How rats perform spatial working memory tasks: Limitations in the use of egocentric and idiothetic working memory

Rats of the Dark Agouti strain were trained on delayed alternation under conditions that should encourage egocentric working memory. In two experiments a T-maze was set within a cross-maze so that different arms could be used for the sample and test runs. The maze had high opaque side-walls, and testing was conducted in low light levels so that distal visual cues might be eliminated. By rotating the maze 90° between the sample and choice run and by using two identical mazes set side by side it was possible to nullify other spatial strategies. Experiments 1 and 2 showed that rats preferentially used place information, intramaze cues, and direction cues, even though only egocentric or idiothetic (nonmatch-to-turn) working memory could successfully solve every trial. Rats were able to maintain an accurate sense of location within the maze even though distal cues were not visible and the animal was moved between the sample and choice runs. Experiment 2 confirmed that another rat strain (Long-Evans) shows the same learning profiles. Both experiments indicate that rats are very poor at using either egocentric or idiothetic information to alternate, and that retention delays as short as 10 s can eliminate the use of these forms of memory.     

How rats perform spatial working memory tasks: limitations in the use of egocentric and idiothetic working memory

Rats of the Dark Agouti strain were trained on delayed alternation under conditions that should encourage egocentric working memory. In two experiments a T-maze was set within a cross-maze so that different arms could be used for the sample and test runs. The maze had high opaque side-walls, and testing was conducted in low light levels so that distal visual cues might be eliminated. By rotating the maze 90° between the sample and choice run and by using two identical mazes set side by side it was possible to nullify other spatial strategies. Experiments 1 and 2 showed that rats preferentially used place information, intramaze cues, and direction cues, even though only egocentric or idiothetic (nonmatch-to-turn) working memory could successfully solve every trial. Rats were able to maintain an accurate sense of location within the maze even though distal cues were not visible and the animal was moved between the sample and choice runs. Experiment 2 confirmed that another rat strain (Long-Evans) shows the same learning profiles. Both experiments indicate that rats are very poor at using either egocentric or idiothetic information to alternate, and that retention delays as short as 10 s can eliminate the use of these forms of memory.     

Comprehension of human pointing gestures in horses (Equus caballus)

Twenty domestic horses (Equus caballus) were tested for their ability to rely on different human gesticular cues in a two-way object choice task. An experimenter hid food under one of two bowls and after baiting, indicated the location of the food to the subjects by using one of four different cues. Horses could locate the hidden reward on the basis of the distal dynamic-sustained, proximal momentary and proximal dynamic-sustained pointing gestures but failed to perform above chance level when the experimenter performed a distal momentary pointing gesture. The results revealed that horses could rely spontaneously on those cues that could have a stimulus or local enhancement effect, but the possible comprehension of the distal momentary pointing remained unclear. The results are discussed with reference to the involvement of various factors such as predisposition to read human visual cues, the effect of domestication and extensive social experience and the nature of the gesture used by the experimenter in comparative investigations.     

Directed forgetting and directed remembering in visual working memory

A defining characteristic of visual working memory is its limited capacity. This means that it is crucial to maintain only the most relevant information in visual working memory. However, empirical research is mixed as to whether it is possible to selectively maintain a subset of the information previously encoded into visual working memory. Here we examined the ability of participants to use cues to either forget or remember a subset of the information already stored in visual working memory. In Experiment 1, participants were cued to either forget or remember 1 of 2 groups of colored squares during a change-detection task. We found that both types of cues aided performance in the visual working memory task but that observers benefited more from a cue to remember than a cue to forget a subset of the objects. In Experiment 2, we show that the previous findings, which indicated that directed-forgetting cues are ineffective, were likely due to the presence of invalid cues that appeared to cause observers to disregard such cues as unreliable. In Experiment 3, we recorded event-related potentials and show that an electrophysiological index of focused maintenance is elicited by cues that indicate which subset of information in visual working memory needs to be remembered, ruling out alternative explanations of the behavioral effects of retention-interval cues. The present findings demonstrate that observers can focus maintenance mechanisms on specific objects in visual working memory based on cues indicating future task relevance. (PsycINFO Database Record (c) 2012 APA, all rights reserved).     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) discriminate between knowing and not knowing and collect information as needed before acting

