Memory systems in the rat: effects of reward probability,context, and congruency between working and reference memory

The interaction of working and reference memory was studied in rats on an eight-arm radial maze. In two experiments, rats were trained to perform working memory and reference memory tasks. On working memory trials, they were allowed to enter four randomly chosen arms for reward in a study phase and then had to choose the unentered arms for reward in a test phase. On reference memory trials, they had to learn to visit the same four arms on the maze on every trial for reward. Retention was tested on working memory trials in which the interval between the study and test phase was 15 s, 15 min, or 30 min. At each retention interval, tests were performed in which the correct WM arms were either congruent or incongruent with the correct RM arms. Both experiments showed that congruency interacted with retention interval, yielding more forgetting at 30 min on incongruent trials than on congruent trials. The effect of reference memory strength on the congruency effect was examined in Experiment 1, and the effect of associating different contexts with working and reference memory on the congruency effect was studied in Experiment 2.     

Anisomycin impairs long-term working memory in a delayed alternation task

A long-term temporal component of working memory of rats trained on the radial maze has been shown to be susceptible to disruption by the protein synthesis inhibitor, anisomycin. It is not clear whether protein synthesis played a role in working memory because accurate performance on the radial maze required the storage of a large amount of information, or because the information was to be held in store for relatively long periods of time. This experiment tested these hypotheses by assessing the effect of anisomycin on choice accuracy in a comparatively simple spatial delayed alternation task. Results indicate that under the present training conditions, protein involvement in working memory is related more to the length of the retention interval than to the amount of information retained.     

Wistar rats with high versus low rearing activity differ in radial maze performance

Substantial work has shown that rats although identical in stock, sex, age, and housing conditions can differ considerably in terms of behavior and physiology. Such individual differences, which can be detected by specific behavioral screening tests, are rather stable, that is, they probably reflect a behavioral disposition or trait. Here, we asked whether and how such differences might affect performance in a task of spatial learning and memory, the radial maze. As in our previous work, we used the degree of rearing activity in a novel open field to assign male adult outbred Wistar rats into those with high versus low rearing activity (HRA/LRA rats). They were then tested in a plus-maze for possible differences in anxiety-related behavior. Finally, and most importantly, they were food deprived and underwent maze training using an 8-arm radial maze with four non-baited and four baited arms. One of these arms consistently contained a larger bait size than the other three. In the open field, HRA rats not only showed more rearing behavior, but also more locomotor activity than LRA rats. In the plus-maze, HRA rats again showed more locomotion, but did not differ in open arm time or percentage of open arm entries, that is, conventional measures of anxiety-related behavior. In the radial maze, HRA rats consistently needed less time to consume all pellets than LRA rats, which was due to faster locomotion on the arms and less time spent at the food pits (especially in baited arms) of HRA rats. During the initial days of training, they were also more efficient in obtaining all food pellets available. Furthermore, HRA rats visited more arms and made relatively less reference memory errors than LRA rats. This allowed them to forage food quickly, but was paralleled by more working memory errors than in LRA rats. In general, working memory errors were more frequent in the arm with the large bait size, but there were no indications that HRA and LRA rats responded differently dependent on reward size. Finally, LRA rats lost slightly more weight than HRA rats during the period of food deprivation. These results are discussed with respect to the role of cognitive and motivational mechanisms, which as subject-inherent factors can contribute substantially to inter-individual variability in the radial maze.     

Validation of a rodent model of episodic memory

Episodic memory consists of representations of specific episodes that happened in the past. Modeling episodic memory in animals requires careful examination of alternative explanations of performance. Putative evidence of episodic-like memory may be based on encoding failure or expectations derived from well-learned semantic rules. In Experiment 1, rats were tested in a radial maze with study and test phases separated by a retention interval. The replenishment of chocolate (at its study-phase location) depended on two factors: time of day (morning vs. afternoon) and the presence or absence of chocolate pellets at the start of the test phase. Because replenishment could not be decoded until the test phase, rats were required to encode the study episode. Success in this task rules out encoding failure. In Experiment 2, two identical mazes in different rooms were used. Chocolate replenishment was trained in one room, and then they were asked to report about a recent event in a different room, where they had no expectation that the memory assessment would occur. Rats successfully answered the unexpected question, ruling out use of expectations derived from well-learned semantic rules. Our behavioral methods for modeling episodic memory may have broad application for assessments of genetic, neuroanatomical, neurochemical, and neurophysiological bases of both episodic memory and memory disorders such as those that occur in Alzheimer’s disease.     

