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.     

Memory for frequency in rats: role of the hippocampus and medial prefrontal cortex

On a radial arm maze rats were tested for frequency memory of specific spatial locations, a task that presumably involves the coding of temporal information. On any trial during the study phase rats were allowed to visit three different spatial locations only once and one spatial location twice. During the test phase the rats were given a choice between a spatial location that had been visited once and spatial location that had been visited twice. The rats were reinforced for selecting the twice-visited spatial location. The number of spatial locations between a repetition (lag) was varied from one to three. After extensive training rats displayed memory for frequency only for a lag of three spatial locations, i.e., they displayed a repetition lag effect. Animals then received control, medial prefrontal cortex, or hippocampal lesions. Upon subsequent retests control rats continued to display frequency memory, but animals with medial prefrontal cortex or hippocampal lesions displayed a marked impairment. These data support the idea that both the hippocampus and medial prefrontal cortex code temporal order information.     

Reward, novelty and spontaneous alternation

It has been suggested that rats' propensity for “win-shift” behaviour in spatial memory and spontaneous alternation tests reflects a species-specific foraging strategy which leads them to avoid places where they have recently found food. An alternative explanation is that they avoid places which are familiar. In three experiments using a T-maze, we evaluated these accounts by comparing the probability of avoiding or re-entering a recently visited arm, as a function of whether food had or had not been found on the previous visit. Each rat received a series of 16 exposure-test trial pairs over 8 days. Neither alternation nor repetition of the previous choice was differentially reinforced. Experiments I and II forced rats to enter a specific arm before a subsequent choice, and differed in the overall probability of reward; in Experiment III all choices were free. In all three experiments the probability of alternating was greater after nonreward than after reward. This effect occurred more reliably on later tests within a day, little difference appearing on earlier tests. It was concluded that there was no evidence for a spontaneous “win-shift” tendency as such, and that these and other results can be adequately accounted for by a combination of exploratory tendencies (spontaneous alternation) and the conventional effects of reward.     

The role of exploration in win-shift and win-stay performance on a radial maze

Win-shift spatial memory tasks in a radial maze reinforce animals for avoiding previously visited rewarded arms; win-stay tasks reinforce them for returning to those arms. Win-shift tasks have generally been found much easier to perform, and this may be explained either in terms of foraging models which postulate avoidance of locations where food has been found, or in terms of the predominance of spontaneous alternation (exploration). Experiment 1 examined spontaneous alternation behavior in the radial maze as a function of whether the first visit to an arm had been rewarded or not, and showed that alternation was more probable after nonreward than after reward in both hungry and thirsty rats (a result which conflicts with the foraging account of the win-shift superiority). Experiment 2 replicated the finding that win-stay discrimination performance was inferior to win-shift. A manipulation (lengthening the delay between initial and test choices) which weakens spontaneous alternation, reduced, but did not reverse, the win-shift superiority. In Experiment 3, in order to eliminate the influence of spontaneous alternation, versions of the win-stay and win-shift tasks were devised in which, unlike the original task, all arms were familiar at the choice trial. Under those conditions win-stay was performed better than win-shift. It is concluded that spontaneous alternation plays a major role in many spatial memory tasks, and that the results can best be accounted for by combining principles of exploration and simple associative learning, without recourse to foraging models.     

Manipulations of start and food locations affect navigation on a foraging task

Rats were able to search multiple food cups in a foraging task and successfully return to a fixed, but not a variable, start location. Reducing the number of food cups to be searched resulted in an improvement in performance in the variable start condition. Performance was better when only one or two food cups had to be visited but was still impaired if the food was not found in the first cup searched. Variable start locations impaired performance when only one food cup had to be searched, if that cup was moved over the table. These findings suggest that there is an interaction between memory processes and the navigational processes that allows an animal to return to its start location after a foraging trip. It appears that a fixed location for the food or the start point of a foraging trip is a necessary precondition for accurate performance.     

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.     

