Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes)

In a recent article MacNeilage, Studdert-Kennedy, and Lindblom (1987) proposed that nonhuman primate handedness may be contingent on the specific task requirements with visual-spatial tasks yielding left-hand preferences and fine motor tasks producing right-hand preferences. This study reports hand preferences in the manipulation of joysticks by 2 rhesus monkeys (Macaca mulatta) and 3 chimpanzees (Pan troglodytes). Reach data were also collected on these same subjects and served as a basis for comparison with preference data for manipulation of the joystick. The data indicated that all 5 subjects demonstrated significant right-hand preferences in manipulating the joystick. In contrast, no significant hand preferences were found for the reach data. Reaction time data also indicated that the right hand could perform a perceptual-motor task better than the left hand in all 5 subjects. Overall, the data indicate that reach tasks may not be sensitive enough measures to produce reliable hand preferences, whereas tasks that assess fine motor control produce significant hand preferences.     

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.     

Monkeys perform as well as apes and humans in a size discrimination task

Whether the cognitive competences of monkeys and apes are rather similar or whether the larger-brained apes outperform monkeys in cognitive experiments is a highly debated topic. Direct comparative analyses are therefore essential to examine similarities and differences among species. We here compared six primate species, including humans, chimpanzees, bonobos, gorillas (great apes), olive baboons, and long-tailed macaques (Old World monkeys) in a task on fine-grained size discrimination. Except for gorillas, subjects of all taxa (i.e. humans, apes, and monkeys) were able to discriminate three-dimensional cubes with a volume difference of only 10 % (i.e. cubes of 50 and 48 mm side length) and performed only slightly worse when the cubes were presented successively. The minimal size discriminated declined further with increasing time delay between presentations of the cubes, highlighting the difficulty to memorize exact size differences. The results suggest that differences in brain size, as a proxy for general cognitive abilities, did not account for variation in performance, but that differential socio-ecological pressures may better explain species differences. Our study highlights the fact that differences in cognitive abilities do not always map neatly onto phylogenetic relationships and that in a number of cognitive experiments monkeys do not fare significantly worse than apes, casting doubt on the assumption that larger brains per se confer an advantage in such kinds of tests.     

Comparative and familial analysis of handedness in great apes

Historically, population-level handedness has been considered a hallmark of human evolution. Whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. This paper summarizes published data on handedness in great apes. Comparative analysis indicated that chimpanzees and bonobos show population-level right handedness, whereas gorillas and orangutans do not. All ape species showed evidence of population-level handedness when considering specific tasks. Familial analyses in chimpanzees indicated that offspring and maternal (but not paternal) handedness was significantly positively correlated, but this finding was contingent upon the classification criteria used to evaluate hand preference. Overall, the proportion of right handedness is lower in great apes compared with humans, and various methodological and theoretical explanations for this discrepancy are discussed.     

A comparative review of the primate motor system

Primates have evolved separately from other mammals since the late Cretaceous, and during this time the two major extant primate groups, prosimians (lorises, lemurs, and tarsiers) and anthropoids (monkeys, apes, and humans) arose. Concurrently, structures within the central nervous system acquired primate characteristics. Not all of the uniquely primate features have been identified in the brain, but several are well known. The pyramidal system, the best studied motor system, shows a distinct primate pattern in its terminal connections in the spinal cord. Other descending systems are less well known, but primate specializations in the vestibular system and red nucleus have been observed. The primary and secondary motor cortices are topographically separated in primates, suggesting one basis for increased complexity. Given the size of the brain, structures in the basal ganglia are relatively enlarged in primates as compared with other mammals, whereas the cerebellum has the same relative size.     

The Role of Similarity Analysis in Understanding Movement

Primates have evolved separately from other mammals since the late Cretaceous, and during this time the two major extant primate groups, prosimians (lorises, lemurs, and tarsiers) and anthropoids (monkeys, apes, and humans) arose. Concurrently, structures within the central nervous system acquired primate characteristics. Not all of the uniquely primate features have been identified in the brain, but several are well known. The pyramidal system, the best studied motor system, shows a distinct primate pattern in its terminal connections in the spinal cord. Other descending systems are less well known, but primate specializations in the vestibular system and red nucleus have been observed. The primary and secondary motor cortices are topographically separated in primates, suggesting one basis for increased complexity. Given the size of the brain, structures in the basal ganglia are relatively enlarged in primates as compared with other mammals, whereas the cerebellum has the same relative size.     

