Some labels that are recognized on landmarks by the honeybee (Apis mellifera)

Freely flying bees were trained in a situation that resembled the natural task of a bee arriving at a foraging site that was located by a landmark. The bees' task was to locate the reward in the arm of the Y-choice apparatus, where a black pattern on a white background was displayed in one arm versus a white target in the other arm, at a range of 27 cm. The alternative patterns for the training included previously identified cues. They were: an oblique bar, three parallel oblique bars, an oblique grating, a square cross, six spokes, a large or a small spot, a spotty modulation, or a ring. The trained bees were given a variety of interleaved tests to discover the labels they had used to identify the patterns. A label is defined as the coincidence of cues that contributed to the recognition of a single landmark. The bees learned, firstly, the black area at the expected place, secondly, modulation caused by edges at the expected place. These cues were quantified and always available. In addition, the orientation cue was learned from a grating that covered the target, but was ignored in a single bar. The bees learned the positions of the centres of black and of radial symmetry. In tests, they also recognized unfamiliar cues that were not displayed in the training. The cues and preferences were similar to those used to discriminate between two targets. The new experiments validate some old conclusions that have been controversial for 40 years.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Pattern recognition in honeybees: eidetic imagery and orientation discrimination

The roles of eidetic imagery and orientational cues, respectively, in the discrimination of visual patterns by honeybees (Apis mellifera) were evaluated by training the bees to discriminate between patterns consisting of periodic, black and white square wave gratings. Training and tests with a number of different pairs of patterns revealed that bees use orientational cues almost exclusively, if such are present, and make use of eidetic images only when orientational cues are not available. On the other hand, if a pattern carries strong orientational cues, bees learn the orientation even if it is irrelevant to the discrimination task on which they are trained.     

Learning Auditory Space: Generalization and Long-Term Effects

Background

Previous findings have shown that humans can learn to localize with altered auditory space cues. Here we analyze such learning processes and their effects up to one month on both localization accuracy and sound externalization. Subjects were trained and retested, focusing on the effects of stimulus type in learning, stimulus type in localization, stimulus position, previous experience, externalization levels, and time.

Method

We trained listeners in azimuth and elevation discrimination in two experiments. Half participated in the azimuth experiment first and half in the elevation first. In each experiment, half were trained in speech sounds and half in white noise. Retests were performed at several time intervals: just after training and one hour, one day, one week and one month later. In a control condition, we tested the effect of systematic retesting over time with post-tests only after training and either one day, one week, or one month later.

Results

With training all participants lowered their localization errors. This benefit was still present one month after training. Participants were more accurate in the second training phase, revealing an effect of previous experience on a different task. Training with white noise led to better results than training with speech sounds. Moreover, the training benefit generalized to untrained stimulus-position pairs. Throughout the post-tests externalization levels increased. In the control condition the long-term localization improvement was not lower without additional contact with the trained sounds, but externalization levels were lower.

Conclusion

Our findings suggest that humans adapt easily to altered auditory space cues and that such adaptation spreads to untrained positions and sound types. We propose that such learning depends on all available cues, but each cue type might be learned and retrieved differently. The process of localization learning is global, not limited to stimulus-position pairs, and it differs from externalization processes.     

Generalization in visual recognition by the honeybee (Apis mellifera) : A review and explanation

During a century of studies on honeybee vision, generalization was the word for the acceptance of an unfamiliar pattern in the place of the training pattern, or the ability to learn a common factor in a group of related patterns. The ideas that bees generalize one pattern for another, detect similarity and differences, or form categories, were derived from the use of the same terms in the human cognitive sciences. Recent work now reveals a mechanistic explanation for bees. Small groups of ommatidia converge upon feature detectors that respond selectively to certain parameters that are in the pattern: modulation in the receptors, edge orientations, or to areas of black or colour. Within each local region of the eye the responses of each type of feature detector are summed to form a cue. The cues are therefore not in the pattern, but are local totals in the bee. Each cue has a quality, a quantity and a position on the eye, like a neuron response. This summation of edge detector responses destroys the local pattern based on edge orientation but preserves a coarse, sparse and simplified version of the panorama. In order of preference, the cues are: local receptor modulation, positions of well-separated black areas, a small black spot, colour and positions of the centres of each cue, radial edges, the averaged edge orientation and tangential edges. A pattern is always accepted by a trained bee that detects the expected cues in the expected places and no unexpected cues. The actual patterns are irrelevant. Therefore we have an explanation of generalization that is based on experimental testing of trained bees, not by analogy with other animals.Historically, generalization appeared when the training patterns were regularly interchanged to make the bees examine them. This strategy forced the bees to ignore parameters outside the training pattern, so that learning was restricted to one local eye region. This in turn limited the memory to one cue of each type, so that recognition was ambiguous because the cues were insufficient to distinguish all patterns. On the other hand, bees trained on very large targets, or by landing on the pattern, learned cues in several eye regions, and were able to recognize the coarse configural layout.     

