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.     

Memory without awareness: pigeons do not show metamemory in delayed matching to sample

Metamemory, the ability to report on memory strength, is clearly established in rhesus macaques (Macaca mulatta) by converging evidence from several paradigms. In contrast, A. Inman and S. J. Shettleworth (1999) found no conclusive evidence of metamemory in pigeons. The authors studied pigeons further in 3 paradigms, with multiple tests of metamemory in each. Pigeons encountered a safe alternative to a matching-to-sample test either before (Experiment 2) or concurrently with (Experiment 3) the matching test. Choices of the safe option did not vary consistently with matching accuracy or change in trials with omitted samples in the way predicted for an animal with metamemory. In Experiment 4, confidence ratings following completion of the matching test also did not vary consistently as predicted by metamemory.     

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.     

Acquisition and maintenance of delayed matching-to-sample in tufted capuchin monkeys

Delayed matching-to-sample (DMTS) is a commonly used procedure to investigate short-term memory. For the study of functions of forgetting, the delay between the disappearance of the sample stimulus and appearance of choices is manipulated. The intertrial interval (ITI) is also varied to assess interference effects. Performance decrements have been observed as delay increases and, in some cases, performance recovery occurs when ITIs are increased. Other studies indicate that the higher the ITI/delay ratio, the greater the accuracy in DMTS. In this study, 2 experiments investigated DMTS performances of 3 tufted capuchin monkeys as function of delay and ITI. In Experiment 1, alternation of gradual increases of delay and ITI was effective in producing ≥90% accuracy at delays as long as 90 s. Individual monkeys differed in the highest value of delay at which this criterion was met. In Experiment 2, the monkeys were exposed to 5-s DMTS with different ITIs to assess the effects of various ITI/delay ratios on accuracy. Highest accuracy tended to occur at the higher ITI/delay ratios.     

Reverse-reward learning in squirrel monkeys (Saimiri sciureus): retesting after 5 years, and assessment on qualitative transfer

Seven squirrel monkeys (Saimiri sciureus) previously trained on reverse-reward tasks were presented with the original "1-versus-4" task after a 5-year interval without reverse-reward experience (Experiment 1). None of them reliably selected the smaller food array; however, at around chance level, their performance was superior to when they were first exposed to the task almost 6 years previously, suggesting some long-term memory retention. One naive monkey consistently selected the larger array, as expected. In Experiment 2, trials consisting of 1 versus 1 piece of two qualitatively different types of food were interspersed among familiar 1-versus-4 trials. None of five monkeys tested reliably selected the less-preferred food to get the more preferred food as the reward, and one monkey scored below chance. However, when one piece of low-preference food was paired with four pieces of high-preference food (Experiment 3), all four monkeys tested avoided reaching for the latter and thereby obtained it as the reward; two monkeys obtained perfect scores on these trials. These two monkeys were trained on a specific qualitative reverse-reward pairing and then again tested on new pairings (Experiment 4), but transfer was incomplete. Compound trials that pit quantity against quality in novel ways appear taxing for squirrel monkeys, despite competence in reverse-reward on both dimensions separately.     

Monkeys (Macaca mulatta and Cebus apella) track, enumerate, and compare multiple sets of moving items

Despite many demonstrations of numerical competence in nonhuman animals, little is known about how well animals enumerate moving stimuli. In this series of experiments, rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella) performed computerized tasks in which they had to enumerate sets of stimuli. In Experiment 1, rhesus monkeys compared two sets of moving stimuli. Experiment 2 required comparisons of a moving set and a static set. Experiment 3 included human participants and capuchin monkeys to assess all 3 species' performance and to determine whether responding was to the numerical properties of the stimulus sets rather than to some other stimulus property such as cumulative area. Experiment 4 required both monkey species to enumerate subsets of each moving array. In all experiments, monkeys performed above chance levels, and their responses were controlled by the number of items in the arrays as opposed to nonnumerical stimulus dimensions. Rhesus monkeys performed comparably to adult humans when directly compared although capuchin performance was lower.     

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.     

