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.     

Uniquely primate,uniquely human

Two hypotheses about primate cognition are proposed. First, it is proposed that primates, but not other mammals, understand categories of relations among external entities. In the physical domain primates have special skills in tasks such as oddity, transitivity, and relation matching that require facility with relational categories; in the social domain primates have special skills in understanding the third-party social relationships that hold among other individuals in their groups. Second, it is proposed that humans, but not other primates, understand the causal and intentional relations that hold among external entities. In the physical domain only humans understand causal forces as mediating the connection between sequentially ordered events; in the social domain only humans understand the behavior of others as intentionally directed and controlled by desired outcomes. Both these uniquely primate and these uniquely human cognitive skills are hypothesized to have their origins in adaptations for negotiating complex social interactions.     

The role of propulsive muscles of the shoulder during quadrupedalism in vervet monkeys (Cercopithecus aethiops): implications for neural control of locomotion in primates

In comparative anatomical studies of the shoulder, the humeral retractors are often grouped together as propulsive muscles, which are important in the propulsive stroke of the forelimb during quadrupedal locomotion. Electromyographic (EMG) analyses of these muscles in opossums, cats, and dogs in general have confirmed such conclusions. An EMG study of chimpanzee shoulder muscles during knuckle-walking found, however, that the humeral retractors are either inactive or perform a function unrelated to propulsion (Larson & Stern, 1987). This contrast in muscle recruitment patterns between chimpanzees and more "typical" mammalian quadrupeds was attributed to the derived morphology of the chimpanzee shoulder. The present study examines the activity patterns of the humeral retractors in the vervet monkey, a primate more closely resembling nonprimate mammals in its shoulder morphology. The results of this EMG analysis show that despite the significant differences in anatomy between chimpanzees and vervets, the two species display very similar muscle recruitment patterns during quadrupedalism, and there is evidence for this same pattern in other species of primates. These differences in muscle activity patterns between primates and nonprimate mammals may be related to changes in the neurological control of locomotion in primates due to the evolutionary development of manipulative abilities in the primate forelimb.     

The Role of Propulsive Muscles of the Shoulder During Quadrupedalism in Vervet Monkeys (Cercopithecus aethiops)

In comparative anatomical studies of the shoulder, the humeral retractors are often grouped together as propulsive muscles, which are important in the propulsive stroke of the forelimb during quadrupedal locomotion. Electromyographic (EMG) analyses of these muscles in opossums, cats, and dogs in general have confirmed such conclusions. An EMG study of chimpanzee shoulder muscles during knuckle-walking found, however, that the humeral retractors are either inactive or perform a function unrelated to propulsion (Larson & Stern, 1987). This contrast in muscle recruitment patterns between chimpanzees and more “typical” mammalian quadrupeds was attributed to the derived morphology of the chimpanzee shoulder. The present study examines the activity patterns of the humeral retractors in the vervet monkey, a primate more closely resembling nonprimate mammals in its shoulder morphology. The results of this EMG analysis show that despite the significant differences in anatomy between chimpanzees and vervets, the two species display very similar muscle recruitment patterns during quadrupedalism, and there is evidence for this same pattern in other species of primates. These differences in muscle activity patterns between primates and nonprimate mammals may be related to changes in the neurological control of locomotion in primates due to the evolutionary development of manipulative abilities in the primate forelimb.     

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.     

Communicative and other cognitive characteristics of bottlenose dolphins

Scientists have tried to capture the rich cognitive life of dolphins through field and laboratory studies of their brain anatomy, social lives, communication and perceptual abilities. Encopheliration quotient data sugest a level of intelligence or cognitive processing in the large-brained dolphin that is closer to the human range than are our nearest primate relatives. Field studies indicate a fission-fusion type of social structure, showing social complexity rivaling that found in chimpanzee societies. Notably, cetaceans are the only mammals other than humans that clearly demonstrate vocal learning and parallels in stages of vocal learning have been reported for humans, birds and dolphins. The dolphin's vocal plasticity from infancy through adulthood, in what is probably an 'open' communication system, is likely to be related to their fission-fusion social structure and, specifically, to the fluidity of their short-term associations. However, conflicting evidence exists on the composition and organization of the dolphins whistle repertoire. In general, the level of dolphin performance on complex auditory learning and memory tasks has been compared with that of primates on similar visual tasks; however, dolphins have also demonstrated sophistrcated visual processing abilities. Laboratory studies have also provided suggestive, evidence of minor self-recognition in the dolphin, an ability previously thought to be exclusive to humans humans and apes.     

