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.     

Flexible cue use in food-caching birds

An animal’s memory may be limited in capacity, which may result in competition among available memory cues. If such competition exists, natural selection may favor prioritization of different memory cues based on cue reliability and on associated differences in the environment and life history. Food-caching birds store numerous food items and appear to rely on memory to retrieve caches. Previous studies suggested that caching species should always prioritize spatial cues over non-spatial cues when both are available, because non-spatial cues may be unreliable in a changing environment; however, it remains unclear whether non-spatial cues should always be ignored when spatial cues are available. We tested whether mountain chickadees (Poecile gambeli), a food-caching species, prioritize memory for spatial cues over color cues when relocating previously found food in an associative learning task. In training trials, birds were exposed to food in a feeder where both spatial location and color were associated. During subsequent unrewarded test trials, color was dissociated from spatial location. Chickadees showed a significant pattern of inspecting feeders associated with correct color first, prior to visiting correct spatial locations. Our findings argue against the hypothesis that the memory of spatial cues should always take priority over any non-spatial cues, including color cues, in food-caching species, because in our experiment mountain chickadees chose color over spatial cues. Our results thus suggest that caching species may be more flexible in cue use than previously thought, possibly dependent upon the environment and complexity of available cues.     

Spatial relational memory in 9-month-old macaque monkeys

This experiment assesses spatial and nonspatial relational memory in freely moving 9-mo-old and adult (11-13-yr-old) macaque monkeys (Macaca mulatta). We tested the use of proximal landmarks, two different objects placed at the center of an open-field arena, as conditional cues allowing monkeys to predict the location of food rewards hidden in one of two sets of three distinct locations. Monkeys were tested in two different conditions: (1) when local visual cues marked the two sets of potentially baited locations, so that monkeys could use both local and spatial information to discriminate these locations from never-baited locations; and (2) when no local visual cues marked the two sets of potentially baited locations, so that monkeys had to rely on a spatial relational representation of the environment to discriminate these locations. No 9-mo-old or adult monkey associated the presence of the proximal landmarks, at the center of the arena, with the presence of food in one set of three distinct locations. All monkeys, however, discriminated the potentially baited locations in the presence of local visual cues, thus providing evidence of visual discrimination learning. More importantly, all 9-mo-old monkeys tested discriminated the potentially baited locations in absence of the local visual cues, thus exhibiting evidence of spatial relational learning. These findings indicate that spatial memory processes characterized by a relational representation of the environment are present as early as 9 mo of age in macaque monkeys.     

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.     

Rhesus monkeys use geometric and nongeometric information during a reorientation task

Rhesus monkeys (Macaca mulata) were subjected to a place finding task in a rectangular room perfectly homogeneous and without distinctive featural information. Results of Experiment 1 show that monkeys rely on the large-scale geometry of the room to retrieve a food reward. Experiments 2 and 3 indicate that subjects use also nongeometric information (colored wall) to reorient. Data of Experiments 4 and 5 suggest that monkeys do not use small angular cues but that they are sensitive to the size of the cues (Experiments 6, 7, and 8). Our findings strengthen the idea that a mechanism based on the geometry of the environment is at work in several mammalian species. In addition, the present data offer new perspectives on spatial cognition in animals that are phylogenetically close to humans. Specifically, the joint use of both geometric and landmark-based cues by rhesus monkeys tends to demonstrate that spatial processing became more flexible with evolution.     

Searching beneath the shelf in macaque monkeys: evidence for a gravity bias or a foraging bias?

The reasons underpinning search biases in 2 species of macaque monkeys (Macaca mulatta and Macaca arctoides) were explored over the course of 3 experiments requiring monkeys to search for a hidden food reward. The results reveal that monkeys are adept at exploiting perceptual cues to locate a food reward but are unable to use physical constraints such as solidity as cues to the reward's location. Monkeys prefer to search for a food reward beneath a solid shelf, not because they have an expectation that the reward should be there, but rather because, in the absence of usable cues, this bias emerges as a default search option. It is hypothesized that this bias may have its roots in a history of competition for food resources.     

Do common ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>) rely on human or conspecific gaze cues to detect hidden food?

The ability of non-human animals to use experimenter-given cues in object-choice tasks has recently gained interest. In such experiments, the location of hidden food is indicated by an experimenter, e.g. by gazing, pointing or touching. Whereas dogs apparently outperform all other species so far tested, apes and monkeys have problems in using such cues. Since only mammalian species have been tested, information is lacking about the evolutionary origin of these abilities. We here present the first data on object-choice tasks conducted with an avian species, the common raven. Ravens are highly competitive scavengers, possessing sophisticated cognitive skills in protecting their food caches and pilfering others’ caches. We conducted three experiments, exploring (i) which kind of cues ravens use for choosing a certain object, (ii) whether ravens use humans’ gaze for detecting hidden food and (iii) whether ravens would find hidden food in the presence of an informed conspecific who potentially provides gaze cues. Our results indicate that ravens reliably respond to humans’ touching of an object, but they hardly use point and gaze cues for their choices. Likewise, they do not perform above chance level in the presence of an informed conspecific. These findings mirror those obtained for primates and suggest that, although ravens may be aware of the gaze direction of humans and conspecifics, they apparently do not rely on this information to detect hidden food.     

