Information seeking by rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella)

Animal metacognition is an active, growing research area, and one part of metacognition is flexible information-seeking behavior. In Roberts et al. (2009), pigeons failed an intuitive information-seeking task. They basically refused, despite multiple fostering experiments, to view a sample image before attempting to find its match. Roberts et al. concluded that pigeons’ lack of an information-seeking capacity reflected their broader lack of metacognition. We report a striking species contrast to pigeons. Eight rhesus macaques and seven capuchin monkeys passed the Roberts et al. test of information seeking—often in their first testing session. Members of both primate species appreciated immediately the lack of information signaled by an occluded sample, and the need for an information-seeking response to manage the situation. In subsequent testing, macaques demonstrated flexible/varied forms of information management. Capuchins did not. The research findings bear on the phylogenetic distribution of metacognition across the vertebrates, and on the underlying psychological requirements for metacognitive and information-seeking performances.     

Metamemory in tufted capuchin monkeys (Cebus apella)

Whereas evidence for metacognition by nonhuman primates has been obtained in great apes and old world monkeys, it is weaker in new world monkeys. For instance, capuchin monkeys may fail to recognize their own knowledge of the location of invisible bait. In the present study, we tested whether tufted capuchin monkeys would flexibly change their behavior in a delayed matching-to-sample (DMTS) test depending upon the strength of their memory trace of the sample. In Experiment 1, two monkeys were tested on a modified 9-alternative DMTS task with various delays on a computerized display. In some trials, the monkeys could choose whether to go for a memory test or for a simple key touch as an escape from the test. In other trials, they were forced to go for the memory test. Both monkeys escaped from the memory test more often when their matching accuracy on forced tests was lower. In one of the monkeys, the matching accuracies on chosen memory tests decreased more slowly as a function of delay length, and were higher after long delays than those on forced memory tests. This suggests that at least one capuchin monkey was able to recognize the strength of his own memory trace. Experiment 2 employed occasional no-sample tests, in which the monkeys faced the task choice without presentation of any sample for the trial. The monkey who was successful in Experiment 1 declined the memory test more often in no-sample trials than regular trials, further indicating metamemory in this individual. In Experiment 3, this successful monkey received a task, in which he was sometimes able to choose between shape MTS or texture MTS tasks. However, his matching accuracies did not differ between chosen tasks and forced tasks. Thus, the metamemory possessed by this new world monkey species may be more like a flag, showing strength of memory trace, than an elaborate representation showing details of the memory trace.     

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.     

Sequential responding and planning in capuchin monkeys (Cebus apella)

Previous experiments have assessed planning during sequential responding to computer generated stimuli by Old World nonhuman primates including chimpanzees and rhesus macaques. However, no such assessment has been made with a New World primate species. Capuchin monkeys (Cebus apella) are an interesting test case for assessing the distribution of cognitive processes in the Order Primates because they sometimes show proficiency in tasks also mastered by apes and Old World monkeys, but in other cases fail to match the proficiency of those other species. In two experiments, eight capuchin monkeys selected five arbitrary stimuli in distinct locations on a computer monitor in a learned sequence. In Experiment 1, shift trials occurred in which the second and third stimuli were transposed when the first stimulus was selected by the animal. In Experiment 2, mask trials occurred in which all remaining stimuli were masked after the monkey selected the first stimulus. Monkeys made more mistakes on trials in which the locations of the second and third stimuli were interchanged than on trials in which locations were not interchanged, suggesting they had already planned to select a location that no longer contained the correct stimulus. When mask trials occurred, monkeys performed at levels significantly better than chance, but their performance exceeded chance levels only for the first and the second selections on a trial. These data indicate that capuchin monkeys performed very similarly to chimpanzees and rhesus monkeys and appeared to plan their selection sequences during the computerized task, but only to a limited degree.     

How capuchin monkeys (Cebus apella) quantify objects and substances

Humans and nonhuman animals appear to share a capacity for nonverbal quantity representations. But what are the limits of these abilities? Results of previous research with human infants suggest that the ontological status of an entity as an object or a substance affects infants' ability to quantify it. We ask whether the same is true for another primate species-the New World monkey Cebus apella. We tested capuchin monkeys' ability to select the greater of two quantities of either discrete objects or a nonsolid substance. Participants performed above chance with both objects (Experiment 1) and substances (Experiment 2); in both cases, the observed performance was ratio dependent. This finding suggests that capuchins quantify objects and substances similarly and do so via analog magnitude representations.     

