Spatial pattern learning in rats: control by an iterative pattern.

Rats searched in a matrix of vertical poles for food hidden on top of the poles. The only information available about the location of the food was the consistent spatial pattern of the baited poles, which was a checkerboard. This spatial pattern of hidden-food locations came to control the choices of poles made by the rats. The experiments ruled out the possibility that this control can be explained by the acquisition of simple response tendencies to move from pole to pole. Instead, this behavioral control of choices was attributed to the development of a representation of the checkerboard pattern of baited locations. Spatial pattern learning may have mechanisms in common with other forms of pattern learning.     

No evidence for overshadowing or facilitation of spatial pattern learning by visual cues

Two experiments were conducted to examine the effects of redundant and relevant visual cues on spatial pattern learning. Rats searched for hidden food items on the tops of poles that formed a square (Experiment 1) or a checkerboard (Experiment 2) pattern. The experimental groups were trained with visual cues that specified the locations of the baited poles. All groups were tested without visual cues so that any overshadowing or facilitation of spatial pattern learning by visual cues could be detected. Spatial choices were controlled by the spatial pattern and by the visual cues in both experiments. However, there was no evidence of overshadowing or facilitation of spatial pattern learning by visual cues in either experiment. The results are consistent with the idea that the representation of the spatial pattern that guides choices is not controlled by the same learning processes as those that produce associations between visual cues and food locations.     

Object-goal positioning influences spatial representation in rats

Three tests investigated how the geometric relation between object/landmarks and goals influenced spatial choice behavior in rats. Two groups searched for hidden food in an object-filled circular arena containing 24 small poles. For the “Proximal” group, four distinct objects in a square configuration were placed close to four baited poles. For the “Distal” group, the identical configuration of objects was rotated 45° relative to the poles containing the hidden food. The Proximal group learned to locate the baited poles more quickly than the Distal group. Tests with removed and rearranged landmarks indicated that the two groups learned to use the objects differently. The results suggested that close proximity of objects to goals encouraged their use as beacons, while greater distance of objects from goals resulted in the global encoding of the geometric properties of the arena and the use of the objects as landmarks. Received: 22 June 1998 / Accepted after revision: 23 January 1999     

A consistent but non-coincident visual pattern facilitates the 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: visual pattern or visual random. 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 visual pattern group, four locations were marked in a distinct color and arranged in a diamond pattern that moved to a random location independent of the hidden spatial pattern from trial to trial throughout the experimental session. For participants in the visual random group, four random locations were marked with a distinct color and moved to random locations independent from the hidden spatial pattern from trial to trial throughout the experimental session. As a result, the visual cues for the visual pattern group were consistent but not coincident with the hidden spatial pattern, whereas the visual cues for the visual random group were neither consistent nor coincident with the hidden spatial pattern. Results indicated that participants in both groups learned the spatial configuration of goal locations and that the presence of consistent but noncoincident visual cues facilitated the learning of spatial relations among locations.     

Does affective information influence domestic dogs’ (<Emphasis Type="Italic">Canis lupus familiaris</Emphasis>) point-following behavior?

Several studies have examined dogs’ (Canis lupus familiaris) comprehension and use of human communicative cues. Relatively few studies have, however, examined the effects of human affective behavior (i.e., facial and vocal expressions) on dogs’ exploratory and point-following behavior. In two experiments, we examined dogs’ frequency of following an adult’s pointing gesture in locating a hidden reward or treat when it occurred silently, or when it was paired with a positive or negative facial and vocal affective expression. Like prior studies, the current results demonstrate that dogs reliably follow human pointing cues. Unlike prior studies, the current results also demonstrate that the addition of a positive affective facial and vocal expression, when paired with a pointing gesture, did not reliably increase dogs’ frequency of locating a hidden piece of food compared to pointing alone. In addition, and within the negative facial and vocal affect conditions of Experiment 1 and 2, dogs were delayed in their exploration, or approach, toward a baited or sham-baited bowl. However, in Experiment 2, dogs continued to follow an adult’s pointing gesture, even when paired with a negative expression, as long as the attention-directing gesture referenced a baited bowl. Together these results suggest that the addition of affective information does not significantly increase or decrease dogs’ point-following behavior. Rather these results demonstrate that the presence or absence of affective expressions influences a dogs’ exploratory behavior and the presence or absence of reward affects whether they will follow an unfamiliar adult’s attention-directing gesture.     