Androgens and aggressive behavior in primates: A review

This review deals with possible central and peripheral effects of androgens upon primate aggressive behavior. One problem that clouds interpretation of experimental work is that measurements of dominance have often been employed, such as competition tests for food and water. Such measures often do not correlate with those obtained by quantifying aggressive interactions. It should be remembered that very few of the 188 primate species have been studied experimentally and that great behavioral and physiological diversity occurs within the order. Therefore, generalizations about the effects of androgens upon aggressive behavior in primates (including man) should be made with caution. Testosterone has an organizing influence upon the foetal brain of rhesus monkeys and may affect the development of neural mechanisms which govern aggression in males. More data are required on primates, however, since rhesus monkeys show some important differences from rodents as regards the effects of androgen upon sexual differentiation of the hypothalamus. In future, marmosets may provide a suitable model for such studies, because there is evidence that sexual differentiation of brain by androgen occurs postnatally in these monkeys. At puberty, male primates show a variety of behavioral changes and, during adulthood, males of seasonally breeding species may be more aggressive during the mating season, when testosterone levels are maximal. This does not indicate a causative relationship between testosterone and aggressive responses, because castration and androgen treatments have little effect upon aggression in prepubertal or adult males of several primate species. Androgens have pronounced effects on sexual responses in adult male monkeys, but their central effects upon aggression are much less important than among rodents. Elec trical stimulation of hypothalamic pathways has been employed to evoke aggressive behavior in marmosets and rhesus monkeys. In the rhesus, preliminary evidence indicates that such pathways show some sensitivity to androgens. In rodents it is known that these areas are richly supplied with monoaminergic neurons, which play an important role in aggressive behavior. There is little evidence on primates, however, and this remains a crucial topic for future research. Peripheral effects of androgens should also be considered. Many prosimians and New World monkeys use scent-marking behaviors and, in males, androgen-dependent chemical cues may be involved in sexual recognition and territorial behavior. This possibility awaits investigation. Finally, plasma testosterone levels may alter as a function of aggression itself; thus levels decrease if male rhesus monkeys are defeated by conspecifics. This might occur because neural events associated with giving (or receiving) aggression also influence pituitary function and hence alter gonadal testosterone secretion. Theoretically, it is possible that such changes in circulating testosterone might affect aggressive behavior via a feedback action on the brain, but the experimental evidence does not support such a view.     

Experimental field study of hand preference in wild black-horned (<Emphasis Type="Italic">Cebus nigritus</Emphasis>) and white-faced (<Emphasis Type="Italic">Cebus capucinus</Emphasis>) capuchins: evidence for individual and species differences

In this experimental field investigation, we compare the degree to which wild capuchins in Brazil (Cebus nigritus) and Costa Rica (Cebus capucinus) exhibit individual- and population-level handedness during three visually-guided tasks. These tasks required reaching to remove a large leaf covering a hidden food reward, seizing the food reward, and manipulating a tool (pulling a wooden dowel) in order to obtain access to an embedded food reward. Studies in some populations of captive capuchins indicate evidence for both individual hand preferences and population-level handedness. In this study, six of eight wild C. capucinus and six of seven wild C. nigritus exhibited a significant hand preference during individual tasks, but no individual exhibited a consistent preference across all three tasks. Task-specialization, or the tendency for most individuals in the same group or population to use the same hand to accomplish a particular task, also was evaluated. Cebus nigritus showed a significant bias toward the use of the right hand in removing the leaf. Although the number of individual capuchins in both species that manipulated the dowels was limited (N = 7), each individual that manipulated the dowels in eight or more instances had a positive handedness index, suggesting a greater use of the right hand to accomplish this task. Overall, our results provide preliminary support for individual- and population-level handedness in wild capuchin monkeys.     

Gambling primates: reactions to a modified Iowa Gambling Task in humans,chimpanzees and capuchin monkeys

Humans will, at times, act against their own economic self-interest, for example, in gambling situations. To explore the evolutionary roots of this behavior, we modified a traditional human gambling task, the Iowa Gambling Task (IGT), for use with chimpanzees, capuchin monkeys and humans. We expanded the traditional task to include two additional payoff structures to fully elucidate the ways in which these primate species respond to differing reward distributions versus overall quantities of rewards, a component often missing in the existing literature. We found that while all three species respond as typical humans do in the standard IGT payoff structure, species and individual differences emerge in our new payoff structures. Specifically, when variance avoidance and reward maximization conflicted, roughly equivalent numbers of apes maximized their rewards and avoided variance, indicating that the traditional payoff structure of the IGT is insufficient to disentangle these competing strategies. Capuchin monkeys showed little consistency in their choices. To determine whether this was a true species difference or an effect of task presentation, we replicated the experiment but increased the intertrial interval. In this case, several capuchin monkeys followed a reward maximization strategy, while chimpanzees retained the same strategy they had used previously. This suggests that individual differences in strategies for interacting with variance and reward maximization are present in apes, but not in capuchin monkeys. The primate gambling task presented here is a useful methodology for disentangling strategies of variance avoidance and reward maximization.     