Distinguishing between new and used traces: Differential effects of electroconvulsive shock on memories for places presented and places passed

In a radial maze test of spatial memory, rats enter relatively novel arms while avoiding locations visited a few hours earlier. Certainly, new memories are acquired for arms entered during the retention test. However, the mnemonic consequences of avoiding arms previously entered are not as clearly predicted; old memories might remain unchanged and yet guide behavior, or the use of old memories during a retention test might renew such memories. The possibilities were evaluated in two experiments in which rats performed in a 12-arm radial maze. Each day the arms were randomly sorted into three sets: A, B, C. Each trial began with forced choices of the 4 arms in Set A and ended after 4 hr in an 8-choice test in which the 4 arms not yet visited (Set B) contained food reward. When electroconvulsive shock (ECS) occurred immediately after Set A choices, accuracy during the test was high; when ECS was administered 2 hr after Set A, choices during the test were less accurate. Old memories therefore appear to be more susceptible than new memories to ECS-induced amnesia. In other trials, an extra retention test was given at the mid-point (2 hr) of the retention interval; this 8-choice test consisted of the remaining 4 arms (Set C) and the original 4 arms (Set A). When ECS was administered after the intermediate test, memory for arms in Set A was 2 hr old (but had just been used), while memory for arms in Set C was new (0 hr). The retention test 2 hr later (testing B vs. A or B vs. C) revealed that ECS had an amnestic effect on the recently used memory for arms in Set A but had no effect on the newly acquired memory for arms in Set C. With respect to ECS-induced amnesia, therefore, memories used in a retention test resemble memories that have aged more than memories that have been newly acquired.     

Exposure to Spatial Cues Facilitates Visual Discrimination but Not Spatial Guidance

The performance in a radial-arm maze of two groups of rats with restricted access to extra-maze visual cues was studied. One group received extensive exposure to the visual environment of the maze, whereas the second group was never exposed to the environment, aside from their experience in the maze itself. Spatial exposure resulted in a slightly improved ability to discriminate between previously visited and unvisited spatial locations, which can be explained on the basis of general perceptual learning processes. However, there was no evidence that spatial exposure resulted in control of choices by the spatial relations among the maze locations. These results are discussed in terms of theories of spatial learning which appeal to perceptual learning and cognitive mapping.     

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging. This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).     

A direct assessment of the role of expectation in inhibition of return

An object hidden among distractors can be found more efficiently if previously searched locations are not reinspected. The inhibition-of-return (IOR) phenomenon indexes the tendency to avoid reinspections. Two accounts of IOR, that it is due to inhibition and that it is due to expectation, are generally regarded as incompatible. The relevant evidence to date, however, has been indirect: Inhibition or expectation has been inferred from response times or similar indirect measures. This article reports the first direct measure of IOR, obtained by asking observers to predict the location of the next target in a display containing eight possible locations on an imaginary circle. On any given trial, the previously cued location was chosen less frequently (impairment)--and the opposite location was chosen more frequently (facilitation)--than chance (choice of all other locations was at chance). The impairment is consistent with both inhibition and expectation accounts; the facilitation is consistent only with expectation accounts. This work also shows that inhibition and expectation are not necessarily incompatible: Implementing expectations may entail inhibiting previously cued locations.     

Rapid spatial learning in a velvet ant (<Emphasis Type="Italic">Dasymutilla coccineohirta</Emphasis>)

Spatial learning has been examined in a variety of animals to determine what cues are used to navigate through a complex environment. A common feature of previously studied vertebrates and invertebrates is their need to return to a previously visited site for mating, nesting, foraging or predator avoidance. Velvet ants (Hymenoptera: Mutillidae) are cursorial parasitoids with flightless females that must walk through complex terrain to find ground dwelling host larvae burrows. Velvet ants are not central-place foragers (they do not return to an established nest site) so much of the previous work on spatial learning does not directly apply in this context. It was assumed that females primarily use chemosensory cues for navigation and burrow location instead of visual learning. This study, however, demonstrates that velvet ant females are able to use visual landmarks to find an inconspicuous exit in an aversion-motivation spatial learning task. A significant number of velvet ants learned to locate the exit after seven training trials and went to the previous location of the exit even after the maze had been rotated, showing that landmarks external to the maze were used to learn the escape location.     

The influence of cognitive load on spatial search performance

During search, executive function enables individuals to direct attention to potential targets, remember locations visited, and inhibit distracting information. In the present study, we investigated these executive processes in large-scale search. In our tasks, participants searched a room containing an array of illuminated locations embedded in the floor. The participants’ task was to press the switches at the illuminated locations on the floor so as to locate a target that changed color when pressed. The perceptual salience of the search locations was manipulated by having some locations flashing and some static. Participants were more likely to search at flashing locations, even when they were explicitly informed that the target was equally likely to be at any location. In large-scale search, attention was captured by the perceptual salience of the flashing lights, leading to a bias to explore these targets. Despite this failure of inhibition, participants were able to restrict returns to previously visited locations, a measure of spatial memory performance. Participants were more able to inhibit exploration to flashing locations when they were not required to remember which locations had previously been visited. A concurrent digit-span memory task further disrupted inhibition during search, as did a concurrent auditory attention task. These experiments extend a load theory of attention to large-scale search, which relies on egocentric representations of space. High cognitive load on working memory leads to increased distractor interference, providing evidence for distinct roles for the executive subprocesses of memory and inhibition during large-scale search.     