Motivation and memory in zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>) foraging behavior

Remembering combinations of information such as what resources have been seen in which locations could play an important role in enhancing individual survival through increased foraging success. To date, there have been relatively few investigations of avian memory involving more than one category of information. This study explored zebra finches’ (Taeniopygia guttata) capacity to recall two categories in combination, namely food-type and spatial location. Birds were trained to remove variously weighted flaps to find two types of food hidden beneath. Memory for food-types and locations was assessed by pre-feeding the birds to satiety on and devaluing one food-type, and then testing the birds’ efficiency at finding the non-devalued food. When allowed one trial to learn locations of two food rewards that were hidden beneath lightly weighted flaps, birds performed better than chance at locating a food reward. However, they did not preferentially search for the non pre-fed food, suggesting that they were unable to recall both food type and location in combination. Zebra finches made fewer errors when tested on the one-trial task using more heavily weighted flaps than with lightly weighted flaps; there was equivocal evidence that they remembered which food type was hidden where on this task. When given repeated exposures to the locations of the two food rewards, finches located a food reward more accurately than on the one-trial tasks, and were also more likely to recall the locations of the different food types. In this foraging paradigm, experience and motivation may have influenced the birds’ performance.     

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.     

Lesions of the caudate nucleus selectively impair "reference memory" acquisition in the radial maze

Groups of Long-Evans rats with bilateral lesions of the caudate nucleus, sham lesions, or no lesions were given one trial per day in an eight-arm radial maze. The same four maze arms were baited on each trial. The remaining four arms never contained food. Optimal performance required animals to enter each of the baited arms only once on each trial and to avoid entering the arms in the unbaited set. Rats with caudate lesions learned to enter each of the baited arms only once on each trial. However, these rats were severely impaired in learning to avoid entering the arms in the unbaited set. Implications for dual-memory theories are discussed.     

The stability and flexibility of spatial categories

Four experiments examined the flexibility and stability with which children and adults organize locations into categories based on their spatiotemporal experience with locations. Seven-, 9-, 11-year-olds, and adults learned the locations of 20 objects in an open, square box. During learning, participants experienced the locations in four spatiotemporally defined groups (i.e., four sets of nearby locations learned together in time). At test, participants attempted to place the objects in the correct locations without the aid of the dots marking the locations. Children and adults displaced the objects toward the corners of the box consistent with the organization they experienced during learning, suggesting that they used spatiotemporal experience to organize the locations into groups. Importantly, the pattern of organization remained the same following a long delay for all four age groups, demonstrating stability. For adults, this organization shifted after a new pattern of spatiotemporal experience was introduced, suggesting that adults' categories based on spatiotemporal experience are quite flexible. Children only exhibited flexibility when the new pattern of spatiotemporal organization was consistent with available perceptual cues, demonstrating that the flexibility with which children organize locations into categories is intimately tied to both remembered and perceptual sources of information.     

Inferences about guessing and knowing by chimpanzees (Pan troglodytes)

The visual perspective-taking ability of 4 chimpanzees (Pan troglodytes) was investigated. The subjects chose between information about the location of hidden food provided by 2 experimenters who randomly alternated between two roles (the guesser and the knower). The knower baited 1 of 4 obscured cups so that the subjects could watch the process but could not see which of the cups contained the reward. The guesser waited outside the room until the food was hidden. Finally, the knower pointed to the correct cup while the guesser pointed to an incorrect one. The chimpanzees quickly learned to respond to the knower. They also showed transfer to a novel variation of the task, in which the guesser remained inside the room and covered his head while the knower stood next to him and watched a third experimenter bait the cups. The results are consistent with the hypothesis that chimpanzees are capable of modeling the visual perspectives of others.     

Tracking and inferring spatial rotation by children and great apes

Finding hidden objects in space is a fundamental ability that has received considerable research attention from both a developmental and a comparative perspective. Tracking the rotational displacements of containers and hidden objects is a particularly challenging task. This study investigated the ability of 3-, 5-, 7-, and 9-year-old children and great apes (chimpanzees, bonobos, gorillas, and orangutans) to (a) visually track rotational displacements of a baited container on a platform and (b) infer its displacements by using the changes of position or orientation of 3 landmarks: an object on a container, the color of the containers, and the color of the platform on which the containers rested. Great apes and 5-year-old and older children successfully tracked visible rotations, but only children were able to infer the location of a correct cup (with the help of landmarks) after invisible rotations. The ability to use landmarks changed with age so that younger children solved this task only with the most explicit marker on the baited container, whereas older children, particularly 9-year-olds, were able to use landmark orientation to infer correct locations.     

