Right hemisphere dominance for the production of facial expression in monkeys.

In humans, the left side of the face (right hemisphere of the brain) is dominant in emotional expression. In rhesus monkeys, the left side of the face begins to display facial expression earlier than the right side and is more expressive. Humans perceive rhesus chimeras created by pairing the left half of the face with its mirror-reversed duplicate as more expressive than chimeras created by right-right pairings. That the right hemisphere determines facial expression, and the left hemisphere processes species-typical vocal signals, suggests that human and nonhuman primates exhibit the same pattern of brain asymmetry for communication.

Language discrimination by human newborns and by cotton-top tamarin monkeys.

Humans, but no other animal, make meaningful use of spoken language. What is unclear, however, is whether this capacity depends on a unique constellation of perceptual and neurobiological mechanisms or whether a subset of such mechanisms is shared with other organisms. To explore this problem, parallel experiments were conducted on human newborns and cotton-top tamarin monkeys to assess their ability to discriminate unfamiliar languages. A habituation-dishabituation procedure was used to show that human newborns and tamarins can discriminate sentences from Dutch and Japanese but not if the sentences are played backward. Moreover, the cues for discrimination are not present in backward speech. This suggests that the human newborns' tuning to certain properties of speech relies on general processes of the primate auditory system.

Amodal completion of acoustic signals by a nonhuman primate.

Evidence of amodal completion exists for both visual and auditory stimuli in humans. The importance of this mechanism in forming stable representations of sensory information suggests that it may be common among multiple modalities and species. Here we show that a species of nonhuman primate amodally completes biologically meaningful acoustic stimuli, which provides evidence that the neural mechanism mediating this aspect of auditory perception is shared among primates, and perhaps other taxonomic groups as well.

Perseveration, inhibition and the prefrontal cortex: a new look.

Perseverative actions are often the result of inhibitory problems; however, inhibitory problems do not always lead to perseverative actions. Some problems of inhibition have been attributed to immaturity of, or severe damage to, the prefrontal cortex. Research in this area has generally failed both to take into account species differences in prefrontal function that lead to different perseverative errors and to distinguish between perseverative errors that arise from a failure to inhibit salient emotions or motivational drives and errors that arise from an inability to engage in conceptual change. Recent studies on humans, chimpanzees, rhesus macaques, Japanese macaques, cotton-top tamarins and marmosets support this notion.

The auditory behaviour of primates: a neuroethological perspective.

The ethological approach has already provided rich insights into the auditory neurobiology of a number of different taxa (e.g. birds, frogs and insects). Understanding the ethology of primates is likely to yield similar insights into the specializations of this taxa's auditory system for processing species-specific vocalisations. Here, we review the recent advances made in our understanding of primate vocal perception and its neural basis.

Rhesus monkey copulation calls: honest signals for female choice?

In a wide variety of mating systems, female choice is based on the assessment of male signals, both morphological and behavioural, presumed to correlate with fitness. A crucial problem, therefore, is for females to determine whether the signal represents an 'honest' reflection of male fitness. A dominant theoretical perspective in evolutionary biology suggests that signals are honest if and only if they are costly to produce. At present, there are relatively few empirical studies of the costs and benefits of signalling in the mating context, and this is especially the case for Primates. In this paper, I examine the possibility that copulations calls--vocalizations that often elicit aggressive competition within the mating arena--are honest signals of male quality. Observations of rhesus monkey (Macaca mulatta) mating behaviour reveal that the proportion of copulating males who call decreases as competition for oestrous females increases. Males who call during copulation are more likely to be aggressively attacked than males who are silent during copulation. However, males who give copulation calls obtain more matings than males who do not, and this is true for high- and low-ranking males. Because of the cost-benefit tradeoffs, copulation calls are interpreted as honest indicators of quality that may serve an important function in female mate choice.

Spontaneous number representation in semi-free-ranging rhesus monkeys.

