An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly

The photoreceptor terminals of newly eclosed female flies, Musca domestica, have been sampled in the first optic neuropile (or lamina) in one of two ways: first, in large number (n = 760) from single sections and second, from serial electron micrographs of the six terminals within each of three cartridges. Both sampling methods concur in assessing the number of synapses established with the two principal monopolar relay interneurons, L1 and L2, within each cartridge. Each receptor is calculated to be presynaptic at about 200 ± 40 (2 SE) synapses. This value considerably exceeds previous estimates, primarily because we took careful account of the appearance of synapses in different section planes. The number of these synapses correlates highly with the area of receptor terminal presynaptic membrane, so that each synapse is allotted, on average, about 1.6 μm2. The synapses are evenly graded in their distribution with an unexplained 23% decrease in both membrane perimeter and synapse number halfway along their receptor terminal's length. The numbers of synapses per receptor did not vary systematically within two horizontal (3 × 20 cartridge) strips of frontal, equatorial lamina sampled. Individual synapses are elongate tetrads (Burkhardt and Braitenberg, ′76) with two pairs of postsynaptic elements. The first pair is invariably contributed by the interneurons L1 and L2 (one each). The second pair comes either from the α processes of an amacrine cell or from a glial cell. In the distal lamina, however, L3 contributes one of the two postsynaptic processes, the second being αor glial. The overall ratio of postsynaptic involvement at distal synapses (α:glial:L3) is 55%, 20%, and 12% respectively, the remainder being unidentified.

[1]  C. Levinthal,et al.  Structure and development of neuronal connections in isogenic organisms: variations and similarities in the optic system of Daphnia magna. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Boschek Cb On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. , 1971 .

[3]  I A Meinertzhagen,et al.  The accuracy of the patterns of connexions of the first- and second-order neurons of the visual system of Calliphora , 1970, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  E. Macagno Number and distribution of neurons in leech segmental ganglia , 1980, The Journal of comparative neurology.

[5]  S. Laughlin Neural integration in the first optic neuropile of dragonflies , 1973 .

[6]  E. Reynolds THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[7]  N. Strausfeld,et al.  Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. , 1977, Science.

[8]  I. Meinertzhagen,et al.  Regulation in the number of fly photoreceptor synapses: The effects of alterations in the number of presynaptic cells , 1982, The Journal of comparative neurology.

[9]  D. Purves,et al.  Elimination of synapses in the developing nervous system. , 1980, Science.

[10]  Erroneous projection of retinula axons beneath a dislocation in the retinal equator of Calliphora. , 1972, Brain research.

[11]  J. Dowling,et al.  Cellular and synaptic organization in the lamina of the dragon-fly Sympetrum rubicundulum , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[12]  R. W. West Superficial warming of epoxy blocks for cutting of 25-150 m sections to be resectioned in the 40-90 nm range. , 1972, Stain technology.

[13]  M. Oberdorfer The neural organization of the first optic ganglion of the principal eyes of jumping spiders (Salticidae) , 1977, The Journal of comparative neurology.

[14]  T. Waterman,et al.  Golgi EM evidence for visual information channelling in the crayfish lamina ganglionaris , 1977, Brain Research.

[15]  I. Meinertzhagen,et al.  Synaptogenesis in the first optic neuropile of the fly's visual system , 1982, Journal of neurocytology.

[16]  M. Springer A simple holder for efficient mass staining of thin sections for electron microscopy. , 1974, Stain technology.

[17]  N. Strausfeld,et al.  Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly's eye. , 1973, Brain research.

[18]  O. Trujillo-Cenóz Some aspects of the structural organization of the intermediate retina of dipterans. , 1965, Journal of ultrastructure research.

[19]  O. Trujillo-Cenóz,et al.  Compound eye of dipterans: anatomical basis for integration--an electron microscope study. , 1966, Journal of ultrastructure research.

[20]  S. Benzer,et al.  Development of the Drosophila retina, a neurocrystalline lattice. , 1976, Developmental biology.

[21]  M. Abercrombie Estimation of nuclear population from microtome sections , 1946, The Anatomical record.

[22]  S. Easter,et al.  Retinal synaptic arrays: Continuing development in the adult goldfish , 1979, The Journal of comparative neurology.

[23]  G. Hafner The ultrastructure of retinula cell endings in the compound eye of the crayfish , 1974, Journal of neurocytology.

[24]  C. Govind,et al.  Correlation between presynaptic dense bodies and tranmitter output at lobster neuromuscular terminals by serial section electron microscopy , 1979, Brain Research.

[25]  P M Field,et al.  A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei. , 1973, Brain research.