Neural control of the velum in larvae of the gastropod, Ilyanassa obsoleta

Journal of Experimental Biology

Volumn 209, Issue 23, 2006, Pages 4676-4689

  Braubach, Oliver R ^a   Dickinson, Amanda J G ^a,b   Evans, Carol C E ^a,c   Croll, Roger P ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

Cilia; Dopamine; FMRFamide; Leu enkephalin; Mollusc; Monoamines; Muscle; Neuropeptides; Norepinephrine; Serotonin; Veliger

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; EUKARYOTIC FLAGELLUM; GASTROPOD; HISTOLOGY; LARVA; MOTOR ACTIVITY; NERVE CELL; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CILIA; GASTROPODA; LARVA; MOTOR ACTIVITY; NEURONS;

ANIMALIA; CAENOGASTROPODA; EUKARYOTA; GASTROPODA; ILYANASSA OBSOLETA; MOLLUSCA;

EID: 33845964604     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.02556     Document Type: Article

References (82)

1. Aiello, E. (1990). Nervous control of gill ciliary activity in Mytilus edulis. In Neurobiology of Mytilus edulis (ed. G. B. Stefano), pp. 189-208. Manchester, New York: Manchester University Press.
2. Amenta, F., Bronzetti, E., Felici, L., Ricci, A. and Tayebati, S. K. (1999). Dopamine D2-like receptors on human peripheral blood lymphocytes: a radioligand binding assay and immunocytochemical study. J. Auton. Pharmacol. 19, 151-159.
3. Arkett, S. A., Mackie, G. O. and Single, C. L. (1987). Neuronal control of ciliary locomotion in a gastropod veliger (Calliostoma). Biol. Bull. 173, 513-526.
4. Arkett, S. A., Chia, F., Goldberg, J. I. and Koss, R. (1989). Identified settlement receptor cells in a nudibranch veliger respond to specific cue. Biol. Bull. 176, 155-160.
5. Ascher, P. (1972). Inhibitory and excitatory effects of dopamine on Aplysia neurones. J. Physiol. 225, 173-209.
6. Audesirk, G., McCaman, R. E. and Willows, A. O. D. (1979). The role of serotonin in the control of pedal ciliary activity by identified neurons in Tritonia diomedea. Comp. Biochem. Physiol. 62, 87-91.
7. Beiras, R. and Widdows, J. (1995). Effects of the neurotransmitters dopamine, serotonin and norepinephrine on the ciliary activity of mussel (Mytilis edulis) larvae. Mar. Biol. 122, 597-603.
8. Blake, J. R. and Sleigh, M. A. (1974). Mechanics of ciliary locomotion. Biol. Rev. Camb. Philos. Soc. 49, 85-125.
9. Brezden, B. L., Yeoman, M. S., Gardner, D. R. and Benjamin, P. R. (1999). FMRFamide-activated Ca2+ channels in Lymnaea heart cells are modulated by 'SEEPLY', a neuropeptide encoded on the same gene. J. Neurophysiol. 81, 1818-1826.
10. Cadet, P. (2004). Nitric oxide modulates the physiological control of ciliary activity in the marine mussel Mytilus edulis via morphine: novel mu opiate receptor splice variants. Neuro Endocrinol. Lett. 25, 184-190.
11. Cain, S. D. and Woodward, O. H. (2002). The use of multiple transmitters controlling ciliary beating on the foot on the sea slug, Tritonia diomedea. Integr. Comp. Biol. 42, 1205.
12. Cann-Moisan, C., Nicolas, L. and Robert, R. (2002). Ontogenetic changes in the contents of dopamine, norepinephrine and serotonin in larvae and postlarvae of the bivalve Pecten maximus. Aquat. Living Resour. 15, 313-318.
13. Carter, G. S. (1928). On the structure of the cells bearing the velar cilia of the nudibranch veliger. J. Exp. Biol. 6, 97-109.
14. Catapane, E. J. (1983). Comparative study of the control of lateral ciliary activity in marine bivalves. Comp. Biochem. Physiol. 75C, 403-405.
15. Chase, R. (2002). Behavior and its Neural Control in Gastropod Molluscs. New York: Oxford University Press.
16. Chia, F. S. and Buckland-Nicks, J. (1984). Locomotion of marine invertebrate: a review. Can. J. Zool. 62, 1205-1222.
17. Cole, A. G., Mashkournia, A., Parries, S. C. and Goldberg, J. I. (2002). Regulation of early embryonic behavior by nitric oxide in the pond snail Helisoma trivolvis. J. Exp. Biol. 205, 3143-3152.
18. Coon, S. L., Bonar, D. B. and Weiner, R. M. (1985). Induction of settlement and metamorphosis of the Pacific oyster, Crassostrea gigas (Thunberg) by L-DOPA and catecholamines. J. Exp. Mar. Biol. Ecol. 94, 211-221.
