Remembrance of places you passed: social spatial working memory in rats

Pairs of rats were tested in a radial-arm maze to determine whether the spatial choices made by one rat affect the subsequent spatial choices of the other rat. In a free-choice procedure, rats showed an increased tendency to choose the location that had most recently been chosen by a foraging partner but a decreased tendency to visit locations that the foraging partner had visited earlier. Forced-choice procedures were used to better control the social stimulus and the interactions between the rats. Under some conditions, locations were chosen later in the choice sequence of a subject rat if another rat had been observed choosing that location. Odor and other physical traces of the other rat's visits were ruled out as explanations for this effect. The results demonstrate the existence of working memory for locations visited by a familiar conspecific.     

Memory for frequency in rats: role of the hippocampus and medial prefrontal cortex

On a radial arm maze rats were tested for frequency memory of specific spatial locations, a task that presumably involves the coding of temporal information. On any trial during the study phase rats were allowed to visit three different spatial locations only once and one spatial location twice. During the test phase the rats were given a choice between a spatial location that had been visited once and spatial location that had been visited twice. The rats were reinforced for selecting the twice-visited spatial location. The number of spatial locations between a repetition (lag) was varied from one to three. After extensive training rats displayed memory for frequency only for a lag of three spatial locations, i.e., they displayed a repetition lag effect. Animals then received control, medial prefrontal cortex, or hippocampal lesions. Upon subsequent retests control rats continued to display frequency memory, but animals with medial prefrontal cortex or hippocampal lesions displayed a marked impairment. These data support the idea that both the hippocampus and medial prefrontal cortex code temporal order information.     

Gerbils in space: performance on the 17-arm radial maze.

In Experiment 1 six hungry gerbils received six trials per day on a 17-arm radial maze. During each trial the subjects were allowed to choose freely among the arms, each of which contained a food pellet, until each arm had been visited once or until eight minutes had elapsed. An error was recorded when the subject entered a previously visited arm. The gerbils quickly learned not to re-enter previously visited arms and generally made errors on fewer than 15% of entries, performance comparable to that of the rat and superior to that of other species tested in the radial arm maze. The intertrial-interval duration did not affect accuracy of arm choices during acquisition but did influence asymptotic accuracy. Accuracy did not change systematically over the six trials. A high proportion of arm entries were to nearby arms. Errors occurred most often towards the end of a trial. Odor cues were not important. When the number of trials per day was reduced from six to one, accuracy deteriorated slightly. In Experiment 2 neither the transposition of extramaze cues nor the placement of the maze in a different room had large disruptive effects on accuracy. In Experiment 3 the addition of three explicit intramaze brightness cues aided accuracy, perhaps by permitting the subjects to decompose the large maze into three smaller mazes, although there was no direct evidence that this was the case. Implications of a number of these results for models of spatial maze performance were discussed.     

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.     

Memory for temporal order of new and familiar spatial location sequences: role of the medial prefrontal cortex

Rats with medial prefrontal cortex or sham control lesions were tested on an eight-arm radial maze task to examine memory for the temporal order of a variable and a constant sequence of spatial locations as a function of temporal distance. During the study phase of each trial, rats were allowed to visit each of eight arms once in an order that was randomly selected or fixed for that trial. The test phase required the rats to choose which of two arms occurred earlier in the sequence of arms visited during the study phase. The arms selected as test arms varied according to temporal distance (0, 2, 4, or 6) or the number of arms that occurred between the two test arms in the study phase. For the variable sequences based on new information, control rats showed an increasing temporal distance function. Relative to control rats, medial prefrontal cortex-lesioned rats displayed a temporal order memory deficit across all distances. For the constant sequence based on familiar information, control rats performed well across all distances. Relative to controls, the medial prefrontal cortex-lesioned rats displayed a performance deficit. The results support the idea that the medial prefrontal cortex contributes to mnemonic operations associated with temporal order for new and familiar spatial location information.     

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.     