Food priming and short-term retention in the delayed alternation task

The delayed alternation task, with rats as subjects, was used to assess the effects of a priming food reward on subsequent retention of a reinforced target location in a T maze. Subjects received a pretrial feeding, followed by a forced-choice rewarded entry into one goal box of the maze (the “cuing” run). Following a delay interval (5–60 s), the subjects were allowed to choose either goal, with reward available only in the one not entered on the cuing run. Priming significantly reduced such alternation after 30- and 60-s delays (Experiment 1), whereas administering the reward following the cuing run had no effect on choice behavior (Experiment 2). In the third study, prefeeding had a decremental effect when the following cuing run was reinforced, but no decrement occurred when reinforcement was omitted on the cuing run. The results suggest that food reward enhances retention of spatial information, but priming reduces this effect.     

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.     

Discrimination of what,when, and where: Implications for episodic-like memory in rats

We investigated the discrimination of what, when, and where in rats (n = 5) using an eight-arm radial maze. Rats received daily training consisting of forced-choice visits to four baited arms, one of which was randomly chosen each day to contain chocolate (Phase 1). In Phase 2, all eight arms were available. After a short (30 min) retention interval (RI), the four arms that were not available in Phase 1 provided food. After a long (4 h) RI, the four remaining arms plus the arm containing chocolate provided food (i.e., the chocolate arm replenished). The rats visited the chocolate location after the long RI more than after the short RI. Next, chocolate was paired with lithium chloride, and subsequent testing used the long RI. The rats visited the chocolate location less after the taste-aversion manipulation than in previous training, demonstrating knowledge of what, when, and where. Implications for episodic-like memory are discussed.     

Place and direction learning in a spatial T-maze task by neonatal piglets

Pigs are a valuable animal model for studying neurodevelopment in humans due to similarities in brain structure and growth. The development and validation of behavioral tests to assess learning and memory in neonatal piglets are needed. The present study evaluated the capability of 2-week old piglets to acquire a novel place and direction learning spatial T-maze task. Validity of the task was assessed by the administration of scopolamine, an anti-cholinergic drug that acts on the hippocampus and other related structures, to impair spatial memory. During acquisition, piglets were trained to locate a milk reward in a constant place in space, as well as direction (east or west), in a plus-shaped maze using extra-maze visual cues. Following acquisition, reward location was reversed and piglets were re-tested to assess learning and working memory. The performance of control piglets in the maze improved over time (P < 0.0001), reaching performance criterion (80 % correct) on day 5 of acquisition. Correct choices decreased in the reversal phase (P < 0.0001), but improved over time. In a separate study, piglets were injected daily with either phosphate-buffered saline (PBS; control) or scopolamine prior to testing. Piglets administered scopolamine showed impaired performance in the maze compared to controls (P = 0.03), failing to reach performance criterion after 6 days of acquisition testing. Collectively, these data demonstrate that neonatal piglets can be tested in a spatial T-maze task to assess hippocampal-dependent learning and 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.     

Choosing schedules of signaled appetitive events over schedules of unsignaled ones

Two experiments were completed allowing albino rats to choose between signaled and unsignaled reward conditions. These experiments examined the effects on preference of (1) response dependent versus response-independent reward and, (2) food pellets versus chocolate milk as the reward. All subjects preferred the signaled condition over the unsignaled condition, whether exposed to response-dependent, or to response-independent delivery of rewards. Preference was controlled most effectively by presenting both the signal itself and the correlated stimulus identifying the signaled condition. The signal presented alone (Extinction 3) controlled preference more effectively than did the stimulus correlated with the signaled condition (Extinction 2). The second experiment showed that the quality of the reinforcer (pellets and chocolate milk) did not affect preference for signaled reward since all subjects preferred the signaled condition at levels comparable to those observed in Experiment 1, with food pellets. These results, along with others, argue against species differences, response-dependency, and reinforcer quality as variables affecting the direction of preference.     

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.     

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.     

