Animal memory: The contribution of generalization decrement to delayed conditional discrimination retention functions

Delayed conditional discriminations in which a sample indicates which comparison stimulus is correct have typically been used in working memory research with animals. Following acquisition with no (0-sec) delay between the offset of the sample and the onset of the comparison stimuli, delays of variable duration are introduced. The resulting retention functions are taken as a measure of memory. We suggest that, in addition to memory loss due to the delay, the comparison of matching accuracy at the 0-sec training delay with relatively novel test delays may produce a generalization decrement that varies as a function of increasing delay. We tested this hypothesis by training pigeons with a mixed delay procedure from the start and found that the retention functions for these pigeons were significantly shallower than those for a control group trained with 0-sec delays and tested with longer delays, and, although reduced in magnitude, the differences persisted for as many as 15 sessions. We propose that a measure of animals’ working memory can be obtained uninfluenced by a generalization decrement if they have received comparable training with all of the delays that are tested.     

Pigeons’ memory for event duration: Intertrial interval and delay effects

The effects of within-session variations in the intertriai interval (ITI) and delay on pigeons’ memory for event duration were studied in delayed symbolic matching-to-sample tasks. Pigeons were trained to peck one color following a long (8 sec) sample and another color following a short (2 sec) sample. In the first three experiments, the baseline conditions included a 10-sec delay (retention interval) and a 45-sec ITI. During testing, the delay was varied from 0 to 20 sec, and the ITI that preceded the trial was varied from 5 to 90 sec. When the ITI and delay were manipulated separately (Experiments 1 and 2), the pigeons displayed a choose-short tendency when the delay was longer than 10 sec or when the ITI was longer than 45 sec, and a choose-long tendency when either the delay or the ITI was shorter than these baseline values. These effects occurred whether the sample was food access or light. When the ITI and delay were manipulated together, the pigeons showed a large choose-long error tendency when the short delay was tested together with a short ITI, and no systematic error tendency when the short delay was tested together with a longer ITI. A very large choose-short error tendency emerged on trials with a long delay and a long ITI; a reduced choose-short tendency was present when the long delay was presented together with a short ITI. In Experiment 4, the baseline conditions were a 0-sec delay and a 45-sec ITI. In this case variations in the ITI had a smaller and unidirectional effect: the pigeons showed a choose-long error tendency when the ITI was decreased, but no effect of ITI increases. Two hypotheses were proposed and discussed: (1) that pigeons judge sample durations relative to a background time composed of the ITI and delay, and (2) that the delay and ITI effects might arise from a combination of subjective shortening and proactive effects of samples from previous trials.     

Event-duration discrimination by pigeons: The choose-short effect may result from retention-test novelty

Pigeons trained on a conditional event-duration discrimination typically “choose short” when retention intervals are inserted between samples and comparisons. In two experiments, we tested the hypothesis that this effect results from ambiguity produced by the similarity of the novel retention intervals and the familiar intertrial interval by training pigeons with retention intervals from the outset and, for one group, in addition, making retention intervals distinctive from the intertrial intervals. In Experiment 1, when the retention intervals (0–4 sec) were not distinctive from the intertrial intervals, the pigeons did not show a clear choose-short effect even when extended retention intervals (8 sec) were introduced. When the retention intervals were distinctive, the pigeons showed a choose-long effect (they appeared to time through the retention interval), but it was relatively weak until the retention intervals were extended to 8 sec. In Experiment 2, when pigeons were discouraged from timing through the retention intervals by making the intertrial intervals and retention intervals salient distinct events and using long (up to 16-sec) retention intervals in training, parallel retention functions were found. It appears that when ambiguity is removed, forgetting by pigeons does not occur by the process of subjective shortening. These experiments suggest that the accurate interpretation of results of animal memory research using differential-duration samples must consider the novelty of the retention intervals on test trials as well as their similarity to other trial events.     

