod species known to date. Volume 2. Myopsid and oegopsid squids (FAO Species catalogue for fishery purposes, Vol. 4(2)). Rome: FAO. 605 p.

  • Kerbl, A., Handschuh, S., Nödl, M.-T., Metscher, B., Walzl, M., & Wanninger, A. (2013). Micro-CT in cephalopod research: Investigating the internal anatomy of a sepiolid squid using a non-destructive technique with special focus on the ganglionic system. Journal of Experimental Marine Biology and Ecology, 447, 140–148.

    Article  Google Scholar 

  • Kunze, P. (1972). Comparative studies of arthropod superposition eyes. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 76(4), 347–357.

    Google Scholar 

  • Lauder, G. V. (1981). Form and function: structural analysis in evolutionary morphology. Paleobiology, 7(4), 430–442.

    Google Scholar 

  • Le Gall, S., Feral, C., Van Minnen, J., & Marchand, C. R. (1988). Evidence for peptidergic innervation of the endocrine optic gland in Sepia by neurons showing FMRFamide-like immunoreactivity. Brain Research, 462(1), 83–88.

    Article  PubMed  Google Scholar 

  • Lythgoe, J. N. (1979). The ecology of vision (p. 270). Oxford: Clarendon Press.

    Google Scholar 

  • Maddock, L., & Young, J. Z. (1987). Quantitative differences among the brains of cephalopods. Journal of Zoology, 212(4), 739–767.

    Article  Google Scholar 

  • Makino, A., & Miyazaki, T. (2010). Topographical distribution of visual cell nuclei in the retina in relation to the habitat of five species of Decapodiformes (Cephalopoda). Journal of Molluscan Studies, 76(2), 180–185.

    Article  Google Scholar 

  • Mangold, K., & Boletzky, S. (1973). New data on reproductive biology and growth of Octopus vulgaris. Marine Biology, 19(1), 7–12.

    Article  Google Scholar 

  • Marquis, F. (1989). Die Embryonalentwicklung des Nervensystems von Octopus vulgaris Lam. (Cephalopoda. Octopoda), eine histologische Analyse. Verhandlungen der naturforschenden Gesellschaft Basel, 99, 23–76.

    Google Scholar 

  • Martin, R. (1965). On the structure and embryonic development of the giant fibre system of the squid Loligo vulgaris. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 67, 77–85.

    Article  CAS  PubMed  Google Scholar 

  • Martin, R., & Rungger, D. (1966). Zur Struktur und Entwicklung des Riesenfasersystems erster Ornung von Sepia officinalis L. (Cephalopoda). Zeitschrift für Zellforschung und Mikroskopische Anatomie, 74, 454–463.

    Article  CAS  PubMed  Google Scholar 

  • Martin, G. R., Wilson, K.-J., Wild, J. M., Parsons, S., Kubke, M. F., & Corfield, J. (2007). Kiwi forego vision in the guidance of their nocturnal activities. PLoS ONE, 2(2), e198.

    Article  PubMed Central  PubMed  Google Scholar 

  • Meister, G. (1972). Organogenese von Loligo vulgaris Lam. (Mollusca, Cephalopoda, Teuthoidea, Myopsida, Loliginidae). Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere, 59, 247–300.

    Google Scholar 

  • Messenger, J. B. (1967a). The effects on locomotion of lesions to the viso-motor system in Octopus. Proceedings of the Royal Society B: Biological Sciences, 167, 252–281.

    Article  CAS  Google Scholar 

  • Messenger, J. B. (1967b). The peduncle lobe: a viso-motor centre in Octopus. Proceedings of the Royal Society B: Biological Sciences, 167, 225–251.

    Article  CAS  Google Scholar 

  • Messenger, J. B. (1968). The visual attack of the cuttlefish, Sepia officinalis. Animal Behaviour, 16(2), 342–357.

    Article  CAS  PubMed  Google Scholar 

  • Messenger, J. B. (1979). The nervous system of Loligo: IV. The peduncle and olfactory lobes. Philosophical Transactions of the Royal Society, B: Biological Sciences, 285(1008), 275–309.

    Article  Google Scholar 

  • Nixon, M., & Mangold, K. (1996). The early life of Octopus vulgaris (Cephalopoda: Octopodidae) in the plankton and at settlement: a change in lifestyle. Journal of Zoology, 239(2), 301–327.