Previous research has shown that animals possess considerable numerical abilities. However, this work was based on experiments involving extensive training, a small number of captive subjects and relatively artificial testing procedures. We present the results of experiments on over 200 semi-free-ranging rhesus monkeys using a task which involves no training and mimics a natural foraging problem. The subjects observed two experimenters place pieces of apple, one at a time, into each of two opaque containers. The experimenters then walked away so that the subjects could approach. The monkeys chose the container with the greater number of apple slices when the comparisons were one versus two, two versus three, three versus four and three versus five slices. They failed at four versus five, four versus six, four versus eight and three versus eight slices. Controls established that it was the representation of number which underlay their successful choices rather than the amount of time spent placing apple pieces into the box or the volume of apple placed in the box. The failures at values greater than three slices stand in striking contrast to other animal studies where training was involved and in which far superior numerical abilities were demonstrated. The range of success achieved by rhesus monkeys in this spontaneous-number task matches the range achieved by human infants and corresponds to the range encoded in the syntax of natural languages.

Artifactual kinds and functional design features: what a primate understands without language.

Of several domains of knowledge, humans appear to be born with an innately structured representational system for making sense of objects, what properties individuate them, how they move in space, and what causes them to move from one location to another. They also appear to make simple conceptual cuts between artifactual kinds and living kinds. The basis for this distinction seems to be a combination of crucial functional properties, together with a teleological (i.e., historical/intentional) stance, one that asks 'What was this object designed for?'. Although non-human primates also appear to have considerable understanding of objects, and often use objects as tools, it is not clear whether they draw a distinction between artifactual and living kinds, and if so, what factors guide this distinction. As a step in addressing this problem, I present experiments on a small New World monkey, the cotton-top tamarin (Saguinus oedipus oedipus), designed to reveal their understanding of the functional properties of tools using a procedure associated with minimal training. Specifically, the experiments explored whether tamarins distinguish between relevant and irrelevant properties of a tool, and further, understand that some features can be transformed with little cost to functionality. The first experiment was a means-end task and involved using a cane-like object (a tool) to access a piece of food. In this experiment, there were always two choices: either the food was immediately accessible because it was located on the inside of the cane's hook or less readily accessible because it was located on the outside of the hook. Most of the tamarins reached criterion on this task within a few sessions, consistently picking the cane with the most accessible food. Subsequent experiments (2-4) involved property changes (i.e., its color, texture, size and shape) that had either significant or relatively insignificant effects on the tool's function. In general, the tamarins appeared tolerant of all property transformations as evidenced by the fact that they selected each object at least once. However, clear preferences also emerged suggesting that some properties had a more significant impact on the tool's functionality. Thus, in head-to-head competitions, tools with color or texture changes were selectively preferred over tools with shape or size changes. This makes sense color and texture do not effect the tool's function, whereas shape and size do. The final experiments involved both novel and familiar objects that, based on their current configuration, could readily be used as tools, in contrast with objects that required considerable manipulation to convert into a tool. Consistently, the tamarins preferred possible over convertible tools, and when two convertible tools were presented at the same time, they preferred the tool that required the fewest changes to the required motor response. Results suggest that the tamarins distinguish between relevant and irrelevant properties of a tool and this distinction is based on functionality, on having good design. This ability is especially surprising given the fact that tamarins do not naturally use tools, and infrequently come into contact with artifacts. Results are discussed in light of current theories concerning the representational foundations of natural kinds, and in particular, artifactual kinds.

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.

Segmentation of the speech stream in a non-human primate: statistical learning in cotton-top tamarins.

Previous work has shown that human adults, children, and infants can rapidly compute sequential statistics from a stream of speech and then use these statistics to determine which syllable sequences form potential words. In the present paper we ask whether this ability reflects a mechanism unique to humans, or might be used by other species as well, to acquire serially organized patterns. In a series of four experimental conditions, we exposed a New World monkey, the cotton-top tamarin (Saguinus oedipus), to the same speech streams used by Saffran, Aslin, and Newport (Science 274 (1996) 1926) with human infants, and then tested their learning using similar methods to those used with infants. Like humans, tamarins showed clear evidence of discriminating between sequences of syllables that differed only in the frequency or probability with which they occurred in the input streams. These results suggest that both humans and non-human primates possess mechanisms capable of computing these particular aspects of serial order. Future work must now show where humans' (adults and infants) and non-human primates' abilities in these tasks diverge.