A comparison of visual and auditory short-term memory in monkeys (Cebus apella)

Using a visual and an acoustic sample set that appeared to favour the auditory modality of the monkey subjects, in Experiment 1 retention gradients generated in closely comparable visual and auditory matching (go/no-go) tasks revealed a more durable short-term memory (STM) for the visual modality. In Experiment 2, potentially interfering visual and acoustic stimuli were introduced during the retention intervals of the auditory matching task. Unlike the case of visual STM, delay-interval visual stimulation did not affect auditory STM. On the other hand, delay-interval music decreased auditory STM, confirming that the monkeys maintained an auditory trace during the retention intervals. Surprisingly, monkey vocalizations injected during the retention intervals caused much less interference than music. This finding, which was confirmed by the results of Experiments 3 and 4, may be due to differential processing of “arbitrary” (the acoustic samples) and species-specific (monkey vocalizations) sounds by the subjects. Although less robust than visual STM, auditory STM was nevertheless substantial, even with retention intervals as long as 32 sec.     

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.     

A comparative analysis of global and local processing of hierarchical visual stimuli in young children (Homo sapiens) and monkeys (Cebus apella)

Results obtained with preschool children (Homo sapiens) were compared with results previously obtained from capuchin monkeys (Cebus apella) in matching-to-sample tasks featuring hierarchical visual stimuli. In Experiment 1, monkeys, in contrast with children, showed an advantage in matching the stimuli on the basis of their local features. These results were replicated in a 2nd experiment in which control trials enabled the authors to rule out that children used spurious cues to solve the matching task. In a 3rd experiment featuring conditions in which the density of the stimuli was manipulated, monkeys' accuracy in the processing of the global shape of the stimuli was negatively affected by the separation of the local elements, whereas children's performance was robust across testing conditions. Children's response latencies revealed a global precedence in the 2nd and 3rd experiments. These results show differences in the processing of hierarchical stimuli by humans and monkeys that emerge early during childhood.     

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.     

Delaying gratification for food and tokens in capuchin monkeys (Cebus apella) and chimpanzees (Pan troglodytes): when quantity is salient, symbolic stimuli do not improve performance

Capuchin monkeys have been tested for the capacity to delay gratification for accumulating rewards in recent studies and have exhibited variable results. Meanwhile, chimpanzees have consistently excelled at this task. However, neither species have ever been tested at accumulating symbolic tokens instead of food items, even though previous reports indicate that tokens sometimes facilitate performance in other self-control tasks. Thus, in the present study, we tested capuchin monkeys and chimpanzees for their capacity to delay gratification in a delay maintenance task, in which an experimenter presented items, one at a time, to within reach of an animal for as long as the animal refrained from taking them. In Experiment 1, we assessed how long capuchin monkeys could accumulate items in the delay maintenance task when items were food rewards or tokens exchangeable for food rewards. Monkeys accumulated more food rewards than they did tokens. In Experiment 2, we tested capuchin monkeys and chimpanzees in a similar accumulation test. Whereas capuchins again accumulated more food than tokens, all chimpanzees but one showed no difference in performance in the two conditions. These findings provide additional evidence that chimpanzees exhibit greater self-control capacity in this task than do capuchin monkeys and indicate that symbolic stimuli fail to facilitate delay maintenance when they do not abstract away from the quantitative dimension of the task. This is consistent with previous findings on the effects of symbols on self-control and illuminates what makes accumulation a particularly challenging task.     

Attention allocation modulates the processing of hierarchical visual patterns: a comparative analysis of capuchin monkeys (Cebus apella) and humans

Humans show a global advantage when processing hierarchical visual patterns, and they detect the global level of stimulus structure more accurately and faster than the local level in several stimulus contexts. By contrast, capuchins (Cebus apella) and other monkey species show a strong local advantage. A key factor which, if manipulated, could cause an inversion of this effect in monkeys is still to be found. In this study, we examined whether it was possible to induce attention allocation to global and local levels of perceptual analysis in capuchin monkeys and if by doing so, their local dominance could be reversed. We manipulated attentional bias using a matching-to-sample (MTS) task where the proportion of trials requiring global and local processing varied between conditions. The monkeys were compared with humans tested with the same paradigm. Monkeys showed a local advantage in the local bias condition but a global advantage in the global bias condition. The role of attention in processing was confined to the local trials in a first phase of testing but extended to both local and global trials in the course of task practice. Humans exhibited an overall global dominance and an effect of attentional bias on the speed of processing of the global and local level of the stimuli. These results indicate a role for attention in the processing of hierarchical stimuli in monkeys and are discussed in relation to the extent to which they can explain the differences between capuchin monkeys and humans observed in this and other studies.     

