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.     

Chunking during serial learning by a pigeon: II. Integrity of a chunk on a new list

Can a group of items that a pigeon chunks on one list function as such on a second list? In Experiment 1, the ordinal position of the chunk was held constant across both lists. Following training on a list of colors and achromatic geometric forms (A----B----C----D'----E'), the integrity of the color chunk [A----B----C] was maintained on a list of five colors (A----B----C----F----G) even though the basis for establishing that chunk was eliminated. The integrity of the chunk [A----B----C] was also maintained on a new list of colors and forms (A----B----C----D*----E*). In Experiment 2, the ordinal position of a chunk established on list1 (A----B----C'----D') was changed on list 2. As shown by positive transfer between lists 1 and 2, the integrity of the chunks [A----B] and [C'----D'] was maintained on lists X'----A----B----Y' and X'----C'----D'----Y', respectively. Conversely, the heterogeneous list X'----B----C'----Y' took longer to learn than the original list.     

A positional coding mechanism in pigeons after learning multiple three-item lists

Pigeons were trained on three three-item lists (List 1: A₁ → B₁ → C_1; List 2: A₂ → B₂ → C_2; List 3: A₃ → B₃ → C₃). After sessions in which any one of the three lists could be presented on a trial, derived-maintained list and derived-changed list probe trials were introduced. The derived list probe trials were composed of three items, one drawn from each of the training lists. On derived-maintained probe trials, each item was in the same ordinal position it occupied during training (e.g., A₃ → B₁ → C₂). On derived-changed probe trials, items that occupied the second and third position during training were exchanged (e.g., A₂ → C₃ → B₁). The performance of subjects on derived-maintained probe trials was significantly above chance and no different to that observed on the training lists. In contrast, subjects’ performance on derived-changed probe trials was significantly below chance. To our knowledge, this is the first study that has demonstrated pigeons are able to learn and retain multiple three-item lists. In addition, subjects’ performance on the derived-maintained probe trials suggests that they acquire knowledge of each list item’s ordinal position when learning multiple lists.     

“Counting” serially presented stimuli by human and nonhuman primates and pigeons

Much of Stewart Hulse's career was spent analyzing how animals can extract patterned information from sequences of stimuli. Yet an additional form of information contained in a sequence may be the number of times different elements occurred. Experiments that required numerical discrimination between different stimulus items presented in sequence are analyzed for primates and pigeons. It is shown that a model based on magnitude discrimination can account well for data from human and nonhuman primate experiments. Similar experiments carried out with pigeons showed a strong recency effect not found with primates. The pigeon data are modeled successfully, however, by assuming that representations of events decay as other events are presented.     

Pigeons' categorization may be exclusively nonanalytic

Recent theoretical and empirical developments in human category learning have differentiated an analytic, rule-based system of category learning from a nonanalytic system that integrates information across stimulus dimensions. In the present study, the researchers applied this theoretical distinction to pigeons' category learning. Pigeons learned to categorize stimuli varying in the tilt and width of their internal striping. The matched category problems had either a unidimensional (rule-based) or multidimensional (information-integration) solution. Whereas humans and nonhuman primates strongly dimensionalize these stimuli and learn rule-based tasks far more quickly than information-integration tasks, pigeons learned the two tasks equally quickly to the same accuracy level. Pigeons may represent a cognitive system in which the commitment to dimensional analysis and category rules was not strongly made. Their performance could suggest the character of the ancestral vertebrate categorization system from which that of primates emerged.     

Global-feature classification can be acquired more rapidly than local-feature classification in both humans and pigeons

When humans process visual stimuli, global information often takes precedence over local information. In contrast, some recent studies have pointed to a local precedence effect in both pigeons and nonhuman primates. In the experiment reported here, we compared the speed of acquisition of two different categorizations of the same four geometric figures. One categorization was on the basis of a local feature, the other on the basis of a readily apparent global feature. For both humans and pigeons, the global-feature categorization was acquired more rapidly. This result reinforces the conclusion that local information does not always take precedence over global information in nonhuman animals.     

Generalized relational matching by guinea baboons (Papio papio) in two-by-two-item analogy problems

Analogical reasoning is considered the hallmark of human reasoning, but some studies have demonstrated that language- and symbol-trained chimpanzees can also reason analogically. Despite the potential adaptive value of this ability, evidence from other studies strongly suggests that other nonhuman primates do not have this capacity for analogical reasoning. In our three experiments, 6 of 29 baboons acquired the ability to perform a relational matching-to-sample (RMTS) task in which pairs of shapes composed relational displays. Five of these 6 monkeys then transferred this ability to RMTS tasks using novel exemplars of identity (elements in a pair are the same) and nonidentity (elements in a pair are different) relations. This transfer occurred even on trials in which the incorrect pair shared an element with the sample pair with which it was being compared. The baboons retained this ability 12 months later. The findings from our study of symbol-naive monkeys indicate that although language and symbol training facilitate conceptual thinking in nonhuman primates, such training is not a prerequisite for analogical reasoning.     