Recognition and categorization of biologically significant objects by rhesus monkeys (Macaca mulatta): the domain of food.

To survive, organisms must be able to identify edible objects. However, we know relatively little about how humans and other species distinguish food items from non-food items. We tested the abilities of semi-free-ranging rhesus monkeys (Macaca mulatta) to learn rapidly that a novel object was edible, and to generalize their learning to other objects, in a spontaneous choice task. Adult monkeys watched as a human experimenter first pretended to eat one of two novel objects and then placed replicas of the objects at widely separated locations. Monkeys selectively approached the object that the experimenter had previously eaten, exhibiting a rapidly induced preference for the apparently edible object. In further experiments in which the same objects were used as tools or were manipulated at the face but not eaten, we fail to observe an approach bias, providing evidence that the monkeys' pattern of approach in the earlier experiments was specific to objects that were eaten. Subsequent experiments tested how monkeys generalized their preference for an edible object by first allowing them to watch a human experimenter eat one of two objects and then presenting them with new objects composed of the same substance but differing from the original, edible object in shape or color. Monkeys ignored changes in the shape of the object and generalized from one edible object to another on the basis of color in conjunction with other substance properties. Finally, we extended this work to infant rhesus monkeys and found that, like adults, they too used color to generalize to novel food objects. In contrast to adults, however, infants extended this pattern of generalization to objects that were acted on in other ways. These results suggest that infant monkeys form broader object categories than adults, and that food categories become sharpened as a function of maturational or experiential factors.

What guides a search for food that has disappeared? Experiments on cotton-top tamarins (Saguinus oedipus).

When food is launched down a vertically positioned S-shaped opaque tube, cotton-top tamarins (Saguinus oedipus) search for the food in the position directly beneath the release point, even though over several trials it never appears in this position (B. M. Hood et al., 1999). Experiment 1 showed that when the trajectory of the food shifts from the vertical to the horizontal plane, tamarins no longer show systematic perseverative errors and, in general, perform better on this invisible displacement task. Experiment 2 showed that tamarins with experience on the horizontal task show less of a bias when tested on the vertical task but nonetheless fail overall to solve this invisible displacement problem; their performance is substantially worse than it was on the horizontal task. Experiment 3 revealed that when the vertically positioned tube is replaced by an occluded ramp, tamarins consistently search in the compartment below the release point, even though most of the tamarins had experience in Experiments 1 and 2. Overall, results indicate that tamarins have a significant gravity bias when searching for food that has disappeared along the vertical plane but also have more general problems finding food that has moved out of sight.

The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments.

The authors' goal was to provide a better understanding of the relationship between vocal production and perception in nonhuman primate communication. To this end, the authors examined the cotton-top tamarin's (Saguinus oedipus) combination long call (CLC). In Part 1 of this study, the authors carried out a series of acoustic analyses designed to determine the kind of information potentially encoded in the tamarin's CLC. Using factorial analyses of variance and multiple discriminant analyses, the authors explored whether the CLC encodes 3 types of identity information: individual, sex, and social group. Results revealed that exemplars could be reliably assigned to these 3 functional classes on the basis of a suite of spectrotemporal features. In Part 2 of this study, the authors used a series of habituation-dishabituation playback experiments to test whether tamarins attend to the encoded information about individual identity. The authors 1st tested for individual discrimination when tamarins were habituated to a series of calls from 1 tamarin and then played back a test call from a novel tamarin; both opposite- and same-sex pairings were tested. Results showed that tamarins dishabituated when caller identity changed but transferred habituation when caller identity was held constant and a new exemplar was played (control condition). Follow-up playback experiments revealed an asymmetry between the authors' acoustic analyses of individual identity and the tamarins' capacity to discriminate among vocal signatures; whereas all colony members have distinctive vocal signatures, we found that not all tamarins were equally discriminable based on the habituation-dishabituation paradigm.