Ordinal judgments of symbolic stimuli by capuchin monkeys (Cebus apella) and rhesus monkeys (Macaca mulatta): the effects of differential and nondifferential reward

Ordinal learning was investigated in capuchin monkeys (Cebus apella) and rhesus monkeys (Macaca mulatta). In Experiment 1, both species were presented with pairings of the Arabic numerals 0 to 9. Some monkeys were given food rewards equal to the value of the numeral selected and some were rewarded with a single pellet only for choosing the higher numeral within the pair. Both species learned to select the larger numeral, but only rhesus monkeys that were differentially rewarded performed above chance levels when presented with novel probe pairings. In Experiment 2, the monkeys were first presented with arrays of 5 familiar numerals (from the range 0 to 9) and then arrays of 5 novel letters (from the range A to J) with the same reward outcomes in place as in Experiment 1. Both species performed better with the numerals, suggesting that an ordinal sequence of all stimuli had been learned during Experiment 1, rather than a matrix of two-choice discriminations.     

Self-control and tool use in tufted capuchin monkeys (Cebus apella)

Self-control is defined as forgoing immediate gratification to obtain a greater reward. Tool use may relate to self-control because both behaviors may require foresight and deliberate control over one's actions. The authors assessed 20 capuchin monkeys (Cebus apella) for the ability to delay gratification in a tool task. Subjects were given rod-shaped food items that could either be consumed immediately or be carried to an apparatus and used to extract a more preferred food. The authors found that some monkeys were able to exhibit self-control. Monkeys with relatively more tool use experience demonstrated the greatest levels of self-control. These results indicate that capuchins are capable of delaying gratification when a higher quality reinforcer is present and that tool experience can influence levels of self-control in this task.     

Implicit and explicit category learning by capuchin monkeys (Cebus apella)

Current theories of human categorization differentiate an explicit, rule-based system of category learning from an implicit system that slowly associates regions of perceptual space with response outputs. The researchers extended this theoretical differentiation to the category learning of New World primates. Four capuchins (Cebus apella) learned categories of circular sine-wave gratings that varied in bar spatial frequency and orientation. The rule-based and information-integration tasks, respectively, had one-dimensional and two-dimensional solutions. Capuchins, like humans, strongly dimensionalized the stimuli and learned the rule-based task more easily. The results strengthen the suggestion that nonhuman primates have some structural components of humans' capacity for explicit categorization, which in humans is linked to declarative cognition and consciousness. The results also strengthen the primate contrast to other vertebrate species that may lack the explicit system. Therefore, the results raise important questions about the origins of the explicit categorization system during cognitive evolution and about its overall phylogenetic distribution.     

An assessment of memory awareness in tufted capuchin monkeys (Cebus apella)

Humans, apes, and rhesus monkeys demonstrate memory awareness by collecting information when ignorant and acting immediately when informed. In this study, five capuchin monkeys searched for food after either watching the experimenter bait one of four opaque tubes (seen trials), or not watching (unseen trials). Monkeys with memory awareness should look into the tubes before making a selection only on unseen trials because on seen trials they already know the location of the food. In Experiment 1, one of the five capuchins looked significantly more often on unseen trials. In Experiment 2, we ensured that the monkeys attended to the baiting by interleaving training and test sessions. Three of the five monkeys looked more often on unseen trials. Because monkeys looked more often than not on both trial types, potentially creating a ceiling effect, we increased the effort required to look in Experiment 3, and predicted a larger difference in the probability of looking between seen and unseen trials. None of the five monkeys looked more often on unseen trials. These findings provide equivocal evidence for memory awareness in capuchin monkeys using tests that have yielded clear evidence in humans, apes, and rhesus monkeys.     

