Primacy in animals’ working memory: Artifacts

In response to commentaries on an earlier review (Gaffan, 1992), it is acknowledged that there is more recent evidence for primacy in animals’ list memory, which is not susceptible to the methodological criticisms discussed in the review. However, methods advocated by the commentators are liable to produce spurious assessments of primacy, and the original objections still stand.     

Recognition memory for lists of visual stimuli in monkeys and humans

In Experiment 1, short-term memory for lists of visual stimuli was studied in four squirrel monkeys (Saimiri sciureus). A delayed-matching procedure was used in which a subject was presented with lists containing one, three, or six stimulus patterns, and memory for serial positions was probed by requiring the subject to choose between a list item and a nonlist item. The rate of item presentation was varied, as was the delay between the final item on a list and the retention test. In Experiment 2, the same procedures were used to compare recognition memory in four monkeys and four humans. Although differences in the levels and shapes of the serial-position curves appeared between species, both monkeys and humans showed primacy and recency effects. The presentation time of stimuli had a negligible effect on performance in both monkeys and humans, whereas delay significantly affected human retention but not monkey retention.     

Interstimulus interval and viewing time effects in monkey list memory

Two rhesus monkeys were tested in 6- and 10-item list memory tasks for performance changes as a function of the exposure duration of the list stimuli and the interstimulus interval (ISI) between successive list stimuli. Accuracy increased with longer item exposure duration and tended to decrease with longer ISI duration. Humans, by contrast, typically show increases in accuracy with ISI, a result taken as evidence of rehearsal. The decrease in accuracy for monkeys suggests that they were not using rehearsal processes in these list memory experiments. Further tests in which choice accuracy with predictable ISIs was compared with choice accuracy with unpredictable ISIs also yielded no evidence of rehearsal by the monkeys. This apparent absence of rehearsal mechanisms in monkeys, in situations also shown to support human rehearsal, is discussed as a potential difference in the visual working memory processes of the two species.     

Rats do show primacy and recency effects in memory for lists of spatial locations: A reply to Gaffan

It has been demonstrated that rats display both primacy and recency effects in list-learning experiments for both item- and order-recognition memory for spatial location information. Contrary to a suggestion made by Gaffan (1992) that previous demonstrations of primacy effects in rats are not valid due to statistical and methodological problems, we show that (1) it is not likely that our results are due to experimenter bias and/or nonindependence of trials, (2) primacy and recency effects are obtained whether or not one uses a training criterion, and (3) when many of the published reports from our laboratory are combined, the number of subjects and trials are sufficient to evaluate the validity of primacy and recency effects in list-learning experiments.     

Rats’ memory for serially presented flavors: Effects of interstimulus interval and generalization decrement

In four experiments, the effect of sequential exposure to a series of five novel flavors on the subsequent neophobic response of water-deprived rats to those flavors when they were presented simultaneously was examined. After a list-test interval of 30 min and a list-interstimulus interval of 10 sec, the rats generally consumed more of the first and last flavors presented in the initial sequence. This finding was taken to reflect the existence of primacy and recency effects. Experiment 1 provided evidence that successive contamination can occur between flavors in the initial list, making subsequent recognition of later flavors in the list more difficult. However, this effect was overcome by presentation of water between each flavor during the list exposure. Experiments 2 and 4 showed that primacy was not a necessary result of successive contamination in this procedure, by demonstrating that increasing the interstimulus interval between list items decreased the size of the primacy effect. This result suggests that rats’ memory for serially presented items may be controlled by mechanisms different from those typically implicated in the human verbal memory literature. In Experiment 3, the question of whether the testing procedure adopted here could have introduced sources of artifactually produced serialposition effects was explored, but no such influence was found.     