The role of lip configuration in monkey vocalizations: experiments using xylocaine as a nerve block.

Human and nonhuman primates commonly alter the configuration of their lips during vocal production and thereby modify vocal tract length and shape. In nonhuman primates, however, the effects of lip configuration on call structure are unknown. This study was designed to investigate the importance of lip configuration in rhesus monkey (Macaca mulatta) vocal production by temporarily blocking lip movement with injections of xylocaine. For "coo" vocalizations, an affiliative contact call that is normally produced with protruded lips, the xylocaine treatment had no statistically significant effect on call duration or characteristics of the fundamental frequency (i.e., features associated with respiration and laryngeal function). However, the two formant frequencies (i.e., features resulting from the filtering properties of the supralaryngeal cavity) of the call were significantly effected. Specifically, formant frequencies increased, as would be expected from an individual incapable of compensating for a shortened vocal tract. In contrast to coos, xylocaine had no statistically significant effect on the acoustic structure of "noisy screams," a call given in response to being attacked by a dominant and produced with retracted lips (i.e., a shortened vocal tract). Results suggest that for some vocalizations, lip configuration may be essential for achieving the intended acoustic target, whereas for other vocalizations, it is less important.

The evolution of nonhuman primate vocalizations: effects of phylogeny, body weight, and social context.

E. S. Morton proposed that, in birds and mammals, individuals tend to produce low-frequency atonal vocalizations in highly aggressive situations, whereas they typically produce high-frequency tonal vocalizations during nonaggressive or fearful situations. This hypothesis, referred to as the "motivation-structural (MS) rules," is based on two assumptions: the frequency of a vocalization is negatively correlated with body weight, and large animals are dominant over smaller animals, and thus aggressive vocalizations tend to have a lower pitch than fearful vocalizations. The relationship between body weight and frequency is examined using data on 36 nonhuman primate species representing 23 genera and 474 vocalizations. Results show that there is a statistically significant negative correlation between body weight and frequency: larger species produce relatively lower-pitched vocalizations than smaller species. A test of Morton's MS rules provided overall support for the predicted relationship between motivational state and frequency (i.e., high-frequency calls were produced by fearful individuals, and low-frequency calls were produced by aggressive individuals) but no support for the expected relationship between motivational state and tonality. However, the motivational state-frequency pairing was confounded by the fact that some taxonomic groups (Platyrrhini and Catarrhini) showed a much stronger level of association than other groups (Prosimii and Hominoidea). In summary, therefore, the nonhuman primate data provide only partial support for MS rules. At least three factors may have influenced the outcome of the current test. First, in some species, motivational state may be more closely associated with other acoustic parameters than absolute frequency and tonality. Second, the acoustic structure of nonhuman primate vocalizations is, at least in some cases, more closely associated with an external referent than with the caller's internal state. And third, features of the species-typical habitat have had direct selective effects on signal structure, optimizing for effective propagation through the environment.

Articulatory and social factors influence the acoustic structure of rhesus monkey vocalizations: a learned mode of production?

This report presents results that show that the acoustic structure of the "coo" vocalization of rhesus macaques (Macaca mulatta) varies between members of different matrilines. In the case examined, members of one matriline produce coos that are acoustically distinctive from all other matrilines and the difference is primarily due to spectral dampening and the presence of energy bands between the primary harmonics of the call. Perceptually, these acoustic modifications lead to what human listeners hear as a "nasal" utterance, suggesting the possibility of supralaryngeal filtering. Moreover, because nasal-sounding coos were only produced by members of one matriline, learning may be the primary cause of such intrafamilial similarities.

Costs of deception: cheaters are punished in rhesus monkeys (Macaca mulatta).

