Characteristics of pigeons’ spatial working memory in an open-field task

Although pigeons seem to require special training before they will display accurate spatial working memory in radial-arm mazes, they readily show accurate working memory for recently visited feeder locations in an open-field analog of the radial maze. In this task, pigeons forage among sites located on the floor of an open room, with no constraints on the path they take between sites. Experiment 1 suggested that pigeons’ working memory for recently visited sites is facilitated if they are permitted to develop a stable reference memory “map” of the location of the sites with respect to landmarks in the room: Pigeons for which the landmarks remained constant from day to day displayed more accurate working memory than did pigeons for which the landmarks were rearranged between daily trials. The second experiment investigated the durability of pigeons’ working memory, using a forced-choice procedure. Accuracy remained high for retention intervals of up to 32 min, but dropped significantly with a 2-h delay.     

Pigeons’ spatial memory: V. Proactive interference in the delayed matching of key location paradigm occurs only under restricted conditions

In the delayed matching of key location procedure, pigeons must remember the location of the sample key in order to choose correctly between two comparison keys. The deleterious effect of short intertrial intervals on key location matching found in previous studies suggested that pigeons’ short-term spatial memory is affected by proactive interference. However, because a reward expectancy mechanism may account for the intertriai interval effect, additional research aimed at demonstrating proactive interference was warranted. In Experiment 1, matching accuracy did not decline from early to late trials within a session, a finding inconsistent with a proactive interference effect. In Experiment 2, evidence suggestive of proactive interference was found: Matching was more accurate when the locations that served as distractors and as samples were chosen from different sets. However, this effect could have been due to differences in task difficulty, and the results of the two subsequent experiments provided no evidence of proactive interference. In Experiment 3, the distractor on Trialn was either the location that had served as the sample on Trialn ? 1 or one that had been a sample on earlier trials. Matching accuracy was not inferior on the former type of trial. In Experiment 4, the stimuli that served as samples and distractors were taken from sets containing 2, 3, 5, or 9 locations. Matching accuracy was no worse, actually slightly better, with smaller memory set sizes. Overall, these findings suggested that pigeons’ memory for spatial location may be immune to proactive interference. However, when, in Experiment 5, an intratrial manipulation was used, clear evidence of proactive interference was found: Matching accuracy was considerably lower when the sample was preceded by the distractor for that trial than when it was preceded by the sample or by nothing. Possible reasons why interference was produced by intratrial but not intertrial manipulations are discussed, as are implications of these data for models of pigeons’ short-term spatial memory.     

Further studies of pigeons’ spatial working memory in the open-field task

In Experiments 1 and 2, pigeons’ spatial working memory in an open-field setting was examined under conditions that differed in terms of working-memory load (number of sites visited prior to a retention test) at various delays between initial choices and the retention test. In Experiment 1, pigeons were tested under two conditions of memory load (three or five sites visited prior to the delay) and two delay intervals (15 and 60 min). Accuracy declined as a function of delay but was not affected significantly by memory load. In Experiment 2A, pigeons were tested under three conditions of memory load (two, four, or six sites visited prior to the delay). In separate phases, the delay was 2, 15, and 60 min. Accuracy was not affected by memory load in any of these phases. In Experiment 2B, three conditions of memory load (two, four, or six sites visited prior to the delay) were tested at two delays (2 and 60 min) within a test phase. Accuracy declined with increasing delay, but memory load again had no significant effects. These results are inconsistent with previous suggestions that pigeons’ retention of spatial information may decline as working-memory load is increased. In Experiment 3, cue-manipulation tests confirmed that pigeons’ choice behavior in the open-field task is controlled by memory for previously visitad room locations.     

A comparison of the short-term memory performances of pigeons and jackdaws

Two experiments employed a delayed conditional discrimination procedure in which half the trials began with the presentation of food and half with no food; following a retention interval, subjects were presented with a choice between red and green keys, a response to one of which was reinforced according to whether the trial had started with food or no food. In Experiment 1, after 38 training sessions during which the retention interval was gradually increased, pigeons performed at a moderate level with intervals of 5 to 7.5 sec. A final test produced a steep forgetting function for food trials, but not for no-food trials; performance was unaffected by the duration of the intertriai interval (10 or 40 sec). Experiment 2 used the delayed conditional discrimination procedure to compare short-term memory in jackdaws (Corvus monedulus) with that in pigeons. Although the performance of the jackdaws was below that of the pigeons at the start of training, they showed more rapid learning over long delays, and, in the final test, a shallower forgetting function for food trials than that shown by pigeons. The results suggested superior short-term memory in jackdaws, which may help to explain the better performance of corvids in general when compared with that of pigeons in certain complex learning tasks.     