Experience and materials affect combinatorial construction in tufted capuchin monkeys (Cebus apella)

Three movement procedures can combine nesting cups into seriated structures. Reliance on these procedures changes with age in human children, and the putatively most advanced emerges as a predominant procedure at 3 or more years. Six monkeys' (Cebus apella) combinatorial procedures and successes at nesting seriated cups were evaluated. The current study examined whether the procedures used (a) shift toward more efficient procedures after unguided experience, (b) are dependent on the type of object being combined, and (c) can be altered by specific training history. All factors produced a change in procedure for some individuals, suggesting that combinatorial procedure is a product of the dynamic influences of preexisting tendencies to act in certain ways, of environmental circumstances, and of prior experiences. Some monkeys preferred the putatively most cognitively complex procedure.     

Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task

The ability of 3 capuchin monkeys (Cebus apella) to use experimenter-given cues to solve an object-choice task was assessed. The monkeys learned to use explicit gestural and postural cues and then progressed to using eye-gaze-only cues to solve the task, that is, to choose the baited 1 of 2 objects and thus obtain a food reward. Increasing cue-stimulus distance and introducing movement of the eyes impeded the establishment of effective eye-gaze reading. One monkey showed positive but imperfect transfer of use of eye gaze when a novel experimenter presented the cue. When head and eye orientation cues were presented simultaneously and in conflict, the monkeys showed greater responsiveness to head orientation cues. The results show that capuchin monkeys can learn to use eye gaze as a discriminative cue, but there was no-evidence for any underlying awareness of eye gaze as a cue to direction of attention.     

Analogical reasoning in a capuchin monkey (Cebus apella)

Previous evidence has suggested that analogical reasoning (recognizing similarities among object relations when the objects themselves are dissimilar) is limited to humans and apes. This study investigated whether capuchin monkeys (Cebus apella) can use analogical reasoning to solve a 3-dimensional search task. The task involved hiding a food item under 1 of 2 or 3 plastic cups of different sizes and then allowing subjects to search for food hidden under the cup of analogous size in their own set of cups. Four monkeys were exposed to a series of relational matching tasks. If subjects reached criterion on these tasks, they were exposed to relational transfer tasks involving novel stimuli. Three of the monkeys failed to reach criterion on the basic relational matching tasks and therefore were not tested further. One monkey, however, revealed above-chance performance on a series of transfer tasks with 3 novel stimuli. This evidence suggests that contrary to previous arguments, a member of a New World monkey species can solve an analogical problem.     

Ordinal representation of numeric quantities by brown capuchin monkeys (Cebus apella)

Using techniques established by E. M. Brannon and H. S. Terrace (2000) with rhesus macaques (Macaca mulatta), the authors tested the ability of brown capuchins (Cebus apella) to order arrays of items ranging in quantity from 1 to 9. Three monkeys were trained on a touch screen to select the quantities 1-4 in ascending order. The monkeys exhibited successful transfer of this ability to novel representations of the quantities 1-4 and to pairs of the novel quantities 5-9. Patterns of responding with respect to numeric distance and magnitude were similar to those seen in human subjects, suggesting the use of similar psychological processes. The capuchins demonstrated an ordinal representation of quantity equivalent to that shown in Old World monkeys.     

Auditory--visual cross-modal perception of communicative stimuli in tufted capuchin monkeys (Cebus apella)

Research on cross-modal performance in nonhuman primates is limited to a small number of sensory modalities and testing methods. To broaden the scope of this research, the authors tested capuchin monkeys (Cebus apella) for a seldom-studied cross-modal capacity in nonhuman primates, auditory-visual recognition. Monkeys were simultaneously played 2 video recordings of a face producing different vocalizations and a sound recording of 1 of the vocalizations. Stimulus sets varied from naturally occurring conspecific vocalizations to experimentally controlled human speech stimuli. The authors found that monkeys preferred to view face recordings that matched presented vocal stimuli. Their preference did not differ significantly across stimulus species or other stimulus features. However, the reliability of the latter set of results may have been limited by sample size. From these results, the authors concluded that capuchin monkeys exhibit auditory-visual cross-modal perception of conspecific vocalizations.     

Generative aspects of manipulation in tufted capuchin monkeys (Cebus apella).

