Social working memory: Memory for another rat's spatial choices can increase or decrease choice tendencies

In two experiments using a radial-arm maze, pairs of rats made choices among eight maze locations, each containing a large quantity of one of two food types. The choices made by 1 rat affected the choices made by the other rat. Under most conditions, visits by 1 rat increased the tendency of the other rat to subsequently choose that maze location. However, the effect depended on the quality of the food available in a particular location. When it was possible for the rats to observe each other on the maze arms and a rat had experienced that a location contained the less preferred food type, a previous visit to that location by the foraging partner decreased the tendency to visit that location. These effects are attributed to working memory for the spatial choices of another rat, and they indicate that memory produced by a rat’s own visit to a maze location is integrated with memory for the behavior of another rat to determine spatial choice     

Rat spatial memory: Resistance to retroactive interference at long retention intervals

An attempt was made to disrupt memory for spatial information by interpolating a task of high similarity to the to-be-remembered task during a long retention interval. Rats were trained in an 8-arm maze in which choosing each arm without repetition was the optional strategy. A 4-h delay was imposed between the 4th and 5th choices. At various times during the retention interval, the rats ran a second identical maze located in another room. No evidence of retroactive interference was observed. In the second experiment, the rat was required to remember the interpolated spatial task during the retention test. This was accomplished by allowing the rat to make four choices in the first maze and then, after a variable period of time, four choices in the second maze. Four hours after exposure to each maze, retention was tested. Choice accuracy on the retention tests was high and equivalent on both mazes. Requiring the rat to remember which arms it had visited in a second maze did not impair memory for the first maze. These results demonstrate that rats can segregate spatial memories established in different contexts with considerable proficiency.     

The existence and extent of spatial working memory ability in honeybees

Honeybees foraged from six locations, each of which was baited with sugar solution prior to each experimental trial. Under a variety of conditions, bees exhibited a small but reliable tendency to avoid revisits to locations that they had visited earlier during the experimental trial. These results replicate those of Brown and Demas (1994), who concluded that bees use working memory to discriminate previously visited locations from those not yet visited. The present experiments included procedures that allowed alternatives to this explanation to be more completely ruled out. The extent of spatial working memory performance exhibited by honeybees in these experiments appears to be limited by a process other than working memory capacity, perhaps the ability of bees to discriminate among several locations in close proximity to one another.     

In the dark II: spatial choice when access to extrinsic spatial cues is eliminated

Rats were tested in a specially constructed radial-arm maze that eliminated access to extramaze visual cues and allowed any effects of intramaze cues to be controlled. Despite this, choice accuracy was controlled by the spatial location of previously visited arms. Part of this control was attributed to vestibular or kinesthetic cues. This conclusion was corroborated by the finding that when explicit visual cues were moved from their standard (trained) spatial locations to novel locations, control of spatial choices was completely disrupted. The latter finding indicates that cues intrinsic to the rat (kinesthetic or vestibular information) and cues extrinsic to the rat (visual stimuli) operate in an integrated fashion.     

Spatial memory in rats: Resistance to retroactive interference

Treatments that interfere with animals’ short-term retention (e.g., in delayed matching-to-sample) were studied using a spatial memory task. Rats performed in an eight-arm radial maze in which choosing each arm without repetition was the optimal behavior. Performances were interrupted between fourth and fifth choices for a delay of 15 sec to 2 min. A variety of events occurring during the delay interval did not disrupt memories for prior choices (as assessed by the accuracy of postdelay choices). The ineffective treatments included variations in visual and auditory environments, removal from the maze, food consumed during the delay, a distinctive odor added to the maze, or combinations of these manipulations. Additionally, performance on another spatial task (a four-arm maze) during the delay between Choices 4 and 5 did not interfere with performance in the eight-arm maze. These findings suggest that rats’ memories for spatial locations are immune to retroactive interference, at least within the range of conditions reported, and that the rat can successfully segregate memories for spatial locations established in different contexts.     

Spatial patterns and memory for locations

Rats obtained food from the tops of vertical poles in a 5 × 5 matrix of locations. On each trial, the baited locations formed one of the two possible exemplars of a checkerboard spatial pattern. During training, locations that had been visited earlier in the trial were indicated by a visual cue. Following training, performance with and without the visual cues was compared. Spatial choices were controlled by the checkerboard spatial pattern. The visual cues enhanced the ability of rats to avoid revisits of locations. However, the visual cues did not enhance control by the spatial pattern, as would be expected if the same spatial memories were involved in avoidance of revisits and coding the location of baited locations.     

