Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly,Papilio xuthus

Abstract

The compound eye of the butterfly Papilio xuthus is composed of three types of spectrally heterogeneous ommatidia. The ommatidia, which contain nine photoreceptor cells, R1-9, bear four (type I), three (type II), or two (type III) classes of spectral receptors in fixed combinations. The photoreceptors send their axons to the lamina, the first optic ganglion, where the R1-9 axons originating from a single ommatidium, together with some second-order neurons, form a neuronal bundle, called a lamina cartridge. We investigated the axonal structure of photoreceptors in the lamina to determine whether the cartridge structure is different between the three ommatidial types. We first characterized a photoreceptor by measuring its spectral sensitivity and then injected Lucifer Yellow. We subsequently identified the type of ommatidium of the injected photoreceptor via histological sections. We further observed the axonal structure of the photoreceptor in the lamina by laser confocal microscopy. We found that the number and length of axon collaterals markedly differ between the spectral receptors. Those having the most extensive axon collaterals, which extend into six or more surrounding cartridges, are violet receptors (R1 and R2 of type II ommatidia). UV receptors (R1 or R2 of type I ommatidia) also send collaterals into two to four neighboring cartridges. Blue receptors (R1 or R2 of type I ommatidia, R1 and R2 of type III ommatidia) have short collaterals restricted to their own cartridges. We thus conclude that the neuronal circuit of the lamina cartridge differs between the three types of ommatidia.