Simultaneous temporal and spatial processing

Rats searched for food that was contingent on time and place in an open field. One location was active at a time, the active location moved in a clockwise direction after each reward, and each location was repeated several times on each daily session. When a location was active, the first response after a fixed interval produced food. The intervals associated with each of the four locations were consistently 60, 30, 30 and 60 sec. For independent groups, inspecting an inactive location had no consequence (n = 7) or reduced the amount of food delivered at the active location (n = 6). The rates of inspecting active and inactive locations increased before the associated intervals elapsed, with preferential responding at the active locations. Rates of anticipation at active locations failed to superimpose when plotted as a function of proportional time. Simultaneous temporal and spatial processing contributed to the failure of proportional timing.     

Tactics to obtain a hidden food item in chimpanzee pairs (Pan troglodytes)

Five dyads of chimpanzees were tested in a competitive situation, as a pilot study to examine chimpanzees' understanding of conspecifics' knowledge. A human experimenter baited one of five containers in an outdoor enclosure. Chimpanzee A (witness) could see where the food was hidden, while chimpanzee B (witness-of-witness) could not see the baited place but could observe the chimpanzee A watching the food being hidden. Then the two were released into the enclosure. This procedure was repeated for a certain number of days along with a control condition in which neither could see the baited location. The witness-of-witness developed tactics to forestall the witness in two pairs. The witness misled the witness-of-witness by taking a route to an empty container in several cases. These episodes might represent examples of deception. Tactics and counter-tactics thus developed through the interaction between the witness and the witness-of-witness, illustrating the high social intelligence of chimpanzees. An examination of the changes in tactics suggests a possibility that the witness-of-witness understands the witness's knowledge of the location of hidden food. Accepted after revision: 22 May 2001 Electronic Publication     

Rats form cognitive maps from spatial configurations of proximal arm cues in an enclosed 4-arm radial maze

Rats were trained to select a final, remaining baited arm following a 6- to 10-min delay following their entries into three experimenter-selected baited arms in an enclosed 4-arm radial maze containing different proximally cued arms. Rats’ accuracy in selecting the remaining baited arm was disrupted when the spatial configuration of arm cues was randomly varied over trials following initial training with one configuration in Experiment 1. In Experiment 2, the same rats acquired this task with the original and a new configuration of the same arm cues when each consistently occurred at a specific time of day (one in the morning, the other in the afternoon). Randomly varying the temporal presentations of these configurations following acquisition disrupted rats’ choice accuracy more within the new than the original configuration. Other rats in Experiment 3 learned this task with two configurations containing different types of arm cues (full arm inserts, objects at the arm entrances). When required to relearn this task with recombined configurations of pairs of arm cues from of each configuration, only rats presented pairs of arms arranged differently from that in their original configurations were unable to reacquire the task. Together these results support a cognitive map hypothesis more than a proximal arm cue list hypothesis. These findings were discussed in terms of recent versions of cognitive map theory (Benhamou, 1998; Poucet, 1993) and the possible limits of such processing (Roberts, 2001).     

Apes' use of iconic cues in the object-choice task

In previous studies great apes have shown little ability to locate hidden food using a physical marker placed by a human directly on the target location. In this study, we hypothesized that the perceptual similarity between an iconic cue and the hidden reward (baited container) would help apes to infer the location of the food. In the first two experiments, we found that if an iconic cue is given in addition to a spatial/indexical cue - e.g., picture or replica of a banana placed on the target location - apes (chimpanzees, bonobos, orangutans, gorillas) as a group performed above chance. However, we also found in two further experiments that when iconic cues were given on their own without spatial/indexical information (iconic cue held up by human with no diagnostic spatial/indexical information), the apes were back to chance performance. Our overall conclusion is that although iconic information helps apes in the process of searching hidden food, the poor performance found in the last two experiments is due to apes' lack of understanding of the informative (cooperative) communicative intention of the experimenter.     

Capuchin monkeys (Cebus apella) use positive, but not negative, auditory cues to infer food location

Nonhuman primates appear to capitalize more effectively on visual cues than corresponding auditory versions. For example, studies of inferential reasoning have shown that monkeys and apes readily respond to seeing that food is present (“positive” cuing) or absent (“negative” cuing). Performance is markedly less effective with auditory cues, with many subjects failing to use this input. Extending recent work, we tested eight captive tufted capuchins (Cebus apella) in locating food using positive and negative cues in visual and auditory domains. The monkeys chose between two opaque cups to receive food contained in one of them. Cup contents were either shown or shaken, providing location cues from both cups, positive cues only from the baited cup, or negative cues from the empty cup. As in previous work, subjects readily used both positive and negative visual cues to secure reward. However, auditory outcomes were both similar to and different from those of earlier studies. Specifically, all subjects came to exploit positive auditory cues, but none responded to negative versions. The animals were also clearly different in visual versus auditory performance. Results indicate that a significant proportion of capuchins may be able to use positive auditory cues, with experience and learning likely playing a critical role. These findings raise the possibility that experience may be significant in visually based performance in this task as well, and highlight that coming to grips with evident differences between visual versus auditory processing may be important for understanding primate cognition more generally.     