Spatial pattern learning in the radial arm maze

Rats experienced a spatial pattern of baited and unbaited arms in an eight-arm radial maze. The spatial pattern remained constant over trials, but the spatial locations that were baited varied unpredictably. Although there was no evidence of control by the spatial pattern during free choice training trials, the rats’ ability to locate baited arms in forced choice test trials was superior to that of animals in a control condition for which maze arms were not baited in a consistent spatial pattern. This is consistent with the results of experiments showing that spatial choices by rats in a pole box maze are controlled by abstract spatial patterns.     

Time-place learning in the eight-arm radial maze

Rats (n=4) searched for food on an eight-arm radial maze. Daily 56-min sessions were divided into eight 7-min time zones, during each of which a different location provided food; locations were randomized across subjects before training. The rats obtained multiple pellets within each time zone by leaving and returning to the correct location. Evidence that the rats had knowledge about the temporal and spatial features of the task includes the following. The rats anticipated locations before they became active and anticipated the end of the currently active locations. The rats discriminated currently active locations from earlier and forthcoming active locations in the absence of food transition cues. After the rats had left the previously active location, they visited the next correct location more often than would be expected by chance in the absence of food transition cues. The rats used handling or opening doors as a cue to visit the first location and timed successive 7-min intervals to get to subsequent locations.     

Rats remember not wisely but too well

Rats were trained in a three-alternative spatial delayed matching-to-sample task in a starburst maze. Samples consisted of rewarded forced choices of one arm, and retention was indicated by rats’ returning to that arm after a 90-sec delay. If a rat made an error on its first choice, it was returned to the start compartment and allowed a second choice. Unlike in previous experiments with this task, all three arms were available during the animals’ second choices. The rats tended to perseverate in their second choices by returning to the arm that they had erroneously visited on their first choice. In Experiment 1, the accuracy of second choices following first-choice errors was below chance during the first block of sessions, when a 90-sec delay intervened between the first choice and the second choice, and at chance during the second block of sessions, when a short (5–6 see) delay intervened between first and second choices. In Experiment 2, long-delay and short-delay sessions were randomly presented to naive subjects. Similar results were obtained. In both experiments, the tendency to repeat the erroneous first choice was greater when long delays separated the two choices than when short delays were used. The results suggest that rats make their first-choice errors because they erroneously encode or remember the location of the sample and that they base their second choices on the same erroneous-memory. The increase in perseveration at long delays implies some kind of rehearsal-like mechanism that slows forgetting of the memory controlling the first choice.     

Retroactive inhibition in rat spatial memory

Two experiments were carried out in which rats first were given four forced choices on an eight-arm radial maze, then were given interpolated maze experiences, and finally were given a free choice retention test on the first maze. In Experiment 1, interpolated experiences consisted of forced choices made on one, two, or three other mazes, each placed in a different room. Retroactive inhibition (RI) was not found with one and two interpolated mazes but was found with three interpolated mazes. In Experiments 2a and 2b, an attempt was made to produce RI within a single context by using two mazes placed side by side or on top of one another and by using interpolated forced choices that were different, random, or the same with respect to forced choices onMaze 1. These conditions failed to yield any evidence of RI. In Experiment 2c, forced choices were followed by interpolated direct placements on the same maze on different, random, or the same maze arms, and retention tests revealed RI under these conditions. It was concluded that rats encode memories of specific places visited in space and that RI will arise only if (1) memory is greatly overloaded with interpolated information or (2) an interpolated visit is made to exactly that position in space to which an animal must travel in order to achieve a correct choice on the retention test.     

Characteristics of pigeons’ spatial working memory in an open-field task

Although pigeons seem to require special training before they will display accurate spatial working memory in radial-arm mazes, they readily show accurate working memory for recently visited feeder locations in an open-field analog of the radial maze. In this task, pigeons forage among sites located on the floor of an open room, with no constraints on the path they take between sites. Experiment 1 suggested that pigeons’ working memory for recently visited sites is facilitated if they are permitted to develop a stable reference memory “map” of the location of the sites with respect to landmarks in the room: Pigeons for which the landmarks remained constant from day to day displayed more accurate working memory than did pigeons for which the landmarks were rearranged between daily trials. The second experiment investigated the durability of pigeons’ working memory, using a forced-choice procedure. Accuracy remained high for retention intervals of up to 32 min, but dropped significantly with a 2-h delay.     

