Use of win-stay and win-shift strategies in place and cue tasks by medial caudate putamen (MCPu) lesioned rats

This study investigated the behavioral function of the medial caudate putamen (MCPu) in the solving of maze tasks. MCPu lesioned rats (n = 35) and control rats (n = 35) were trained for the place or cue task (the four baited arms and four unbaited arms task) in an eight-arm radial maze, which requires the win-stay or the win-shift strategy. In Experiment 1, in which the place task was used, MCPu lesioned rats could learn the task in the win-shift condition, but not in the win-stay condition. MCPu lesioned rats made a lot of unbaited errors in the win-stay condition, as they persistently chose adjacent arms. Control rats could learn the tasks in both conditions. In Experiment 2, in which the cue task was used, MCPu lesioned rats and control rats could learn the tasks in both the win-stay and the win-shift conditions. If anything, the performance of MCPu rats was a little better than that of control rats in the win-stay condition. The results of these two experiments revealed that the MCPu was involved in solving the win-stay place task, but not the win-shift place, win-stay cue, and win-shift cue tasks. These findings suggest that the MCPu plays an important role in utilizing both spatial information and switching foraging strategies flexibly and efficiently, that is, processing complicated visuospatial cognition.     

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.     

Does reward depletion influence spatial memory performance?

If spatial memory tasks are considered as foraging problems, it can be predicted that rats' difficulty in learning a win-stay task—revisiting part of a maze where food has recently been found—should be partly overcome if the food is not fully consumed at the first visit (nondepleted reward) rather than being all eaten (depleted reward). Three experiments confirmed and further analysed this result. Experiments 1 and 2 showed that it does not depend on the amount of food initially found; nor is win-stay performance affected by the amount of food actually eaten. Experiment 3 suggested that the effects of nondepleted reward are mainly due to the animals' being interrupted while eating, and very little to the fact that uneaten food is left behind. The results are discussed with regard to their implications for learning theory, and for the application of foraging theory to learning and memory experiments.     

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.     

Win-stay behaviour in the rat

The Law of Effect dictates that animals will repeat the just-reinforced response “win-stay”, and yet there have been apparent violations of this by rats running for food in mazes, in the form of “win-shift” behaviour. Four experiments analysed the conditions determining win-stay and win-shift behaviour. All the experiments employed a schedule in which reinforcement was distributed across two choices, and in which the probability of reinforcement for the first response after previous reinforcement was equivalent for the two options. Despite this lack of programmed differential reinforcement, rats showed a significant win-stay tendency in Experiment 1, with no spatial bias. Experiments 2 and 3 used respectively a Y-maze and an operant chamber in which responding required a return to a central choice point. In both situations, significant win-shift behaviour resulted initially, at relatively high frequencies of reinforcement, but this win-shift changed to significant win-stay over many sessions, and with intermittent reinforcement. Experiment 4 introduced explicitly non-reinforced trials and demonstrated a “lose-shift” tendency, parallel to win-stay. Possible artefacts underlying win-stay and win-shift behaviour are rejected, and various mechanisms for these effects, including theories of optimal choice and associative learning, are discussed.     

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.     

Overcoming unlearned response biases: delayed escape following errors facilitates acquisition of win-stay and win-shift working memory water-escape tasks in rats

Previous research has demonstrated that perseveration in escape situations is an unlearned response bias of rats and mice which is difficult to overcome. In Experiment I, Sprague-Dawley rats were trained to a criterion of nine correct choices in 10 consecutive trials in a win-stay working memory water-escape task wherein an escape platform was hidden in one of two compartments. Subjects were given a forced choice on an Information Trial followed by a free choice on a Test Trial 5 min later. Subjects who were given a 30-s forced swim in the incorrect section following errors on the Test Trial showed faster acquisition and less use of response perseveration than control subjects. In Experiment II, the delayed escape procedure was used to compare acquisition of win-stay and win-shift strategies. Contrary to previous research both groups learned the tasks, although the win-stay group showed better performance. It is concluded that unlearned response biases of perseverating and returning to previous escape sites can be overcome if experimental conditions are appropriately arranged.     

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.     

