One-trial spatial learning: wild hummingbirds relocate a reward after a single visit

Beaconing to rewarded locations is typically achieved by visual recognition of the actual goal. Spatial recognition, on the other hand, can occur in the absence of the goal itself, relying instead on the landmarks surrounding the goal location. Although the duration or frequency of experiences that an animal needs to learn the landmarks surrounding a goal have been extensively studied with a variety of laboratory tasks, little is known about the way in which wild vertebrates use them in their natural environment. Here, we allowed hummingbirds to feed once only from a rewarding flower (goal) before it was removed. When we presented a similar flower at a different height in another location, birds frequently returned to the location the flower had previously occupied (spatial recognition) before flying to the flower itself (beaconing). After experiencing three rewarded flowers, each in a different location, they were more likely to beacon to the current visible flower than they were to return to previously rewarded locations (without a visible flower). These data show that hummingbirds can encode a rewarded location on the basis of the surrounding landmarks after a single visit. After multiple goal location manipulations, however, the birds changed their strategy to beaconing presumably because they had learned that the flower itself reliably signalled reward.     

Do rufous hummingbirds (<Emphasis Type="Italic">Selasphorus rufus</Emphasis>) use visual beacons?

Animals are often assumed to use highly conspicuous features of a goal to head directly to that goal (‘beaconing’). In the field it is generally assumed that flowers serve as beacons to guide pollinators. Artificial hummingbird feeders are coloured red to serve a similar function. However, anecdotal reports suggest that hummingbirds return to feeder locations in the absence of the feeder (and thus the beacon). Here we test these reports for the first time in the field, using the natural territories of hummingbirds and manipulating flowers on a scale that is ecologically relevant to the birds. We compared the predictions from two distinct hypotheses as to how hummingbirds might use the visual features of rewards: the distant beacon hypothesis and the local cue hypothesis. In two field experiments, we found no evidence that rufous hummingbirds used a distant visual beacon to guide them to a rewarded location. In no case did birds abandon their approach to the goal location from a distance; rather they demonstrated remarkable accuracy of navigation by approaching to within about 70 cm of a rewarded flower’s original location. Proximity varied depending on the size of the training flower: birds flew closer to a previously rewarded location if it had been previously signalled with a small beacon. Additionally, when provided with a beacon at a new location, birds did not fly directly to the new beacon. Taken together, we believe these data demonstrate that these hummingbirds depend little on visual characteristics to beacon to rewarded locations, but rather that they encode surrounding landmarks in order to reach the goal and then use the visual features of the goal as confirmation that they have arrived at the correct location.     

Cue learning by rufous hummingbirds (Selasphorus rufus)

The authors investigated the use by wild-living rufous hummingbirds (Selasphorus rufus) of flower color pattern and flower position for remembering rewarded flowers. Birds were presented with arrays of artificial flowers, a proportion of which was rewarded. Once the locations were learned by the birds, the array was moved 2 m, and flower color pattern and/or rewarded positions were manipulated. The birds' ability to learn which were the rewarded flowers in this 2nd array was much more strongly affected by whether the rewarded flowers occupied the same positions as in the 1st array than by their color patterns.     

Spatial relational learning in rufous hummingbirds (Selasphorus rufus)

There is increasing evidence that animals can learn abstract spatial relationships, and successfully transfer this knowledge to novel situations. In this study, rufous hummingbirds (Selasphorus rufus) were trained to feed from either the lower or the higher of two flowers. When presented with a test pair of flowers, one of which was at a novel height, they chose the flower in the appropriate spatial position rather than the flower at the correct height. This response may also have been influenced by a preference for taller flowers as acquisition of the task during experimental training occurred more readily when the reward flower was the taller of the pair. Thus, it appears that although learning abstract relationships may be a general phenomenon across contexts, and perhaps across species, the ease with which they are learned and the context in which they are subsequently used may not be the same.     

