Cognitive imitation in 2-year-old children (<Emphasis Type="Italic">Homo sapiens</Emphasis>): a comparison with rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

Here we compare the performance of 2-year-old human children with that of adult rhesus macaques on a cognitive imitation task. The task was to respond, in a particular order, to arbitrary sets of photographs that were presented simultaneously on a touch sensitive video monitor. Because the spatial position of list items was varied from trial to trial, subjects could not learn this task as a series of specific motor responses. On some lists, subjects with no knowledge of the ordinal position of the items were given the opportunity to learn the order of those items by observing an expert model. Children, like monkeys, learned new lists more rapidly in a social condition where they had the opportunity to observe an experienced model perform the list in question, than under a baseline condition in which they had to learn new lists entirely by trial and error. No differences were observed between the accuracy of each species' responses to individual items or in the frequencies with which they made different types of errors. These results provide clear evidence that monkeys and humans share the ability to imitate novel cognitive rules (cognitive imitation).     

KNOWLEDGE OF THE ORDINAL POSITION OF LIST ITEMS IN RHESUS MONKEYS

Abstract —What is learned during mastery of a serial task: associations between adjacent and remote items, associations between an item and its ordinal position, or both? A dear answer to this question is lacking in the literature on human serial memory because it is difficult to control for a "naive" subject's linguistic competence and extensive experience with serial tasks. In this article, we present evidence that rhesus monkeys encode the ordinal positions of items of an arbitrary list when there is no requirement to do so. First, monkeys learned four nonverbal lists (1–4). each containing four novel items (photographs of natural objects). The monkeys then learned four 4-item lists that were derived exclusively and exhaustively from Lists 1 through 4, one item from each list. On two derived lists, each item s original ordinal position was maintained. Those lists were acquired with virtually no errors. The two remaining derived lists, on which the original ordinal position of each item was changed, were as difficult to learn as novel lists. The immediate acquisition of lists on which ordinal position was maintained shows that knowledge of ordinal position can develop without the benefit of language, extensive list-learning experience, or explicit instruction to encode ordinal information.     

Serial list combination by monkeys (Macaca mulatta): test cues and linking

This investigation assessed prospective bases of non-human primate cognitive operations that support serial list memory. Four macaques learned 3-, 5-item ordered lists of objects (as two-choice problems) and then either did or did not (in a within-subject design) receive training on pairs that linked the three original lists into a 15-item serial order. Next, subjects experienced selective exposure trials on object pairs that either maintained or contrasted to the serial position relationships seen during original learning. Subsequent comprehensive tests assessed the interactive effects of linking and exposure conditions on choosing in accord with a combined 15-item serial order. Linking readily induced monkeys to merge lists into a 15-item order, but restricting early exposure to pairs with the same positional relationships as original training slowed, but did not prevent, list combination. Exposure to positional relationships congruent with the combined (15-item) list and different from those of original 5-item training aided both expression of the linking effect and acquisition after no link training. Thus, list linking facilitated serial reorganization by inducing release from error derived from memory for prior learned positional relationships. The task was recommended as a prospective evaluator of continuity of cognitive processes among species.     

Visual list memory in capuchin monkeys (Cebus apella)

Memory of 3 capuchin monkeys, Cebus apella, was tested with lists of 4 travel-slide pictures and different retention intervals. They touched different areas of a video monitor to indicate whether a test picture was in a list. At short retention intervals (0 s, 1 s, 2 s), memory was good for the last list items (recency effect). At a 10-s retention interval, memory improved for 1st list items (primacy effect). At long retention intervals (20 s and 30 s), primacy effects were strong and recency effects had dissipated. The pattern of retention-interval changes was similar to rhesus monkeys, humans, and pigeons. The time course of recency dissipation was similar to rhesus monkeys. The capuchin's superior tool-use ability was discussed in relation to whether it reflects a superior general cognitive ability, such as memory. In terms of visual memory, capuchin monkeys were not shown to be superior to rhesus monkeys.     

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.     

Serial expertise of rhesus macaques

Here we describe the development of serial expertise in 4 experimentally naive rhesus monkeys that learned, by trial and error, the correct order in which to respond to 3-, 4-, and 7-item lists of arbitrarily selected photographs. The probabilities of guessing the correct sequence on 3-, 4-, and 7-item lists were, respectively, 1/6, 1/24, and 1/5040. Each monkey became progressively more efficient at determining the correct order in which to respond on new lists. During subsequent testing, the subjects were presented with all possible pairs of the 28 items used to construct the four 7-item lists (excluding pairs of items that occupied the same ordinal position in different lists). Subjects responded to pairs from different lists in the correct order 91% of the time on the first trials on which these pairs were presented. These features of subjects' performance, which cannot be attributed to procedural memory, satisfy two criteria of declarative memory: rapid acquisition of new knowledge and flexible application of existing knowledge to a new problem.     

