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Evolutionary remodeling in a visual system through extensive changes in the synaptic connectivity of homologous neurons

Published online by Cambridge University Press:  02 June 2009

S. R. Shaw  and
D. Moore
S. R. Shaw
Affiliation:
Department of Psychology, Dalhousie University, Life Sciences Center, Halifax, Nova Scotia, Canada
D. Moore*
Affiliation:
Department of Psychology, Dalhousie University, Life Sciences Center, Halifax, Nova Scotia, Canada
*
D. Moore&s current address is Department of Biological Sciences, East Tennessee State University, Johnson City, TN.
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Abstract

The cellular mechanisms by which nervous systems evolve to match evolutionary changes occurring in the rest of the body remain largely unexplored. In a distal visual neuropil of a previously unexamined ancient dipteran family, Stratiomyidae, homologues of all of the periodic neurons known already from more recent Diptera can be recognized, occupying the same locations within the unit structure. This points to extreme developmental stasis for more than 200 million years, conserving both cell identity and position. The arborizations that some neurons make also have remained conservative, but others show marked differences between families in both size and branching patterns. At the electron-microscopical level, extensive differences in synaptic connectivity are found, some sufficient to radically redefine the systems roles of particular neurons. The findings bear out an earlier prediction that changes in the connectivity matrix linking conserved neurons may have been a major factor in implementing evolutionary change in the nervous system.

Keywords

Synaptic evolutionNeural remodelingInsect visionGolgi electron microscopyDipteran synapses
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 5 , November 1989 , pp. 405 - 410
Copyright
Copyright © Cambridge University Press 1989

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References

Boschek, C.B. (1971). On the fine structure of the peripheral retina and lamina ganglionaris of the fly (Musca domestica). Zeitschrift für Zellforschung 118, 369–409.CrossRefGoogle ScholarPubMed
Bullock, T.H. (1980). Reassessment of neural connectivity and its specification. In Information Processing in the Nervous System, ed. Pinsker, H.M. & Willis, W.D., pp. 199–220. New York: Raven Press.Google Scholar
Cajal, S.R. & Sánchez, D. (1915). Contribución al conocimiento de los centros nerviosos de los insectos. Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid, 13, 1–167.Google Scholar
Campos-Ortega, J.A. & Strausfeld, N.J. (1973). Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly&s eye. Brain Research 59, 119–136.CrossRefGoogle ScholarPubMed
Dumont, J.P.C. & Robertson, R.M. (1986). Neuronal circuits: an evolutionary perspective. Science 233, 849–853.CrossRefGoogle ScholarPubMed
Fischbach, K.-F. & Dittrich, A.P.M. (1989). The optic lobe of Drosophila melanogaster, I: A Golgi analysis of wild-type structure. Cell and Tissue Research (in press).CrossRefGoogle Scholar
Hardie, R.C. (1983). Projection and connectivity of sex-specific photoreceptors in the compound eye of the male housefly (Musca domestica). Cell and Tissue Research 233, 1–21.CrossRefGoogle ScholarPubMed
Hardie, R.C. (1985). Functional organization of the fly retina. In progress in Sensory Physiology, Vol. 5, ed. Ottoson, D., pp. 1–79. Heidelberg: Springer Verlag.Google Scholar
Meinertzhagen, I.A. & O&Neil, S.D. (1988). The lamina cartridge in the optic lobe of Drosophila. Society for Neuroscience Abstracts 14, 376.Google Scholar
Ribi, W.A. (1978). Gap junctions coupling photoreceptor axons in the first optic ganglion of the fly. Cell and Tissue Research 195, 299–308.CrossRefGoogle ScholarPubMed
Ribi, W.A. (1983). Electron microscopy of Golgi-impregnated neurons. In Functional Neuroanatomy, ed. Strausfeld, N.J., pp. 1–18. Berlin: Springer-Verlag.Google Scholar
Shaw, S.R. (1981). Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially Diptera. In Neurones without Impulses, ed. Roberts, A. & Bush, B.M.H., pp. 61–116. Cambridge, England: Cambridge University Press.Google Scholar
Shaw, S.R. (1984). Early visual processing in insects. Journal of Experimental Biology 112, 225–251.Google Scholar
Shaw, S.R. (1989). The retina-lamina pathway in insects, particularly Diptera, viewed from an evolutionary perspective. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 186–212. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Shaw, S.R., Fröhlich, A. & Meinertzhagen, I.A. (1989). Direct connections between the R7ì8 and Rl-6 photoreceptor subsystems in the dipteran visual system. Cell and Tissue Research 257, 295–302.CrossRefGoogle Scholar
Shaw, S.R. & Meinertzhagen, I.A. (1986). Evolutionary progression at synaptic connections made by identified homologous neurones. Proceedings of the National Academy of Sciences of the U.S.A. 83, 7961–7965.Google Scholar
Shaw, S.R. & Stowe, S. (1982). Freeze-fracture evidence for gap junctions connecting the axon terminals of dipteran photoreceptors. Journal of Cell Science 53, 115–141.Google Scholar
Srinivasan, M.V., Laughlin, S.B. & Dubs, A. (1982). Predictive coding: a fresh view of inhibition in the retina. Proceedings of the Royal Society B (London) 216, 427–459.Google ScholarPubMed
Strausfeld, N.J. & Campos-Ortega, J.A. (1972). Some interrelationships between the first and second synaptic regions of the fly&s (Musca domestica L.) visual system. In Information Processing in the Visual System of Arthropods, ed. Wehner, R., pp. 23–30. Berlin: Springer-Verlag.Google Scholar
Strausfeld, N.J. & Campos-Ortega, J.A. (1973 a). L3, the 3rd second-order neuron of the first visual ganglion in the “neural superposition” eye of Musca domestica. Zeitschrift für Zellforschung 139, 397–403.Google Scholar
Strausfeld, N.J. & Campos-Ortega, J.A. (1973 b). The L4 monopolar neurone: a substrate for lateral interaction in the visual system of the fly (Musca domestica L.). Brain Research 59, 97–117.Google Scholar
Strausfeld, N.J. & Campos-Ortega, J.A. (1977). Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195, 894–897.CrossRefGoogle ScholarPubMed
Strausfeld, N.J. & Nässel, D.R. (1981). Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and Insects. In Handbook of Sensory Physiology, Vol. VIIì6B, ed. Autrum, H., pp. 1–134. Heidelberg: Springer-Verlag.Google Scholar
Woodley, N.E. (1989). Phylogeny and classification of the “orthorrhaphous” Brachycera. In Manual of Nearctic Diptera, Vol. 3, ed. McAlpine, J.F., Ottawa: Agriculture Canada-, pp. 1371–1395.Google Scholar