On the basis of observational and experimental evidence, several authors have proposed that contagious yawn is linked to our capacity for empathy, thus presenting a powerful tool to explore the root of empathy in animal evolution. The evidence for the occurrence of contagious yawning and its link to empathy, however, is meagre outside primates and only recently domestic dogs have demonstrated this ability when exposed to human yawns. Since dogs are unusually skilful at reading human communicative behaviors, it is unclear whether this phenomenon is deeply rooted in the evolutionary history of mammals or evolved de novo in dogs as a result of domestication. Here we show that wolves are capable of yawn contagion, suggesting that such ability is a common ancestral trait shared by other mammalian taxa. Furthermore, the strength of the social bond between the model and the subject positively affected the frequency of contagious yawning, suggesting that in wolves the susceptibility of yawn contagion correlates with the level of emotional proximity. Moreover, female wolves showed a shorter reaction time than males when observing yawns of close associates, suggesting that females are more responsive to their social stimuli. These results are consistent with the claim that the mechanism underlying contagious yawning relates to the capacity for empathy and suggests that basic building blocks of empathy might be present in a wide range of species.
The neuropeptide oxytocin plays a central role in prosocial and parental behavior in non-human mammals as well as humans. It has been suggested that oxytocin may affect visual processing of infant faces and emotional reaction to infants. Healthy male volunteers (N = 13) were tested for their ability to detect infant or adult faces among adult or infant faces (facial visual search task). Urine samples were collected from all participants before the study to measure the concentration of oxytocin. Urinary oxytocin positively correlated with performance in the facial visual search task. However, task performance and its correlation with oxytocin concentration did not differ between infant faces and adult faces. Our data suggests that endogenous oxytocin is related to facial visual cognition, but does not promote infant-specific responses in unmarried men who are not fathers.
oxytocin; social cognition; infant; visual search; cognitive task
Evaluating the familiarity of faces is critical for social animals as it is the basis of individual recognition. In the present study, we examined how face familiarity is reflected in neural activities in our closest living relative, the chimpanzee. Skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of familiar and unfamiliar chimpanzee faces (Experiment 1) and human faces (Experiment 2). The ERPs evoked by chimpanzee faces differentiated unfamiliar individuals from familiar ones around midline areas centered on vertex sites at approximately 200 ms after the stimulus onset. In addition, the ERP response to the image of the subject’s own face did not significantly diverge from those evoked by familiar chimpanzees, suggesting that the subject’s brain at a minimum remembered the image of her own face. The ERPs evoked by human faces were not influenced by the familiarity of target individuals. These results indicate that chimpanzee neural representations are more sensitive to the familiarity of conspecific than allospecific faces.
Chimpanzee; Face recognition; Familiarity; Self recognition; Species effect; Memory; Comparative neuroscience; Social cognition; Event-related potentials
Atypical development of face processing is a major characteristic in autism spectrum disorder (ASD), which could be due to atypical interactions between subcortical and cortical face processing. The current study investigated the saccade planning towards faces in ASD. Seventeen children with ASD and 17 typically developing (TD) children observed a pair of upright or inverted face configurations flashed sequentially in two different spatial positions. The reactive saccades of participants were recorded by eye-tracking. The results did not provide evidence of overall impairment of subcortical route in ASD, However, the upright, but not the inverted, face configuration modulated the frequency of vector sum saccades (an index of subcortical control) in TD, but not in ASD. The current results suggests that children with ASD do not have overall impairment of the subcortital route, but the subcortical route may not be specialized to face processing.
autism spectrum disorder; face processing; subcortical route; superior colliculus; double saccade; eye tracking
By using the gap overlap task, we investigated disengagement from faces and objects in children (9-17 years old) with and without autism spectrum disorder (ASD) and its neurophysiological correlates. In typically developing (TD) children, faces elicited larger gap effect, an index of attentional engagement, and larger saccade-related event-related potentials (ERPs), compared to objects. In children with ASD, by contrast, neither gap effect nor ERPs differ between faces and objects. Follow-up experiments demonstrated that instructed fixation on the eyes induces larger gap effect for faces in children with ASD, whereas instructed fixation on the mouth can disrupt larger gap effect in TD children. These results suggest a critical role of eye fixation on attentional engagement to faces in both groups.
