Emergent spatial goals in an integrative model of the insect central complex.

The insect central complex appears to encode and process spatial information through vector manipulation. Here, we draw on recent insights into circuit structure to fuse previous models of sensory-guided navigation, path integration and vector memory. Specifically, we propose that the allocentric encoding of location provided by path integration creates a spatially stable anchor for converging sensory signals that is relevant in multiple behavioural contexts. The allocentric reference frame given by path integration transforms a goal direction into a goal location and we demonstrate through modelling that it can enhance approach of a sensory target in noisy, cluttered environments or with temporally sparse stimuli. We further show the same circuit can improve performance in the more complex navigational task of route following. The model suggests specific functional roles for circuit elements of the central complex that helps explain their high preservation across insect species.

Impact of central complex lesions on innate and learnt visual navigation in ants.

Wood ants are excellent navigators, using a combination of innate and learnt navigational strategies to travel between their nest and feeding sites. Visual navigation in ants has been studied extensively, however, we have little direct evidence for the underlying neural mechanisms. Here, we perform lateralized mechanical lesions in the central complex (CX) of wood ants, a midline structure known to allow an insect to keep track of the direction of sensory cues relative to its own orientation and to control movement. We lesioned two groups of ants and observed their behaviour in an arena with a large visual landmark present. The first group of ants were naïve and when intact such ants show a clear innate attraction to the conspicuous landmark. The second group of ants were trained to aim to a food location to the side of the landmark. The general heading of naïve ants towards a visual cue was not altered by the lesions, but the heading of ants trained to a landmark adjacent food position was affected. Thus, CX lesions had a specific impact on learnt visual guidance. We also observed that lateralised lesions altered the fine details of turning with lesioned ants spending less time turning to the side ipsilateral of the lesion. The results confirm the role of the CX in turn control and highlight its important role in the implementation of learnt behaviours that rely on information from other brain regions.

A unified mechanism for innate and learned visual landmark guidance in the insect central complex.

Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can elicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimal cue integration.

A motion compensation treadmill for untethered wood ants (Formica rufa): evidence for transfer of orientation memories from free-walking training.

The natural scale of insect navigation during foraging makes it challenging to study under controlled conditions. Virtual reality and trackball setups have offered experimental control over visual environments while studying tethered insects, but potential limitations and confounds introduced by tethering motivates the development of alternative untethered solutions. In this paper, we validate the use of a motion compensator (or 'treadmill') to study visually driven behaviour of freely moving wood ants (Formica rufa). We show how this setup allows naturalistic walking behaviour and preserves foraging motivation over long time frames. Furthermore, we show that ants are able to transfer associative and navigational memories from classical maze and arena contexts to our treadmill. Thus, we demonstrate the possibility to study navigational behaviour over ecologically relevant durations (and virtual distances) in precisely controlled environments, bridging the gap between natural and highly controlled laboratory experiments.

Modeling visual-based pitch, lift and speed control strategies in hoverflies.

To avoid crashing onto the floor, a free falling fly needs to trigger its wingbeats quickly and control the orientation of its thrust accurately and swiftly to stabilize its pitch and hence its speed. Behavioural data have suggested that the vertical optic flow produced by the fall and crossing the visual field plays a key role in this anti-crash response. Free fall behavior analyses have also suggested that flying insect may not rely on graviception to stabilize their flight. Based on these two assumptions, we have developed a model which accounts for hoverflies´ position and pitch orientation recorded in 3D with a fast stereo camera during experimental free falls. Our dynamic model shows that optic flow-based control combined with closed-loop control of the pitch suffice to stabilize the flight properly. In addition, our model sheds a new light on the visual-based feedback control of fly´s pitch, lift and thrust. Since graviceptive cues are possibly not used by flying insects, the use of a vertical reference to control the pitch is discussed, based on the results obtained on a complete dynamic model of a virtual fly falling in a textured corridor. This model would provide a useful tool for understanding more clearly how insects may or not estimate their absolute attitude.

Role of the light source position in freely falling hoverflies' stabilization performances.

