Landmarks, beacons, or panoramic views: What do pigeons attend to for guidance in familiar environments?

Birds and social insects represent excellent systems for understanding visually guided navigation. Both animal groups use surrounding visual cues for homing and foraging. Ants extract sufficient spatial information from panoramic views, which naturally embed all near and far spatial information, for successful homing. Although egocentric panoramic views allow for parsimonious explanations of navigational behaviors, this potential source of spatial information has been mostly neglected during studies of vertebrates. Here we investigate how distinct landmarks, a beacon, and panoramic views influence the reorientation behavior in pigeons (Columba livia). Pigeons were trained to search for a location characterized by a beacon and several distinct landmarks. Transformation tests manipulated aspects of the landmark configuration, allowing for a dissociation among navigational strategies. Quantitative image and path analyses provided support that the panoramic view was used by the pigeons. Although the results from some individuals support the use of beaconing, overall the pigeons relied predominantly on the panoramic view when spatial cues provided conflicting information regarding the goal location. Reorientation based on vector and bearing information derived from distinct landmarks as well as environmental geometry failed to account fully for the results. Thus, the results of our study support that pigeons can use panoramic views for reorientation in familiar environments. Given that the current model for landmark use by pigeons posits the use of different vectors from an object, a global panorama-matching strategy suggests a fundamental change in the theory of how pigeons use surrounding visual cues for localization.

CATER: Combined Animal Tracking & Environment Reconstruction.

Quantifying the behavior of small animals traversing long distances in complex environments is one of the most difficult tracking scenarios for computer vision. Tiny and low-contrast foreground objects have to be localized in cluttered and dynamic scenes as well as trajectories compensated for camera motion and drift in multiple lengthy recordings. We introduce CATER, a novel methodology combining an unsupervised probabilistic detection mechanism with a globally optimized environment reconstruction pipeline enabling precision behavioral quantification in natural environments. Implemented as an easy to use and highly parallelized tool, we show its application to recover fine-scale motion trajectories, registered to a high-resolution image mosaic reconstruction, of naturally foraging desert ants from unconstrained field recordings. By bridging the gap between laboratory and field experiments, we gain previously unknown insights into ant navigation with respect to motivational states, previous experience, and current environments and provide an appearance-agnostic method applicable to study the behavior of a wide range of terrestrial species under realistic conditions.

Scanning behaviour in ants: an interplay between random-rate processes and oscillators.

At the start of a journey home or to a foraging site, ants often stop, interrupting their forward movement, turn on the spot a number of times, and fixate in different directions. These scanning bouts are thought to provide visual information for choosing a path to travel. The temporal organization of such scanning bouts has implications about the neural organisation of navigational behaviour. We examined (1) the temporal distribution of the start of such scanning bouts and (2) the dynamics of saccadic body turns and fixations that compose a scanning bout in Australian desert ants, Melophorus bagoti, as they came out of a walled channel onto open field at the start of their homeward journey. Ants were caught when they neared their nest and displaced to different locations to start their journey home again. The observed parameters were mostly similar across familiar and unfamiliar locations. The turning angles of saccadic body turning to the right or left showed some stereotypy, with a peak just under 45°. The direction of such saccades appears to be determined by a slow oscillatory process as described in other insect species. In timing, however, both the distribution of inter-scanning-bout intervals and individual fixation durations showed exponential characteristics, the signature for a random-rate or Poisson process. Neurobiologically, therefore, there must be some process that switches behaviour (starting a scanning bout or ending a fixation) with equal probability at every moment in time. We discuss how chance events in the ant brain that occasionally reach a threshold for triggering such behaviours can generate the results.

An intrinsic oscillator underlies visual navigation in ants.

Many insects display lateral oscillations while moving, but how these oscillations are produced and participate in visual navigation remains unclear. Here, we show that visually navigating ants continuously display regular lateral oscillations coupled with variations of forward speed that strongly optimize the distance covered while simultaneously enabling them to scan left and right directions. This pattern of movement is produced endogenously and conserved across navigational contexts in two phylogenetically distant ant species. Moreover, the oscillations' amplitude can be modulated by both innate or learnt visual cues to adjust the exploration/exploitation balance to the current need. This lower-level motor pattern thus drastically reduces the degree of freedom needed for higher-level strategies to control behavior. The observed dynamical signature readily emerges from a simple neural circuit model of the insect's conserved pre-motor area known as the lateral accessory lobe, offering a surprisingly simple but effective neural control and endorsing oscillation as a core, ancestral way of moving in insects.