The win-stay rule in foraging decisions by free-ranging titi monkeys (Callicebus cupreus cupreus) and Tamarins (Saguinus imperator imperator and Saguinus fuscicollis weddelli)

Rainforest primates need to apply distinct foraging rules for efficiently using the spatial knowledge of the distribution of resources showing different temporal patterns of renewal. A win-stay rule is very important for exploiting abundant, long-lasting resources. Here, the author tests the use of this rule in wild groups of emperor tamarins (Saguinus imperator imperator), saddle-back tamarins (Saguinus fuscicollis weddelli), and titi monkeys (Callicebus cupreus cupreus) during a series of foraging tasks. Four feeding stations composed of 8 visually similar feeding platforms (2 containing a food reward and 6 containing a sham reward) were constructed. The location of food rewards was reliable during some experiments and unreliable during others. All 3 species consistently adopted a win-stay rule for returning to reward platforms when their location was predictable over time but stopped using it when their spatial distribution changed randomly across experimental trials.     

Preference for spatial cues in a non-storing songbird species

Male mammals typically outperform their conspecific females on spatial tasks. A sex difference in cues used to solve the task could underlie this performance difference as spatial ability is reliant on appropriate cue use. Although comparative studies of memory in food-storing and non-storing birds have examined species differences in cue preference, few studies have investigated differences in cue use within a species. In this study, we used a one-trial associative food-finding task to test for sex differences in cue use in the great tit, Parus major. Birds were trained to locate a food reward hidden in a well covered by a coloured cloth. To determine whether the colour of the cloth or the location of the well was learned during training, the birds were presented with three wells in the test phase: one in the original location, but covered by a cloth of a novel colour, a second in a new location covered with the original cloth and a third in a new location covered by a differently coloured cloth. Both sexes preferentially visited the well in the training location rather than either alternative. As great tits prefer colour cues over spatial cues in one-trial associative conditioning tasks, cue preference appears to be related to the task type rather than being species dependent.     

REM restriction persistently alters strategy used to solve a spatial task

We tested the hypothesis that rapid eye movement (REM) sleep is important for complex associative learning by restricting rats from entering REM sleep for 4 h either immediately after training on an eight-box spatial task (0-4 REMr) or 4 h following training (4-8 REMr). Both groups of REM-restricted rats eventually reached the same overall performance level as did nonrestricted controls, but 0-4 REMr animals were delayed in their improvement in the first few days and lagged behind controls in the middle portion of the training period. More importantly, performance gains of 0-4 REMr rats depended more on simple local cues throughout the 15-d study since, unlike control and 4-8 REMr animals, their error rate increased after daily disruption of the relationship between local (intramaze) cues and the food reward. Thus, although overall performance was only subtly and transiently impaired, due to the ability to use alternate, nonspatial behavioral strategies, complex associative (spatial) learning was persistently impaired by restricting REM for a short critical period each day.     

Evidence of blocking with geometric cues in a virtual watermaze

Three computer based experiments, testing human participants in a non-immersive virtual watermaze task, used a blocking design to assess whether two sets of geometric cues would compete in a manner described by associative models of learning. In stage 1, participants were required to discriminate between visually distinct platforms. In stage 2, additional spatial information was provided by the shape or the color of the walls of the pool. In a test trial, the platforms were removed and the spatial knowledge acquired regarding the position of the platform was assessed. Experimental groups were compared against control groups which did not receive stage 1 training. The unique color of the correct platform, in Experiments 1 and 3, disrupted learning about the colored walls but not the geometry of the pool. In Experiment 2, the correct platform was identifiable from its position within the three platform array. Learning the relative position of the correct platform within the array disrupted learning about its position relative to the geometry of the pool, but not to the colored walls. The results suggest that learning the position of a goal in relation to the geometry of the environment can be blocked but only by an alternative geometric cue.     