The Effect of Retention Interval Task Difficulty on Young Children's Prospective Memory: Testing the Intention Monitoring Hypothesis

The current study examined the impact of retention interval task difficulty on 4- and 5-year-olds’ prospective memory (PM) to test the hypothesis that children periodically monitor their intentions during the retention interval and that disrupting this monitoring may result in poorer PM performance. In addition, relations among PM, working memory, theory of mind (ToM), and 2 types of planning were investigated. Children (N = 64) were randomly assigned to an easy or difficult filler task during the retention interval prior to the PM task. Five-year-olds outperformed 4-year-olds on the PM task, and children receiving the easy filler task outperformed those receiving the difficult filler task. Further, working memory, planning, and ToM were positively associated with PM for children receiving the difficult filler task but not for children receiving the easy filler task. Findings are interpreted with respect to the predictions of the intention monitoring hypothesis as well as the multiprocess framework of PM.     

Damage to the retrosplenial cortex produces specific impairments in spatial working memory

Mounting evidence indicates that the retrosplenial cortex (RSP) has a critical role in spatial navigation. The goal of the present study was to characterize the specific nature of spatial memory deficits that are observed following damage to RSP. Rats with RSP lesions or sham lesions were first trained in a working memory task using an 8-arm radial arm maze. Rats were allowed 5 min to visit each arm and retrieve food pellets and a 5-s delay was imposed between arm choices. Consistent with previous research, rats with RSP damage committed more errors than controls. In particular, RSP-lesioned rats committed more errors of omission (failing to visit an arm of the maze), but there were no lesion effects on errors of commission (revisiting an arm). Neither group of rats exhibited a turn bias (i.e., always turning a certain direction when choosing an arm). At the end of the training phase of the experiment, both groups had reached asymptote and committed very few errors. In the subsequent test phase, a longer delay (30-s) was imposed during some sessions. Both control and RSP-lesioned rats continued to make few errors during sessions with the standard 5-s delay, but RSP-lesioned rats were impaired at the 30-s delay and committed more errors of commission, consistent with an increase in taxing spatial working memory.     

Hippocampal stimulation disrupts spatial working memory even 8 h after acquisition

The present experiment used hippocampal stimulation to determine the temporal gradient of consolidation of spatial working memory. Rats were trained to perform a spatial working memory task on a radial maze with 12 arms. Each rat went to the ends of 6 arms to obtain a food reward. After 8 h, the rat chose among all the arms to find the ones not previously chosen (and consequently still having food). During some test sessions, the hippocampus was stimulated electrically either at a current level just high enough to produce an electrophysiological seizure, or at a current level below this seizure threshold. Stimulation occurred at one of five intervals (0 to 8 h) following the completion of the first six choices. During other test sessions, the hippocampus was not stimulated. After seizure stimulation, the number of retroactive errors (returning to arms chosen prior to stimulation) increased at all delay intervals; the number of proactive errors (returning to arms chosen after stimulation) increased only with the delay of 8 h. Subthreshold stimulation had no influence on either type of error. These results indicate that normal hippocampal function is required for the maintenance of spatial information in working memory, and that the time course of consolidation of this information is significantly greater than that seen in other types of memory, or consolidation may not take place at all.     

The use of tokens as rewards and tools by chimpanzees (Pan troglodytes)

This paper explores the effectiveness of token rewards in maintaining chimpanzees (Pan troglodytes) in working at intellectually costly tasks, and studies the "saving" behavior of the subjects, investigating the factors that can condition it. Two experiments were run. Tokens were introduced as rewards in a matching-to-sample task and used as exchange tools for food by three adult female chimpanzees. Subjects' performances were maintained at constant high levels of accuracy, suggesting that the tokens were almost equivalent to direct food rewards. The results also showed the emergence of saving behavior. The subjects spontaneously saved the tokens during the matching-to-sample task before exchanging them for food. The chimpanzees also learned a new symbolic discrimination task, with tokens as the reward. During this learning process a rarely reported phenomenon emerged: one of the subjects showed symmetry, a form of stimulus equivalence. Accepted after revision: 7 August 2001 Electronic Publication     

No functional role of attention-based rehearsal in maintenance of spatial working memory representations

