Conserved and Convergent Organization in the Optic Lobes of Insects and Isopods, with Reference to Other Crustacean Taxa

Journal of Comparative Neurology

Volumn 467, Issue 2, 2003, Pages 150-172

  Sinakevitch, I ^a   Douglass, J K ^a   Scholtz, G ^b   Loesel, R ^c   Strausfeld, N J ^a,d  

^a UNIVERSITY OF ARIZONA   (United States)

^b HUMBOLDT UNIVERSITY   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

Crustaceans; Evolution; Immunocytology; Insects; Optic lobes

Indexed keywords

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRANCHIOPOD; COMPARATIVE ANATOMY; CONVERGENT EVOLUTION; CRUSTACEA; CUCCATI BUNDLE; EYE DEVELOPMENT; INSECT; ISOPOD; MALACOSTRACA; MORPHOLOGICAL TRAIT; NEBALIA PUGETTENSIS; NERVE CELL; NERVE FIBER; NEUROANATOMY; NEUROPIL; NONHUMAN; OPTIC CHIASM; OPTIC LOBE; OPTIC TECTUM; PLESIOMORPHY; PRIORITY JOURNAL; RETINA; TAXONOMIC IDENTIFICATION; TRIOPS; VISUAL SYSTEM;

ANIMALS; CRUSTACEA; EVOLUTION; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; INSECTS; ISOPODA; NERVE NET; NEURONS; NEUROPIL; OPTIC LOBE; SILVER STAINING;

EID: 0041704183     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10925     Document Type: Article

References (86)