Humans use memory awareness to determine whether relevant knowledge is available before acting, as when we determine whether we know a phone number before dialing. Such metacognition, or thinking about thinking, can improve selection of appropriate behavior. We investigated whether rhesus monkeys (Macaca mulatta) are capable of a simple form of metacognitive access to the contents of short-term memory. Monkeys chose among four opaque tubes, one of which concealed food. The tube containing the reward varied randomly from trial to trial. On half the trials the monkeys observed the experimenter baiting the tube, whereas on the remaining trials their view of the baiting was blocked. On each trial, monkeys were allowed a single chance to select the tube containing the reward. During the choice period the monkeys had the opportunity to look down the length of each tube, to determine if it contained food. When they knew the location of the reward, most monkeys chose without looking. In contrast, when ignorant, monkeys often made the effort required to look, thereby learning the location of the reward before choosing. Looking improved accuracy on trials on which monkeys had not observed the baiting. The difference in looking behavior between trials on which the monkeys knew, and trials on which they were ignorant, suggests that rhesus monkeys discriminate between knowing and not knowing. This result extends similar observations made of children and apes to a species of Old World monkey, suggesting that the underlying cognitive capacities may be widely distributed among primates.     

Spatial memory in the rat on a hierarchical maze

Rats were trained and tested on a hierarchical radial maze, which consisted of eight primary alleys radiating from a central platform and three secondary alleys which branched off the end of each primary alley. In four experiments, rats in groups 1, 2, and 3 were tested on maze configurations consisting of one, two, or three secondary alleys, respectively, at the end of each primary alley. In Experiment 1, each group was trained to collect food pellets in the secondary alleys. By the end of training, rats in each group collected all pellets efficiently, with little repetition of entrances into either primary or secondary alleys. In Experiments 2 and 3, tests were carried out which required retention of entrances into secondary alleys, as well as primary alleys. Two trials were run in succession, with selected secondary alleys blocked on trial 1 but open and baited with food on trial 2. Animals in groups 2 and 3 showed very accurate retention of blocked secondary alleys, regardless of variation in pattern and number of alleys blocked. A fourth experiment controlled for the possible use of food cues in Experiments 2 and 3 by rebaiting all secondary alleys between trials 1 and 2. Subjects continued to choose previously blocked alleys on trial 2, thus demonstrating that choice of blocked alleys was based on memory and not on a tendency to approach visual or olfactory food cues. Several findings of these experiments suggest that memories for primary and secondary alley choices are encoded and stored within separate memory systems. Possible coding mechanisms for these systems are discussed with reference to a process of cognitive mapping.     

Working memory theory of hippocampal function needs qualification

To compare the predictive value of "cognitive map" and "working memory" theories of hippocampal function, the performance of rats with dorsal hippocampal lesions was compared to that of control rats in a series of experiments. In Experiment I, experimental rats learned a spatial alternation task with normal ease, but in Experiment II, they were significantly impaired on an elevated 8-arm radial maze. In Experiment III, the performance of the same experimental and control rats was compared on two versions of a 16-arm enclosed radial maze. In the first version, carpet inserts served as cues to mark eight unbaited arms and each of the remaining arms contained one food pellet. While both experimental and control rats successfully avoided the set of cued arms, experimental rats reentered uncued baited arms more frequently than did control rats. In the second version no intramaze cues were provided, but the spatial distribution of baited and unbaited arms remained the same as that used in the first version. In this uncued version, experimental rats both entered unbaited arms and reentered baited arms more frequently than did control rats, i.e., they were impaired in both "reference" and "working" memory. These findings are compatible with the hypothesis that hippocampal lesions result in an impaired capacity to form cognitive maps but they are not compatible with the working memory hypothesis. Furthermore, twelve separate evaluators classed experimental rats as using fewer mapping and more orientation strategies than control rats in the 8-arm maze.     

