Significance To move efficiently, animals must continuously work out their x,y,z positions with respect to real-world objects, and many animals have a pair of eyes to achieve this. How photoreceptors actively sample the eyes’ optical image disparity is not understood because this fundamental information-limiting step has not been investigated in vivo over the eyes’ whole sampling matrix. This integrative multiscale study will advance our current understanding of stereopsis from static image disparity comparison to a morphodynamic active sampling theory. It shows how photomechanical photoreceptor microsaccades enable Drosophila superresolution three-dimensional vision and proposes neural computations for accurately predicting these flies’ depth-perception dynamics, limits, and visual behaviors.

Plasticity is a crucial aspect of neuronal physiology essential for proper development and continuous functional optimization of neurons and neural circuits. Despite extensive studies of different visual systems, little is known about plasticity in mature microvillar photoreceptors. Here we investigate changes in electrophysiological properties and gene expression in photoreceptors of the adult cockroach, after exposure to constant light (CL) or constant dark (CD) for several months. After CL, we observed a decrease in mean whole-cell capacitance, a proxy for cell membrane area, from 362 ± 160 to 157 ± 58 pF, and a decrease in absolute sensitivity. However, after CD, we observed an increase in capacitance to 561 ± 155 pF and an increase in absolute sensitivity. Small changes in the expression of light-sensitive channels and signaling molecules were detected in CD retinas, together with a substantial increase in the expression of the primary green-sensitive opsin (GO1). Accordingly, light-induced currents became larger in CD photoreceptors. Even though normal levels of GO1 expression were retained in CL photoreceptors, light-induced currents became much smaller, suggesting that factors other than opsin are involved. Latency of phototransduction also decreased significantly in CL photoreceptors. Sustained voltage-activated K conductance was not significantly different between the experimental groups. The reduced capacitance of CL photoreceptors expanded their bandwidth, increasing the light-driven voltage signal at high frequencies. However, voltage noise was also amplified, probably because of unaltered expression of TRPL channels. Consequently, information transfer rates were lower in CL than in control or CD photoreceptors. These changes in whole-cell capacitance and electrophysiological parameters suggest that structural modifications can occur in the photoreceptors to adapt their function to altered environmental conditions. The opposing patterns of modifications in CL and CD photoreceptors differ profoundly from previous findings in photoreceptors.

Insect photoreceptors utilize two light-activated channels, TRP and TRPL, in their phototransduction cascades, but the American cockroach Periplaneta americana depends strongly on TRPL. Saari et al. show that TRPL generates high-gain and high-noise phototransduction suitable for dim light vision.

Visual transduction in rhabdomeric photoreceptors is compartmentalized and discretized. Signals of individual microvilli, the quantum bumps, are electrotonically summed, producing a graded response. Intrinsic dispersion of quantum bump latencies is thought to introduce noise and degrade signal transfer. Here, we found profound differences in the information rate and signaling bandwidth between in vitro patch-clamp and in vivo intracellular recordings of Periplaneta americana photoreceptors and traced them to the properties of quantum bumps and membrane resistance. Comparison of macroscopic and elementary light responses revealed differences in quantum bump summation and membrane resistance in vivo versus in vitro. Modeling of voltage bumps suggested that current bumps in vivo should be much bigger and faster than those actually recorded in vitro. Importantly, the group-average latency of dark-adapted photoreceptors was 30 ± 8 ms in intracellular ( n = 34) versus 70 ± 19 ms in patch-clamp ( n = 57) recordings. Duration of composite responses increased with mean latency because bump dispersion depended on mean latency. In vivo, latency dispersion broadened the composite response by 25% on average and slowed its onset. However, in the majority of photoreceptors, the characteristic durations of multiphoton impulse responses to 1-ms stimuli did not exceed the durations of mean voltage bumps. Consistently, we found strong associations between the latency and onset kinetics of the macroscopic response, on the one hand and the higher-frequency signal gain and information rate of the photoreceptor, on the other hand, indicating a direct connection between quantum bump latency and its dispersion and the signaling bandwidth. NEW & NOTEWORTHY When stimulated by light, microvilli of rhabdomeric photoreceptors produce discrete signals characterized by variable latencies. We show that this intrinsic latency dispersion restricts signaling bandwidth and information rate of photoreceptors in Periplaneta americana. Profound differences are found between the properties of photoreceptor responses in vivo and in vitro.

