The relationship between problem solving and inhibitory control: cotton-top tamarin (Saguinus oedipus) performance on a reversed contingency task

To explore the relationship between problem solving and inhibitory control, the authors present 4 experiments on cotton-top tamarins (Saguinus oedipus) using a reverse-reward contingency task. In Experiment 1, 1 group of tamarins was given a choice between a small and a large quantity of food. Whichever quantity the tamarins reached for first, they received the alternative. The tamarins consistently picked the larger quantity, thereby receiving the smaller. A 2nd group of tamarins was given the same task, except that if they reached for the larger quantity of food, they received nothing. The tamarins continued to pick the larger quantity, even though this resulted in no food. In addition, most of the tamarins continued to pick the larger quantity even when the food payoff for choosing the smaller quantity was increased (Experiment 2) or when the visual salience of the food was reduced (Experiment 3). Experiment 4 was based on the finding that chimpanzees (Pan troglodytes) that have been trained on the concept of number can solve the reversed contingency task if the food is replaced by Arabic numerals. With the help of a color association, and a higher cost incurred by picking the color associated with 3 food items, the tamarins learned to pick the color associated with 1 food item. These results are compared with those obtained from studies of other primate species, highlighting the importance of comparative studies of problem solving that use comparable methods.     

The role of landmarks in cotton-top tamarin spatial foraging: evidence for geometric and non-geometric features

We report experiments on captive cotton-top tamarins (Saguinus oedipus) designed to explore two components of spatial foraging. First, do tamarins have the capacity to extract geometric information concerning the spatial relationship between a landmark and a piece of food located above or below it? Second, when tamarins use a landmark to find a target location, what non-geometric features of the landmark do they encode? To explore these problems, we created an artificial jungle environment and trained subjects to find food either above or below a target object (i.e., landmark). Once subjects successfully located the food, we transformed various features associated with the landmark, including its color, orientation, and shape; we also manipulated the landmark-food reward distance, the overall shape of the jungle, and the number and position of landmarks. Results showed that the tamarins' success in finding the food reward was not affected by landmark color, orientation, number, or overall shape of the jungle, suggesting that with respect to the particular test conditions, these features are not relevant to the representation of a landmark. Subjects also generalized to novel landmark-food distances, suggesting that they had integrated geometric (i.e., above/below) with non-geometric (i.e., color/shape) features. Performance was negatively affected by changes to the shape of the landmark, indicating that this feature is critical to the representation of a landmark. Accepted after revision: 7 August 2001 Electronic Publication     

Colour versus quantity as cues in reverse-reward-competent squirrel monkeys (Saimiri sciureus)

To assess the relative salience of colour and quantity cues, squirrel monkeys previously trained to reach for the smaller of two quantities of food in a reverse-reward contingency task received colour discrimination training. After initial failure to discriminate between two colours of dots under a differential reinforcement regime, they learned the task when the S- colour was associated with zero reward. The monkeys then showed good retention on the original reverse-reward task of 1 versus 4 with pairs of dots presented in S+ or S- colours. However, on "mismatch" trials of 1S- versus 4S+ , only 2 of 4 monkeys tested showed a preference--1 monkey chose based on quantity, the other based on colour. Individual differences and the possible roles of overshadowing and blocking are discussed.     

Colour versus quantity as cues in reverse-reward-competent squirrel monkeys (Saimiri sciureus)

To assess the relative salience of colour and quantity cues, squirrel monkeys previously trained to reach for the smaller of two quantities of food in a reverse-reward contingency task received colour discrimination training. After initial failure to discriminate between two colours of dots under a differential reinforcement regime, they learned the task when the S? colour was associated with zero reward. The monkeys then showed good retention on the original reverse-reward task of 1 versus 4 with pairs of dots presented in S + or S? colours. However, on “mismatch” trials of 1S? versus 4S + , only 2 of 4 monkeys tested showed a preference—1 monkey chose based on quantity, the other based on colour. Individual differences and the possible roles of overshadowing and blocking are discussed.     

