Guidance by odors in honeybee navigation

Animal navigation is guided by multiple sensory cues. Here, we ask whether and how olfactory stimuli emanating from places other than the trained feeding site redirect the flight paths of honeybees. The flight trajectories of individual bees were registered using harmonic radar tracking. Sensory cues (compass direction, distance, visual cues en route and close to the feeding site) associated with the trained flight route dominated wayfinding, but a learned odorant carried by air flow induced excursions into the wind. These redirections were largely restricted to rather small deviations from the trained route (<60°, <200 m) and occurred only if the animal did not receive the trained odorant stimulus at the trained feeding site. Under certain conditions, larger excursions were observed. These findings are discussed in the context of odor guidance of honeybees over longer distances (>300 m from the hive).     

The retrieval of visuo-spatial memories by honeybees

Summary In order to explore how honeybees manage to retrieve the right landmark-memory in the right place, we trained bees along a short foraging route which consisted of two identical huts 33 m apart. Bees entered each hut to collect a drop of sucrose on the floor. The location of the drop was defined by the same arrangement of four blue and yellow cylindrical landmarks. However, in one hut the drop was between two yellow cylinders and in two other it was to the east of the blue cylinders. On tests with the sucrose missing, bees tended to search in the appropriate area in each hut (Fig. 1), thus showing that they used cues other than the sight of the local landmarks to select the appropriate memory.In a second experiment, the position of the sucrose was specified by yellow cylinders in one hut and by blue triangles in the other. When the arrays were swapped between huts, bees searched in the position specified by the array they encountered (Fig. 2). Thus, memories can be triggered by visual features of local landmarks.Bees were also trained outside to collect food from two platforms 40 m apart. The location of sucrose on one platform was defined by yellow cylinders, and on the other it was defined by blue triangles. When these arrays were exchanged between platforms, bees searched on each platform as though the landmarks had not been swapped. It seems that the more distant surroundings, which fill most of the visual field, may be more potent than the local landmarks in deciding which memory should be retrieved.It is argued that one role of distant landmarks and other contextual cues is to ensure that bees retrieve the correct memory of a constellation of local landmarks while the bees are still some distance away from their goal. Even at a short distance, a bee's current image of local landmarks may differ considerably from its stored representation of those landmarks as seen from the goal. Accurate recall of the appropriate memory will be more certain if it is primed by relatively distant landmarks which present a more constant image as a bee moves in the vicinity of its goal.     

Memory and sun compensation by honey bees

Summary Experiments with two species of honey bees (Apis mellifera andA. cerana) have revealed that bees form a detailed memory of the spatial and temporal pattern of the sun's azimuthal movement, using local landmarks as a reference for the learning. These experiments were performed on overcast days, and consisted of removing a hive from one site in which bees had been trained to find food by flying along a prominent landmark, and displacing it to a similar site in which the landmark was aligned in a different compass direction. On overcast days, bees which flew along the landmark in the new site oriented their waggle dances in the hive as if they had actually flown in the training site. Thus, they confused the two sets of landmarks and set their dance angles according to a memory of the sun's position relative to the original landmarks. Furthermore, the dances changed in correspondence with the sun's azimuthal shift over several hours, even reflecting (approximately) the regular temporal variations in the rate of shift; such features of the sun's course must therefore be stored in memory. The primary mechanism underlying the learning of this pattern is probably similar to that proposed by New and New (1962): bees store in memory several time-linked solar azimuthal positions relative to features of the landscape, and refer to this stored array when they need to determine an unknown azimuth intermediate between two known positions.During the cloudy-day displacement experiments, celestial cues often appeared to bees in the new site, contradicting the stored information on which they had been basing their dances. Although most bees quickly adopted the dance angle reflecting their actual direction of flight relative to the sun, some later reverted to the original dance angle, indicating that the information on which it was based had remained in memory when the new information was being expressed; other bees performed bimodal dances which expressed both sets of information in alternate waggle runs. The separation in memory implied by these behaviors may reflect a neural strategy for updating a previously stored relationship between celestial and terrestrial references with new information presented by seasonal changes in the sun's course or by newly learned landmarks.     