Systems of Spatial Reference in Human Memory

Seven experiments examined the spatial reference systems used in memory to represent the locations of objects in the environment. Participants learned the locations of common objects in a room and then made judgments of relative direction using their memories of the layout (e.g., "Imagine you are standing at the shoe, facing the lamp; point to the clock"). The experiments manipulated the number of views that observers were allowed to experience, the presence or absence of local and global reference systems (e.g., a rectangular mat on which objects were placed and the walls of the room, respectively), and the congruence of local and global reference systems. Judgments of relative direction were more accurate for imagined headings parallel to study views than for imagined headings parallel to novel views, even with up to three study views. However, study views misaligned with salient reference systems in the environment were not strongly represented if they were experienced in the context of aligned views. Novel views aligned with a local reference system were, under certain conditions, easier to imagine than were novel views misaligned with the local reference system. We propose that learning and remembering the spatial structure of the surrounding environment involves interpreting the layout in terms of a spatial reference system. This reference system is imposed on the environment but defined by egocentric experience.     

Dominance of global visual properties at birth

Six experiments are reported that were aimed at demonstrating the presence in newborns of a perceptual dominance of global over local visual information in hierarchical patterns, similar to that observed in adults (D. Navon, 1977, 1981). The first four experiments showed that, even though both levels of visual information were detectable by the newborn (Experiments 1A and 1B), global cues enjoyed some advantage over local cues (Experiments 2 and 3). Experiments 4A and 4B demonstrated that the global bias was strictly dependent on the low spatial frequency content of the stimuli and vanished after selective removal of low spatial frequencies. The results are interpreted as suggesting parallels between newborns' visual processing and processing later in development.     

Association, inhibition, and object permanence in dogs' (Canis familiaris) spatial search

The relative role of associative processes and the use of explicit cues about object location in search behavior in dogs (Canis familiaris) was assessed by using a spatial binary discrimination reversal paradigm in which reversal conditions featured: (1) a previously rewarded location and a novel location, (2) a previously nonrewarded location and a novel location, or (3) a previously rewarded location and a previously nonrewarded location. Rule mediated learning predicts a similar performance in these different reversal conditions whereas associative learning predicts the worst performance in Condition 3. Evidence for an associative control of search emerged when no explicit cues about food location were provided (Experiment 1) but also when dogs witnessed the hiding of food in the reversal trials (Experiment 2) and when they did so in both the prereversal and the reversal trials (Experiment 3). Nevertheless, dogs performed better in the prereversal phase of Experiment 3 indicating that their search could be informed by the knowledge of the food location. Experiment 4 confirmed the results of Experiments 1 and 2, under a different arrangement of search locations. We conclude that knowledge about object location guides search behavior in dogs but it cannot override associative processes.     

Distance perception across spatial discontinuities

We investigated the use of nested contact relations in perceiving the relative distance of locations on discontinuous surfaces. Observers viewed computer-generated displays under monocular static conditions and adjusted a marker to match the perceived distance of a cube. The marker and cube were raised above the ground by two different platforms separated by a gap. The relative heights and distances of the platforms were varied. We found the following: (1) When spatially discontinuous surfaces are coplanar, locations of objects resting on these surfaces appear to be compared directly, bypassing relations with the underlying ground plane. (2) Spatial displacement between the platforms produces a bias, in the direction of the displacement, in the perceived relative locations of objects resting on the platforms. This suggests that local spatial relations between objects and their platforms are only partially integrated with more global spatial relations between the discontinuous surfaces of the platforms.     

Juvenile domestic pigs (Sus scrofa domestica) use human-given cues in an object choice task

Research on the comprehension of human-given cues by domesticated as well as non-domesticated species has received considerable attention over the last decade. While several species seem to be capable of utilizing these cues, former work with domestic pigs (Sus scrofa domestica) has shown inconclusive results. In this study, we investigated the use of human-given cues in an object choice task by young domestic pigs (N = 17; 7 weeks of age) who had very limited human contact prior to the experiments. Subjects had to choose between two bowls of which only one was baited with a reward. Over the course of five experiments, pigs were able to use proximal and, with some constraints, also distal pointing cues presented in both a dynamic-sustained and in a momentary manner. When the experimenter was pointing from the incorrect bowl towards the correct one, most of the subjects had problems solving the task—indicating that some form of stimulus/local enhancement affected pigs’ decision making. Interestingly, pigs were able to utilize the body and head orientation of a human experimenter to locate the hidden reward but failed to co-orient when head or body orientation of the experimenter was directed into distant space with no bowls present. Control trials ruled out the possibility that other factors (e.g. odour cues) affected subjects’ choice behaviour. Learning during experiments played a minor role and only occurred in three out of twelve test conditions. We conclude that domestic pigs, even at a very young age, are skilful in utilizing various human-given cues in an object choice task—raising the question whether pigs only used stimulus/local enhancement and associative learning processes or whether they were able to comprehend the communicative nature of at least some of these cues.     

Global/local processing of hierarchical visual stimuli in a conflict–choice task by capuchin monkeys (<Emphasis Type="Italic">Sapajus</Emphasis> spp.)