Landmark Stability: Further Studies Pointing to a Role in Spatial Learning

Two experiments were conducted to investigate the possible role of landmark stability in spatial learning. Rats were trained to search in a large arena for food hidden at a consistent distance and direction from either a single radially symmetric landmark or an array of two landmarks. We varied the relative degree to which the landmark array and/or the cues of the training context predicted the location of food, without varying the conditional probability of food being available given either cue. Experiment 1 used vestibular disorientation to ensure control of search location by experimenter-controlled cues. The results showed that making either a single landmark or a cluster of two adjacent landmarks the sole spatial predictor of reward location reduced the accuracy of search compared to a condition where both the landmark array and context cues were reliable spatial predictors. Varying global landmark stability had no effect when training was conducted using an array of two landmarks located some distance from each other. Context cues, when tested alone, triggered very little searching in appropriate locations, and the absolute magnitude of control over search was insufficient to account for the superiority of stable landmarks. The better learning with a stable landmark, and the dependence of this effect on the geometrical arrangement of landmarks, points to the conditions of spatial learning involving additional principles to those of simple associative conditioning. Experiment 2 examined landmark stability using a single landmark and fixed directional cues in the absence of vestibular disorientation. This also revealed a relative advantage of landmark stability, but animals with a landmark that moved from trial to trial did show some evidence of learning. Context cues when tested alone had minimal influence. Parametric manipulation of landmark stability offers a novel way of influencing spatial learning and thus understanding better the process through which egocentric representations of perceived space are transformed into allocentric representations of the real world. The purpose of this paper is to describe two experiments concerned with identifying the psychological processes of allocentric spatial learning. The results point to the idea that landmark stability is an important factor in spatial learning. Specifically, they reveal that whether or not a landmark will be used for the purpose of representing the location of another object (including hidden objects) is influenced by whether it is perceived as geometrically stable with respect to at least one other landmark and/or certain geometric features of the environment. This phenomenon is relevant to the application of associative learning principles to the spatial domain.     

Use of geometry for spatial reorientation in children applies only to symmetric spaces

Proponents of the geometric module hypothesis argue that following disorientation, many species reorient by use of macro‐environment geometry. It is suggested that attention to the surface layout geometry of natural terrain features may have been selected for over evolutionary time due to the enduring and unambiguous location information it provides. Paradoxically, however, tests of the hypothesis have been exclusively conducted in symmetric (hence ‘unnatural’ and geometrically ambiguous) environments. The present series of studies examines reorientation by 18‐month–3‐year‐old children in a rectangular versus irregular quadrilateral enclosure (Study 1), a rectangular versus irregular quadrilateral array (Study 2) and an isosceles versus irregular triangular array (Study 3). Children were successful in symmetric but not asymmetric environments, casting doubt on the functional argument for an empirical basis of the geometric module hypothesis.     

Geometric determinants of human spatial memory

Geometric alterations to the boundaries of a virtual environment were used to investigate the representations underlying human spatial memory. Subjects encountered a cue object in a simple rectangular enclosure, with distant landmarks for orientation. After a brief delay, during which they were removed from the arena, subjects were returned to it at a new location and orientation and asked to mark the place where the cue had been. On some trials the geometry (size, aspect ratio) of the arena was varied between presentation and testing. Responses tended to lie somewhere between a location that maintained fixed distances from nearby walls and a location that maintained fixed ratios of the distances between opposing walls. The former were more common after expansions and for cued locations nearer to the edge while the latter were more common after contractions and for locations nearer to the center. The spatial distributions of responses predicted by various simple geometric models were compared to the data. The best fitting model was one derived from the response properties of 'place cells' in the rat hippocampus, which matches the 'proximities' 1/(d+c) of the cue to the four walls of the arena, where d is the distance to a wall and c is a global constant. Subjects also tended to adopt the same orientation at presentation and testing, although this was not due to using a view matching strategy, which could be ruled out in 50% of responses. Disoriented responses were most often seen where the cued location was near the center of the arena or where the long axis of a rectangular arena was changed between presentation and testing, suggesting that the geometry of the arena acts as a weak cue to orientation. Overall, the results suggest a process of visual landmark matching to determine orientation, combined with an abstract representation of the proximity of the cued location to the walls of the arena consistent with the neural representation of location in the hippocampus.     

Geometric rule learning by Clark's nutcrackers (Nucifraga columbiana)

Clark's nutcrackers (Nucifraga columbiana) were trained to search in a location defined by its geometric relationship to 2 landmarks. Two groups were trained to search at different points along the line connecting the landmarks, and 2 groups were trained to find the 3rd point of a triangle, on the basis of either direction or distance from the landmarks. All groups learned and transferred to new interlandmark distances. However, the constant-distance group learned more slowly, searched less accurately, and showed less transfer than the other 3 groups. When tested with new orientations of the landmarks, the birds tended to follow small but not large rotations. When tested with a single landmark, birds in the half, quarter, and constant-bearing groups searched in the appropriate direction from the landmark, but birds in the distance group did not. These results demonstrate that nutcrackers can learn a variety of geometric principles, that directional information may be weighted more heavily than distance information, and that the birds can use both absolute and relative information about spatial relationships.     