Insect navigation: Bumblebees walk the walk.

A new study shows that bumblebees can display path integration while walking in a small laboratory arena. This opens a new avenue for studying how insects' brains can encode direction and distance.

Aversive view memories and risk perception in navigating ants.

Many ants establish foraging routes through learning views of the visual panorama. Route models have focused primarily on attractive view use, which experienced foragers orient towards to return to known sites. However, aversive views have recently been uncovered as a key component of route learning. Here, Cataglyphis velox rapidly learned aversive views, when associated with a negative outcome, a period of captivity in vegetation, triggering increases in hesitation behavior. These memories were based on the accumulation of experiences over multiple trips with each new experience regulating forager hesitancy. Foragers were also sensitive to captivity time differences, suggesting they possess some mechanism to quantify duration. Finally, we analyzed foragers' perception of risky (i.e. variable) versus stable aversive outcomes by associating two sites along the route with distinct captivity schedules, a fixed or variable duration, with the same mean across training. Foragers exhibited fewer hesitations in response to risky outcomes compared to fixed ones, indicating they perceived risky outcomes as less severe. Results align with a logarithmic relationship between captivity duration and hesitations, suggesting that aversive stimulus perception is a logarithm of its actual value. We discuss how aversive view learning could be executed within the mushroom bodies circuitry following a prediction error rule.

Movements, embodiment and the emergence of decisions. Insights from insect navigation.

We readily infer that animals make decisions, but what this implies is usually not clearly defined. The notion of 'decision-making' ultimately stems from human introspection, and is thus loaded with anthropomorphic assumptions. Notably, the decision is made internally, is based on information, and precedes the goal directed behaviour. Also, making a decision implies that 'something' did it, thus hints at the presence of a cognitive mind, whose existence is independent of the decision itself. This view may convey some truth, but here I take the opposite stance. Using examples from research in insect navigation, this essay highlights how apparent decisions can emerge without a brain, how actions can precede information or how sophisticated goal directed behaviours can be implemented without neural decisions. This perspective requires us to shake off the idea that behaviour is a consequence of the brain; and embrace the concept that movements arise from - as much as participate in - distributed interactions between various computational centres - including the body - that reverberate in closed-loop with the environment. From this perspective we may start to picture how a cognitive mind can be the consequence, rather than the cause, of such neural and body movements.

Fruit flies can learn non-elemental olfactory discriminations.

Associative learning allows animals to establish links between stimuli based on their concomitance. In the case of Pavlovian conditioning, a single stimulus A (the conditional stimulus, CS) is reinforced unambiguously with an unconditional stimulus (US) eliciting an innate response. This conditioning constitutes an 'elemental' association to elicit a learnt response from A+ without US presentation after learning. However, associative learning may involve a 'complex' CS composed of several components. In that case, the compound may predict a different outcome than the components taken separately, leading to ambiguity and requiring the animal to perform so-called non-elemental discrimination. Here, we focus on such a non-elemental task, the negative patterning (NP) problem, and provide the first evidence of NP solving in Drosophila. We show that Drosophila learn to discriminate a simple component (A or B) associated with electric shocks (+) from an odour mixture composed either partly (called 'feature-negative discrimination' A+ versus AB-) or entirely (called 'NP' A+B+ versus AB-) of the shock-associated components. Furthermore, we show that conditioning repetition results in a transition from an elemental to a configural representation of the mixture required to solve the NP task, highlighting the cognitive flexibility of Drosophila.

Towards a multi-level understanding in insect navigation.

To understand the brain is to understand behaviour. However, understanding behaviour itself requires consideration of sensory information, body movements and the animal's ecology. Therefore, understanding the link between neurons and behaviour is a multi-level problem, which can be achieved when considering Marr's three levels of understanding: behaviour, computation, and neural implementation. Rather than establishing direct links between neurons and behaviour, the matter boils down to understanding two transitions: the link between neurons and brain computation on one hand, and the link between brain computations and behaviour on the other hand. The field of insect navigation illustrates well the power of such two-sided endeavour. We provide here examples revealing that each transition requires its own approach with its own intrinsic difficulties, and show how modelling can help us reach the desired multi-level understanding.