Paw preference is not affected by postural demand in a nonprimate mammal (Felis silvestris catus)

Previously, it has been thought that handedness is unique to humans. Recently, it has been found that hand or paw preferences are common among a variety of vertebrate species. Different models have been put forth to describe the evolution of primate handedness. In this study we aimed to explore whether these models can also be used to predict manual laterality in nonprimate mammalian groups. The cat (Felis silvestris catus) is a good nonprimate model for manual laterality, as cats frequently use paws to catch and hold prey. Cats were exposed to two standardized manual laterality tasks, differing in postural demand. Subjects (N = 28) were forced to use either a stable or unstable body posture (i.e., sitting or standing vs. vertical clinging) to extract food items from a plastic box attached at two different heights. We revealed that cats exhibited paw preferences at an individual level with about 40% left, 30% right, 30% nonlateralized subjects. Postural demand was linked to task difficulty: the unstable body posture was found to be significantly more difficult than the stable body posture. However, these differences in postural demand and task difficulty did not lead to differences in direction or strength of paw preference. Findings suggested that nonprimate mammals differ from primates in their sensitivity to task related factors, such as postural demand. Results coincide with those of some prosimians, providing support for the hypothesis that postural demand and the associated task complexity became influencing factors on manual laterality in the course of primate evolution.     

Chimpanzee handedness revisited: 55 years since Finch (1941)

Chimpanzees and other great apes have long held the fascination of psychologists because of their morphological and behavioral similarities to humans. This paper describes the historical interest in studies on chimpanzee handedness and reviews current findings. Data are presented which suggest that transient changes in posture result in the transient expression of right-handedness in chimpanzees. The role of tool use as an evolutionary mechanism underlying the expression of right-handedness is challenged. Rather, emphasis is placed on the role of bimanual feeding as a behavioral adaptation for the expression of handedness. Suggestions for further research on the nature of nonhuman primate handedness are made in light of these findings.     

Capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) use conspecifics’ emotional expressions to evaluate emotional valence of objects

Emotional expressions provide important clues to other individuals’ emotional states, as well as the environmental situations leading to such states. Although monkeys often modify their behavior in response to others’ expressions, it is unclear whether this reflects understanding of emotional meanings of expressions, or simpler, non-cognitive processes. The present study investigated whether a New World monkey species, tufted capuchin monkeys, recognize objects as elicitors of others’ expressions. Observer monkeys witnessed another individual (demonstrator) reacting either positively or negatively to the contents of one of two containers and were then allowed to choose one of the containers. The observer preferred the container that evoked positive expressions in the demonstrator and avoided the container that evoked negative expressions. Thus, the monkeys appropriately associated the emotional valence of others’ expressions with the container. This finding supports the view that the ability to represent others’ emotions is not limited to humans and apes.     

On the evolution of handedness: a speculative analysis of Darwin's views and a review of early studies of handedness in "the nearest allies of man"

Scientists today who seek clues into the evolutionary origins of human handedness make extensive use of evidence from comparative studies, that is, studies that ask whether handedness occurs in other species, especially apes and monkeys, as the Darwinian principle of continuity would seem to imply, or whether it is uniquely human. Early investigations had the same goal and drew on much the same kind of evidence. In this article, I review studies of animal handedness in the period before 1859, when Darwin published On the Origin of Species, and afterward, through the 1st decade of the 20th century. Inasmuch as Darwin's published writings contain hardly any statements about handedness and none at all about its evolution and continuity across species, I also speculate about what Darwin himself might have said on the subject. To do this, I draw on his statements on related matters, such as the form and structure of the hand and the transition from a quadrupedal to bipedal stance, on other writers' reports and opinions about handedness with which he was familiar or likely to have been familiar, and finally, on clues from his own and only statement about animal handedness in an unpublished letter. I conclude by asking whether and how early investigators, lacking any statement by Darwin on the evolution of handedness, invoked his theory of evolution and his views on related matters in the interpretation of their findings.     

