A quantitative method for studying behaviour in small groups of monkeys in captivity

A method is described in which the behaviour of individual animals is recorded to minimise order effects and observer differences in studying a small group of captive monkeys. Gross activity profiles were obtained using time sampling and a modified event recording technique. The application of this simple and relatively unambiguous recording method to the study of social behaviour is indicated.     

Eye contact by non-human primates toward a human observer

Eye contact by monkeys toward a staring observer is a quantifiable reliable and sensitive behavioural measure. Early social deprivation, an increase in age, a new cage, and an increase in distance all decreased the frequency of eye contact. Young female rhesus monkeys made more contact than young males. Large differences in eye contact occurred between species of non-human primates. The results are considered in relation to both an arousal theory and an attention theory.     

An observational learning task using Barnes maze in rats

Observational learning, which modulates one’s own behavior by observing the adaptive behavior of others, is crucial for behaving efficiently in social communities. Although many behavioral experiments have reported observational learning in monkeys and humans, its neural mechanisms are still unknown. In order to conduct neuroscientific researches with recording neural activities, we developed an observational learning task for rats. We designed the task using Barnes circular maze and then tested whether rats (observers) could actually improve their learning by observing the behavior of other rats (models) that had already acquired the task. The result showed that the observer rats, which were located in a metal wire mesh cylinder at the center of the maze and allowed to observe model rats escaping to the goal in the maze, demonstrated significantly faster escape behavior than the model rats. Thus, the present study confirmed that rats can efficiently learn the behavioral task by observing the behavior of other rats; this shows that it is conceivable to elucidate the neural mechanisms of social interaction by analyzing neural activity in observer rats performing the observational learning task.     

Dynamic social adaptation of motion-related neurons in primate parietal cortex

Social brain function, which allows us to adapt our behavior to social context, is poorly understood at the single-cell level due largely to technical limitations. But the questions involved are vital: How do neurons recognize and modulate their activity in response to social context? To probe the mechanisms involved, we developed a novel recording technique, called multi-dimensional recording, and applied it simultaneously in the left parietal cortices of two monkeys while they shared a common social space. When the monkeys sat near each other but did not interact, each monkey's parietal activity showed robust response preference to action by his own right arm and almost no response to action by the other's arm. But the preference was broken if social conflict emerged between the monkeys-specifically, if both were able to reach for the same food item placed on the table between them. Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other. Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations. Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.     

神农架川金丝猴投食群的社会行为谱

为探讨人工投食条件下川金丝猴的社会行为类型,2007年1月-2008年10月,采用行为取样法和全事件记录法对湖北神农架自然保护区投食猴群的社会行为进行观察。确定投食群有45种典型社会行为,其中打架、抢食、抱腰、吻背、爬伏、邀配与以往对笼养和野生川金丝猴的研究有差别。     

Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi's monkeys (Callimico goeldii)

Neophobia, defined as showing caution toward novel features of the environment, is widespread in birds and mammals; it can be affected by ecology, early experience, and social context. In this study, we aimed to (i) investigate the response to novel food in adult common marmosets and Goeldi's monkeys and (ii) assess the role of social influences. We used an experimental paradigm employed previously with capuchin monkeys and children, in which a subject (observer) was presented with a novel food under three conditions: (i) Presence: group members did not have food; (ii) Different color: group members received familiar food whose color differed from that of the observer's novel food; (iii) Same color: group members received familiar food of the same color as the observer's novel food. Although most common marmosets tasted and/or ate the novel food, none of the Goeldi's monkeys ate it and only two sampled it. Differences in home range size and early social experience might explain the divergent behavior of the two species. Observers of both species similarly attended to group members and their visual attention increased with the number of group members eating, especially when the observer's and group members' foods were perceptually similar. However, we observed social influences on explorative behavior in Goeldi's monkeys but not on explorative or eating behavior in common marmosets. This result might be explained by the different pattern of response to novel food observed in the two species. Moreover, social influences on Goeldi's monkeys' behavior were nonspecific, i.e. they were not based on an appreciation that the food is safe because eaten by group members.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Communicative signals and social behaviour of some African monkeys: A comparative study

The individual spacing in a monkey troop varies with species. Patas monkeys disperse more than baboons. Individual friendships or hostility, pregnancy, health, and status may also affect the individual distance. The troop structure and troop size vary with the habitat. Forest-canopy monkeys may have a “master male” but no leader such as have those in the savanna. The latter also make use of more elaborate visual signals and may possess coloured genitalia and other easily recognized structures which are given a communicative function. The baboons were found to make use of more signals than the other monkeys studied. Assertive, aggressive, friendly, and appeasing signals are described. Visual appeasing signals are missing among guenons and patas monkeys. Both have a “master male” which spends much time at a distance from the troop. These peculiarities as well as the birth of a healthy vervet-patas hybrid in Ibadan causes the author to suggest that the generic differentiation between the patas and the guenons should be abandoned. There was nothing to suggest that grooming reflects the social ranking. Nor were there any signs that oestric cycling or having an infant-I affected the animal's social status. Such influences would also upset the social stability.     