Use of water flow direction to provide spatial information in a small-scale orientation task

Experiments were designed to investigate whether three-spined sticklebacks Gasterosteus aculeatus can use direction of water flow as an orientation cue. The fish had to learn the location of a food patch in a channel where water flow direction was the only reliable indicator of the food patch position. Fish from two ponds and two rivers were trained and tested in the spatial task to determine whether river three-spined sticklebacks are more adept at using water flow as a spatial cue than fish from ponds. All fish were able to use water flow to locate the food patch but one of the two river groups was significantly faster at learning the patch location. When the task was reversed so that fish that had formerly been trained to swim downstream now had to learn to swim upstream and vice versa both river groups learned the reversed task faster than the two pond groups. In a second experiment, to investigate whether fish from ponds or rivers vary in the type of spatial cue that they prefer to use, fish from one pond and one river were given a choice between two different types of spatial cue: flow direction or visual landmarks. A test trial in which these two cues were put into conflict revealed that the river population showed a strong preference for flow direction whilst the pond population preferred to use visual landmarks.     

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.     

Visual resolution of the orientation cue by the honeybee (Apis mellifera)

Bees were trained to discriminate between a pattern with two or more black bars and a similar pattern with the bars at right angles. Earlier measures of the resolution of oblique black and white regular gratings of different periods were confirmed. The positions of the training bars were shifted every 5 min to prevent the bees from using their locations as cues. To measure the length of the detectors of edge orientation, the trained bees were tested with targets filled with parallel short black/white edges of various lengths. The minimum individual length of edge required to discriminate the orientation cue was found to be near 3 degrees, and similar for vertical, horizontal and oblique edges. This is the first time that this kind of resolution has been measured in an invertebrate. The bees learn and recognize the edge orientation, not the lay-out of the pattern.     

Learning of colour and position cues in domestic chicks: Males are better at position,females at colour

Male and female chicks were trained to discriminate between two boxes for food reinforcement. The correct box was indicated by a colour cue (red or brown) and a position cue (right or left). After learning, the colour and the position cues were dissociated: the right-left location of the two boxes was alternated between trials according to a semi-random sequence.The chicks were thus retrained to discriminate either on the basis of colour (irrespective of position) or on the basis of position (irrespective of colour). There were no sex differences, during training, with both position and colour cues. However, during re-training females performed better on the colour learning task and males performed better on the position learning task.     

Pattern vision of the honeybee (Apis mellifera). What is an oriented edge?

Pairs of black patterns on a white background, one rewarded the other not, were presented vertically each in one arm of a Y-maze. During training the locations of the black areas were changed every 5 min to prevent the bees using them as cues, but cues from edges were kept consistent. Bees detect orientation even in a gradient that subtends 36° from black to white (normal to the edge). Orientation cues in short lengths of edge are detected and summed on each side of the fixation point, irrespective of the lay-out of the pattern. Edges at right angles reduce the total orientation cue. The polarity of edges in a sawtooth grating is weakly discriminated, but not the orientation of a fault line where two gratings meet. Edge quality can be discriminated, but is not recognised in unfamiliar orientations. When spot location is excluded as a cue, the orientation of a row of spots or squares which individually provide no net orientation cue is not discriminated. In conclusion, when locations of black areas are shuffled, the bees remember the sum of local orientation cues but not the global pattern, and there is no re-assembly of a pattern based on differently oriented edges. A neuronal model consistent with these results is presented. Accepted: 5 March 2000     

