Multimodal interactions in insect navigation

Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species’ sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities

Wing and body motion during flight initiation in Drosophila revealed by automated visual tracking

The fruit fly Drosophila melanogaster is a widely used model organism in studies of genetics, developmental biology and biomechanics. One limitation for exploiting Drosophila as a model system for behavioral neurobiology is that measuring body kinematics during behavior is labor intensive and subjective. In order to quantify flight kinematics during different types of maneuvers, we have developed a visual tracking system that estimates the posture of the fly from multiple calibrated cameras. An accurate geometric fly model is designed using unit quaternions to capture complex body and wing rotations, which are automatically fitted to the images in each time frame. Our approach works across a range of flight behaviors, while also being robust to common environmental clutter. The tracking system is used in this paper to compare wing and body motion during both voluntary and escape take-offs. Using our automated algorithms, we are able to measure stroke amplitude, geometric angle of attack and other parameters important to a mechanistic understanding of flapping flight. When compared with manual tracking methods, the algorithm estimates body position within 4.4±1.3% of the body length, while body orientation is measured within 6.5±1.9 deg. (roll), 3.2±1.3 deg. (pitch) and 3.4±1.6 deg. (yaw) on average across six videos. Similarly, stroke amplitude and deviation are estimated within 3.3 deg. and 2.1 deg., while angle of attack is typically measured within 8.8 deg. comparing against a human digitizer. Using our automated tracker, we analyzed a total of eight voluntary and two escape take-offs. These sequences show that Drosophila melanogaster do not utilize clap and fling during take-off and are able to modify their wing kinematics from one wingstroke to the next. Our approach should enable biomechanists and ethologists to process much larger datasets than possible at present and, therefore, accelerate insight into the mechanisms of free-flight maneuvers of flying insects

多対象物のトラッキングとそのハエ行動解析への応用

Tohoku University橋本浩一課

Visual stimulation of saccades in magnetically tethered Drosophila

Flying fruit flies, Drosophila melanogaster, perform `body saccades', in which they change heading by about 90° in roughly 70 ms. In free flight, visual expansion can evoke saccades, and saccade-like turns are triggered by similar stimuli in tethered flies. However, because the fictive turns in rigidly tethered flies follow a much longer time course, the extent to which these two behaviors share a common neural basis is unknown. A key difference between tethered and free flight conditions is the presence of additional sensory cues in the latter, which might serve to modify the time course of the saccade motor program. To study the role of sensory feedback in saccades, we have developed a new preparation in which a fly is tethered to a fine steel pin that is aligned within a vertically oriented magnetic field, allowing it to rotate freely around its yaw axis. In this experimental paradigm, flies perform rapid turns averaging 35° in 80 ms, similar to the kinematics of free flight saccades. Our results indicate that tethered and free flight saccades share a common neural basis, but that the lack of appropriate feedback signals distorts the behavior performed by rigidly fixed flies. Using our new paradigm, we also investigated the features of visual stimuli that elicit saccades. Our data suggest that saccades are triggered when expanding objects reach a critical threshold size, but that their timing depends little on the precise time course of expansion. These results are consistent with expansion detection circuits studied in other insects, but do not exclude other models based on the integration of local movement detectors

Enhanced flight performance by genetic manipulation of wing shape in Drosophila

Insect wing shapes are remarkably diverse and the combination of shape and kinematics determines both aerial capabilities and power requirements. However, the contribution of any specific morphological feature to performance is not known. Using targeted RNA interference to modify wing shape far beyond the natural variation found within the population of a single species, we show a direct effect on flight performance that can be explained by physical modelling of the novel wing geometry. Our data show that altering the expression of a single gene can significantly enhance aerial agility and that the Drosophila wing shape is not, therefore, optimized for certain flight performance characteristics that are known to be important. Our technique points in a new direction for experiments on the evolution of performance specialities in animals

Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster

Flies rely heavily on visual feedback for several aspects of flight control. As a fly approaches an object, the image projected across its retina expands, providing the fly with visual feedback that can be used either to trigger a collision-avoidance maneuver or a landing response. To determine how a fly makes the decision to land on or avoid a looming object, we measured the behaviors generated in response to an expanding image during tethered flight in a visual closed-loop flight arena. During these experiments, each fly varied its wing-stroke kinematics to actively control the azimuth position of a 15°×15° square within its visual field. Periodically, the square symmetrically expanded in both the horizontal and vertical directions. We measured changes in the fly's wing-stroke amplitude and frequency in response to the expanding square while optically tracking the position of its legs to monitor stereotyped landing responses. Although this stimulus could elicit both the landing responses and collision-avoidance reactions, separate pathways appear to mediate the two behaviors. For example, if the square is in the lateral portion of the fly's field of view at the onset of expansion, the fly increases stroke amplitude in one wing while decreasing amplitude in the other, indicative of a collision-avoidance maneuver. In contrast, frontal expansion elicits an increase in wing-beat frequency and leg extension, indicative of a landing response. To further characterize the sensitivity of these responses to expansion rate, we tested a range of expansion velocities from 100 to 10000° s^(-1). Differences in the latency of both the collision-avoidance reactions and the landing responses with expansion rate supported the hypothesis that the two behaviors are mediated by separate pathways. To examine the effects of visual feedback on the magnitude and time course of the two behaviors, we presented the stimulus under open-loop conditions, such that the fly's response did not alter the position of the expanding square. From our results we suggest a model that takes into account the spatial sensitivities and temporal latencies of the collision-avoidance and landing responses, and is sufficient to schematically represent how the fly uses integration of motion information in deciding whether to turn or land when confronted with an expanding object

