奨励賞発表

Oxytocin has drawn significant research attention for its role in modulating mammalian social behavior. Despite generally conserved roles, oxytocin can function differently even in closely related species. Previous studies have shown that bonobos and chimpanzees, humans’ two closet relatives, demonstrate considerable behavioral differences, including that bonobos look more at others’ eyes than chimpanzees. Oxytocin is known to increase attention to another’s eyes in many mammalian species (e.g. dogs, monkeys, and humans), yet this effect has not been tested in any nonhuman great ape species. This study examined how intranasally-administered oxytocin affects eye contact in bonobos and chimpanzees using eye-tracking. Following administration of either oxytocin or saline control with a nebulizer, chimpanzees (n = 6) and bonobos (n = 5) were shown images of conspecific faces while their eye movement was recorded. Oxytocin changed the eye-looking behavior of bonobos and chimpanzees differently. We found that oxytocin increased eye contact in bonobos, but caused an opposite effect, moderate eye avoidance, in chimpanzees. Given the importance of eye contact in their social interactions, our results suggest that oxytocin may play modulatory roles in bonobos’ and chimpanzees’ species-specific social behavior and underscore the importance of oxytocin in hominid social evolution.

Social primates must recognise developmental stages of other conspecifics in order to behave appropriately. Infant faces have peculiar morphological characteristics – relatively large eyes, a small nose, and small mouth – known as baby schema. In addition, the infant faces of many primate species have unique skin coloration. However, it is unclear which features serve as critical cues for chimpanzees to recognise developmental changes in their faces. The present study aimed to investigate the relative contributions of facial shape and colour to age categorisation in chimpanzees. We used a symbolic matching-to-sample task in which chimpanzees were trained to discriminate between adult and infant faces. Then, we tested how their age category judgments transferred to a series of morphed faces which systematically differed in facial shape and colour. Statistical image quantification analysis revealed significant differences both in shape and colour between adult and infant faces. However, we found that facial coloration contributed to age categorisation in chimpanzees more than facial shape. Our results showed that chimpanzees use unique infantile facial coloration as a salient cue when discriminating between adult and infant faces. The display of their developmental stages through facial colour may help chimpanzees to induce appropriate behaviour from other individuals.

Facial expressions are subtle signals, central for communication and emotion in mammals. In humans, facial expressions are automatically classified as a whole (e.g. happy face), i.e., there is a global and emotionally-linked categorisation, but people fail to detect subtle cues (e.g. brow raise). Moreover, the same configuration (e.g. lip corners pulled backwards exposing teeth) can convey widely different information depending on the species (e.g. human: happiness; chimp: fear). The gold standard FACS (Facial Action Coding System) for investigating human facial behavior avoids errors of meaning, by objectively measuring movement linked to each facial muscle (coded as Action Units, AUs). Here we follow similar methodology previously published AnimalFACS (www.animalFACS.com) from seven species, to create the CalliFACS for the common marmoset. First, we determined the marmoset facial muscles by examining dissections and diffusion MRI scans. Second, we analysed over 5hrs of video (frame-by-frame) from 100 marmosets in a wide range of populations and contexts, to classify individual facial movements into AUs. We identified 15 AUs (independent muscle movements), 15 Action Descriptors (by non-mimetic muscles) and 4 Ear Action Descriptors. CalliFACS is a scientific tool to better understand the common marmoset’s communication and expression, and can be used also to evaluate marmoset welfare.

Cochlear implants, a surgical intervention to insert a stimulating electrode into the cochlea, allow hearing-impaired individuals to regain auditory perception. Infrared neural stimulation has a potential for clinical support of auditory deficits because the infrared laser light can penetrate the tissues and stimulate the cochlear nerve. Here we show that auditory perception could be evoked by the laser irradiation of auditory nerves. We trained head-fixed Mongolian gerbils (Meriones unguiculatus) on a classical delay conditioning task. Repetitive infrared laser irradiation pulses to the lateral side of the cochlea from the ear canal through a tympanic membrane were paired with a drop of water. After the training, gerbils showed conditioned licking responses to the repetitive pulses. In test sessions following the training, lasers with various intensities (radiant energy: 0.2 to 19.1 mJ/cm²) were presented as probe stimuli. Higher licking rate was observed as the radiant energy increased. In a subsequent experiment, white noise (sound pressure level: 35, 50, 65, 80, 95 dB SPL) was presented as a masking stimulus during the laser stimulating period. A lower licking rate was observed as the masking stimulus intensified. These results indicate that the infrared neural stimulation of the auditory nerve produces auditory perception, and the perceptual level can be controlled by changing the radiant energy. This research will be an important step for the clinical application of cochlear implants for auditory deficits.

Song is an important signal for songbirds to evaluate potential mates. Previous studies found that early developmental auditory experience shapes how birds recognize songs later in life. In some species where only males learn and produce song, it has been reported that both sexes similarly prefer their father’s song over unfamiliar songs despite the sexual dimorphism of singing behavior. However, the function of such selective responses to father’s song has not been fully uncovered. In this study, we conducted 2 experiments with Bengalese finches (Lonchura striata var. domestica) in order to understand the ecological meaning of the preference to father’s song, especially in females. In the first experiment, we quantified song preference by phonotaxis assay and compared the behavior between sexes across development. As birds became sexually matured, females retained strong preference to father’s song while males did not. To examine if this sex difference is related to female mate choice, we tested female song preference using a sexual receptive display in the second experiment. We found that father’s song induced the display more frequently than unfamiliar songs in all individuals we tested (8 birds). These results suggest that female Bengalese finches are sexually imprinted on their father’s song when they are young and use that song memory for future mate choice.