19. Couper, J. M. and Leise, E. M. (1996). Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biol. Bull. 191, 178-186.
20. Croll, R. P. (2000). Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails. Microsc. Res. Tech. 49, 570-578.
21. Croll, R. P. and Dickinson, A. J. G. (2004). Form and function of the larval nervous system in molluscs. Invertebr. Reprod. Dev. 46, 173-187.
22. Croll, R. P. and Voronezhskaya, E. E. (1995). Early FMRFamide-like immunoreactive cells in gastropod neurogenesis. Acta Biol. Hung. 46, 295-303.
23. Croll, R. P., Jackson, D. L. and Voronezhskaya, E. E. (1997). Catecholamine-containing cells in larval and post-larval bivalve molluscs. Biol. Bull. 193, 116-124.
24. Degnan, B. M., Degnan, S. M., Fentenany, G. and Morse, D. E. (1997). A Mox homeobox gene in the gastropod mollusc Haliotis rufescens is differentially expressed during larval morphogenesis and metamorphosis. FEBS Lett. 411, 119-122.
25. Dickinson, A. J. G. (2002). Neural and Muscular Development in Gastropod Larva. PhD thesis, Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada.
26. Dickinson, A. J. G. and Croll, R. P. (2003). Development of the larval nervous system of the gastropod Ilyanassa obsoleta. J. Comp. Neurol. 466, 197-218.
27. Dickinson, A. J. G., Nason, J. and Croll, R. P. (1999). Histochemical localization of FMRFamide, serotonin and catecholamine in embryonic Crepidula fornicata (Prosobranchia: Gastropoda). Zoomorphology 119, 49-62.
28. Dickinson, A. J., Croll, R. P. and Voronezhskaya, E. E. (2000). Development of embryonic cells containing serotonin, catecholamines, and FMRFamide-related peptides in Aplysia californica. Biol. Bull. 199, 305-315.
29. Diefenbach, T. J., Koehncke, N. K. and Goldberg, J. I. (1991). Characterization and development of rotational behavior in Helisoma embryos: Role of endogenous serotonin. J. Neurobiol. 22, 922-934.
30. Doran, S. A., Tran, C. H., Eskicioglu, C., Stachniak, T., Ahn, K. C. and Goldberg, J. I. (2003). Constitutive and permissive roles of nitric oxide activity in embryonic ciliary cells. Am. J. Physiol. 285, R348-R355.
31. Doran, S. A., Koss, R., Tran, C. H., Christopher, K. J., Gallin, W. J. and Goldberg, J. I. (2004). Effect of serotonin on ciliary beating and intracellular calcium concentration in identified populations of embryonic ciliary cells. J. Exp. Biol. 207, 1415-1429.
32. Fong, P. P., Huminski, P. T. and D'Urso, L. M. (1998). Induction and potentiation of parturition in fingernail clams (Sphaerium striatinum) by selective serotonin re-uptake inhibitors (SSRIs). J. Exp. Zool. 280, 260-264.
33. Fox, L. E. and Lloyd, P. E. (2002). Mechanisms involved in persistent facilitation of neuromuscular synapses in Aplysia. J. Neurophysiol. 87, 2018-2030.
34. Fretter, V. (1967). The prosobranch veliger. Proc. Malacol. Soc. London 37, 357-366.
35. Fuller, R. W. (1996). Fluoxetine effects on serotonin function and aggressive behavior. Ann. NY Acad. Sci. 794, 90-97.
36. Gainey, L. F., Jr, Vining, K. J., Doble, K. E., Waldo, J. M., Candelario-Martinez, A. and Greenberg, M. J. (1999). An endogenous SCP-related peptide modulates ciliary beating in the gills of a venerid clam, Mercenaria mercenaria. Biol. Bull. 197, 159-173.
37. Geerts, I. S., Matthys, K. E., Herman, A. G. and Bult, H. (1999). Involvement of 5-HT1B receptors in collar-induced hypersensitivity to 5-hydroxytryptamine of the rabbit carotid artery. Br. J. Pharmacol. 127, 1327-1336.
38. 2+ regulates the phosphorylation and the dephosphorylation of ciliary proteins via the NO pathway. J. Gen. Physiol. 124, 527-540.
39. Green, K. A., Harris, S. J. and Cottrell, G. A. (1996). Dopamine directly activates a ligand-gated channel in snail neurones. Pflugers Arch. 431, 639-644.
40. Heiss, W. D., Hoyer, J. and Thalhammer, G. (1976). Antipsychotic drugs and dopamine-mediated responses in Aplysia neurons. J. Neural Transm. 39, 187-208.