1. Averof M, Akam M. 1995. Insect-crustacean relationships: insights from comparative developmental and molecular studies. Philos Trans R Soc Lond B 347:293-303.
2. Bodian D. 1937. A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat Rec 69:153-162.
3. Boore JL, Lavrov DV, Brown WM. 1998. Gene translocation links insects and crustaceans. Nature 392:667-668.
4. Braitenberg V. 1970. Ordnung und Orientierung der Elemente im Sehsystem der Fliege. Kybernetik 7:235-242.
5. Brusca RC, Wilson GDF. 1991. A phylogenetic analysis of the Isopoda with some classificatory recommendations. Mem Queensland Mus 31:143-204.
6. Buchner E, Bader R, Buchner S, Cox J, Emson PC, Flory E, Heizmann CW, Hemm S, Hofbauer A, Oertel WH. 1988. Cell-specific immunoprobes for the brain of normal and mutant Drosophila melanogaster. I. Wild-type visual system. Cell Tissue Res 253:357-370.
7. Buschbeck EK, Strausfeld NJ. 1996. Visual motion-detection circuits in flies: small-field retinotopic elements responding to motion are evolutionarily conserved across taxa. J Neurosci 16:4563-4578.
8. Buschbeck EK, Strausfeld NJ. 1997. The relevance of neural architecture to visual performance: phylogenetic conservation and variation in dipteran visual systems. J Comp Neurol 383:59-75.
9. Cajal SR, De Castro F. 1933. Elementos de Técnica micrografica del sistemo nervioso. Madrid: Tipografican Artistica Alameda.
10. Cajal SR, Sánchez SD. 1915. Contribución al conocimiento de los centros nerviosos de los insectos Parte I Retina y centros opticos. Trab Lab Invest Biol Univ Madrid 13:1-168.
11. Datum KH, Weiler R, Zettler F. 1986. Immunocytochemical demonstration of γ-amino butyric acid and glutamic acid decarboxylase in R7 photoreceptors and C2 centrifugal fibres in the blowfly visual system. J Comp Physiol A 159:241-249.
12. DeVoe RD, Kaiser W, Ohm J, Stone LS. 1982. Horizontal movement detectors of honeybees: directionally-selective visual neurons in the lobula and brain. J Comp Physiol A 147:155-170.
13. Dohle W. 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name 'Tetraconata' for the monophyletic unit Crustacea+Hexapoda. In: Deuve T, editor. Origin of the hexapoda. Ann Soc Entomol Fr 37:85-103.
14. Douglass JK, Strausfeld NJ. 1995. Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons. J Neurosci 15:5596-5611.
15. Douglass JK, Strausfeld NJ. 2003a. Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion detecting circuits. J Comp Neurol 457:326-344.
16. Douglass JK, Strausfeld NJ. 2003b. Retinotopic motion-sensitive pathways in dipteran optic lobes. Microsc Res Tech 62:132-150.
17. Elofsson R, Dahl E. 1970. The optic neuropils and chiasmata of Crustacea. Z Zellforsch Mikrosk Anat 107:343-360.
18. Fischbach KF. 1982. Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. Dev Biol 95:1-18.
19. Fischbach K-F, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441-475.
20. Franceschini N. 1975. Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In: Snyder AW, Menzel R, editors. Photoreceptor optics. Berlin, Heidelberg, New York: Springer. p 98-125.
21. Friedrich N, Tautz D. 1995. Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of the myriapods. Nature 376:165-167.
22. Fuller H, Eckert M, Blechschmidt K. 1989. Distribution of GABA-like immunoreactive neurons in the optic lobes of Periplaneta americana. Cell Tissue Res 255:225-233.
23. Giribet G, Edgecombe GE, Wheeler WC. 2001. Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157-161.
24. Haas F, Waloszek D, Hartenberger R. 2003. Devonohexapodus bocksbergensis, a new marine hexapod from the lower Devonian Hunsrück Slates, and the origin of Atelocerata and Hexapoda. Org Divers Evol 3:39-54.
25. Hanström B. 1926a. Untersuchungen über die relative Grösse der Gehirnzentren verschiedener Arthropoden unter Berücksichtigung der Lebensweise. Z Mikrosk Anat Zellforsch 7:135-190.
26. Hanström B. 1926b. Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. 1968 reprint. Amsterdam: A. Asher.
27. Hariyama T, Meyer-Rochow VB, Kawauchi T, Takaku Y, Tsukahara Y. 2001. Diurnal change in retinula cell sensitivities and receptive fields. Two-dimensional angular sensitivity functions in the apposition eyes of Ligia exotica. Crustacea Isopoda. J Exp Biol 204:239-248.
28. Harzsch S. 2002. The phylogenetic significance of crustacean optic neuropils and chiasmata: a re-examination. J Comp Neurol. 453:10-21.
