Contrast of hand preferences between communicative gestures and non-communicative actions in baboons: Implications for the origins of hemispheric specialization for language

Gestural communication is a modality considered in the literature as a candidate for determining the ancestral prerequisites of the emergence of human language. As reported in captive chimpanzees and human children, a study in captive baboons revealed that a communicative gesture elicits stronger degree of right-hand bias than non-communicative actions. It remains unclear if it is the communicative nature of this manual behavior which induces such patterns of handedness. In the present study, we have measured hand use for two uninvestigated behaviors in a group of captive olive baboons: (1) a non-communicative self-touching behavior (“muzzle wipe” serving as a control behavior), (2) another communicative gesture (a ritualized “food beg”) different from the one previously studied in the literature (a species-specific threat gesture, namely “hand slap”) in the same population of baboons. The hand preferences for the “food beg” gestures revealed a trend toward right-handedness and significantly correlated with the hand preferences previously reported in the hand slap gesture within the same baboons. By contrast, the hand preferences for the self-touching behaviors did not reveal any trend of manual bias at a group-level nor correlation with the hand preferences of any communicative gestures. These findings provide additional support to the hypothesized existence in baboons of a specific communicative system involved in the production of communicative gestures that may tend to a left-hemispheric dominance and that may differ from the system involved in purely motor functions. The hypothetical implications of these collective results are discussed within the theoretical framework about the origins of hemispheric specialization for human language.     

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.     

Tool use by chimpanzees (Pan troglodytes) of the Arnhem Zoo community

Abstract: Chimpanzees have a large repertoire of tool-use behaviors. This study reports on the variety and the extent of tool use exhibited by the chimpanzees of the Arnhem Zoo community in The Netherlands, living in an enriched captive setting since 1971. The use of tools by 29 chimpanzees aged from 0 to 37 years was observed. We identified 13 types of tool use comparable to those found in the wild. Some of these types of tool use seem to be specific to this community, and can be explained by the ecological characteristics of this captive setting. Chimpanzees started to use tools from the age of 2 years. Young chimpanzees, from 5 to 9 years old, showed a greater repertoire of tool use than infants and adults. All types of tool use in the community have appeared by the age of 10, the age of puberty for chimpanzees. Multivariate analysis was applied for the 29 individuals by 13 types of tool use in a one-zero matrix. The results show two major categories of tool use, one in a practical or substantial context and the other in a nonpractical or play context. The subjects clustered into groups reflecting developmental stages, although there are great individual differences. In conclusion, this captive community provides a unique opportunity to clarify the details of tool use by chimpanzees.     

Bubble ring play of bottlenose dolphins (Tursiops truncatus): implications for cognition

Research on the cognitive capacities of dolphins and other cetaceans (whales and porpoises) has importance for the study of comparative cognition, particularly with other large-brained social mammals, such as primates. One of the areas in which cetaceans can be compared with primates is that of object manipulation and physical causality, for which there is an abundant body of literature in primates. The authors supplemented qualitative observations with statistical methods to examine playful bouts of underwater bubble ring production and manipulation in 4 juvenile male captive bottlenose dolphins (Tursiops truncatus). The results are consistent with the hypothesis that dolphins monitor the quality of their bubble rings and anticipate their actions during bubble ring play.     

Lion-tailed macaques (Macaca silenus) manufacture and use tools

Lion-tailed macaques (Macaca silenus) in captive social groups spontaneously manufactured and used tools to extract syrup from an apparatus that was designed to accommodate probing behavior. An attempt to replicate these findings with mandrills (Mandrillus sphinx) was unsuccessful. This report is the first to describe spontaneous manufacture of tools in any group of Old World monkeys and provides evidence of greater continuity among primates for the expression of complex cognitive abilities. These data are consistent with hypotheses that lion-tailed macaques have extensive propensities for advanced sensorimotor skills and that omnivorous, extractive foraging is associated with the manufacture and use of tools. I present a proximate model that integrates sensorimotor and social factors to account for diverse expression of tool-related behavior.     

Use of human visual attention cues by olive baboons (Papio anubis) in a competitive task

The ability of 4 olive baboons (Papio anubis) to use human gaze cues during a competitive food task was investigated. Three baboons used head orientation as a cue, and 1 individual also used eye direction alone. As the baboons did not receive prior training with gestural cues, their performance suggests that the competitive paradigm may be more appropriate for testing nonhuman primates than the standard object-choice paradigm. However, the baboons were insensitive to whether the experimenter could actually perceive the food item, and therefore the use of visual orientation cues may not be indicative of visual perspective-taking abilities. Performance was disrupted by the introduction of a screen and objects to conceal food items and by the absence of movement in cues presented.     