Flexible memory processing by rats: use of prospective and retrospective information in the radial maze

Four experiments investigated the content of the memory used by rats in mediating retention intervals interpolated during performance in a 12-arm radial maze. The delay occurred following either the 2nd, 4th, 6th, 8th, or 10th choice. A 15-min delay had the greatest disruptive effect when interpolated in the middle of the choice sequence and less of an effect when it occurred either earlier or later. This pattern of results was obtained when either a free- or forced-choice procedure was used prior to the delay and regardless of whether postdelay testing consisted of completion of the maze or two-alternative forced-choice tests. Assuming that the disruptive effect of a delay is a function of memory load, this implies that the rats used information about previously visited arms (retrospective memory) following an earlier interpolated delay but information about anticipated choices (prospective memory) following a delay interpolated late in the choice sequence. There appeared to be a recency effect only in the early and middle delay conditions. This provides converging evidence for the dual-code hypothesis. No evidence for prospective memory was obtained following a 60-min delay.     

Looking behaviour and preference for artworks: The role of emotional valence and location

The position of an item influences its evaluation, with research consistently finding that items occupying central locations are preferred and have a higher subjective value. The current study investigated whether this centre-stage effect (CSE) is a result of bottom-up gaze allocation to the central item, and whether it is affected by item valence. Participants (n = 50) were presented with three images of artistic paintings in a row and asked to choose the image they preferred. Eye movements were recorded for a subset of participants (n = 22). On each trial the three artworks were either similar but different, or were identical and with positive valence, or were identical and with negative valence. The results showed a centre-stage effect, with artworks in the centre of the row preferred, but only when they were identical and of positive valence. Significantly greater gaze allocation to the central and left artwork was not mirrored by equivalent increases in preference choices. Regression analyses showed that when the artworks were positive and identical the participants' last fixation predicted preference for the central art-work, whereas the fixation duration predicted preference if the images were different. Overall the result showed that item valence, rather than level of gaze allocation, influences the CSE, which is incompatible with the bottom-up gaze explanation. We propose that the centre stage heuristic, which specifies that the best items are in the middle, is able to explain these findings and the centre-stage effect.     

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.     

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.     

Reward, novelty and spontaneous alternation

It has been suggested that rats' propensity for “win-shift” behaviour in spatial memory and spontaneous alternation tests reflects a species-specific foraging strategy which leads them to avoid places where they have recently found food. An alternative explanation is that they avoid places which are familiar. In three experiments using a T-maze, we evaluated these accounts by comparing the probability of avoiding or re-entering a recently visited arm, as a function of whether food had or had not been found on the previous visit. Each rat received a series of 16 exposure-test trial pairs over 8 days. Neither alternation nor repetition of the previous choice was differentially reinforced. Experiments I and II forced rats to enter a specific arm before a subsequent choice, and differed in the overall probability of reward; in Experiment III all choices were free. In all three experiments the probability of alternating was greater after nonreward than after reward. This effect occurred more reliably on later tests within a day, little difference appearing on earlier tests. It was concluded that there was no evidence for a spontaneous “win-shift” tendency as such, and that these and other results can be adequately accounted for by a combination of exploratory tendencies (spontaneous alternation) and the conventional effects of reward.     

Radial maze analog for pigeons: Evidence for flexible coding strategies may result from faulty assumptions

Previous research with the radial maze has found evidence that rats can remember both places that they have already been (retrospective coding) and places they have yet to visit (prospective coding; Cook, R. G., Brown, M. F., & Riley, D. A. (1985). Flexible memory processing by rats: Use of prospective and retrospective information in the radial maze. Journal of Experimental Psychology: Animal Behaviour Processes, 11, 453-469). Such dual coding also has been found in pigeons using a radial maze analog in which insertion of a delay at different points during a trial affects performance differentially depending on where in the trial it is inserted. When a delay is interpolated either early or late in a trial, there is minimal disruption of performance compared with when it is interpolated in the middle of the trial. However, the analysis required with this procedure requires the assumption that if errors made on control trials are subtracted from errors made in delay trials, the remaining errors can be directly attributed to the delay. But errors may also be attributed to the changing criterion for making a response as the trial proceeds. Furthermore, the animal’s tendency to choose alternatives in a systematic order may also affect its need to remember the sequence of choices made (and yet to be made) on each trial. In the present research, we avoided having to make this assumption by giving the pigeons a two-alternative choice at the time of testing and by randomly determining for the pigeon the order of predelay choices on each trial. This change in procedure resulted in comparable performance as a function of where in the trial the test occurred on both control and delay trials. The effect of the delay was to produce a general decrement in performance independent of where it occurred in the trial.     