What guides a search for food that has disappeared? Experiments on cotton-top tamarins (Saguinus oedipus).

When food is launched down a vertically positioned S-shaped opaque tube, cotton-top tamarins (Saguinus oedipus) search for the food in the position directly beneath the release point, even though over several trials it never appears in this position (B. M. Hood et al., 1999). Experiment 1 showed that when the trajectory of the food shifts from the vertical to the horizontal plane, tamarins no longer show systematic perseverative errors and, in general, perform better on this invisible displacement task. Experiment 2 showed that tamarins with experience on the horizontal task show less of a bias when tested on the vertical task but nonetheless fail overall to solve this invisible displacement problem; their performance is substantially worse than it was on the horizontal task. Experiment 3 revealed that when the vertically positioned tube is replaced by an occluded ramp, tamarins consistently search in the compartment below the release point, even though most of the tamarins had experience in Experiments 1 and 2. Overall, results indicate that tamarins have a significant gravity bias when searching for food that has disappeared along the vertical plane but also have more general problems finding food that has moved out of sight.     

Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus)

Helping others at no cost to oneself is a simple way to demonstrate other-regarding preferences. Yet, primates exhibit mixed results for other-regarding preferences: chimpanzees and tamarins do not show these effects, whereas capuchin monkeys and marmosets preferentially give food to others. One factor of relevance to this no-cost food donation is the payoff to the donor. Though donors always receive the same payoffs regardless of their choice, previous work varies in whether they receive either a food reward or no food reward. Here, I tested cotton-top tamarins in a preferential giving task. Subjects could choose from two tools, one of which delivered food to a partner in an adjacent cage and the other of which delivered food to an empty cage. Thus, subjects could preferentially give or withhold food from a partner. I varied whether subjects received food payoffs, whether a partner was present or absent, and whether the partner was a non-cagemate or the subject’s mate. Results showed that the subjects’ overall motivation to pull either tool declined when they did not receive any food. Additionally, they did not preferentially donate or withhold food, regardless of their own payoff or their relationship with the partner. Thus, cotton-top tamarins do not take advantage of cost-free food giving, either when they might gain in the future (mates) or when they have no opportunity for future interactions (non-cagemates).     

How the great apes (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) perform on the reversed contingency task: the effects of food quantity and food visibility

S. T. Boysen and G. G. Berntson (1995) found that chimpanzees performed poorly on a reversed contingency task in which they had to point to the smaller of 2 food quantities to acquire the larger quantity. The authors compared the performance of 4 great ape species (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) on the reversed contingency task while manipulating food quantity (0-4 or 1-4) and food visibility (visible pairs or covered pairs). Results showed no systematic species differences but large individual differences. Some individuals of each species were able to solve the reversed contingency task. Both quantity and visibility of the food items had a significant effect on performance. Subjects performed better when the disparity between quantities was smaller and the quantities were not directly visible.     

Natural choice in chimpanzees (Pan troglodytes): Perceptual and temporal effects on selective value

In three experiments, four chimpanzees made choices between two visible food options to assess the validity of the selective value effect (the assignment of value to only the most preferred type of food presented in a comparison). In Experiment 1, we established that all chimpanzees preferred single banana pieces to single apple pieces before presenting the critical test. In this test two chimpanzees preferred a mix of one banana piece and one apple piece to a single banana piece when both banana pieces were approximately the same size, but two chimpanzees were indifferent between the two options, exhibiting the selective value effect. In Experiment 2, when the banana pieces in both options were more closely equated in size, the chimpanzees were biased to choose the single banana piece over the mixed array even though this was the smaller total amount of food. However, in Experiment 3, when we introduced longer intervals between each trial, the chimpanzees preferred the mixed set and thus the larger total amount of food. The results demonstrate that only some chimpanzees exhibit the choice pattern indicative of the selective value effect, and they do so only when item size is not carefully controlled and trials are presented quickly in succession. Thus, the behavior pattern originally labeled the selective value effect may actually be explained by a combination of chimpanzees’ sensitivity to small differences in preferred food amount and chimpanzees tendency to avoid less preferred foods that would delay the acquisition of further preferred food items.     