Comparing cognition by integrating concept learning,proactive interference,and list memory

This article describes an approach for training a variety of species to learn the abstract concept of same/different, which in turn forms the basis for testing proactive interference and list memory. The stimulus set for concept-learning training was progressively doubled from 8, 16, 32, 64, 128 . . . to 1,024 different pictures with novel-stimulus transfer following learning. All species fully learned the same/different abstract concept: capuchin and rhesus monkeys learned more readily than pigeons; nutcrackers and magpies were at least equivalent to monkeys and transferred somewhat better following initial training sets. A similar task using the 1,024-picture set plus delays was used to test proactive interference on occasional trials. Pigeons revealed greater interference with 10-s than with 1-s delays, whereas delay time had no effect on rhesus monkeys, suggesting that the monkeys’ interference was event based. This same single-item same/different task was expanded to a 4-item list memory task to test animal list memory. Humans were tested similarly with lists of kaleidoscope pictures. Delays between the list and test were manipulated, resulting in strong initial recency effects (i.e., strong 4th-item memory) at short delays and changing to a strong primacy effect (i.e., strong 1st-item memory) at long delays (pigeons 0-s to 10-s delays; monkeys 0-s to 30-s delays; humans 0-s to 100-s delays). Results and findings are discussed in terms of these species’ cognition and memory comparisons, evolutionary implications, and future directions for testing other species in these synergistically related tasks.     

Serial position effects in social transmission of food preference: Retention/demonstration intervals

The effects of retention and demonstration intervals on serial position were evaluated in two experiments with Long-Evans rats. A list of 3 demonstrators that had eaten one of three flavored foods was presented to naive observers. In Experiment 1, there were four groups, three groups with a retention interval compared with one group with a zero retention interval or no retention interval. In Experiment 2, the demonstration interval was reduced. Intervals of 15, 5, 2, and 1 min were used. In Experiment 1, primacy decreased gradually in the four groups as the retention interval was increased in duration. In Experiment 2, primacy also decreased gradually, and recency occurred with the 1-min demonstrator interval. The increase in the duration of the retention interval reduced primacy. The reduction in the duration of the demonstration interval decreased primacy and produced recency.     

Primacy,recency, and the variability of data in studies of animals’ working memory

The performance measures in many experiments on animal memory are expected to have an underlying binomial distribution, with additional variance contributed, for example, by between- subject differences. This paper examines whether the data from published studies of serial position effects (primacy and recency) in animals’ working memory conform to that expectation. In most cases, the variance, when it can be estimated, is consistent with those statistical assumptions, but in certain studies, it is significantly smaller than expected. This is usually a sign of faulty procedure or analysis, and possible causes are discussed. The conclusion is that much of the evidence for primacy in animals is unsatisfactory, on statistical or other methodological grounds. The analytic approach outlined here might usefully be applied to detect potential problems with other experiments of a similar type, especially when manually operated apparatus is employed, and to improve their statistical power.     

Visual recognition memory in squirrel monkeys

Squirrel monkeys (Saimiri sciureus) were trained on visual recognition memory tasks in a Wisconsin General Testing Apparatus with a trial-unique procedure that used 250 objects as stimuli. In Experiment 1, acquisition of a trial-unique delayed non-match-to-sample task (DNMS) was compared with acquisition of a trial-unique delayed match-to-sample (DMS) task. The DNMS task was learned in significantly fewer trials and with significantly fewer errors. Two animals in the DNMS group demonstrated highly accurate retention of the DNMS strategy despite an 11-month hiatus in experimental testing. In Experiment 2, the same procedures were used to study the learning of lists of 3, 5, 10, or 20 serially presented items. Although the animals were able to accurately remember lists of up to 20 items, there was no evidence of serial position effects.     

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.     

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.     