Olive baboons communicate intentionally by pointing

A pointing gesture creates a referential triangle that incorporates distant objects into the relationship between the signaller and the gesture’s recipient. Pointing was long assumed to be specific to our species. However, recent reports have shown that pointing emerges spontaneously in captive chimpanzees and can be learned by monkeys. Studies have demonstrated that both human children and great apes use manual gestures (e.g. pointing), and visual and vocal signals, to communicate intentionally about out-of-reach objects. Our study looked at how monkeys understand and use their learned pointing behaviour, asking whether it is a conditioned, reinforcement-dependent response or whether monkeys understand it to be a mechanism for manipulating the attention of a partner (e.g. a human). We tested nine baboons that had been trained to exhibit pointing, using operant conditioning. More specifically, we investigated their ability to communicate intentionally about the location of an unreachable food reward in three contexts that differed according to the human partner’s attentional state. In each context, we quantified the frequency of communicative behaviour (auditory and visual signals), including gestures and gaze alternations between the distal food and the human partner. We found that the baboons were able to modulate their manual and visual communicative signals as a function of the experimenter’s attentional state. These findings indicate that monkeys can intentionally produce pointing gestures and understand that a human recipient must be looking at the pointing gesture for them to perform their attention-directing actions. The referential and intentional nature of baboons’ communicative signalling is discussed.     

Using Automated Learning Devices for Monkeys (ALDM) to study social networks

Social network analysis has become a prominent tool to study animal social life, and there is an increasing need to develop new systems to collect social information automatically, systematically, and reliably. Here we explore the use of a freely accessible Automated Learning Device for Monkeys (ALDM) to collect such social information on a group of 22 captive baboons (Papio papio). We compared the social network obtained from the co-presence of the baboons in ten ALDM testing booths to the social network obtained through standard behavioral observation techniques. The results show that the co-presence network accurately reflects the social organization of the group, and also indicate under which conditions the co-presence network is most informative. In particular, the best correlation between the two networks was obtained with a minimum of 40 days of computer records and for individuals with at least 500 records per day. We also show through random permutation tests that the observed correlations go beyond what would be observed by simple synchronous activity, to reflect a preferential choice of closely located testing booths. The use of automatized cognitive testing therefore presents a new way of obtaining a large and regular amount of social information that is necessary to develop social network analysis. It also opens the possibility of studying dynamic changes in network structure with time and in relation to the cognitive performance of individuals.     

Comparing responses to novel objects in wild baboons (<Emphasis Type="Italic">Papio ursinus</Emphasis>) and geladas (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>)

Behavioral flexibility is considered by some to be one of the hallmarks of advanced cognitive ability. One measure of behavioral flexibility is how subjects respond to novel objects. Despite growing interest in comparative cognition, no comparative research on neophilia in wild primates has been conducted. Here, we compare responses to novel objects in wild chacma baboons (Papio ursinus) and geladas (Theropithecus gelada). Baboons and geladas are closely related taxa, yet they differ in their ecology and degree of social tolerance: (1) baboons are habitat and dietary generalists, whereas geladas have one of the most specialized primate diets (90% grass); (2) baboons exhibit an aversion toward extra-group individuals, whereas geladas typically exhibit an attraction toward them. Using subjects of all age and sex classes, we examined responses to three different objects: a plastic doll, a rubber ball, and a metal can. Overall, baboon subjects exhibited stronger responses to the objects (greater neophilia and exploration) than gelada subjects, yet we found no evidence that the geladas were afraid of the objects. Furthermore, baboons interacted with the objects in the same way they might interact with a potential food item. Responses were unrelated to sex, but immatures showed more object exploration than adults. Results corroborate novel object research conducted in captive populations and suggest that baboons and geladas have differences in behavioral flexibility (at least in this cognitive domain) that have been shaped by ecological (rather than social) differences between the two species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Tool selectivity in a non-primate,the New Caledonian crow (Corvus moneduloides)

We present an experiment showing that New Caledonian crows are able to choose tools of the appropriate size for a novel task, without trial-and-error learning. This species is almost unique amongst all animal species (together with a few primates) in the degree of use and manufacture of polymorphic tools in the wild. However, until now, the flexibility of their tool use has not been tested. Flexibility, including the ability to select an appropriate tool for a task, is considered to be a hallmark of complex cognitive adaptations for tool use. In experiment 1, we tested the ability of two captive birds (one male, one female), to select a stick (from a range of lengths provided) matching the distance to food placed in a horizontal transparent pipe. Both birds chose tools matching the distance to their target significantly more often than would be expected by chance. In experiment 2, we used a similar task, but with the tools placed out of sight of the food pipe, such that the birds had to remember the distance of the food before selecting a tool. The task was completed only by the male, who chose a tool of sufficient length significantly more often than chance but did not show a preference for a matching length. Electronic Publication     