Das Landschaftsgedächtnis der Bienen. Kleine Gehirne – überraschendes Orientierungsvermögen

We have used a new device, the harmonic radar, to monitor continously the flight paths of bees. Bees are well oriented within the area they have explored during their orientation flights. Bees transported and released at an unexpected site within this area are not lost but fly back to the hive on direct routes after a short search phase. Bees that have been trained to a feeding place may fly first to the feeding place and then back to the hive indicating that they are able to decide between two destinations for their fast return flights. Since bees could not use a beacon at the indicated goals or the structure of the horizon we conclude that their navigation memory is organized according to a geometric map.     

Daytime Sleep Enhances Consolidation of the Spatial but Not Motoric Representation of Motor Sequence Memory

Motor sequence learning is known to rely on more than a single process. As the skill develops with practice, two different representations of the sequence are formed: a goal representation built under spatial allocentric coordinates and a movement representation mediated through egocentric motor coordinates. This study aimed to explore the influence of daytime sleep (nap) on consolidation of these two representations. Through the manipulation of an explicit finger sequence learning task and a transfer protocol, we show that both allocentric (spatial) and egocentric (motor) representations of the sequence can be isolated after initial training. Our results also demonstrate that nap favors the emergence of offline gains in performance for the allocentric, but not the egocentric representation, even after accounting for fatigue effects. Furthermore, sleep-dependent gains in performance observed for the allocentric representation are correlated with spindle density during non-rapid eye movement (NREM) sleep of the post-training nap. In contrast, performance on the egocentric representation is only maintained, but not improved, regardless of the sleep/wake condition. These results suggest that motor sequence memory acquisition and consolidation involve distinct mechanisms that rely on sleep (and specifically, spindle) or simple passage of time, depending respectively on whether the sequence is performed under allocentric or egocentric coordinates.     

When do objects become landmarks? A VR study of the effect of task relevance on spatial memory

We investigated how objects come to serve as landmarks in spatial memory, and more specifically how they form part of an allocentric cognitive map. Participants performing a virtual driving task incidentally learned the layout of a virtual town and locations of objects in that town. They were subsequently tested on their spatial and recognition memory for the objects. To assess whether the objects were encoded allocentrically we examined pointing consistency across tested viewpoints. In three experiments, we found that spatial memory for objects at navigationally relevant locations was more consistent across tested viewpoints, particularly when participants had more limited experience of the environment. When participants' attention was focused on the appearance of objects, the navigational relevance effect was eliminated, whereas when their attention was focused on objects' locations, this effect was enhanced, supporting the hypothesis that when objects are processed in the service of navigation, rather than merely being viewed as objects, they engage qualitatively distinct attentional systems and are incorporated into an allocentric spatial representation. The results are consistent with evidence from the neuroimaging literature that when objects are relevant to navigation, they not only engage the ventral "object processing stream", but also the dorsal stream and medial temporal lobe memory system classically associated with allocentric spatial memory.     

Impaired representation of geometric relationships in humans with damage to the hippocampal formation

The pivotal role of the hippocampus for spatial memory is well-established. However, while neurophysiological and imaging studies suggest a specialization of the hippocampus for viewpoint-independent or allocentric memory, results from human lesion studies have been less conclusive. It is currently unclear whether disproportionate impairment in allocentric memory tasks reflects impairment of cognitive functions that are not sufficiently supported by regions outside the medial temporal lobe or whether the deficits observed in some studies are due to experimental factors. Here, we have investigated whether hippocampal contributions to spatial memory depend on the spatial references that are available in a certain behavioral context. Patients with medial temporal lobe lesions affecting systematically the right hippocampal formation performed a series of three oculomotor tasks that required memory of a spatial cue either in retinal coordinates or relative to a single environmental reference across a delay of 5000 ms. Stimulus displays varied the availability of spatial references and contained no complex visuo-spatial associations. Patients showed a selective impairment in a condition that critically depended on memory of the geometric relationship between spatial cue and environmental reference. We infer that regions of the medial temporal lobe, most likely the hippocampal formation, contribute to behavior in conditions that exceed the potential of viewpoint-dependent or egocentric representations. Apparently, this already applies to short-term memory of simple geometric relationships and does not necessarily depend on task difficulty or integration of landmarks into more complex representations. Deficient memory of basic geometric relationships may represent a core deficit that contributes to impaired performance in allocentric spatial memory tasks.     