Features enhance the encoding of geometry

Successful navigation within an environment requires that the traveler establish the correct heading—a process referred to as orienting. Many studies have now shown that humans and non-human animals can use the geometric properties of an enclosure to orient. In the present study, two groups of Clark’s nutcrackers (Nucifraga columbiana) were trained, in a reference memory task, to find food hidden in one of four containers arranged to form a rectangular array. One group had unique objects placed next to each of the containers, whereas the second group had identical objects placed next to each of the containers. Here, I show for the first time that for the Clark’s nutcracker, the distinctive properties of these objects enhanced the encoding of the array’s geometry compared to the learning of geometric properties from an array of identical objects, which remained at chance after substantial amounts of training. Subsequent transformation tests showed that an object not associated with reward, but sharing the same geometric properties as the correct object, may have had inhibitory qualities. Furthermore, by systematically removing objects from the array, I show that although nutcrackers encoded the geometry of the array, they did not encode a complete featural representation of the objects within the array.     

Global and local spatial landmarks: their role during foraging by Columbian ground squirrels (Spermophilus columbianus)

Locating food and refuge is essential for an animal's survival. However, little is known how mammals navigate under natural conditions and cope with given environmental constraints. In a series of six experiments, I investigated landmark-based navigation in free-ranging Columbian ground squirrels (Spermophilus columbianus). Squirrels were trained individually to find a baited platform within an array of nine identical platforms and artificial landmarks set up on their territories. After animals learned the location of the food platform in the array, the position of the latter with respect to local artificial, local natural, and global landmarks was manipulated, and the animal's ability to find the food platform was tested. When only positions of local artificial landmarks were changed, squirrels located food with high accuracy. When the location of the array relative to global landmarks was altered, food-finding accuracy decreased but remained significant. In the absence of known global landmarks, the presence of a familiar route and natural local landmarks resulted in significant but not highly accurate performance. Squirrels likely relied on multiple types of cues when orienting towards a food platform. Local landmarks were used only as a secondary mechanism of navigation, and were not attended to when a familiar route and known global landmarks were present. This study provided insights into landmark use by a wild mammal in a natural situation, and it demonstrated that an array of platforms can be employed to investigate landmark-based navigation under such conditions.     

Great apes’ strategies to map spatial relations

We investigated reasoning about spatial relational similarity in three great ape species: chimpanzees, bonobos, and orangutans. Apes were presented with three spatial mapping tasks in which they were required to find a reward in an array of three cups, after observing a reward being hidden in a different array of three cups. To obtain a food reward, apes needed to choose the cup that was in the same relative position (i.e., on the left) as the baited cup in the other array. The three tasks differed in the constellation of the two arrays. In Experiment 1, the arrays were placed next to each other, forming a line. In Experiment 2, the positioning of the two arrays varied each trial, being placed either one behind the other in two rows, or next to each other, forming a line. Finally, in Experiment 3, the two arrays were always positioned one behind the other in two rows, but misaligned. Results suggested that apes compared the two arrays and recognized that they were similar in some way. However, we believe that instead of mapping the left–left, middle–middle, and right–right cups from each array, they mapped the cups that shared the most similar relations to nearby landmarks (table’s visual boundaries).     

Reorientation in a rhombic environment: No evidence for an encapsulated geometric module

Reorientation behavior of young children has been described as dependent upon a geometric module that is incapable of interacting with landmark information. Whereas previous studies typically used rectangular spaces that provided geometric information about distance, we used a rhombic space that allowed us to explore the way children use geometric information about angles. Reorientation was studied in manipulatory space (Experiment 1) and locomotor space (Experiment 2) in the presence and absence of a salient landmark. In the absence of salient landmarks, 4- to 6-year-olds used geometric features to reorient in both spaces. When a salient landmark was available in manipulatory space, 4-year-olds used the landmark and ignored the geometry. Five- and 6-year-olds used the geometry, but in combination with the landmark. In locomotor space, this combined use was already seen at age 4, and increased with age. Taken together, these results offer no support for the notion that reorientation behavior in young children depends on an informationally encapsulated geometric module.     