Those cheating rats: male and female rats use odor trails in a water-escape "working memory" task.

Three-month-old Sprague-Dawley rats were trained on a working memory win-stay (spatial delayed matching-to-sample) water-escape task with the escape platform location the same for all subjects on a given trial, a procedure that maximizes the buildup of an odor trail to the escape platform. In subsequent tests during which the location of the escape platform varied randomly between subjects, the rats, especially the females, while continuing to perform above chance level, made increased errors. Varying the platform location between subjects eliminated odor trail as a nonambiguous cue for locating the escape platform. In a second experiment females performed better than males on a reference memory odor trail discrimination task which involved following the path of like-gender "pathmaker" rats to the escape platform. The relatively poor use of odor trails by the males was associated with a high frequency of choosing a preferred choice section or returning to the choice section selected first on the immediately preceding trial (perseveration). Collectively, the two experiments demonstrate that rats can use either working memory or odor trails to locate an escape platform in a water maze, and that they, especially females, will use odor trails in a working memory task if odor trails are available. Clearly, the location of the escape platform should be varied randomly between subjects in tests of working memory.     

The role of response and reward in spatial memory

Two experiments were conducted to determine the role of the response and of reward in spatial working memory. Rats were initially trained on a four-arm maze to run to the end of each arm for a single pellet of food. On subsequent tests, rats were first placed at the end of one, two, or three arms. In Experiment 1, the arms on which the rat was placed (“placed arms”) had food which the rat was allowed to eat, whereas in Experiment 2 these placed arms did not have food. Following the placements the rat was allowed to choose among the four arms; only unplaced arms contained food. Two measures indicated that the response made a slight but reliable contribution to spatial memory. (a) When a rewarded arm was still available, choice accuracy after placements was less than choice accuracy on tests in which no placements had occurred; this difference diminished over test days. (b) When all four arms had been chosen once, the rats were more likely to go back to a placed arm rather than an unplaced arm. No influence of the presence or absence of food on the placed arms was found. These data demonstrate that the response of running down an arm, but not the reward outcome at the end, had a small influence on the memorability of a visit. Overall, above chance performance in the spatial working memory task was maintained without either running to the arm or obtaining food on it.     

The role of the hippocampus in the retrieval of a spatial location

Based on computational models of the hippocampus, it has been suggested that a possible mechanism for memory retrieval is pattern completion, wherein an autoassociative network recalls previous patterns of activity given noisy or degraded cues. However, there are few behavioral data examining pattern completion per se in the hippocampus. Here, we present a study in which rats were tested on a spatial location retrieval paradigm, each trial of which consisted of a sample and choice phase. During the sample phase, rats were trained to displace an object in one of 15 possible locations to retrieve a food reward and return to the start-box on a cheeseboard maze. The object was then removed and the same location was re-baited for the choice phase. The rats' accuracy in returning to the correct location was recorded. On test trials, visual extramaze cues, vestibular cues, or both were manipulated to assess pattern completion in normal rats. Subjects were then randomly assigned to receive a cortical control, a sham, or a dorsal and ventral hippocampal lesion and were retested on the task. Control and unoperated rats were able to perform the task when visual extramaze or vestibular cues were reliable, but not when they were manipulated. Rats with hippocampal lesions were impaired in the baseline condition, as well as during all manipulations. These results support the hypothesis that the hippocampus supports the retrieval of a spatial location, possibly through a process of pattern completion.     

Rats know when they remember: transfer of metacognitive responding across odor-based delayed match-to-sample tests

Metamemory entails cognitively assessing the strength of one’s memories. We tested the ability of nine Long-Evans rats to distinguish between remembering and forgetting by presenting a decline option that allowed a four-choice odor-based delayed match to sample (DMTS) tests to be by-passed. Rats performed significantly better on tests they chose to take than on tests they were forced to take, indicating metacognitive responding. However, rather than control by internal mnemonic cues, one alternative explanation is that decline use is based on external test-specific cues that become associated with increased rewards overtime. To examine this possibility, we tested rats on three generalization tests in which external contingencies were inconsistent and therefore could not serve as discriminative cues. Rats transferred adaptive use of the decline response in tests that eliminated memory by presenting no sample, increased memory by presenting multiple samples, and both weakened and strengthened memory by varying the retention interval. Further, subjects chose to take or decline the test before encountering the memory test, providing evidence that rats based their metacognitive responding on internal cues rather than external ones. To our knowledge, this is the first robust evidence for metamemory in rats using the DMTS decline-test paradigm in which several possible sources of external stimulus control can be ruled out.     