Pigeons’ short-term memory for temporal and visual stimuli in delayed matching-to-sample

In the present experiment, we compared directly pigeons’ short-term memory of temporal and visual stimuli in a delayed matching-to-sample task. The sample stimuli consisted of red and green lights presented for 5 and 30 sec, followed by a retention interval and blue and yellow comparisons. For subjects in the visual group, duration was irrelevant and the color of the sample was the conditional cue. For animals in the temporal group, color was irrelevant and duration of the sample was the conditional stimulus. The results showed that acquisition of the matching task was faster and accuracy was higher in the visual than in the temporal group. More importantly, memory of either sample generally declined at a similar rate when the duration of the retention interval was increased and when the intertrial interval was reduced. Taken together, the results indicate that with 1–8-sec retention intervals, short-term memory for temporal stimuli is similar to that found with color-visual samples. The findings are discussed in terms of retrospective and prospective processing.     

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.     

The effect of scopolamine on reference and working memory in pigeons

A comparison of the effects of scopolamine hydrobromide on working memory and reference memory in White Carneaux pigeons was undertaken by means of a modified delayed matching-to-sample procedure. Performance on working-memory trials was disrupted by decreases in sample duration and intertriai interval and by increases in delay interval. Performance on reference memory trials was not disrupted by any of these parametric manipulations. In Experiment 1, the pigeons received injections of scopolamine hydrobromide (0.01, 0.05, or 0.1 mg/kg), scopolamine methyl bromide (0.1 mg/kg), or saline prior to test sessions. In Experiment 2, the pigeons received injections of scopolamine hydrobromide (0.01 or 0.03 mg/kg), scopolamine methyl bromide (0.03 mg/kg), or saline. In both experiments, scopolamine hydrobromide had greater disruptive effects on working-memory trials than on reference-memory trials. The centrally active form of scopolamine disrupted working-memory trial accuracy more than the peripherally active form. However, no drug dose × delay interval interaction was obtained. Thus, the interference on working-memory-trial accuracy produced by central cholinergic blockade would not appear to be due to alterations in the active maintenance of information during the delay interval.     

Stimulus preference and the transitivity of preference

Four pigeons were exposed to multiple schedules with concurrent variable interval (VI) components and then tested for preference transfer. Half of the pigeons were trained on a multiple concurrent VI 20-sec, VI 40-sec/cuncurrent VI 4G-sec5 VI 80-sec schedule. The remaining pigeons were trained on a multiple concurrent VI 80-sec, VI 40-sec/concurrent VI 40-sec, VI 20-sec schedule-After stability criteria for time and response proportions were simultaneously met, four preference transfer tests were conducted with the stimuli associated with the VI 40-sec schedules. During the transfer tests, each pigeon allocated a greater proportion of responses (M=0,79) and time (M=0.82) to the stimulus associated with the VI 40-sec schedule that was paired with the VI 80-sec schedule than lo the VI 40-sec schedule stimulus paired with the VI 20-sec schedule. Absolute reinforcement rates on the two VI 40 sec schedules were approximately equal and unlikely to account for the observed preference. Nor was the preference consistent with the differences in local reinforcement rates associated with the two stimuli. Instead, the results were interpreted in terms of the differential value that stimuli acquire as a function of previous pairings with alternative schedules of reinforcement.     

Long-term habituation is produced by distributed training at long ISIs and not by massed training or short ISIs inCaenorhabditis elegans

To begin an investigation of the cellular processes that underlie long-term memory in the nematodeCaenorhabditis elegans, it is first necessary to determine thatC. elegans is capable of retention over 24 h, and to investigate the factors that may influence the expression of long-term memory. In the present study, the effects of stimuli number, interstimulus interval (ISI), and training procedure on long-term retention of habituation were tested inC. elegans. At a long (60-sec) ISI, distributed training sessions produced long-term habituation retained for 24 h, whereas massed training sessions or training with few stimuli did not. When training was performed at a short (10-sec) ISI, long-term habituation was not detectable with testing at either a 10- or a 60-sec ISI. The long-term habituation observed after distributed training sessions at a 60-sec ISI was consistently expressed when the training procedures were varied. Thus it is clear thatC. elegans can reliably express long-term retention for distributed training sessions at a 60-sec ISI, making the system a candidate for further investigations into the cellular processes supporting memory.     

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.     