Facilitation of learning spatial relations among locations by visual cues: Implications for theoretical accounts of spatial learning

Human participants searched in a real environment or interactive 3-D virtual environment open field for four hidden goal locations arranged in a 2 × 2 square configuration in a 5 × 5 matrix of raised bins. The participants were randomly assigned to one of two groups: cues 1 pattern or pattern only. The participants experienced a training phase, followed by a testing phase. Visual cues specified the goal locations during training only for the cues 1 pattern group. Both groups were then tested in the absence of visual cues. The results in both environments indicated that the participants learned the spatial relations among goal locations. However, visual cues during training facilitated learning of the spatial relations among goal locations: In both environments, the participants trained with the visual cues made fewer errors during testing than did those trained only with the pattern. The results suggest that learning based on the spatial relations among locations may not be susceptible to cue competition effects and have implications for standard associative and dual-system accounts of spatial learning.     

Bonobos, chimpanzees, gorillas, and orang utans use feature and spatial cues in two spatial memory tasks

Animals commonly use feature and spatial strategies when remembering places of interest such as food sources or hiding places. We conducted three experiments with great apes to investigate strategy preferences and factors that may shape them. In the first experiment, we trained 17 apes to remember 12 different food locations on the floor of their sleeping room. The 12 food locations were associated with one feature cue, so that feature and spatial cues were confounded. In a single test session, we brought the cues into conflict and found that apes, irrespective of species, showed a preference for a feature strategy. In the second experiment, we used a similar procedure and trained 25 apes to remember one food location on a platform in front of them. On average, apes preferred to use a feature strategy but some individuals relied on a spatial strategy. In the final experiment, we investigated whether training might influence strategy preferences. We tested 21 apes in the platform set-up and found that apes used both, feature and spatial strategies irrespective of training. We conclude that apes can use feature and spatial strategies to remember the location of hidden food items, but that task demands (e.g. different numbers of search locations) can influence strategy preferences. We found no evidence, however, for the role of training in shaping these preferences.     

Facilitation of learning spatial relations among locations by visual cues: generality across spatial configurations

Spatial pattern learning permits the learning of the location of objects in space relative to each other without reference to discrete visual landmarks or environmental geometry. In the present experiment, we investigated conditions that facilitate spatial pattern learning. Specifically, human participants searched in a real environment or interactive 3-D 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 three groups: Pattern Only, Landmark + Pattern, or Cues + Pattern. All participants experienced a Training phase followed by a Testing phase. Visual cues were coincident with the goal locations during Training only in the Cues + Pattern group whereas a single visual cue at a non-goal location maintained a consistent spatial relationship with the goal locations during Training only in the Landmark + Pattern group. All groups were then tested in the absence of visual cues. Results in both environments indicated that participants in all three groups learned the spatial configuration of goal locations. The presence of the visual cues during Training facilitated acquisition of the task for the Landmark + Pattern and Cues + Pattern groups compared to the Pattern Only group. During Testing the Landmark + Pattern and Cues + Pattern groups did not differ when their respective visual cues were removed. Furthermore, during Testing the performance of these two groups was superior to the Pattern Only group. Results generalize prior research to a different configuration of spatial locations, isolate spatial pattern learning as the process facilitated by visual cues, and indicate that the facilitation of learning spatial relations among locations by visual cues does not require coincident visual cues.     

Social effects on rat spatial choice in an open field task

Pairs of rats foraged in trials either together or separately in an open field apparatus for pellets hidden in discreet locations in a 5 × 5 matrix. Trial duration was either 1 or 4 min. The tendency to choose locations that had earlier been visited by another rat was examined by comparing the choices made in the presence and absence of the other rat. Rats avoided visits to locations that had earlier been visited by the other rat, but only if they had also visited the same location earlier in a short duration trial. This pattern of results is consistent with earlier findings from experiments using the radial arm maze. Furthermore, when rats did visit locations that had earlier been visited by the other rat in a long duration trial, they tended to be locations that had been visited longer ago by the other rat than would be expected. This suggests a forgetting function for social memories. These data provide evidence that the social memory reported in earlier studies using the radial-arm maze can be found in other experimental paradigms and that at least some of its properties are common in the two paradigms.