29. Harzsch S, Walossek D. 2001. Neurogenesis in the developing visual system of the branchiopod crustacean Triops longicaudatus (LeConte, 1846): corresponding patterns of compound-eye formation in Crustacea and Insecta? Dev Genes Evol. 211:37-43.
30. Hausen K, Egelhaaf M. 1989. Neural mechanisms of visual course control in insects. In: Stavenga GG, Hardie RC, editors. Facets of vision. Heidelberg, New York: Springer. p 391-424.
31. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
32. Hofbauer A, Campos-Ortega JA. 1990. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Rouxs Arch Dev Biol 198:264-274.
33. Holmgren N. 1916. Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. K Svenska Vetensk Akad Handl 56:1-303.
34. Homberg U, Kingan TG, Hildebrand JG. 1987. Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1-24.
35. Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W. 2001. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154-157.
36. Kirschfeld K. 1967. Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Exp Brain Res 3:248-270.
37. Labandeira CC, Beal BS, Hueber FM. 1988. Early insect diversification: evidence from a Lower Devonian bristletail from Quebec. Science 242: 913-916.
38. Land MF, Nilsson D-E. 2002. Animal eyes. Oxford: Oxford University Press
39. Loesel R, Nässel DR, Strausfeld NJ. 2002. Common design in a unique midline neuropil in the brains of arthropods. Arth Struct Dev 31:77-91.
40. Meinertzhagen IA. 1973. Development of the compound eye and optic lobe of insects. In: Young D, editor. Developmental neurobiology of arthropods. Cambridge: Cambridge University Press. p 51-104.
41. Meinertzhagen IA. 1976. The organization of perpendicular fibre pathways in the insect optic lobe. Philos Trans R Soc Lond B 274:555-596.
42. Meinertzhagen IA. 1991. Evolution of the cellular organization of the arthropod compound eye and optic lobe. In: Cronly-Dillon JP, Gregory RL, editors. Vision and visual dysfunction. Vol. 2. Evolution of the eye and visual system. London: Macmillan Press. p 341-363.
43. Meinertzhagen IA, Hanson TE. 1993. The development of the optic lobe. In: Bate M, Martinez-Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 1363-1491.
44. Meyer EP, Matute C, Streit P, Nässel DR. 1986. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84: 207-216.
45. Meyerowitz EM, Kankel DR. 1978. A genetic analysis of visual system development in Drosophila melanogaster. Dev Biol 62:112-142.
46. Nardi F, Spinsanti G, Boore JL, Carapelli A, Dallai R, Frati F. 2003. Hexapod origins: monophyletic or paraphyletic? Science 299:1887-1889.
47. Nässel DR, Geiger G. 1983. Neuronal organization in fly optic lobes altered by laser ablations early in development or by mutations of the eye. J Comp Neurol 217:86-102.
48. Nilsson D-E, Osorio D. 1997. Homology and parallelism in arthropod sensory processing. In: Fortey RA, Thomas RH, editors. Arthropod relationships. London: Chapman and Hall. p 317-332.
49. Osorio D. 1991. Patterns of function and evolution in the arthropod optic lobe. In: Cronly-Dillon JP, Gregory RL, editors. Vision and visual dysfunction. Vol. 2. Evolution of the eye and visual system. London: Macmillan Press. p 203-229.
50. Osorio D, Bacon JP. 1994. A good eye for arthropod evolution. Bioessays 16:419-424.
51. Paulus HF. 2000. Phylogeny of the Myriapoda-Crustacea-Insecta: a new attempt using photoreceptor structure. J Zool Syst Evol Res 38:189-208.
52. Retzius G. 1891a. Zur Kenntnis des centralen Nervensystems der Würmer, Das Nervensystem der Annulaten. Biol Untersuch Neue Folge 2:1-28.
53. Retzius G. 1891b. Das Nervensystem der Lumbriciden. Biol Untersuch Neue Folge 3:1-16.
54. Ribi WA. 1975. The neurons of the first optic ganglion of the bee Apis mellifera. Adv Anat Embryol Cell Biol 50:1-43.
55. Richter S. 2002. The tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Org Divers Evol 2:217-237.
56. Richter S, Scholtz G. 2001. Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113-136.
57. Rodriguez J, Deinhardt F. 1960. Preparation of a semipermanent mounting medium for fluorescent antibodies studies. Virology 12:316-317.
58. Schäfer S, Bicker G. 1986. Distribution of GABA-like immunoreactivity in the brain of the honey bee. J Comp Neurol 246:287-300.
59. Scholtz G. 2000. Evolution of the nauplius stage in malacostracan crustaceans. J Zool Syst Evol Res 398:175-187.