Objective fidelity evaluation in multisensory virtual environments: auditory cue fidelity in flight simulation

We argue that objective fidelity evaluation of virtual environments, such as flight simulation, should be human-performance-centred and task-specific rather than measure the match between simulation and physical reality. We show how principled experimental paradigms and behavioural models to quantify human performance in simulated environments that have emerged from research in multisensory perception provide a framework for the objective evaluation of the contribution of individual cues to human performance measures of fidelity. We present three examples in a flight simulation environment as a case study: Experiment 1: Detection and categorisation of auditory and kinematic motion cues; Experiment 2: Performance evaluation in a target-tracking task; Experiment 3: Transferrable learning of auditory motion cues. We show how the contribution of individual cues to human performance can be robustly evaluated for each task and that the contribution is highly task dependent. The same auditory cues that can be discriminated and are optimally integrated in experiment 1, do not contribute to target-tracking performance in an in-flight refuelling simulation without training, experiment 2. In experiment 3, however, we demonstrate that the auditory cue leads to significant, transferrable, performance improvements with training. We conclude that objective fidelity evaluation requires a task-specific analysis of the contribution of individual cues.     

No evidence that consistent auditory cues facilitate learning of spatial relations among locations

Human participants searched in a dynamic three-dimensional computer-generated virtual-environment open-field search task for four hidden goal locations arranged in a diamond configuration located in a 5×5 matrix of raised bins. Participants were randomly assigned to one of two groups: Consistent or Inconsistent. All participants experienced 30 trials in which four goal locations maintained the same spatial relations to each other (i.e., a diamond pattern), but this diamond pattern moved to random locations within the 5×5 matrix from trial-to-trial. For participants in the Consistent group, each goal location within the pattern always provided a unique and consistent auditory cue throughout the experimental session. For participants in the Inconsistent group, the same distinct auditory cues were provided for each goal location; however, the locations of these auditory cues within the pattern itself were randomized from trial-to-trial throughout the experimental session. Results indicated that participants in both groups learned the spatial configuration of goal locations, but the presence of consistent auditory cues did not facilitate the learning of spatial relations among locations.     

Orientation discrimination and categorization of photographs of natural objects by pigeons

In Experiment 1, pigeons trained to discriminate rightside-up and upside-down orientations of slides of natural scenes with humans successfully transferred to new slides of the same kind. Experiment 2 revealed that both the orientations of the human figures and of the background scenes controlled the discrimination. When they were oppositely oriented, the background orientation cue was dominant. In Experiment 3 slides showing objects on a white background were presented either rightside up or upside down, with each slide presented in one orientation only. One group of pigeons learned to classify the slides according to their orientations. The other group learned to classify the slides according to arbitrary groupings. When the slides were shown rotated by 180 degrees, the latter group continued to discriminate the individual slides (i.e., the pigeons showed orientation invariance). The former group classified the rotated slides according to their orientations (i.e., orientation discrimination). In Experiment 4, pigeons learned the orientation discrimination with separate sets of human and bird figures. Partial reversal training in one object class transferred to the rest of stimuli in this object class but did not to the other object class. These results suggest that pigeons can learn to discriminate photographs on the basis of orientation but that orientation-based equivalence relationship is not formed between object classes.     

Breakfast in the nook and dinner in the dining room: time-of-day discrimination in rats

Four studies were conducted which demonstrate that most (63%) male Sprague-Dawley rats can attain criterion, nine correct choices over ten consecutive trials, on a time-of-day discrimination in an elevated T-maze, but that the task is relatively difficult. The discrimination required that the rats go to one goal arm during a morning session and the other in an afternoon session. The sessions always began at the same time and were at least 6 h apart. A larger proportion of rats attained criterion and required fewer trials when the discriminative cue was a maze insert providing visual and tactile stimulation (0.72), orientation and position of the maze in the room (0.88), or the rats were required to always make the same left or right turn (0.94). Also, once criterion was attained, rats trained on time-of-day discrimination only made about 70% correct choices with continued training. Housing the rats with continuous light, all laboratory noises masked with white noise, and a random feeding schedule did not prevent them from acquiring the time-place discrimination. Testing the rats with a random number of trials during morning and afternoon sessions and with added or omitted sessions revealed that the rats did not use response or session alternation strategies to perform the discrimination. Also, the particular experimenter administering the morning or afternoon sessions did not serve as a cue for the discrimination. The relative difficulty of the task suggests that time of day does not normally function as a discriminative stimulus for choices, but probably as a contextual stimulus. Further, performance of the task in the absence of time-of-day cues suggests that the discrimination is based on event memory combined with an internal timing mechanism.     