The influence of snowfall,temperature and social relationships on sleeping clusters of Japanese monkeys during winter in Shiga Heights

We studied Japanese monkeys (Macaca fuscata) of the Shiga A₁ troop at their sleeping sites in Shiga Heights, Japan, for 41 nights during 3 winters. Monkeys chose their sleeping sites in Japanese cedars and in deciduous broad-leaved forests on non-snowing nights and in Japanese cedar forests on snowing nights. We counted 399 sleeping clusters in which 2 or more monkeys remained in physical contact through the night and 43 solitary sleeping monkeys, though monkeys did not maintain physical contact with others in the daytime. We found 397 clusters on tree branches and 2 clusters on rocks. The mean size of huddling clusters was 3.06±1.22 SD. The cluster size (3.17±1.26 SD) at lower ambient temperatures between −7 and −4°C was larger than that at higher temperatures between −2 and 4°C (cluster size 2.88±1.13 SD). Most clusters were composed of kin. Females kept close to related females in the daytime and huddled with them at night. The highest-ranking male mainly huddled with his kin and his familiar females. Other males kept farther apart from each other in the daytime, probably to avoid social conflicts. Through cold winter nights, however, such males reduced inter-individual distances and huddled with other males. Japanese monkeys appear to recognize three types of inter-individual distances: an intimate distance less than 1 m, a personal distance of 1–3 m and a social distance of 3–20 m; they change their inter-individual distances according to social and ecological circumstances.     

Scratching as a Window into the Emotional Responses of Wild Tufted Capuchin Monkeys

Emotional responses to social interactions and the associated behavioural measures (e.g., self‐directed behaviours, SDBs) have been little studied in New World monkeys, especially in wild settings. In this study, we investigated the factors affecting anxiety in a wild group of tufted capuchin monkeys (Cebus apella nigritus) using self‐scratching (hereafter scratching) as its measure. Scratching was more strongly affected by the social context than by individual characteristics. Indeed, inter‐individual variability was not explained by the age, sex and dominance rank of the monkeys. The monkeys scratched themselves more often when being distant from other group members than when in close proximity with them, suggesting that even short‐distance separation from group members may be an important factor affecting capuchins emotional response. The risk of receiving aggression seemed also to elicit anxiety, as scratching was higher when in proximity to more dominant individuals and females, which were the categories of group members that were more aggressive. By contrast, scratching was lower when in proximity to more secure partners, like kin. Finally, scratching rates following the receipt of aggression were higher than at baseline, indicating a post‐conflict increase in anxiety. Overall, our results contribute to the understanding of the factors affecting emotional responses in capuchin monkeys, confirming and expanding previous findings in other animal species.     

Assessment of individual differences in the preferred proximity to a human feeder by partitioned raisin test, with two species of macaque monkeys

All animals must acquire food and mates by approaching them despite possibilities of accompanying risks and thus are frequently encountered with approach-avoidance conflicts in daily lives. Behavioral individual differences in such situations may be considered as one of the most biologically fundamental personality trains. “Partitioned raisin test” was devised to assess this trait with macaque monkeys. It involved throwing raisins into groups of monkeys and observing the preferred distance of each from the human feeder, a source of possible harm. The test was administered to 4 groups of Japanese monkeys (30 total) and 3 groups of rhesus monkeys (19 total), all l-yr-old and matched in history. Individual differences in the preferred proximity to the feeder, as expressed by the Proximity Index (PI), were found in both species.PI was not correlated with a measure of dominance over the raisins. Individual differences inPI were also not due to territorial effects unrelated to the location of the feeder.PI was stable in five of the six monkeys re-tested after one year of interval in a newly organized group, where there supposedly had been a change in their social structure. Partitioned raisin test was shown to be capable of depicting individual differences related to differential approach bias in an approach-avoidance conflict situation. Although possible confounding effects by social factors need to be delineated in the following studies, the method may provide a handy and widely applicable way for the assessment of this trait with monkeys.     