Win-shift and win-stay learning in the short-beaked echidna (<Emphasis Type="Italic">Tachyglossus aculeatus</Emphasis>)

Numerous previous investigators have explained species differences in spatial memory performance in terms of differences in foraging ecology. In three experiments we attempted to extend these findings by examining the extent to which the spatial memory performance of echidnas (or "spiny anteaters") can be understood in terms of the spatio-temporal distribution of their prey (ants and termites). This is a species and a foraging situation that have not been examined in this way before. Echidnas were better able to learn to avoid a previously rewarding location (to "win-shift") than to learn to return to a previously rewarding location (to "win-stay"), at short retention intervals, but were unable to learn either of these strategies at retention intervals of 90 min. The short retention interval results support the ecological hypothesis, but the long retention interval results do not. Electronic Publication     

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.     

Systemic and local administration of estradiol into the prefrontal cortex or hippocampus differentially alters working memory

The influence of estradiol on learning and memory is dependent on a number of factors. The effects of physiological levels of estradiol on the acquisition of a spatial working memory task mediated by the prefrontal cortex (PFC) and the hippocampus were examined in Experiment 1. Ovariectomized Long-Evans rats received daily injections of estradiol or vehicle were tested on the win-shift version of the radial arm maze. A high dose of estradiol benzoate (5 microg) enhanced acquisition of the task, whereas a low dose of estradiol (0.3 microg) increased the number of errors committed over 17 days of testing. Experiment 2 was conducted to examine site-specific influences of estradiol on spatial working memory in well-trained rats. Saline and estradiol cyclodextrin (0.1 and 0.9 microg) were infused into the prelimbic region of the PFC or dorsal hippocampus 40 min prior to testing on the win-shift task. Infusions of estradiol into both brain areas attenuated saline-infusion disruptions in working memory. Specifically, the higher dose of estradiol facilitated working memory when infused into the PFC, whereas the lower dose of estradiol facilitated performance when infused into the dorsal hippocampus. Moreover, working memory was significantly impaired 24 h after infusions of estradiol into the dorsal hippocampus but not the PFC. These data provide further evidence for the notion that estradiol can dose-dependently alter memory processes and suggest that facilitation or disruptions of working memory by estradiol are site- and time-specific.     

Spontaneous alternation and pattern of reinforcement

In Experiment I, rats were given one pair of trials per day in a T-maze; group RN were rewarded on the first trial only, NR were rewarded on the second trial only, while RR were rewarded on both trials. Alternation was approximately the same for all groups, and there was little decline in alternation over 28 days. There was, however, a difference in the choice behaviour on trials when rats failed to alternate, NR and RR, but not RN, choosing according to a position preference. These results are incompatible with several earlier theories of spontaneous alternation, and the hypothesis was put forward that alternation is initially part of an exploratory tendency, but that, when the maze becomes explored, the exploratory tendency dies down, and alternation only continues when rats have been reinforced (primarily or secondarily) for alternating. This hypothesis was tested in a second experiment, similar to the first but in which one group of rats was not rewarded on either trial; as predicted, this group showed significantly more decline in alternation than rewarded rats.     

Rats' sensitivity to their direction of movement and spontaneous alternation behaviour

The response of rats to their prior direction of movement was examined in three spontaneous alternation experiments. In the first, a straight alley run interpolated between two T-maze trials increased goal arm alternation when it was in the same direction as that of the animal's first T-maze goal arm entry and decreased the alternation tendency when it was in the opposite direction. Experiment II found that multiple runs in one direction in a straight alley increased the likelihood that rats would subsequently enter the goal arm of a T-maze which permitted movement in an opposite direction. In the third experiment, rats entered those goal arms of an eight-arm radial maze which permitted movement in any direction which was different from that during a preceding straight alley trial. The results of these experiments indicate that rats are quite sensitive to their direction of movement and use it as a cue in guiding their behaviour in a variety of experimental situations.     

Mice (Mus musculus) learn a win-shift but not a win-stay contingency under water escape motivation

Twenty mice (Mus musculus), the second filial generation offspring from a C57BL/6 and DBA/2J cross, received spatial win-shift and win-stay water escape training within a mixed design in which all mice received both types of training. Acquisition under win-shift was superior to win-stay with respect to errorless trials and latencies regardless of the order in which the procedures were experienced. Win-stay responding did not exceed chance levels during any training phase. These data contradict the claim that win-stay training is the more easily acquired of the 2 acquisition strategies under aversive motivation.     