autism spectrum disorder; face; disengagement; saccade-related ERPs; gap overlap task
Many social animals have a species-specific repertoire of affiliative behaviours that characterise individualised relationships within a group. To date, however, quantitative studies on intragroup affiliative behaviours in social carnivores have been limited. Here, we investigated the social functions of the two most commonly observed affiliative behaviours in captive African lions (Panthera leo): head rubbing and licking. We conducted behavioural observations on a captive group of lions composed of 7 males and 14 females, and tested hypotheses regarding three social functions: tension reduction, social bonding, and social status expression. Disproportionately frequent male–male and female-to-male head rubbing was observed, while more than 95% of all licking interactions occurred in female–female dyads. In accordance with the social bond hypothesis, and in disagreement with the social status expression hypothesis, both head rubbing and licking interactions were reciprocal. After controlling for spatial association, the dyadic frequency of head rubbing was negatively correlated with age difference while licking was positively correlated with relatedness. Group reunion after daily separation did not affect the frequencies of the affiliative behaviours, which was in disagreement with the predictions from the tension reduction hypothesis. These results support the social bond hypothesis for the functions of head rubbing and licking. Different patterns of affiliative behaviour between the sexes may reflect differences in the relationship quality in each sex or the differential predisposition to licking due to its original function in offspring care.
Previous research has demonstrated that the way human adults look at others’ faces is modulated by their cultural background, but very little is known about how such a culture-specific pattern of face gaze develops. The current study investigated the role of cultural background on the development of face scanning in young children between the ages of 1 and 7 years, and its modulation by the eye gaze direction of the face. British and Japanese participants’ eye movements were recorded while they observed faces moving their eyes towards or away from the participants. British children fixated more on the mouth whereas Japanese children fixated more on the eyes, replicating the results with adult participants. No cultural differences were observed in the differential responses to direct and averted gaze. The results suggest that different patterns of face scanning exist between different cultures from the first years of life, but differential scanning of direct and averted gaze associated with different cultural norms develop later in life.
In humans, the susceptibility to yawn contagion has been theoretically and empirically related to our capacity for empathy. Because of its relevance to evolutionary biology, this phenomenon has been the focus of recent investigations in non-human species. In line with the empathic hypothesis, contagious yawning has been shown to correlate with the level of social attachment in several primate species. Domestic dogs (Canis familiaris) have also shown the ability to yawn contagiously. To date, however, the social modulation of dog contagious yawning has received contradictory support and alternative explanations (i.e., yawn as a mild distress response) could explain positive evidence. The present study aims to replicate contagious yawning in dogs and to discriminate between the two possible mediating mechanisms (i.e., empathic vs. distress related response). Twenty-five dogs observed familiar (dog’s owner) and unfamiliar human models (experimenter) acting out a yawn or control mouth movements. Concurrent physiological measures (heart rate) were additionally monitored for twenty-one of the subjects. The occurrence of yawn contagion was significantly higher during the yawning condition than during the control mouth movements. Furthermore, the dogs yawned more frequently when watching the familiar model than the unfamiliar one demonstrating that the contagiousness of yawning in dogs correlated with the level of emotional proximity. Moreover, subjects’ heart rate did not differ among conditions suggesting that the phenomenon of contagious yawning in dogs is unrelated to stressful events. Our findings are consistent with the view that contagious yawning is modulated by affective components of the behavior and may indicate that rudimentary forms of empathy could be present in domesticated dogs.
Most previous studies suggest diminished susceptibility to contagious yawning in children with autism spectrum disorder (ASD). However, it could be driven by their atypical attention to the face. To test this hypothesis, children with ASD and typically developing (TD) children were shown yawning and control movies. To ensure participants' attention to the face, an eye tracker controlled the onset of the yawning and control stimuli. Results demonstrated that both TD children and children with ASD yawned more frequently when they watched the yawning stimuli than the control stimuli. It is suggested therefore that the absence of contagious yawning in children with ASD, as reported in previous studies, might relate to their weaker tendency to spontaneously attend to others' faces.
