Environmental impact on visual perception modulates behavioral responses of schooling fish to looming predators.

Aggregation in social fishes has evolved to improve safety from predators. The individual interaction mechanisms that govern collective behavior are determined by the sensory systems that translate environmental information into behavior. In dynamic environments, shifts in conditions impede effective visual sensory perception in fish schools, and may induce changes in the collective response. Here, we consider whether environmental conditions that affect visual contrast modulate the collective response of schools to looming predators. By using a virtual environment to simulate four contrast levels, we tested whether the collective state of minnow fish schools was modified in response to a looming optical stimulus. Our results indicate that fish swam slower and were less polarized in lower contrast conditions. Additionally, schooling metrics known to be regulated by non-visual sensory systems tended to correlate better when contrast decreased. Over the course of the escape response, schools remained tightly formed and retained the capability of transferring social information. We propose that when visual perception is compromised, the interaction rules governing collective behavior are likely to be modified to prioritize ancillary sensory information crucial to maximizing chance of escape. Our results imply that multiple sensory systems can integrate to control collective behavior in environments with unreliable visual information.

Why flying insects gather at artificial light.

Explanations of why nocturnal insects fly erratically around fires and lamps have included theories of "lunar navigation" and "escape to the light". However, without three-dimensional flight data to test them rigorously, the cause for this odd behaviour has remained unsolved. We employed high-resolution motion capture in the laboratory and stereo-videography in the field to reconstruct the 3D kinematics of insect flights around artificial lights. Contrary to the expectation of attraction, insects do not steer directly toward the light. Instead, insects turn their dorsum toward the light, generating flight bouts perpendicular to the source. Under natural sky light, tilting the dorsum towards the brightest visual hemisphere helps maintain proper flight attitude and control. Near artificial sources, however, this highly conserved dorsal-light-response can produce continuous steering around the light and trap an insect. Our guidance model demonstrates that this dorsal tilting is sufficient to create the seemingly erratic flight paths of insects near lights and is the most plausible model for why flying insects gather at artificial lights.

Stabilizing responses to sideslip disturbances in Drosophila melanogaster are modulated by the density of moving elements on the ground.

Stabilizing responses to sideslip disturbances are a critical part of the flight control system in flies. While strongly mediated by mechanoreception, much of the final response results from the wide-field motion detection system associated with vision. In order to be effective, these responses must match the disturbance they are aimed to correct. To do this, flies must estimate the velocity of the disturbance, although it is not known how they accomplish this task when presented with natural images or dot fields. The recent finding, that motion parallax in dot fields can modulate stabilizing responses only if perceived below the fly, raises the question of whether other image statistics are also processed differently between eye regions. One such parameter is the density of elements moving in translational optic flow. Depending on the habitat, there might be strong differences in the density of elements providing information about self-motion above and below the fly, which in turn could act as selective pressures tuning the visual system to process this parameter on a regional basis. By presenting laterally moving dot fields of different densities we found that, in Drosophila melanogaster, the amplitude of the stabilizing response is significantly affected by the number of elements in the field of view. Flies countersteer strongly within a relatively low and narrow range of element densities. But this effect is exclusive to the ventral region of the eye, and dorsal stimuli elicit an unaltered and stereotypical response regardless of the density of elements in the flow. This highlights local specialization of the eye and suggests the lower region may play a more critical role in translational flight stabilization.

Light environment drives evolution of color vision genes in butterflies and moths.

Opsins, combined with a chromophore, are the primary light-sensing molecules in animals and are crucial for color vision. Throughout animal evolution, duplications and losses of opsin proteins are common, but it is unclear what is driving these gains and losses. Light availability is implicated, and dim environments are often associated with low opsin diversity and loss. Correlations between high opsin diversity and bright environments, however, are tenuous. To test if increased light availability is associated with opsin diversification, we examined diel niche and identified opsins using transcriptomes and genomes of 175 butterflies and moths (Lepidoptera). We found 14 independent opsin duplications associated with bright environments. Estimating their rates of evolution revealed that opsins from diurnal taxa evolve faster-at least 13 amino acids were identified with higher dN/dS rates, with a subset close enough to the chromophore to tune the opsin. These results demonstrate that high light availability increases opsin diversity and evolution rate in Lepidoptera.