60. Schram FR. 1970. Isopods from the Pennsylvanian of Illinois. Science 169:854-855.
61. Seguela P, Geffard M, Buijs RM, Le Moal M. 1984. Antibodies against gamma-aminobutyric acid: specificity studies and immunocytochemical results. Proc Natl Acad Sci U S A 81:3888-3892.
62. Shaw SR. 1989. The retina-lamina pathway in insects particularly Diptera viewed from an evolutionary perspective. In: Stavenga PG, Hardie RC, editors. Facets of vision. Berlin, Heidelberg, New York: Springer Verlag. p 186-212.
63. Shaw SR. 1990. The photoreceptor axon projection and its evolution in the neural superposition eye of some primitive brachyceran Diptera. Brain Behav Evol 35:107-125.
64. Shaw SR, Meinertzhagen IA. 1986. Evolution of synaptic connections among homologous neurons. Proc Natl Acad Sci U S A 83:7961-7965.
65. Shaw SR, Moore D. 1989. Evolutionary remodeling in a visual system through extensive changes in the synaptic connectivity of homologous neurons. Vis Neurosci 3:405-410.
66. Sinakevitch I, Geffard M, Pelhate M, Lapied B. 1996. Anatomy and targets of dorsal unpaired median (DUM) neurons in the terminal abdominal ganglion of the male cockroach Periplaneta americana L. J Comp Neurol 367:147-163.
67. Sinakevitch I, Strausfeld NJ, Douglass JK. 2000. Comparisons of GABAergic organization in insects and isopods support divergent evolution of their visual neuropils. Soc Neurosci Abstr 26:697.
68. Strausfeld NJ. 1971. The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z Zellforsch 121:377-441.
69. Strausfeld NJ. 1976. Atlas of an insect brain. Berlin, Heidelberg, New York: Springer.
70. Strausfeld NJ. 1989. Insect vision and olfaction: common design principles of neuronal organization. In: Singh RN, Strausfeld NJ, editors. Proceedings of the International Conference on the Neural Organization of Sensory Systems (ICONOSS). New York: Plenum. p 319-353.
71. Strausfeld NJ. 1998. Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52:186-206.
72. Strausfeld NJ, Blest AD. 1970. Golgi studies on insects. I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond B 258:81-134.
73. Strausfeld NJ, Campos-Ortega JA. 1977. Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195: 894-897.
74. Strausfeld NJ, Gilbert C. 1992. Small-field neurons associated with oculomotor and optomotor control in muscoid flies. Cellular organization. J Comp Neurol 316:56-71.
75. Strausfeld NJ, Hausen K. 1977. The resolution of neuronal assemblies after cobalt injection into neuropil. Proc R Soc Lond B 199:463-476.
76. Strausfeld NJ, Hildebrand JG. 1999. Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9:634-639.
77. Strausfeld NJ, Lee JK. 1991. Neuronal basis for parallel visual processing in the fly. Vis Neurosci 7:13-33.
78. Strausfeld NJ, Meinertzhagen IA. 1996. The insect neuron: morphologies, structures and relationships to neuroarchitecture. In: Harrison FW, Locke M, editors. Microscopic anatomy of invertebrates. New York: Wiley-Liss. p 487-538.
79. Strausfeld NJ, Nässel DR. 1980. Neuroarchitecture of brain regions that subserve the compound eyes of crustacea and insects. In: Autrum HJ, editor. Handbook of sensory physiology VII/6B. Berlin, Heidelberg, New York: Springer. p 1-132.
80. Strausfeld NJ, Kong A, Milde JJ, Gilbert C, Ramaiah L. 1995. Oculomotor control in calliphorid flies: GABAergic organization in heterolateral inhibitory pathways. J Comp Neurol 361:298-320.
81. Wicklein M, Strausfeld N J. 2000. Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca Sexta. J Comp Neurol 424:356-376.
82. Wildt M, Harzsch S. 2002. A new look at an old visual system: structure and development of the compound eyes and optic ganglia of the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda, Anostraca). J Neurobiol 52:117-132.
83. Wilson K, Cahill V, Ballment E, Benzie J. 2000. The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol Biol Evol 17:863-874.
84. Winther AME, Nassel DR. 2001. Intestinal peptides as circulating hormones: release of tachykinin-related peptide from the midgut of locust and cockroach. J Exp Biol 204:1269-1280.
85. Zawarzin AA. 1913. Histologische Studien über Insekten. 4. Die optischen Ganglien der Aeschnalarven. Z Wiss Zool 108:175-257.
86. Zawarzin AA. 1924. Zur Morphologie der Nervenzentren. Das Bauchmark der Insekten. Ein Beitrag zur vergleichenden Histologie. Z Wiss Zool 122:323-424.