Serial list linking by macaque monkeys (Macaca mulatta): list property limitations

Four sophisticated macaque monkeys (Macaca mulatta) learned 6 different, 15-item ordinal lists (via conditional, 2-choice discriminations) as part of a study assessing some properties of serial list memory in monkeys. After assuring that the first 3 lists were well retained, the researchers attempted to link these by training only the 2 end-item pairs that ordered all 45 items into an inclusive series. A 20-day test of possible pairings among these 45 items was then conducted. Subsequently, the other 3 lists were trained and tested for retention, but no link training was provided. Then, a test like the one that had followed linking was administered. Unlike previous outcomes with three 5-item lists, linking did not yield immediate merger of three 15-item lists into a 45-item list, although 45-item lists were acquired after sufficient exposure to the testing/training regimen under both linking and nonlinking conditions. List length as a limiting factor in linking suggested processing restrictions analogous to those observed in human list memory. Results supported further investigation of list-linking characteristics.     

A primacy effect in monkeys when list position is relevant

In Experiment 1 (1a and 1b), Rhesus monkeys (Macaca mulatta) learned lists of two-choice visual discriminations in which list position was relevant to discrimination performance. For example, Stimulus A was the rewarded stimulus if it was presented at List Position 1, but was not rewarded if it was presented at any other position in the list; similarly, Stimulus B was rewarded only at List Position 2, and so on. In learning these lists, all animals showed a marked primacy effect. In Experiment 2 (2a and 2b), Rhesus monkeys and Cynomolgus monkeys (M. fascicularis) learned lists of visual discriminations in which each visual stimulus occupied a fixed position in a list, but list position was not relevant to discrimination performance. For example, Stimulus E was always rewarded, and was always presented at List Position 1. To increase the salience of list beginning as a distinctive event, successive presentations of the list were separated by 24-hr intervals. In Experiment 2 there was no primacy effect, however. These results show for the first time that a primacy effect can be obtained in visual discrimination learning by monkeys. Furthermore, they suggest that it is obtained only when list position is relevant to the discrimination learning task.     

Mechanisms of same/different abstract-concept learning by rhesus monkeys (Macaca mulatta)

Experiments with 9 rhesus monkeys (Macaca mulatta) showed, for the first time, that abstract-concept learning varied with the training stimulus set size. In a same/different task, monkeys required to touch a top picture before choosing a bottom picture (same) or white rectangle (different) learned rapidly. Monkeys not required to touch the top picture or presented with the top picture for a fixed time learned slowly or not at all. No abstract-concept learning occurred after 8-item training but progressively improved with larger set sizes and was complete following 128-item training. A control monkey with a constant 8-item set ruled out repeated training and testing. Contrary to the unique-species account, it is argued that different species have quantitative, not qualitative, differences in abstract-concept learning.     

The influence of acoustic and semantic similarity on long-term memory for word sequences

It has been shown that short-term memory (STM) for word sequences is grossly impaired when acoustically similar words are used, but is relatively unaffected by semantic similarity. This study tests the hypothesis that long-term memory (LTM) will be similarly affected. In Experiment I subjects attempted to learn one of four lists of 10 words. The lists comprised either acoustically or semantically similar words (A and C) or control words of equal frequency (B and D). Lists were learned for four trials, after which subjects spent 20 min. on a task involving immediate memory for digits. They were then asked to recall the word list. The acoustically similar list was learned relatively slowly, but unlike the other three lists showed no forgetting. Experiment II showed that this latter paradox can be explained by assuming the learning score to depend on both LTM and STM, whereas the subsequent retest depends only on LTM. Experiment III repeats Experiment I but attempts to minimize the effects of STM during learning by interposing a task to prevent rehearsal between the presentation and testing of the word sequences. Unlike STM, LTM proved to be impaired by semantic similarity but not by acoustic similarity. It is concluded that STM and LTM employ different coding systems.     

Serial learning by rhesus monkeys: II. Learning four-item lists by trial and error

Three rhesus macaque monkeys were trained to produce novel 4-item lists (A-->B-->C-->D) on which all items were displayed from the start of training. Subjects were previously trained to produce 4-item lists by adding one item at a time (A, A-->B, A-->B-->C, and A-->B-->C-->D; lists K. B. Swartz et al., 1991). Those lists could be mastered by responding to each new item last. To learn lists on which all items were displayed from the start of training, subjects had to recall the consequences of errors and correct responses to each item. Errors ended the trial; correct responses to A, B, or C allowed the trial to continue. A correct response to D produced food reward. Although the probability of executing a 4-item list correctly by chance was .04, each subject mastered 4 novel 4-item lists by trial and error. The ability of monkeys to use a trial-and-error strategy to learn novel lists provides a basis for studying the development of serial expertise in animals.     

