Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila

As animals move through the world in search of resources, they change course in reaction to both external sensory cues and internally-generated programs. Elucidating the functional logic of complex search algorithms is challenging because the observable actions of the animal cannot be unambiguously assigned to externally- or internally-triggered events. We present a technique that addresses this challenge by assessing quantitatively the contribution of external stimuli and internal processes. We apply this technique to the analysis of rapid turns (“saccades”) of freely flying Drosophila melanogaster. We show that a single scalar feature computed from the visual stimulus experienced by the animal is sufficient to explain a majority (93%) of the turning decisions. We automatically estimate this scalar value from the observable trajectory, without any assumption regarding the sensory processing. A posteriori, we show that the estimated feature field is consistent with previous results measured in other experimental conditions. The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior. We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions. Our results suggest that comparatively few saccades in free-flying conditions are a result of an intrinsic spontaneous process, contrary to previous suggestions. We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens

Celestial navigation in Drosophila

Many casual observers typecast Drosophila melanogaster as a stationary pest that lurks around fruit and wine. However, the omnipresent fruit fly, which thrives even in desert habitats, likely established and maintained its cosmopolitan status via migration over large spatial scales. To perform long-distance dispersal, flies must actively maintain a straight compass heading through the use of external orientation cues, such as those derived from the sky. In this Review, we address how D. melanogaster accomplishes long-distance navigation using celestial cues. We focus on behavioral and physiological studies indicating that fruit flies can navigate both to a pattern of linearly polarized light and to the position of the sun – the same cues utilized by more heralded insect navigators such as monarch butterflies and desert ants. In both cases, fruit flies perform menotaxis, selecting seemingly arbitrary headings that they then maintain over time. We discuss how the fly's nervous system detects and processes this sensory information to direct the steering maneuvers that underlie navigation. In particular, we highlight recent findings that compass neurons in the central complex, a set of midline neuropils, are essential for navigation. Taken together, these results suggest that fruit flies share an ancient, latent capacity for celestial navigation with other insects. Furthermore, they illustrate the potential of D. melanogaster to help us to elucidate both the cellular basis of navigation and mechanisms of directed dispersal on a landscape scale

Optic Flow Based Visual Guidance: From Flying Insects to Miniature Aerial Vehicles

International audienc

Optic Flow Based Autopilots: Speed Control and Obstacle Avoidance

International audienceThe explicit control schemes presented here explain how insects may navigate on the sole basis of optic flow (OF) cues without requiring any distance or speed measurements: how they take off and land, follow the terrain, avoid the lateral walls in a corridor and control their forward speed automatically. The optic flow regulator, a feedback system controlling either the lift, the forward thrust or the lateral thrust, is described. Three OF regulators account for various insect flight patterns observed over the ground and over still water, under calm and windy conditions and in straight and tapered corridors. These control schemes were simulated experimentally and/or implemented onboard two types of aerial robots, a micro helicopter (MH) and a hovercraft (HO), which behaved much like insects when placed in similar environments. These robots were equipped with opto-electronic OF sensors inspired by our electrophysiological findings on houseflies' motion sensitive visual neurons. The simple, parsimonious control schemes described here require no conventional avionic devices such as range finders, groundspeed sensors or GPS receivers. They are consistent with the the neural repertoire of flying insects and meet the low avionic payload requirements of autonomous micro aerial and space vehicles

Celestial navigation in Drosophila

Many casual observers typecast Drosophila melanogaster as a stationary pest that lurks around fruit and wine. However, the omnipresent fruit fly, which thrives even in desert habitats, likely established and maintained its cosmopolitan status via migration over large spatial scales. To perform long-distance dispersal, flies must actively maintain a straight compass heading through the use of external orientation cues, such as those derived from the sky. In this Review, we address how D. melanogaster accomplishes long-distance navigation using celestial cues. We focus on behavioral and physiological studies indicating that fruit flies can navigate both to a pattern of linearly polarized light and to the position of the sun – the same cues utilized by more heralded insect navigators such as monarch butterflies and desert ants. In both cases, fruit flies perform menotaxis, selecting seemingly arbitrary headings that they then maintain over time. We discuss how the fly's nervous system detects and processes this sensory information to direct the steering maneuvers that underlie navigation. In particular, we highlight recent findings that compass neurons in the central complex, a set of midline neuropils, are essential for navigation. Taken together, these results suggest that fruit flies share an ancient, latent capacity for celestial navigation with other insects. Furthermore, they illustrate the potential of D. melanogaster to help us to elucidate both the cellular basis of navigation and mechanisms of directed dispersal on a landscape scale

