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.

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.

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.

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.

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.

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.

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.

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.

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.

How do field of view and resolution affect the information content of panoramic scenes for visual navigation? A computational investigation.

The visual systems of animals have to provide information to guide behaviour and the informational requirements of an animal's behavioural repertoire are often reflected in its sensory system. For insects, this is often evident in the optical array of the compound eye. One behaviour that insects share with many animals is the use of learnt visual information for navigation. As ants are expert visual navigators it may be that their vision is optimised for navigation. Here we take a computational approach in asking how the details of the optical array influence the informational content of scenes used in simple view matching strategies for orientation. We find that robust orientation is best achieved with low-resolution visual information and a large field of view, similar to the optical properties seen for many ant species. A lower resolution allows for a trade-off between specificity and generalisation for stored views. Additionally, our simulations show that orientation performance increases if different portions of the visual field are considered as discrete visual sensors, each giving an independent directional estimate. This suggests that ants might benefit by processing information from their two eyes independently.

Optimal cue integration in ants.

In situations with redundant or competing sensory information, humans have been shown to perform cue integration, weighting different cues according to their certainty in a quantifiably optimal manner. Ants have been shown to merge the directional information available from their path integration (PI) and visual memory, but as yet it is not clear that they do so in a way that reflects the relative certainty of the cues. In this study, we manipulate the variance of the PI home vector by allowing ants (Cataglyphis velox) to run different distances and testing their directional choice when the PI vector direction is put in competition with visual memory. Ants show progressively stronger weighting of their PI direction as PI length increases. The weighting is quantitatively predicted by modelling the expected directional variance of home vectors of different lengths and assuming optimal cue integration. However, a subsequent experiment suggests ants may not actually compute an internal estimate of the PI certainty, but are using the PI home vector length as a proxy.

How variation in head pitch could affect image matching algorithms for ant navigation.

Desert ants are a model system for animal navigation, using visual memory to follow long routes across both sparse and cluttered environments. Most accounts of this behaviour assume retinotopic image matching, e.g. recovering heading direction by finding a minimum in the image difference function as the viewpoint rotates. But most models neglect the potential image distortion that could result from unstable head motion. We report that for ants running across a short section of natural substrate, the head pitch varies substantially: by over 20 degrees with no load; and 60 degrees when carrying a large food item. There is no evidence of head stabilisation. Using a realistic simulation of the ant's visual world, we demonstrate that this range of head pitch significantly degrades image matching. The effect of pitch variation can be ameliorated by a memory bank of densely sampled along a route so that an image sufficiently similar in pitch and location is available for comparison. However, with large pitch disturbance, inappropriate memories sampled at distant locations are often recalled and navigation along a route can be adversely affected. Ignoring images obtained at extreme pitches, or averaging images over several pitches, does not significantly improve performance.

Multiple sources of celestial compass information in the Central Australian desert ant Melophorus bagoti.

The Central Australian desert ant Melophorus bagoti is known to use celestial cues for compass orientation. We manipulated the available celestial cues for compass orientation for ants that had arrived at a feeder, were captured and then released at a distant test site that had no useful terrestrial panoramic cues. When tested in an enclosed transparent box that blocked some or most of the ultraviolet light, the ants were still well oriented homewards. The ants were again significantly oriented homewards when most of the ultraviolet light as well as the sun was blocked, or when the box was covered with tracing paper that eliminated the pattern of polarised light, although in the latter case, their headings were more scattered than in control (full-cue) conditions. When the position of the sun was reflected 180° by a mirror, the ants headed off in an intermediate direction between the dictates of the sun and the dictates of unrotated cues. We conclude that M. bagoti uses all available celestial compass cues, including the pattern of polarised light, the position of the sun, and spectral and intensity gradients. They average multiple cues in a weighted fashion when these cues conflict.

Visual scanning behaviours and their role in the navigation of the Australian desert ant Melophorus bagoti.

Ants are excellent navigators, using a combination of innate strategies and learnt information to guide habitual routes. The mechanisms underlying this behaviour are little understood though one avenue of investigation is to explore how innate sensori-motor routines are used to accomplish route navigation. For instance, Australian desert ant foragers are occasionally observed to cease translation and rotate on the spot. Here, we investigate this behaviour using high-speed videography and computational analysis. We find that scanning behaviour is saccadic with pauses separated by fast rotations. Further, we have identified four situations where scanning is typically displayed: (1) by naïve ants on their first departure from the nest; (2) by experienced ants departing from the nest for their first foraging trip of the day; (3) by experienced ants when the familiar visual surround was experimentally modified, in which case frequency and duration of scans were proportional to the degree of modification; (4) when the information from visual cues is at odds with the direction indicated by the ant's path integration system. Taken together, we see a general relationship between scanning behaviours and periods of uncertainty.