    Article  Google Scholar 

  • Nixon, M., & Mangold, K. (1998). The early life of Sepia officinalis, and the contrast with that of Octopus vulgaris (Cephalopoda). Journal of Zoology, 245(04), 407–421.

    Article  Google Scholar 

  • Nixon, M., & Young, J. Z. (2003). The brains and lives of cephalopods (p. 408). Oxford: Oxford University Press.

    Google Scholar 

  • Norman, M. (2003). Cephalopods - A world guide (2nd ed., p. 320). Hackenheim: Conch books.

    Google Scholar 

  • Novicki, A., Budelmann, B. U., & Hanlon, R. T. (1990). Brain pathways of the chromatophore system in the squid Lolliguncula brevis. Brain Research, 519(1–2), 315–323.

    Article  CAS  PubMed  Google Scholar 

  • Packard, A. (1972). Cephalopods and fish: the limits of convergence. Biological Reviews, 47(2), 241–307.

    Article  CAS  Google Scholar 

  • Pfefferkorn, A. (1915). Das Nervensystem der Octopoden. Zeitschrift für Wissenschaftliche Zoologie, 114, 425–531.

    Google Scholar 

  • Poirier, R., Chichery, R., & Dickel, L. (2004). Effects of rearing conditions on sand digging efficiency in juvenile cuttlefish. Behavioural Processes, 67(2), 273–279.

    Article  CAS  PubMed  Google Scholar 

  • Richardson, K. C., Jarett, L., & Finke, E. H. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology, 35, 313–323.

    CAS  PubMed  Google Scholar 

  • Richter, K. (1913). Das Nervensystem der Oegopsiden. Zeitschrift für Wissenschaftliche Zoologie, 106, 289–408.

    Google Scholar 

  • Roper, C. F. E., Sweeney, M. J., & Nauen, C. E. (1984). Cephalopods of the world. An annotated and illustrated catalogue of species of interest to fisheries (Vol. 3, FAO Fisheries Synopsis). Rome: FAO. 277 p.

  • Ruthensteiner, B. (2008). Soft Part 3D visualization by serial sectioning and computer reconstruction. Zoosymposia, 1, 63–100.

    Article  Google Scholar 

  • Ruthensteiner, B., & Heß, M. (2008). Embedding 3D models of biological specimens in PDF publications. Microscopy Research and Technique, 71(11), 778–786.

    Article  PubMed  Google Scholar 

  • Scharpf, E., Haszprunar, G., & Heß, M. Coleoid cephalopod retinae - a comparative morphological approach. In 3rd International Symposium Coleoid Cephalopods through Time, Luxemburg, 2008 (pp. 25–27).

  • Schkaff, B. (1914). Zur Kenntnis des Nervensystems der Myopsiden. Zeitschrift für Wissenschaftliche Zoologie, 109, 591–630.

    Google Scholar 

  • Shigeno, S., & Yamamoto, M. (2002). Organization of the nervous system in the pygmy cuttlefish, Idiosepius paradoxus Ortmann (Idiosepiidae, Cephalopoda). Journal of Morphology, 254(1), 65–80.

    Article  PubMed  Google Scholar 

  • Shigeno, S., Kidokoro, H., Tsuchiya, K., Segawa, S., & Yamamoto, M. (2001a). Development of the brain in the oegopsid squid, Todarodes pacificus: an atlas from hatchling to juvenile. Zoological Science, 18(8), 1081–1096.

    Article  Google Scholar 

  • Shigeno, S., Kidokoro, H., Tsuchiya, K., Segawa, S., & Yamamoto, M. (2001b). Development of the brain in the oegopsid squid, Todarodes pacificus: an atlas up to the hatching stage. Zoological Science, 18(4), 527–541.

    Article  Google Scholar 

  • Shigeno, S., Tsuchiya, K., & Segawa, S. (2001c). Conserved topological patterns and heterochronies in loliginid cephalopods: comparative developmental morphology of the oval squid Sepioteuthis lessoniana. Invertebrate Reproduction & Development, 39(3), 161–174.

    Article  Google Scholar 

  • Shigeno, S., Tsuchiya, K., & Segawa, S. (2001d). Embryonic and paralarval development of the central nervous system of the loliginid squid Sepioteuthis lessoniana. The Journal of Comparative Neurology, 437(4), 449–475.