Can squirrel monkeys (Saimiri sciureus) learn self-control? A study using food array selection tests and reverse-reward contingency

Eight squirrel monkeys (Saimiri sciureus) were presented with 2 stimulus arrays, namely 1 and 4 pieces of food, but they received only the array other than the one they reached for. In this reverse-reward condition, all monkeys initially showed a strong preference for the larger array. One monkey learned to reach toward the smaller array when a large-or-none reward contingency was applied (i.e., no reward followed a reach toward the larger array, but this array was given for a reach toward the smaller array). When correction trials and time-out were added to the large-or-none procedure, all remaining monkeys except 1 learned this form of self-control. Performance was maintained when correction trials were discontinued, the original reverse-reward condition was rerun, and novel array-size pairs were presented. This study demonstrates one form of self-control in a New World primate and shows the reverse-reward procedure to be a potentially valuable method for assessing species and individual differences in self-control and numerosity-related abilities.     

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.     

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.     

Can rhesus monkeys spontaneously subtract?

Animals, including pigeons, parrots, raccoons, ferrets, rats, New and Old World monkeys, and apes are capable of numerical computations. Much of the evidence for such capacities is based on the use of techniques that require training. Recently, however, several studies conducted under both laboratory and field conditions have employed methods that tap spontaneous numerical representations in animals, including human infants. In this paper, we present the results of 11 experiments exploring the capacity of semi-free-ranging adult rhesus monkeys to spontaneously compute (i.e. single trial, no training) the outcome of subtraction events. In the basic design, we present one quantity of objects on one stage, a second quantity on a second stage, occlude both stages, and then remove one or no objects from each stage. Having watched these events, a subject is then allowed to approach one stage and eat the food objects behind the occluder. Results show that rhesus monkeys correctly compute the outcome of subtraction events involving three or less objects on each stage, even when the identity of the objects is different. Specifically, when presented with two food quantities, rhesus monkeys select the larger quantity following subtractions of one piece of food from two or three; this preference is maintained when subjects must distinguish food from non-food subtractions, and when food is subtracted from either one or both initial quantities. Furthermore, rhesus monkeys are capable of representing zero as well as equality when two identical quantities are contrasted. Results are discussed in light of recent attempts to determine how number is represented in the brains of animals lacking language.     

Primate Numerical Competence: Contributions Toward Understanding Nonhuman Cognition

Nonhuman primates represent the most significant extant species for comparative studies of cognition, including such complex phenomena as numerical competence, among others. Studies of numerical skills in monkeys and apes have a long, though somewhat sparse history, although questions for current empirical studies remain of great interest to several fields, including comparative, developmental, and cognitive psychology; anthropology; ethology; and philosophy, to name a few. In addition to demonstrated similarities in complex information processing, empirical studies of a variety of potential cognitive limitations or constraints have provided insights into similarities and differences across the primate order, and continue to offer theoretical and pragmatic directions for future research. An historical overview of primate numerical studies is presented, as well as a summary of the 17‐year research history, including recent findings, of the Comparative Cognition Project at The Ohio State University Chimpanzee Center. Overall, the archival literature on number‐related skills and counting in nonhuman primates offers important implications for revising our thinking about comparative neuroanatomy, cross‐species (human/ape) cognitive similarities and differences, and the evolution of cognition represented by the primate continuum.     

Metacognitive-like information seeking in lion-tailed macaques: a generalized search response after all?

Previous research has demonstrated that Old World primates (both apes and monkeys) seek information about the location of a hidden food item, unless they are privy to the hiding process. This has been cited as evidence of metacognition. However, these results could also be interpreted using non-metacognitive accounts, including a generalized search response to uncertainty, in which subjects reach for food when it is seen, or search for food until it is spotted. In the present research, lion-tailed macaques were tested on an object-choice task. Conditions varied with respect to the visibility of the baiting process, and whether the location of the hidden food could be inferred by logical exclusion. Additionally, the hidden food could be located visually before a choice was made, by peering under the objects through a Plexiglas tray. Across conditions, monkeys consistently looked for the food when it had not been seen, even if its location could be inferred, despite the fact that these monkeys are capable of inference by exclusion. This suggests that apparently ‘metacognitive’ information seeking in monkeys may instead reflect a generalized search strategy. Alternatively, it is possible that monkeys only have metacognitive access to certain types of knowledge, including that obtained visually. Results are discussed with respect to the likelihood of metacognition in this species and the evolutionary emergence of metacognition across species.     

A comparative analysis of serial ordering in ring-tailed lemurs (Lemur catta)

Research over the last 25 years has demonstrated that animals are able to organize sequences in memory and retrieve ordered sequences without language. Qualitative differences have been found between the serial organization of behavior in pigeons and monkeys. Here the authors test serial ordering abilities in ring-tailed lemurs, a strepsirrhine primate whose ancestral lineage diverged from that of monkeys, apes, and humans approximately 63 million years ago. Lemurs' accuracy and response times were similar to monkeys, thus suggesting that they may share mechanisms for serial organization that dates to a common primate ancestor.