Evolution and the nonlegal equivalent of aggressive criminal behavior

Within the framework of modern evolutionary theory, arguments are reviewed that the nonlegal equivalent of aggressive criminal behavior may have evolved by natural selection among mammals, particularly primates, as part of their overall approach to reproduction. If so, the commission of aggressive crimes (or their nonlegal equivalent) by humans, and even efforts to prevent fellow social group members from being victimized by aggressive crimes, may also be partially explainable in natural selection terms. The plausibility of this deduction was explored, first, by specifying the three elements that a human act must have to be regarded as an aggressive crime. Summarily, these were that (1) injury to a victim must be a likely result of the act, (2) the act must be intended, and (3) the act must elicit negative responses from those witnessing it. The primate behavior literature was examined for evidence that some behavior of nonhumans met all three conditions. Affirmative results were obtained. Therefore, while further research is in order, human aggressive criminal behavior, as well as human efforts to control it, seem to have close parallels in other primates. This would be consistent with the notion that aggressive criminal behavior (along with its condemnation by fellow group members) is part of a social system produced and sustained by natural selection.     

Evolution of the brain and intelligence

Intelligence has evolved many times independently among vertebrates. Primates, elephants and cetaceans are assumed to be more intelligent than 'lower' mammals, the great apes and humans more than monkeys, and humans more than the great apes. Brain properties assumed to be relevant for intelligence are the (absolute or relative) size of the brain, cortex, prefrontal cortex and degree of encephalization. However, factors that correlate better with intelligence are the number of cortical neurons and conduction velocity, as the basis for information-processing capacity. Humans have more cortical neurons than other mammals, although only marginally more than whales and elephants. The outstanding intelligence of humans appears to result from a combination and enhancement of properties found in non-human primates, such as theory of mind, imitation and language, rather than from 'unique' properties.     

Not here,there! Possible referential gesturing during allogrooming by wild bonnet macaques, <Emphasis Type="Italic">Macaca radiata</Emphasis>

Intentional referential gestures, a fundamental building block of symbolic human language, have been reported from a range of species, including non-human primates. While apes are known to spontaneously use intentional gestures, only captive macaques, amongst non-ape primates, appear to intentionally display learnt gestures. On the other hand, referential gestures have so far been reported only in chimpanzees, amongst non-human primates. We document here, for the first time, potentially referential gesturing, used intentionally as well, in a monkey species, the bonnet macaque Macaca radiata, in the wild. Bonnet macaques use four distinct actions during allogrooming, possibly to indicate a particular body part intended to be groomed. These acts were successful in drawing the recipients’ attention to the indicated part, which they began to groom subsequently. This study enriches our understanding of non-ape primate gestural communication and adds to the growing evidence for early human language-like capacities in non-human species.     

Right hemisphere dominance for emotion processing in baboons

Asymmetries of emotional facial expressions in humans offer reliable indexes to infer brain lateralization and mostly revealed right hemisphere dominance. Studies concerned with oro-facial asymmetries in nonhuman primates largely showed a left-sided asymmetry in chimpanzees, marmosets and macaques. The presence of asymmetrical oro-facial productions was assessed in Olive baboons in order to determine the functional cerebral asymmetries. Two affiliative behaviors (lipsmack, copulation call) and two agonistic ones (screeching, eyebrow-raising) were recorded. For screeching, a strong and significant left hemimouth bias was found, but no significant bias was observed for the other behaviors. These results are discussed in the light of the available literature concerning asymmetrical oro-facial productions in nonhuman primates. In addition, these findings suggest that human hemispheric specialization for emotions has precursors in primate evolution.     