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.     

Are consonant intervals music to their ears? Spontaneous acoustic preferences in a nonhuman primate

Humans find some sounds more pleasing than others; such preferences may underlie our enjoyment of music. To gain insight into the evolutionary origins of these preferences, we explored whether they are present in other animals. We designed a novel method to measure the spontaneous sound preferences of cotton-top tamarins, a species that has been extensively tested for other perceptual abilities. Animals were placed in a V-shaped maze, and their position within the maze controlled their auditory environment. One sound was played when they were in one branch of the maze, and a different sound for the opposite branch; no food was delivered during testing. We used the proportion of time spent in each branch as a measure of preference. The first two experiments were designed as tests of our method. In Experiment 1, we used loud and soft white noise as stimuli; all animals spent most of their time on the side with soft noise. In Experiment 2, tamarins spent more time on the side playing species-specific feeding chirps than on the side playing species-specific distress calls. Together, these two experiments suggest that the method is effective, providing a spontaneous measure of preference. In Experiment 3, however, subjects showed no preference for consonant over dissonant intervals. Finally, tamarins showed no preference in Experiment 4 for a screeching sound (comparable to fingernails on a blackboard) over amplitude-matched white noise. In contrast, humans showed clear preferences for the consonant intervals of Experiment 3 and the white noise of Experiment 4 using the same stimuli and a similar method. We conclude that tamarins' preferences differ qualitatively from those of humans. The preferences that support our capacity for music may, therefore, be unique among the primates, and could be music-specific adaptations.     

Does effort influence inequity aversion in cotton-top tamarins (Saguinus oedipus)?

The human sense of fairness entails sensitivity not just to equality, the equal division of resources, but also to merit, the relationship between an individual’s share of resources and how hard they worked for their share. Recent evidence suggests that our sensitivity to equality has deep phylogenetic roots: several nonhuman animal species show an aversion to unequal reward distributions. However, the extent to which nonhuman animals share sensitivity to merit remains poorly understood, largely because previous studies have failed to properly manipulate work effort in inequity aversion tasks. Here, we tested whether cotton-top tamarins (Saguinus oedipus) would exhibit a differential response to inequity when acquiring rewards was either (1) effortful or (2) effortless. Subjects engaged in a pulling task in which they had an opportunity to deliver a disadvantageously unequal distribution of food to themselves and a partner (one piece for self, four pieces for partner). We made delivery effortful by adding a weight to the pulling handle. Critically, effort was calibrated to each individual. Results show that individuals varied markedly in their response to effort, highlighting the importance of manipulating work effort at the individual level. Overall, subjects showed little aversion to inequity. However, subjects were slightly less likely to accept inequity when doing so was effortful, although this effect was pronounced in only one individual. Our findings suggest a new method for capturing individual variation in effort and for studying the roots of the concept of merit in nonhuman animals.     

Is your choice my choice? The owners’ effect on pet dogs’ (Canis lupus familiaris) performance in a food choice task

This study investigates the influence of owners on their dogs’ performance in a food choice task using either different or equal quantities of food. Fifty-four pet dogs were tested in three different conditions. In Condition 1 we evaluated their ability to choose between a large and small amount of food (quantity discrimination task). In Condition 2 dogs were again presented with a choice between the large and small food quantity, but only after having witnessed their owner favouring the small quantity. In Condition 3 dogs were given a choice between two equally small quantities of food having witnessed their owner favouring either one or the other. A strong effect of the owner on the dogs’ performance was observed. In Condition 1 dogs as a group chose significantly more often the large food quantity, thus showing their ability to solve the quantity discrimination task. After observing their owner expressing a preference for the small food quantity they chose the large quantity of food significantly less than in the independent choice situation. The tendency to conform to the owner’s choice was higher when the dogs had to choose between equally small quantities of food (Condition 3) rather than between a large and a small one (Condition 2). These results provide evidence that dogs can be influenced by their owners even when their indications are clearly in contrast with direct perceptual information, thus leading dogs to ultimately make counterproductive choices.     