The current study investigated the role of cultural norms on the development of face-scanning. British and Japanese adults’ eye movements were recorded while they observed avatar faces moving their mouth, and then their eyes toward or away from the participants. British participants fixated more on the mouth, which contrasts with Japanese participants fixating mainly on the eyes. Moreover, eye fixations of British participants were less affected by the gaze shift of the avatar than Japanese participants, who shifted their fixation to the corresponding direction of the avatar’s gaze. Results are consistent with the Western cultural norms that value the maintenance of eye contact, and the Eastern cultural norms that require flexible use of eye contact and gaze aversion.
cross-cultural study; eye contact; eye-tracking; face scanning; gaze processing
Eye contact has a fundamental role in human social interaction. The special appearance of the human eye (i.e., white sclera contrasted with a coloured iris) implies the importance of detecting another person's face through eye contact. Empirical studies have demonstrated that faces making eye contact are detected quickly and processed preferentially (i.e., the eye contact effect). Such sensitivity to eye contact seems to be innate and universal among humans; however, several studies suggest that cultural norms affect eye contact behaviours. For example, Japanese individuals exhibit less eye contact than do individuals from Western European or North American cultures. However, how culture modulates eye contact behaviour is unclear. The present study investigated cultural differences in autonomic correlates of attentional orienting (i.e., heart rate) and looking time. Additionally, we examined evaluative ratings of eye contact with another real person, displaying an emotionally neutral expression, between participants from Western European (Finnish) and East Asian (Japanese) cultures. Our results showed that eye contact elicited stronger heart rate deceleration responses (i.e., attentional orienting), shorter looking times, and higher ratings of subjective feelings of arousal as compared to averted gaze in both cultures. Instead, cultural differences in the eye contact effect were observed in various evaluative responses regarding the stimulus faces (e.g., facial emotion, approachability etc.). The rating results suggest that individuals from an East Asian culture perceive another's face as being angrier, unapproachable, and unpleasant when making eye contact as compared to individuals from a Western European culture. The rating results also revealed that gaze direction (direct vs. averted) could influence perceptions about another person's facial affect and disposition. These results suggest that cultural differences in eye contact behaviour emerge from differential display rules and cultural norms, as opposed to culture affecting eye contact behaviour directly at the physiological level.
Advancement of non-invasive brain imaging techniques has allowed us to examine details of neural activities involved in affective processing in humans; however, no comparative data are available for chimpanzees, the closest living relatives of humans. In the present study, we measured event-related brain potentials in a fully awake adult chimpanzee as she looked at affective and neutral pictures. The results revealed a differential brain potential appearing 210 ms after presentation of an affective picture, a pattern similar to that in humans. This suggests that at least a part of the affective process is similar between humans and chimpanzees. The results have implications for the evolutionary foundations of emotional phenomena, such as emotional contagion and empathy.
Languages, like genes, evolve by a process of descent with modification. This striking similarity between biological and linguistic evolution allows us to apply phylogenetic methods to explore how languages, as well as the people who speak them, are related to one another through evolutionary history. Language phylogenies constructed with lexical data have so far revealed population expansions of Austronesian, Indo-European and Bantu speakers. However, how robustly a phylogenetic approach can chart the history of language evolution and what language phylogenies reveal about human prehistory must be investigated more thoroughly on a global scale. Here we report a phylogeny of 59 Japonic languages and dialects. We used this phylogeny to estimate time depth of its root and compared it with the time suggested by an agricultural expansion scenario for Japanese origin. In agreement with the scenario, our results indicate that Japonic languages descended from a common ancestor approximately 2182 years ago. Together with archaeological and biological evidence, our results suggest that the first farmers of Japan had a profound impact on the origins of both people and languages. On a broader level, our results are consistent with a theory that agricultural expansion is the principal factor for shaping global linguistic diversity.
linguistic evolution; phylogenetics; Japonic languages
We tested for an association between variable number of tandem repeats in the canine androgen receptor (AR) gene and personality differences in Japanese Akita Inu dogs. The polymorphic trinucleotide (CAG) repeat region coding for glutamine in exon 1 of the AR gene was genotyped using genomic DNA obtained from 171 dogs. Three alleles (23, 24 and 26 repeats) were detected, and the allele frequency differed with the coat colour. We assessed the personality profiles of 100 fawn-coloured dogs (54 males and 46 females) based on a questionnaire answered by each dog's owner. The questionnaire consisted of five sub-scales (sociability, playfulness, neuroticism, aggressiveness, distractibility), and the psychometric properties were acceptable based upon internal consistency of the subscales. We found that male dogs with a short allele conferring increased AR function had higher aggressiveness scores than male dogs with longer alleles. By contrast, no evidence was found for a relationship between AR gene variants and personality in females. To our knowledge, our findings provide the first evidence of polymorphism in the AR gene being associated with canine aggression.