Win-shift and win-stay learning in the rainbow lorikeet (Trichoglossus haematodus)

The tendency to win-shift (to better learn to avoid, rather than return to, recently rewarded locations) has been demonstrated in a variety of nectarivorous birds and in honeybees. It is hypothesized to be a cognitive adaptation to the depleting nature of nectar. In the present study we report the first attempt to test for a win-shift bias in a nectarivorous parrot, the rainbow lorikeet (Trichoglossus hematodus). This species differs from others tested for a win-shift bias in that it is a facultative, rather than an obligate, nectarivore. We tested a captive-reared population of the birds on a shift/stay task at long and short retention intervals. The data show no evidence of either a win-shift or a win-stay bias. The birds demonstrated efficient spatial search ability and above chance performance for both shift and stay contingencies at long and short delays. These data suggest that an innate tendency to win-shift may not be present in all avian nectarivores, or that the role experience plays in shaping such behaviors is different for different species.     

A test of the reward-value hypothesis

Rats retain source memory (memory for the origin of information) over a retention interval of at least 1 week, whereas their spatial working memory (radial maze locations) decays within approximately 1 day. We have argued that different forgetting functions dissociate memory systems. However, the two tasks, in our previous work, used different reward values. The source memory task used multiple pellets of a preferred food flavor (chocolate), whereas the spatial working memory task provided access to a single pellet of standard chow-flavored food at each location. Thus, according to the reward-value hypothesis, enhanced performance in the source memory task stems from enhanced encoding/memory of a preferred reward. We tested the reward-value hypothesis by using a standard 8-arm radial maze task to compare spatial working memory accuracy of rats rewarded with either multiple chocolate or chow pellets at each location using a between-subjects design. The reward-value hypothesis predicts superior accuracy for high-valued rewards. We documented equivalent spatial memory accuracy for high- and low-value rewards. Importantly, a 24-h retention interval produced equivalent spatial working memory accuracy for both flavors. These data are inconsistent with the reward-value hypothesis and suggest that reward value does not explain our earlier findings that source memory survives unusually long retention intervals.     

Sex differences in aversive memory in rats: Possible role of extinction and reactive emotional factors

Studies usually show better spatial learning in males and stronger emotional memory in females. Spatial memory differences could relate to diverse strategies, while dissimilar stress reactions could cause emotional memory differences. We compared male and female rats in two emotional (classical emotional conditioning and aversive discrimination memory) and two emotionally “neutral” tasks: (1) plus-maze discriminative avoidance, containing two open and two enclosed arms, one of which presenting aversive stimuli (light/noise). No differences were found in learning, retrieving, or basal emotional levels, while only male rats presented extinction of the task; (2) contextual fear conditioning – a cage was paired to mild foot shocks. Upon reexposure, freezing behavior was decreased in females; (3) spontaneous alternation – the animals were expected to alternate among the arms of a four-arm maze. No differences between genders were found and (4) open-field habituation was addressed in an arena which the rats were allowed to explore for 10 min. Habituation was similar between genders. Differences were found only in tasks with strong emotional contexts, where different fear responses and stress effects could be determinant. The lack of extinction of discriminative avoidance by females points out to stronger consolidation and/or impaired extinction of aversive memories.     

Memory for feeding in rats' spatial and visual choice behaviour

Four experiments with mazes examined the effects of feeding upon rats' subsequent choice between spatially or visually distinct alternatives. It is concluded that rats can recall both whether any food remained at the cessation of feeding (nondepletion) and whether or not feeding was interrupted; both features can be associated with the place where they occurred. The memory of nondepleted food evokes an unlearned tendency to return to the place where it was present (“win-stay” behaviour). The memory of interruption transiently had a similar effect in naive animals but eventually exerts a more nonspecific influence, which facilitates not only win-stay learning but its opposite, win-shift. The nondepletion effect was also obtained when the alternatives were defined by a visual cue (brightness) rather than spatial location. The determinants of staying and shifting are discussed in terms of reward memory and exploration.     

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.     

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.