Spatial memory for food hidden by rats (Rattus norvegicus) on the radial maze: studies of memory for where,what, and when

Rats (Rattus norvegicus) were allowed to hide food items on an 8-arm radial maze by carrying the items from the center to boxes at the end of each arm. Retrieval tests given after rats had hidden 4 items showed that they selectively returned to the maze arms where food had been hidden (Experiments 1 and 2). When rats were allowed to hide pieces of cheese (refed food) and pretzels (less preferred food) on different arms, they both hid and retrieved cheese before pretzels (Experiments 2-5). In Experiment 6, rats chose between arms where cheese and pretzels were hidden,with cheese degraded at one delay interval but not the other. Together, these experiments indicate memory for what and where but not when.     

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.     

Temporary inactivation of the dorsal entorhinal cortex impairs acquisition and retrieval of spatial information

We tested the effects of temporary inactivation of the dorsal entorhinal cortex on spatial discrimination using a conditioned cue preference (CCP) paradigm. The three phases of the procedure were: pre-exposure: unreinforced exploration of the center platform and two adjacent arms of an eight-arm radial maze; training: rats were confined to the ends of the two arms on alternate days – one arm always contained food and the other never contained food; testing: unreinforced exploration of the center platform and the two arms. Rats that received bilateral infusions of saline into the dorsal entorhinal cortex before the training trials or before the test trial spent significantly more time in the arm that previously contained food than in the arm that never contained food, demonstrating that they had acquired and were able to express information that discriminated between the two adjacent maze arms. In contrast, rats that received bilateral, intra-entorhinal infusions of muscimol, a gamma-aminobutyric acid_a (GABA_a) agonist, before either training or testing spent equal amounts of time in the two arms, indicating that they failed to acquire and were unable to express this information. Interactions between the entorhinal cortex and hippocampus in the acquisition and expression of the information required for this discrimination are discussed.     

The effects of cache modification on food caching and retrieval behavior by rats

Rats cached pieces of cheese on four different arms of an eight-arm radial maze. On a retrieval test given 45 min later, rats learned to return to arms where food was cached before arms where food had not been cached. Tests were then performed in which cache sites on one side of the maze were always modified (pilfered or degraded), but cache sites on the other side of the maze were left intact. In all of these tests, it was found over repeated trials that rats continued to distribute cached food equally between the two sides of the maze. Measures of the order in which arms were visited showed no caching preference but a preference in food retrieval for the side of the maze where food caches were not altered. These findings suggest that rats’ caching behavior is not affected by its consequences.     

Chunking versus foraging search patterns by rats in the hierarchically baited radial maze

Rats were exposed to a radial maze containing six black smooth arms and six wire-grid-covered arms and a striped 'exit arm' in experiment 1. The probability of a black or grid arm being baited (5/6 vs 1/6) with sunflower seeds was associated with its proximal cue for some rats (the Relevant Arm Cue group) but not for others (the Irrelevant Arm Cue group). All rats could terminate a trial and receive a highly preferred morsel of apple by entering the exit arm only after having sampled all six seed-baited arms. Relevant Arm Cue rats usually chose some arms from the more densely baited set before choosing an arm from the less densely baited set and made fewer reentries than Irrelevant Arm Cue rats. Although such clustered, higher choice accuracy in the Relevant Arm Cue group corresponds to human clustered, better recall of verbal items from lists hierarchically organized by categories, these rats did not similarly exhaustively retrieve items (arm locations). That is, when required to terminate a trial by entering the 'exit' arm for an apple morsel after having sampled all seed-baited arms, both groups were equally unable to withhold making nonrewarded premature exits. This nonexhaustive foraging search pattern was maintained in the next two experiments in which the radial maze was reduced to three black and three grid arms along with the striped 'exit' arm and in which black and grid arm cues were paired with number of seeds (eight or one) in an arm for Relevant Arm Cue rats. Although Relevant Arm Cue rats displayed perfect clustering by entering all eight-seeded arms before a one-seeded arm, they made more premature exits and reentries into eight-seeded arms in experiment 2 or when forced to enter all eight-seeded arms in experiment 3 than did Irrelevant Arm Cue rats. These foraging tendencies prevent accurate estimations of the amount of information (i.e., arm locations) rats can 'chunk'. Electronic Publication     

