Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster

Many invertebrates have supplementary extraocular photoreceptors that often are implicated in circadian rhythms. An extraretinal group of candidate ph otoreceptors in the fruit fly, Drosophila melanogaster, has been revealed p reviously at the posterior margin of the compound eye by using a photorecep tor-specific monoclonal antibody (Hofbauer and Buchner [1989] Naturwissen 7 6:335-336), but it never has been characterized. Here, we report the fine s tructure of this cell cluster reported by Hofbauer and Buchner, which is ca lled "eyelet," as well as the further candidacy of their visual pigment and neurotransmitter. Eyelet forms a specialized, pigmented organ with cells t hat have numerous microvilli arranged into coherent rhabdomeres. The presen ce of rhabdomeric microvilli is a defining feature of a photoreceptor, repo rted here for the first time in eyelet. The rhabdomeres exhibit Rh6 opsin-l ike immunoreactivity, which provides evidence that the photoreceptors are f unctional: they fail to immunostain with antibodies against NINAE (Rh1), Rh 4, or Rh5. The photoreceptors have been shown previously to exhibit histami ne-like immunoreactivity, but they also stain with a monoclonal antiserum r aised against Drosophila choline acetyltransferase (ChAT), suggesting that the photoreceptors not only may contain histamine but also can synthesize a cetylcholine. A ChAT-immunoreactive axon bundle originating from eyelet ter minates in the cortex of the anterior medulla. This bundle also is seen wit h reduced silver stains. Electron microscopic examination revealed four axo n profiles of similar size in this bundle, indicating that eyelet contains at least four photoreceptors. The pathway of eyelet's axon bundle coincides with the precocious pathway of Bolwig's nerve that arises from the larval organ of sight. The origin and possible function of eyelet are discussed. J . Comp. Neurol. 412:193-202, 1999. (C) 1999 Wiley-Liss, Inc.