    Article  CAS  PubMed  Google Scholar 

  • Tompsett, D. H. (1939). Sepia (L.M.B.C. memoirs on typical British marine plants and animals, Vol. 32): University Press. 184 p.

  • Villanueva, R., Nozais, C., & Boletzky, S. V. (1995). The planktic life of octopuses. Nature, 377(6545), 107–107.

    Article  CAS  Google Scholar 

  • Villanueva, R., Nozais, C., & Boletzky, S. V. (1996). Swimming behaviour and food searching in planktic Octopus vulgaris Cuvier from hatching to settlement. Journal of Experimental Marine Biology and Ecology, 208(1–2), 169–184.

    Google Scholar 

  • Warrant, E. J., & Locket, N. A. (2004). Vision in the deep sea. Biological Reviews, 79(3), 671–712.

    Article  PubMed  Google Scholar 

  • Warrant, E. J., & McIntyre, P. (1991). Strategies for retinal design in arthropod eyes of low F-number. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 168(4), 499–512.

    Article  Google Scholar 

  • Wells, M. J. (1958). Factors affecting reactions to Mysis by newly hatched Sepia. Behaviour, 13(1–2), 96–111.

    Article  Google Scholar 

  • Wells, M. J., & Wells, J. (1959). Hormonal control of sexual maturity in Octopus. The Journal of Experimental Biology, 36(1), 1–33.

    Google Scholar 

  • Wells, M. J., & Young, J. Z. (1972). The median inferior frontal lobe and touch learning in the octopus. The Journal of Experimental Biology, 56(2), 381–402.

    CAS  PubMed  Google Scholar 

  • West, J. A., Sivak, J. G., & Doughty, M. J. (1995). Microscopical evaluation of the crystalline lens of the squid (Loligo opalescens) during embryonic development. Experimental Eye Research, 60(1), 19–35.

    Article  CAS  PubMed  Google Scholar 

  • Willekens, B., Vrensen, G., Jacob, T., & Duncan, G. (1984). The ultrastructure of the lens of the cephalopod Sepiola: a scanning electron microscopic study. Tissue & Cell, 16(6), 941–950.

    Article  CAS  Google Scholar 

  • Wirz, K. (1954). Etudes quantitatives sur le systeme nerveux des Cephalopodes. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences, 238(12), 1353–1355.

    CAS  PubMed  Google Scholar 

  • Wirz, K. (1959). Étude biométrique du système nerveux des céphalopodes: Presses universitaires de France. 40 p.

  • Wollesen, T., Loesel, R., & Wanninger, A. (2008). FMRFamide-like immunoreactivity in the central nervous system of the cephalopod mollusc, Idiosepius notoides. Acta Biologica Hungarica, 59, 111–116.

    Article  PubMed  Google Scholar 

  • Wollesen, T., Loesel, R., & Wanninger, A. (2009). Pygmy squids and giant brains: mapping the complex cephalopod CNS by phalloidin staining of vibratome sections and whole-mount preparations. Journal of Neuroscience Methods, 179(1), 63–67.

    Article  CAS  PubMed  Google Scholar 

  • Wollesen, T., Cummins, S. F., Degnan, B. M., & Wanninger, A. (2010a). FMRFamide gene and peptide expression during central nervous system development of the cephalopod mollusk, Idiosepius notoides. Evolution & Development, 12(2), 113–130.

    Article  CAS  Google Scholar 

  • Wollesen, T., Degnan, B. M., & Wanninger, A. (2010b). Expression of serotonin (5-HT) during CNS development of the cephalopod mollusk, Idiosepius notoides. Cell and Tissue Research, 342(2), 161–178.

    Article  CAS  PubMed  Google Scholar 

  • Wollesen, T., Nishiguchi, M. K., Seixas, P., Degnan, B. M., & Wanninger, A. (2012a). The VD1/RPD2 alpha 1-neuropeptide is highly expressed in the brain of cephalopod mollusks. Cell and Tissue Research, 348(3), 439–452.

    Article  CAS  PubMed  Google Scholar 

  • Wollesen, T., Sukhsangchan, C., Seixas, P., Nabhitabhata, J., & Wanninger, A. (2012b). Analysis of neurotransmitter distribution in brain development of benthic and pelagic octopod cephalopods. Journal of Morphology, 273(7), 776–790.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto, M. (1985). Ontogeny of the visual system in the cuttlefish Sepiella japonica. I. Morphological differentiation of the visual cell. The Journal of Comparative Neurology, 232(3), 347–361.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto, M., Shimazaki, Y., & Shigeno, S. (2003). Atlas of the embryonic brain in the pygmy squid, Idiosepius paradoxus. Zoological Science, 20(2), 163–179.