Similarities between human and animal spatial memory: Item and order information

Human subjects, sitting at the center of a circle of eight lights, were tested on analogues of radial-maze item-recognition (Roberts & Smythe, 1979) and order-recognition (Kesner & Novak, 1982) tasks. Subjects in the item-recognition condition saw a list of seven lights, and then the nonlist (eighth) light was tested against the first, fourth, or seventh light from the list. The subjects were required to point toward the nonlist light. Subjects in the order-recognition condition saw a series of eight lights, followed by a test of the first and second, fourth and fifth, or seventh and eighth serial positions. They were asked to point toward the light with the earlier serial position. Subjects’ item-recognition serial-position curves exhibited a recency effect with a 0-sec retention interval (Experiments 1 and 2), and were U-shaped (Experiment 1) or flat (Experiment 2) with a 30-sec retention interval. Subjects’ order-recognition serial-position curves were U-shaped at both retention intervals. Subjects’ reported mnemonics were, generally, unrelated to their choice accuracy. The results suggest analogous memory processes in animals and humans.     

Systematic errors in pigeons’ memory for event duration: Interaction between training and test delay

Pigeons trained to choose different stimuli following short- and long-duration signals make disproportionately more “short” choices (i.e., “choose-short errors”) following an increase in the retention interval and more “choose-long errors” following a decrease in this delay. The present experiment provided a systematic investigation of how these selective errors depend on the relationship between the training delay and the test delay. Pigeons were first trained with a 0-sec delay between the signal (2- or 8-sec food presentations) and the choice stimuli (red- and blue-lit keys). On subsequent test trials with 5- and 10-sec delays, choose-short errors predominated. Next, the birds were trained with a constant 10-sec delay and then tested with shorter or longer delays on some trials. The birds now responded accurately and without selective errors at the 10-sec training delay, but made choose-long errors at shorter delays and choose-short errors at longer delays. Finally, the birds were trained with a constant 20-sec delay and then tested with shorter and longer delays. Choose-long errors again appeared at shorter test delays, choose-short errors at longer test delays, and no differential errors at the 20-sec training delay. The selectivity of these errors generally increased with the absolute difference between the training and test delay. Theoretical implications of these results are discussed.     

Ontogenetic forgetting of stimulus attributes

The effects of age on the forgetting of stimulus attributes in a differential fear-conditioning paradigm were examined with 18- and 70-day-old rats tested in either the original conditions or shifted stimulating conditions at one of three retention intervals (1, 48, and 120 h). Adults displayed significant shifts at each retention interval, with those tested in the original context displaying greater fear than those tested in the shifted conditions. By contrast, by 48 h the 18-day-olds had forgotten the specific attributes of the training situation and began treating the two stimulating conditions as functionally equivalent (Experiment 1). In Experiment 2, we tracked the ontogenetic emergence of adult-like memory for stimulus attributes and found a dramatic increase in memory capability by 25 days of age. Experiment 3 illustrated that the forgotten memory attributes of infants may be retrieved by administering a 90-sec cuing treatment 10 min prior to the 48-h test. Implications for the phenomenon of infantile amnesia are discussed.     

Processing of empty and filled time intervals in pigeons

Pigeons were trained initially with 2- and 8-sec empty or filled intervals as sample stimuli. Interval onset and termination was signaled by 1-sec start and stop markers. Following retention and psychophysical testing, both groups were trained with the alternative type of interval, and the tests were repeated. Group empty-first demonstrated a choose-long effect with both empty and filled intervals. Group filled-first demonstrated a weak (and nonsignificant) choose-short effect with filled intervals and a robust choose-long effect with empty intervals. Both groups tended to time the markers and to add that duration to the sample duration only on filled-interval trials. Initial training with empty intervals alters the way pigeons process temporal information on filled-interval trials, whereas initial training with filled intervals has little effect on the processing of temporal information on empty-interval trials.     

Stimulus modality and short-term memory in rats

Two experimental paradigms are presented aimed at determining the retention of auditory and visual information over brief delay intervals. First, a conditional delayed matching-to-sample procedure was used in which rats were required to symbolically match the modality of the sample stimulus with one of two comparison stimuli. In the second experiment, subjects were trained and tested using a Konorski-type procedure. Despite the conceptual and procedural differences between the two procedures, subjects in both experiments showed steeper forgetting functions for visual events than for auditory events, while performance levels at 0-sec delay intervals were equivalent for both stimuli. These results, when taken together with related research conducted with pigeons, suggest that content of memory may have important influences on the short-term retention abilities of animal subjects.     