Ventral motion parallax enhances fruit fly steering to visual sideslip.

Flies and other insects use incoherent motion (parallax) to the front and sides to measure distances and identify obstacles during translation. Although additional depth information could be drawn from below, there is no experimental proof that they use it. The finding that blowflies encode motion disparities in their ventral visual fields suggests this may be an important region for depth information. We used a virtual flight arena to measure fruit fly responses to optic flow. The stimuli appeared below (n = 51) or above the fly (n = 44), at different speeds, with or without parallax cues. Dorsal parallax does not affect responses, and similar motion disparities in rotation have no effect anywhere in the visual field. But responses to strong ventral sideslip (206° s-1) change drastically depending on the presence or absence of parallax. Ventral parallax could help resolve ambiguities in cluttered motion fields, and enhance corrective responses to nearby objects.

Small eyes in dim light: Implications to spatio-temporal visual abilities in Drosophila melanogaster.

Fruit flies, Drosophila melanogaster, are active over a range of light intensities in the wild, but lab-reared flies are often tested only in bright light. Similarly, scarce feeding during larval stages-common in nature-generates smaller adults, and a wide range of eye sizes not found in well-fed lab colonies. Both dimmer light and smaller eyes limit light capture and have undetermined effects on visual behaviors such as flight. In this study, we used moving sinusoidal gratings to test spatial acuity, temporal acuity, and contrast threshold of female flies of varying eye sizes at different light intensities. We also investigated vision in the smaller and often neglected male fruit flies. As light intensity drops from 50.1 lx to 0.3 lx, flies have a reduced spatial acuity (females: from 0.1 to 0.06 cycles per degree, CPD, males: 0.1 to 0.04 CPD) and temporal acuity (females: from 50 Hz to 10 Hz, males: 25 Hz to 10 Hz), and an increased contrast detection threshold (females: from 10% to 29%, males: 19% to 48%). We find no major sex-specific differences after accounting for eye size. Visual abilities in both small (eye area of 0.1-0.17 mm2) and large flies (0.17-0.23 mm2) suffer at 0.3 lx compared to 50.1 lx, but small flies suffer more (spatial acuity: 0.03 vs 0.06 CPD, contrast threshold: 76% vs 57%, temporal acuity: 5 Hz vs 10 Hz). Our results suggest visual abilities of small flies suffer more than large flies at low light levels, possibly leading to size- and light intensity-dependent effects on foraging, navigation, and flight.

Small fruit flies sacrifice temporal acuity to maintain contrast sensitivity.

Holometabolous insects, like fruit flies, grow primarily during larval development. Scarce larval feeding is common in nature and generates smaller adults. Despite the importance of vision to flies, eye size scales proportionately with body size, and smaller eyes confer poorer vision due to smaller optics. Variable larval feeding, therefore, causes within-species differences in visual processing, which have gone largely unnoticed due to ad libitum feeding in the lab that results in generally large adults. Do smaller eyes have smaller ommatidial lenses, reducing sensitivity, or broader inter-ommatidial angles, reducing acuity? And to what extent might neural processes adapt to these optical challenges with temporal and spatial summation? To understand this in the fruit fly, we generated a distribution of body lengths (1.67-2.34 mm; n = 24) and eye lengths (0.33-0.44 mm; n = 24), resembling the distribution of wild-caught flies, by removing larvae from food during their third instar. We find smaller eyes (0.19 vs.0.07 mm2) have substantially fewer (978 vs. 540, n = 45) and smaller ommatidia (222 vs. 121 µm2;n = 45) separated by slightly wider inter-ommatidial angles (4.5 vs.5.5°; n = 34). This corresponds to a greater loss in contrast sensitivity (<50%) than spatial acuity (<20%). Using a flight arena and psychophysics paradigm, we find that smaller flies lose little spatial acuity (0.126 vs. 0.118CPD; n = 45), and recover contrast sensitivity (2.22 for both; n = 65) by sacrificing temporal acuity (26.3 vs. 10.8Hz; n = 112) at the neural level. Therefore, smaller flies sacrifice contrast sensitivity to maintain spatial acuity optically, but recover contrast sensitivity, almost completely, by sacrificing temporal acuity neurally.