Hippocampus lesions impair landmark array spatial learning in homing pigeons: a laboratory study

Hippocampal (HF)-lesioned pigeons display impaired homing ability when flying over familiar terrain, where they are presumably relying on a map-like representation of familiar landmarks to navigate. However, research carried out in the field precludes a direct test of whether hippocampal lesions compromise the ability of homing pigeons to navigate by familiar landmarks. To examine more thoroughly the relationship between hippocampus and landmark spatial learning, control, neostriatum-lesioned, and HF-lesioned homing pigeons were trained on two open field, laboratory, conditional discrimination tasks. One was a visual landmark array task, and the other was a room color discrimination task. For the tasks, the correct of three differently colored food bowls was determined by the spatial relationship among a group of five landmarks and room color, respectively. Intact control birds successfully learned both tasks, while neostriatum-lesioned birds successfully learned the landmark array task-the only task on which they were trained. By contrast, HF-lesioned birds successfully learned the room color task but were unable to learn the landmark array task. The data support the hypothesis that homing performance deficits observed in the field following hippocampal lesions are in part a consequence of an impairment in the ability of lesioned pigeons to use familiar visual landmarks for navigation.     

Sex differences and the effect of instruction on reorientation abilities by humans

This study examined whether differences in the amount of information provided to men and women, in the form of verbal instruction, influenced their encoding during a reorientation task. When a navigator needs to orient, featural (e.g., colour or texture) and geometry (e.g., metric information) are used to determine which direction to begin traveling. The current study used a spatial reorientation task to examine how men and women use featural and geometric cues and whether the content of the task’s instructions influenced how these cues were used. Participants were trained to find a target location in a rectangular room with distinctive objects situated at each corner. Once the participants were accurately locating the target, various tests manipulating the spatial information were conducted. We found both men and women encoded the featural cues, and even though the features provided reliable information, participants generally showed an encoding of geometry. However, when participants were not provided with any information about the spatial aspects of the task in the instructions, they failed to encode geometry. We also found that women used distant featural cues as landmarks when the featural cue closest to the target was removed, whereas men did not. Yet, when the two types of cues were placed in conflict, both sexes weighed featural cues more heavily than geometric cues. The content of the task instructions also influenced how cues were relied upon in this conflict situation. Our results have important implications for our understanding of how spatial cues are used for reorientation.     

Flexible learning and use of multiple-landmark information by pigeons (Columba livia) in a touch screen-based goal searching task

Three touch screen-based experiments were conducted to investigate whether pigeons would learn to use configural information about a goal's location in relation to a multiple-landmark array. In Experiment 1, 4 pigeons (Columba livia) were trained to peck a computer monitor at a location that constituted the third vertex of a hypothetical triangle defined by 2 different landmarks. The landmarks appeared in 3 orientations during the training, and the pigeons' goal-searching ability easily transferred to the landmarks presented in 3 novel orientations. Each landmark was asymmetric, so we next examined whether the pigeons used (a) the small-scale, local orientation information that could be inferred from each landmark individually, or (b) the large-scale, configural information that could be inferred from the spatial arrangement of multiple landmarks taken as a whole. Even when each single landmark appeared by itself, the pigeons were able to locate the goal accurately, suggesting that the large-scale, configural information was not essential. However, when 1 landmark locally pointed to a location that was consistent with the triangular configuration and the other landmark locally pointed to a different location, the pigeons predominantly pecked at the configurally array-consistent location. These results suggest that the pigeons redundantly learned both the large-scale, configural strategy and the local, single-landmark strategy, but they mainly used the latter information, and used the former information solely to disambiguate conflicts when the 2 landmarks pointed toward different targets. Such flexible learning and use of redundant information may reflect the pigeons' adaptation to unstable wild environments during their evolutionary history.     