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).     

Noncontingent reinforcement competes with response performance

Noncontingent reinforcement is a commonly used procedure to decrease levels of problem behavior. Goals of this intervention are to decrease motivation, responding, and the functional relation between behavior and consequences, but it could also possibly compete with performance of alternative desirable responses. In the current study, we assessed the effects of noncontingent reinforcement arranged from 0% to 100% of sessions on performance of alternative responding across two experiments. Experiment 1 assessed manding (i.e., requests) maintained by attention and tangibles with a child with developmental disabilities and Experiment 2 assessed keypecking maintained by food with six pigeons. We extended previous research by (a) showing that noncontingent reinforcement competes with both the acquisition and maintenance (performance) of an alternative response, (b) extending the generality of the findings across nonhuman and human participants, and (c) eliminating influence of sequence effects through random manipulations of noncontingent value in pigeons. Overall, greater amounts of noncontingent reinforcement competed with both acquisition and maintenance of alternative responding.     

How we use rules to select actions: A review of evidence from cognitive neuroscience

Much of our behavior is guided by rules, or prescribed guides for action. In this review, I consider the current state of knowledge of how rules are learned, stored in the brain, and retrieved and used as the need arises. The focus is primarily on studies in humans, but the review is informed by relevant studies in nonhuman primates. Ventrolateral prefrontal cortex (VLPFC) has been implicated in rule learning, retrieval from long-term memory, and on-line maintenance during task preparation. Interactions between VLPFC and temporal cortex are required for rule retrieval in nonhuman primates, and brain imaging findings in humans suggest that rule knowledge is stored in the posterior middle temporal gyrus. Dorsolateral PFC appears to be more closely related to rule-based response selection than to rule retrieval. An important task for the future is to explain how PFC, basal ganglia, and temporal, parietal, and motor cortices interact to produce rule-guided behavior.     

Post-choice information processing by pigeons

In a conditional discrimination (matching-to-sample), a sample is followed by two comparison stimuli, one of which is correct, depending on the sample. Evidence from previous research suggests that if the stimulus display is maintained following an incorrect response (the so-called penalty-time procedure), acquisition by pigeons is facilitated. The present research tested the hypothesis that the penalty-time procedure allows the pigeons to review and learn from the maintained stimulus display following an incorrect choice. It did so by including a penalty-time group for which, following an incorrect choice, the sample changed to match the incorrect comparison, thus providing the pigeons with post-choice misinformation. This misinformation group acquired the matching task significantly slower than the standard penalty-time group (that had no change in the sample following an error). Furthermore, acquisition of matching by a control group that received no penalty time fell midway between the other two groups, suggesting that the pigeons did not merely take more care in making choices because of the aversiveness of penalty-time. Thus, it appears that in the acquisition of matching-to-sample, when the stimulus display is maintained following an incorrect choice, the pigeons can review or acquire information from the display. This is the first time that such an effect has been reported for a nonhuman species.     

Cognitive precedence for local information in hierarchical stimulus processing by pigeons

Four experiments investigated the processing of hierarchical stimuli by pigeons. Using a 4 alternative divided-attention task, 4 pigeons were food-reinforced for accurately identifying letters arranged as either hierarchical global- or local-relevant stimuli or as size-matched filled stimuli. Experiment 1 found that task acquisition was faster with local-relevant than global-relevant stimuli. This difference was not due to letter size. Experiment 2 demonstrated successful transfer to a novel irrelevant letter configuration. Experiments 3 and 4 tested pigeons' responses to conflict probe stimuli composed of equally discriminable relevant letters at each level. These tests revealed that all of the pigeons showed a cognitive precedence for local information early in processing, with the pigeons using different cues to initiate the processing of global information. This local advantage contrasts with previously reported results for humans and pigeons but is similar to that reported for nonhuman primates. Alternatives attempting to reconcile these contrasting comparative results are considered.     

Development of ordinal sequence perception in infancy

Perception of the ordinal position of a sequence element is critical to many cognitive and motor functions. Here, the prediction that this ability is based on a domain‐general perceptual mechanism and, thus, that it emerges prior to the emergence of language was tested. Infants were habituated with sequences of moving/sounding objects and then tested for the ability to perceive the invariant ordinal position of a single element (Experiment 1) or the invariant relative ordinal position of two adjacent elements (Experiment 2). Experiment 1 tested 4‐ and 6‐month‐old infants and showed that 4‐month‐old infants focused on conflicting low‐level sequence statistics and, therefore, failed to detect the ordinal position information, but that 6‐month‐old infants ignored the statistics and detected the ordinal position information. Experiment 2 tested 6‐, 8‐, and 10‐month‐old infants and showed that only 10‐month‐old infants detected relative ordinal position information and that they could only accomplish this with the aid of concurrent statistical cues. Together, these results indicate that a domain‐general ability to detect ordinal position information emerges during infancy and that its initial emergence is preceded and facilitated by the earlier emergence of the ability to detect statistical cues.     