Integrating information about location and value of resources by white-faced saki monkeys (<Emphasis Type="Italic">Pithecia pithecia</Emphasis>)

Most studies of spatial memory in primates focus on species that inhabit large home ranges and have dispersed, patchy resources. Researchers assume that primates use memory to minimize distances traveled between resources. We investigated the use of spatial memory in a group of six white-faced sakis (Pithecia pithecia) on 12.8-ha Round Island, Guri Lake, Venezuela during a period of fruit abundance. The sakis’ movements were analyzed with logistic regressions, a predictive computer model and a computer model that simulates movements. We considered all the resources available to the sakis and compared observed distances to predicted distances from a computer model for foragers who know nothing about the location of resources. Surprisingly, the observed distances were four times greater than the predicted distances, suggesting that the sakis passed by a majority of the available fruit trees without feeding. The odds of visiting a food tree, however, were significantly increased if the tree had been visited in the previous 3 days and had more than 100 fruit. The sakis’ preferred resources were highly productive fruit trees, Capparis trees, and trees with water holes. They traveled efficiently to these sites. The sakis choice of feeding sites indicate that they combined knowledge acquired by repeatedly traveling through their home range with ‘what’ and ‘where’ information gained from individual visits to resources. Although the sakis’ foraging choices increased the distance they traveled overall, choosing more valued sites allowed the group to minimize intragroup feeding competition, maintain intergroup dominance over important resources, and monitor the state of resources throughout their home range. The sakis’ foraging decisions appear to have used spatial memory, elements of episodic-like memory and social and nutritional considerations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Disruption of delayed memory for a sequence of spatial locations following CA1- or CA3-lesions of the dorsal hippocampus

Axon-sparing neurotoxic lesions of CA1 or CA3 were produced in the dorsal hippocampus to test dissociative lesion effects on spatial working memory for sequential items. Rats were required to remember four different sections sequentially presented on a newly devised maze (i.e., Tulum maze) during a study phase. Each section was cued by a unique object that was specifically associated with each location within the section during the study phase. Following a 15-s delay and during the test phase, rats were required to revisit the location within a section randomly chosen among the previously visited sections in the absence of the cued object. Both CA1 and CA3 lesions similarly disrupted accurate relocation of a previously visited place. However, differential effects of the CA1 and CA3 lesions were observed in serial position curves. CA3-lesions disrupted performance for the first three serial positions, but did not disrupt performance for the last serial position (recency). In contrast, CA1-lesions disrupted performance for all serial positions. The results suggest that temporal separation of spatial memory may depend on the conjoint function of CA1 and CA3 of the hippocampus with a disruption of a spatial pattern completion process following CA3 lesions and a disruption of a temporal pattern separation process following a CA1 lesion.     

Gerbils in space: performance on the 17-arm radial maze.

In Experiment 1 six hungry gerbils received six trials per day on a 17-arm radial maze. During each trial the subjects were allowed to choose freely among the arms, each of which contained a food pellet, until each arm had been visited once or until eight minutes had elapsed. An error was recorded when the subject entered a previously visited arm. The gerbils quickly learned not to re-enter previously visited arms and generally made errors on fewer than 15% of entries, performance comparable to that of the rat and superior to that of other species tested in the radial arm maze. The intertrial-interval duration did not affect accuracy of arm choices during acquisition but did influence asymptotic accuracy. Accuracy did not change systematically over the six trials. A high proportion of arm entries were to nearby arms. Errors occurred most often towards the end of a trial. Odor cues were not important. When the number of trials per day was reduced from six to one, accuracy deteriorated slightly. In Experiment 2 neither the transposition of extramaze cues nor the placement of the maze in a different room had large disruptive effects on accuracy. In Experiment 3 the addition of three explicit intramaze brightness cues aided accuracy, perhaps by permitting the subjects to decompose the large maze into three smaller mazes, although there was no direct evidence that this was the case. Implications of a number of these results for models of spatial maze performance were discussed.     

Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys

An individual’s foraging activity can be influenced by the choices made by nearby conspecifics. The interest shown in the location and characteristics of a feeding patch may depend on the feeding success of a conspecific there, a process that needs to be distinguished from choices guided by rewards to the observer itself. We investigated how rewards for both self and others influence the foraging choices of captive capuchin monkeys (Cebus apella). Thirteen adult capuchins observed familiar female conspecific models explore one of three opaque boxes under three conditions. In the first, there were no rewards available to either monkey; in the second, rewards were available to the model only; and in the third, both monkeys could retrieve a reward. Under all conditions, subjects more often explored the same box as the model than was expected by chance. Thus, without ever receiving a reward themselves or without seeing another receive rewards, subjects’ searches were directed at the box explored by another monkey. The tendency to match the model’s choice increased if the subject was rewarded. We compared these results to control conditions in which the model was either absent, or present but not allowed to demonstrate. Subjects’ located the reward less often in control conditions, than in the experimental conditions. We conclude that extrinsic rewards, while helpful, are not required for partners to influence the foraging choices of capuchins, and that the unrewarded copying of foraging choices demonstrated here may provide the basis for additional social influences on learning. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007)     

Abnormal patterns of maze patrolling in the mutant mouse staggerer

Two experiments describe the abnormal patterns of maze patrolling of adult mutant staggerer mice. The clinical symptoms of this mutant involve exclusively postural and gait abnormalities, apparently due to a disruption of cerebellar architecture leading to a vast reduction in cell numbers and size of this structure. This clinical feature can easily account for the first clear difference reported in these experiments, involving a reduction in the total ambulatory activity in a maze by this mutant. The more interesting result involves different qualitative aspects of the maze patrolling by staggers, compared to normal litter-mate controls. The experiments measured the distribution of subjects' visits to different maze locations, and varied the configuration and the amount of familiarization with the maze. Neither of these factors significantly influenced the basic results. These were the staggerers confined their ambulatory activity to a smaller number of different locations, which were more intensively visited compared to normals, and the staggerers showed a pronounced tendency to return to the place that was most recently visited, compared to a tendency by the normals to avoid that location. It is suggested that these results could be due either to abnormal novelty reactions or to a reduced tendency to pursue an initiated trajectory.     

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.     

Memory for temporal order of new and familiar spatial location sequences: role of the medial prefrontal cortex

Rats with medial prefrontal cortex or sham control lesions were tested on an eight-arm radial maze task to examine memory for the temporal order of a variable and a constant sequence of spatial locations as a function of temporal distance. During the study phase of each trial, rats were allowed to visit each of eight arms once in an order that was randomly selected or fixed for that trial. The test phase required the rats to choose which of two arms occurred earlier in the sequence of arms visited during the study phase. The arms selected as test arms varied according to temporal distance (0, 2, 4, or 6) or the number of arms that occurred between the two test arms in the study phase. For the variable sequences based on new information, control rats showed an increasing temporal distance function. Relative to control rats, medial prefrontal cortex-lesioned rats displayed a temporal order memory deficit across all distances. For the constant sequence based on familiar information, control rats performed well across all distances. Relative to controls, the medial prefrontal cortex-lesioned rats displayed a performance deficit. The results support the idea that the medial prefrontal cortex contributes to mnemonic operations associated with temporal order for new and familiar spatial location information.     

Serial position curves in spatial memory of rats: Primacy and recency effects

Memory for lists of items was tested in rats (N = 18) in an 8-arm radial maze. In Experiment 1 trials consisted of a study phase, in which the rat could freely choose five arms to obtain a food reward, and a test phase in which the animal was presented with a choice between a novel and a previously visited arm. The rat received additional food reinforcement only when visiting the novel arm. The two phases of a trial were separated by a retention interval of 30 sec or of 4, 16 or 60 min. It was found that recall of the five free arm choices was related to the serial position of the previously visited arm. There was a significant recency effect at the 30-sec delay. With longer retention intervals this disappeared, and a significant primacy effect could be observed. In Experiment 2 the same animals were given forced arm entries during the study phase and delays of 30 sec or 4 or 16 min before the test phase. Again, there was a trend towards a recency effect after the shorter delays and a significant primacy effect after the 16-min interval. These results show that, in the recall of lists of spatial items, rats have serial position curves with primacy and recency effects, depending on the length of the retention interval.