Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ

Journal of Comparative Neurology

Volumn 386, Issue 3, 1997, Pages 507-528

  Kempf, Stephen C ^a,d   Page, Louise R ^b   Pires, Anthony ^c  

^a AUBURN UNIVERSITY   (United States)

^b UNIVERSITY OF VICTORIA   (Canada)

^c DICKINSON COLLEGE   (United States)

^d AUBURN UNIVERSITY   (United States)

Author keywords

Apical ganglion; Apical organ; Immunocytochemistry; Larva; Ultrastructure; Veliger

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; EMBRYO DEVELOPMENT; IMMUNOHISTOCHEMISTRY; LARVAL DEVELOPMENT; MOLLUSC; NERVE CELL NETWORK; NERVE GROWTH; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; SENSE ORGAN; SEROTONINERGIC NERVE CELL;

ANIMALS; AXONS; CELL MEMBRANE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DENDRITES; EMBRYO, NONMAMMALIAN; GANGLIA, INVERTEBRATE; IMMUNOHISTOCHEMISTRY; LARVA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MOLLUSCA; NERVOUS SYSTEM; NEURONS; SEROTONIN; SPECIES SPECIFICITY;

EID: 0030768867     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970929)386:3<507::AID-CNE12>3.0.CO;2-7     Document Type: Article

References (85)