Large scale homing in honeybees

Honeybee foragers frequently fly several kilometres to and from vital resources, and communicate those locations to their nest mates by a symbolic dance language. Research has shown that they achieve this feat by memorizing landmarks and the skyline panorama, using the sun and polarized skylight as compasses and by integrating their outbound flight paths. In order to investigate the capacity of the honeybees' homing abilities, we artificially displaced foragers to novel release spots at various distances up to 13 km in the four cardinal directions. Returning bees were individually registered by a radio frequency identification (RFID) system at the hive entrance. We found that homing rate, homing speed and the maximum homing distance depend on the release direction. Bees released in the east were more likely to find their way back home, and returned faster than bees released in any other direction, due to the familiarity of global landmarks seen from the hive. Our findings suggest that such large scale homing is facilitated by global landmarks acting as beacons, and possibly the entire skyline panorama.     

Spatial memory and orientation strategies in the elasmobranch<Emphasis Type="Italic"> Potamotrygon motoro</Emphasis>

We investigated whether juvenile freshwater stingrays (Potamotrygon motoro) can solve spatial tasks by constructing a cognitive map of their environment. Two experimental conditions were run: allocentric and ego-allocentric. Rays were trained to locate food within a four-arm maze placed in a room with visual spatial cues. The feeding location (goal) within the maze (room) remained constant while the starting position varied for the allocentrically but not for the ego-allocentrically trained group. After training, all rays solved the experimental tasks; however, different orientation strategies were used within and between groups. Allocentrically trained rays reached the goal via novel routes starting from unfamiliar locations, while ego-allocentrically trained rays primarily solved the task on the basis of an egocentric turn response. Our data suggest that P. motoro orients by constructing a visual cognitive map of its environment, but also uses egocentric and/or other orientation strategies alone or in combination for spatial orientation, a choice which may be governed by the complexity of the problem. We conclude that spatial memory functions are a general feature of the vertebrate brain.     

Influence of visual targets and landmarks on honey bee foraging and waggle dancing

Animals use diverse sensory stimuli to navigate their environment and to recognize rewarding food sources.Honey bees use visual atributes of the targeted food source,such as its color,shape,size,direction and distance from the hive,and the landmarks around it to navigate during foraging.They transmit the location information of the food source to other bees if it is highly rewarding.To investigate the relative importance of these attributes,we trained bees to feeders in two different experiments.In the first experiment,we asked whether bees prefer to land on(a)a similar feeder at a different distance on the same heading or on(b)a visually distinct feeder located at the exact same location.We found that,within a short foraging range,bees relied heavily on the color and the shape of the food source and to a lesser extent on its distance from the hive.In the second experiment,we asked if moving the main landmark or the feeder(visual target)influenced recruitment dancing for the feeder.We found that foragers took longer to land and danced fewer circuits when the location of the food source,or a major landmark associated with it,changed.These results demonstrate that prominent visual atributes of food sources and landmarks are evidently more reliable than distance information and that foraging bees heavily utilize these visual cues at the later stages of their journey.     

