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The development of a long, coiled, optic nerve in the stalk-eyed fly Cyrtodiopsis whitei

Abstract

In the stalk-eyed fly Cyrtodiopsis whitei (Diopsidae; Diptera), the relatively long optic nerve develops within the tight lumen of a very short eyestalk. Axonal growth is generally considered in terms of path finding, selective fasciculation, and towing. Physical forces that are necessary for axon lengthening are generated either by the growth cone or by the growth of surrounding tissues. Therefore, it is surprising to encounter a loosely coiled nerve apparently lacking any attachments that could allow for pull, or towing, of the nerve. In this study, we used histological sections and whole-mount preparations to confirm that the optic nerve of the stalk-eyed fly indeed elongates without the external application of tension to the nerve. Secondly, we examined the distribution of cytoskeletal elements and selected proteins that may be involved in axon extension. Staining against the vesicle fusion proteins SNAP-24 and SNAP-25 consistently results in stronger staining in the rapidly extending optic nerve than in a control nerve, suggesting a possible role of these proteins in the extension process. On a gross morphological level, SNAP-24/25 as well as the cytoskeletal elements actin and tubulin are uniformly distributed throughout the lengths of the growing nerve, suggesting that nerve elongation is distributed rather than localized. Finally, we identified glia as a possible source for tension within the nerve bundle. Glia proliferate rapidly in the optic nerve but not in the control nerve. Much work continues to focus on the growth of axons in culture, but this study is one of the few that considers the dynamics of nerve bundle extension as a whole.

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Acknowledgements

We would like to thank Dr. Gerald S. Wilkinson for generously providing flies and much help on rearing them. Drs. Hugo Bellen and David Deitcher kindly provided us with antibodies. Dr. David Deitcher provided much help with the Western blot. We thank Drs. Pat Rivlin, Ilya Vilinsky, and Heather Hoy for comments on the manuscript and Brandon Loveall for technical assistance.

Author information

Correspondence to Elke K. Buschbeck.

Additional information

This research is supported by the National Science Foundation (IBN-9974512 and IBN-211770).

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Buschbeck, E.K., Hoy, R.R. The development of a long, coiled, optic nerve in the stalk-eyed fly Cyrtodiopsis whitei. Cell Tissue Res 321, 491–504 (2005). https://doi.org/10.1007/s00441-005-1142-4

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Keywords

  • Nerve growth
  • Axon elongation
  • Eyestalk
  • Glia
  • Cyrtodiopsis whitei (Insecta)