1. Aiello, E. (1974) Control of ciliary activity in metazoa. In M.A. Sleigh (ed): Cilia and Flagella. London: Academic Press, pp. 353-376.
2. Arkett, S.A., F.-S. Chia, J.I. Goldberg, and R. Koss (1989) Identified settlement receptor cells in a nudibranch veliger respond to specific cue. Biol. Bull. 176:155-160.
3. Audesirk, G. (1978) Properties of central motor neurons exciting locomotory cilia in Tritonia diomedea. J. Comp. Physiol. A. 128:259-267.
4. Audesirk, G., R.E. McCaman, and A.O.D. Willows (1979) The role of serotonin in the control of pedal ciliary activity by identified neurons in Tritonia diomedea. Comp. Biochem. Physiol. 62C:87-91.
5. Barlow, L.A., and J.W. Truman (1992) Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone Haliotis rufescens. J. Neurobiol. 23:829-844.
6. Bickell, L.R., and S.C. Kempf (1983) Larval and metamorphic morphogenesis in the nudibranch Melibe leonina (Mollusca: Opisthobranchia). Biol. Bull. 165:119-138.
7. Bisgrove, B.W., and R.D. Burke (1986) Development of serotonergic neurons in embryos of the sea urchin Strongylocentrotus purpuratus. Dev. Growth Dif. 28:569-574.
8. Bisgrove, B.W., and R.D. Burke (1987) Development of the nervous system of the pluteus larva of Strongylocentrotus droebachiensis. Cell Tissue Res. 248:335-343.
9. Bonar, D.B. (1978) Ultrastructure of a cephalic sensory organ in larvae of the gastropod Phestilla sibogae (Aeolidacea, Nudibranchia). Tissue Cell. 10:153-165.
10. Bonar, D.B., and M.G. Hadfield (1974) Metamorphosis of the marine gastropod Phestilla sibogae Bergh (Nudibranchia: Aeolidacea). I. Light and electron microscopic analysis of larval and metamorphic stages. J. Exp. Marine Biol. Ecol. 16:227-255.
11. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye binding. Anal. Biochem. 72:248-254.
12. Burke, R.D. (1978) The structure of the nervous system of the pluteus larva of Strongylocentrotus purpuratus. Cell Tissue Res. 191:233-247.
13. Burke, R.D. (1983) Neural control of metamorphosis in Dendraster excentricus. Biol. Bull. 164:176-188.
14. Burke, R.D., D.G. Brand, and B.W. Bisgrove (1986) Structure of the nervous system of the auricularia larva of Parastichopus californicus. Biol. Bull. 170:450-460.
15. Buznikov, G.A., and B.N. Manukhin (1962) The effect of serotonin on motor activity in nudibranch embryos. Zh. Obshch. Biol. 21:347-352.
16. Carroll, D.J., and S.C. Kempf (1990) Laboratory culture of the aeolid nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia): Some aspects of its development and life history. Biol. Bull. 179:243-253.
17. Carroll, D.J., and S.C. Kempf (1994) Changes occur in the central nervous system of the nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia) during metamorphosis. Biol. Bull. 186:202-212.
18. Chia, F.-S., and R. Koss (1979) Fine structural studies of the nervous system and apical organ in the planula larva of the sea anemone Anthopleura elegantissima. J. Morphol. 160:275-298.
19. Chia, F.-S., and R. Koss (1984) Fine structure of the cephalic sensory organ in the larva of the nudibranch Rostanga pulchra (Mollusca, Opisthobranchia, Nudibranchia). Zoomorphol. 104:131-139.
20. Conklin, E.G. (1897) The embryology of Crepidula. J. Morphol. 13:1-226.
21. Couper, J.M., and E.M. Leise (1996) Serotonin injections induce metamorphosis in larvae of the gastropod mollusc. Ilyanassa obsoleta. Biol. Bull. 191:178-186.
22. Cragg, S.M., and D.J. Crisp (1991) The biology of scallop larvae. In S.E. Shumway (ed): Biology, Ecology and Aquaculture of Scallops. Amsterdam: Elsevier, pp. 75-132.
23. Diefenbach, T.J., N.K. Koehncke, and J.I. Goldberg (1991) Characterization and development of rotational behavior in Helisoma embryos: Role of endogenous serotonin. J. Neurobiol. 22:922-934.
24. Elekes, K. (1991) Serotonin-immunoreactive varicosities in the cell body layer and neural sheath of the snail, Helix pomatia, ganglia: An electron microscopic immunocytochemical study. Neuroscience 42:583-591.
25. Giloh, H., and J.W. Sedat (1982) Fluorescence microscopy: Reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. Science 217:1252-1255.
26. Goldberg, J.L, N.K. Koehncke, K.J. Christopher, C. Neumann, and T.J. Diefenbach (1994) Pharmacological characterization of a serotonin receptor involved in an early embryonic behavior of Helisoma trivolvis. J. Neurobiol. 25:1545-1557.
27. Harris, L.G. (1975) Studies on the life history of two coral-eating nudibranchs of the genus Phestilla. Biol. Bull. 149:539-550.
28. Hay-Schmidt, A. (1989) The nervous system of the actinotroch larva of Phoronis muelleri (Phoronida). Zoomorphol. 108:333-351.
29. Hay-Schmidt, A. (1990a) Distribution of catecholamine-containing, serotonin-like and neuropeptide FMRFamide-like immunoreactive neurons and processes in the nervous system of the actinotroch larva of Phoronis muelleri (Phoronida). Cell Tissue Res. 259:105-118.