My Hand or Yours? Markedly Different Sensitivity to Egocentric and Allocentric Views in the Hand Laterality Task

In the hand laterality task participants judge the handedness of visually presented stimuli--images of hands shown in a variety of postures and views--and indicate whether they perceive a right or left hand. The task engages kinaesthetic and sensorimotor processes and is considered a standard example of motor imagery. However, in this study we find that while motor imagery holds across egocentric views of the stimuli (where the hands are likely to be one's own), it does not appear to hold across allocentric views (where the hands are likely to be another person's). First, we find that psychophysical sensitivity, d', is clearly demarcated between egocentric and allocentric views, being high for the former and low for the latter. Secondly, using mixed effects methods to analyse the chronometric data, we find high positive correlation between response times across egocentric views, suggesting a common use of motor imagery across these views. Correlations are, however, considerably lower between egocentric and allocentric views, suggesting a switch from motor imagery across these perspectives. We relate these findings to research showing that the extrastriate body area discriminates egocentric ('self') and allocentric ('other') views of the human body and of body parts, including hands.     

Influence of habitat complexity on route learning among different populations of climbing perch (Anabas testudineus Bloch, 1792)

Animals use different behavioral strategies to maximize their fitness in the natural environment. Learning and memory are critical in this context, allowing organisms to flexibly and rapidly respond to environmental changes. We studied how the physical characteristics of the native habitat influence the spatial learning capacity of Anabas testudineus belonging to four different populations collected from two streams and two ponds, in a linear maze. Stream fish were able to learn the route faster than pond fish irrespective of the presence or absence of landmarks in the maze. However, climbing perch collected from ponds learned the route faster in the maze provided with landmarks than in Plain maze. The results indicate that fish inhabiting a lotic ecosystem use egocentric cues in route learning rather than visual cues like landmarks. A local landmark may be a more reliable cue in route learning in a relatively stable habitat like a pond. In flowing aquatic systems, water flow may continually disrupt the visual landscape and thus landmarks as visual cues become unreliable. Spatial learning is thus a fine-tuned response to the complexity of the habitat and early rearing conditions may influence the spatial learning ability in fish.     

Complementary Roles of the Hippocampus and the Dorsomedial Striatum during Spatial and Sequence-Based Navigation Behavior

We investigated the neural bases of navigation based on spatial or sequential egocentric representation during the completion of the starmaze, a complex goal-directed navigation task. In this maze, mice had to swim along a path composed of three choice points to find a hidden platform. As reported previously, this task can be solved by using two hippocampal-dependent strategies encoded in parallel i) the allocentric strategy requiring encoding of the contextual information, and ii) the sequential egocentric strategy requiring temporal encoding of a sequence of successive body movements associated to specific choice points. Mice were trained during one day and tested the following day in a single probe trial to reveal which of the two strategies was spontaneously preferred by each animal. Imaging of the activity-dependent gene c-fos revealed that both strategies are supported by an overlapping network involving the dorsal hippocampus, the dorsomedial striatum (DMS) and the medial prefrontal cortex. A significant higher activation of the ventral CA1 subregion was observed when mice used the sequential egocentric strategy. To investigate the potential different roles of the dorsal hippocampus and the DMS in both types of navigation, we performed region-specific excitotoxic lesions of each of these two structures. Dorsal hippocampus lesioned mice were unable to optimally learn the sequence but improved their performances by developing a serial strategy instead. DMS lesioned mice were severely impaired, failing to learn the task. Our data support the view that the hippocampus organizes information into a spatio-temporal representation, which can then be used by the DMS to perform goal-directed navigation.     

Sex-inducing effect of a hydrophilic fraction on reproductive switching in the planarian Dugesia ryukyuensis (Seriata, Tricladida)

Background

Insects are known to rely on terrestrial landmarks for navigation. Landmarks are used to chart a route or pinpoint a goal. The distant panorama, however, is often thought not to guide navigation directly during a familiar journey, but to act as a contextual cue that primes the correct memory of the landmarks.

Results

We provided Melophorus bagoti ants with a huge artificial landmark located right near the nest entrance to find out whether navigating ants focus on such a prominent visual landmark for homing guidance. When the landmark was displaced by small or large distances, ant routes were affected differently. Certain behaviours appeared inconsistent with the hypothesis that guidance was based on the landmark only. Instead, comparisons of panoramic images recorded on the field, encompassing both landmark and distal panorama, could explain most aspects of the ant behaviours.