Prospective and retrospective time perception are related to mental time travel: Evidence from Alzheimer’s disease

Unlike prospective time perception paradigms, in which participants are aware that they have to estimate forthcoming time, little is known about retrospective time perception in normal aging and Alzheimer’s disease (AD). Our paper addresses this shortcoming by comparing prospective and retrospective time estimation in younger adults, older adults, and AD patients. In four prospective tasks (lasting 30 s, 60 s, 90 s, or 120 s) participants were asked to read a series of numbers and to provide a verbal estimation of the reading time. In four other retrospective tasks, they were not informed about time judgment until they were asked to provide a verbal estimation of four elapsed time intervals (lasting 30 s, 60 s, 90 s, or 120 s). AD participants gave shorter verbal time estimations than older adults and younger participants did, suggesting that time is perceived to pass quickly in these patients. For all participants, the duration of the retrospective tasks was underestimated as compared to the prospective tasks and both estimations were shorter than the real time interval. Prospective time estimation was further correlated with mental time travel, as measured with the Remember/Know paradigm. Mental time travel was even higher correlated with retrospective time estimation. Our findings shed light on the relationship between time perception and the ability to mentally project oneself into time, two skills contributing to human memory functioning. Finally, time perception deficits, as observed in AD patients, can be interpreted in terms of dramatic changes occurring in frontal lobes and hippocampus.     

Spatial memory in rats after 25 hours

We investigated the time course of spatial-memory decay in rats using an eight-arm radial maze. It is well established that performance remains high with retention intervals as long as 4 h, but declines to chance with a 24-h retention interval (Beatty, W. W., & Shavalia, D. A. (1980b). Spatial memory in rats: time course of working memory and effect of anesthetics. Behavioral & Neural Biology, 28, 454-462). It is possible that 24 h reflects a genuine retention limitation of rat spatial memory. Alternatively, it may be possible to identify factors that might support memory performance even after very long delays. The current experiment was conducted to test the above two hypotheses. We evaluated performance using two intertrial intervals (24 and 48 h) and two retention intervals (1 and 25 h). Increasing the intertrial interval produced an approximately constant increase in performance for both retention intervals. This improvement is consistent with a trial-spacing effect (i.e., the superiority of spaced over massed trials). Rat spatial memory apparently lasts at least 25 h.     

Exposure to Spatial Cues Facilitates Visual Discrimination but Not Spatial Guidance

The performance in a radial-arm maze of two groups of rats with restricted access to extra-maze visual cues was studied. One group received extensive exposure to the visual environment of the maze, whereas the second group was never exposed to the environment, aside from their experience in the maze itself. Spatial exposure resulted in a slightly improved ability to discriminate between previously visited and unvisited spatial locations, which can be explained on the basis of general perceptual learning processes. However, there was no evidence that spatial exposure resulted in control of choices by the spatial relations among the maze locations. These results are discussed in terms of theories of spatial learning which appeal to perceptual learning and cognitive mapping.     

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.     

Serial learning in rats: A test of three hypotheses

Findings obtained by providing rats with a single fixed series of events, A-B-C-…, often are equally compatible with three alternative serial learning interpretations: that the signal for items is (A) their position in the series (position view), (B) the prior item of the series (chaining view), and (C) one, two, or more prior items of the series (sequential view). By employing a novel procedure of supplying rats with two different series, rather than a single series, it was possible to choose between the three alternatives. Employing 10 and 0, 0.045 g, Noyes pellets as items, rats in both runway experiments reported here received a three trial series, either a 10-0-10 series or a 0-0-10 series. In Experiment 1, the other series was a single 0 pellet trial (along with 10-0-10) or a single 10 pellet trial (along with 0-0-10). In Experiment 2, the other series was either 0-0 (along with 10-0-10) or 10-0 (along with 0-0-10). Considering both experiments, findings were consistent with the sequential view but not with either the position view or the chaining view. The possibility was suggested that, under some other experimental conditions, particularly those not employing reward events as items, greater control over discriminative responding might be exercised by position cues than by item cues.     