In the last two decades, comparative research has addressed the issue of how the global and local levels of structure of visual stimuli are processed by different species, using Navon-type hierarchical figures, i.e. smaller local elements that form larger global configurations. Determining whether or not the variety of procedures adopted to test different species with hierarchical figures are equivalent is of crucial importance to ensure comparability of results. Among non-human species, global/local processing has been extensively studied in tufted capuchin monkeys using matching-to-sample tasks with hierarchical patterns. Local dominance has emerged consistently in these New World primates. In the present study, we assessed capuchins’ processing of hierarchical stimuli with a method frequently adopted in studies of global/local processing in non-primate species: the conflict–choice task. Different from the matching-to-sample procedure, this task involved processing local and global information retained in long-term memory. Capuchins were trained to discriminate between consistent hierarchical stimuli (similar global and local shape) and then tested with inconsistent hierarchical stimuli (different global and local shapes). We found that capuchins preferred the hierarchical stimuli featuring the correct local elements rather than those with the correct global configuration. This finding confirms that capuchins’ local dominance, typically observed using matching-to-sample procedures, is also expressed as a local preference in the conflict–choice task. Our study adds to the growing body of comparative studies on visual grouping functions by demonstrating that the methods most frequently used in the literature on global/local processing produce analogous results irrespective of extent of the involvement of memory processes.     

Infant use of relative motion as information for form: Evidence for spatiotemporal integration of complex motion displays

Previous studies of infants’ ability to integrate and to utilize relative motion as information for form in the absence of structural cues have primarily involved motions that are uniform in rate, direction, and path within the form to be constructed. In the present study, we examined infants’ ability to integrate relative motion information from motions that are nonuniform along these dimensions, and from this integrative process to construct a coherently rotating two-dimensional form. Infants’ ability to integrate nonuniform motion was measured with regard to their ability to discriminate the rotating form from a noncoherent control display containing the same absolute motions. The results showed that discrimination of the coherent and incoherent displays was not demonstrated until 7 months of age. Two additional experiments were conducted to rule out the possibility that this discrimination was based on the detection of local regions of coherence, rather than the perception of the global rotating form. In both experiments, the results did not support discrimination based exclusively on local cues alone. From the combined results of all three experiments, we conclude that infants demonstrate the capacity to integrate the information contained within nonuniform trajectories into a coherent structure by 7 months of age.     

Capuchin monkeys’ use of human and conspecific cues to solve a hidden object-choice task

Learning by watching others can provide valuable information with adaptive consequences, such as identifying the presence of a predator or locating a food source. The extent to which nonhuman animals can gain information by reading the cues of others is often tested by evaluating responses to human gestures, such as a point, and less often evaluated by examining responses to conspecific cues. We tested whether ten brown capuchin monkeys (Cebus [Sapajus] apella) were able to use cues from monkeys and a pointing cue from a human to obtain hidden rewards. A monkey could gain access to a reward hidden in one of two locations by reading a cue from a conspecific (e.g., reaching) or a human pointing. We then tested whether they could transfer this skill from monkeys to humans, from humans to monkeys, and from one conspecific to another conspecific. One group of monkeys was trained and tested using a conspecific as the cue-giver and was then tested with a human cue-giver. The second group of monkeys was trained and tested with a human cue-giver and was then tested with a monkey cue-giver. Monkeys that were successful with a conspecific cue-giver were also tested with a novel conspecific cue-giver. Monkeys learned to use a human point and conspecific cues to obtain rewards. Monkeys that had learned to use the cues of a conspecific to obtain rewards performed significantly better than expected by chance when they were transferred to the cues of a novel conspecific. Monkeys that learned to use a human point to obtain rewards performed significantly better than expected by chance when tested while observing conspecific cues. Some evidence suggested that transferring between conspecific cue-givers occurred with more facility than transferring across species. Results may be explained by simple rules of association learning and stimulus generalization; however, spontaneous flexible use of gestures across conspecifics and between different species may indicate capuchins can generalize learned social cues within and partially across species.     

A comparative analysis of global and local processing of hierarchical visual stimuli in young children (Homo sapiens) and monkeys (Cebus apella)

Results obtained with preschool children (Homo sapiens) were compared with results previously obtained from capuchin monkeys (Cebus apella) in matching-to-sample tasks featuring hierarchical visual stimuli. In Experiment 1, monkeys, in contrast with children, showed an advantage in matching the stimuli on the basis of their local features. These results were replicated in a 2nd experiment in which control trials enabled the authors to rule out that children used spurious cues to solve the matching task. In a 3rd experiment featuring conditions in which the density of the stimuli was manipulated, monkeys' accuracy in the processing of the global shape of the stimuli was negatively affected by the separation of the local elements, whereas children's performance was robust across testing conditions. Children's response latencies revealed a global precedence in the 2nd and 3rd experiments. These results show differences in the processing of hierarchical stimuli by humans and monkeys that emerge early during childhood.