The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments

The authors' goal was to provide a better understanding of the relationship between vocal production and perception in nonhuman primate communication. To this end, the authors examined the cotton-top tamarin's (Saguinus oedipus) combination long call (CLC). In Part 1 of this study, the authors carried out a series of acoustic analyses designed to determine the kind of information potentially encoded in the tamarin's CLC. Using factorial analyses of variance and multiple discriminant analyses, the authors explored whether the CLC encodes 3 types of identity information: individual, sex, and social group. Results revealed that exemplars could be reliably assigned to these 3 functional classes on the basis of a suite of spectrotemporal features. In Part 2 of this study, the authors used a series of habituation-dishabituation playback experiments to test whether tamarins attend to the encoded information about individual identity. The authors 1st tested for individual discrimination when tamarins were habituated to a series of calls from 1 tamarin and then played back a test call from a novel tamarin; both opposite- and same-sex pairings were tested. Results showed that tamarins dishabituated when caller identity changed but transferred habituation when caller identity was held constant and a new exemplar was played (control condition). Follow-up playback experiments revealed an asymmetry between the authors' acoustic analyses of individual identity and the tamarins' capacity to discriminate among vocal signatures; whereas all colony members have distinctive vocal signatures, we found that not all tamarins were equally discriminable based on the habituation-dishabituation paradigm.     

Waiting by mistake: Symbolic representation of rewards modulates intertemporal choice in capuchin monkeys,preschool children and adult humans

In the Delay choice task subjects choose between a smaller immediate option and a larger delayed option. This paradigm, also known as intertemporal choice task, is frequently used to assess delay tolerance, interpreting a preference for the larger delayed option as willingness to wait. However, in the Delay choice task subjects face a dilemma between two preferred responses: “go for more” (i.e., selecting the larger, but delayed, option) vs. “go for sooner” (i.e., selecting the immediate, but smaller, option). When the options consist of visible food amounts, at least some of the choices of the larger delayed option might be due to a failure to inhibit a prepotent response towards the larger option rather than to a sustained delay tolerance. To disentangle this issue, we tested 10 capuchin monkeys, 101 preschool children, and 88 adult humans in a Delay choice task with food, low-symbolic tokens (objects that can be exchanged with food and have a one-to-one correspondence with food items), and high-symbolic tokens (objects that can be exchanged with food and have a one-to-many correspondence with food items). This allows evaluating how different methods of representing rewards modulate the relative contribution of the “go for more” and “go for sooner” responses. Consistently with the idea that choices for the delayed option are sometimes due to a failure at inhibiting the prepotent response for the larger quantity, we expected high-symbolic tokens to decrease the salience of the larger option, thus reducing “go for more” responses. In fact, previous findings have shown that inhibiting prepotent responses for quantity is easier when the problem is framed in a symbolic context. Overall, opting for the larger delayed option in the visible-food version of the Delay choice task seems to partially result from an impulsive preference for quantity, rather than from a sustained delay tolerance. In capuchins and children high-symbolic stimuli decreased the individual’s preference for the larger reward by distancing from its appetitive features. Conversely, the sophisticated symbolic skills of adult humans prevented the distancing effect of high-symbolic stimuli in this population, although this result may be due to methodological differences between adult humans and the other two populations under study. Our data extend the knowledge concerning the influence of symbols on both human and non-human primate behavior and add a new element to the interpretation of the Delay choice task. Since high-symbolic stimuli decrease the individual’s preference for the larger reward by eliminating those choices due to prepotent responses towards the larger quantity, they allow to better discriminate responses based on genuine delay aversion. Thus, these findings invite greater caution in interpreting the results obtained with the visible-food version of the Delay choice task, which may overestimate delay tolerance.     