Level of deprivation does not affect degree of discounting in pigeons

Two experiments tested the effects of food deprivation on discounting in pigeons. An adjusting-amount procedure was used to estimate the subjective value of food at delays ranging from 1 to 24 s. Experiment 1 compared pigeons’ discounting of delayed food reinforcers at 75 %–80 % and 90 %–95 % of free-feeding weight. Experiment 2 compared discounting under 1- and 23-h food deprivation. In both experiments at both deprivation levels, discounting was well described by the hyperboloid discounting function. No systematic effect of level of deprivation on degree of discounting was observed in either experiment. This finding is consistent with the view that pigeons’ choices are controlled by the relative, rather than the absolute, value of reinforcers.     

Exploring the limits of spatial memory in rats,using very large mazes

In Experiment 1, rats foraged for food in six successive phases with 8, 16, 24, 32, 40, and 48 arms attached in random locations to a large radial maze. The percentage of novel choices appeared to be determined more by spatial proximity than by number of arms. In Experiment 2, rats foraged for food in four successive phases with 8, 16, 24, and 48 arms attached to the maze in spread-out or tight configurations. Performance was poor in the tight configurations regardless of the number of arms. Performance was excellent in the 8-arm spread-out condition but declined as 16 and, then again, 24 arms were added. Thus, spatial separation, not number of locations, was the chief determinant of performance in the first two experiments. In Experiment 3, in successive phases, 8, 16, 24, 32, 40, 48, 16, and 8 food towers were set in a circle on the floor, with the spatial separation between adjacent towers held constant at 33 cm. The percentage of novel choices declined as 8 towers became 16 and did not change again with 24, 32, 40, or 48 towers in place but then increased again as 16 towers became 8. In Experiment 4, in successive phases, 8, 16, 24, and 32 food towers were set in a circle, with the spatial separation between adjacent towers held constant at 66 cm. The percentage of novel choices declined as 8 towers became 16 and again as 16 towers became 24 but did not decline further. These data were discussed in terms of the fundamental problems posed by variations in the number of food locations in the pursuit of the limit of spatial memory in rats.     

Time-of-day discriminative learning in homing pigeons,Columba livia

Pigeons were trained on an operant procedure to discriminate between morning and afternoon when location did not vary (Experiment 1). The pigeons were placed on a fixed interval (FI) schedule in the morning and on a different FI schedule in the afternoon. Probe trials that occurred at the beginning of the training sessions were examined. The pigeons responded differently, depending on the time of day, reflecting the learning of a stable 24-h memory representation of the association between the FI schedules and the time of day. The pigeons from Experiment 1 were then clock shifted and tested twice, to determine whether they were relying on an endogenous circadian oscillator, an hourglass mechanism influenced by the photoperiod, or environmental noise to make the time-of-day discrimination (Experiment 2). The results of the second experiment indicated a circadian mechanism was most important for the observed time-of-day learning.     

Differences in feeding ecology predict differences in performance between golden lion tamarins (Leontopithecus rosalia) and Wied’s marmosets (Callithrix kuhli) on spatial and visual memory tasks

Golden lion tamarins (Leontopithecus rosalia) and Wied’s marmosets (Callithrix kuhli) exhibited adaptive differences in performance on several distinct memory tasks. On both an open-field analogue of a radial arm maze and a spatial delayed matching-to-sample task, the marmosets performed better than the tamarins after short (5-min) retention intervals, but only the tamarins continued to perform above chance after long (24- or 48-h) retention intervals. The marmosets also required less training than the tamarins did to learn a color memory task, but again only the tamarins performed above chance when the retention interval was increased to 24 h. The results of these experiments are consistent with predictions based on knowledge of the feeding ecology of these species in the wild and raise the possibility that they possess different visuospatial memory abilities specialized for tracking the spatial and temporal distribution of their principal foods.     

On the role of trial outcomes in delayed discriminations

Delayed simple discriminations are typically retained more accurately over longer delays by pigeons than are delayed conditional discriminations (e.g., Honig & Wasserman, 1981). In two experiments, we investigated the extent to which trial outcomes contribute to this difference by comparing performances when all trials ended with food reinforcement versus when only half of the trials did. Experiment 1 showed that when food was presented on all trials, contingent upon either pecking or not pecking the test stimulus, levels of retention and rates of forgetting were comparable for these two tasks. By contrast, Experiment 2 showed better retention of delayed simple than delayed conditional discriminations when half of the trials ended with food and the other half in extinction. Furthermore, delayed simple discriminations were retained more accurately with food versus no-food outcomes than with food at the end of every trial, whereas the reverse was true for delayed conditional discriminations. These findings indicate that retention differences between these tasks are another instance of the differential outcomes effect.     