Stimulus control of spatial behavior on the eight-arm maze in rats

Rats were trained on an eight-arm, elevated radial maze in a large cylindrical chamber where extramaze stimuli could be manipulated. The first experiment indicated that rats could use extramaze stimuli to locate the arms if such stimuli were available, whereas they performed less effectively and tended to employ response chaining if these stimuli were not available. The second experiment demonstrated that maze performance was disrupted by transposition of the stimuli but was relatively unaffected by rotation of the same stimuli. The third experiment suggested that the disruptive effect of stimulus transposition might be due to a “resetting” process elicited by the alteration in the configuration of the stimuli after stimulus transposition. These results suggest that when extramaze stimuli are available, rats tend to use such stimuli in a configurational manner to locate the arms rather than as a list of items processed independently of their spatial relationships to each other.     

Dorsal hippocampus function in learning and expressing a spatial discrimination

Learning to discriminate between spatial locations defined by two adjacent arms of a radial maze in the conditioned cue preference paradigm requires two kinds of information: latent spatial learning when the rats explore the maze with no food available, and learning about food availability in two spatial locations when the rats are then confined in one arm with food and the other with no food. Previous research showed that a functional dorsal hippocampus is not required for latent learning. The present experiments show that it is required for learning about food availability, and during retrieval of both types of information.     

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.     

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.     

Role of context in perceptual learning in maze discriminations

Three experiments with rats in a maze examined the effects of pre-exposure to the relevant discriminative stimuli (rubber and sandpaper-covered maze arms) or the extra-maze context (the maze was surrounded either by black curtains or by variety of extra-maze landmarks) on the learning of a discrimination between rubber and sandpaper arms. In Experiment 1, pre-exposure to the extra-maze context facilitated subsequent discrimination learning. Experiments 2 and 3 showed that pre-exposure to rubber and sandpaper arms facilitated subsequent discrimination learning only when these cues were presented in the same context during pre-exposure and discriminative training. Taken together, the results are consistent with the hypothesis that a major cause of perceptual learning is the latent inhibition of stimuli or features common to the two discriminative stimuli, and that such latent inhibition may be disrupted by a radical change of context.     

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.     

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.     

Residential-maze behavior of spontaneously hypertensive rats

Spontaneously hypertensive rats (SHR) exhibit elevated levels of ambulation after transfer to a novel environment compared to the Wistar-Kyoto rat (NR). The present experiment compared long-term activity of SHR and NR in a residential maze to determine whether the SHR exhibit elevated levels of locomotor activity under undisturbed, baseline conditions in addition to enhanced reactivity to stimuli. The SHR were much more active visiting more arms of the maze than the NR during the initial hours following transfer to the maze, and during hours around dark onset and light onset. However, the SHR also exhibited higher levels of activity than the NR under baseline conditions. While the NR visited the arm containing food more frequently than other arms, the SHR exhibited no such preference. These data show that both stimulus-induced and basal levels of ambulation are increased in the SHR compared to its normotensive genetical counterpart.     

Vasopressin disrupts radial-maze performance in rats

The memory enhancing properties of vasopressin, observed in active and passive avoidance procedures, could derive from its influence on central systems, but may also be mediated by its endocrinological properties. Very little is known about the effects of vasopressin on behavior in procedures other than the active and passive avoidance paradigms. The present experiments were designed to assess the effects of vasopressin on behavior observed in the eight-arm radial maze. In Experiment I, male Wistar rats (N = 7), which had been extensively trained to collect food from all eight arms in a radial maze, were subcutaneously injected with different doses of vasopressin 5 min before the start of the session (0.00, 1.25, 3.75, and 6.25 micrograms/kg). In Experiment II, another group of male Wistar rats (N = 7) received the same doses of vasopressin after having been extensively trained to collect food from four of the eight arms. In both experiments, subjects spent more time in the maze as the dose of vasopressin was increased. Vasopressin also disrupted performance by preventing the subjects from visiting all of the baited arms in the maze. Performance thus decreased, not because of the fact that vasopressin interfered with memory processes, but because of the fact that it produced behavioral inhibition. Thus, if vasopressin affects memory processes, such effects are likely to be mediated through vasopressin's actions on endocrine and behavioral systems, rather than through a direct action on the neural substrate underlying memory functioning.     

Effects of scopolamine on repeated acquisition of radial-arm maze performance by rats.