Conclusion

Ants navigating along a familiar route do not focus on obvious landmarks or filter out distal panoramic cues, but appear to be guided by cues covering a large area of their panoramic visual field, including both landmarks and distal panorama. Using panoramic views seems an appropriate strategy to cope with the complexity of natural scenes and the poor resolution of insects' eyes. The ability to isolate landmarks from the rest of a scene may be beyond the capacity of animals that do not possess a dedicated object-perception visual stream like primates.     

How do insects use path integration for their navigation?

 We combine experimental findings on ants and bees, and build on earlier models, to give an account of how these insects navigate using path integration, and how path integration interacts with other modes of navigation. At the core of path integration is an accumulator. This is set to an initial state at the nest and is updated as the insect moves so that it always reports the insect's current position relative to the nest. Navigation that uses path integration requires, in addition, a way of storing states of the accumulator at significant places for subsequent recall as goals, and a means of computing the direction to such goals. We discuss three models of how path integration might be used for this process, which we call vector navigation. Vector navigation is the principal means of navigating over unfamiliar terrain, or when landmarks are unavailable. Under other conditions, insects often navigate by landmarks, and ignore the output of the vector navigation system. Landmark navigation does not interfere with the updating of the accumulator. There is an interesting symmetry in the use of landmarks and path integration. In the short term, vector navigation can be independent of landmarks, and landmark navigation needs no assistance from path integration. In the longer term, visual landmarks help keep path vector navigation calibrated, and the learning of visual landmarks is guided by path integration. Received: 6 June 1999 / Accepted in revised form: 20 March 2000     

Place cells,navigational accuracy,and the human hippocampus.

The hippocampal formation in both rats and humans is involved in spatial navigation. In the rat, cells coding for places, directions, and speed of movement have been recorded from the hippocampus proper and/or the neighbouring subicular complex. Place fields of a group of the hippocampal pyramidal cells cover the surface of an environment but do not appear to do so in any systematic fashion. That is, there is no topographical relation between the anatomical location of the cells within the hippocampus and the place fields of these cells in an environment. Recent work shows that place cells are responding to the summation of two or more Gaussian curves, each of which is fixed at a given distance to two or more walls in the environment. The walls themselves are probably identified by their allocentric direction relative to the rat and this information may be provided by the head direction cells. The right human hippocampus retains its role in spatial mapping as demonstrated by its activation during accurate navigation in imagined and virtual reality environments. In addition, it may have taken on wider memory functions, perhaps by the incorporation of a linear time tag which allows for the storage of the times of visits to particular locations. This extended system would serve as the basis for a spatio-temporal event or episodic memory system.     

Optic flow informs distance but not profitability for honeybees

How do flying insects monitor foraging efficiency? Honeybees (Apis mellifera) use optic flow information as an odometer to estimate distance travelled, but here we tested whether optic flow informs estimation of foraging costs also. Bees were trained to feeders in flight tunnels such that bees experienced the greatest optic flow en route to the feeder closest to the hive. Analyses of dance communication showed that, as expected, bees indicated the close feeder as being further, but they also indicated this feeder as the more profitable, and preferentially visited this feeder when given a choice. We show that honeybee estimates of foraging cost are not reliant on optic flow information. Rather, bees can assess distance and profitability independently and signal these aspects as separate elements of their dances. The optic flow signal is sensitive to the nature of the environment travelled by the bee, and is therefore not a good index of flight energetic costs, but it provides a good indication of distance travelled for purpose of navigation and communication, as long as the dancer and recruit travel similar routes. This study suggests an adaptive dual processing system in honeybees for communicating and navigating distance flown and for evaluating its energetic costs.     