Behavioural and neurophysiological evidence for face identity and face emotion processing in animals

Visual cues from faces provide important social information relating to individual identity, sexual attraction and emotional state. Behavioural and neurophysiological studies on both monkeys and sheep have shown that specialized skills and neural systems for processing these complex cues to guide behaviour have evolved in a number of mammals and are not present exclusively in humans. Indeed, there are remarkable similarities in the ways that faces are processed by the brain in humans and other mammalian species. While human studies with brain imaging and gross neurophysiological recording approaches have revealed global aspects of the face-processing network, they cannot investigate how information is encoded by specific neural networks. Single neuron electrophysiological recording approaches in both monkeys and sheep have, however, provided some insights into the neural encoding principles involved and, particularly, the presence of a remarkable degree of high-level encoding even at the level of a specific face. Recent developments that allow simultaneous recordings to be made from many hundreds of individual neurons are also beginning to reveal evidence for global aspects of a population-based code. This review will summarize what we have learned so far from these animal-based studies about the way the mammalian brain processes the faces and the emotions they can communicate, as well as associated capacities such as how identity and emotion cues are dissociated and how face imagery might be generated. It will also try to highlight what questions and advances in knowledge still challenge us in order to provide a complete understanding of just how brain networks perform this complex and important social recognition task.     

Social Suppressive Behavior Is Organized by the Spatiotemporal Integration of Multiple Cortical Regions in the Japanese Macaque

Under social conflict, monkeys develop hierarchical positions through social interactions. Once the hierarchy is established, the dominant monkey dominates the space around itself and the submissive monkey tries not to violate this space. Previous studies have shown the contributions of the frontal and parietal cortices in social suppression, but the contributions of other cortical areas to suppressive functions remain elusive. We recorded neural activity in large cortical areas using electrocorticographic (ECoG) arrays while monkeys performed a social food-grab task in which a target monkey was paired with either a dominant or a submissive monkey. If the paired monkey was dominant, the target monkey avoided taking food in the shared conflict space, but not in other areas. By contrast, when the paired monkey was submissive, the target monkey took the food freely without hesitation. We applied decoding analysis to the ECoG data to see when and which cortical areas contribute to social behavioral suppression. Neural information discriminating the social condition was more evident when the conflict space was set in the area contralateral to the recording hemisphere. We found that the information increased as the social pressure increased during the task. Before food presentation, when the pressure was relatively low, the parietal and somatosensory–motor cortices showed sustained discrimination of the social condition. After food presentation, when the monkey faced greater pressure to make a decision as to whether it should take the food, the prefrontal and visual cortices started to develop buildup responses. The social representation was found in a sustained form in the parietal and somatosensory–motor regions, followed by additional buildup form in the visual and prefrontal cortices. The representation was less influenced by reward expectation. These findings suggest that social adaptation is achieved by a higher-order self-regulation process (incorporating motor preparation/execution processes) in accordance with the embodied social contexts.     

Neocortex size predicts deception rate in primates

Human brain organization is built upon a more ancient adaptation, the large brain of simian primates: on average, monkeys and apes have brains twice as large as expected for mammals of their size, principally as a result of neocortical enlargement. Testing the adaptive benefit of this evolutionary specialization depends on finding an association between brain size and function in primates. However, most cognitive capacities have been assessed in only a restricted range of species under laboratory conditions. Deception of conspecifics in social circumstances is an exception, because a corpus of field data is available that encompasses all major lines of the primate radiation. We show that the use of deception within the primates is well predicted by the neocortical volume, when observer effort is controlled for; by contrast, neither the size of the rest of the brain nor the group size exert significant effects. These findings are consistent with the hypothesis that neocortical expansion has been driven by social challenges among the primates. Complex social manipulations such as deception are thought to be based upon rapid learning and extensive social knowledge; thus, learning in social contexts may be constrained by neocortical size.     

Inexpensive outdoor enclosure for Japanese macaques used in biobehavioral research

For studies of alcohol self-administration in a monkey social group, we effectively and humanely enclosed nine Japanese macaques (Macaca fuscata) in an ellipse 32 x 40m, with a 1 m high chain-link fence surmounted by a 3 m curtain of electrically conductive nylon net. High-voltage brief-pulse charges prevent climbing on the net. Materials for this fence cost less than $14.50 per running meter. Weeds and grass grew freely within the ellipse, and seven dead trees interconnected with ropes permitted climbing and swinging. An open, roofed gazebo provided sun and rain shelter, and its single wall blocked the prevailing wind. Mouth activated drinkometer spouts in the corral supplied solutions for voluntary alcohol self-administration. Automatic counters informed an observer of exact doses consumed by each subject. Another observer recorded the frequency of occurrence of various social behaviors. A small kennel run, roofed over with chain-link fencing, connected the corral with a paddock-like, partially heated building, to and from which the monkeys usually had free access. It contained three interconnected chain-link pens. A raceway opening from the pens incorporated a squeeze cage used for weighing animals, drawing blood samples, or administering medications. This unique facility promotes the psychological well-being of research primates, which is being mandated by federal law.     