Pigeons’ (Columba livia) hierarchical organization of local and global cues in touch screen tasks

Redundant encoding of local and global spatial cues is a common occurrence in many species. However, preferential use of the each type of cue seems to vary across species and tasks. In the current study, pigeons (Columba livia) were trained in three experiments on a touch screen task which included redundant local positional cues and global spatial cues. Specifically, pigeons were required to choose the middle out of three choice squares, such that the position within the array provided local information and the location on the screen provided global information. In Experiment 1, pigeons were trained and tested on vertically aligned arrays. In Experiment 2, pigeons were trained and tested on horizontally aligned arrays, and in Experiment 3, pigeons were trained and tested with vertical, horizontal and diagonally aligned arrays. The results indicate that preference for cue type depends upon the type of spatial information being encoded. Specifically, on vertical and diagonally aligned arrays, pigeons preferred global cues, whereas on horizontally aligned arrays, pigeons preferred local cues.     

The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback

The capacity to learn enables animals to match their phenotypic response to a changing environment on the basis of experience but learning is likely to incur costs such as the cost of making mistakes or the energetic cost of processing information. Little is known about how animals optimize the use of learned behaviour within their natural environments such that potential costs are minimized. We investigated whether the use of local landmarks in learning orientation routes by the three-spined stickleback, Gasterosteus aculeatus, varied in response to the visual stability of their natural habitats. Sticklebacks collected from five fast-flowing rivers and five ponds were trained to locate a hidden reward in a T-maze. Locating the reward required the fish to learn a body-centred algorithmic behaviour (turn left or right) or to follow plant landmarks. Probe trials, in which these cues conflicted, revealed which spatial cue the fish was using. Pond fish appeared to rely more than river fish on visual landmarks, which is consistent with the suggestion that even within a species, learned behaviour is fine-tuned in response to local environmental conditions. Landmarks may be reliable indicators of location only in stable pond habitats. In rivers, turbulence and flow may continually disrupt the visual landscape such that river fish may benefit from learning orientation routes only if learning is constrained so that unreliable visual cues are ignored. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Orientation Transfer in Vernier and Stereoacuity Training

Human performance on various visual tasks can be improved substantially via training. However, the enhancements are frequently specific to relatively low-level stimulus dimensions. While such specificity has often been thought to be indicative of a low-level neural locus of learning, recent research suggests that these same effects can be accounted for by changes in higher-level areas–in particular in the way higher-level areas read out information from lower-level areas in the service of highly practiced decisions. Here we contrast the degree of orientation transfer seen after training on two different tasks—vernier acuity and stereoacuity. Importantly, while the decision rule that could improve vernier acuity (i.e. a discriminant in the image plane) would not be transferable across orientations, the simplest rule that could be learned to solve the stereoacuity task (i.e. a discriminant in the depth plane) would be insensitive to changes in orientation. Thus, given a read-out hypothesis, more substantial transfer would be expected as a result of stereoacuity than vernier acuity training. To test this prediction, participants were trained (7500 total trials) on either a stereoacuity (N = 9) or vernier acuity (N = 7) task with the stimuli in either a vertical or horizontal configuration (balanced across participants). Following training, transfer to the untrained orientation was assessed. As predicted, evidence for relatively orientation specific learning was observed in vernier trained participants, while no evidence of specificity was observed in stereo trained participants. These results build upon the emerging view that perceptual learning (even very specific learning effects) may reflect changes in inferences made by high-level areas, rather than necessarily fully reflecting changes in the receptive field properties of low-level areas.     

