The interface between morphology and action planning: a comparison of two species of New World monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities.

Capuchin Monkeys Exercise Self-control by Choosing Token Exchange Over an Immediate Reward

Self-control is a prerequisite for complex cognitive processes such as cooperation and planning. As such, comparative studies of self-control may help elucidate the evolutionary origin of these capacities. A variety of methods have been developed to test for self-control in non-human primates that include some variation of foregoing an immediate reward in order to gain a more favorable reward. We used a token exchange paradigm to test for self-control in capuchin monkeys (Cebus apella). Animals were trained that particular tokens could be exchanged for food items worth different values. To test for self-control, a monkey was provided with a token that was associated with a lower-value food. When the monkey exchanged the token, the experimenter provided the monkey with a choice between the lower-value food item associated with the token or another token that was associated with a higher-value food. If the monkey chose the token, they could then exchange it for the higher-value food. Of seven monkeys trained to exchange tokens, five demonstrated that they attributed value to the tokens by differentially selecting tokens for higher-value foods over tokens for lower-value foods. When provided with a choice between a food item or a token for a higher-value food, two monkeys selected the token significantly more than expected by chance. The ability of capuchin monkeys to forego an immediate food reward and select a token that could then be traded for a more preferred food demonstrated some degree of self-control. Thus, results suggest a token exchange paradigm could be a successful technique for assessing self-control in this New World species.

The Interface Between Morphology and Action Planning: a Comparison of Two Species of New World Monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities. (C) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Audience Effects in COgnitive Task Performance in Capuchin Monkeys (Cebus apella)

Primates as a taxonomic Order have the largest brains corrected for body size in the animal kingdom. These large brains have allowed primates to evolve the capacity to demonstrate advanced cognitive processes across a wide array of abilities. Nonhuman primates are particularly adept at social learning, defined as the modification of behavior by observing the actions of others. Additionally, primates often exploit resources differently depending on their social context. In this study, capuchin monkeys (Cebus apella) were tested on a cognitive task in three social contexts to determine if social context influenced their performance on the task. The three social contexts included: alone, having a dominant individual in an adjacent compartment, and having a subordinate individual in the adjacent compartment. The benefits to this design were thatthe social context was the only variable influencing performance, whereas in previous studies investigating audience effects other animals could physically and directly influence a subject's performance in an open testing situation. Based on past studies, Ipredicted that the presence of a dominant individual would reduce cognitive task performance compared to the other conditions. The cognitive test used was a match-tosample discrimination task in which animals matched combinations of eight geometric shapes. Animals were trained on this task in an isolated context until they reached a baseline level of proficiency and were then tested in the three social contexts in a random order multiple times. Two subjects (Mt and Dv) have successfully completed trials under all conditions. Results indicated that there were no significant difference in taskperformance across the three conditions (Dv x^2 (1) = 0.42, p=0.58; Mt x^2 (1) = 0.02, p=0.88). In all conditions, subjects performed significantly above chance (i.e., 39/60 trials determined by a binomial distribution). Results are contrary to previous studies thatreport low status monkeys 'play dumb' when testing in a mixed social context, possibly because other studies did not account for aggressive interference by dominants while testing. Results of this study suggest that the mere presence of a dominant individualdoes not necessarily affect performance on a cognitive task, but rather the imminence of physical aggression is the most important factor influencing testing in a social context.

The contexts of scratching behavior and postconflict behavior in squirrel monkeys (Saimiri sciureus)

Self-directed behavior (SDB), such as scratching, is a reliable indicator of emotional arousal in non-human primates. In contrast, affiliative behavior, such as social grooming, has been shown to have a calming effect in primates and reduce arousal. In order to test whether the expression of SDB was related to arousal, the scratching behavior of eight captive squirrel monkeys (Saimiri sciureus) was compared across four social contexts (huddling, proximity to others, solitary and post-conflict). In addition,rates of scratching were examined before and after affiliative behavior during the postconflict context. I tested for this effect by using the post-conflict/matched control(PC/MC) method in which post-conflict (PC) behavior of an animal is compared to thebehavior of the same animal in a baseline, nonaggressive situation or a matched control(MC). Context and associated scratching data were obtained from a total of 98 hours of focal sample data. Scratching was significantly lower while animals were huddling thanthe other two contexts. Scratching rates while solitary were significantly higher than those occurring while animals were in proximity. Scratching was also higher in PC than MC. Following conflict, animals were significantly more likely to make contact withthird parties not involved in aggression. Most of these (79%) were a third party approaching a combatant. Further, scratching rates decreased following post-conflict third party contacts and the decrease was not due to a general decrease in scratching thatmight have been occurring after the aggressive interaction. Huddling behavior appears to reduce arousal in squirrel monkeys and may act as a tension-reduction mechanism. The elevated scratching in the solitary context may suggest that squirrel monkeys may be engaged in activities while solitary, such as vigilant behavior that may increase arousal. The third party post conflict affiliative contacts observed were the first such interactions observed in squirrel monkeys. The fact that these third contacts reduced scratching ratesin the combatants indicates that 'consolation' may have been demonstrated in this species. The overall pattern of results suggested that scratching was reliable behavioral indicator of anxiety in squirrel monkeys. These results indicate that overt behavior can be used to assess emotional states in this and other species, acting as a mediator to understanding how emotions regulate social behavior.