Intrinsic control of muscle attachment sites matching.

Myogenesis is an evolutionarily conserved process. Little known, however, is how the morphology of each muscle is determined, such that movements relying upon contraction of many muscles are both precise and coordinated. Each Drosophila larval muscle is a single multinucleated fibre whose morphology reflects expression of distinctive identity Transcription Factors (iTFs). By deleting transcription cis-regulatory modules of one iTF, Collier, we generated viable muscle identity mutants, allowing live imaging and locomotion assays. We show that both selection of muscle attachment sites and muscle/muscle matching is intrinsic to muscle identity and requires transcriptional reprogramming of syncytial nuclei. Live-imaging shows that the staggered muscle pattern involves attraction to tendon cells and heterotypic muscle-muscle adhesion. Unbalance leads to formation of branched muscles, and this correlates with locomotor behavior deficit. Thus, engineering Drosophila muscle identity mutants allows to investigate, in vivo, physiological and mechanical properties of abnormal muscles.

Each muscle in the body has a unique size, shape and set of attachment points. Animals need all of their muscles to have the correct identity to help maintain posture and control movement. A specific set of proteins, called transcription factors, co-ordinate and regulate gene activity in cells so that each muscle develops in the right way. To create a muscle, multiple precursor cells fuse together to form a muscle fibre, which then elongates and attaches to specific sites. Correct attachment is critical so that the fibre is properly oriented. When this process goes wrong, for example in disease, muscle fibres sometimes attach to the wrong site; they become branched and cannot work properly. Collier is a transcription factor protein that controls muscle identity in the fruit fly Drosophila melanogaster. However, like many transcription factors, Collier also has several other roles throughout the body. This made it difficult to evaluate the effect of the protein on the formation of specific muscles. Here, Carayon et al. managed to selectively deactivate Collier in just one muscle per body section in the larvae of fruit flies. This showed that the transcription factor is needed throughout muscle development; in particular, it is required for muscle fibres to select the correct attachment sites, and to be properly oriented. Affected muscles showed an altered orientation, with branched fibres attaching to the wrong site. Even minor changes, which only affect a single muscle from each body segment, greatly impaired the movement of the larvae. The work by Carayon et al. offers a new approach to the study of muscular conditions. Branched muscles are seen in severe human illnesses such as Duchenne muscular dystrophy. Studying the impact of these changes in a living animal could help to understand how this disease progress, and how it can be prevented.

Route-following ants respond to alterations of the view sequence.

Ants can navigate by comparing the currently perceived view with memorised views along a familiar foraging route. Models regarding route-following suggest that the views are stored and recalled independently of the sequence in which they occur. Hence, the ant only needs to evaluate the instantaneous familiarity of the current view to obtain a heading direction. This study investigates whether ant homing behaviour is influenced by alterations in the sequence of views experienced along a familiar route, using the frequency of stop-and-scan behaviour as an indicator of the ant's navigational uncertainty. Ants were trained to forage between their nest and a feeder which they exited through a short channel before proceeding along the homeward route. In tests, ants were collected before entering the nest and released again in the channel, which was placed either in its original location or halfway along the route. Ants exiting the familiar channel in the middle of the route would thus experience familiar views in a novel sequence. Results show that ants exiting the channel scan significantly more when they find themselves in the middle of the route, compared with when emerging at the expected location near the feeder. This behaviour suggests that previously encountered views influence the recognition of current views, even when these views are highly familiar, revealing a sequence component to route memory. How information about view sequences could be implemented in the insect brain, as well as potential alternative explanations to our results, are discussed.

Rapid Aversive and Memory Trace Learning during Route Navigation in Desert Ants.

The ability of bees and ants to learn long visually guided routes in complex environments is perhaps one of the most spectacular pieces of evidence for the impressive power of their small brains. Whereas flying bees can visit flowers in an optimized sequence over kilometers, walking solitary foraging ants can precisely recapitulate routes of up to 100 m in complex environments [1]. It is clear that route following depends largely on learned visual information and we have a good idea of how visual memories can guide individuals along them [2-6], as well as how this is implemented in the insect brain [7, 8]. However, little is known about the mechanisms that control route learning and development. Here we show that ants (Melophorus bagoti and Cataglyphis fortis) navigating in their natural environments can actively learn a route detour to avoid a pit trap. This adaptive flexibility depends on a mechanism of aversive learning based on memory traces of recently encountered stimuli, reflecting the laboratory paradigm of trace conditioning. The views experienced before falling into the trap become associated with the ensuing negative outcome and thus trigger salutary turns on the subsequent trip. This drives the ants to orient away from the goal direction and avoid the trap. If the pit trap is avoided, the novel views experienced during the detour become positively reinforced and the new route crystallizes. We discuss how such an interplay between appetitive and aversive memories might be implemented in insect neural circuitry.