The representations underlying infants' choice of more: object files versus analog magnitudes

A new choice task was used to explore infants' spontaneous representations of more and less. Ten- and 12-month-old infants saw crackers placed sequentially into two containers, then were allowed to crawl and obtain the crackers from the container they chose. Infants chose the larger quantity with comparisons of 1 versus 2 and 2 versus 3, but failed with comparisons of 3 versus 4, 2 versus 4, and 3 versus 6. Success with visible arrays ruled out a motivational explanation for failure in the occluded 3-versus-6 condition. Control tasks ruled out the possibility that presentation duration guided choice, and showed that presentation complexity was not responsible for the failure with larger numbers. When crackers were different sizes, total surface area or volume determined choice. The infants' pattern of success and failure supports the hypothesis that they relied on object-file representations, comparing mental models via total volume or surface area rather than via one-to-one correspondence between object files.     

Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food-choice for conspecifics

The issue whether non-human primates have other-regarding preference and/or inequity aversion has been under debate. We investigated whether tufted capuchin monkeys are sensitive to others’ reward in various experimental food sharing settings. Two monkeys faced each other. The operator monkey chose one of two food containers placed between the participants, each containing a food item for him/herself and another for the recipient. The recipient passively received either high- or low-value food depending on the operator’s choice, whereas the operator obtained the same food regardless of his/her choice. The recipients were either the highest- or lowest-ranking member of the group, and the operators were middle-ranking. In Experiment 1, the operators chose the high-value food for the subordinate recipient more frequently than when there was no recipient, whereas they were indifferent in their choice for the dominant. This differentiated behavior could have been because the dominant recipient frequently ate the low-value food. In Experiment 2, we increased the difference in the value of the two food items so that both recipients would reject the low-value food. The results were the same as in Experiment 1. In Experiment 3, we placed an opaque screen in front of the recipient to examine effects of visual contact between the participants. The operators’ food choice generally shifted toward providing the low-value food for the recipient. These results suggest that capuchins are clearly sensitive to others’ reward and that they show other-regarding preference or a form of inequity aversion depending upon the recipients and the presence of visual contact.     

“We will work for you” – Social influence may suppress individual food preferences in a communicative situation in dogs

The level of motivation (i.e. incentive power) is thought to be one of the most important factors affecting performance and learning in various tasks. We investigated whether reward quality has an effect on the performance of family dogs in a two-way object choice test in which they can find the hidden food by relying on distal momentary human pointing cues. In three experiments we varied (1) the type of food reward according to the subjects’ own preference; (2) the quality of the reward offered at the same time in the indicated and not-indicated locations; and (3) the order of the high or low quality rewards in consecutive sessions. In Experiment 1, we first tested whether dogs prefer one kind of reward over another. Then one group was tested with the ‘preferred’ food as reward in the indicated bowl, while dogs in the other group received the ‘non-preferred’ food as reward. We did not find any difference between the performance and choice latencies of the two groups. In Experiment 2 for the first group, the indicated bowl contained a piece of carrot and the not-indicated bowl was empty. In the second group the indicated bowl contained carrot, but the not-indicated bowl contained sausage. According to a preliminary preference test, most dogs prefer sausage over carrot invariably. After 20 trials, the two groups performed surprisingly similarly. There was no difference found between groups in the number of correct choices, incorrect choices and non-choices. However, the comparison between the first and last five trials revealed that subjects who found sausage when they chose the not-indicated bowl (did not follow the pointing) chose the non-indicated bowl significantly more often toward the end of their test session. In Experiment 3, each dog received two sessions with 12 pointing trials in each. For the first session, one group was rewarded with sausage and the other with carrot upon choosing the indicated bowl. In the second session, the indicated bowl contained dry dog food for both groups. We found that correct choices and response latencies did not change over two sessions in the ‘sausage’ group. In the ‘carrot’ group, the dogs chose faster in the second session, but their performance did not improve; in fact, they chose the not-indicated bowl more often than the indicated bowl. As a conclusion, we can say that reward quality had some effect on dogs’ choice behavior in these experiments. The drop in their performance was not drastic, taking into account the general refusal to eat one of the ‘rewards’ (carrot) during the preference tests and also during the test trials. It seems that incentive contrast may play a relatively minor role in dog-human social interactions. Appropriate reward quality can be very important in asocial problem solving tasks, but, when interacting with humans, following human signals may override the effect of changed incentive power.     