The present study systematically examined the role of attention in maintenance of spatial representations in working memory as proposed by the attention-based rehearsal hypothesis [Awh, E., Jonides, J., & Reuter-Lorenz, P. A. (1998). Rehearsal in spatial working memory. Journal of Experimental Psychology - Human Perception and Performance, 24(3), 780-790]. Three main issues were examined. First, Experiments 1-3 demonstrated that inhibition and not facilitation of visual processing is often observed at the memorized location during the retention interval. This inhibition was caused by keeping a location in memory and not by the exogenous nature of the memory cue. Second, Experiment 4 showed that inhibition of the memorized location does not lead to any significant impairment in memory accuracy. Finally, Experiment 5 connected current results to the previous findings and demonstrated facilitation of processing at the memorized location. Importantly, facilitation of processing did not lead to more accurate memory performance. The present results challenge the functional role of attention in maintenance of spatial working memory representations.     

Enhanced long-term and impaired short-term spatial memory in GluA1 AMPA receptor subunit knockout mice: Evidence for a dual-process memory model

The GluA1 AMPA receptor subunit is a key mediator of hippocampal synaptic plasticity and is especially important for a rapidly-induced, short-lasting form of potentiation. GluA1 gene deletion impairs hippocampus-dependent, spatial working memory, but spares hippocampus-dependent spatial reference memory. These findings may reflect the necessity of GluA1-dependent synaptic plasticity for short-term memory of recently visited places, but not for the ability to form long-term associations between a particular spatial location and an outcome. This hypothesis is in concordance with the theory that short-term and long-term memory depend on dissociable psychological processes. In this study we tested GluA1^−/− mice on both short-term and long-term spatial memory using a simple novelty preference task. Mice were given a series of repeated exposures to a particular spatial location (the arm of a Y-maze) before their preference for a novel spatial location (the unvisited arm of the maze) over the familiar spatial location was assessed. GluA1^−/− mice were impaired if the interval between the trials was short (1 min), but showed enhanced spatial memory if the interval between the trials was long (24 h). This enhancement was caused by the interval between the exposure trials rather than the interval prior to the test, thus demonstrating enhanced learning and not simply enhanced performance or expression of memory. This seemingly paradoxical enhancement of hippocampus-dependent spatial learning may be caused by GluA1 gene deletion reducing the detrimental effects of short-term memory on subsequent long-term learning. Thus, these results support a dual-process model of memory in which short-term and long-term memory are separate and sometimes competitive processes.     

Spatial working memory effects in early visual cortex

The present study investigated how spatial working memory recruits early visual cortex. Participants were required to maintain a location in working memory while changes in blood oxygen level dependent (BOLD) signals were measured during the retention interval in which no visual stimulation was present. We show working memory effects during the retention period in early visual cortex which were retinotopically organized in the sense that evoked BOLD responses were specific to the position of the remembered location on an imaginary clock. We demonstrate that this activity is similar to activity observed in conditions in which participants have to direct spatial attention to the same location. We suggest that during the retention interval modulation of neurons coding the remembered location evoke a baseline shift, providing converging evidence for the notion that spatial working memory may use spatial attention as a rehearsal mechanism.     

Acute Ethanol Administration Impairs Spatial Performance While Facilitating Nonspatial Performance in Rats

Acute ethanol administration produces learning and memory impairments similar to those found following lesions to the hippocampal system in rats. For example, both ethanol and hippocampal lesions impair performance on spatial learning and memory tasks while sparing performance on many nonspatial learning and memory tasks. Lesions to the hippocampal system can also alter the nature of the information that the animal uses to guide its behavior, from using spatial information to using individual cues. In the present experiment, rats were trained, while sober, to navigate on an eight-arm radial arm maze to a specific arm for food reward. During training, the rewarded arm was always in the same specific location and contained well-defined cues. After the rat learned the task, a memory test was conducted under different doses of ethanol (0.0 g/kg [saline control], 1.0, 1.5, or 2.0 g/kg, intraperitoneal). On the test day the maze was rotated so that the cued arm was 90 degrees to the right of its original position. During testing, intact rats showed a significant bias to approach the place where they had been previously rewarded, even though the cue was no longer located there. Acute ethanol administration dose dependently reduced approaches to the rewarded place. However, ethanol administration did not result in increases in random choices; rather, it resulted in a dose-dependent increase in approaches to the cued arm, now in a new location. These results extend previous research showing that acute ethanol administration and lesions to the hippocampal system produce similar effects on learning and memory in rats.