From a functional perspective, deception can evolve in animal populations but should be constrained by the costs associated with detection. It then follows that withholding information should be more prevalent as a form of deception than active falsification of information because of the relative difficulties associated with detecting cheaters. Empirical studies of deception have focused on the benefits of cheating but have provided no data on the costs associated with being detected as a cheater. I present results from field experiments on rhesus monkeys (Macaca mulatta) which show that individuals discovering food announce their discoveries by calling on 45% of all trials. Discoverers who failed to call, but were detected with food by other group members, received significantly more aggression than vocal discoverers. Moreover, silent female discoverers ate significantly less food than vocal females. This demonstrates that there are significant costs to withholding information. Such costs may constrain the frequency with which deception occurs in this and other populations.

Tinkering with minds from the past.

Cognitive scientists argue that in the absence of language, non-human animal conceptual representations are either impoverished or completely absent. One might make comparable claims about human infants, who enter the world with different conceptual representations from adults. Nonetheless, we often treat human infants like miniature adults. This is a mistake. I argue that research on human cognition, and in particular its domain specific knowledge systems, can only succeed if it adopts a comparative perspective. To carry out this agenda, however, we require methods that can be used across species. Focusing on how numerical abilities evolved, I describe experiments on two non-human primates, representing different phylogenetic branches. Our experimental procedure--the preferential looking time technique--was designed to assess what prelinguistic human infants know about the physical and psychological world, but it is ideal for non-human animals, especially when one wishes to explore spontaneous cognitive capacities in the absence of training. Results reveal that up to a certain age, human infants and non-human primates are indistinguishable in terms of numerical competence. We must now focus on how language, together with other cognitive facilities, bring the human child to a level of numerical sophistication that exceeds non-human animals, and why non-human animal capacities stop where they do.

Old age and its behavioral manifestations: a study on two species of macaque.

Observations from two studies on the behavior of stumptail and Japanese macaques revealed that old females were generally less active and involved in fewer social interactions than young adult females. Old females typically avoided or maintained sufficient distance from others to decrease the possibility of interaction, but were neither excluded from social interactions nor out-competed in rank-related situations. The data strongly suggest that the old females selectively withdrew from social interactions and maintained their rank over younger members of the group. Three possible explanations are discussed for the differences in behavior between old and young adult macaque females. (1) Old females with older offspring are less likely to interact with others than old females with younger offspring; (2) old females obtain fewer benefits from social interaction than young adult females, and (3) older females have less energy to disburse for social interaction due to physiological deterioration. The age of the youngest offspring did not account for the decline in social interactions among old females. It was concluded that active withdrawal from social interactions on the part of old females is likely to be the result of both a decrease in the benefits obtained from sociality and an overall physiological deterioration.

Is there teaching in nonhuman animals?

We derive a simple operational definition of teaching that distinguishes it from other forms of social learning where there is no active participation of instructors, and then discuss the constituent parts of the definition in detail. From a functional perspective, it is argued that the instructor's sensitivity to the pupil's changing skills or knowledge, and the instructor's ability to attribute mental states to others, are not necessary conditions of teaching in nonhuman animals, as assumed by previous work, because guided instruction without these prerequisites could still be favored by natural selection. A number of cases of social interaction in several orders of mammals and birds that have been interpreted as evidence of teaching are then reviewed. These cases fall into two categories: situations where offspring are provided with opportunities to practice skills ("opportunity teaching"), and instances where the behavior of young is either encouraged or punished by adults ("coaching"). Although certain taxonomic orders appear to use one form of teaching more often than the other, this may have more to do with the quality of the current data set than with inherent species-specific constraints. We suggest several directions for future research on teaching in nonhuman animals that will lead to a more thorough understanding of this poorly documented phenomenon. We argue throughout that adherence to conventional, narrow definitions of teaching, generally derived from observations of human adult-infant interactions, has caused many related but simpler phenomena in other species to go unstudied or unrecorded, and severely limits further exploration of this topic.