Combining sky and earth: desert ants (Melophorus bagoti) show weighted integration of celestial and terrestrial cues.

Insects typically use celestial sources of directional information for path integration, and terrestrial panoramic information for view-based navigation. Here we set celestial and terrestrial sources of directional information in conflict for homing desert ants (Melophorus bagoti). In the first experiment, ants learned to navigate out of a round experimental arena with a distinctive artificial panorama. On crucial tests, we rotated the arena to create a conflict between the artificial panorama and celestial information. In a second experiment, ants at a feeder in their natural visually-cluttered habitat were displaced prior to their homing journey so that the dictates of path integration (feeder to nest direction) based on a celestial compass conflicted with the dictates of view-based navigation (release point to nest direction) based on the natural terrestrial panorama. In both experiments, ants generally headed in a direction intermediate to the dictates of celestial and terrestrial information. In the second experiment, the ants put more weight on the terrestrial cues when they provided better directional information. We conclude that desert ants weight and integrate the dictates of celestial and terrestrial information in determining their initial heading, even when the two directional cues are highly discrepant.

Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit.

Ants use multiple sources of information to navigate, but do not integrate all this information into a unified representation of the world. Rather, the available information appears to serve three distinct main navigational systems: path integration, systematic search and the use of learnt information--mainly via vision. Here, we report on an additional behaviour that suggests a supplemental system in the ant's navigational toolkit: 'backtracking'. Homing ants, having almost reached their nest but, suddenly displaced to unfamiliar areas, did not show the characteristic undirected headings of systematic searches. Instead, these ants backtracked in the compass direction opposite to the path that they had just travelled. The ecological function of this behaviour is clear as we show it increases the chances of returning to familiar terrain. Importantly, the mechanistic implications of this behaviour stress an extra level of cognitive complexity in ant navigation. Our results imply: (i) the presence of a type of 'memory of the current trip' allowing lost ants to take into account the familiar view recently experienced, and (ii) direct sharing of information across different navigational systems. We propose a revised architecture of the ant's navigational toolkit illustrating how the different systems may interact to produce adaptive behaviours.

Snapshots in ants? New interpretations of paradigmatic experiments.

Ants can use visual information to guide long idiosyncratic routes and accurately pinpoint locations in complex natural environments. It has often been assumed that the world knowledge of these foragers consists of multiple discrete views that are retrieved sequentially for breaking routes into sections controlling approaches to a goal. Here we challenge this idea using a model of visual navigation that does not store and use discrete views to replicate the results from paradigmatic experiments that have been taken as evidence that ants navigate using such discrete snapshots. Instead of sequentially retrieving views, the proposed architecture gathers information from all experienced views into a single memory network, and uses this network all along the route to determine the most familiar heading at a given location. This algorithm is consistent with the navigation of ants in both laboratory and natural environments, and provides a parsimonious solution to deal with visual information from multiple locations.

Information content of visual scenes influences systematic search of desert ants.

Many animals - including insects - navigate visually through their environment. Solitary foraging desert ants are known to acquire visual information from the surrounding panorama and use it to navigate along habitual routes or to pinpoint a goal such as the nest. Returning foragers that fail to find the nest entrance engage in searching behaviour, during which they continue to use vision. The characteristics of searching behaviour have typically been investigated in unfamiliar environments. Here we investigated in detail the nest-searching behaviour of Melophorus bagoti foragers within the familiar visual environment of their nest. First, by relating search behaviour to the information content of panoramic (360 deg) images, we found that searches were more accurate in visually cluttered environments. Second, as observed in unfamiliar visual surrounds, searches were dynamic and gradually expanded with time, showing that nest pinpointing is not rigidly controlled by vision. Third, contrary to searches displayed in unfamiliar environments, searches observed here could be modelled as a single exponential search strategy, which is similar to a Brownian walk, and there was no evidence of a Lévy walk. Overall, our results revealed that searching behaviour is remarkably flexible and varies according to the relevance of information provided by the surrounding visual scenery.

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.

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.