Rats form cognitive maps from spatial configurations of proximal arm cues in an enclosed 4-arm radial maze

Rats were trained to select a final, remaining baited arm following a 6- to 10-min delay following their entries into three experimenter-selected baited arms in an enclosed 4-arm radial maze containing different proximally cued arms. Rats’ accuracy in selecting the remaining baited arm was disrupted when the spatial configuration of arm cues was randomly varied over trials following initial training with one configuration in Experiment 1. In Experiment 2, the same rats acquired this task with the original and a new configuration of the same arm cues when each consistently occurred at a specific time of day (one in the morning, the other in the afternoon). Randomly varying the temporal presentations of these configurations following acquisition disrupted rats’ choice accuracy more within the new than the original configuration. Other rats in Experiment 3 learned this task with two configurations containing different types of arm cues (full arm inserts, objects at the arm entrances). When required to relearn this task with recombined configurations of pairs of arm cues from of each configuration, only rats presented pairs of arms arranged differently from that in their original configurations were unable to reacquire the task. Together these results support a cognitive map hypothesis more than a proximal arm cue list hypothesis. These findings were discussed in terms of recent versions of cognitive map theory (Benhamou, 1998; Poucet, 1993) and the possible limits of such processing (Roberts, 2001).     

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     

Response biases do not underlie the radial maze deficit in rats with mediodorsal thalamus lesions

Previous results indicating that radial maze performance in animals with mediodorsal thalamic lesions is deficient cannot exclude the possibility that these impairments are due to altered motor mechanisms (response biases). The present study sought to eliminate this potentially confounding variable by using a procedure which tests memory for serial position. This procedure involved experimenter-controlled arm entry (number and order) on a radial arm maze. Following this sequence, animals were presented with one previously entered arm along with an arm not yet visited on that trial. Avoidance of the previously entered arm constituted memory for the prior sequence. Thus, this task represents a form of a win-shift or nonmatching-to-sample task. Seven animals were given ibotenic acid lesions of the mediodorsal nucleus and nine others were given sham operations; 2 weeks later testing in the above procedure was conducted. Results indicated that, although control subjects could differentiate between entered and unentered arms without difficulty, animals with lesions were unable to exhibit this distinction. Much of their memory for arms previously entered in a sequence was at chance level, regardless of the placement of the tested arm in the sequence. Some tendency toward increased errors with longer sequences of arm entries was noted. This may indicate that animals with lesions were susceptible to proactive interference from previous choices. Regardless, even without the opportunity to develop or exhibit response biases, animals lesioned in the mediodorsal nucleus were unable to perform this win-shift task reliably. Thus, discrimination among maze arms is impaired after lesion of the mediodorsal nucleus and this impairment is independent of the motor response patterns which emerge during solution of a conventional radial maze task.     

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.     

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.     

Golden hamsters on the eight-arm maze in light and darkness: The role of dead reckoning

This paper examines whether golden hamsters can rely on dead reckoning (getting positional information from updated signals generated during locomotion) on an eight-arm maze. Two groups of hamsters were tested: Group L under ordinary room light, Group D in darkness. To enhance the role of dead reckoning, each subject could climb from its own home cage onto the central platform of the maze. In a first experimental phase (15 trials), the L subjects learned to master the maze through developing a locomotor rule (arm chaining) after three to four trials. The D subjects developed arm chaining less readily and fluctuated more in their performance than did the L subjects. In a second experimental phase (15 trials), four arms were blocked at the beginning of each trial. In both experimental groups the performance decreased, yet remained well above chance level. Success and arm chaining were positively correlated in Phase 1 and negatively correlated with success in Phase 2. We assume that in Phase 2 the L subjects switched to the predominant use of visual cues, and the D subjects to dead reckoning.     