Large-billed crows (Corvus macrorhynchos) have retrospective but not prospective metamemory

Evidence of metamemory, the ability to monitor one’s own memory, has been obtained in some primates, but it appears to be weaker in other species. In this study, we examined whether crows flexibly modulate their behavior by monitoring the strength of memory trace in a delayed matching-to-sample task using two paradigms. First, crows performing a memory test were given an escape option to decline taking the test (prospective metamemory). Second, crows were given the escape option as a “not confident” report after completing the test (retrospective metamemory). Accurate memory performance yielded a reward with a higher probability, whereas inaccurate memory performance resulted in no such recompense. The escape option yielded a reward with a lower probability. In the prospective metamemory test, crows escaped the memory test more frequently with longer delay intervals than they did with shorter delay intervals but no more frequently in the sample-omission than the sample-present trials, indicating that the crows decided to take the test or decline it by using the delay interval as a cue. In contrast, in the retrospective metamemory test, the crows escaped the memory test more frequently when their memory-test response was incorrect than correct and more frequently in the sample-omission than the sample-present trials, indicating that the crows recognized confidence regarding their choice in the memory test and utilized the escape option to maximize reward probability. Although these results suggest that crows retrospectively monitor the strength of memory trace, their prospective metamemory ability has not yet been confirmed in the present paradigm.     

Automated testing of cognitive performance in monkeys: Use of a battery of computerized test systems by a troop of semi-free-ranging baboons (<Emphasis Type="Italic">Papio papio</Emphasis>)

Fagot and Paleressompoulle (2009) published an automated learning device for monkeys (ALDM) to test the cognitive functions of nonhuman primates within their social groups, but the efficiency of the ALDM procedure with large groups remains unknown. In the present study, 10 ALDM systems were provided ad lib to a troop of 26 semi-free-ranging baboons that were initially naive with computerized testing. The test program taught baboons to solve two-alternative forced choice (2AFC) and matching-to-sample (MTS) tasks. A million trials were recorded for the group during a period of 85 days (Experiment 1). Their analysis shows that 75% of the baboons participated at high frequencies and quickly learned the 2AFC and MTS tasks. In Experiment 2, we compared the baboons’ behavior when the ADLM systems were either accessible or closed. ALDM reduced frequencies of object-directed behaviors, but had no overt consequence on social conflicts. In Experiment 3, we tested the process of the global or local attributes of visual stimuli in MTS-trained baboons in order to illustrate the efficiency of ALDM for behavioral studies requiring complex experimental designs. Altogether, the results of the present study validate the use of ALDM to efficiently test monkeys in large social groups. ALDM has a strong potential for a variety of scientific disciplines, including for biomedical research. Supplemental materials for this article may be downloaded from http://brm.psychonomic-journals.org/content/supplemental.     

Rats know when they remember: transfer of metacognitive responding across odor-based delayed match-to-sample tests

Metamemory entails cognitively assessing the strength of one’s memories. We tested the ability of nine Long-Evans rats to distinguish between remembering and forgetting by presenting a decline option that allowed a four-choice odor-based delayed match to sample (DMTS) tests to be by-passed. Rats performed significantly better on tests they chose to take than on tests they were forced to take, indicating metacognitive responding. However, rather than control by internal mnemonic cues, one alternative explanation is that decline use is based on external test-specific cues that become associated with increased rewards overtime. To examine this possibility, we tested rats on three generalization tests in which external contingencies were inconsistent and therefore could not serve as discriminative cues. Rats transferred adaptive use of the decline response in tests that eliminated memory by presenting no sample, increased memory by presenting multiple samples, and both weakened and strengthened memory by varying the retention interval. Further, subjects chose to take or decline the test before encountering the memory test, providing evidence that rats based their metacognitive responding on internal cues rather than external ones. To our knowledge, this is the first robust evidence for metamemory in rats using the DMTS decline-test paradigm in which several possible sources of external stimulus control can be ruled out.     

