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The Journal of Neuroscience, January 21, 2009, 29(3):828-841; doi:10.1523/JNEUROSCI.1022-08.2009

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Development/Plasticity/Repair
Photoreceptor Neurons Find New Synaptic Targets When Misdirected by Overexpressing runt in Drosophila

Tara N. Edwards¹ and Ian A. Meinertzhagen^1,2

Departments of ¹Biology and ²Psychology, Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1

Correspondence should be addressed to Ian A. Meinertzhagen, Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1. Email: iam{at}dal.ca

As a neuron differentiates, it adopts a suite of features specific to its particular type. Fly photoreceptors are of two types: R1–R6, which innervate the first optic neuropile, the lamina; and R7–R8, which innervate the second, the medulla. Photoreceptors R1–R6 normally have large light-absorbing rhabdomeres, express Rhodopsin1, and have synaptic terminals that innervate the lamina. In Drosophila melanogaster, we used the yeast GAL4/UAS system to drive exogenous expression of the transcription factor Runt in subsets of photoreceptors, resulting in aberrant axonal pathfinding and, ultimately, incorrect targeting of R1–R6 synaptic terminals to the medulla, normally occupied by terminals from R7 and R8. Even when subsets of their normal R1–R6 photoreceptor inputs penetrate the lamina, to terminate in the medulla, normal target cells within the lamina persist and maintain expression of cell-specific markers. Some R1–R6 photoreceptors form reciprocal synaptic inputs with their normal lamina targets, whereas supernumerary terminals targeted to the medulla also form synapses. At both sites, tetrad synapses form, with four postsynaptic elements at each release site, the usual number in the lamina. In addition, the terminals at both sites are invaginated by profiles of glia, at organelles called capitate projections, which in the lamina are photoreceptor sites of vesicle endocytosis. The size and shape of the capitate projection heads are identical at both lamina and medulla sites, although those in the medulla are ectopic and receive invaginations from foreign glia. This uniformity indicates the cell-autonomous determination of the architecture of its synaptic organelles by the presynaptic photoreceptor terminal.

Key words: Drosophila melanogaster; medulla; synaptogenesis; axonal targeting; capitate projection; photoreceptor

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Received March 7, 2008; revised Nov. 28, 2008; accepted Dec. 6, 2008.

Correspondence should be addressed to Ian A. Meinertzhagen, Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1. Email: iam{at}dal.ca

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