The stabilization of plummeting hoverflies was filmed and analysed in terms of their wingbeat initiation times as well as the crash and stabilization rates. The flies experienced near-weightlessness for a period of time that depended on their ability to counteract the free fall by triggering their wingbeats. In this paradigm, hoverflies' flight stabilization strategies were investigated here for the first time under two different positions of the light source (overhead and bottom lighting). The crash rates were higher in bottom lighting conditions than with top lighting. In addition, adding a texture to the walls reduced the crash rates only in the overhead lighting condition. The position of the lighting also significantly affected both the stabilization rates and the time taken by the flies to stabilize, which decreased and increased under bottom lighting conditions, respectively, whereas textured walls increased the stabilization rates under both lighting conditions. These results support the idea that flies may mainly base their flight control strategy on visual cues and particularly that the light distribution in the visual field may provide reliable, efficient cues for estimating their orientation with respect to an allocentric reference frame. In addition, the finding that the hoverflies' optic flow-based motion detection ability is affected by the position of the light source in their visual field suggests the occurrence of interactions between movement perception and this visual vertical perception process.

To crash or not to crash: how do hoverflies cope with free-fall situations and weightlessness?

Insects' aptitude to perform hovering, automatic landing and tracking tasks involves accurately controlling their head and body roll and pitch movements, but how this attitude control depends on an internal estimation of gravity orientation is still an open question. Gravity perception in flying insects has mainly been studied in terms of grounded animals' tactile orientation responses, but it has not yet been established whether hoverflies use gravity perception cues to detect a nearly weightless state at an early stage. Ground-based microgravity simulators provide biologists with useful tools for studying the effects of changes in gravity. However, in view of the cost and the complexity of these set-ups, an alternative Earth-based free-fall procedure was developed with which flying insects can be briefly exposed to microgravity under various visual conditions. Hoverflies frequently initiated wingbeats in response to an imposed free fall in all the conditions tested, but managed to avoid crashing only in variably structured visual environments, and only episodically in darkness. Our results reveal that the crash-avoidance performance of these insects in various visual environments suggests the existence of a multisensory control system based mainly on vision rather than gravity perception.

Behavioural evidence for a visual and proprioceptive control of head roll in hoverflies (Episyrphus balteatus).

The ability of hoverflies to control their head orientation with respect to their body contributes importantly to their agility and their autonomous navigation abilities. Many tasks performed by this insect during flight, especially while hovering, involve a head stabilization reflex. This reflex, which is mediated by multisensory channels, prevents the visual processing from being disturbed by motion blur and maintains a consistent perception of the visual environment. The so-called dorsal light response (DLR) is another head control reflex, which makes insects sensitive to the brightest part of the visual field. In this study, we experimentally validate and quantify the control loop driving the head roll with respect to the horizon in hoverflies. The new approach developed here consisted of using an upside-down horizon in a body roll paradigm. In this unusual configuration, tethered flying hoverflies surprisingly no longer use purely vision-based control for head stabilization. These results shed new light on the role of neck proprioceptor organs in head and body stabilization with respect to the horizon. Based on the responses obtained with male and female hoverflies, an improved model was then developed in which the output signals delivered by the neck proprioceptor organs are combined with the visual error in the estimated position of the body roll. An internal estimation of the body roll angle with respect to the horizon might explain the extremely accurate flight performances achieved by some hovering insects.

Mushroom Bodies Are Required for Learned Visual Navigation, but Not for Innate Visual Behavior, in Ants.

Visual navigation in ants has long been a focus of experimental study [1-3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MBs) may be the substrate for visual memory in navigation tasks [5-7], while computational modeling shows that MB neural architecture could support this function [8, 9]. There is, however, no direct evidence that ants require MBs for visual navigation. Here we show that lesions of MB calyces impair ants' visual navigation to a remembered food location yet leave their innate responses to visual cues unaffected. Wood ants are innately attracted to large visual cues, but we trained them to locate a food source at a specific angle away from such a cue. Subsequent lesioning of the MB calyces using procaine hydrochloride injection caused ants to revert toward their innate cue attraction. Handling and saline injection control ants still approached the feeder. Path straightness of lesioned and control ants did not differ from each other but was lower than during training. Reversion toward the cue direction occurred irrespective of whether the visual cue was ipsi- or contralateral to the lesion site, showing this is not due simply to an induced motor bias. Monocular occlusion did not diminish ants' ability to locate the feeder, suggesting that MB lesions are not merely interrupting visual input to the calyx. The demonstrated dissociation between innate and learned visual responses provides direct evidence for a specific role of the MB in navigational memory.