Yuko Hattori

Spontaneous synchronized tapping to an auditory rhythm in a chimpanzee

Humans actively use behavioral synchrony such as dancing and singing when they intend to make affiliative relationships. Such advanced synchronous movement occurs even unconsciously when we hear rhythmically complex music. A foundation for this tendency may be an evolutionary adaptation for group living but evolutionary origins of human synchronous activity is unclear. Here we show the first evidence that a member of our closest living relatives, a chimpanzee, spontaneously synchronizes her movement with an auditory rhythm: After a training to tap illuminated keys on an electric keyboard, one chimpanzee spontaneously aligned her tapping with the sound when she heard an isochronous distractor sound. This result indicates that sensitivity to, and tendency toward synchronous movement with an auditory rhythm exist in chimpanzees, although humans may have expanded it to unique forms of auditory and visual communication during the course of human evolution.

Cooperative problem solving by tufted capuchin monkeys (Cebus apella): Spontaneous division of labor, communication, and reciprocal altruism.

Using an experimentally induced cooperation task, the authors investigated whether tufted capuchin monkeys (Cebus apella) share the following 3 characteristics of cooperation with humans: division of labor, communication, and reciprocal altruism. In Experiment 1, the authors trained individual monkeys to perform the necessary sequence of actions for rewards and tested them in pairs to assess whether they could solve the task by spontaneously dividing the sequence of actions. All pairs solved this task. In Experiment 2, monkeys worked in the cooperation task and a task requiring no partner help. They looked at the partner significantly longer in the former task than in the latter, but communicative intent could not be determined. In Experiment 3, only 1 of 2 participants obtained a reward on each trial. Monkeys maintained cooperation when their roles were reversed on alternate trials. Their cooperative performances demonstrated division of labor; results suggest task-related communication and reciprocal altruism.

Tufted capuchin monkeys (Cebus apella) show understanding of human attentional states when requesting food held by a human

Researchers have investigated to what extent non-human primates understand others’ attentional states, as this ability is considered an important prerequisite for theory of mind. However, previous studies using food requesting tasks have failed to show that non-human primates attribute perception to others as a function of their attentional states. One possible reason is that food requesting tasks may require subjects not only to take into account an experimenter’s attentional state but also to direct it toward the food. The present study tested tufted capuchin monkeys’ (Cebus apella) understanding of others’ attentional states in a food requesting task. In the first situation, monkeys were required only to attract an experimenter’s attention. In the second situation, the monkeys were required to both attract the experimenter’s attention and direct it toward food on a table. The results revealed that capuchin monkeys showed evidence of understanding the experimenter’s attentional variations only in the former condition. This suggests that previous tasks, requiring referential gestures, lacking in most non-human primates, failed to reveal sensitivity to human attentional states because the subjects might not have understood the requesting situation. In conclusion, capuchin monkeys can understand variations in others’ attentional states, although this ability appears limited compared to what is seen in humans.

Searching for the origins of musicality across species.

In the introduction to this theme issue, Honing et al. suggest that the origins of musicality—the capacity that makes it possible for us to perceive, appreciate and produce music—can be pursued productively by searching for components of musicality in other species. Recent studies have highlighted that the behavioural relevance of stimuli to animals and the relation of experimental procedures to their natural behaviour can have a large impact on the type of results that can be obtained for a given species. Through reviewing laboratory findings on animal auditory perception and behaviour, as well as relevant findings on natural behaviour, we provide evidence that both traditional laboratory studies and studies relating to natural behaviour are needed to answer the problem of musicality. Traditional laboratory studies use synthetic stimuli that provide more control than more naturalistic studies, and are in many ways suitable to test the perceptual abilities of animals. However, naturalistic studies are essential to inform us as to what might constitute relevant stimuli and parameters to test with laboratory studies, or why we may or may not expect certain stimulus manipulations to be relevant. These two approaches are both vital in the comparative study of musicality.

Quality before quantity: rapid learning of reverse-reward contingency by capuchin monkeys (Cebus apella).

Capuchin monkeys (Cebus apella) were tested on a reverse-reward task involving different quantities of the same food, or an identical quantity of different foods. All monkeys tested first on the qualitative version spontaneously mastered the task, whereas only one of four spontaneously mastered the quantitative version. No monkey reached criterion when the tasks were switched, although almost all did so following remedial procedures after the study. The results suggest that (a) qualitative reverse-reward is easier than quantitative versions of the problem, (b) quality and quantity dimensions are processed differently in food-related tasks, and (c) capuchin monkeys can show rapid and spontaneous learning of reverse-reward contingencies.

