Multiple acoustic features underlie vocal signal recognition in tamarins: antiphonal calling experiments.

We examine which acoustic features are relevant for recognition of the cotton-top tamarin (Saguinus oedipus) combination long-call. This vocalization, emitted by both males and females, functions in maintaining group cohesion, territory defense and mate attraction. Using the tamarins' natural antiphonal vocal response to hearing a combination long-call as the primary measure of recognition, we presented subjects with synthetic exemplars of combination long-calls in which we manipulated across one of three acoustic dimensions: frequency, time and amplitude. Results indicated that although acoustic features in the frequency and time domains are important for combination long-call recognition, the changes in amplitude within and between syllables are not. Furthermore, while the fundamental frequency appears to be the used to encode information about the frequency contour, the temporal information is derived from the harmonics. Overall, these results suggest that tamarins use a specific suite of acoustic features for combination long-call recognition.

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.

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.

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.

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.

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.

The units of perception in the antiphonal calling behavior of cotton-top tamarins (Saguinus oedipus): playback experiments with long calls.

We investigated how the acoustic structure of the cotton-top tamarin monkey's (Saguinus oedipus) combination long call relates to the antiphonal calling behavior of conspecifics. Combination long calls can function as contact calls and are produced by socially isolated individuals. Often conspecifics respond to these calls with their own long calls. Structurally, these calls are always composed of one or more 'chirps' followed by two or more 'whistles'. We compared the antiphonal calling responses to playbacks of complete, naturally produced long calls versus single whistles or single chirps. Subjects responded significantly more to whole calls than to either syllable-type alone. Thus, our data suggest that, in terms of the antiphonal calling behavior of socially isolated conspecifics, the whole long call is the unit of perception.

Cotton-top tamarins (Saguinus oedipus) fail to show mirror-guided self-exploration.

To investigate the problem of inter- and intraspecific differences on the mirror test, we conducted two experiments on cotton-top tamarins. Experiment 1 employed a technique similar to one used recently on chimpanzees, and provided no evidence of mirror-mediated touching of the marked area. In a control condition, involving colored dye applied to one arm, two subjects also failed to show self-directed touching, even though they clearly looked at their newly dyed arm. Under these test conditions, cotton-top tamarins fail to show mirror-guided self-exploration. Experiment 2 examined whether this failure was due to insufficient mirror exposure, as well as other details of the testing conditions. In particular, we replicated the design of a previously successful experiment on mirror-mediated recognition in tamarins [Hauser et al., 1995], providing four new animals with a protracted period (three weeks) of mirror exposure prior to dying their hair. In parallel with results from Experiment 1, we observed no evidence of mirror-mediated behavior (recognition) in Experiment 2.

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.

Visual representation in the wild: how rhesus monkeys parse objects.

Visual object representation was studied in free-ranging rhesus monkeys. To facilitate comparison with humans, and to provide a new tool for neurophysiologists, we used a looking time procedure originally developed for studies of human infants. Monkeys' looking times were measured to displays with one or two distinct objects, separated or together, stationary or moving. Results indicate that rhesus monkeys used featural information to parse the displays into distinct objects, and they found events in which distinct objects moved together more novel or unnatural than events in which distinct objects moved separately. These findings show both commonalities and contrasts with those obtained from human infants. We discuss their implications for the development and neural mechanisms of higher-level vision.

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.

The role of temporal cues in rhesus monkey vocal recognition: orienting asymmetries to reversed calls.

An understanding of the acoustic cues that animals use to categorize their vocalizations has important implications for the way we design neuroethological investigations of auditory function. Compared to other species, we know relatively little about the kinds of acoustic features used by nonhuman primates to recognize and categorize vocalizations. To further our understanding, this study explores the role of temporal features in recognition of conspecific vocalizations by rhesus macaques (Macaca mulatta). Experiments were designed to extend an earlier set of findings showing that adult rhesus macaques selectively turn with the right ear leading when a conspecific vocalization is played 180 degrees behind them, but turn left or not at all when a non-conspecific signal is played. Two call types were used as stimuli: shrill barks (alarm call) and harmonic arches (food call). We found that for normal calls, rhesus macaques turned to the right - supporting earlier findings - but for time- reversed shrill barks and harmonic arches, subjects oriented to the left. These results suggest that for at least a subset of calls, rhesus macaques use temporal cues to recognize conspecific vocal signals. The asymmetry of the behavioral response, and the corresponding asymmetry in the time-amplitude waveform, may have important implications for studies of temporal coding in the primate auditory system.

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.

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.

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.

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.

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.

Numerical representations in primates.

Research has demonstrated that human infants and nonhuman primates have a rudimentary numerical system that enables them to count objects or events. More recently, however, studies using a preferential looking paradigm have suggested that preverbal human infants are capable of simple arithmetical operations, such as adding and subtracting a small number of visually presented objects. These findings implicate a relatively sophisticated representational system in the absence of language. To explore the evolutionary origins of this capacity, we present data from an experiment with wild rhesus monkeys (Macaca mulatta) that methodologically mirrors those conducted on human infants. Results suggest that rhesus monkeys detect additive and subtractive changes in the number of objects present in their visual field. Given the methodological and empirical similarities, it appears that nonhuman primates such as rhesus monkeys may also have access to arithmetical representations, although alternative explanations must be considered for both primate species.

Self-recognition in primates: phylogeny and the salience of species-typical features.

Self-recognition has been explored in nonlinguistic organisms by recording whether individuals touch a dye-marked area on visually inaccessible parts of their face while looking in a mirror or inspect parts of their body while using the mirror's reflection. Only chimpanzees, gorillas, orangutans, and humans over the age of approximately 2 years consistently evidence self-directed mirror-guided behavior without experimenter training. To evaluate the inferred phylogenetic gap between hominoids and other animals, a modified dye-mark test was conducted with cotton-top tamarins (Saguinus oedipus), a New World monkey species. The white hair on the tamarins' head was color-dyed, thereby significantly altering a visually distinctive species-typical feature. Only individuals with dyed hair and prior mirror exposure touched their head while looking in the mirror. They looked longer in the mirror than controls, and some individuals used the mirror to observe visually inaccessible body parts. Prior failures to pass the mirror test may have been due to methodological problems, rather than to phylogenetic differences in the capacity for self-recognition. Specifically, an individual's sensitivity to experimentally modified parts of its body may depend crucially on the relative saliency of the modified part (e.g., face versus hair). Moreover, and in contrast to previous claims, we suggest that the mirror test may not be sufficient for assessing the concept of self or mental state attribution in nonlinguistic organisms.

Left hemisphere dominance for processing vocalizations in adult, but not infant, rhesus monkeys: field experiments.

In humans, the left hemisphere of the brain is dominant for processing language. To assess the evolutionary origins of this neuropsychological mechanism, playback experiments were conducted on a large population of free-ranging rhesus monkeys (Macaca mulatta). Playbacks provided an equal opportunity to orient the right or left ear toward the speaker. Results revealed that 61 of 80 adult rhesus favored the right ear (left hemisphere) when vocalizations from their own repertoire were heard but favored the left ear when listening to heterospecific vocalizations. In contrast, infants less than a year old showed no perceptual asymmetry for conspecific or heterospecific calls. Thus, like humans, adult rhesus monkeys also evidence left hemisphere dominance for processing species-specific vocalizations. The emergence of such asymmetry, however, may depend on both differential maturation of the two hemispheres and experience with the species-typical vocal repertoire.