Linking of serially ordered lists by macaque monkeys (Macaca mulatta): list position influences

Five monkeys (Macaca mulatta) were trained on 2 sets of 3 5-item serially ordered lists. Then, each set was either linked or not in a counterbalanced, within-subject design. Linking entailed training on the 2 pairs that ordered the 3 5-item lists into a single overall 15-item series. Choices on novel pairings after linking conditions attempted to define the unique contributions of knowledge of within-list ordinal position and between-lists link training. With linkage, the series was immediately treated as a 15-item ordered list. Without linkage, choices reflected list positions from initial learning, but continued testing with directional reward yielded gradual ordering into a 15-item list. Apparently, monkeys remembered and used initial list-position information, but linkage allowed inference of an integrated serial relationship among items. Results supported primate list memory as an organizational process.     

An experimental analysis of memory processing

Rhesus monkeys were trained and tested in visual and auditory list-memory tasks with sequences of four travel pictures or four natural/environmental sounds followed by single test items. Acquisitions of the visual list-memory task are presented. Visual recency (last item) memory diminished with retention delay, and primacy (first item) memory strengthened. Capuchin monkeys, pigeons, and humans showed similar visual-memory changes. Rhesus learned an auditory memory task and showed octave generalization for some lists of notes--tonal, but not atonal, musical passages. In contrast with visual list memory, auditory primacy memory diminished with delay and auditory recency memory strengthened. Manipulations of interitem intervals, list length, and item presentation frequency revealed proactive and retroactive inhibition among items of individual auditory lists. Repeating visual items from prior lists produced interference (on nonmatching tests) revealing how far back memory extended. The possibility of using the interference function to separate familiarity vs. recollective memory processing is discussed.     

Response strategies in list learning by orangutans (Pongo pygmaeus x P. abelii)

Rhesus monkeys (Macaca mulatta) develop strategies to acquire and execute serial lists (K. B. Swartz & S. A. Himmanen, 2001). Serial probe recognition studies of list memory have demonstrated similarities across monkeys and humans (S. F. Sands & A. A. Wright, 1980). The present study extended the investigation of list learning and memory to determine whether orangutans (Pongo pygmaeus x P. abelii) would show evidence of subjective organization of photographic lists in a manner similar to that shown by humans learning a list of unrelated words (E. Tulving, 1962). No evidence for the effective use of a subjective organization strategy was found, but the orangutans developed a right-to-left spatial response strategy, which emerged during the acquisition of 5-item lists. This strategy was an effective way to reduce the load on working memory when presented with a complex array of items.     

The simultaneous learning effect: why does simultaneous task learning improve retention?

Despite the prevalence of encoding variables that have been shown to influence the rate of learning, very few affect the rate of forgetting of verbal material. However, when a list of words is learned simultaneously with other lists, the rate of forgetting is markedly lower than that of single-task learning. Although the magnitude of this simultaneous learning effect is large compared with typical list learning effects, it has received little empirical attention. Experiments 1 and 2 tested the hypothesis that the simultaneous learning effect is the result of a differential contribution of short-term memory during encoding. The results showed that the advantage for simultaneous task learning was obtained even under conditions that minimized the potential effects of short-term memory. Experiment 3 revealed that the simultaneous learning effect was larger when the specific items learned simultaneously were the same on each learning trial than when they were different. This finding supported a cuing explanation of the effect: the items from the other lists act as retrieval cues during delayed recall.     

Ordinal-list integration for symbolic, arbitrary, and analog stimuli by rhesus macaques (Macaca mulatta)

Two numeral-trained monkeys learned to produce 3 5-item lists of Arabic numerals, colors, and arbitrary signs in the correct sequence. The monkeys then responded at above-chance levels when the authors tested them with nonrewarded pair-wise comparisons of items from different lists, indicating their use of ordinal-position information. The authors also tested the monkeys with nonrewarded pair-wise comparisons of an analog quantity and an item from 1 of the 3 learned lists. Although the monkeys were not trained to serially order analog quantities, 1 monkey correctly integrated the analog quantities with the lists of numerals, colors, and signs. The consistent use of an ordinal rule, despite different types of training and varying degrees of experience with the 4 types of stimuli, suggested that the monkey had a robust concept of ordinality.     

