Abstract
Inside compound eyes, photoreceptors contract to light changes, sharpening retinal images of the moving world in time. Current methods to measure these so-called photoreceptor microsaccades in living insects are spatially limited and technically challenging. Here, we present goniometric high-speed deep pseudopupil (GHS-DPP) microscopy to assess how the rhabdomeric insect photoreceptors and their microsaccades are organised across the compound eyes. This method enables non-invasive rhabdomere orientation mapping, whilst their microsaccades can be locally light-activated, revealing the eyes’ underlying active sampling motifs. By comparing the microsaccades in wild-type Drosophila’s open rhabdom eyes to spam-mutant eyes, reverted to an ancestral fused rhabdom state, and honeybee’s fused rhabdom eyes, we show how different eye types sample light information. These results show different ways compound eyes initiate the conversion of spatial light patterns in the environment into temporal neural signals and highlight how this active sampling can evolve with insects’ visual needs.
Highlights
Inside compound eyes, photoreceptors contract to light changes, sharpening retinal images of the moving world in time
With similar microsaccades occurring in synaptically decoupled photoreceptors[4], the results demonstrated active sampling inside an ommatidium for the first time[4]
Because Drosophila has a small head and fairly transparent cuticle, the infrared goniometric high-speed deep pseudopupil (GHS-deep pseudopupil (DPP)) microscopy makes it straightforward to record, measure and map the DPP pattern changes across the eyes
Summary
Left and right eye DPP patterning rotate systematically and mirror-symmetrically. We first inspected the wild-type and spam flies’ DPP patterns in still images taken under antidromic infrared illumination in perceptual darkness (Fig. 4). The fast axial DPP brightness changes systematically time-locked with the corresponding lateral DPP movements (Fig. 5d–f), consistent with both phenotypes having the same photomechanical phototransduction origin Both the wild-type and spam had similar looking microsaccade kinematics and probabilities (Fig. 5d–f), but the overall displacement amplitudes appeared much smaller in spam (Fig. 5d). The recordings showed slow wave-like lateral retina movements, occurring about 2–3 times in a minute, and gradual axial creep, almost certainly[5] pulling the observed rhabdoms inwards (DPP darkening) These spontaneous, presumably muscle-activity-induced, components (Fig. 7d) differed clearly from the ultrafast photomechanical photoreceptor microsaccades (Fig. 7c). They were largely unsynchronised in time, and most crucially, showed 10–100 times slower dynamics, broadly comparable to our earlier findings of intraocular muscle activity in Drosophila[4,5]
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