Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails

Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular neurobiology. Recent work has exploited both these fields of study by examining the ontogeny of the nervous system in these animals. Much of this...

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Published inMicroscopy research and technique Vol. 49; no. 6; pp. 570 - 578
Main Author Croll, Roger P.
Format Journal Article
LanguageEnglish
Published New York John Wiley & Sons, Inc 15.06.2000
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Online AccessGet full text
ISSN1059-910X
1097-0029
DOI10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q

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Abstract Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular neurobiology. Recent work has exploited both these fields of study by examining the ontogeny of the nervous system in these animals. Much of this work has focussed upon the development of specific transmitter phenotypes to provide vignettes of neuronal subpopulations that can be traced from early embryonic life through to adulthood. While such studies have generally confirmed previous explanations of gangliogenesis in gastropods, they have also indicated the presence of several neurons that appear earlier and in positions inconsistent with classical views of gastropods neurogenesis. The earliest of these cells contain FMRFamide‐related peptides and have anteriorly projections that mark the future locations of ganglia and interconnecting pathways that will comprise the postembryonic central nervous system. These posterior, peptidergic cells, as well as certain, apical, monoaminergic neurons, disappear and apparently die near the end of embryonic life. Finally, populations of what appear to be peripheral sensory neurons begin to express catecholamines by around midway through embryonic life. Like several of the neurons expressing a variety of transmitters in the developing central ganglia, the catecholaminergic peripheral cells persist into postembryonic life. Transmitter phenotypes, cell shapes and locations, and neuritic morphologies all suggest that many of the neurons observed in early embryonic pond snails have recognizable homologues across the molluscs. Such observations have profoundly altered our views of neurogenesis in gastropods over the last few years. They also suggest the promise for pond snails as fruitful models for studying the roles and mechanisms for pioneering fibres, cues triggering apoptosis, and contrasting origins and mechanisms employed for generating central vs. peripheral neurons within a single organism. Microsc. Res. Tech. 49:570–578, 2000. © 2000 Wiley‐Liss, Inc.
AbstractList Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular neurobiology. Recent work has exploited both these fields of study by examining the ontogeny of the nervous system in these animals. Much of this work has focussed upon the development of specific transmitter phenotypes to provide vignettes of neuronal subpopulations that can be traced from early embryonic life through to adulthood. While such studies have generally confirmed previous explanations of gangliogenesis in gastropods, they have also indicated the presence of several neurons that appear earlier and in positions inconsistent with classical views of gastropods neurogenesis. The earliest of these cells contain FMRFamide-related peptides and have anteriorly projections that mark the future locations of ganglia and interconnecting pathways that will comprise the postembryonic central nervous system. These posterior, peptidergic cells, as well as certain, apical, monoaminergic neurons, disappear and apparently die near the end of embryonic life. Finally, populations of what appear to be peripheral sensory neurons begin to express catecholamines by around midway through embryonic life. Like several of the neurons expressing a variety of transmitters in the developing central ganglia, the catecholaminergic peripheral cells persist into postembryonic life. Transmitter phenotypes, cell shapes and locations, and neuritic morphologies all suggest that many of the neurons observed in early embryonic pond snails have recognizable homologues across the molluscs. Such observations have profoundly altered our views of neurogenesis in gastropods over the last few years. They also suggest the promise for pond snails as fruitful models for studying the roles and mechanisms for pioneering fibres, cues triggering apoptosis, and contrasting origins and mechanisms employed for generating central vs. peripheral neurons within a single organism.
Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular neurobiology. Recent work has exploited both these fields of study by examining the ontogeny of the nervous system in these animals. Much of this work has focussed upon the development of specific transmitter phenotypes to provide vignettes of neuronal subpopulations that can be traced from early embryonic life through to adulthood. While such studies have generally confirmed previous explanations of gangliogenesis in gastropods, they have also indicated the presence of several neurons that appear earlier and in positions inconsistent with classical views of gastropods neurogenesis. The earliest of these cells contain FMRFamide-related peptides and have anteriorly projections that mark the future locations of ganglia and interconnecting pathways that will comprise the postembryonic central nervous system. These posterior, peptidergic cells, as well as certain, apical, monoaminergic neurons, disappear and apparently die near the end of embryonic life. Finally, populations of what appear to be peripheral sensory neurons begin to express catecholamines by around midway through embryonic life. Like several of the neurons expressing a variety of transmitters in the developing central ganglia, the catecholaminergic peripheral cells persist into postembryonic life. Transmitter phenotypes, cell shapes and locations, and neuritic morphologies all suggest that many of the neurons observed in early embryonic pond snails have recognizable homologues across the molluscs. Such observations have profoundly altered our views of neurogenesis in gastropods over the last few years. They also suggest the promise for pond snails as fruitful models for studying the roles and mechanisms for pioneering fibres, cues triggering apoptosis, and contrasting origins and mechanisms employed for generating central vs. peripheral neurons within a single organism.Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular neurobiology. Recent work has exploited both these fields of study by examining the ontogeny of the nervous system in these animals. Much of this work has focussed upon the development of specific transmitter phenotypes to provide vignettes of neuronal subpopulations that can be traced from early embryonic life through to adulthood. While such studies have generally confirmed previous explanations of gangliogenesis in gastropods, they have also indicated the presence of several neurons that appear earlier and in positions inconsistent with classical views of gastropods neurogenesis. The earliest of these cells contain FMRFamide-related peptides and have anteriorly projections that mark the future locations of ganglia and interconnecting pathways that will comprise the postembryonic central nervous system. These posterior, peptidergic cells, as well as certain, apical, monoaminergic neurons, disappear and apparently die near the end of embryonic life. Finally, populations of what appear to be peripheral sensory neurons begin to express catecholamines by around midway through embryonic life. Like several of the neurons expressing a variety of transmitters in the developing central ganglia, the catecholaminergic peripheral cells persist into postembryonic life. Transmitter phenotypes, cell shapes and locations, and neuritic morphologies all suggest that many of the neurons observed in early embryonic pond snails have recognizable homologues across the molluscs. Such observations have profoundly altered our views of neurogenesis in gastropods over the last few years. They also suggest the promise for pond snails as fruitful models for studying the roles and mechanisms for pioneering fibres, cues triggering apoptosis, and contrasting origins and mechanisms employed for generating central vs. peripheral neurons within a single organism.
Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular neurobiology. Recent work has exploited both these fields of study by examining the ontogeny of the nervous system in these animals. Much of this work has focussed upon the development of specific transmitter phenotypes to provide vignettes of neuronal subpopulations that can be traced from early embryonic life through to adulthood. While such studies have generally confirmed previous explanations of gangliogenesis in gastropods, they have also indicated the presence of several neurons that appear earlier and in positions inconsistent with classical views of gastropods neurogenesis. The earliest of these cells contain FMRFamide‐related peptides and have anteriorly projections that mark the future locations of ganglia and interconnecting pathways that will comprise the postembryonic central nervous system. These posterior, peptidergic cells, as well as certain, apical, monoaminergic neurons, disappear and apparently die near the end of embryonic life. Finally, populations of what appear to be peripheral sensory neurons begin to express catecholamines by around midway through embryonic life. Like several of the neurons expressing a variety of transmitters in the developing central ganglia, the catecholaminergic peripheral cells persist into postembryonic life. Transmitter phenotypes, cell shapes and locations, and neuritic morphologies all suggest that many of the neurons observed in early embryonic pond snails have recognizable homologues across the molluscs. Such observations have profoundly altered our views of neurogenesis in gastropods over the last few years. They also suggest the promise for pond snails as fruitful models for studying the roles and mechanisms for pioneering fibres, cues triggering apoptosis, and contrasting origins and mechanisms employed for generating central vs. peripheral neurons within a single organism. Microsc. Res. Tech. 49:570–578, 2000. © 2000 Wiley‐Liss, Inc.