Capuchin monkeys (Cebus apella) let lesser rewards pass them by to get better rewards

Self-control is defined as foregoing an immediate reward to gain a larger delayed reward. Methods used to test self-control comparatively include inter-temporal choice tasks, delay of gratification tasks, and accumulation tasks. To date, capuchin monkeys have shown different levels of self-control across tasks. This study introduced a new task that could be used comparatively to measure self-control in an intuitive context that involved responses that required no explicit training. Capuchin monkeys (Cebus apella) were given a choice between two food items that were presented on a mechanized, revolving tray that moved those foods sequentially toward the monkeys. A monkey could grab the first item or wait for the second, but was only allowed one item. Most monkeys in the study waited for a more highly preferred food item or a larger amount of the same food item when those came later, and they inhibited the prepotent response to grab food by not reaching out to take less-preferred foods or smaller amounts of food that passed directly in front of them first. These data confirm that the mechanisms necessary for self-control are present in capuchin monkeys and indicate that the methodology can be useful for broader comparative assessments of self-control.     

Learning from others’ mistakes in capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

We investigated whether tufted capuchin monkeys (Cebus apella) learn from others' mistakes. We prepared three kinds of transparent containers having the same appearance: one that could be opened by the lid, one that could be opened from the bottom, and one that could be opened either way. Using each of the first two one-way-open type containers, the monkeys were trained to copy the human demonstrator's action to open the container and obtain a piece of sweet potato contained therein. After this training, the demonstrator showed the monkeys an action that would open or fail to open the third, two-way-open type container. None of the monkeys reliably opened the container by spontaneously compensating for the demonstrator's failure (Experiment 1). In Experiment 2, the same subjects were trained to correct their own mistakes immediately after failure, before we introduced the same test as in Experiment 1. This experience did not result in subjects using the demonstrator's failure to produce a successful action. In Experiment 3, we placed two monkeys face to face. In this situation, the second monkey was presented with the container after the first monkey failed to open it. As a result, two capuchin monkeys capitalized on the partner's failure to correctly guide his/her behavior. Thus, the monkeys monitored not only the outcome of the others' action, but also that action per se. This result suggests that not only humans and apes, but also monkeys may understand the meaning of others' actions in social learning.     

Cooperative problem solving by tufted capuchin monkeys (Cebus apella): spontaneous division of labor, communication, and reciprocal altruism

Using an experimentally induced cooperation task, the authors investigated whether tufted capuchin monkeys (Cebus apella) share the following 3 characteristics of cooperation with humans: division of labor, communication, and reciprocal altruism. In Experiment 1, the authors trained individual monkeys to perform the necessary sequence of actions for rewards and tested them in pairs to assess whether they could solve the task by spontaneously dividing the sequence of actions. All pairs solved this task. In Experiment 2, monkeys worked in the cooperation task and a task requiring no partner help. They looked at the partner significantly longer in the former task than in the latter, but communicative intent could not be determined. In Experiment 3, only 1 of 2 participants obtained a reward on each trial. Monkeys maintained cooperation when their roles were reversed on alternate trials. Their cooperative performances demonstrated division of labor; results suggest task-related communication and reciprocal altruism.     

I know you are not looking at me: capuchin monkeys’ (<Emphasis Type="Italic">Cebus apella</Emphasis>) sensitivity to human attentional states

The present study asked whether capuchin monkeys recognize human attentional states. The monkeys requested food from the experimenter by extending an arm (pointing) toward the baited one of two transparent cups. On regular trials the experimenter gave the food immediately to the monkeys upon pointing but on randomly inserted test trials she ignored the pointing for 5 s during which she displayed different attentional states. The monkeys looked at the experimenter's face longer when she looked at the monkeys than when she looked at the ceiling in Experiment 1, and longer when she oriented her head midway between the two cups with eyes open than when she did so with eyes closed in Experiment 2. However, the monkeys showed no differential pointing in these conditions. These results suggest that capuchins are sensitive to eye direction but this sensitivity does not lead to differential pointing trained in laboratory experiments. Furthermore, to our knowledge, this is the first firm behavioral evidence that non-human primates attend to the subtle states of eyes in a food requesting task.