41. Hernadi, L., Erdelyi, L., Hiripi, L. and Elekes, K. (1998). The organization of serotonin-, dopamine-, and FMRFamide-containing neuronal elements and their possible role in the regulation of spontaneous contraction of the gastrointestinal tract in the snail Helix pomatia. J. Neurocytol. 27, 761-775.
42. Hurwitz, I., Cropper, E. C., Vilim, F. S., Alexeeva, V., Susswein, A. J., Kupfermann, I. and Weiss, K. R. (2000). Serotonergic and peptidergic modulation of the buccal mass protractor muscle (12) in Aplysia. J. Neurophysiol. 84, 2810-2820.
43. Kandel, E. R. (1976). Cellular Basis of Behavior. San Francisco: Freeman.
44. Kempf, S. C., Page, L. R. and Pires, A. (1997). 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. J. Comp. Neurol. 386, 507-528.
45. Kuang, S., Doran, S. A., Wilson, R. J., Goss, G. G. and Goldberg, J. I. (2002). Serotonergic sensory-motor neurons mediate a behavioral response to hypoxia in pond snail embryos. J. Neurobiol. 52, 73-83.
46. Kupfermann, I. and Weiss, K. R. (1982). Activity of an identified serotonergic neuron in free moving Aplysia correlates with behavioral arousal. Brain Res. 241, 334-337.
47. Leise, E. M. and Hadfield, M. G. (2000). An inducer of molluscan metamorphosis transforms activity patterns in a larval nervous system. Biol. Bull. 199, 241-250.
48. Lin, M. F. and Leise, E. M. (1996). Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta. J. Comp. Neurol. 374, 180-193.
49. Longin, A., Souchier, C., Ffrench, M. and Bryon, P. A. (1993). Comparison of anti-fading agents used in fluorescence microscopy: image analysis and laser confocal microscopy study. J. Histochem. Cytochem. 41, 1833-1840.
50. Mackie, G. O., Singla, C. L. and Thiriot-Quievreux, C. (1976). Nervous control of ciliary activity in gastropod larvae. Biol. Bull. 151, 182-199.
51. Malanga, C. J. (1975). Dopaminergic stimulation of fromtal ciliary activity in the gill of Mytilus edulis. Comp. Biochem. Physiol. 51C, 25-34.
52. Marois, R. and Carew, T. J. (1997a). Ontogeny of serotonergic neurons in Aplysia californica. J. Comp. Neurol. 386, 477-490.
53. Marois, R. and Carew, T. J. (1997b). Projection patterns and target tissues of serotonergic cells in larval Aplysia californica. J. Comp. Neurol. 386, 491-506.
54. Marois, R. and Croll, R. P. (1991). Factors influencing hatching synchrony within the egg mass of the pond snail, Lymnaea stagnalis. Invertebr. Reprod. Dev. 19, 139-146.
55. Marois, R. and Croll, R. P. (1992). Development of serotonergic cells within the embryonic central nervous system of the pond snail, Lymnaea stagnalis. J. Comp. Neurol. 322, 255-265.
56. 2+ and catecholamines on swimming cilia of the trochophore larva of the polychaete Spirobranchus giganteus (Pallas). J. Exp. Mar. Biol. Ecol. 95, 245-255.
57. McCaman, M. W. (1984). Neurochemistry of invertebrates. In Handbook of Neurochemistry. Vol. 7 (ed. A. Lajtha), pp. 613-700. New York: Plenum Press.
58. Miller, S. E. and Hadfield, M. G. (1986). Ontogeny of phototaxis and metamorphic competence in larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). J. Exp. Mar. Biol. Ecol. 97, 95-112.
59. Nilsson, S. and Holmgren, S. (1994). Comparative Physiology and Evolution of the Autonomic Nervous System. Chur, Switzerland: Harwood Academic Publishers.
60. Page, L. R. and Parries, S. C. (2000). Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J. Comp. Neurol. 418, 383-401.
61. Pani, A. K. and Croll, R. P. (1995). Distribution of catecholamines, indoleamines, and their precursors and metabolites in the scallop, Placopecten magellanicus (Bivalvia, Pectinidae). Cell. Mol. Neurobiol. 15, 371-386.
62. Paparo, A. A. and Murphy, J. A. (1975). The effect of Ca on the rate of beating of lateral cilia in Mytilus edulis. I. A response to perfusion with 5-HT, DA, BOL and PBZ. Comp. Biochem. Physiol. 50C, 9-14.