Pigeons exhibit higher accuracy for chosen memory tests than for forced memory tests in duration matching-to-sample

Following training to match 2- and 8-sec durations of feederlight to red and green comparisons with a 0-sec baseline delay, pigeons were allowed to choose to take a memory test or to escape the memory test. The effects of sample omission, increases in retention interval, and variation in trial spacing on selection of the escape option and accuracy were studied. During initial testing, escaping the test did not increase as the task became more difficult, and there was no difference in accuracy between chosen and forced memory tests. However, with extended training, accuracy for chosen tests was significantly greater than for forced tests. In addition, two pigeons exhibited higher accuracy on chosen tests than on forced tests at the short retention interval and greater escape rates at the long retention interval. These results have not been obtained in previous studies with pigeons when the choice to take the test or to escape the test is given before test stimuli are presented. It appears that task-specific methodological factors may determine whether a particular species will exhibit the two behavioral effects that were initially proposed as potentially indicative of metacognition.     

A bowed serial-position function in habituation of sequential stimuli

The effect of serial position was examined in a study of habituation of the vasoconstrictive orienting response in rabbits. In a procedure analogous to a recognition memory test, subjects received multiple exposures to an invariant list of stimuli before their response was assessed to an isolated item that had consistently occupied either the first, middle, or last position in the list. A reliably bowed serial-position function was obtained, with the least habituation (poorest retention) occurring for the item that had occupied the middle position in the list. The finding of both a primacy and a recency effect parallels the most general finding in studies of human memory and encourages a compatible account of habituation in infrahuman subjects. The result was discussed in terms of the opportunities for differential rehearsal of list items and contextual cues at different positions in the list.     

Monkey auditory list memory: tests with mixed and blocked retention delays

A rhesus monkey was tested in an auditory list memory task with blocked and mixed retention delays. Each list of four natural or environmental sounds (from a center speaker) was followed by a retention delay (0, 1, 2, 10, 20, or 30 sec) and then by a recognition test (from two side speakers). The monkey had been tested for 12 years in tasks with blocked delays. An earlier (4 years prior) blocked-delay test was repeated, with virtually identical results. The results from the mixed-delay test were likewise similar. Thus, the peculiarities of blocked-delay testing, such as delay predictability or differences in list spacing, apparently do not alter this monkey’s memory for auditory lists. It is concluded from this and other evidence that the monkey’s serial position functions reflect mnemonic processes that change with changes in retention delay and are not artifacts of the blocked-delay procedure. The nature of the monkey’s auditory memory is discussed.     

In search of consolidation of short-term memory in nonhuman animals

Wixted (Annual Review of Psychology, 55, 235 – 269, 2004) has argued that forgetting is due to consolidation failure. Previous research with humans and nonhuman animals has reported evidence for consolidation in intermediate or long-term memory (LTM). The present study examines whether consolidation occurs in short-term memory in pigeons. Delayed matching-to-sample accuracy was reduced when retroactive interference (an extraneous task in Experiment 1 or houselight illumination in Experiment 2) was interpolated in the retention interval. Accuracy was not greater, however, when interference occurred at the end of the retention interval, as compared with when it occurred at the beginning. That is, there was no evidence for consolidation in short-term memory for pigeons. We did find, however, the beginning–end effect originally reported by Roberts and Grant (Journal of Experimental Psychology: Animal Behavior Processes, 4, 219–236, 1978) and the recovery from forgetting reported by White and Brown (Journal of the Experimental Analysis of Behavior, 96, 177–189, 2011). The results are discussed in relation to temporal distinctiveness theory as an alternative to consolidation.     

Proactive interference in monkeys: Delay and intersample interval effects are noncomparable

Two prominent theories of proactive interference in animal memory predict that the effects of varying the interval between the interfering and to-be-remembered stimulus in a delayed-matching-to-sample paradigm ought to be comparable to the effects of manipulating the retention interval. To assess this prediction, monkeys were tested in a situation in which a sample was presented, followed by a variable intersample interval, whereupon a second sample was presented. After a delay interval, a choice test was given between the two stimuli that had served as samples. The correct choice was always the most recently presented sample stimulus, and the initial sample of a sequence provided a potential source of proactive interference. In two experiments, delay interval altered performance, whereas interstimulus interval had little or no effect. In a third experiment, using a small set of sample stimuli, intertriai interval altered proactive interference, but again interstimulus interval had no effect. One way of accounting for these data is in terms of distinct short- and long-term memory processes.     