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.     

Biodefense research and the U.S. regulatory structure whither nonhuman primate moral standing?

Biodefense and emerging infectious disease animal research aims to avoid or ameliorate human disease and suffering arising from the natural outbreak or intentional deployment of some of the world's most dreaded pathogens. Research to develop medical countermeasures to these diseases faces a difficult challenge since the products usually cannot be tested for efficacy in human beings. The U.S. Food and Drug Administration's Animal Rule may be increasingly used to overcome this challenge by allowing researchers to translate animal data into medical countermeasures without human subject efficacy testing. Yet the Animal Rule also has significant implications for increased intensive nonhuman primate research. We argue that despite the common belief that nonhuman primates have a fairly high level of moral standing and the protections for animals that are crucial to the U.S. regulations guiding animal research, the Animal Rule specifically and the regulations generally raise serious problems for the attribution of moral standing to nonhuman primates. We argue, however, that the burden of proof is on a position denying all moral standing to nonhuman primates and compare the implications of the U.S. regulatory structure in this regard with some recent developments in the European Union.     

Transfer of metacognitive skills and hint seeking in monkeys

Metacognition is knowledge that can be expressed as confidence judgments about what one knows (monitoring) and by strategies for learning what one does not know (control). Although there is a substantial literature on cognitive processes in animals, little is known about their metacognitive abilities. Here we show that rhesus macaques, trained previously to make retrospective confidence judgments about their performance on perceptual tasks, transferred that ability immediately to a new perceptual task and to a working memory task. We also show that monkeys can learn to request "hints" when they are given problems that they would otherwise have to solve by trial and error. This study demonstrates, for the first time, that nonhuman primates share with humans the ability to monitor and transfer their metacognitive ability both within and between different cognitive tasks, and to seek new knowledge on a need-to-know basis.     

Evidence for kinship information contained in the rhesus macaque (Macaca mulatta) face

The ability to recognize kin is an important social skill for primates. Humans are adept at using facial similarity to recognize likely kin, and there is evidence that nonhuman primates are also able to use facial similarity to make judgments about kinship. However, if and how nonhuman primate faces actually contain kinship information remains unclear. To test whether there is objectively measurable facial similarity in related nonhuman primates, we compared facial measurements from related (paternal half-sisters) and unrelated adult female rhesus macaques (Macaca mulatta). Facial measurements were first summarized into 5 factors using a principal component analysis. Differences in these factors between the faces of related macaques were compared with differences between the faces of random unrelated macaques and of age-matched unrelated macaques. The difference in facial measurements between related macaques was significantly smaller than the difference in facial measurements of either group of unrelated macaques, constituting an objective measure of facial similarity in macaque kin. These results indicate that kinship information is contained in the rhesus macaque face and suggest that nonhuman primates may rely in part on facial similarity to distinguish kin.     

Core knowledge

Compex cognitive skills such as reading and calculation and complex cognitive achievements such as formal science and mathematics may depend on a set of building block systems that emerge early in human ontogeny and phylogeny. These core knowledge systems show characteristic limits of domain and task specificity: Each serves to represent a particular class of entities for a particular set of purposes. By combining representations from these systems, however, human cognition may achieve extraordinary flexibility. Studies of cognition in human infants and in nonhuman primates therefore may contribute to understanding unique features of human knowledge.     

Auditory and visual serial position functions obey different laws

Rhesus monkeys were tested in serial probe recognition tasks with either travel slide pictures or natural sounds. Tests with four-item lists produced serial position functions that were essentially opposite in shape for the two modalities and changed in opposite ways with retention interval. For visual memory, the primacy effect grew and the recency effect dissipated with retention interval. Capuchin monkeys, humans, and pigeons showed similar results. For auditory memory with rhesus monkeys, the recency effect grew and the primacy effect dissipated with retention interval. These results taken together, along with results from rehearsal tests of monkeys and humans, implicate two passive memory processes with different time courses. Interference among items within auditory lists was manipulated by varying the time between items and categories of items. Interference across lists was manipulated by varying the item pool size and, hence, item repetitions. Changes in the auditory serial position functions indicated that proactive and retroactive interference may have been instrumental in these dynamically changing serial position functions. Implications for theories and models of memory are discussed.     

An analysis of immediate serial recall performance in a macaque

There has been considerable research into the ability of nonhuman primates to process sequential information, a topic that is of interest in part because of the extensive involvement of sequence processing in human language use. Surprisingly, no previous study has unambiguously tested the ability of nonhuman primates to encode and immediately reproduce a novel temporal sequence of perceptual events, the ability tapped in the immediate serial recall (ISR) task extensively studied in humans. We report here the performance of a rhesus macaque on a spatial ISR task, closely resembling tasks widely used in human memory research. Detailed analysis of the monkey’s recall performance indicates a number of important parallels with human ISR, consistent with the idea that a single mechanism for short-term serial order memory may be shared across species.