The Expression Of Motor Planning In Squirrel Monkeys (Saimiri sciureus) And Brown Capuchins (Cebus apella)

Multiple recent studies provide evidence that both human and nonhuman primates possess motor planning abilities. I tested for the demonstration of motor planning in two previously untested primate species through two experiments. In the first experiment, I compared the extent to which squirrel monkeys (Saimiri sciureus) and brown capuchins (Cebus apella) plan their movements in a grasping task. Individuals were presented with an inverted cup that required being turned and held upright in order to extract a food reward from the inside of the cup. This task was most efficiently solved by using an initially awkward inverted grasp that affords a comfortable hand and arm orientation at the end of the movement (known as end-state comfort). While certain individuals from both species exhibited end-state comfort, many of the capuchins never demonstrated this type of motor planning. Furthermore, the squirrel monkeys used the efficient grasp significantly more than the capuchins. In the second experiment, I presented the capuchins with another grasping task to test if they would express motor planning abilities in a different context. Here, the capuchins were offered a dowel that was baited on either the left or right end. A radial grasp with the thumb pointing towards the baited end was considered to be the most efficient grasp because it afforded a comfortable final position. The capuchins switched hands and used an overhand radial grasp on the dowel significantly more often than not, thus demonstrating motor planning in this task. The grasps typically utilized by these two closely related species differ considerably in that capuchins are capable of exercising precision grips, whereas squirrel monkeys are limited to whole-handed power grips. Moreover, unlike capuchins, squirrel monkeys are not particularly dexterous nor are they capable of precise manipulative actions. It is therefore more beneficial for squirrel monkeys to plan their movements efficiently because they are less capable of compensating for inappropriate initial grasps. Due to the appreciable variability in the expression of motor planning skills across species, I proposed that morphological constraints might explain the observed discrepancies in movement planning among different primate species.

Brown Capuchins (Cebus apella) Exhibit Self-Control on a Delay of Gratification Food Exchange Task When Food Options Differ Qualitatively

Self-control allows an individual to obtain a more preferred outcome by forgoing an immediate interest. Self-control is an advanced cognitive process because it involves the ability to weigh the costs and benefits of impulsive versus restrained behavior, determine the consequences of such behavior, and make decisions based on the most advantageous course of action. Self-control has been thoroughly explored in Old World primates, but less so in New World monkeys. There are many ways to test self-control abilities in non-human primates, including exchange tasks in which an animal must forgo an immediate, less preferred reward to receive a delayed, more preferred reward. I examined the self-control abilities of six capuchin monkeys using a task in which a monkey was given a less preferred food and was required to wait a delay interval to trade the fully intact less preferred food for a qualitatively higher, more preferred food. Partially eaten pieces of the less preferred food were not rewarded, and delay intervals increased on an individual basis based on performance. All six monkeys were successful in inhibiting impulsivity and trading a less preferred food for a more preferred food at the end of a delay interval. The maximum duration each subject postponed gratification instead of responding impulsively was considered their delay tolerance. This study was the first to show that monkeys could inhibit impulsivity in a delay of gratification food exchange task in which the immediate and delayed food options differed qualitatively and a partially eaten less preferred food was not rewarded with the more preferred food at the end of a delay interval. These results show that New World monkeys possess advanced cognitive abilities similar to those of Old World primates.

The Use of Human and Conspecific Gestures By Capuchin Monkeys to Solve an Object-Choice Task

Most primates live in highly complex social systems, and therefore have evolved similarly complex methods of communicating with each other. One type of communication is the use of manual gestures, which are only found in primates. No substantial evidence exists indicating that monkeys use communicative gestures in the wild. However, monkeys may demonstrate the ability to learn and/or use gestures in certain experimental paradigms since they¿ve been shown to use other visual cues such as gaze. The purpose of this study was to investigate if ten brown capuchin monkeys (Cebus apella) were able to use gestural cues from monkeys and a pointing cue from a human to obtain a hidden reward. They were then tested to determine if they could transfer this skill from monkeys to humans and from humans to monkeys. One group of monkeys was trained and tested using a conspecific as the cue giver, and was then tested with a human cue-giver. The second group of monkeys began training and testing with a human cue giver, and was then tested with a monkey cue giver. I found that two monkeys were able to use gestural cues from conspecifics (e.g., reaching) to obtain a hidden reward and then transfer this ability to a pointing cue from a human. Four monkeys learned to use the human pointing cue first, and then transferred this ability to use the gestural cues from conspecifics to obtain a hidden reward. However, the number of trials it took for each monkey to transfer the ability varied considerably. Some subjects spontaneously transferred in the minimum number of trials needed to reach my criteria for successfully obtaining hidden rewards (N = 40 trials), while others needed a large number of trials to do so (e.g. N = 190 trials). Two subjects did not perform successfully in any of the conditions in which they were tested. One subject successfully used the human pointing cue and a human pointing plus vocalization cue, but did not learn the conspecific cue. One subject learned to use the conspecific cue but not the human pointing cue. This was the first study to test if brown capuchin monkeys could use gestural cues from conspecifics to solve an object choice task. The study was also the first to test if capuchins could transfer this skill from monkeys to humans and from humans to monkeys. Results showed that capuchin monkeys were able to flexibly use communicative gestures when they were both unintentionally given by a conspecific and intentionally given by a human to indicate a source of food.