30. Hay-Schmidt, A. (1990b) Catecholamine-containing, serotonin-like, and FMRFamide-like immunoreactive neurons and processes in the nervous system of the early actinotroch larva of Phoronis vancouverensis (Phoronida): Distribution and development. Can. J. Zool. 68:1525-1536.
31. Hay-Schmidt, A. (1990c) Catecholamine-containing, serotonin-like and neuropeptide FMRFamide-like immunoreactive cells and processes in the nervous system of the pilidium larva (Nemertini). Zoomorphol. 700:231-244.
32. Hay-Schmidt, A. (1992) Ultrastructure and immunohistochemistry of the nervous system of the larvae of Lingula anatina and Glottidia sp. (Brachiopoda). Zoomorphol. 112:189-205.
33. Hay-Schmidt, A. (1995) The larval nervous system of Polygordius lacteus Scheinder, 1868 (Polygordiidae, Polychaeta): Immunocytochemical data. Acat Zoologica. 76:121-140.
34. Hernadi, L., K. Elekes, and K.S.-Rosa (1989) Distribution of serotonin-containing neurons in the central nervous system of the snail Helix pomatia. Comparison of immunocytochemical and 5,6-dihydroxytryptamine labeling. Cell Tissue Res. 257:313-323.
35. Jagersten, G. (1972) Evolution of the Metazoan Life Cycle. London: Academic Press.
36. Kempf, S.C., and A.O.D. Willows (1977) Laboratory culture of the nudibranch Tritonia diomedea Bergh (Tritoniidae: Opisthobranchia) and some aspects of its behavioral development. J. Exp. Marine Biol. Ecol. 30:261-276.
37. Kempf, S.C., B. Masinovsky, and A.O.D. Willows (1987) A simple neuronal system characterized by a monoclonal antibody to SCP neuropeptides in embryos and larvae of Tritonia diomedea (Gastropoda, Nudibranchia). J. Neurobiol. 18:217-236.
38. Kempf, S.C., A. Saini, and A. Jones (1991) The ontogeny of neural systems expressing SCP-like and serotonin-like antigens in Berghia verrucicornis. Soc. Neurosci. Abstr. 17:1356.
39. Kempf, S.C., G.V. Chun, and M.G. Hadfield (1992) An immunocytochemical search for potential neurotransmitters in larvae of Phestilla sibogae (Gastropoda, Opisthobranchia). Comp. Biochem. Physiol. 101C:299-305.
40. Korobstsov, G.N., and D.A. Sakharov (1971) The role of ionic environment in nervous and hormonal control of ciliary beating in molluscan larvae. Zh. Evol. Biokhim. Fisiol. 7:238-240.
41. Koshtoyants, K.S., G.A. Buznikov, and B.N. Manukhin (1961) The possible role of 5-hydroxytryptamine in the motor activity of embryos of some marine gastropods. Comp. Biochem. Physiol. 3:20-26.
42. Krstulovic, A.M. (1982) Investigations of catecholamine metabolism using high-performance liquid chromatography: Analytical methodology and clinical applications. J. Chromatogr. 229:1-34.
43. Lacalli, T.C. (1981) Structure and development of the apical organ in trochophores of Spirobranchus polycerus, Phyllodoce maculata, and Phyllodoce mucosa (Polychaeta). Proc. R. Soc. London B 212:381-402.
44. Lacalli, T.C. (1983) The brain and central nervous system of Muller's larva. Can. J. Zool. 61:39-51.
45. Lacalli, T.C. (1984) Structure and organization of the nervous system in the trochophore larva of Spirobranchus. Phil. Trans. R. Soc. London B 306:79-135.
46. Lacalli, T.C. (1990) Structure and organization of the nervous system in the actinotroch larva of Phoronis vancouverensis. Phil. Trans. R. Soc. London B 327:655-685.
47. Lacalli, T.C. (1994) Apical organs, epithelial domains, and the origin of the chordate central nervous system. Am. Zool. 34:533-541.
48. Leise, E.M. (1996) The fluorescent dye DASPEI selectively stains the apical ganglion in larval Ilyanassa obsoleta (Mollusca, Gastropoda). Microsc. Res. Tech. 33:496-500.
49. Leise, E.M., and M.G. Hadfield (1991) Chemosensory response to metamorphic inducer activates a central pattern generator in a larval mollusc. Soc. Neurosci. Abstr. 17:1391.
50. Lin, M.-F., and E.M. Leise (1996a) Gangliogenesis in the prosobranch gastropod Ilyanassa ohsoleta. J. Comp. Neurol. 374:180-193.
51. Lin, M.-F., and E.M. Leise (1996b) NADPH-diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod mollusc Ilyanassa obsoleta. J. Comp. Neurol. 374:194-203.
52. Mackie, G.O., A.N. Spencer, and R. Strathmann (1969) Electrical activity associated with ciliary reversal in an echinoderm larva. Nature. 223:1384-1385.
53. Mackie, G.O., C.L. Singla, and C. Thiriot-Quievreux (1976) Nervous control of ciliary activity in gastropod larvae. Biol. Bull. 151:182-199.
54. Marois, R., and T.J. Carew (1989) Pre-metamorphic development of serotonin immunoreactivity in Aplysia. Soc. Neurosci. Abstr. 15:1121.
55. Marois, R., and T.J. Carew (1990) The gastropod nervous system in metamorphosis. J. Neurobiol. 21:1053-1071.
56. Marois, R., and R.P. Croll (1992) Development of serotonin-like immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J. Comp. Neurol. 322:255-265.