Tool choice on the basis of rigidity in capuchin monkeys

Wild capuchin monkeys select stone tools to crack open nuts on the basis of their weight and friability, two non-visual functional properties. Here, we investigated whether they would select new stick-like tools on the basis of their rigidity. In Experiment 1, subjects faced an out-of-reach reward and a choice of three unfamiliar tools differing in color, diameter, material, and rigidity. In order to retrieve the reward, capuchins needed to select the rigid tool exemplar. Capuchins gathered information regarding tools’ pliability either by (1) manipulating the tools themselves (manipulation condition), (2) observing a human demonstrator repeatedly bending the tools (observation condition), or (3) seeing the tools placed on a platform without any manipulation taking place (visual static condition). Subjects selected the rigid tool above chance levels in both the manipulation and observation conditions, but not in the visual static condition. In Experiment 2, subjects needed to select and use a flexible tool to access a liquid reward (as opposed to the rigid tool, as in previous experiment). Again, capuchins selected above chance levels the appropriate tool (i.e., flexible), thus demonstrating a good appreciation of the relation between the tool properties and the task requirements.     

Automatic testing of cognitive performance in baboons maintained in social groups

Laboratory procedures used to study the cognitive functions of primates traditionally have involved removal of the subjects from their living quarters to be tested singly in a remote experimental room. This article presents an alternative research strategy favoring testing primates while they are maintained in their social group. The automatic learning device for monkeys (ALDM) is a computerized test system controlled by an automatic radio frequency identification of subjects. It is provided ad lib inside the social group of monkeys, for voluntary self-testing on a 24-h schedule. Nine baboons were tested with ALDM during a 7-month period. Experiments were performed to assess learning in motor control and abstract reasoning tasks. The results revealed high trial frequencies and excellent learning performance, even in tasks involving the highest cognitive complexities. A different study using ALDM with a group of 3 rhesus monkeys revealed social influences on learning. Beyond its interest for cognitive psychologists, ALDM is of interest for pharmacologists and cognitive neuroscientists working with nonhuman primates. ALDM also can serve as an enrichment tool for captive animals and may be used to study a variety of species other than primates.     

Spontaneous performance of wild baboons on three novel food-access puzzles

Although the technical problem-solving expertise of nonhuman primates has been investigated extensively in captivity, few species have been tested in their natural habitats. Here I examine the physical cognition of wild savanna baboons (Papio anubis), a species that occupies an omnivorous foraging niche in which a variety of embedded food items are extracted and processed. Baboons were tested on three puzzles, each involving high-quality food that required removal from a novel obstruction: (1) a string-pulling puzzle in which food was hung from tree branches, (2) a twig-dipping puzzle in which food was embedded in a vertical tube, and (3) a stick-pushing puzzle in which food was contained in a horizontal conduit. The baboons failed to solve the second and third puzzles even when tools had been appropriately positioned in advance. And although they solved the first puzzle, their actions (running while holding food that was still attached to the string), suggested they did not fully comprehend the string’s connective property. The baboons’ performance might reflect the time constraints of life in the wild, which relative to captivity may provide fewer opportunities for the development of understanding about the physical properties of objects and their potential uses as tools. Further experiments on the physical cognition of baboons and many other primate species in their natural habitats would help test this ontogenetic hypothesis. Such field experiments would be especially fruitful if they continued to target extractive foragers like baboons: these experiments could simultaneously provide a test of phylogenetic hypotheses that invoke extractive foraging as the key stimulus for brain expansion in savanna-dwelling hominids. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Ventral encoding of functional affordances: A neural pathway for identifying errors in action

Functional tool usage is a critical aspect of our daily lives. Not only must we know which tools to use for a specific action goal, we must also know how to manipulate those tools in meaningful way to achieve the goal of the action. The purpose of this study was to identify the regions of the brain critical to supporting the process of understanding errors in tool manipulation. Using fMRI, neural activations were recorded while subjects were presented with images demonstrating typical action scenes (screwdriver used on a screw), but with the tool being manipulated either correctly (screwdriver held by handle) or incorrectly (screwdriver held by bit rather than handle). Activations in fMRI for identifying correct over incorrect tool manipulation were seen along the canonical parietofrontal action network, while activations for identifying incorrect over correct tool manipulation were primarily seen at superior temporal areas and insula. We expand our hypotheses about ventral brain networks identifying contextual error to further suggest mechanisms for understanding functional tool actions, which collectively we regard as functional affordances. This proposes a fundamental role for ventral brain areas in functional action understanding.     

