Immunolocalization suggests a role of the histamine‐gated chloride channel PxHCLB in spectral opponent processing in butterfly photoreceptors

Abstract

Spectrally opponent responses, that is, wavelength‐dependent inversions of response polarity, have been observed at the level of photoreceptors in butterflies. As inter‐photoreceptor connections have been found in the butterfly Papilio xuthus, and histamine is the only neurotransmitter so far identified in insect photoreceptors, we hypothesize that histaminergic sign‐inverting synapses exist in the lamina between different spectral receptors as a mechanism for spectral opponency as in the medulla of Drosophila. Here, we localized two histamine‐gated chloride channels, PxHCLA (Drosophila Ort homolog) and PxHCLB (Drosophila HisCl1 homolog), in the visual system of Papilio xuthus by using specific antisera. The antiPxHCLA labeling was associated with the membrane of nonphotoreceptor cells that are postsynaptic to photoreceptors, while the antiPxHCLB labeling overlapped with photoreceptor axons, indicating that PxHCLB is expressed at inter‐photoreceptor synapses: PxHCLB is likely involved in producing spectral opponency at the first visual synapses. Color processing in Papilio may appear earlier than previously hypothesized in insect visual systems.

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

“…Photoreceptors are interconnected in the lamina cartridges in an ommatidial type-specific manner in Papilio (Takemura and Arikawa 2006). We have previously hypothesized that a histamine-gated chloride channel, PxHCLB, is involved in these connections (Akashi et al 2018;Chen et al 2019). The present results clearly indicate that the interphotoreceptor connections are indeed inhibitory synapses that utilize chloride currents, providing further support for this account.…”

“…The LMCs are postsynaptic to the photoreceptors in the cartridge with various spectral sensitivities (Takemura and . Interestingly, the photoreceptors are also postsynaptic to other photoreceptors: They are mutually connected via histamine-gated chloride channels in a configuration that depends on the ommatidial type (Takemura and Arikawa 2006;Akashi et al 2018;Chen et al 2019).…”

Color vision in insects: insights from Drosophila

“…In contrast, bee and butterfly ommatidia have a so-called fused rhabdom, where the light-sensitive structures of the individual photoreceptors are grouped closely together and acts as a light guide 1 3 in butterflies and bees, where synaptic interactions in the lamina are likely involved in color opponent processing or in increasing wavelength specificity (Takemura et al 2005;Chen et al 2013), lvfs in Drosophila pass the lamina without making synapses (Fig. 4, Chen et al 2019;Meinertzhagen and O'Neil 1991;Menzel and Backhaus 1991;Menzel and Blakers 1976;Ribi 1981;Takemura and Arikawa 2006). The terminals of R7 and R8 in Drosophila are often described to 'precisely' terminate in medulla layer m6 and m3, respectively ( Fig.…”

“…These two mechanisms are of different importance in R7 and R8: in R7, either of the mechanisms is sufficient for color opponent processing, whereas in R8 both mechanisms are required and must act together for detectable color opponency (Schnaitmann et al 2018). Inhibitory photoreceptor responses, synaptic contacts between photoreceptors, and expression of PxHCLB, the homolog of Drosophila HisCl1in Papilio xuthus suggest that related neuronal mechanisms underlie early color opponent processing in butterflies and flies (Takemura and Arikawa 2006;Takemura et al 2013;Schnaitmann et al 2018;Chen et al 2019). Differences between Drosophila and butterflies exist in the precise site where interactions take place.…”

“…In Papilio xuthus, the major site of PxHCLB expression is the lamina with additional neuronal expression in the medulla. Furthermore, vfs as well as svfs express the histamine receptor PxHCLB and interphotoreceptor connectivity is more complex than in Drosophila (Chen et al 2019).…”