Metacognition in wild Japanese macaques: cost and stakes influencing information-seeking behavior.

Metacognition allows us to evaluate memories and knowledge, thus enabling us to distinguish between what we know and what we do not. Studies have shown that species other than humans may possess similar abilities. However, the number of species tested was limited. Testing ten free-ranging Japanese macaques (Macaca fuscata) on a task in which they had to find food hidden inside one of the four opaque tubes, we investigated whether these subjects would seek information when needed. The monkeys could look inside the tubes before selecting one. We varied three parameters: the baiting process, the cost that monkeys had to pay to look inside the tubes, and the reward at stake. We assessed whether and how these parameters would affect the monkeys' tendency to look inside the tube before selecting one. When they were not shown which tube contained the reward, nine monkeys looked significantly more frequently in at least one condition. Half of them tended to reduce their looks when the cost was high, but only when they already knew the location of the reward. When a high-quality reward was at stake, four monkeys tended to look more inside the tubes, even though they already knew the reward's location. Our results are consistent with those of rhesus macaques, suggesting that metacognitive-like abilities may be shared by Cercopithecidae, and that, at least some monkeys may be aware of their lack of knowledge.

Metacognition in Japanese macaques (Macaca fuscata): does impulsivity explain unnecessary looks in the tubes task?

Potential metacognitive abilities, such as monitoring and controlling cognitive processes, have been revealed in some primate species. In the tubes task, apes and macaques showed higher content-checking behavior when unaware of a reward's location, but they also periodically inspected the tubes when aware, especially when a more appealing reward was involved. Some attribute this to the pleasure of looking at the reward. This study investigates whether the unnecessary tube-checking behavior observed in nine wild Japanese macaques, previously tested for metacognition using the tubes task, can be solely attributed to impulsivity. The macaques' propensity to look inside a single tube containing food they cannot immediately reach was measured and compared to their behavior in the tubes task. Results indicated that looking inside the baited tube increased as reward quality improved. However, macaques displaying unnecessary tube inspections in metacognitive tests showed less impulsivity to look. This intriguing result counters the notion that excessive looking in the tubes task is solely due to impulsive looking, prompting us to advocate for further research into the relationship between inhibition and metacognitive performance.

Production of regular rhythm induced by external stimuli in rats.

Rhythmic ability is important for locomotion, communication, and coordination between group members during the daily life of animals. We aimed to examine the rhythm perception and production abilities in rats within the range of a subsecond to a few seconds. We trained rats to respond to audio-visual stimuli presented in regular, isochronous rhythms at six time-intervals (0.5-2 s). Five out of six rats successfully learned to respond to the sequential stimuli. All subjects showed periodic actions. The actions to regular stimuli were faster than randomly presented stimuli in the medium-tempo conditions. In slower and faster tempo conditions, the actions of some subjects were not periodic or phase-matched to the stimuli. The asynchrony regarding the stimulus onset became larger or smaller when the last stimulus of the sequence was presented at deviated timings. Thus, the actions of the rats were tempo matched to the regular rhythm, but not completely anticipative. We also compared the extent of phase-matching and variability of rhythm production among the interval conditions. In interval conditions longer than 1.5 s, variability tended to be larger. In conclusion, rats showed a tempo matching ability to regular rhythms to a certain degree, but maintenance of a constant tempo to slower rhythm conditions was difficult. Our findings suggest that non-vocal learning mammals have the potential to produce flexible rhythms in subsecond timing.

Examination of the joint Simon effect in rats: Changes in task performance based on actions of the partner.

Nonhuman animals have demonstrated various cooperative behaviors; however, many examples can be interpreted as individual contributions to a task rather than true behavioral coordination. In this study, we used the joint Simon task in rats to determine whether the presence of and task sharing with a partner affected performance in a joint activity. Rats were trained to discriminate between two auditory stimuli (3 and 12 kHz tones) and individually performed an auditory Simon task. They were paired with another rat and tested to perform half of the task, while the other rat performed the other half (joint task condition). The Simon effect was confirmed when the two rats completed half of a joint task. In contrast, when they were placed side by side but only one rat completed half of the task, the Simon effect was not observed. Further analyses revealed that the Simon effect observed in the joint task could not be explained by the simple addition of the two half tasks. In conclusion, task sharing affected individual performance in rats.

An exploratory study of behavioral traits and the establishment of social relationships in female laboratory rats.

There is growing evidence that social relationships influence individual fitness through various effects. Clarifying individual differences in social interaction patterns and determinants for such differences will lead to better understanding of sociality and its fitness consequences for animals. Behavioral traits are considered one of the determining factors of social interaction. The purpose of this study was to explore the effects of individual behavioral traits on social relationship building in laboratory rats (Rattus norvegicus), a highly social species. Initially, the following behavioral characteristics were measured in individuals: tameness (glove test), activity (open field test), exploration (novel object test), sociability (three-chamber test), and boldness (elevated plus maze test). We then used DeepLabCut to behaviorally track three groups of four individuals (12 total) and analyze social behaviors such as approach and avoidance behaviors. Principal component analysis based on behavioral test results detected behavioral traits interpreted as related to exploration, boldness, activity, and tameness, but not sociability. In addition, behavioral tracking results showed consistent individual differences in social behavior indices such as isolation time and partner preference. Furthermore, we found that different components were correlated with different phases of social behavior; exploration and boldness were associated with the early stages of group formation, whereas activity was associated with later stages of relationship building. From these results, we derived hypothesize that personality traits related to the physical and social environment have a larger influence in the relationship formation phase, and the behavioral trait of activity becomes important in the maintenance phase of relationships. Future studies should examine this hypothesis by testing larger group sizes and ensuring there is less bias introduced into group composition.