Author Croll, Roger P.
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Smith SA, Nason J, Croll RP. 1998. Distribution of catecholamines in the sea scallop, Placopecten magellanicus. Can J Zool 76: 1254-1262.
Granzow B, Rowell CHF. 1981. Further observations on the serotonergic cerebral neurons of Helisoma (Mollusca, Gastropoda): The case for homology with the metacerebral giant cells. J Exp Biol 90: 283-305.
Hunter T. 1986. Spinning embryos enhance diffusion through gelatinous egg masses. J Exp Mar Biol Ecol 96: 303-308.
Kandel ER, Kriegstein A, Schacher S. 1981. Development of the central nervous system of Aplysia in terms of the differentiation of its specific identifiable cells. Neuroscience 5: 2033-2063.
Hadfield MG, Pennington JT. 1990. Nature of the metamorphic signal and its internal transduction in larvae of the nudibranch, Phestilla sibogae. Bull Mar Sci 46: 455-464.
Santama N, Wheeler CH, Skingsley DR, Yeoman MS, Bright K, Kaye I, Burke JF, Benjamin PR. 1995b. Identification, distribution and physiological activity of three novel neuropeptides of Lymnaea: EFLRIamide and pQFYRIamide encoded by the FMRFamide gene, and a related peptide. Eur J Neurosci 7: 234-246.
Purchon RD. 1977. The biology of the mollusca. Oxford: Pergamon Press.
Marois R, Carew TJ. 1997a. Fine structure of the apical ganglion and its serotonergic cells in the larva of Aplysia californica. Biol Bull 192: 388-398.
Goldberg JI, Kater SB. 1989. Expression and function of the neurotransmitter serotonin during development of the Helisoma nervous system. Dev Biol 131: 483-495.
Hadfield MG, Scheuer D. 1985. Evidence for a soluble metamorphic inducer in Phestilla sibogae: ecological, chemical, and biological data. Bull Mar Sci 37: 556-566.
Raven CP. 1966. Morphogenesis: the analysis of molluscan development. Oxford: Pergamon Press.
Pires A, Woollacott RM. 1997. Serotonin and dopamine have opposite effects on phootaxis in larvae of the bryozoan Bugula neritina. Biol Bull 192: 399-409.
Diefenbach TJ, Koehncke NK, Goldberg JI. 1991. Characterization and development of rotational behavior in Helisoma embryos: role of endogenous serotonin. J Neurobiol 22: 922-934.
Kempf SC, Page LR, 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.
Ghysen A, Dambly-Chaudiere C. 1989. Genesis of the Drosophila peripheral nervous system. Trends Genet 5: 251-255.
Lin M-F, Leise EM. 1996. Gangliogenesis in the prosobranch gastropod Ilyanassa obsoleta. J Comp Neurol 374: 180-193.
Bulloch TH, Horridge GA. 1965. Structure and function in the nervous systems of invertebrates. San Francisco: W.H. Freeman.
Voronezhskaya EE, Hiripi L, Elekes K, Croll RP. 1999. Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis I: Embryonic development of dopaminergic neurons and dopamine-dependent behaviors. J Comp Neurol 404: 297-309.
Doe CQ, Goodman CS. 1985. Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111: 193-205.
Voronezhskaya EE, Elekes K. 1993. Distribution of serotonin-like immunoreactive neurons in the embryonic nervous system of lymnaeid and planorbid snails. Neurobiology 1: 371-383.
Croll RP, Chiasson BJ. 1989. Post-embryonic development of serotonin-like immunoreactivity in the central nervous system of the snail, Lymnaea stagnalis. J Comp Neurol 280: 122-142.