Humans often show rhythmic turn-taking on various motor behaviors, such as Mochi-tsuki, which may reflect humans’ highly social trait. Rhythmic turn-taking can be seen also among non-human animals in the wild; however, those are expressed as innate and stereotypic behaviors. Here, we report that budgerigars, known as a highly social species and exhibiting rhythmic motoric behaviors, changed peck timing depending on the partner in an alternate key pecking task. We used an operant conditioning system consisting of two separate cages, each of which equipped a response key and a food dispenser, so that two birds could work facing each other. Each of the two birds pecked an illuminated key located at the bird’s own side alternately. Six pecks in total were required for a food reward. Thus, each of them made inter response intervals (IRIs) using the partner’s preceding peck. One bird made shorter IRI when paired with a specific bird while the IRIs were longer when the bird paired with another bird. Results of a preference test suggest that the birds might adjust the timing of own movement to others when paired with much preferable birds.

Behavioral synchronization, including phenomena such as contagious yawning and facial mimicry, has gained increased scientific attention. It is a fundamental ability required for social animals to maintain group cohesion and operate in collective behavior. This study examined the possibility of synchronized urination in captive chimpanzees (Pan troglodytes). To our knowledge, no previous study has examined such a phenomenon. We aimed to quantitatively demonstrate the existence of synchronized urination of captive chimpanzees. We then investigated the effects of social closeness on such synchronization to investigate possible functions of the phenomenon. We observed 4 groups of captive chimpanzees (N=20) for cumulative 193 hours at Kumamoto Sanctuary. We recorded all urinations with a resolution of 1 second as well as grooming interactions and physical proximity at 2-minute intervals. The observed results were then compared to a simulation (100 sessions) of random urination timings. We found synchronizations within 65 seconds occurred at a higher rate than predicted by the simulation. We did not find a clear relationship with social bond strength so far, which needs further investigation with larger sample size.

Human receive information not only through direct experience but also through referential media such as videos. Human experience is expanded by the ability to utilize information which refer to particular events and objects that are out-of-sight. However, it is unclear whether and to what extent such referential competence is shared in non-linguistic animals. To address this, we tested whether chimpanzees can garner video information about relevant events, which is not directly observed. Five chimpanzees first observed food-hiding in one room. A half banana was baited into one of the two cups (green/red) by an experimenter. Chimpanzee then moved to the next room received a choice test. Food-hiding was demonstrated either directly in front of them (Real condition) or through video (Video condition). Two individuals performed better than chance in both conditions suggests that chimpanzees may share the ability to acquire information based on referential media–referent association with humans. Conversely, the remaining three individuals failed in both conditions suggests that spatial dissociation and/or temporal delay between observation and choice test may be causes of failure. Future studies need to test if their understanding of referential function of video can be facilitated by improving task continuity in space and time.

Some non-human species seek information according to their current state of knowledge, like humans. In the present study, we tested whether a giraffe (Giraffa camelopardalis) would seek information based on his knowledge state. In experiment 1, we put a target on one of three tables. When the giraffe pointed towards it by extending his neck, he received a reward from an experimenter. In the test trials, the subject had to look over a panel that covered the tabletop to see the target location. However, the subject never spontaneously learned to do this. In experiment 2, we successfully trained the subject to look over a panel to see the target on the tabletop, and then in test trials we used combinations of transparent and opaque panels. The subject looked over the panel for the target more often when it was behind an opaque panel than a transparent one. But he also did this even when the target was behind the only opaque panel. This result suggests that the giraffe was collecting information according to his knowledge state, but did not engage in reasoning by exclusion.

In group-living animals, forming and maintaining social bonds between individuals is crucial for social survival. To form and maintain a social bond, it is necessary for two individuals to inhibit aggressive or submissive behavior dependently on their relative dominance but also to facilitate affiliative behavior between them. Previous studies have revealed the involvement of the Oxytocin / Vasopressin systems in pair bonds and mother-infant bonds but recently suggested even in same-sex bonds. However, it remains unknown whether these systems are involved in either inhibition of dominance-dependent agonism or facilitation of affiliation in same-sex bonds. In this study, we investigated the involvement of vasopressin systems in male-male bonds of large-billed crows (Corvus macrorhynchos). In their non-breeding aggregations, males form dominance ranks but also social bonds characterized by exchanging affiliative behaviors. We examined the effects of peripheral administration of V1aR antagonist (SR-49059; V1aRA) on social behavior between bonded males in comparison to between non-bonded males. After V1aRA injection to either a dominant or a subordinate of bonded (or non-bonded) males, we measured their social interactions for a 30-min trial in an aviary. Injection to a dominant or a subordinate was conducted in separate trials. It was found that V1aRA reduced affiliative behavior but increased dominance-dependent agonistic behavior between bonded males. V1aRA did not affect the behavior of non-bonded males. These results suggest the role of V1aR in the inhibition of agonistic behavior and the facilitation of affiliative behavior as a basis for male-male bonds.