Independent effects of geometry and landmark in a spontaneous reorientation task: a study of two species of fish

While disoriented humans and animals use both landmarks and environmental geometry to guide their navigation, it is not clear what kinds of cognitive mechanisms underlie these behaviors. Because traditional tests of trained navigation behavior in environments containing both landmarks and geometric information may cloud our insight into the nature of these processes, the present study tested the spontaneous use of landmarks and environmental shape by two species of fish-Redtail Splitfins (Xenotoca eiseni) and Zebrafish (Danio rerio). The results suggest that while geometry is spontaneously used by both species and both sexes to compute relative position or direction, the spontaneous use of landmarks is limited to direct beaconing and complicated by attraction to features and variability across species and sex. These findings support the view that while multiple cues may ultimately guide behavior, the computation of orientation and relative positions is specified by geometric input and is independent from other navigation processes such as beaconing.     

The psychophysics of uneconomical choice: non-linear reward evaluation by a nectar feeder

Uneconomical choices by humans or animals that evaluate reward options challenge the expectation that decision-makers always maximize the return currency. One possible explanation for such deviations from optimality is that the ability to sense differences in physical value between available alternatives is constrained by the sensory and cognitive processes for encoding profitability. In this study, we investigated the capacity of a nectarivorous bat species (Glossophaga commissarisi) to discriminate between sugar solutions with different concentrations. We conducted a two-alternative free-choice experiment on a population of wild electronically tagged bats foraging at an array of computer-automated artificial flowers that recorded individual choices. We used a Bayesian approach to fit individual psychometric functions, relating the strength of preferring the higher concentration option to the intensity of the presented stimulus. Psychometric analysis revealed that discrimination ability increases non-linearly with respect to intensity. We combined this result with a previous psychometric analysis of volume perception. Our theoretical analysis of choice for rewards that vary in two quality dimensions revealed regions of parameter combinations where uneconomic choice is expected. Discrimination ability may be constrained by non-linear perceptual and cognitive encoding processes that result in uneconomical choice.     

Transfer of spatial behaviour controlled by a landmark array with a distinctive shape

In two experiments, rats swam to a submerged platform in one corner of a rectangular or kite-shaped array created by four identical landmarks attached to the walls of a circular pool. After training in the rectangular array, rats expressed a preference for the corner in the kite-shaped array that was geometrically equivalent to where the platform was located previously. After training in either array, the removal of two landmarks from the rectangular array, or the landmark at the apex of the kite-shaped array, did not affect the control over searching exerted by the remaining landmarks. The results imply that rats use local rather than global spatial representations when searching for a hidden goal with reference to an array of landmarks.     

Solving small spaces: investigating the use of landmark cues in brown capuchins (Cebus apella)

Some researchers have recently argued that humans may be unusual among primates in preferring to use landmark information when reasoning about some kinds of spatial problems. Some have explained this phenomenon by positing that our species’ tendency to prefer landmarks stems from a human-unique trait: language. Here, we test this hypothesis—that preferring to use landmarks to solve such tasks is related to language ability—by exploring landmark use in a spatial task in one non-human primate, the brown capuchin monkey (Cebus apella). We presented our subjects with the rotational displacement task, in which subjects attempt to relocate a reward hidden within an array of hiding locations which are subsequently rotated to a new position. Over several experiments, we varied the availability and the salience of a landmark cue within the array. Specifically, we varied (1) visual access to the array during rotation, (2) the type of landmark, (3) the consistency of the landmark qualities, and (4) the amount of exposure to the landmark. Across Experiments 1 through 4, capuchins did not successfully use landmarks cues, suggesting that non-linguistic primates may not spontaneously use landmarks to solve some spatial problems, as in this case of a small-scale dynamic spatial task. Importantly, we also observed that capuchins demonstrated some capacity to learn to use landmarks in Experiment 4, suggesting that non-linguistic creatures may be able to use some landmarks cues in similar spatial tasks with extensive training.     

Use of cue configuration geometry for spatial orientation in human infants (Homo sapiens)

Research with both rats and human infants has found that after inertial disorientation, the geometry of an enclosed environment is used in preference over distinctive featural information during goal localization. Infants (Homo sapiens, 18-24 months) were presented with a toy search task involving inertial disorientation in 1 of 2 conditions. In the identical condition, 4 identical hiding boxes in a rectangular formation were set within a circular enclosure. In the distinctive condition, 4 distinctive hiding boxes were used. Infants searched the goal box and its rotational equivalent significantly more than would be expected by chance in the identical condition, showing that they were sensitive to the geometric configuration of the array of boxes. Unlike the results of studies using a rectangular enclosure, however, in the distinctive condition, infants searched at the correct location significantly more than at other locations.