Opponent processes in visual memories: A model of attraction and repulsion in navigating insects' mushroom bodies.

Solitary foraging insects display stunning navigational behaviours in visually complex natural environments. Current literature assumes that these insects are mostly driven by attractive visual memories, which are learnt when the insect's gaze is precisely oriented toward the goal direction, typically along its familiar route or towards its nest. That way, an insect could return home by simply moving in the direction that appears most familiar. Here we show using virtual reconstructions of natural environments that this principle suffers from fundamental drawbacks, notably, a given view of the world does not provide information about whether the agent should turn or not to reach its goal. We propose a simple model where the agent continuously compares its current view with both goal and anti-goal visual memories, which are treated as attractive and repulsive respectively. We show that this strategy effectively results in an opponent process, albeit not at the perceptual level-such as those proposed for colour vision or polarisation detection-but at the level of the environmental space. This opponent process results in a signal that strongly correlates with the angular error of the current body orientation so that a single view of the world now suffices to indicate whether the agent should turn or not. By incorporating this principle into a simple agent navigating in reconstructed natural environments, we show that it overcomes the usual shortcomings and produces a step-increase in navigation effectiveness and robustness. Our findings provide a functional explanation to recent behavioural observations in ants and why and how so-called aversive and appetitive memories must be combined. We propose a likely neural implementation based on insects' mushroom bodies' circuitry that produces behavioural and neural predictions contrasting with previous models.

The role of attractive and repellent scene memories in ant homing (Myrmecia croslandi).

Solitary foraging ants rely on vision when travelling along routes and when pinpointing their nest. We tethered foragers of Myrmecia croslandi on a trackball and recorded their intended movements when the trackball was located on their normal foraging corridor (on-route), above their nest and at a location several metres away where they have never been before (off-route). We found that at on- and off-route locations, most ants walk in the nest or foraging direction and continue to do so for tens of metres in a straight line. In contrast, above the nest, ants walk in random directions and change walking direction frequently. In addition, the walking direction of ants above the nest oscillates on a fine scale, reflecting search movements that are absent from the paths of ants at the other locations. An agent-based simulation shows that the behaviour of ants at all three locations can be explained by the integration of attractive and repellent views directed towards or away from the nest, respectively. Ants are likely to acquire such views via systematic scanning movements during their learning walks. The model predicts that ants placed in a completely unfamiliar environment should behave as if at the nest, which our subsequent experiments confirmed. We conclude first, that the ants' behaviour at release sites is exclusively driven by what they currently see and not by information on expected outcomes of their behaviour; and second, that navigating ants might continuously integrate attractive and repellent visual memories. We discuss the benefits of such a procedure.

The Central Complex as a Potential Substrate for Vector Based Navigation.

Insects use path integration (PI) to maintain a home vector, but can also store and recall vector-memories that take them from home to a food location, and even allow them to take novel shortcuts between food locations. The neural circuit of the Central Complex (a brain area that receives compass and optic flow information) forms a plausible substrate for these behaviors. A recent model, grounded in neurophysiological and neuroanatomical data, can account for PI during outbound exploratory routes and the control of steering to return home. Here, we show that minor, hypothetical but neurally plausible, extensions of this model can additionally explain how insects could store and recall PI vectors to follow food-ward paths, take shortcuts, search at the feeder and re-calibrate their vector-memories with experience. In addition, a simple assumption about how one of multiple vector-memories might be chosen at any point in time can produce the development and maintenance of efficient routes between multiple locations, as observed in bees. The central complex circuitry is therefore well-suited to allow for a rich vector-based navigational repertoire.

Running paths to nowhere: repetition of routes shows how navigating ants modulate online the weights accorded to cues.

