Photoreceptor projections and receptive fields in the dorsal rim area and main retina of the locust eye

Abstract

In many insect species, photoreceptors of a small dorsal rim area of the eye are specialized for sensitivity to the oscillation plane of polarized skylight and, thus, serve a role in sky compass orientation. To further understand peripheral mechanisms of polarized-light processing in the optic lobe, we have studied the projections of photoreceptors and their receptive fields in the main eye and dorsal rim area of the desert locust, a model system for polarization vision analysis. In both eye regions, one photoreceptor per ommatidium, R7, has a long visual fiber projecting through the lamina to the medulla. Axonal fibers from R7 receptors of the dorsal rim area have short side branches throughout the depth of the dorsal lamina and maintain retinotopic projections to the dorsal medulla following the first optic chiasma. Receptive fields of dorsal rim photoreceptors are considerably larger (average acceptance angle 33°) than those of the main eye (average acceptance angle 2.04°) and, taken together, cover almost the entire sky. The data challenge previous reports of two long visual fibers per ommatidium in the main eye of the locust and provide data for future analysis of peripheral networks underlying polarization opponency in the locust brain.

The evolutionary diversity of insect retinal mosaics: common design principles and emerging molecular logic

“…The exclusive expression of the Blue Rhodopsin in the locust DRA was surprising, given that UV receptors of low polarization sensitivity had previously been described in the locust DRA [59], where DRA ommatidia form a fan-shaped array of detectors [60,61] (Figure 3I). Interestingly, in the main part of the locust retina, seven Svf PRs express a long-wavelength (green) Rhodopsin, five of which also co-express the Blue Rhodopsin, leaving two proximal PRs (R1 and R4) which are exclusively Green-sensitive [50,62]). The remaining single Lvf cell (R7) expresses either a UV (Type I) or a Blue (Type II) Rhodopsin, thus defining two subtypes of ommatidia that are distributed randomly with a ratio that is virtually identical to the one reported in Drosophila (Type I: 65%, Type II: 35%) (Figure 3J).…”

“…The remaining single Lvf cell (R7) expresses either a UV (Type I) or a Blue (Type II) Rhodopsin, thus defining two subtypes of ommatidia that are distributed randomly with a ratio that is virtually identical to the one reported in Drosophila (Type I: 65%, Type II: 35%) (Figure 3J). Despite these important similarities, it must be pointed out that the recent demonstration of only one Lvf cell per ommatidium in locusts was quite different from flies, honeybees, and butterflies [23,62,63]. The functional implications of one versus two Lvf cells per ommatidium are not clear, yet the advantage of comparing a delayed signal propagating through a multi-synaptic Svf→Lamina pathway versus a faster Lvf channel into the medulla has been proposed for the Locust DRA [62].…”

“…Despite these important similarities, it must be pointed out that the recent demonstration of only one Lvf cell per ommatidium in locusts was quite different from flies, honeybees, and butterflies [23,62,63]. The functional implications of one versus two Lvf cells per ommatidium are not clear, yet the advantage of comparing a delayed signal propagating through a multi-synaptic Svf→Lamina pathway versus a faster Lvf channel into the medulla has been proposed for the Locust DRA [62]. Taken together, the extreme molecular specialization of the DRA in both crickets and locusts is reminiscent of the Monarch DRA, while non-DRA ommatidia form potentially homogeneous territories in crickets, or two stochastically distributed subtypes in locusts.…”

Ultrastructure of GABA- and Tachykinin-Immunoreactive Neurons in the Lower Division of the Central Body of the Desert Locust

“…Photoreceptors in a specialized dorsal rim area of the compound eye are sensitive to the oscillation plane of celestial polarized light (Labhart and Meyer, 1999; Schmeling et al, 2014, 2015). Signals are transferred via a specific pathway to the CBL (Homberg et al, 2003; Pfeiffer and Kinoshita, 2012; Held et al, 2016; Schmitt et al, 2016).…”

Can invertebrates see the e-vector of polarization as a separate modality of light?

“…Because of both a restriction of the DRA to the dorsal-most eye part and strongly enlarged visual fields of the ommatidia, this condition is indeed met in some insects, such as crickets, locusts and cockchafers (Fig. 5B) (Blum and Labhart, 2000; Labhart et al, 1992; Schmeling et al, 2015). By comparing the output signals of the differently tuned polop neurons, such DRAs could, in principle, determine e-vector orientation within their common visual field.…”