Tracking nutrient decisions in Drosophila melanogaster

Animals integrate external sensory information and current metabolic needs to adapt their behavior in order to survive. Accordingly, many organisms can detect an internal nutritional imbalance and adjust their nutritional choices to restore homeostasis. Detailed quantitative analyses of nutrient-choice behaviors are needed to deepen our understanding of how neural circuits integrate internal state information and drive compensatory behavior when facing metabolic challenges. During this project, we developed an automated video tracking setup to characterize how metabolic and reproductive states interact to shape exploitation and exploration decisions taken by the adult fruit fly Drosophila melanogaster, to achieve nutritional homeostasis. We find that these two states have specific effects on the decisions to stop on and leave proteinaceous food patches. Furthermore, the internal nutrient state defines the exploration-exploitation trade-off: nutrient deprived flies focus on specific patches while satiated flies explore more globally. We provide few examples of how our paradigm could be used in the dissection of the genetic and neuronal pathways underlying nutrient decisions: First, we show that olfaction is not required for the compensatory high yeast feeding after amino acid deprivation, but that it mediates the efficient recognition of yeast as an appropriate food source in mated females. Second, we show that octopamine is required to mediate homeostatic postmating responses without affecting internal nutrient sensing. Third, we show how gustation is required to sustain interest for protein-rich resources upon amino acid deprivation. Our results provide a quantitative description of how the fly changes behavioral decisions to achieve homeostatic nutrient balancing and provide a framework for future detailed mechanistic dissection of such decisions

Active Vision Strategies in Predation

Visual predation requires precise and accurate behaviour, for which many predators have evolved excellent visual skills. However, an animal's visual abilities are greatly affected by how it moves its eyes, known as active vision. Insects have immobile eyes but can direct their gaze by moving their heads and bodies. This thesis examines three predatory insects with different predatory strategies, to understand the extent to which active vision can be used in predation. The first experimental chapter considers the African praying mantid, Sphodromantis lineola. Praying mantids are stationary terrestrial predators, which use their extremely mobile necks to visually track prey until it is within reach. By using statistical models, we identified what factors elicited strikes and, importantly, their success rate. The timing of head movements greatly increased the chances of strike success, with earlier movements increasing the success rate. The second experimental chapter addresses how darting robber flies, Psilonyx annulatus, aerially attack static prey. Prior to attacking, darting robber flies translate their body around a central point, assessing their prey. After assessment, they attack from a position correlated with the target's absolute size, not its angular size. Prey is beyond the robber fly's stereopsis range during the period of assessment. Assessments of differently sized targets have similarities with the behaviour exhibited by jumping insects, which use motion parallax, a form of active vision, to assess jump distance, suggesting darting robber flies also use motion parallax to predate. The final experimental chapter considers killer flies, Coenosia attenuata, which chase moving targets aerially. Killer flies use a combination of gravity and wing acceleration to increase their speed when chasing prey from above. This increased speed restricts the flies' ability to steer. However, killer flies create strong looming stimuli which may trigger their prey to produce evasive manoeuvres, thereby slowing down. Moreover, by travelling faster towards their prey, killer flies may avoid losing track of it, a real danger when chasing moving prey with low- resolution eyes potentially avoided thanks to active vision. By employing active vision, each of the predators considered can achieve impressive performances, despite relying on very different strategies to capture prey. The use of active vision can increase the success of already excellent visual predators and improve the performance of predator with limited vision. However, active vision can also substantially alter predatory behaviour, leading to a trade- off between the advantages in visual perception active vision can bring and the disadvantage in behavioural efficiency of active vision strategies

What does the honeybee see? And how do we know?

This book is the only account of what the bee, as an example of an insect, actually detects with its eyes. Bees detect some visual features such as edges and colours, but there is no sign that they reconstruct patterns or put together features to form objects. Bees detect motion but have no perception of what it is that moves, and certainly they do not recognize “things” by their shapes. Yet they clearly see well enough to fly and find food with a minute brain. Bee vision is therefore relevant to the construction of simple artificial visual systems, for example for mobile robots. The surprising conclusion is that bee vision is adapted to the recognition of places, not things. In this volume, Adrian Horridge also sets out the curious and contentious history of how bee vision came to be understood, with an account of a century of neglect of old experimental results, errors of interpretation, sharp disagreements, and failures of the scientific method. The design of the experiments and the methods of making inferences from observations are also critically examined, with the conclusion that scientists are often hesitant, imperfect and misleading, ignore the work of others, and fail to consider alternative explanations. The erratic path to understanding makes interesting reading for anyone with an analytical mind who thinks about the methods of science or the engineering of seeing machines

Optimal searching behaviour generated intrinsically by the central pattern generator for locomotion.

Efficient searching for resources such as food by animals is key to their survival. It has been proposed that diverse animals from insects to sharks and humans adopt searching patterns that resemble a simple Lévy random walk, which is theoretically optimal for 'blind foragers' to locate sparse, patchy resources. To test if such patterns are generated intrinsically, or arise via environmental interactions, we tracked free-moving Drosophila larvae with (and without) blocked synaptic activity in the brain, suboesophageal ganglion (SOG) and sensory neurons. In brain-blocked larvae, we found that extended substrate exploration emerges as multi-scale movement paths similar to truncated Lévy walks. Strikingly, power-law exponents of brain/SOG/sensory-blocked larvae averaged 1.96, close to a theoretical optimum (µ ≅ 2.0) for locating sparse resources. Thus, efficient spatial exploration can emerge from autonomous patterns in neural activity. Our results provide the strongest evidence so far for the intrinsic generation of Lévy-like movement patterns