Landmark maps for honeybees

Experiments by Fabre (1915), Thorpe (1950), Chmurzynski (1964), and most recently Gould (1986) suggest that insects have maps of their terrain which enable them to find their way directly to a goal when they are displaced several hundred metres from it. This paper discusses what might constitute an insect's map in terms of a two-part computational model. The first part describes how an insect reaches a goal when the insect is sufficiently close that it can see some of the landmarks which are visible from the goal. The second part considers the problem of navigating when there is no similarity between the view from the release-site and the view from the goal.We start from a model designed to explain how a bee might return to a goal using a two-dimensional snapshot of the landscape seen from the goal (Collett and Cartwright 1983). To guide its return, the model bee continuously compares its snapshot with its current retinal image and moves so as to reduce the discrepancy between the two. Bees can only be guided in the right direction by the difference between current retinal image and snapshot when there is some resemblance between the two. In a realistically cluttered world, snapshot and retinal image become very dis-similar only a short distance from the goal.To increase the distance from which a model bee can return, the bee takes two snapshots at the goal. The first snapshot excludes landmarks near to the goal and the second snapshot includes them. With close landmarks filtered from both snapshot and retinal image, the match between the two deteriorates gradually as the bee moves away from the goal. A model bee using a filtered snapshot and image finds its way back to the neighbourhood of the goal from a relatively long distance (Fig. 2). The bee then switches to the second snapshot and is guided to the precise spot by its memory of the close landmarks.For longer range guidance, the model bee is equipped with an album of snapshots, each taken at a different location within the terrain. Linked to each snapshot is a vector encoding the distance and direction from the place where the snapshot was taken to the hive. When the bee is displaced to a new position, it selects the snapshot which best matches its current image and follows the associated home-vector back to the hive (Fig. 3). Such a hive-centred map can also be used to devise novel routes to places other than the hive. For instance, a bee can reach a foraging site from anywhere in its terrain by adding the home-vector recalled at the starting position to a vector specifying the distance and direction of the foraging site from the hive. The sum of these two vectors defines a direct trajectory to the foraging site.     

Honey bees store landmarks in an egocentric frame of reference

Honey bees are well known to rely on stored landmark information to locate a previously visited site. While various mechanisms underlying insect navigation have been thoroughly explored, little is yet known about the degree of integration of spatial parameters to form higher-level spatial representations. In this paper we explore the basic interactions between landmark cues and directional cues, which stand at the basis of our understanding of piloting mechanisms. A novel experimental paradigm allowed us independent manipulation of each parameter in a highly controlled environment. The approach taken was twofold: cue-conflict experiments were first conducted to examine the interactions between positional cues and directional cues. The bees were then successively deprived of sensory cues to question the dependence of landmark navigation on context cues. Our results confirm previous findings that landmark cues are used in concert with external directional cues if present. Conversely, the bees' ability to locate a food site was not disrupted in the absence of an external directional reference. Thus, bees store landmark memories in an egocentric frame of reference and only loose and facultative associations between visual memories and compass cues are formed.     

How do insects represent familiar terrain?

We argue here that ants and bees have a piecemeal representation of familiar terrain. These insects remember no more than what is needed to sustain the separate and parallel strategies that they employ when travelling between their nest and foraging sites. One major strategy is path integration. The insect keeps a running tally of its distance and direction from the nest and so can always return home. This global path integration is enhanced by long-term memories of significant sites that insects store in terms of the coordinates (direction and distance) of these sites relative to the nest. With these memories insects can plan routes that are steered by path integration to such sites. Quite distinct from global path integration are memories associated with familiar routes. Route memories include stored views of landmarks along the route with, in some cases, local vectors linked to them. Local vectors by encoding the direction and/or distance from one landmark to the next, or from one landmark to a goal, help an insect keep to a defined route. We review experiments showing that although local vectors can be recalled by recognising landmarks, the global path integration system is independent of landmark information and that landmarks do not have positional coordinates associated with them. The major function of route landmarks is thus procedural, telling an insect what action to perform next, rather than its location relative to the nest.