Release from proactive interference by experimental amnesia: electroconvulsive shock improves radial-arm maze performance in rats

Rats were trained in an eight-arm radial maze and tested using a proactive interference (PI) procedure. Each test trial consisted of forced choices of four randomly selected arms followed, after a 2-h delay, by free choices among all eight arms. Normally, rats chose correctly during the free choices by entering and retrieving food from the four arms not yet visited during the test trial. Occasionally, an interference trial preceded the test trial by 1.5 or 3 h; interference trials consisted of forced choices of another four arms and an immediate test. The presence of an interference trial lowered test-trial performance (PI). Electroconvulsive shock (ECS) administered immediately after the interference trial had no effect; i.e., PI was still observed. When ECS was administered at the midpoint of the 3-h intertrial interval, performance increased to control (no ECS, no PI) levels. Such release from PI, however, was not obtained, and test-trial performance remained inaccurate when ECS was delivered immediately after the forced choices of the test trial (either 1.5 or 3 h after the interference trial).     

Abnormal patterns of maze patrolling in the mutant mouse staggerer

Two experiments describe the abnormal patterns of maze patrolling of adult mutant staggerer mice. The clinical symptoms of this mutant involve exclusively postural and gait abnormalities, apparently due to a disruption of cerebellar architecture leading to a vast reduction in cell numbers and size of this structure. This clinical feature can easily account for the first clear difference reported in these experiments, involving a reduction in the total ambulatory activity in a maze by this mutant. The more interesting result involves different qualitative aspects of the maze patrolling by staggers, compared to normal litter-mate controls. The experiments measured the distribution of subjects' visits to different maze locations, and varied the configuration and the amount of familiarization with the maze. Neither of these factors significantly influenced the basic results. These were the staggerers confined their ambulatory activity to a smaller number of different locations, which were more intensively visited compared to normals, and the staggerers showed a pronounced tendency to return to the place that was most recently visited, compared to a tendency by the normals to avoid that location. It is suggested that these results could be due either to abnormal novelty reactions or to a reduced tendency to pursue an initiated trajectory.     

Constructing a self: The role of self-structure and self-certainty in social anxiety

Current cognitive models stress the importance of negative self-perceptions in maintaining social anxiety, but focus predominantly on content rather than structure. Two studies examine the role of self-structure (self-organisation, self-complexity, and self-concept clarity) in social anxiety. In study one, self-organisation and self-concept clarity were correlated with social anxiety, and a step-wise multiple regression showed that after controlling for depression and self-esteem, which explained 35% of the variance in social anxiety scores, self-concept clarity uniquely predicted social anxiety and accounted for an additional 7% of the variance in social anxiety scores in an undergraduate sample (N = 95) and the interaction between self-concept clarity and compartmentalisation (an aspect of evaluative self-organisation) at step 3 of the multiple regression accounted for a further 3% of the variance in social anxiety scores. In study two, high (n = 26) socially anxious participants demonstrated less self-concept clarity than low socially anxious participants (n = 26) on both self-report (used in study one) and on computerised measures of self-consistency and confidence in self-related judgments. The high socially anxious group had more compartmentalised self-organisation than the low anxious group, but there were no differences between the two groups on any of the other measures of self-organisation. Self-complexity did not contribute to social anxiety in either study, although this may have been due to the absence of a stressor. Overall, the results suggest that self-structure has a potentially important role in understanding social anxiety and that self-concept clarity and other aspects of self-structure such as compartmentalisation interact with each other and could be potential maintaining factors in social anxiety. Cognitive therapy for social phobia might influence self-structure, and understanding the role of structural variables in maintenance and treatment could eventually help to improve treatment outcome.