63. Pechenik, J. A., Li, W. and Cochrane, D. E. (2002). Timing is everything: the effects of putative dopamine antagonists on metamorphosis vary with larval age and experimental duration in the prosobranch gastropod Crepidula fornicata. Biol. Bull. 202, 137-147.
64. Pires, A. and Penniman, J. R. (2003). Neural correlates of settlement and metamorphic competence in gastropod veliger larvae. Program No. 606.16.2003 Abstract Viewer/Itinerary Planner, Washington, DC. Society for Neuroscience, 2003. Online.
65. Pires, A., Croll, R. P. and Hadfield, M. G. (2000a). Catecholamines modulate metamorphosis in the opisthobranch gastropod, Phestilla sibogae. Biol. Bull. 198, 319-331.
66. Pires, A., Guilbault, T. R., Mitten, J. V. and Skiendzielewski, J. A. (2000b). Catecholamines in larvae and juveniles of the prosobranch gastropod, Crepidula fornicata. Comp. Biochem. Physiol. 127C, 37-47.
67. Plummer, J. T. (2002). The bivalve larval nervous system. MSc Thesis, Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada.
68. Seeman, P. (2002). Atypical antipsychotics: mechanism of action. Can. J. Psychiatry 47, 27-38.
69. Stommel, E. W. and Stephens, R. E. (1985). Cyclic AMP and calcium in the differential control of Mytilus gill cilia. J. Comp. Physiol. A 157, 451-459.
70. Strathmann, R. R. and Leise, E. M. (1979). On feeding mechanisms and clearance rates of mulluscan veligers. Biol. Bull. 157, 524-535.
71. Surman, A. J. and Doggrell, S. A. (1993). Alprenolol and bromoacetylalprenololmenthane are competitive slowly reversible antagonists at the beta 1-adrenoceptors of rat left atria. J. Cardiovasc. Pharmacol. 21, 35-39.
72. Swann, J. W., Pierson, M. G. and Dahlstrom, A. (1982a). Dopaminergic innervation of Aplysia gill muscle. Cell. Mol. Neurobiol. 2, 325-331.
73. Swann, J. W., Sinback, C. N., Kebabian, P. R. and Carpenter, D. O. (1982b). Motoneurons which may utilize dopamine as their neurotransmitter. Cell. Mol. Neurobiol. 2, 309-324.
74. Swann, J. W., Sinback, C. N., Pierson, M. G. and Carpenter, D. O. (1982c). Dopamine produces muscle contractions and modulates motoneuron-induced contractions in Aplysia gill. Cell. Mol. Neurobiol. 2, 291-308.
75. Testa, R., Guarneri, L., Ibba, M., Strada, G., Poggesi, E., Taddei, C., Simonazzi, I. and Leonardi, A. (1993). Characterization of alpha I-adrenoceptor subtypes in prostate and prostatic urethra of rat, rabbit, dog and man. Eur. J. Pharmacol. 249, 307-315.
76. Thavaradhara, K. and Leise, E. M. (2001). Localization of nitric oxide synthase-like immunoreactivity in the developing nervous system of the snail Ilyanassa obsoleta. J. Neurocytol. 30, 449-456.
77. Uhler, G. C., Huminski, P. T., Les, F. T. and Fong, P. P. (2000). Cilia-driven rotational behavior in gastropod (Physa elliptica) embryos induced by serotonin and putative serotonin reuptake inhibitors (SSRIs). J. Exp. Zool. 286, 414-421.
78. Voronezhskaya, E. E., Pavlova, G. A. and Sakharov, D. A. (1993). Effects of haloperidol and methylergometrine on embryonic motility and development of the pond snail Lymnaea stagnalis [in Russian]. Ontogenesis 24, 40-47.
79. Voronezhskaya, E. E., Hiripi, L., Elekes, K. and Croll, R. P. (1999). Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis. I: Embryonic development of dopaminergic neurons and dopamine-dependent behaviours. J. Comp. Neurol. 404, 297-309.
80. Wada, Y., Mogami, Y. and Baba, S. A. (1997). Modification of ciliary beating in sea urchin larvae induced by neurotransmitters: Beat-plane rotation and control of frequency fluctuation. J. Exp. Biol. 200, 9-18.
81. Willins, D. L., Berry, S. A., Alsayegh, L., Backstrom, J. R., Sanders-Bush, E., Friedman, L. and Roth, B. L. (1999). Clozapine and other 5-hydroxytryptamine-2A receptor antagonists alter the subcellular distribution of 5-hydroxytryptamine-2A receptors in vitro and in vivo. Neuroscience 91, 599-606.
82. Willows, A. O. D., Pavlova, G. A. and Phillips, N. E. (1997). Modulation of ciliary beat frequency by neuropeptides from identified molluscan neurons. J. Exp. Biol. 200, 1433-1439.