Neurite morphogenesis of identified visual interneurons and its relationship to photoreceptor synaptogenesis in the flies, Musca domestica and Drosophila melanogaster.
The first neuropile, or lamina, of the fly's optic lobe comprises a model set of identified neurons that are arrayed in cylindrical modules, called cartridges. The cartridge acquires adult form only in the second half of the fly's pupal life. All cells are by then correctly located within each of the lamina's cartridges (Drosophila, Musca), becoming invested by glial cells after 75% of pupal development (P + 75%). In adult cartridges, two lamina cells, L1 and L2, receive input from photoreceptor terminals R1-R6, at so-called tetrad synapses that form in the pupa when these cells' dendrites contact R1-R6. Single-section electron microscopy (EM, Drosophila) and serial-EM reconstructions of L1 and L2 (Musca) reveal relationships between the morphogenesis of L1/L2 dendrites and the formation of tetrads. Neurite outgrowth is initially (P + 55%) random and neurites are unbranched; many neurites invaginate surrounding terminals of R1-R6 but, later, embrace the outer surfaces of these. The maximum profusion of neurites at P + 74% coincides with peak numbers of nascent tetrads; neurites then branch vertically, in the lamina's depth. Later, neurites failing to reach R1-R6's outer surfaces regress. Down the length of their axons, L1 and L2's neurites initially form a random sequence, L1 partnering L1 as often as L2, etc., but beginning at P + 74%, L1 partners L2, and L2 partners L1, with progressive strictness. L1 has more neurites overall than L2. These observations are consistent with the following hypotheses: a neurite only survives if it contacts a presynaptic site; a synapse only survives if it progressively acquires the appropriate number and combination of postsynaptic neurites, culminating in a tetrad; an interaction exists between the neurites of L1 and L2, so that the growth of one respects the pattern of growth of the other.
Meinertzhagen
I A
IA
Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada. iam@is.dal.ca
Piper
S T
ST
Sun
X J
XJ
Fröhlich
A
A
D000818:Animals; D048429:Cell Size / Q000502:physiology; D003712:Dendrites / Q000502:physiology / Q000648:ultrastructure; D004331:Drosophila melanogaster; D020439:Growth Cones / Q000502:physiology / Q000648:ultrastructure; D006793:Houseflies; D007091:Image Processing, Computer-Assisted; D007395:Interneurons / Q000502:physiology / Q000648:ultrastructure*; D008854:Microscopy, Electron; D016501:Neurites / Q000502:physiology / Q000648:ultrastructure*; D019581:Neuropil / Q000648:ultrastructure; D009899:Optic Lobe, Nonmammalian / Q000166:cytology; D017956:Photoreceptor Cells, Invertebrate / Q000502:physiology / Q000648:ultrastructure*; D011679:Pupa / Q000166:cytology; D013569:Synapses / Q000502:physiology / Q000648:ultrastructure*; D014795:Visual Pathways / Q000166:cytology / Q000254:growth & development