Testing complex animal cognition: Concept learning,proactive interference,and list memory

This article describes an approach for assessing and comparing complex cognition in rhesus monkeys and pigeons by training them in a sequence of synergistic tasks, each yielding a whole function for enhanced comparisons. These species were trained in similar same/different tasks with expanding training sets (8, 16, 32, 64, 128 … 1024 pictures) followed by novel‐stimulus transfer eventually resulting in full abstract‐concept learning. Concept‐learning functions revealed better rhesus transfer throughout and full concept learning at the 128 set, versus pigeons at the 256 set. They were then tested in delayed same/different tasks for proactive interference by inserting occasional tests within trial‐unique sessions where the test stimulus matched a previous sample stimulus (1, 2, 4, 8, 16 trials prior). Proactive‐interference functions revealed time‐based interference for pigeons (1, 10 s delays), but event‐based interference for rhesus (no effect of 1, 10, 20 s delays). They were then tested in list‐memory tasks by expanding the sample to four samples in trial‐unique sessions (minimizing proactive interference). The four‐item, list‐memory functions revealed strong recency memory at short delays, gradually changing to strong primacy memory at long delays over 30 s for rhesus, and 10 s for pigeons. Other species comparisons and future directions are discussed.     

Reversible Verbal Memory Integration Deficits in Obstructive Sleep Apnoea

When presented with novel but semantically related elements after learning verbal material, healthy participants tend to endorse these items as previously learned. This reflects the normal integration and association of novel verbal information into long-term memory. How obstructive sleep apnoea (OSA) negatively impacts verbal memory performance, and whether deficits are reversible following positive airway pressure (PAP) treatment, remain elusive. We investigated immediate and delayed OSA- and PAP treatment-related effects on verbal memory integration, using a false memory paradigm. Twenty-three patients with OSA learned lists of words semantically related to target non-presented words (1) at baseline after a polysomnography diagnosis night, (2) after a consecutive polysomnography night under PAP titration, and (3) after three months of compliant PAP treatment. At each session, participants learned 10 different lists of words, each list comprising 15 semantically related items. They had then to recognize 15 minutes later (after an intermediate vigilance task) previously learned words within a list including studied words (learned), unstudied but semantically related items (lures), and non-related unstudied items (controls). Sleep quality and fatigue questionnaires, and psychomotor vigilance tests (PVT) were administered at each session. PAP treatment led to OSA remission and improvement in objective and subjective sleep quality. Crucially, recognition of learned and lure words increased after the first night under treatment and remained stable three months later, suggesting successful memory integration and restoration of semantic processes. No treatment-related outcome was found on PVT performance. OSA exerts a detrimental but PAP-reversible effect on verbal learning and semantic memory integration mechanisms underlying the acquisition of novel memory representations.     

Auditory list memory and interference processes in monkeys.

Memory of 2 rhesus monkeys (Macaca mulatta) was tested in a serial probe recognition task with lists of 4 natural or environmental sounds, different retention intervals, and different manipulations of interference. At short retention intervals, increasing the separation of list items reduced the primacy effect and produced a recency effect. Similar results were shown by increasing interference across lists through item repetitions or making the first 2 list items high-interference items. These results indicated that decreasing first-item performance reduced proactive interference on memory of the last list items. At long (20 s) retention intervals, making the last list items of high interference reduced the recency effect, reduced retroactive interference, and produced a primacy effect. Taken together, interference plays a role in determining the primacy and recency effects of the serial-position function.     

How is the serial order of a verbal sequence coded? Some comparisons between models

Current models of verbal short-term memory (STM) propose various mechanisms for serial order. These include a gradient of activation over items, associations between items, and associations between items and their positions relative to the start or end of a sequence. We compared models using a variant of Hebb's procedure in which immediate serial recall of a sequence improves if the sequence is presented more than once. However, instead of repeating a complete sequence, we repeated different aspects of serial order information common to training lists and a subsequent test list. In Experiment 1, training lists repeated all the item-item pairings in the test list, with or without the position-item pairings in the test list. Substantial learning relative to a control condition was observed only when training lists repeated item-item pairs with position-item pairs, and position was defined relative to the start rather than end of a sequence. Experiment 2 attempted to analyse the basis of this learning effect further by repeating fragments of the test list during training, where fragments consisted of either isolated position-item pairings or clusters of both position-item and item-item pairings. Repetition of sequence fragments led to only weak learning effects. However, where learning was observed it was for specific position-item pairings. We conclude that positional cues play an important role in the coding of serial order in memory but that the information required to learn a sequence goes beyond position-item associations. We suggest that whereas STM for a novel sequence is based on positional cues, learning a sequence involves the development of some additional representation of the sequence as a whole.