    Article  PubMed  Google Scholar 

  • Yamazaki, A., Yoshida, M., & Uematsu, K. (2002). Post-hatching development of the brain in Octopus ocellatus. Zoological Science, 19(7), 763–771.

    Article  PubMed  Google Scholar 

  • Young, J. Z. (1962). The optic lobes of Octopus vulgaris. Philosophical Transactions of the Royal Society, B: Biological Sciences, 245(718), 19–58.

    Article  Google Scholar 

  • Young, J. Z. (1965a). The buccal nervous system of Octopus. Philosophical Transactions of the Royal Society, B: Biological Sciences, 249(755), 27–44.

    Article  Google Scholar 

  • Young, J. Z. (1965b). The centres for touch discrimination in Octopus. Philosophical Transactions of the Royal Society, B: Biological Sciences, 249(755), 45–67.

    Article  Google Scholar 

  • Young, J. Z. (1965c). The nervous pathways for poisoning, eating and learning in Octopus. The Journal of Experimental Biology, 43(3), 581–593.

    CAS  PubMed  Google Scholar 

  • Young, J. Z. (1965d). The organization of a memory system. Proceedings of the Royal Society B: Biological Sciences, 163(992), 285–320.

    Article  CAS  Google Scholar 

  • Young, J. Z. (1970). Neurovenous tissues in cephalopods. Philosophical Transactions of the Royal Society, B: Biological Sciences, 257(815), 309–321.

    Article  CAS  Google Scholar 

  • Young, J. Z. (1971). The anatomy of the nervous system of Octopus vulgaris (p. 690). Oxford: Clarendon Press.

    Google Scholar 

  • Young, J. Z. (1974). The central nervous system of Loligo. I. The optic lobe. Philosophical Transactions of the Royal Society B: Biological Sciences, 267(885), 263–302.

    Article  CAS  Google Scholar 

  • Young, J. Z. (1976a). The ‘cerebellum’ and the control of eye movements in cephalopods. Nature, 264(5586), 572–574.

    Article  CAS  PubMed  Google Scholar 

  • Young, J. Z. (1976b). The nervous system of Loligo. II. Suboesophageal centres. Philosophical Transactions of the Royal Society B: Biological Sciences, 274(930), 101–167.

    Article  CAS  Google Scholar 

  • Young, J. Z. (1977). The nervous system of Loligo. III. Higher motor centres: the basal supraoesophageal lobes. Philosophical Transactions of the Royal Society B: Biological Sciences, 276(948), 351–398.

    Article  Google Scholar 

  • Young, J. Z. (1979). The nervous system of Loligo. V. The vertical lobe complex. Philosophical Transactions of the Royal Society, B: Biological Sciences, 285(1009), 311–354.

    Article  Google Scholar 

  • Young, J. Z. (1983). The distributed tactile memory system of Octopus. Proceedings of the Royal Society B: Biological Sciences, 218(1211), 135–176.

    Article  Google Scholar 

  • Young, R. E., & Vecchione, M. (2004). Oegopsida Orbigny, 1845. Version 18 August 2004 (under construction). http://tolweb.org/Oegopsida/19407/2004.08.18

  • Young, R. E., Vecchione, M., & Mangold, K. M. (2012). Cephalopoda Cuvier 1797. Octopods, squids, nautiluses, etc. Version 04 July 2012 (under construction). http://tolweb.org/Cephalopoda/19386/2012.07.04.

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Acknowledgments

We are very much obligued to Sigurd von Boletzky for providing us with some of his section series and for encouraging us to use them for 3D reconstructions. Furthermore, we want to express our gratitude to Heidemarie Gensler for expert technical assistance and for Anastasia de Motte for improving the English. The study was partially supported by a grant to EW by the Bayerische Eliteförderung.

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Correspondence to Martin Heß.

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Elvira Wild and Martin Heß contributed equally to this work.

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Wild, E., Wollesen, T., Haszprunar, G. et al. Comparative 3D microanatomy and histology of the eyes and central nervous systems in coleoid cephalopod hatchlings. Org Divers Evol 15, 37–64 (2015). https://doi.org/10.1007/s13127-014-0184-4

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