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.

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.

Transport of Functionally Appropriate Tools by Capuchin Monkeys (Cebus apella)

Capuchin monkeys are notable among New World monkeys for their widespread use of tools. They use both hammer tools and insertion tools in the wild to acquire food that would be unobtainable otherwise. Evidence indicates that capuchins transport stones to anvil sites and use the most functionally efficient stones to crack nuts. We investigated capuchins’ assessment of functionality by testing their ability to select a tool that was appropriate for two different tool-use tasks: A stone for a hammer task and a stick for an insertion task. To select the appropriate tools, the monkeys investigated a baited tool-use apparatus (insertion or hammer), traveled to a location in their enclosure where they could no longer see the apparatus, made a selection between two tools (stick or stone), and then could transport the tool back to the apparatus to obtain a walnut. Four capuchins were first trained to select and use the appropriate tool for each apparatus. After training, they were then tested by allowing them to view a baited apparatus and then travel to a location 8 m distant where they could select a tool while out of view of the apparatus. All four monkeys chose the correct tool significantly more than expected and transported the tools back to the apparatus. Results confirm capuchins’ propensity for transporting tools, demonstrate their capacity to select the functionally appropriate tool for two different tool-use tasks, and indicate that they can retain the memory of the correct choice during a travel time of several seconds.

IMPULSE CONTROL AND COOPERATION IN CAPUCHIN MONKEYS (Cebus apella)

The benefits animals derive from living in social groups have produced the evolution of many forms of cooperative behavior. To cooperate, two or more individuals coordinate their actions to accomplish a common goal. One cognitive process that has the potential to influence cooperation is self control. Individuals delaying their impulsive choice for an immediate reward may potentially receive a larger reward later by cooperating with others. In this study, I measured whether brown capuchin monkeys (Cebus apella) were capable of impulse control and whether impulse control was related to cooperation. Impulse control and cooperation were measured using a lazy susan-like apparatus, on which animals could turn a wheel to receive food rewards. The capuchins went through two training phases that taught them how to turn the wheel efficiently to obtain rewards and how to turn the wheel to obtain the larger of two rewards. After training, I tested impulse control by giving the capuchins a choice between a smaller and a larger reward placed at shorter or more distant locations on the wheel. The capuchins demonstrated impulse control in that they tended to inhibit the impulse to select the smaller reward when it was closer and easier to reach and instead selected the larger reward when it was farther away. Cooperation was tested in all possible dyads of seven individuals, a total of 21 dyads, by allowing each dyad 10 trials to work together with effort on the lazy-susan so that each would obtain a reward. Seventeen out of 21 dyads cooperated by simultaneously moving the wheel in the same direction. The correlation between how often a particular dyad cooperated and their average impulse control score was not statistically significant, r(21) = -.125, p = .591. Capuchins demonstrated impulse control and cooperation using this novel apparatus but the two abilities were not related. Other factors such as the unique social relationship between two individuals may play a more prominent role in the motivation to cooperate rather than the cognitive capacity to inhibit behavior.

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.

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.