Automated auditory recognition training and testing

Laboratory training and testing of auditory recognition skills in animals is important for understanding animal communication systems that depend on auditory cues. Songbirds are commonly studied because of their exceptional ability to learn complex vocalizations. In recent years, mounting interest in the perceptual abilities of songbirds has increased the demand for laboratory behavioural training and testing paradigms. Here, we describe and demonstrate the success of a method for auditory discrimination experiments, including all the necessary hardware, training procedures and freely-available, versatile software. The system can run several behavioural training and testing paradigms, including operant (go-nogo, stimulus preference, and two-alternative forced choice) and classical conditioning tasks. The software and some hardware components can be used with any laboratory animal that learns and responds to sensory cues. The peripheral hardware and training procedures are designed for use with songbirds and auditory stimuli. Using the go-nogo paradigm of the training system, we show that adult zebra finches learn to recognize and correctly classify individual female calls and male songs. We also show that learning the task generalizes to new stimulus classes; birds that learned the task with calls subsequently learned to recognize songs faster than did birds that learned the task and songs at the same time.     

Involvement of the sun and the magnetic compass of domestic fowl in its spatial orientation

Domestic chicks are able to find a food goal at different times of day, with the sun as the only consistent visual cue. This suggests that domestic chickens may use the sun as a time-compensated compass, rather than as a beacon. An alternative explanation is that the birds might use the earth's magnetic field. In this study, we investigated the role of the sun compass in a spatial orientation task using a clock-shift procedure. Furthermore, we investigated whether domestic chickens use magnetic compass information when tested under sunny conditions.Ten ISA Brown chicks were housed in outdoor pens. A separate test arena comprised an open-topped, opaque-sided, wooden octagonal maze. Eight goal boxes with food pots were attached one to each of the arena sides. A barrier inside each goal box prevented the birds from seeing the food pot before entering. After habituation, we tested in five daily 5-min trials whether chicks were able to find food in an systematically allocated goal direction. We controlled for the use of olfactory cues and intra-maze cues. No external landmarks were visible. All tests were done under sunny conditions. Circular statistics showed that nine chicks significantly oriented goalwards using the sun as the only consistent visual cue during directional testing. Next, these nine chicks were subjected to a clock-shift procedure to test for the role of sun-compass information. The chicks were housed indoors for 6 days on a light-schedule that was 6 h ahead of the natural light–dark schedule. After clock-shifting, the birds were tested again and all birds except one were disrupted in their goalward orientation. For the second experiment, six birds were re-trained and fitted with a tiny, powerful magnet on the head to disrupt their magnetic sense. The magnets did not affect the chicks’ goalward orientation.In conclusion, although the strongest prediction of the sun-compass hypothesis (significant re-orientation after clock-shifting) was neither confirmed nor refuted, our results suggest that domestic chicks use the sun as a compass rather than as a beacon. These findings suggest that hens housed indoors in large non-cage systems may experience difficulties in orientation if adequate alternative cues are unavailable. Further research should elucidate how hens kept in non-cage systems orient in space in relation to available resources.     

Social learning of a novel foraging patch in families of free-living Florida scrub-jays

Free-living juvenile Florida scrub-jays, Aphelocoma coerulescens, learned to forage in a novel patch (the centre of a ring) when in proximity to other family members that foraged successfully. We were able to distinguish the contributions of social learning and of individual learning, and to show that social learning occurred. The foraging task required individual jays to dig for peanut bits (chopped fragments) buried in sand in the centre of a 33-cm plastic ring. Jays were trained in their family groups to perform the task during a summer season, and were allowed to perform the task in the presence of juveniles (aged 40-85 days) in later years. Jays living in 18 control families received partial exposure to the training situation, but received no exposure to the ring before being presented with the task in the presence of their young. Juveniles in 16 families with trained jays were able to witness demonstrations and to scrounge peanut pieces from the models as they completed the task. These 41 juveniles learned more of the task than the 33 juveniles in control families. Seven juvenile jays and two older, nonbreeding jays in the trained families completed the task at least once, whereas no jays in control families completed the task. A modified task that prevented snatching also prevented transmission of the complete task, although the 22 juveniles that observed the modified task learned more of the task than the 33 control juveniles. Further analysis indicated that demonstrations had their greatest effect in increasing the probability that juveniles would enter the ring. Copyright 2000 The Association for the Study of Animal Behaviour.