Fruit flies are multistable geniuses.

Our sensory systems have evolved to provide us with information about the external world. Such information is useful only insofar as it leads to actions that enhance fitness, and thus, the link between sensation and action has been thoroughly studied in many species. In insects, for example, specific visual stimuli lead to highly stereotyped responses. In contrast, humans can exhibit a wide range of responses to the same stimulus, as occurs most notably in the phenomenon of multistable perception. On this basis, one might think that humans have a fundamentally different way of generating actions from sensory inputs, but Toepfer et al. show that flies show evidence of multistable perception as well. Specifically, when confronted with a sensory stimulus that can yield different motor responses, flies switch from one response to another with temporal dynamics that are similar to those of humans and other animals. This suggests that the mechanisms that give rise to the rich repertoire of sensory experience in humans have correlates in much simpler nervous systems.

The forensically important blow fly, Chrysomya megacephala (Diptera: Calliphoridae), is more likely to walk than fly to carrion at low light levels.

One factor that influences estimates of time since death using entomological evidence is whether or not blow flies nocturnally oviposit. Field studies focusing on egg laying have found it occurs on an inconsistent basis. A key but poorly understood factor in nocturnal oviposition is a blow fly's ability to locate carrion under low light levels. It has been speculated that blow flies are more likely to walk than fly to carrion during the night, but this has not been empirically tested. We directly compared guided walking versus flying using infrared sensors under low light levels in laboratory conditions for Chrysomya megacephala (F.) (Diptera: Calliphoridae), a blow fly previously described to be nocturnal. We found C. megacephala is more likely to walk than fly toward carrion under low light levels (p=0.016). We did not, however, find differences between males and females for walking (p=0.48) or flying (p=0.42) despite male C. megacephala possessing eyes better suited for increased light capture. These results demonstrate the need to better understand where blow flies go at night, as bodies found within a fly's walking distance are more likely to be colonized.

A visual horizon affects steering responses during flight in fruit flies.

To navigate well through three-dimensional environments, animals must in some way gauge the distances to objects and features around them. Humans use a variety of visual cues to do this, but insects, with their small size and rigid eyes, are constrained to a more limited range of possible depth cues. For example, insects attend to relative image motion when they move, but cannot change the optical power of their eyes to estimate distance. On clear days, the horizon is one of the most salient visual features in nature, offering clues about orientation, altitude and, for humans, distance to objects. We set out to determine whether flying fruit flies treat moving features as farther off when they are near the horizon. Tethered flies respond strongly to moving images they perceive as close. We measured the strength of steering responses while independently varying the elevation of moving stimuli and the elevation of a virtual horizon. We found responses to vertical bars are increased by negative elevations of their bases relative to the horizon, closely correlated with the inverse of apparent distance. In other words, a bar that dips far below the horizon elicits a strong response, consistent with using the horizon as a depth cue. Wide-field motion also had an enhanced effect below the horizon, but this was only prevalent when flies were additionally motivated with hunger. These responses may help flies tune behaviors to nearby objects and features when they are too far off for motion parallax.

To keep on track during flight, fruitflies discount the skyward view.