aggression; androgen receptor gene; dogs; gene polymorphisms; personality
Recent empirical evidence for complex cognition in elephants suggests that greater attention to comparative studies between non-human primates and other animals is warranted. We have previously shown that elephants possess the ability to judge the difference between two discrete quantities, and unlike other animals, their choice does not appear to be affected by distance or overall quantity. In this study, we investigated Asian elephants’ ability to perform summation, as exemplified by the ability to combine four quantities into two sums and subsequently compare them. We presented two discrete sums (3–7) to the elephants by baiting two buckets; they were loaded sequentially with two discrete quantities (1–5 pieces) of food per bucket. All three elephants selected the larger grand sum significantly more often than the smaller grand sum. Moreover, their performance was not affected by either distance to the bait or the overall quantity evaluated. Studies report that the performance of other animal species on similar tasks declines as distance to the bait decreases and as the overall quantities evaluated increase. These results suggest that the numerical cognition of Asian elephants may be different from that of other animals, but further study is required to elucidate the differences precisely.
numerical cognition; relative quantity judgment; summation; elephants
In all ages and countries, music and dance have constituted a central part in human culture and communication. Recently, vocal-learning animals such as parrots and elephants have been found to share rhythmic ability with humans. Thus, we investigated the rhythmic synchronization of budgerigars, a vocal-mimicking parrot species, under controlled conditions and a systematically designed experimental paradigm as a first step in understanding the evolution of musical entrainment. We trained eight budgerigars to perform isochronous tapping tasks in which they pecked a key to the rhythm of audio–visual metronome-like stimuli. The budgerigars showed evidence of entrainment to external stimuli over a wide range of tempos. They seemed to be inherently inclined to tap at fast tempos, which have a similar time scale to the rhythm of budgerigars' natural vocalizations. We suggest that vocal learning might have contributed to their performance, which resembled that of humans.
The brain activity of a fully awake chimpanzee being presented with her name was investigated. Event-related potentials (ERPs) were measured for each of the following auditory stimuli: the vocal sound of the subject's own name (SON), the vocal sound of a familiar name of another group member, the vocal sound of an unfamiliar name and a non-vocal sound. Some differences in ERP waveforms were detected between kinds of stimuli at latencies at which P3 and Nc components are typically observed in humans. Following stimulus onset, an Nc-like negative shift at approximately 500 ms latency was observed, particularly in response to SON. Such specific ERP patterns suggest that the chimpanzee processes her name differently from other sounds.
ERPs; auditory processing; name; self; awake chimpanzee
The sound of one's own name is one of the most salient auditory environmental stimuli. Several studies of human brain potentials have revealed some characteristic waveforms when we hear our own names. In a recent work, we investigated event-related potentials (ERPs) in a female chimpanzee and demonstrated that the ERP pattern generated when she heard her own name differed from that generated when she heard other sounds. However, her ERPs did not exhibit a prominent positive shift around 300 ms (P3) in response to her own name, as has been repeatedly shown in studies of human ERPs. The present study collected comparative data for adult humans using basically the same procedure as that used in our previous study of the chimpanzee. These results also revealed no prominent P3 to the human subjects' own names. The lack of increased P3 is therefore likely due to our experimental protocol, in which we presented the subject's own name relatively frequently. In contrast, our results revealed prominent negativity to the subject's own name at around 500 ms in the chimpanzee and around 200 ms in human subjects. This may indicate that initial orientation to the sound of one's own name is delayed in the chimpanzee.
auditory processing; ERP; chimpanzee; name; self
The neural system of our closest living relative, the chimpanzee, is a topic of increasing research interest. However, electrophysiological examinations of neural activity during visual processing in awake chimpanzees are currently lacking.
In the present report, skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of faces and objects in two experiments. In Experiment 1, human faces and stimuli composed of scrambled face images were displayed. In Experiment 2, three types of pictures (faces, flowers, and cars) were presented. The waveforms evoked by face stimuli were distinguished from other stimulus types, as reflected by an enhanced early positivity appearing before 200 ms post stimulus, and an enhanced late negativity after 200 ms, around posterior and occipito-temporal sites. Face-sensitive activity was clearly observed in both experiments. However, in contrast to the robustly observed face-evoked N170 component in humans, we found that faces did not elicit a peak in the latency range of 150–200 ms in either experiment.