Insect ocelli are relatively simple eyes that have been assigned various functions not related to pictorial vision. In some species they function as sensors of ambient light intensity, from which information is relayed to various parts of the nervous system, e.g., for the control of circadian rhythms. In this work we have investigated the possibility that the ocellar light stimulation changes the properties of the optomotor performance of the cockroach Periplaneta americana. We used a virtual reality environment where a panoramic moving image is presented to the cockroach while its movements are recorded with a trackball. Previously we have shown that the optomotor reaction of the cockroach persists down to the intensity of moonless night sky, equivalent to less than 0.1 photons/s being absorbed by each compound eye photoreceptor. By occluding the compound eyes, the ocelli, or both, we show that the ocellar stimulation can change the intensity dependence of the optomotor reaction, indicating involvement of the ocellar visual system in the information processing of movement. We also measured the cuticular transmission, which, although relatively large, is unlikely to contribute profoundly to ocellar function, but may be significant in determining the mean activity level of completely blinded cockroaches.

In the visual systems of insects, different types of photoreceptors contribute to specialized visual channels that mediate distinct functions and behaviors. Large compound eyes of Periplaneta americana contain photoreceptors of two spectral classes, broadband green-sensitive photoreceptors and narrow-band UV-sensitive photoreceptors. Here, we investigated how visual stimulation by UV and green light affects locomotor, resting, and grooming behaviors in P. americana under conditions when light avoidance is not possible. We show that green but not UV light stimulates locomotor activity, inducing paradoxical positive masking. Duration of resting and grooming decreased with increasing light intensity, consistent with development of behavioral stress in response to visual overstimulation. A reaction of full immobility is described under UV light and at higher intensities of green light, with relative periods of immobility and grooming strongly negatively correlated. Low-intensity UV was more effective than low-intensity green light in suppressing grooming and inducing immobility. Our results suggest that locomotor activity in P. americana is mainly regulated by green-sensitive photoreceptors, and that dim UV light can trigger behavioral immobility, whereas both wavelengths induce stress-like reactions at high intensities. Considering the intrinsic UV sensitivity of green-sensitive photoreceptors, the contrasting behavioral responses indicate antagonistic interactions between UV and green visual channels.

The environment can play an important role in animal communication by affecting signal transmission and detection. Variation in the signalling environment is expected to be especially pronounced in widely distributed species, potentially affecting how their signals are detected. Such environmental variability is presumably relevant for sedentary females of a nocturnal capital breeder, the European common glow-worm (Lampyris noctiluca), which produce green light during the night to attract flying males to mate. Being widely distributed in Europe, glow-worm populations are exposed to both rapidly descending, darker summer nights in the south, and slowly dimming, brighter summer nights further north, with the latter potentially posing challenges to the visibility of the female glow. To test how female signalling is affected by latitude, we sampled glowing females during summer nights along a latitudinal gradient in Finland, Northern Europe, and used a novel apparatus to measure the intensity and peak wavelength (hue/colour) of their glow. Surprisingly, females at higher latitudes, similar to those at lower latitudes, were commonly glowing during the brightest (and hence the shortest) nights of the year. Females also glowed brighter in more northern areas, partly due to their larger body size, whereas the colour of their glow was not associated with latitude. Since females glow even during midsummer, independent of latitude, the increase in glow intensity at higher latitudes presumably serves to maintain signal visibility in brighter signalling conditions. Overall, these findings highlight the influence of environmental conditions on the evolution of sexual signals, especially in the context of species distribution range. Significance statement When environmental conditions impact signal transmission and perception, local conditions can have a crucial role in shaping animal communication and signal evolution. To analyse how dark-dependant common glow-worm females cope with variable nocturnal light environments, we used a novel apparatus, presumably not applied to living animals before, to measure female glow intensity at various latitudes along a latitudinal gradient. Interestingly, females did not avoid signalling during the brightest summer nights, but instead, their glow intensity and body size both increased with latitude. These findings suggest that females can ensure visibility to mate-searching males over a range of local conditions. Our study therefore shows how females can adapt to environmental constraints on signal visibility, and how the expression of sexual signals is shaped not only by social interactions but also by the signalling environment.

Neural mechanisms behind stereopsis, which requires simultaneous disparity inputs from two eyes, have remained mysterious. Here we show how ultrafast mirror-symmetric photomechanical contractions in the frontal forward-facing left and right eye photoreceptors give Drosophila super-resolution 3D-vision. By interlinking multiscale in vivo assays with multiscale simulations, we reveal how these photoreceptor microsaccades - by verging, diverging and narrowing the eyes' overlapping receptive fields - channel depth information, as phasic binocular image motion disparity signals in time. We further show how peripherally, outside stereopsis, microsaccadic sampling tracks a forward flying fly's optic flow field to better resolve the world in motion. These results change our understanding of how insect compound eyes work and suggest a general dynamic stereo-information sampling strategy for animals, robots and sensors.