Japanese monkeys living in the Okoppe Basin of the Shimokita Peninsula: The second report of the winter follow-up survey after the aerial spraying of herbicide

In regard to a late winter ecological survey of the Japanese monkeys living in the Okoppe Basin and to investigate the aftereffects of the herbicide which was sprayed aerially by the Aomori Regional Forestry Office, the following results were obtained: Troop Z, one of the three troops found in December, moved restrictively around the upper basin of the Okoppe River during this survey period, which area had been strongly influenced by the spraying. The movements of troop Z could be traced throughout this period and the distance of movement per day, the sleeping places, the population, and the social composition were confirmed. The nomadic range was 2.5 square km, equal to only 15.6% of that of December. The monkeys of troop Z fed mainly the bark and buds of trees. The poisonous residue remaining in the bark and buds is ingested by pregnant female monkeys through feeding and may exert some influence upon the fetus.     

Experimental analysis of the nature of social context in captive groups of squirrel monkeys (Saimiri sciureus)

The nature of social context as a factor affecting grouping behavior is experimentally examined in captive groups of squirrel monkeys by recording the effects of systematic removal and return of individuals on the distributions of non-agonistic interactions and prolonged (huddle) contacts among the remaining group members. Observed changes in the distributions of these interactions among the remaining individuals are analyzed in terms of the age-sex class of the individual(s) removed, age-sex distributions of the individuals remaining, and the classes of dyadic relationships severed by the removals. Results indicate that, at least so far as these spacing-related behaviors are concerned, (1) the social environment does not act as a configurational whole on the grouping behavior of individuals, (2) the effect of social context on grouping behavior may be analyzed as the effects of specific dyadic relationships upon others, and (3) not all dyadic relationships significantly affect all others in a social group, i.e., not all of the social environment is relevant to the interactions between all pairs of individuals.     

Extra-large cluster formation by Japanese macaques (Macaca fuscata) on Shodoshima Island, central Japan, and related factors

Japanese macaques on Shodoshima Island habitually form very large rest clusters, in which 50+ or even 100+ individuals huddle together. This behavior is not seen in any other populations of the species. Mean cluster sizes of two groups of Shodoshima monkeys are three and four in summer and 17 and 16 in winter, respectively. A maximum of 137 individuals have been seen to huddle in one cluster. It is difficult to explain the extra large clusters on Shodoshima only as an adaptive behavior against cold, since Shodoshima is relatively warm in the range of habitats for Japanese macaques. Compared with other groups of Japanese macaques, Shodoshima monkeys show: more frequent affinitive interactions, shorter inter-individual distance, more frequent ignoring of exclusion, more frequent aggression, less intense aggression, and more frequent counter-aggression. These characteristics suggest that the Japanese macaques on Shodoshima have relaxed dominant relations. The specific social organization of Shodoshima monkeys may sustain the formation of extra large clusters. Inter-group comparisons suggest that the social structure of Japanese macaques might be highly plastic, and that Shodoshima monkeys have less despotic, more tolerant social relations than typically reported for this species.     

Development of visual preference for closely related species by infant and juvenile macaques with restricted social experience

Japanese and rhesus monkeys aged between 9 months old and 5 yrs old pressed a lever to see a variety of pictures of seven macaque species. These monkeys had various restricted social experience: namely, either reared by humans with conspecific or heterospecific peers, or cross-fostered between these two species. Rhesus monkeys tended to prefer seeing rhesus monkeys best among the pictures of the seven species without regard to their age or social experience. Japanese monkeys having restricted experience also liked to see rhesus monkeys better than Japanese monkeys, but not the best among the seven species. In a previous study, mother-reared infants of Japanese monkeys preferred seeing pictures of their own species over those of rhesus monkeys. These results suggest a dissociation of the determinants of this basic social preference: rhesus monkeys prefer to see their own species by nature while Japanese monkeys may learn to prefer their own species.     

Changes in the structure of group behavior in callosotomized rhesus monkeys

The studies were performed on 4 intact and 3 callosotomized adult male rhesus monkeys that comprised one social group. Group behaviour of all the monkeys was investigated by the frequency method of social contacts registration. Both aggressive and friendly contacts were registered. The results obtained have shown a considerable decrease in social contacts of callosotomized rhesus monkeys, as compared to normal animals. The aggressive contacts prevailed in the behaviour of the operated monkeys. The data suggest that callosotomy does not only significantly decrease the frequency, but also alters the structure of social contacts in the rhesus monkeys.