Memory persistence of rats in a radial maze varies with training procedure

Different estimations of the time-course of spatial working memory have been reported. Some authors found working memory in the radial maze to be relatively long lasting, while others found more rapid exponential decay. In the present experiments it was attempted to account for the conflicting results by investigating the effects of different training procedures. Two types of training were examined under the same circumstances. A group of seven rats was given a series of delayed trials (5, 20, 60, and 120 min). Every delay was repeated at least four times and the delays were presented in an ascending order. The number of errors decreased at every delay except the last one (120 min), where error levels were constant (.50 errors/trial). The good performance was not based on use of intramaze cues or response chaining. In another group of seven rats the same delays were introduced in a quasi-random order and alternated with uninterrupted trials. The number of errors increased exponentially with the length of the delay. However, when this procedure was repeated, the number of errors decreased. These results suggest that training with delayed trials is a major factor to account for the differences in reports of memory persistence in the radial maze.     

On the comparative efficacy of memories and expectancies as cues for choice behavior in pigeons

The same reliable color cues were equally available to different groups of pigeons trained on a delayed conditional simultaneous visual discrimination task. However, for different groups, prechoice and postchoice food or no-food events were programmed in such a way that, theoretically, memories of these events, expectancies of them, both, or neither could also serve as reliable cues for choice. In the case where both prechoice and postchoice food/no-food events were correlated with correct choices, two ways of correlating the prechoice and postchoice events with one another were examined. For synergism subjects, when the prechoice event was food, the postchoice event was also food, and when the prechoice event was no food, the postchoice event was no food; therefore, on a given trial, the operative memory and expectancy were of the same event. For antagonism subjects, when the prechoice event was food, the postchoice event was no food, and vice versa; thus, for these subjects, the memory and expectancy active on a given trial were of opposite events. Expectancies were found to exert significantly greater control over choice behavior than memories. Moreover, antagonism subjects chose significantly less accurately than synergism subjects or than an expectancy only group. A follow-up experiment confirmed this effect. The relevance of these results to various models of memory and expectancy was addressed.     

Visual perspective taking by dogs (Canis familiaris) in a Guesser–Knower task: evidence for a canine theory of mind?

We tested domestic dogs (N = 16) in a Guesser–Knower task in which they chose between possible locations for hidden food indicated by human informants. In four experiments, the perceptual access of the Guesser and Knower to the hidden food baiting was manipulated. When informants had differing perceptual access to the baiting, dogs preferred the location indicated by the Knower from the start of testing (Experiment 1), even when baiting was done by a third experimenter (Experiments 2–3). However, when there was no difference in perceptual access and both informants either knew or did not know the food location, dogs had no preference between the informants (Experiment 4). Controls ruled out alternative explanations in terms of associative learning, unintentional and olfactory cues. Analysis of individual data showed no significant heterogeneity across dogs, and results were not correlated with age or sex. Dogs’ performances were superior to those of nonhuman primates in previous studies. Although a mentalistic explanation is not required, results add to evidence that dogs have a remarkable sensitivity to cues related to humans’ attentional state, which enables them to respond as if they had a functional theory of mind in the Guesser–Knower task with human informants.     

Hamsters' (Mesocricetus auratus) memory in a radial maze analog: the role of spatial versus olfactory cues

The golden hamster's (Mesocricetus auratus) performance on radial maze tasks has not been studied a lot. Here we report the results of a spatial memory task that involved eight food stations equidistant from the center of a circular platform. Each of six male hamsters depleted the food stations along successive choices. After each choice and a 5-s retention delay, the hamster was brought back to the center of the platform for the next choice opportunity. When only one baited station was left, the platform was rotated to evaluate whether olfactory traces guided hamsters' choices. Results showed that despite the retention delay hamsters performed above chance in searching for food. The choice distributions observed during the rotation probes were consistent with spatial memory and could be explained without assuming guidance by olfactory cues. The radial maze analog we devised could be useful in furthering the study of spatial memory in hamsters.     