Spontaneous alternation behavior in hamsters

Male and female golden hamsters spontaneously alternated successive entries of T-maze arms (derived from a + − maze) rather than body turns during a series of eight consecutive trials except when not confined to the arm chosen on each trial. Only unconfined males failed to alternate on their first opportunity. Confinement to an entered arm for 30 seconds had no effect on females but increased alternation in males. Increasing the visual discriminability of the arms had no effect on alternation in either sex. It was concluded that spontaneous alternation behavior in hamsters depended upon whether or not they were confined to a chosen arm and their sex. It is possible that the phenomenon was escape-related.     

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

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

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.     

Stimulus perseveration in a water maze following exposure to controllable and uncontrollable shock

When placed in a water-filled maze, mice display a pronounced preference for the illuminated over the nonilluminated arm of the maze. Exposure to inescapable shock increased the time spent in the illuminated arm of the maze, and decreased the frequency of entries into the nonilluminated arm. When animals that had received shock entered the nonilluminated arm they exhibited more activity per second than nonstressed animals. Controllability over the stressor enhanced the preference for the illuminated arm; however, the contribution of this variable was dependent on the number of shock trials mice received. Following 180 escapable or inescapable shock presentations the preference for the illuminated arm was enhanced. The propensity to approach the illuminated arm declined following a greater number (360) of escapable shock trials, while the preference for the illuminated arm did not decline in mice that received inescapable shock. Both escapable and inescapable shock were also found to produce a transient disruption of discrimination performance in a task where animals were required to emit a contraprepared response (swim to dark), whereas these treatments were without effect on performance of the highly prepared response of approaching the illuminated arm. It is provisionally suggested that enhancement of the perseveration represents an innate response to stressful stimuli, but as animals learn mastery over the response contingencies, the persistence in adopting such a response strategy wanes. Moreover, despite the differential effects of escapable and inescapable shock on the perseverative tendency, discrimination accuracy may not be differentially affected by these treatments in a task where acquisition progresses quickly and where explicit cues are associated with the correct and incorrect arms of the maze.     

Spatial learning and memory in the tortoise (Geochelone carbonaria)

A single tortoise (Geochelone carbonaria) was trained in an eight-arm radial maze, with the apparatus and general procedures modeled on those used to demonstrate spatial learning in rats. The tortoise learned to perform reliably above chance, preferentially choosing baited arms, rather than returning to arms previously visited on a trial. Test sessions that examined control by olfactory cues revealed that they did not affect performance. No systematic, stereotyped response patterns were evident. In spite of differences in brain structure, the tortoise showed spatial learning abilities comparable to those observed in mammals.     

Spatial memory in rats under restricted viewing conditions

In a procedure devised by J. A. Walker and D. S. Olton (Learning and Motivation, 1979, 10, 73–84), rats were placed on two arms of a four-arm radial maze and then were placed in the center of the maze to test how accurately they could choose the alleys on which they had not been placed. In three experiments, the conditions under which animals viewed the environment from the arms were varied. In Experiment 1, both the extent of spatial view and the exposure time were varied factorially in a within-subjects design; animals viewed the environment down a tunnel or had a 180° or 360° view, and subjects were allowed to view the environment for either 2 or 20 sec. In Experiment 2, a between-subjects design was used, in which different groups of subjects were tested repeatedly under either the tunnel, 180°, or 360° conditions. Both experiments showed that animals could avoid the arms previously visited at no better than a chance level of accuracy in the tunnel viewing condition but could perform with progressively better accuracy at the 180 and 360° viewing conditions. Animals also were more accurate in Experiment 1 after viewing for 20 sec than after viewing for 2 sec. Experiment 3 involved a procedure in which restricted viewing conditions were used both during arm placements and testing. Animals tested under tunnel viewing eventually achieved above-chance performance with this procedure, but did not exceed chance as rapidly as groups tested with 45 and 90° views of the environment. These results suggest that animals can learn about their position in a spatial environment through observation and that an animal's ability to locate its position is directly related to the extent of the surrounding environment it can see and the length of time it is allowed to look. The implications of these findings for list and map hypotheses of spatial memory representation are discussed.     

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.     