Do action systems resist visual illusions?

Arguments about the relative independence of visual modules in the primate brain are not new. Recently, though, these debates have resurfaced in the form of arguments about the extent to which visuomotor reaching and grasping systems are insensitive to visual illusions that dramatically bias visual perception. The first wave of studies of illusory effects on perception and action have supported the idea of independence of motor systems, but recent findings have been more critical. In this article, I review several of these studies, most of which (but not all) can be reconciled with the two-visual-systems model.     

Reciprocity of support in coatis (Nasua nasua)

Primate sociality has received much attention and its complexity has been viewed as a driving force for the evolution of cognitive abilities. Improved analytic techniques have allowed primate researchers to reveal intricate social networks based on the exchange of cooperative acts and services. Although nonprimates are known to show similar behavior (e.g., cooperative hunting, food sharing, coalitions) there seems a consensus that social life is less complex than in primates. Here the authors present the first group-level analysis of reciprocity of social interactions in a social carnivore, the ring-tailed coati (Nasua nasua). The authors found that support in aggressive conflicts is a common feature in coatis and that this behavior is reciprocally exchanged in a manner seemingly as complex as in primates. Given that reciprocity correlations persisted after controlling for the effect of spatial association and subunit membership, some level of scorekeeping may be involved. Further studies will be needed to confirm our findings and understand the mechanisms underlying such reciprocity, but our results contribute to the body of work that has begun to challenge primate supremacy in social complexity and cognition.     

Do domestic dogs (<Emphasis Type="Italic">Canis lupus familiaris</Emphasis>) perceive the Delboeuf illusion?

In the last decade, visual illusions have been repeatedly used as a tool to compare visual perception among species. Several studies have investigated whether non-human primates perceive visual illusions in a human-like fashion, but little attention has been paid to other mammals, and sensitivity to visual illusions has been never investigated in the dog. Here, we studied whether domestic dogs perceive the Delboeuf illusion. In human and non-human primates, this illusion creates a misperception of item size as a function of its surrounding context. To examine this effect in dogs, we adapted the spontaneous preference paradigm recently used with chimpanzees. Subjects were presented with two plates containing food. In control trials, two different amounts of food were presented in two identical plates. In this circumstance, dogs were expected to select the larger amount. In test trials, equal food portion sizes were presented in two plates differing in size: if dogs perceived the illusion as primates do, they were expected to select the amount of food presented in the smaller plate. Dogs significantly discriminated the two alternatives in control trials, whereas their performance did not differ from chance in test trials with the illusory pattern. The fact that dogs do not seem to be susceptible to the Delboeuf illusion suggests a potential discontinuity in the perceptual biases affecting size judgments between primates and dogs.     

The Effects of Prenatal Alcohol Exposure on Behavior: Rodent and Primate Studies

The use of alcohol by women during pregnancy is a continuing problem. In this review the behavioral effects of prenatal alcohol from animal models are described and related to studies of children and adults with FASD. Studies with monkeys and rodents show that prenatal alcohol exposure adversely affects neonatal orienting, attention and motor maturity, as well as activity level, executive function, response inhibition, and sensory processing later in life. The primate moderate dose behavioral findings fill an important gap between human correlational data and rodent mechanistic research. These animal findings are directly translatable to human findings. Moreover, primate studies that manipulated prenatal alcohol exposure and prenatal stress independently show that prenatal stress exacerbates prenatal alcohol-induced behavioral impairments, underscoring the need to consider stress-induced effects in fetal alcohol research. Studies in rodents and primates show long-term effects of prenatal and developmental alcohol exposure on dopamine system functioning, which could underpin the behavioral effects.     

Mouse vocal communication system: Are ultrasounds learned or innate?

Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.     