Evaluating the cognitive and ontogenetic bases of tool use in primates requires comparative data on the generative nature of manipulation, including the frequency and variety of combinations of actions and objects. Thirty-one tufted capuchins (Cebus apella) of 3 age groups devoted significant proportions of time to interaction with objects and substrates. Activity that combined an object with a substrate occurred often; activities that combined 2 portable objects were less frequent. Predictions drawn from neo-Piagetian theory of an ontogenetic link between combinatorial behaviors and the onset of tool use were not supported. The frequency and generative nature of capuchins' manipulative activity, particularly acts combining objects and substrates, could account for their proclivity to use tools. The use of tools by capuchins need not involve the representational abilities proposed by neo-Piagetian theory.     

Identity concept learning in matching-to-sample tasks by tufted capuchin monkeys (Cebus apella)

The abstract concept of equivalence is considered one of the bases of higher-order cognition, and it has been the subject of considerable research in comparative cognition. This study examined the conditions under which tufted capuchin monkeys (Cebus apella) are able to acquire an identity concept. Six capuchin monkeys were trained to solve a visual matching-to-sample (MTS) task on the basis of perceptual identity. The acquisition of the identity rule was inferred from the subject’s ability to solve transfer tests with novel stimuli. We evaluated the ability of the capuchin monkeys to match the shape of novel stimuli after training with both several small stimulus sets (Experiment 1) and a large stimulus set (Experiment 2). Moreover, we examined the ability of capuchins to transfer the concept to novel visual dimensions, such as colour and size and to transfer to novel spatial arrangements of the stimuli (Experiment 2). We demonstrated that the ability of capuchins to match novel stimuli was improved by increasing the number of stimuli used during training (Experiments 1 and 2) and that after a widely applicable identity concept based on the stimulus shape was acquired, the capuchins were able to match stimuli according to an identity rule based on both the colour and size of the stimuli and when the spatial arrangement of the stimuli was varied (Experiment 2). This study is the first to demonstrate that the size of the training set affects the acquisition of an abstract identity concept in an MTS task in non-human primates.     

Ontogenetic dissociation between habit learning and recognition memory in capuchin monkeys (Cebus apella)

The performance of young and adult capuchin monkeys (Cebus apella) on a Concurrent Discrimination Learning (CDL) test and a Delayed Non-Matching to Sample (DNMS) task were investigated. Results indicate that all subjects were able to learn the CDL test with 20-pairs simultaneously and retain this stimulus/reward association within 24-h interval. In contrast, young subjects did not perform the DNMS task with the same proficiency as adults. While adults' scores were above chance across all memory test delays, the young capuchin monkeys performed the test by chance level. These results support the hypothesis that these two tasks require different cognitive processes mediated by two independent neural systems with a differentiated ontogenetic development. Moreover, they provide evidence that this dissociation occurs not only in humans and Old World monkeys but also in the New World capuchin monkeys indicating that this species can be a valuable alternative model for investigations of the neurobiological basis of memory.     

Quantity judgments of sequentially presented food items by capuchin monkeys (Cebus apella)

Recent assessments have shown that capuchin monkeys, like chimpanzees and other Old World primate species, are sensitive to quantitative differences between sets of visible stimuli. In the present study, we examined capuchins’ performance in a more sophisticated quantity judgment task that required the ability to form representations of food quantities while viewing the quantities only one piece at a time. In three experiments, we presented monkeys with the choice between two sets of discrete homogeneous food items and allowed the monkeys to consume the set of their choice. In Experiments 1 and 2, monkeys compared an entirely visible food set to a second set, presented item-by-item into an opaque container. All monkeys exhibited high accuracy in choosing the larger set, even when the entirely visible set was presented last, preventing the use of one-to-one item correspondence to compare quantities. In Experiment 3, monkeys compared two sets that were each presented item-by-item into opaque containers, but at different rates to control for temporal cues. Some monkeys performed well in this experiment, though others exhibited near-chance performance, suggesting that this species’ ability to form representations of food quantities may be limited compared to previously tested species such as chimpanzees. Overall, these findings support the analog magnitude model of quantity representation as an explanation for capuchin monkeys’ quantification of sequentially presented food items.