Stimulus modality affects the accuracy of rhythm production in rats.

Vocal learning species such as humans and parrots show auditory dominance when they synchronize their actions to an external rhythm. However, whether non-vocal-learners show a specific modality dominance in a rhythmic task has scarcely been examined. We predicted that rats, who are nocturnal and known to rely on acoustic communication, would exhibit higher sensitivity to auditory rhythm compared to visual rhythm. We investigated whether performance of a synchronization task by rats differs based on stimulus modality. We trained five rats to press a lever in time to auditory-visual, isochronous stimuli presented at three different tempos. Rats showed a lower correct response rate when auditory stimuli were presented than when visual or auditory-visual stimuli were presented in the 0.5-s inter-onset interval condition. Neither the asynchrony with the stimulus onset, nor the variability of interval production differed significantly based on the stimulus modality. Therefore, contrary to the prediction, they did not show auditory dominance; rather, rats showed poor performance on the task when a visual stimulus was not present. These results are consistent with the gradual audio-motor evolution hypothesis, and suggest that rats share ability for rhythm production, but this might not necessarily depend on auditory modality.

Temporal adjustment of short calls according to a partner during vocal turn-taking in Japanese macaques.

Turn-taking is a common feature in human speech, and is also seen in the communication of other primate species. However, evidence of turn-taking in vocal exchanges within a short time frame is still scarce in nonhuman primates. This study investigated whether dynamic adjustment during turn-taking in short calls exists in Japanese macaques Macaca fuscata. We observed exchanges of short calls such as grunts, girneys, and short, low coos during social interactions in a free-ranging group of Japanese macaques. We found that the median gap between the turns of two callers was 250 ms. Call intervals varied among individuals, suggesting that call intervals were not fixed among individuals. Solo call intervals were shorter than call intervals interrupted by responses from partners (i.e., exchanges) and longer than those between the partner's reply and the reply to that call, indicating that the monkeys did not just repeat calls at certain intervals irrespective of the social situation. The differences in call intervals during exchanged and solo call sequences were explained by the response interval of the partner, suggesting an adjustment of call timing according to the tempo of the partner's call utterance. These findings suggest that monkeys display dynamic temporal adjustment in a short time window, which is comparable with turn-taking in human speech.

Vocalizations during post-conflict affiliations from victims toward aggressors based on uncertainty in Japanese macaques.

We investigated the use of vocalizations called "grunts," "girneys," and "coos" accompanied by post-conflict affiliative interaction between former opponents (reconciliation) in Japanese macaques (Macaca fuscata). Although reconciliation functions to repair bonds, such interactions sometimes entail risks of receiving further aggression. Vocalizations can be used at a distance from the former opponent; thus, we predict that vocalizations are used particularly by victims of a conflict, and are frequently used in situations of uncertainty when it is difficult for them to estimate whether the former opponent will resume aggression. In addition, we predict that vocalizations are effective in preventing further aggression. To test these hypotheses, we conducted observations of post-conflict and matched-control situations in female Japanese macaques living in a free-ranging group. We found that former opponents tended to be attracted to each other within the first minute following a conflict, thus demonstrating reconciliation behavior. Vocalizations were more frequently used by the victims in post-conflict interactions than under control situations; however, this tendency was not found in aggressors. When affiliation with the former opponent occurred, victims were more likely to use vocalizations towards less familiar opponents. These findings suggest that Japanese macaques used vocalizations more often when interacting with less predictable former opponents. Victims were more likely to receive aggression from former aggressors when engaged in affiliations with them than under no such affiliations. No significant differences were found in the probability of the victims receiving aggression, regardless of whether they used vocalizations; thus, whether the victim benefits from using vocalizations in these contexts remains unclear. Japanese macaques form despotic societies and therefore, further aggression was inevitable, to some degree, after a conflict. The use of vocalizations by a victim was found to depend on the nature of their relationship with the aggressor; however, the effectiveness of this behavior requires further investigation.

Social relationships of nulliparous young adult females beyond the ordinary age of the first birth in a free-ranging troop of Japanese macaques (Macaca fuscata).

We describe the social relationships of young adult female Japanese macaques (Macaca fuscata) in a free-ranging troop in Arashiyama, Kyoto, Japan, who remained nulliparous beyond the ordinary age of first birth because of contraceptive administration. We observed 12 young nulliparous adult females (6-9 years old) for 270 h and 10 min from 2 February to 5 October 2010. The majority maintained close relationships with their mothers through proximity and grooming, whereas a few had very infrequent social interactions with their mothers. Most had asymmetrical grooming relationships; the grooming they received from unrelated adult females was less than the grooming they gave. Young adult females who had less frequent interactions with their mothers by either proximity or grooming received more grooming from a larger number of unrelated adult females than did those who had more frequent social interactions with their mothers. These results indicate that most young adult females who remained nulliparous beyond the ordinary age of first birth tended to maintain close relationships with their mothers, and their grooming relationships with unrelated adult females were inversely related to the degree of closeness with their mothers.