Transport of tools to food sites in tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Tool use and transport represent cognitively important aspects of early hominid evolution, and nonhuman primates are often used as models to examine the cognitive, ecological, morphological and social correlates of these behaviors in order to gain insights into the behavior of our early human ancestors. In 2001, Jalles-Filho et al. found that free-ranging capuchin monkeys failed to transport tools (stones) to food sites (nuts), but transported the foods to the tool sites. This result cast doubt on the usefulness of Cebus to model early human tool-using behavior. In this study, we examined the performance of six captive tufted capuchin monkeys (Cebus apella) in a tool transport task. Subjects were provided with the opportunity to transport two different tools to fixed food reward sites when the food reward was visible from the tool site and when the food reward was not visible from the tool site. We found that the subjects quickly and readily transported probing tools to an apparatus baited with syrup, but rarely transported stones to a nut-cracking apparatus. We suggest that the performance of the capuchins here reflects an efficient foraging strategy, in terms of energy return, among wild Cebus monkeys.     

Orangutans (Pongo spp.) may prefer tools with rigid properties to flimsy tools

Preference for tools with either rigid or flexible properties was explored in orangutans (Pongo spp.) through an extension of D. J. Povinelli, J. E. Reaux, and L. A. Theall's (2000) flimsy-tool problem. Three captive orangutans were presented with three unfamiliar pairs of tools to solve a novel problem. Although each orangutan has spontaneously used tools in the past, the tools presented in this study were novel to the apes. Each pair of tools contained one tool with rigid properties (functional) and one tool with flimsy properties (nonfunctional). Solving the problem required selection of a rigid tool to retrieve a food reward. The functional tool was selected in nearly all trials. Moreover, two of the orangutans demonstrated this within the first test trials with each of the three tool types. Although further research is required to test this statistically, it suggests either a preexisting preference for rigid tools or comprehension of the relevant features required in a tool to solve the task. The results of this study demonstrate that orangutans can recognize, or learn to recognize, relevant tool properties and can choose an appropriate tool to solve a problem.     

Strategy-dependent changes in memory: Effects on behavior and brain activity

In the present study, an implicit strategy manipulation was used to explore the contribution of memory strategy to brain activation and behavioral performance. Participants were biased to use either a short-term (maintenance-focused) or long-term (retrieval-focused) memory strategy within a single memory task through manipulation of task context. In comparing directly matched trials across the different task contexts, we observed clear changes in both behavioral performance and brain activity across a network of regions located primarily within lateral and medial frontal cortex. These effects of the memory strategy manipulation suggest that when a retrieval-focused strategy is induced, mnemonic processes are preferentially engaged during the encoding period. In contrast, when a maintenance-focused strategy is induced, mnemonic processes are preferentially engaged during the delay and response periods. Taken together, the results imply that covert cognitive strategies play an important role in modulating brain activation and behavior during memory tasks.     

Effect of target animacy on hand preference in Sichuan snub-nosed monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

Twenty-eight captive Sichuan snub-nosed monkeys (Rhinopithecus roxellana) were involved in the current study. Many individuals showed handedness, with a modest tendency toward left-hand use especially for animate targets, although no group-level handedness was found. There was no significant gender difference in the direction and strength of hand preference for both targets. Females showed a significantly higher overall rate of actions toward animate targets than inanimate targets for both hands, whereas males displayed almost the reversed pattern. There were no significant interactions between lateral hand use and target animacy for either males or females. Most individuals showed rightward or leftward laterality shift trends between inanimate and animate targets. These findings to some extent support the existence of a potential trend concerning a categorical neural distinction between targets demanding functional manipulation (inanimate objects) and those demanding social manipulation (animate objects), even though specialized hand preference based on target animacy has not been fully established in this arboreal Old World monkey species.     

Structural analysis of tool-use by tufted capuchins (Cebus apella) and chimpanzees (Pan troglodytes)

Using Matsuzawa’s hierarchical system of classification, I compared tool-use patterns of tufted capuchins (Cebus apella) to those of chimpanzees (Pan troglodytes). The results indicated that wild C. apella exhibit fewer and less complex tool-use patterns than do captive C. apella and wild and captive P. troglodytes. Although most patterns of tool-use observed among P. troglodytes occur in captive C. apella, there are some notable exceptions, including tool-use in communicative contexts and the use ¶of three-tool combinations. I conclude that C. apella are unique among monkeys in their demonstrated propensities for higher-order combinatorial behavior and are likely capable of using symbolic combinations, although not at the level of complexity that has been demonstrated in ¶P. troglodytes.