Developmental structure in brain evolution

How does evolution grow bigger brains? It has been widely assumed that growth of individual structures and functional systems in response to niche-specific cognitive challenges is the most plausible mechanism for brain expansion in mammals. Comparison of multiple regressions on allometric data for 131 mammalian species, however, suggests that for 9 of 11 brain structures taxonomic and body size factors are less important than covariance of these major structures with each other. Which structure grows biggest is largely predicted by a conserved order of neurogenesis that can be derived from the basic axial structure of the developing brain. This conserved order of neurogenesis predicts the relative scaling not only of gross brain regions like the isocortex or mesencephalon, but also the level of detail of individual thalamic nuclei. Special selection of particular areas for specific functions does occur, but it is a minor factor compared to the large-scale covariance of the whole brain. The idea that enlarged isocortex could be a "spandrel," a by-product of structural constraints later adapted for various behaviors, contrasts with approaches to selection of particular brain regions for cognitively advanced uses, as is commonly assumed in the case of hominid brain evolution.     

New Developments in Understanding Emotional Facial Signals in Chimpanzees

ABSTRACT— There has been little research over the past few decades focusing on similarities and differences in the form and function of emotional signals in nonhuman primates, or whether these communication systems are homologous with those of humans. This is, in part, due to the fact that detailed and objective measurement tools to answer such questions have not been systematically developed for nonhuman primate research. Despite this, emotion research in humans has benefited for over 30 years from an objective, anatomically based facial-measurement tool: the Facial Action Coding System (FACS). In collaboration with other researchers, we have now developed a similar system for chimpanzees (ChimpFACS) and, in the process, have made exciting new discoveries regarding chimpanzees' perception and categorization of emotional facial expressions and similarities in the facial anatomy of chimpanzees and humans, and we have identified homologous facial movements in the two species. Investigating similarities and differences in primate emotional communication systems is essential if we are to understand unique evolutionary specializations among different species.     

A socioecological perspective on primate cognition,past and present

The papers in this special issue examine the relationship between social and ecological cognition in primates. We refer to the intersection of these two domains as socioecological cognition. Examples of socioecological cognition include socially learned predator alarm calls and socially sensitive foraging decisions. In this review we consider how primate cognition may have been shaped by the interaction of social and ecological influences in their evolutionary history. The ability to remember distant, out-of-sight locations is an ancient one, shared by many mammals and widespread among primates. It seems some monkeys and apes have evolved the ability to form more complex representations of resources, integrating “what-where-how much” information. This ability allowed anthropoids to live in larger, more cohesive groups by minimizing competition for limited resources between group members. As group size increased, however, competition for resources also increased, selecting for enhanced social skills. Enhanced social skills in turn made a more sophisticated relationship to the environment possible. The interaction of social and ecological influences created a spiraling effect in the evolution of primate intelligence. In contrast, lemurs may not have evolved the ability to form complex representations which would allow them to consider the size and location of resources. This lack in lemur ecological cognition may restrict the size of frugivorous lemur social groups, thereby limiting the complexity of lemur social life. In this special issue, we have brought together two review papers, five field studies, and one laboratory study to investigate the interaction of social and ecological factors in relation to foraging. Our goal is to stimulate research that considers social and ecological factors acting together on cognitive evolution, rather than in isolation. Cross fertilization of experimental and observational studies from captivity and the field is important for increasing our understanding of this relationship. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition”.     

Language lateralization to the dominant hemisphere: Tool use, gesture and language in hominid evolution

Shared tool use in our hominid ancestry is perhaps the most satisfactory explanation for human dextrality and left-hemisphere language lateralization. Recent palaeoarchaeological evidence suggests that brachiation preceded bipedalism, which in turn preceded advanced tool use, with all three preceding any dramatic increase in brain size and/or the development of speech-related neural structures. Shared tool use probably led to population dextrality, and then to the development of left-hemisphere centres for fine motor coordination and the mediation of serial, segmental, time-dependent and syntactic processes at sensory and more particularly motor levels, including the control of limbs, fingers and articulators. Such centres, initially developed for tool construction and use, would have occupied an intermediate position in the evolutionary sequence. Thus cortically-driven facial gestures may possibly have accompanied manual signing, modulating limbic vocalizations of affect, though a cortical-limbic distinction with respect to communication may be unwarranted. However, the uniqueness of human language is still a matter of debate both with respect to other primates and our own evolutionary ancestors.