Further studies of pigeons’ spatial working memory in the open-field task

In Experiments 1 and 2, pigeons’ spatial working memory in an open-field setting was examined under conditions that differed in terms of working-memory load (number of sites visited prior to a retention test) at various delays between initial choices and the retention test. In Experiment 1, pigeons were tested under two conditions of memory load (three or five sites visited prior to the delay) and two delay intervals (15 and 60 min). Accuracy declined as a function of delay but was not affected significantly by memory load. In Experiment 2A, pigeons were tested under three conditions of memory load (two, four, or six sites visited prior to the delay). In separate phases, the delay was 2, 15, and 60 min. Accuracy was not affected by memory load in any of these phases. In Experiment 2B, three conditions of memory load (two, four, or six sites visited prior to the delay) were tested at two delays (2 and 60 min) within a test phase. Accuracy declined with increasing delay, but memory load again had no significant effects. These results are inconsistent with previous suggestions that pigeons’ retention of spatial information may decline as working-memory load is increased. In Experiment 3, cue-manipulation tests confirmed that pigeons’ choice behavior in the open-field task is controlled by memory for previously visitad room locations.     

Performance of honeybees in analogues of the rodent radial maze

The performance of individual honeybees pretrained to forage at a laboratory window was studied in three rudimentary analogues of the radial maze designed for the study of short-term spatial memory in rats. A linear arrangement of three targets was used in Experiment 1, a triangular arrangement of three targets in Experiment 2, and a rectangular arrangement of four targets in Experiment 3, with reward only for the first response to each of the targets presented on any given trial. Several systematic patterns of responding were observed, with no indication that the choices made by the animals were influenced by memory of targets recently visited.     

Pigeons’ spatial memory: V. Proactive interference in the delayed matching of key location paradigm occurs only under restricted conditions

In the delayed matching of key location procedure, pigeons must remember the location of the sample key in order to choose correctly between two comparison keys. The deleterious effect of short intertrial intervals on key location matching found in previous studies suggested that pigeons’ short-term spatial memory is affected by proactive interference. However, because a reward expectancy mechanism may account for the intertriai interval effect, additional research aimed at demonstrating proactive interference was warranted. In Experiment 1, matching accuracy did not decline from early to late trials within a session, a finding inconsistent with a proactive interference effect. In Experiment 2, evidence suggestive of proactive interference was found: Matching was more accurate when the locations that served as distractors and as samples were chosen from different sets. However, this effect could have been due to differences in task difficulty, and the results of the two subsequent experiments provided no evidence of proactive interference. In Experiment 3, the distractor on Trialn was either the location that had served as the sample on Trialn ? 1 or one that had been a sample on earlier trials. Matching accuracy was not inferior on the former type of trial. In Experiment 4, the stimuli that served as samples and distractors were taken from sets containing 2, 3, 5, or 9 locations. Matching accuracy was no worse, actually slightly better, with smaller memory set sizes. Overall, these findings suggested that pigeons’ memory for spatial location may be immune to proactive interference. However, when, in Experiment 5, an intratrial manipulation was used, clear evidence of proactive interference was found: Matching accuracy was considerably lower when the sample was preceded by the distractor for that trial than when it was preceded by the sample or by nothing. Possible reasons why interference was produced by intratrial but not intertrial manipulations are discussed, as are implications of these data for models of pigeons’ short-term spatial memory.     

Retroactive interference in rat radial maze performance: The role of point of delay interpolation and the similarity and amount of interpolated material

The conditions necessary for producing retroactive interference (RI) were examined in a 12-arm radial maze. Rats were first given either three or nine forced choices in a to-be-remembered maze. During a 2-h delay, they received one or two trials in a second 12-arm maze, located either in a different room or the same room as the to-be-remembered maze. During the postdelay memory test, RI from the interference trials was produced only when nine choices had been made in the to-be-remembered maze and two interference trials had been conducted during the delay interval. RI was not found when only three forced choices had to be retained or after a single interference trial. The similarity between the interpolated and to-be-remembered mazes had no effect on choice accuracy. It was concluded that two conditions are required for the production of RI in the radial maze. First, a “large amount” of information should be resident in working memory. Second, a substantial number of interpolated trials or choices must be made during the delay.     