Flexibility in the use of requesting gestures in squirrel monkeys (Saimiri sciureus)

Three squirrel monkeys, trained to make a requesting gesture, were tested in the presence of a human assistant whose visual attention varied across trials. When food was available in one dish and an empty dish was nearby, the monkeys pointed overwhelmingly toward the former, regardless of where the assistant was looking. Looking at the assistant while pointing (“monitoring”) peaked when she looked at them and when she attempted to engage them in joint attention. When only one dish was present, the monkeys refrained from gesturing if it was empty and if no assistant was present. They gestured more when the assistant made eye contact with them. Furthermore, when the assistants focus of attention switched from the dish or the ceiling to the monkeys, the latter resumed pointing and increased their monitoring of the assistant. This is the first demonstration of such flexible use of an intentionally communicative requesting gesture in New World monkeys. Am. J. Primatol. 72:707–714, 2010.

Attention to combined attention in New World monkeys (Cebus apella, Saimiri sciureus).

Co-orientation by capuchin (Cebus apella) and squirrel (Saimiri sciureus) monkeys in response to familiar humans abruptly switching the direction of their visual attention was recorded. Co-orientation occurred more frequently overall in capuchins than squirrel monkeys. Capuchins showed a tendency to habituate within trials involving consecutive attention switches performed by 2 different people, whereas squirrel monkeys co-oriented more when the 2nd attention switch was by a 2nd actor. These results suggest variable attention-processing abilities in New World monkeys, including differences in summation of attention by others.

Distractor Effect of Auditory Rhythms on Self-Paced Tapping in Chimpanzees and Humans

Humans tend to spontaneously align their movements in response to visual (e.g., swinging pendulum) and auditory rhythms (e.g., hearing music while walking). Particularly in the case of the response to auditory rhythms, neuroscientific research has indicated that motor resources are also recruited while perceiving an auditory rhythm (or regular pulse), suggesting a tight link between the auditory and motor systems in the human brain. However, the evolutionary origin of spontaneous responses to auditory rhythms is unclear. Here, we report that chimpanzees and humans show a similar distractor effect in perceiving isochronous rhythms during rhythmic movement. We used isochronous auditory rhythms as distractor stimuli during self-paced alternate tapping of two keys of an electronic keyboard by humans and chimpanzees. When the tempo was similar to their spontaneous motor tempo, tapping onset was influenced by intermittent entrainment to auditory rhythms. Although this effect itself is not an advanced rhythmic ability such as dancing or singing, our results suggest that, to some extent, the biological foundation for spontaneous responses to auditory rhythms was already deeply rooted in the common ancestor of chimpanzees and humans, 6 million years ago. This also suggests the possibility of a common attentional mechanism, as proposed by the dynamic attending theory, underlying the effect of perceiving external rhythms on motor movement.

Food-related tolerance in capuchin monkeys (Cebus apella) varies with knowledge of the partner's previous food-consumption

Capuchin monkeys, as well as several other primate species, show food-related tolerance in both captive and wild settings. Although researchers have revealed that past experience affects food-related tolerance, it is unclear if and how observing a partner’s previous food consumption affects tolerance. This question is important to determine the proximate mechanism of food-related tolerance, which may lead to food sharing, co-feeding, or tolerated taking. We investigated whether perception of another’s consumption of food affected the rate of tolerant food transfers among brown capuchin monkeys (Cebus apella). First, in the test condition, subjects observed their partner either eating (Eat-In View) or not eating food (No Eat-In View) through a window. In a control condition, the subjects could not observe the same partner behind an opaque screen, while the partner either ate (Eat-Out of View) or did not eat (No Eat-Out of View). After this, the subjects were provided with food to examine how well they tolerated their partner’s access to it through the mesh. Tolerant food transfers were sharply reduced after the subjects had observed their partner eat, but not in the control condition or after they had observed the partner not eating. We consider two possible hypotheses for this behavior, one relates to the internal state of the subject after having seen their partner eat (i.e., increased competitiveness, aggression, or food motivation). The other hypothesis relates to how the subject understands the partner’s motivational state after having witnessed food consumption, perhaps by grasping the partner’s need.

Asymmetric perception of radial expansion/contraction in Japanese macaque (Macaca fuscata) infants.

Visual radial expansion/contraction motion provides important visual information that is used to control several adaptive actions. We investigated radial motion perception in infant Japanese macaque monkeys using an experimental procedure previously developed for human infants. We found that the infant monkeys’ visual preference for the radial expansion pattern was greater than that for the radial contraction pattern. This trend towards an “expansion bias” is similar to that observed in human infants. These results suggest that asymmetrical radial motion processing is a basic visual function common to primates, and that it emerges early in life.