Social effects on spatial choice in the radial arm maze

Social memory was investigated in the context of a spatial working memory task. Pairs of rats were tested in an eight-arm radial maze. Under most conditions, there was a tendency to choose maze locations that had been visited earlier by the other rat. The possibility that this tendency is produced by common preferences for particular maze locations was ruled out. An opposite tendency to avoid visits to locations that had been visited earlier during the trial by another rat was found only when the maze location contained two pellets (rather than an undepletable supply), the rats’ ability to see each other in the maze was restricted to the central arena, and the maze location had been previously visited by the focal rat. The amount of food available in maze locations did not otherwise modulate social influences on spatial choice. The results indicate that memory for a rat’s own previous choices is combined with memory for the choices made by another rat.     

Coding of feature and no-feature events by pigeons performing a delayed conditional discrimination

Pigeons’ performance of a delayed conditional discrimination with presence versus absence of conditional (sample) stimuli was examined in two experiments. The pigeons showed steeper retention functions with feature (i.e., presence) samples (either food or yellow) than with no-feature (i.e., absence) samples (either no food or no yellow). These results suggest that pigeons code features and respond only by default to test stimuli (comparisons) associated with no features. In contrast, the overall superiority of performance on no-feature-sample trials compared with feature-sample trials in both the food/no-food- and yellow/no-yellow-sample tasks was reversed at a 0-sec delay in the food/no-food-sample group, but not in the yellow/non-yellow-sample group. This difference in results with hedonic versus nonhedonic samples suggests that the crossover in delay performance on food/no-food-sample trials is produced by the formation of backward associations between the food-associated comparison stimulus and the food sample.     

Comparing spatial memory in two species of tit: Recalling a single positive location

The performance of a food-storing species, the marsh tit(Parus palustris), was compared with that of a nonstorer, the blue tit(P. caeruleus), in a spatial memory task in which birds had to return to a site where they had previously been allowed to eat part of a piece of peanut. No differences were found between species’ overall performance, but increasing retention interval from 1 min to 24 h brought about a decrease in performance. The results are discussed in relationship to the hypothesis that food-storing birds have a specialized spatial memory capacity.     

Development of excitatory backward associations during the establishment of forward associations in a delayed conditional discrimination by pigeons

The development of excitatory backward associations in pigeons was demonstrated in three experiments involving conditional discriminations with differential outcomes. In Phase 1 of all three experiments, correct comparison choices following one sample were followed by food, whereas correct comparison choices following the other sample were followed by presentation of an empty feeder. In Phase 2, the food and no-food events that served as outcomes in Phase 1 replaced the samples. When the associations tested in Phase 2 were consistent with the comparison-outcome associations developed in Phase 1, transfer performance was significantly better than when the Phase 2 associations were inconsistent with the Phase 1 associations. In Experiment 1, an identity matching-to-sample task was used with red and green samples and red and green comparisons. In Experiment 2, a symbolic matching task was used with shape samples and hue comparisons, and it was shown that the backward associations formed were between the trial outcome (food or no food) and the correct comparison. In Experiment 3, it was determined that the transfer effects observed in these experiments did not depend on either the similarity of behavior directed toward the samples in the training and test phases, or the similarity of food and no-foodexpectancies generated by the samples in Phase 1 to food and no-foodevents presented as samples in Phase 2.     

Time-of-day discrimination by pigeons,Columba livia

Pigeons were trained to discriminate between four keys. One provided food in the mornings, another provided food in the afternoons, and two never provided food. Three experiments were performed to determine whether pigeons could track food availability over a 24-h period. All the subjects appeared to demonstrate time-place associative learning. A fourth experiment was designed to investigate the mechanisms underlying the timing behavior. Lights-on time was shifted back by 6 h, and no decrease in performance was found during the first session following the phase shift. This suggests that a circadian type of timing mechanism with a self-sustaining oscillator mediates time-place learning over a period of 24 h. Further support for this notion was found in a fifth experiment, in which the subjects were tested in constant dim light. In that experiment, the subjects’ continued correct responding provides additional support for a self-sustaining circadian timer.     

Control of pigeons’ keypecking by the left-right arrangement of stimuli

Control of pigeons’ keypecking by conditionalities in the spatial arrangement of two element stimuli (designated A and B) was investigated. In Experiment 1, reinforcement for keypecking was made conditional upon the left-right location of A and B: Reinforcement was available when A was on the left and B was on the right (AB), but not on BA, AA, or BB trials. The pigeons successfully discriminated the rewarded AB configuration, but only after a stage in which a particular element in a particular location (e.g., A on left) primarily controlled pecking. Experiments 2 and 3 systematically replicated these findings and included controls to discount discrimination of the AB compound on the basis of the temporal order (e.g., A followed by B) rather than the spatial configuration of the elements. During a generalization test in Experiment 4, the elements were presented singly either in the left (AX, BX) or right (XA, XB) positions. As would be expected had the animals learned “A on the left, B on the right is rewarded,” responding on AX trials exceeded that on XA trials, and responding on XB trials exceeded that on BX trials.     