Jackson AR, MacRae TW, Croll RP. 1995. Unusual
1990; 10
1981; 90
1997; 193
1983; 3
1949; 8
1992; 322
1995b; 7
1995; 76
1989; 280
1976
1997a; 192
1997; 5
1999; 404
1993; 1
1978
1993; 5
1977
1987; 38
1998; 292
1992; 92
1990; 46
1996b; 22
1990
2000
1993; 72
1997; 386
1980; 76
1987
1997; 17
2000b
2000a
1996; 374
1982
1980
1997; 192
1996; 8
1995; 281
1996; 67
1989
1989; 5
1992; 182
1986; 96
1985; 307
1978; 10
1989; 131
1981; 5
1991
1996; 16
1997b; 386
1999
1988; 126
1990; 68
1984; 4
1991; 22
1995; 46
1984; 7
1995a; 7
1965
1985; 312
1999; 196
1972; 79
1998; 76
1992; 23
1998; 34
1985; 37
1990; 7
1999; 119
1996a; 173
1985; 111
1966
Salimova (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB63) 1987; 38
Kandel (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB37) 1981; 5
Croll (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB10) 1997; 193
Gan (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB21) 1997; 17
Morse (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB52) 1980
Croll (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB7) 1989; 280
Nagy (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB53) 2000
Goldberg (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB23) 1989; 131
Marois (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB46) 1992; 322
Santama (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB65) 1995a; 7
Dyer (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB20) 1996; 67
Greenberg (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB26) 1992; 92
Jacob (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB36) 1984; 4
Hay-Schmidt (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB33) 1995; 76
Hadfield (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB30) 1984; 7
Melancon (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB47) 1997; 17
Landis (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB40) 1988; 126
Oppenheim (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB54) 1999
Page (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB55) 1992; 182
Hadfield (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB29) 1985; 37
Sakharov (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB62) 1976
Dickinson (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB15) 2000
Marois (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB45) 1997b; 386
Mescheryakov (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB48) 1990
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Croll (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB9) 1996b; 22
Voronezhskaya (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB72) 1993; 1
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Moffet (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB49) 1995; 46
Bonar (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB3) 1978; 10
Pires (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB58) 1997; 192
Smith (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB70) 1998; 76
Santama (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB67) 1996; 8
Voronezhskaya (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB75) 1999; 404
Dickinson (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB13) 2000a
Weisblat (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB76) 1985; 312
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Croll (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB6) 1987
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Serfozo (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB69) 1998; 292
Croll (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB8) 1996a; 173
Barlow (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB1) 1992; 23
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Moran (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB50) 1999; 196
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Jackson (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB35) 1995; 281
Bonar (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB4) 1990; 46
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Voronezhskaya (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB73) 1996; 16
Dickinson (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB14) 2000b
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Voronezhskaya (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB74) 1997; 5
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Marois (10.1002/1097-0029(20000615)49:6<570::AID-JEMT7>3.0.CO;2-Q-BIB42) 1989
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Snippet Pond snails have long been the subject of intense scrutiny by researchers interested in general principles of development and also cellular and molecular...
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SubjectTerms Animals
Biomphalaria
catecholamine
Catecholamines - analysis
Embryo, Nonmammalian - metabolism
FMRFamide
FMRFamide - analysis
Ganglia, Invertebrate - metabolism
gastropod
Gastropoda
Helisoma
Immunohistochemistry
Lymnaea
Lymnaea - anatomy & histology
Lymnaea - embryology
mollusc
Mollusca - anatomy & histology
Mollusca - embryology
Nervous System - anatomy & histology
Nervous System - embryology
Nervous System - metabolism
Neurons - metabolism
Neurotransmitter Agents - analysis
serotonin
Title Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails
URI https://api.istex.fr/ark:/67375/WNG-3WC70B8J-G/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2F1097-0029%2820000615%2949%3A6%3C570%3A%3AAID-JEMT7%3E3.0.CO%3B2-Q
https://www.ncbi.nlm.nih.gov/pubmed/10862113
https://www.proquest.com/docview/17668420
https://www.proquest.com/docview/71202841
Volume 49
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