Rats repeatedly acquired the performance of selecting only the four baited arms in an automated eight-arm radial maze, with the arms containing food pellets randomly assigned prior to each session. During each 14-trial (trial: obtain all four pellets) daily session, the number of errors (selecting nonbaited arms or repeating arm selections) showed a within-session decline, and choice accuracy for the first four arm selections showed a positive acceleration across trials for all rats. An index-of-curvature statistic, calculated for total errors, was used to quantify both the within- and between-session improvement of performance. Scopolamine (0.03 to 0.3 mg/kg, ip), but not methylscopolamine (0.3 mg/kg), reduced the accuracy of the first four selections of each trial and increased total within-session errors for all rats. Session times also were increased by scopolamine. An examination of within-session accuracy showed only slight signs of improvement at the higher dosages of scopolamine. The results indicate that behavior in transition states maintained by reinforcement contingencies in the radial maze is similar to that maintained by extended chained schedules, despite the fact that some of the stimuli controlling behavior in the maze are absent at the moment behavior is emitted.     

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.     

Algorithmic responding on the radial maze in rats does not always imply absence of spatial encoding

Two experiments were conducted to determine whether consistent algorithmic response patterning on 8- and 10-arm versions of the radial maze is independent of spatial encoding. On the 8-arm version well-trained hooded rats were tested in darkness, after maze rotation that rendered room cues ambiguous with respect to arm positions, or with room cues unsystematically relocated. Ambiguous maze rotation was also used with well-trained subjects on the 10-arm version. If algorithmic patterning is a learned, non-spatial strategy, animals using it consistently ought not to have been affected by changes in the spatial layout of the test environment, and the type of pattern used by each subject would have remained constant. On the 8-arm radial maze, responses were most often made to arms 2 or 3 from that just visited. In many animals patterns were interchangeable, switching occurring between preferred angles of turn from day to day. Performance fell when animals were tested in darkness and upon ambiguous maze rotation early (but not later) in training. Testing in darkness increased the angle through which animals turned when responding, perhaps due to the disturbance of intramaze cue use. On the 10-arm maze the “consecutive arm” pattern was used persistently by several animals and appeared to protect their performance from disruption by ambiguous maze rotation. Animals not using rigid patterning were adversely affected. However, on both mazes animals using patterning correctly identified maze arms that had been omitted from otherwise patterned choice sequences. Animals adopted continuous patterning only when spatial encoding had been established. Response patterning appears to serve a mnemonic function and in rats complements rather than replaces the use of a spatial representation of the environment. It was concluded that a complex, flexible relationship exists between spatial functioning and its expression via motor responses.     

High ambient temperature reduces rate of body-weight loss produced by wheel running

This study examined the effect of ambient temperature (AT) on the relationship between activity and weight loss. Compared with a neutral AT of 21 degrees C, high ATs of 27-29 degrees C produced a slower rate of weight loss in rats given 1.5-hr food access and 22.5-hr running-wheel access in a standard activity-based anorexia (ABA) procedure (Experiments 1 and 2). The high AT did not affect food intake or wheel running in Experiment 1, but did reduce running in Experiment 2. Switching from neutral to high AT had only a transient effect on weight loss when wheel access was maintained (Experiment 2) but resulted in less weight loss when wheel access was prevented (Experiment 3). Giving rats only 3 hr of wheel access each day at a neutral AT also produced substantial weight loss, but less if for the rest of each day they were maintained at a high AT (Experiment 4).     

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

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

How does the ecological foraging behavior of desert kangaroo rats (Dipodomys deserti) relate to their behavior on radial mazes?

Experiment 1 showed that laboratory-reared desert kangaroo rats, like domestic Norway rats, efficiently search for food on a radial arm maze (RAM) by avoiding revisiting arms within a trial. By placing an RAM on the floor so the animals could approach food from any direction, Experiment 2 tested whether efficient search by kangaroo rats was based on tactics of distance minimizing, central-place foraging, trail following, or meandering. In contrast to the dominant trail-following tactic of domestic Norway rats (Hoffman, Timberlake, Leffel, & Gont, 1999), kangaroo rats tended to distance minimize, whether maze arms were present or not. Experiment 3 indicated that kangaroo rats treated a floor configuration of eight food cups as two patches of four, based on beeline travel between patches and meandering within them. We conclude that similar performance in an elevated RAM by different species can be based on different tactics, and we suggest that a laboratory apparatus can be used to cast light on niche-related mechanisms.