Dissociation of the effect of reinforcer type and response strength on the force of a conditioned response

A dissociation between the effect of reinforcer type and response strength on the force of the pigeon’s keypeck response was shown in three experiments. In Experiment 1, pigeons were trained to peck two conditioned stimuli, one paired with water and another paired with grain. The pigeons made more forceful pecks for grain than for water and also showed a tendency, albeit an unreliable one, to respond on a higher percentage of food trials than water trials. In Experiment 2, the pigeons from Experiment 1 were satiated with either food or water and were then presented with the two conditioned stimuli in an extinction test. It was found that, regardless of the drive state, the pigeons made more forceful pecks to the stimulus that predicted food than to the stimulus that predicted water. In the thirsty group, however, this difference in force was not accompanied by a difference in the percentage of trials with a response. In Experiment 3, pigeons trained with a single reinforcer pecked more often on instrumentally reinforced trials than on Pavlovian conditioning trials, but there was no difference in the force of the pecks. Taken together, these results imply that differences in response strength cannot account for the difference between the force of food- and water-reinforced pecks. Instead, stimulus-substitution theory may provide the best account of the topography of the two types of pecks.     

Associatively activated representations of food events resemble food outcome expectancies more closely than they resemble food-based memories

When Pavlovian stimuli activate representations of food, do these representations resemble memories of food consumed in the recent past or expectancies of food that is imminent? In Experiments 1A and 1B, this question was addressed by training pigeons on a symbolic matching-to-sample task involving different grains as memory cues or as expectancy cues for correct choices. Autoshaping trials involving these same grains were interspersed among matching-to-sample trials, as were test trials involving the substitution of autoshaping stimuli for cues in the matching-to-sample task. Control over choices transferred to autoshaping stimuli in both experiments, suggesting that associatively activated representations of food resemble both memories and expectancies. In Experiment 2, pigeons were trained on a symbolic matching-to-sample task in which food and no-food memory cues (i.e., the samples) were juxtaposed with no-food and food expectancy cues. Subsequently, autoshaping stimuli, which activated representations of food and no food, were substituted for the samples. Choices by the pigeons indicated that associatively activated representations of food-related events resemble expectancies more closely than they do memories.     

Spatial memory and the performance of rats and pigeons in the radial-arm maze

The resource-distribution hypothesis states that the ability of an animal to remember the spatial location of past events is related to the typical distribution of food resources for the species. It appears to predict that Norway rats would perform better than domestic pigeons in tasks requiring spatial event memory. Pigeons, tested in an eight-arm radial maze, exhibited no more than half of the memory capacity observed in rats in the same apparatus and may not have used spatial memory at all. The results were interpreted as supporting the hypothesis.     

Expression of a taste aversion conditioned with an odor-taste compound: Overshadowing is relatively weak in weanlings and decreases over a retention interval in adults

Adult rats were injected with lithium chloride (LiCl) after consumption of a novel flavor (chocolate milk) that either was or was not presented together with a novel ambient odor (banana) as a compound conditioned stimulus (CS). In Experiment 1, the adults’ consumption of the flavor 24 h after conditioning was compared with that of weanling rats given the same conditioning treatment on Postnatal Day 21. The results confirmed previous indications that the reduction in aversion observed for adults conditioned with the compound CS (overshadowing) was weak or nonexistent in weanlings. After a longer retention interval (21 days), there was no evidence of overshadowing in adults despite maintained retention of the basic conditioned aversion. In Experiment 2 this decrease in overshadowing after a long retention interval was replicated with adult animals and extended to a different method of testing. The form of the effect was the same as in Experiment 1: The decrease in overshadowing occurred over the retention interval without loss in retention of the basic taste aversion; the decrease in overshadowing was a consequence of anincrease in the flavor aversion displayed by animals conditioned with the compound CS. The impaired flavor aversion (i.e., the overshadowing) observed shortly after conditioning apparently was due to factors associated with memory retrieval, rather than to reduced attentional or associative strength.     

Sign and goal tracking during delay and trace autoshaping in pigeons

In two experiments, pigeons were exposed to an autoshaping procedure in which a keylight was followed by food under delay or trace conditions, while measures were taken of keypecking and time spent near the key. In Experiment 1, the birds in the trace group spent less time near the key than did the delay birds. Moreover, the trace birds exhibited a pattern of withdrawal from the key during the trial. In Experiment 2, visual observations of the birds’ location and latencies to eat both indicated that the trace birds’ withdrawal from the conditioned stimulus was accompanied by goal tracking. The difference in performance between the delay and trace conditions was taken as evidence that a trace stimulus may exert control over behavior as an occasion setter.