When small flying insects go off their intended course, they use the resulting pattern of motion on their eye, or optic flow, to guide corrective steering. A change in heading generates a unique, rotational motion pattern and a change in position generates a translational motion pattern, and each produces corrective responses in the wingbeats. Any image in the flow field can signal rotation, but owing to parallax, only the images of nearby objects can signal translation. Insects that fly near the ground might therefore respond more strongly to translational optic flow that occurs beneath them, as the nearby ground will produce strong optic flow. In these experiments, rigidly tethered fruitflies steered in response to computer-generated flow fields. When correcting for unintended rotations, flies weight the motion in their upper and lower visual fields equally. However, when correcting for unintended translations, flies weight the motion in the lower visual fields more strongly. These results are consistent with the interpretation that fruitflies stabilize by attending to visual areas likely to contain the strongest signals during natural flight conditions.

Flying fruit flies correct for visual sideslip depending on relative speed of forward optic flow.

As a fly flies through its environment, static objects produce moving images on its retina, and this optic flow is essential for steering and course corrections. Different types of rotation and translation produce unique flow fields, which fly brains are wired to identify. However, a feature of optic flow unique to translational motion is that adjacent images may move across the retina at different speeds, depending on their distance from the observer. Many insects take advantage of this depth cue, called motion parallax, to determine the distance to objects. We wanted to know if differential object speeds affect the corrective responses of fruit flies when they experience unplanned course deviations. We presented tethered flying flies with optic flow and measured their corrective responses to sideways perturbations of images with different relative forward speeds. We found that flying flies attend to the relative speed of dots during forward motion, and adjust their corrective responses to sideslip deviations depending on this cue. With no other distinguishing features (such as brightness or size), flies mounted a greater response to sideways deviations that were signaled by faster moving dots in the forward flow field, those that appeared radially closer by their speeds. This is consistent with the interpretation that fruit flies attend to seemingly nearer objects, and correct more strongly when they indicate a perturbation.

An olfactory circuit increases the fidelity of visual behavior.

Multimodal integration allows neural circuits to be activated in a behaviorally context-specific manner. In the case of odor plume tracking by Drosophila, an attractive odorant increases the influence of yaw-optic flow on steering behavior in flight, which enhances visual stability reflexes, resulting in straighter flight trajectories within an odor plume. However, it is not well understood whether context-specific changes in optomotor behavior are the result of an increased sensitivity to motion inputs (e.g., through increased visual attention) or direct scaling of motor outputs (i.e., increased steering gain). We address this question by examining the optomotor behavior of Drosophila melanogaster in a tethered flight assay and demonstrate that whereas olfactory cues decrease the gain of the optomotor response to sideslip optic flow, they concomitantly increase the gain of the yaw optomotor response by enhancing the animal's ability to follow transient visual perturbations. Furthermore, ablating the mushroom bodies (MBs) of the fly brain via larval hydroxyurea (HU) treatment results in a loss of olfaction-dependent increase in yaw optomotor fidelity. By expressing either tetanus toxin light chain or diphtheria toxin in gal4-defined neural circuits, we were able to replicate the loss of function observed in the HU treatment within the lines expressing broadly in the mushroom bodies, but not within specific mushroom body lobes. Finally, we were able to genetically separate the yaw responses and sideslip responses in our behavioral assay. Together, our results implicate the MBs in a fast-acting, memory-independent olfactory modification of a visual reflex that is critical for flight control.

Theta motion processing in fruit flies.

The tiny brains of insects presumably impose significant computational limitations on algorithms controlling their behavior. Nevertheless, they perform fast and sophisticated visual maneuvers. This includes tracking features composed of second-order motion, in which the feature is defined by higher-order image statistics, but not simple correlations in luminance. Flies can track the true direction of even theta motions, in which the first-order (luminance) motion is directed opposite the second-order moving feature. We exploited this paradoxical feature tracking response to dissect the particular image properties that flies use to track moving objects. We find that theta motion detection is not simply a result of steering toward any spatially restricted flicker. Rather, our results show that fly high-order feature tracking responses can be broken down into positional and velocity components - in other words, the responses can be modeled as a superposition of two independent steering efforts. We isolate these elements to show that each has differing influence on phase and amplitude of steering responses, and together they explain the time course of second-order motion tracking responses during flight. These observations are relevant to natural scenes, where moving features can be much more complex.