Representations of Reward and Movement in Drosophila Dopaminergic Neurons

The neuromodulator dopamine is known to influence both immediate and future behavior, motivating and invigorating an animal’s ongoing movement but also serving as a reinforcement signal to instruct learning. Yet it remains unclear whether this dual role of dopamine involves the same dopaminergic pathways. Although reward-responsive dopaminergic neurons display movement-related activity, debate continues as to what features of an individual’s experience these motor-correlates correspond and how they influence concurrent behavior. The mushroom body, a prominent neuropil in the brain of the fruit fly Drosophila melanogaster, is richly innervated by dopaminergic neurons that play an essential role in the formation of olfactory associations. While dopaminergic neurons respond to reward and punishment to drive associative learning, they have also been implicated in a number of adaptive behaviors and their activity correlates with the behavioral state of an animal and its coarse motor actions. Here, we take advantage of the concise circuit architecture of the Drosophila mushroom body to investigate the nature of motor-related signals in dopaminergic neurons that drive associative learning. In vivo functional imaging during naturalistic tethered locomotion reveals that the activity of different subsets of mushroom body dopaminergic neurons reflects distinct aspects of movement. To gain insight into what facets of an animal’s experience are represented by these movement-related signals, we employed a closed loop virtual reality paradigm to monitor neural activity as animals track an olfactory stimulus and are actively engaged in a goal-directed and sensory-motivated behavior. We discover that odor responses in dopaminergic neurons correlate with the extent to which an animal tracks upwind towards the fictive odor source. In different experimental contexts where distinct motor actions were required to track the odor, dopaminergic neurons become emergently linked to the behavioral metric most relevant for effective olfactory navigation. Subsets of dopaminergic neurons were correlated with the strength of upwind tracking regardless of the identity of the odor and remained so even after the satiety state of an animal was altered. We proceed to demonstrate that transient inhibition of dopaminergic neurons that are positively correlated with upwind tracking significantly diminishes the normal approach responses to an appetitive olfactory cue. Accordingly, activation of those same dopaminergic neurons enhances approach to an odor and even drives upwind tracking in clean air alone. Together, these results reveal that the same dopaminergic pathways that convey reinforcements to instruct learning also carry representations of an animal’s moment-by-moment movements and actively influence behavior. The complex activity patterns of mushroom body dopaminergic neurons therefore represent neither purely sensory nor motor variables but rather reflect the goal or motivation underlying an animal’s movements. Our data suggest a fundamental coupling between reinforcement signals and motivation-related locomotor representations within dopaminergic circuitry, drawing a striking parallel between the mushroom body dopaminergic neurons described here and the emerging understanding of mammalian dopaminergic pathways. The apparent conservation in dopaminergic neuromodulatory networks between mammals and insects suggests a shared logic for how neural circuits assign meaning to both sensory stimuli and motor actions to generate flexible and adaptive behavior

Plume-Tracking Behavior of Flying Drosophila Emerges from a Set of Distinct Sensory-Motor Reflexes

Background: For a fruit fly, locating fermenting fruit where it can feed, find mates, and lay eggs is an essential and difficult task requiring the integration of olfactory and visual cues. Here, we develop an approach to correlate flies’ free-flight behavior with their olfactory experience under different wind and visual conditions, yielding new insight into plume tracking based on over 70 hr of data. Results: To localize an odor source, flies exhibit three iterative, independent, reflex-driven behaviors, which remain constant through repeated encounters of the same stimulus: (1) 190 ± 75 ms after encountering a plume, flies increase their flight speed and turn upwind, using visual cues to determine wind direction. Due to this substantial response delay, flies pass through the plume shortly after entering it. (2) 450 ± 165 ms after losing the plume, flies initiate a series of vertical and horizontal casts, using visual cues to maintain a crosswind heading. (3) After sensing an attractive odor, flies exhibit an enhanced attraction to small visual features, which increases their probability of finding the plume’s source. Conclusions: Due to plume structure and sensory-motor delays, a fly’s olfactory experience during foraging flights consists of short bursts of odor stimulation. As a consequence, delays in the onset of crosswind casting and the increased attraction to visual features are necessary behavioral components for efficiently locating an odor source. Our results provide a quantitative behavioral background for elucidating the neural basis of plume tracking using genetic and physiological approaches

A computational model of the integration of landmarks and motion in the insect central complex.

The insect central complex (CX) is an enigmatic structure whose computational function has evaded inquiry, but has been implicated in a wide range of behaviours. Recent experimental evidence from the fruit fly (Drosophila melanogaster) and the cockroach (Blaberus discoidalis) has demonstrated the existence of neural activity corresponding to the animal's orientation within a virtual arena (a neural 'compass'), and this provides an insight into one component of the CX structure. There are two key features of the compass activity: an offset between the angle represented by the compass and the true angular position of visual features in the arena, and the remapping of the 270° visual arena onto an entire circle of neurons in the compass. Here we present a computational model which can reproduce this experimental evidence in detail, and predicts the computational mechanisms that underlie the data. We predict that both the offset and remapping of the fly's orientation onto the neural compass can be explained by plasticity in the synaptic weights between segments of the visual field and the neurons representing orientation. Furthermore, we predict that this learning is reliant on the existence of neural pathways that detect rotational motion across the whole visual field and uses this rotation signal to drive the rotation of activity in a neural ring attractor. Our model also reproduces the 'transitioning' between visual landmarks seen when rotationally symmetric landmarks are presented. This model can provide the basis for further investigation into the role of the central complex, which promises to be a key structure for understanding insect behaviour, as well as suggesting approaches towards creating fully autonomous robotic agents