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Neurogenesis of cephalic sensory organs of Aplysia californica

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Abstract

The opisthobranch gastropod Aplysia californica serves as a model organism in experimental neurobiology because of its simple and well-known nervous system. However, its nervous periphery has been less intensely studied. We have reconstructed the ontogeny of the cephalic sensory organs (labial tentacles, rhinophores, and lip) of planktonic, metamorphic, and juvenile developmental stages. FMRFamide and serotonergic expression patterns have been examined by immunocytochemistry in conjunction with epifluorescence and confocal laser scanning microscopy. We have also applied scanning electron microscopy to analyze the ciliary distribution of these sensory epithelia. Labial tentacles and the lip develop during metamorphosis, whereas rhinophores appear significantly later, in stage 10 juveniles. Our study has revealed immunoreactivity against FMRFamides and serotonin in all major nerves. The common labial nerve develops first, followed by the labial tentacle base nerve, oral nerve, and rhinophoral nerve. We have also identified previously undescribed neuronal pathways and other FMRFamide-like-immunoreactive neuronal elements, such as peripheral ganglia and glomerulus-like structures, and two groups of conspicuous transient FMRFamide-like cell somata. We have further found two distinct populations of FMRFamide-positive cell somata located both subepidermally and in the inner regions of the cephalic sensory organs in juveniles. The latter population partly consists of sensory cells, suggesting an involvement of FMRFamide-like peptides in the modulation of peripheral sensory processes. This study is the first concerning the neurogenesis of cephalic sensory organs in A. californica and may serve as a basis for future studies of neuronal elements in gastropod molluscs.

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Acknowledgements

The authors are grateful to Marion Stöhr and Manfred Ruppel (Frankfurt) and to Bjarne Bisballe, Henrike Semmler, and Judith Fuchs (Copenhagen) for technical assistance. They also thank Sid Staubach (Frankfurt) and Roger Croll (Halifax) for valuable comments, and Adrienne Jochum (Frankfurt) for proof reading. T.W. is grateful to Patrick J. Walsh, Lynne A. Fieber and Tom R. Capo for the use of their lab facilities. Finally, the authors thank Volker Hartenstein and three anonymous reviewers, whose valuable comments improved an earlier version of this paper.

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  1. Tim Wollesen

    Present address: Department of Cell Biology and Comparative Zoology, Institute of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark

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  1. Institute of Ecology, Evolution and Diversity, J. W. Goethe University, Siesmayerstrasse 70, 60323, Frankfurt am Main, Germany

    Tim Wollesen & Annette Klussmann-Kolb

  2. Department of Cell Biology and Comparative Zoology, Institute of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark

    Andreas Wanninger

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  1. Tim Wollesen
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Correspondence to Tim Wollesen.

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This work was supported by the German Science Foundation (DFG; Kl 1303/3-1 to A.K.K.), SYNTHESYS (DK-TAF-202 to T.W.), the German Academic Exchange Service (DAAD to T.W.), the Danish Natural Science Research Council (FNU; grants 21-04-0356 and 272-05-0174 to A.W.), and the Carlsberg Foundation (grant 2005-1-249 to A.W.).

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Wollesen, T., Wanninger, A. & Klussmann-Kolb, A. Neurogenesis of cephalic sensory organs of Aplysia californica . Cell Tissue Res 330, 361–379 (2007). https://doi.org/10.1007/s00441-007-0460-0

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