57. Marois, R., G.M. Kelly, S. Hockfield, and T.J. Carew (1992) An ultrastructural study of serotonergic cells in the CNS of embryonic and larval Aplysia. Soc. Neurosci. Abstr. 18:1471.
58. Marois, R., P. Hofstadter, and T.J. Carew (1993) Birthdate and identification of serotonergic cells in embryonic and larval Aplysia. Soc. Neurosci. Abstr. 19:1287.
59. B: Immunolabeling of neurons in diverse invertebrates. J. Comp. Neurol. 273:500-512.
60. Miller, S. E., and M.G. Hadfield (1986) Ontogeny of phototaxis and metamorphic competence in larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). J. Exp. Marine Biol. Ecol. 97:95-112.
61. Nakajima, Y. (1986) Presence of a ciliary patch in preoral epithelium of sea urchin plutei. Dev. Growth Dif. 28:243-249.
62. Nakajima, Y. (1988) Serotonergic nerve cells of starfish larvae. In R.D. Burke, P.V. Mladenov, P. Lambert, and R.L. Parsley (eds): Echinoderm Biology. Rotterdam: A.A. Balkema, pp. 235-239.
63. Nakajima, Y., R.D. Burke, and Y. Noda (1993) The structure and development of the apical ganglion in the sea urchin pluteus larvae of Strongylocentrotus drobachiensis and Imespilia globulus. Dev. Growth Dif. 35:531-538.
64. Page, L.R. (1992a) New interpretation of a nudibranch central nervous system based on ultrastructural analysis of neurodevelopment in Melibe leonina. I. Cerebral and visceral loop ganglia. Biol. Bull. 182:348-365.
65. Page, L.R. (1992b) New interpretation of a nudibranch central nervous system based on ultrastructural analysis of neurodevelopment in Melibe leonina. II. Pedal, pleural, and labial ganglia. Biol. Bull. 182:366-381.
66. Page, L.R. (1993) Developmental analysis reveals labial and subradular ganglia and the primary framework of the nervous system in nudibranch gastropods. J. Neurobiol. 24:1443-1459.
67. Page, L.R. (1995) Similarities in form and developmental sequence for three larval shell muscles in nudibranch gastropods. Acta Zool. 76:177-191.
68. Pawlik, J.R. (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr. Marine Biol. Annu. Rev. 30:273-335.
69. Pelseneer, P. (1911) Recherches sur l'embryologie des gastropodes. Mem. Acad. R. Belg. Cl. Sci. 3:1-167.
70. Pires, A., and M.G. Hadfield (1991) Oxidative breakdown products of catecholamines and hydrogen peroxide induce partial metamorphosis in the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). Biol. Bull. 180:310-317.
71. Ram, J.L., F. Zhang, and L.-X. Liu (1991) Contraction, serotonin-elicited modulation, and membrane currents of dissociated fibers of Aplysia buccal muscles. Biol. Bull. 180:276-283.
72. Riggin, R.M., and RT. Kissinger (1977) Determination of catecholamines in urine by reverse-phase liquid chromatography with electrochemical detection. Anal. Chem. 49:2109-2111.
73. Ruppert, E.E. (1978) A review of metamorphosis of turbellarian larvae. In F.S. Chia and M.E. Rice (eds): Settlement and Metamorphosis of Marine Invertebrate Larvae. New York: Elsevier/North Holland Biomedical Press, pp. 65-81.
74. Satterlie, R.A. (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina II. Peripheral modulatory neurons. J. Exp. Biol. 198:905-916.
75. Satterlie, R.A., and T.P. Norekian (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. III. Cerebral neurons. Exp. Biol. 198:917-930.
76. Satterlie, R.A., T.P. Norekian, S. Jordan, and C.J. Kazilek (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. I. Serotonin immunoreactivity in the central nervous system and wings. J. Exp. Biol. 198:895-904.
77. Smith, F.G.W. (1935) The development of Patella vulgata. Phil. Trans. R. Soc. London B 225:95-125.
78. Switzer-Dunlap, M., and M.G. Hadfield (1977) Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory culture. J. Exp. Marine Biol. Ecol. 29:245-261.
79. Syed, N.I., and W. Winlow (1989) Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea stagnalis (L.). Comp. Biochem. Physiol. 93A:633-644.
80. Tardy, J. (1974) Morphogenese du system nerveux chez les mollusques nudibranches. Haliotis 4:61-75.
81. Tardy, J., and S. Dongard (1993) Le complexe apical de la veligere de Ruditapes philippinarum (Adams et Reeve, 1850) mollusque bivalve Veneride. C.R. Acad. Sci. Paris 316:177-184.
82. Thorndyke, M.C., B.D. Crawford, and R.D. Burke (1992) Localization of a SALMFamide neuropeptide in the larval nervous system of the sand dollar Dendraster excentricus. Acta Zool 73:207-212.
83. Uthe, D. (1995) Fine structure of the cephalic sensory organ in veliger larvae of Littorina littorea, (L.) (Mesogastropoda, Littorinidae). Hydrobiologia 309:45-52.
84. Werner, B. (1955) Uber die anatomie, die entwickling und biologie des veligers und der veliconcha von Crepidula fornicata (L.) (Gastropoda Prosobranchia). Helgoland. wiss. Meeresunters. 4:260-315.
85. Wilson, E.B. (1892) The cell lineage of Nereis. J. Morphol. 6:361-481.