Mangabeys (<Emphasis Type="Italic">Cercocebus torquatus lunulatus</Emphasis>) solve the reverse contingency task without a modified procedure

Problem solving often relies on generating new responses while inhibiting others, particularly prepotent ones. A paradigm to study inhibitory abilities is the reverse contingency task (Boysen and Berntson in J Exp Psychol Anim Behav Process 21:82–86, 1995), in which two different quantities of food are offered to an individual who receives the array he did not choose. Therefore, mastery of the task demands selecting the smaller quantity to obtain the larger one. Several non-human primates have been tested in the reverse contingency task. To date, only great apes and rhesus monkeys (Macaca mulatta) have succeeded in the original task, with no need of procedural modifications as the large-or-none contingency, correction trials or symbolic stimuli substituting for actual food quantities. Here, four mangabeys were presented with two stimulus arrays of one and four raisins in the context of the reverse contingency task. Three of them learned to perform the task well above chance without a modified procedure. They also reached above-chance performance when presented with two stimulus arrays of zero and four raisins, despite the initial difficulty of choosing a null quantity. After a period of 7–10 months, in which the animals were not tested on any task, all three subjects continued to perform well, even when presented with novel quantity pairs.     

Probing the limits of tool competence: Experiments with two non-tool-using species (Cercopithecus aethiops and Saguinus oedipus)

Non-human animals vary in their ability to make and use tools. The goal of the present study was to further explore what, if anything, differs between tool-users and non-tool-users, and whether these differences lie in the conceptual or motor domain. We tested two species that typically do not use tools-cotton top tamarins (Saguinus oedipus) and vervet monkeys (Cercopithecus aethiops)-on problems that mirrored those designed for prolific tool users such as chimpanzees. We trained subjects on a task in which they could choose one of two canes to obtain an out-of-reach food reward. After training, subjects received several variations on the original task, each designed to examine a specific conceptual aspect of the pulling problem previously studied in other tool-using species. Both species recognized that effective pulling tools must be made of rigid materials. Subsequent conditions revealed significant species differences, with vervets outperforming tamarins across many conditions. Vervets, but not tamarins, had some recognition of the relationship between a tool's orientation and the position of the food reward, the relationship between a tool's trajectory and the substance that it moves on, and that tools must be connected in order to work properly. These results provide further evidence that tool-use may derive from domain-general, rather than domain-specific cognitive capacities that evolved for tool use per se.     

What do rooks (Corvus frugilegus) understand about physical contact?

Rooks (Corvus frugilegus) do not use tools, but rapidly solve tests of physical cognition. The authors tested whether rooks understand the concept of physical contact using a task comprising a clear horizontal tube containing a stick with a disk attached to it and a piece of food. The rooks chose which side to pull the stick from to make the food accessible. Two configurations were used, with either the food or disk central along the tube. All 8 rooks solved the food-central configuration, but failed the disk-central configuration. Although they did not demonstrate an understanding of contact, further tests established that they could learn to solve these tasks provided there were salient stick cues. This result may arise because sticks are ecologically important for rooks.