Although this pilot study examined a single subject and requires further examination, the observed scalp voltage patterns suggest that selective processing of faces in the chimpanzee brain can be detected by recording surface ERPs. In addition, this non-invasive method for examining an awake chimpanzee can be used to extend our knowledge of the characteristics of visual cognition in other primate species.
The present study explores to what extent Asian elephants show “means–end” behavior. We used captive Asian elephants (N = 2) to conduct four variations of the Piagetian “support” problem, which involves a goal object that is out of reach, but rests on a support within reach. In the first condition, elephants were simultaneously presented with two identical trays serving as the “support”, with the bait on one tray and the other tray left empty. In the next two conditions, the bait was placed on one tray, while additional bait was placed beside the other tray. In the last condition, both trays contained bait, but one of the trays had a small gap which prevented the elephants from reaching the reward. Subjects were required to choose and pull either tray with their trunk and to obtain the bait (i.e. goal). Results showed that one elephant performed all of the support problems significantly above chance after several sessions, suggesting that the elephant was capable of understanding that pulling the tray was the “means” for achieving the “end” of obtaining the bait. This study showed that elephants show means–end behavior when subjected to a Piagetian “support” task, and indicates that such goal-directed behavior occurs in species other than primates.
Asian elephant; Piaget; Means–end problem
This study is the first to report the disturbance of contagious yawning in individuals with autism spectrum disorder (ASD). Twenty-four children with ASD as well as 25 age-matched typically developing (TD) children observed video clips of either yawning or control mouth movements. Yawning video clips elicited more yawns in TD children than in children with ASD, but the frequency of yawns did not differ between groups when they observed control video clips. Moreover, TD children yawned more during or after the yawn video clips than the control video clips, but the type of video clips did not affect the amount of yawning in children with ASD. Current results suggest that contagious yawning is impaired in ASD, which may relate to their impairment in empathy. It supports the claim that contagious yawning is based on the capacity for empathy.
yawning; contagious yawning; autism spectrum disorder; empathy; neuropathology
For decades, the chimpanzee, phylogenetically closest to humans, has been analyzed intensively in comparative cognitive studies. Other than the accumulation of behavioral data, the neural basis for cognitive processing in the chimpanzee remains to be clarified. To increase our knowledge on the evolutionary and neural basis of human cognition, comparative neurophysiological studies exploring endogenous neural activities in the awake state are needed. However, to date, such studies have rarely been reported in non-human hominid species, due to the practical difficulties in conducting non-invasive measurements on awake individuals.
We measured auditory event-related potentials (ERPs) of a fully awake chimpanzee, with reference to a well-documented component of human studies, namely mismatch negativity (MMN). In response to infrequent, deviant tones that were delivered in a uniform sound stream, a comparable ERP component could be detected as negative deflections in early latencies.
The present study reports the MMN-like component in a chimpanzee for the first time. In human studies, various ERP components, including MMN, are well-documented indicators of cognitive and neural processing. The results of the present study validate the use of non-invasive ERP measurements for studies on cognitive and neural processing in chimpanzees, and open the way for future studies comparing endogenous neural activities between humans and chimpanzees. This signifies an essential step in hominid cognitive neurosciences.
Hyperbolic discounting of delayed and probabilistic outcomes has drawn attention in psychopharmacology and neuroeconomics. Sozou's evolutionary theory proposed that hyperbolic delay discounting may be totally attributable to aversion to a decrease in subjective probability of obtaining delayed rewards (SP) which follows a hyperbolic decay function. However, to date, no empirical study examined the hypothesis, although this investigation is important for elucidating the roles of impatience, precaution, and uncertainty aversion in delay discounting processes.
In order to (i) determine the functional form of the relation between delay until receipt and SP, and (ii) examine whether delay discounting is attributable to a decrease in SP, we assessed the subjects' SP and their delay and probability discounting. We examined the fitness of hyperbolic and exponential functions to the assessed SP, and relations between the SP, and delay/probability discounting, and subjective-probability discounting for delayed rewards.
The results demonstrated (a) SP decayed hyperbolically as delay increases, (b) a decay of SP was associated with delay discounting, and (c) subjective-probability discounting did not significantly correlate with delay discounting.
Our results demonstrated (i) hyperbolic decay of SP is related to delay discounting, and (ii) delay discounting is, however, not attributable to precautious foresight in intertemporal choice. Further, a novel parameter of pure time preference is proposed.