Effects of intratrial stimulus change on fixed-interval performance: The roles of clock and memory processes

In two experiments, pigeons were exposed to differentially cued training trials of fixed interval (FI) 30 and 60 sec. In addition, shift trials were presented in which the cue associated with one FI value was presented for a prearranged duration at trial onset, followed by offset of that cue and presentation of the other cue. Response-contingent reinforcement was scheduled during the second cue. During the first shift phase, the FI 30-sec cue was shifted to the FI 60-sec cue; in a second phase, the order of the cue shift was reversed. Inferences about accumulator and memory functions of the internal clock were based upon behavior during both training trials and shift trials. At the end of both shift phases, test-trial FI functions generally superimposed in a manner consistent with accumulator reset on cue shift. Individual differences in clustering of functions were accommodated by variation in reference-memory storage across subjects. This interpretation was tested in Experiment 2 by constraining reference-memory storage on shift trials. These conditions yielded a decrease in between-subject variability and provided data consistent with accumulator reset and control by a single reference-memory value on shift trials.     

Primacy effects in animal memory and human nonverbal memory

Evidence for primacy effects in animals’ list memory is accumulating, despite assertions that these primacy effects may be list-initiation-response artifacts (D. Gaffan, 1983; E. Gaffan, 1992). This evidence comes from list-memory experiments with pigeons and monkeys in which primacy changed with retention interval, experiments with monkeys in which primacy correlated with list length, and experiments with monkeys in which there were no list-initiation responses. Furthermore, there is growing evidence that animal memory is similar to, at least, the nonverbal part of human memory. This evidence comes from human nonverbal-memory experiments in which primacy changed with retention interval (similar to animals) when using kaleidoscope or snowflake stimuli, and similar experiments in which the verbal/nonverbal component was manipulated. Conditions conducive for obtaining primacy effects are discussed.     

Stimulus duration and conditioned reinforcing value measured by a learning-tests procedure

The relationship between the duration of stimuli and their conditioned reinforcing effect was investigated using a learning-tests procedure. In Experiment 1, stimuli were the same duration on training (stimulus → reward) and test (choice response → stimulus). Ten- and 30-sec stimuli provided effective differential conditioned reinforcement but 3-sec stimuli did not. In Experiment 2, different pigeons had each combination of the 3- and 30-sec stimuli on training and test trials. Evidence of conditioned reinforcement was obtained only for the birds with 30-sec stimuli on both training and test. The results were interpreted as indicating that stimuli become effective conditioned reinforcers on test trials only when their duration exceeds the duration of differential short-term memory cues resulting from a difference in the events that precede them on training and test trials.     

Flexible coding of temporal information by pigeons: Event durations as remember and forget cues for temporal samples

The ability of pigeons to use event durations as remember (R) and forget (F) cues for temporal samples was examined. Pigeons were required to indicate whether a houselight sample stimulus was short (2 sec) or long (6 sec) by pecking a red or a green comparison stimulus. After training with a constant 10-sec delay interval, temporal cues (illumination of the center key) were presented 2 sec after the offset of the temporal samples. For one group, a short (2-sec) temporal cue served as the R cue and a long (6-3ec) temporal cue served as the F cue. This was reversed for a second group of birds. During training, comparison stimuli were always presented following the temporal R cue, but never following the temporal F cue. Tests for the effectiveness of the temporal R and F cues showed that F cues were equally effective in reducing matching accuracy in both groups of birds. It was concluded that pigeons used the duration of the cue to determine whether or not to rehearse the memory code for the temporal sample.     

Effects of extended fixed-interval training on reversed scallops

Two groups of pigeons were used to determine if different amounts of fixed-interval training with an added clock resulted in different local response rates when the clock was reversed. One group of seven pigeons received 120 reinforcements on a fixed-interval 90-sec schedule, while the other group received 1200 reinforcements. Following training, the added clock was reversed in extinction. Reversed scallops were obtained for both of the groups. Only the group with extended training showed an increase in responding during the previously reinforced segment of the interval. This suggests the development of greater temporal control with extended training.