Dynamics of optomotor responses in Drosophila to perturbations in optic flow.

For a small flying insect, correcting unplanned course perturbations is essential for navigating through the world. Visual course control relies on estimating optic flow patterns which, in flies, are encoded by interneurons of the third optic ganglion. However, the rules that translate optic flow into flight motor commands remain poorly understood. Here, we measured the temporal dynamics of optomotor responses in tethered flies to optic flow fields about three cardinal axes. For each condition, we used white noise analysis to determine the optimal linear filters linking optic flow to the sum and difference of left and right wing beat amplitudes. The estimated filters indicate that flies react very quickly to perturbations of the motion field, with pure delays in the order of approximately 20 ms and time-to-peak of approximately 100 ms. By convolution the filters also predict responses to arbitrary stimulus sequences, accounting for over half the variance in 5 of our 6 stimulus types, demonstrating the approximate linearity of the system with respect to optic flow variables. In the remaining case of yaw optic flow we improved predictability by measuring individual flies, which also allowed us to analyze the variability of optomotor responses within a population. Finally, the linear filters at least partly explain the optomotor responses to superimposed and decomposed compound flow fields.

Wide-field motion tuning in nocturnal hawkmoths.

Nocturnal hawkmoths are known for impressive visually guided behaviours in dim light, such as hovering while feeding from nectar-bearing flowers. This requires tight visual feedback to estimate and counter relative motion. Discrimination of low velocities, as required for stable hovering flight, is fundamentally limited by spatial resolution, yet in the evolution of eyes for nocturnal vision, maintenance of high spatial acuity compromises absolute sensitivity. To investigate these trade-offs, we compared responses of wide-field motion-sensitive neurons in three species of hawkmoth: Manduca sexta (a crepuscular hoverer), Deilephila elpenor (a fully nocturnal hoverer) and Acherontia atropos (a fully nocturnal hawkmoth that does not hover as it feeds uniquely from honey in bees' nests). We show that despite smaller eyes, the motion pathway of D. elpenor is tuned to higher spatial frequencies and lower temporal frequencies than A. atropos, consistent with D. elpenor's need to detect low velocities for hovering. Acherontia atropos, however, presumably evolved low-light sensitivity without sacrificing temporal acuity. Manduca sexta, active at higher light levels, is tuned to the highest spatial frequencies of the three and temporal frequencies comparable with A. atropos. This yields similar tuning to low velocities as in D. elpenor, but with the advantage of shorter neural delays in processing motion.

Visual stabilization dynamics are enhanced by standing flight velocity.

A flying insect must travel to find food, mates and sites for oviposition, but for a small animal in a turbulent world this means dealing with frequent unplanned deviations from course. We measured a fly's sensory-motor impulse response to perturbations in optic flow. After an abrupt change in its apparent visual position, a fly generates a compensatory dynamical steering response in the opposite direction. The response dynamics, however, may be influenced by superimposed background velocity generated by the animal's flight direction. Here we show that constant forward velocity has no effect on the steering responses to orthogonal sideslip perturbations, whereas constant parallel sideslip substantially shortens the lags and relaxation times of the linear dynamical responses. This implies that for flies stabilizing in sideslip, the control effort is strongly affected by the direction of background motion.

The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant).

Box jellyfish, or cubomedusae (class Cubozoa), are unique among the Cnidaria in possessing lens eyes similar in morphology to those of vertebrates and cephalopods. Although these eyes were described over 100 years ago, there has been no work done on their electrophysiological responses to light. We used an electroretinogram (ERG) technique to measure spectral sensitivity of the lens eyes of the Caribbean species Tripedalia cystophora. The cubomedusae have two kinds of lens eyes, the lower and upper lens eyes. We found that both lens eye types have similar spectral sensitivities, which likely result from the presence of a single receptor type containing a single opsin. The peak sensitivity is to blue-green light. Visual pigment template fits indicate a vitamin A-1 based opsin with peak sensitivity near 500 nm for both eye types.