Contextual cues and memory retrieval in rats: Alleviation of forgetting by a pretest exposure to background stimuli

With a relatively complex maze, reliable forgetting is clearly seen when the training-test interval is 25 days. This forgetting is evidenced by the longer time taken to run the maze and in an increase in the number of errors from the last training trial to the first test trial. In this case, forgetting is a lapse, not a loss, since performance attains the last training trial level at a subsequent test. Furthermore, a reminder which does not in itself contain sufficient information to facilitate performance of a naive animal, significantly improves maze performance of animals which have “forgotten,” even on the first retention test. With the use of additional control groups, it is shown that there must be a memory lapse before contextual cues can be demonstrated to be effective in facilitating memory retrieval.     

Rat spatial memory: Resistance to retroactive interference at long retention intervals

An attempt was made to disrupt memory for spatial information by interpolating a task of high similarity to the to-be-remembered task during a long retention interval. Rats were trained in an 8-arm maze in which choosing each arm without repetition was the optional strategy. A 4-h delay was imposed between the 4th and 5th choices. At various times during the retention interval, the rats ran a second identical maze located in another room. No evidence of retroactive interference was observed. In the second experiment, the rat was required to remember the interpolated spatial task during the retention test. This was accomplished by allowing the rat to make four choices in the first maze and then, after a variable period of time, four choices in the second maze. Four hours after exposure to each maze, retention was tested. Choice accuracy on the retention tests was high and equivalent on both mazes. Requiring the rat to remember which arms it had visited in a second maze did not impair memory for the first maze. These results demonstrate that rats can segregate spatial memories established in different contexts with considerable proficiency.     

Short-term memory for haptic cues in monkeys (Macaca mulatta)

Short-term memory (STM) for haptic information was examined in a delayed matching-to-sample (DMTS) task. Three rhesus monkeys were tested in DMTS with all possible combinations of different-size spheres and cubes as the sample and comparison stimuli. The results showed that the decrease in percentage correct as a function of the retention intervals was relatively independent of the size and shape of the sample and comparison stimuli. In general, at each retention interval, percentage correct was higher when the (1) comparison stimuli differed in both size and shape than when the comparison stimuli differed in only size or shape, (2) size differences between the comparison stimuli increased, and (3) samples were spheres rather than cubes. This pattern of results suggests that dimensions of the haptic stimuli influenced discrimination but had little effect on the animals’ STM. In Experiment 2, the same three monkeys responded to the sample and comparison stimuli with the same hand or responded to the sample with one hand and the comparison stimuli with the opposite hand. The decrease in percentage correct across retention intervals was comparable for all possible hand combinations. These results suggest that the loss of information from STM is comparable when the sample and comparison stimuli are both felt with the same hand or with opposite hands.     

Short-term memory,phonological processing,and reading ability

Verbal short-term memory deficits are a common characteristic of children with reading problems and may markedly increase the difficulty of learning to read. Previous work suggests that the basis of the short-term memory deficit may involve limitations in phonetic coding. In the present paper, a series of experiments are reviewed which examined the role of phonological processes in short-term memory. First, a developmental study is described in which a significant relationship was found between phonetic processes and verbal memory span, but not between phonetic processes and nonverbal memory. Second, additional studies are reviewed which collectively found that children with reading problems are less accurate at phonetic encoding than are good readers, and that performance on phonetic processing corresponds with verbal memory span. No reading group differences were obtained on nonverbal perception or memory tasks. These findings suggest that both developmental and individual differences in verbal memory span are related to the efficiency of phonological processes. Practical implications of current cognitive research are discussed. The research was supported by NIH Grant HD-01994 to Haskins Laboratories.