In the dark: Spatial choice when access to spatial cues is restricted

The cognitive mechanisms involved in spatial choice when access to visual cues is restricted were examined in three experiments using male rats. A specially constructed radial-arm maze was used, in which extramaze visual cues could not be perceived from the central arena, but could be perceived from the maze arms. Choices were very accurate when the maze was not rotated during each trial, but inaccurate when the maze was rotated. This suggests that intramaze cues were involved in the control of choices. However, the data clearly showed that choices were not simply controlled by intramaze cues. Rather, control by intramaze cues interacted in a more complex manner with representations of the spatial locations of goals. Such spatial representations were involved in the control of choice despite the absence of visual spatial cues at the time choices were made.     

Evidence for a shift in the choice criterion of rats in a 12-arm radial maze

Rats were trained in a standard 12-arm radial maze task. Following training, each trial consisted of a sequence of 2, 4, 6, 8, or 10 choices, followed by a 15-min delay, which then was followed by a choice between a single arm and a response manipulandum mounted in the center of the maze. An arm visit was reinforced if the arm had not been visited prior to the delay, whereas a manipulandum response was reinforced if the arm had been visited. It was found that rats are relatively more likely to reject arms by responding to the manipulandum following a delay occurring late in the choice sequence. This indicates that the choice criterion used by rats in the radial maze becomes more strict as the choice sequence progresses. Such a process provides an alternative explanation for some of the data recently reported by Cook, Brown, and Riley (1985).     

Monkey auditory list memory: tests with mixed and blocked retention delays

A rhesus monkey was tested in an auditory list memory task with blocked and mixed retention delays. Each list of four natural or environmental sounds (from a center speaker) was followed by a retention delay (0, 1, 2, 10, 20, or 30 sec) and then by a recognition test (from two side speakers). The monkey had been tested for 12 years in tasks with blocked delays. An earlier (4 years prior) blocked-delay test was repeated, with virtually identical results. The results from the mixed-delay test were likewise similar. Thus, the peculiarities of blocked-delay testing, such as delay predictability or differences in list spacing, apparently do not alter this monkey’s memory for auditory lists. It is concluded from this and other evidence that the monkey’s serial position functions reflect mnemonic processes that change with changes in retention delay and are not artifacts of the blocked-delay procedure. The nature of the monkey’s auditory memory is discussed.     

More evidence of robust spatial associative memory in the pigeon,Columba livia

Willson and Wilkie (1993) developed a novel procedure for assessing pigeons’ memory for the spatial location of food. Only one of four locations (consisting of an illuminated pecking key and grain feeder) provided food each day. Over days, different locations provided food. The pigeons’ tendency to revisit the location that was profitable on the previous day demonstrated memory for food-spatiallocation associations over a period of 24 h, retention longer than previously reported for this species. This basic finding was replicated and extended in three experiments. Experiment 1 demonstrated that location-food discriminations were also remembered well when established with successive rather than concurrent procedures. Experiment 2 demonstrated that pigeons can remember two location-food associations over 24 h. Experiment 3 showed that the discrimination training inherent in this paradigm is important for retention; retention was impaired when only the rewarded location was presented. Overall, this research suggests that cross-species differences in spatial memory performance may be due to quantitative rather than qualitative differences in the memory system underlying performance.     

Exploring the limits of spatial memory in rats,using very large mazes

In Experiment 1, rats foraged for food in six successive phases with 8, 16, 24, 32, 40, and 48 arms attached in random locations to a large radial maze. The percentage of novel choices appeared to be determined more by spatial proximity than by number of arms. In Experiment 2, rats foraged for food in four successive phases with 8, 16, 24, and 48 arms attached to the maze in spread-out or tight configurations. Performance was poor in the tight configurations regardless of the number of arms. Performance was excellent in the 8-arm spread-out condition but declined as 16 and, then again, 24 arms were added. Thus, spatial separation, not number of locations, was the chief determinant of performance in the first two experiments. In Experiment 3, in successive phases, 8, 16, 24, 32, 40, 48, 16, and 8 food towers were set in a circle on the floor, with the spatial separation between adjacent towers held constant at 33 cm. The percentage of novel choices declined as 8 towers became 16 and did not change again with 24, 32, 40, or 48 towers in place but then increased again as 16 towers became 8. In Experiment 4, in successive phases, 8, 16, 24, and 32 food towers were set in a circle, with the spatial separation between adjacent towers held constant at 66 cm. The percentage of novel choices declined as 8 towers became 16 and again as 16 towers became 24 but did not decline further. These data were discussed in terms of the fundamental problems posed by variations in the number of food locations in the pursuit of the limit of spatial memory in rats.