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.     

The role of the dorsal and ventral hippocampus in olfactory working memory

Olfactory working memory and pattern separation for odor information was assessed in male rats using a matching-to-sample for odors paradigm. The odor set consisted of a five aliphatic acids with unbranched carbon chains that varied from two- to six-carbons in length. Each trial consisted of a sample phase followed by a choice phase. During the sample phase, rats would receive one of five different odors. Fifteen seconds later during the choice phase one of the previous odors was presented simultaneously side by side with a different odor that was based on the number of aliphatic acids that varied in the carbon chains from two- to six-carbons in length and rats were allowed to choose between the two odors. The rule to be learned in order to receive a food reward was to always choose the odor that occurred during the study phase. Odor separations of 1, 2, 3 or 4 were selected for each choice phase and represented the carbon chain difference between the study phase odor and the test phase odor. Once an animal reached a criterion of 80–90% correct across all temporal separations based on 40 trials, rats received a control, dorsal hippocampal, or ventral hippocampal lesion and were retested on the task. On postoperative trials, only the ventral hippocampal lesion group was impaired relative to both control and dorsal hippocampal groups groups. There were no effects on odor pattern separation. All groups of rats could discriminate between the odors. The data suggest that the ventral hippocampus, but not dorsal hippocampus, supports working memory for odor information.     

The role of working memory capacity in autobiographical retrieval: individual differences in strategic search

Remembering previous experiences from one's personal past is a principal component of psychological well-being, personality, sense of self, decision making, and planning for the future. In the current study the ability to search for autobiographical information in memory was examined by having college students recall their Facebook friends. Individual differences in working memory capacity manifested itself in the search of autobiographical memory by way of the total number of friends remembered, the number of clusters of friends, size of clusters, and the speed with which participants could output their friends' names. Although working memory capacity was related to the ability to search autobiographical memory, participants did not differ in the manner in which they approached the search and used contextual cues to help query their memories. These results corroborate recent theorising, which suggests that working memory is a necessary component of self-generating contextual cues to strategically search memory for autobiographical information.     

Memory for Objects and Positions: Delayed Non-matching-to-sample in Storing and Non-storing Tits

An operant delayed-non-matching-to-sample task using computer-presented images was used to test memory for position and object (shape and colour) cues in four species of tit (Parus), two food-storing species (P. palustris and P. ater) and two non-storing species (P. major and P. caeruleus). Both storers and non-storers performed successfully at retention intervals as long as 100 sec on all trial types, and there were no significant differences in performance between the two groups on any of the trial types. Performance by both groups was highest on trials in which both object and position cues were available and poorest on trials when object cues only were relevant. These data do not provide support for the hypothesis that food storers have a better memory for spatial cues than do non-storers.     

Acute pain disrupts prospective memory cue detection processes

Prospective memory refers to the planning, retention, retrieval, and execution of intentions for future behaviours and it is integral to the enterprise of daily living. Although prospective memory relies upon retrospective memory and executive processes often disrupted by pain, limited research has explored the influence of acute or chronic pain on the ability to complete prospective memory tasks. In the present study we investigated the influence of acute pain on prospective memory tasks that varied in their demands on executive processes (i.e., non-focal versus focal prospective memory cues). Complex-span working memory tasks were also administered to examine whether individual differences in working memory capacity moderated any negative impact of pain on prospective memory. Acute pain significantly impaired prospective memory performance in conditions that encouraged non-focal strategic processing of prospective memory cues, but not in conditions that encouraged more spontaneous focal processing. Individual differences in working memory capacity did not moderate the effect of acute pain on non-focal prospective memory. These findings provide new insights into prospective memory dysfunction created by painful experiences.