Serial position curves in rats: automatic versus effortful information processing

Rats were trained to remember lists of five arms on an Olton eight-arm radial maze. A forced-choice memory recognition test procedure was used which required the animal to choose between an arm previously visited during the study phase of a trial and an arm not visited. To receive additional food reinforcement, 10 animals were required to return to the previously visited arm (win-stay) and 10 animals were required to choose the novel, unvisited arm (win-shift). In this way, a direct comparison was made between the serial position curves (SPCs) generated by win-stay trained and win-shift trained animals. The results indicated that only win-stay trained animals produced the classical U-shaped SPC, which included significant primacy and recency effects. Win-shift subjects showed only recency effects. These findings are discussed in terms of differential processing requirements for the two procedures. It is suggested that the win-stay rule necessitates relatively more effortful, elaborative processing than does the win-shift rule, which is used automatically.     

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.     

Effects of opiate antagonists on spatial memory in young and aged rats

The effects of post-training opiate antagonist administration on spatial memory were assessed in young and aged male Long Evans rats. In Experiment I rats were trained to visit each arm of an eight-arm radial maze once in a session to obtain a food reward placed at the end of each arm. During training aged rats required significantly more trials to achieve criterion performance when compared to young mature rats. However, administration of the opiate antagonist naloxone (2.0 mg/kg) immediately after each training trial did not significantly alter the rate of achieving accurate performance in either age group. In Experiment II young and aged rats that were previously trained to a comparable criterion on the radial maze were tested on the same maze apparatus in novel spatial environments. When animals were exposed to novel spatial information, the effects of post-trial opiate antagonists were examined using a within-subjects counter-balanced design. In Experiment IIa naloxone (2 mg/kg) enhanced the performance of both young and aged rats. In Experiment IIB naltrexone (1.0 mg/kg) was found to have a comparable effect of enhancing the performance of both age groups. In addition, in Experiment IIb a significant age-related deficit was found in rats tested in novel spatial environments. These results indicate that opiate antagonists are capable of improving memory for new spatial information in both young and aged rats on a task that is sensitive to behavioral deficits during normal aging.     

Chunking by Proximal Arm Cues Facilitates Rats′ Performance in the Radial Maze

Three experiments showed that training rats to chunk a 16-arm radial maze into striped and wire mesh (gridded) arms facilitates their spatial working memory for arm locations. Rats were trained to visit eight unblocked baited arms of a 16-arm radial maze (half-maze run) and then were exposed to the complete maze to sample the remaining eight baited arms (whole-maze run). The initially exposed eight arms were either all striped or all gridded on alternating trials for half the rats (Arm Cue Relevant, ACR group). The remaining rats (Arm Cue Irrelevant, ACI group) received a mixture of striped and gridded arms on their half-maze runs. Following this phase of segmented trials, all rats were exposed only to all 16 arms over a series of trials in the first two experiments. In the third experiment, the initial eight arms were either all striped or all gridded on alternating trials for all rats. During some second, whole-maze runs, however, all arms contained the same proximal cue. ACR rats made fewer reentries than ACI rats in all phases of all experiments. This difference was maintained over increasing delays between half- and whole-maze runs in the first experiment, changes in arm cue and blocking configurations in the second experiment, and removal of differential arm cues in the third experiment.     

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.     

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.     

Social effects on rat spatial choice in an open field task

Pairs of rats foraged in trials either together or separately in an open field apparatus for pellets hidden in discreet locations in a 5 × 5 matrix. Trial duration was either 1 or 4 min. The tendency to choose locations that had earlier been visited by another rat was examined by comparing the choices made in the presence and absence of the other rat. Rats avoided visits to locations that had earlier been visited by the other rat, but only if they had also visited the same location earlier in a short duration trial. This pattern of results is consistent with earlier findings from experiments using the radial arm maze. Furthermore, when rats did visit locations that had earlier been visited by the other rat in a long duration trial, they tended to be locations that had been visited longer ago by the other rat than would be expected. This suggests a forgetting function for social memories. These data provide evidence that the social memory reported in earlier studies using the radial-arm maze can be found in other experimental paradigms and that at least some of its properties are common in the two paradigms.