Chromatic information processing in the first optic ganglion of the butterfly Papilio xuthus

Abstract

The butterfly Papilio xuthus has acute tetrachromatic color vision. Its eyes are furnished with eight spectral classes of photoreceptors, situated in three types of ommatidia, randomly distributed in the retinal mosaic. Here, we investigated early chromatic information processing by recording spectral, angular, and polarization sensitivities of photoreceptors and lamina monopolar cells (LMCs). We identified three spectral classes of LMCs whose spectral sensitivities corresponded to weighted linear sums of the spectral sensitivities of the photoreceptors present in the three ommatidial types. In ~ 25% of the photoreceptor axons, the spectral sensitivities differed from those recorded at the photoreceptor cell bodies. These axons showed spectral opponency, most likely mediated by chloride ion currents through histaminergic interphotoreceptor synapses. The opponency was most prominent in the processes of the long visual fibers in the medulla. We recalculated the wavelength discrimination function using the noise-limited opponency model to reflect the new spectral sensitivity data and found that it matched well with the behaviorally determined function. Our results reveal opponency at the first stage of Papilio's visual system, indicating that spectral information is preprocessed with signals from photoreceptors within each ommatidium in the lamina, before being conveyed downstream by the long visual fibers and the LMCs.

Polarized light sensitivity in Pieris rapae is dependent on both color and intensity

“…S2), albeit with smaller separations among low and high DoLP stimuli owing to lower PS of the photoreceptors. It is unlikely that this inconsistency could be resolved even if downstream opponent processing was considered (Chen et al, 2019) or if photoreceptors were to be compared among different ommatidial types (Takemura and Arikawa, 2005).…”

Evolution of Insect Color Vision: From Spectral Sensitivity to Visual Ecology

“…Chromatic opponency occurs beginning at the stage of photoreceptors. The chromatically opponent responses recorded from photoreceptors in butterflies (20), flies (51), locusts (113), and bees (90) most likely result from histaminergic inhibitory synapses between photoreceptor terminals within and across the lamina and medulla cartridges. Such synapses have been described in flies (50) and butterflies (2,21).…”

Neural mechanism of spatio-chromatic opponency in the Drosophila amacrine neurons

“…15 Because of their sensitivity to spectral and/or spatial contrast, opponent cells have profound implications in spectral information processing and have been intensively studied in vertebrates 16,17 and to a lesser extent in bees, butterflies, and flies. [18][19][20][21][22][23] However, the neural circuit mechanisms generating spatio-chromatic opponency are not known, either in insects or vertebrates. To study the neural mechanism of spatio-chromatic opponency, we used the fruit fly, Drosophila melanogaster, a genetically tractable model organism that has been reported to show color-dependent behavior.…”