Ants are expert navigators, keeping track of the vector to home as they travel, through path integration, and using terrestrial panoramas in view-based navigation. Although insect learning has been much studied, the learning processes in navigation have not received much attention. Here, we investigate in desert ants (Melophorus bagoti) the effects of repeating a well-travelled and familiar route segment without success. We find that re-running a homeward route without entering the nest impacted subsequent trips. Over trips, ants showed more meandering from side to side and more scanning behaviour, in which the ant stopped and turned, rotating to a range of directions. In repeatedly re-running their familiar route, ants eventually gave up heading in the nestward direction as defined by visual cues and turned to walk in the opposite direction. Further manipulations showed that the extent and rate of this path degradation depend on (1) the length of the vector accumulated in the direction opposite to the food-to-nest direction, (2) the specific visual experience of the repeated segment of the route that the ants were forced to re-run, and (3) the visual panorama: paths are more degraded in an open panorama, compared with a visually cluttered scene. The results show that ants dynamically modulate the weighting given to route memories, and that fits well with the recent models, suggesting that the mushroom bodies provide a substrate for the reinforcement learning of views for navigation.

Rotation invariant visual processing for spatial memory in insects.

Visual memory is crucial to navigation in many animals, including insects. Here, we focus on the problem of visual homing, that is, using comparison of the view at a current location with a view stored at the home location to control movement towards home by a novel shortcut. Insects show several visual specializations that appear advantageous for this task, including almost panoramic field of view and ultraviolet light sensitivity, which enhances the salience of the skyline. We discuss several proposals for subsequent processing of the image to obtain the required motion information, focusing on how each might deal with the problem of yaw rotation of the current view relative to the home view. Possible solutions include tagging of views with information from the celestial compass system, using multiple views pointing towards home, or rotation invariant encoding of the view. We illustrate briefly how a well-known shape description method from computer vision, Zernike moments, could provide a compact and rotation invariant representation of sky shapes to enhance visual homing. We discuss the biological plausibility of this solution, and also a fourth strategy, based on observed behaviour of insects, that involves transfer of information from visual memory matching to the compass system.

Ants' navigation in an unfamiliar environment is influenced by their experience of a familiar route.

When displaced experimentally from a food source (feeder) to unfamiliar terrain, ants run off a portion of the homeward vector or its entirety, depending on species and conditions, and then search systematically, turning in loops of ever increasing size. The Australian desert ant Melophorus bagoti runs off a smaller portion of its vector if the test site is more dissimilar to its nest area. Here we manipulated familiarity with the training route between a feeder and the ants' nest to examine its effects when the ants were displaced to a distant site from the feeder. Naïve ants that arrived at an experimentally provided feeder for the first time were compared with experienced ants that had travelled the route for two days. At the unfamiliar test site, naïve ants ran off a longer portion of their vector from path integration than did experienced ants. Naïve ants also spread out in their systematic search slower than did experienced ants. We conclude that as ants learn the views encountered on their familiar route better, they identify more readily unfamiliar views. A scene distant from their nest area may not look as unfamiliar to a naïve ant as it does to an experienced ant.

Neural coding in the visual system of Drosophila melanogaster: How do small neural populations support visually guided behaviours?

All organisms wishing to survive and reproduce must be able to respond adaptively to a complex, changing world. Yet the computational power available is constrained by biology and evolution, favouring mechanisms that are parsimonious yet robust. Here we investigate the information carried in small populations of visually responsive neurons in Drosophila melanogaster. These so-called 'ring neurons', projecting to the ellipsoid body of the central complex, are reported to be necessary for complex visual tasks such as pattern recognition and visual navigation. Recently the receptive fields of these neurons have been mapped, allowing us to investigate how well they can support such behaviours. For instance, in a simulation of classic pattern discrimination experiments, we show that the pattern of output from the ring neurons matches observed fly behaviour. However, performance of the neurons (as with flies) is not perfect and can be easily improved with the addition of extra neurons, suggesting the neurons' receptive fields are not optimised for recognising abstract shapes, a conclusion which casts doubt on cognitive explanations of fly behaviour in pattern recognition assays. Using artificial neural networks, we then assess how easy it is to decode more general information about stimulus shape from the ring neuron population codes. We show that these neurons are well suited for encoding information about size, position and orientation, which are more relevant behavioural parameters for a fly than abstract pattern properties. This leads us to suggest that in order to understand the properties of neural systems, one must consider how perceptual circuits put information at the service of behaviour.