Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal

mystery of yawning 



haut de page













mise à jour du
27 mars 2016
Proc Natl Acad Sci
Bonobos (Pan paniscus) show an attentional bias
toward conspecifics' emotions
Mariska E. Kreta, Linda Jaasmab,
Thomas Biondac, Jasper G. Wijnend


 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
Bonobos respond prosocially toward members of other groups. Tan J, Ariely D, Hare B.
Applying well-established psychological paradigms to our closest relatives represents a promising approach for providing insight into similarities and differences between humans and apes. Numerous articles have been published on the dot-probe task, showing that humans have an attentional bias toward emotions, especially when threatening. For social species like primates, efficiently responding to others' emotions has great survival value. Observational research has shown that, compared with humans and chimpanzees, bonobos excel in regulating their own and others' emotions, thereby preventing conflicts from escalating. The present study is an initial effort to apply a psychological test to the bonobo, and demonstrates that they, like humans, have heightened attention to emotional - compared with neutral - conspecifics, but are mostly drawn.
In social animals, the fast detection of group members' emotional expressions promotes swift and adequate responses, which is crucial for the maintenance of social bonds and ultimately for group survival. The dot-probe task is a well-established paradigm in psychology, measuring emotional attention through reaction times. Humans tend to be biased toward emotional images, especially when the emotion is of a threatening nature. Bonobos have rich, social emotional lives and are known for their soft and friendly character. In the present study, we investigated (i) whether bonobos, similar to humans, have an attentional bias toward emotional scenes compared with conspecifics showing a neutral expression, and (ii) which emotional behaviors attract their attention the most. As predicted, results consistently showed that bonobos' attention was biased toward the location of the emotional versus neutral scene. Interestingly, their attention was grabbed most by images showing conspecifics such as sexual behavior, yawning, or grooming, and not as much&emdash;as is often observed in humans&emdash;by signs of distress or aggression. The results suggest that protective and affiliative behaviors are pivotal in bonobo society and therefore attract immediate attention in this species.

Efficiently responding to others' emotions has great survival value, especially for social species, such as primates, who establish close, long-term bonds with group members (1-3). Previous research in humans has shown that one component of this strong sensitivity to others' emotions is heightened attention to their affective states (4-6). Together with the chimpanzee, the bonobo is the closest living relative of humans. Studying components of their emotional behavior, such as emotional attention, may help us not only to understand this rarely studied species better, but also provide insight into (human) emotions and their evolutionary past (7-9). In the present study, we investigated whether bonobos, like humans, show increased attention to scenes depicting conspecifics showing an emotion or are involved in emotion regulatory behaviors, compared with scenes where conspecifics are in a neutral state.
In natural environments, attention is preferentially sustained by stimuli that have affective significance, in contrast to routine, emotionally neutral events (6, 10). This attentional bias reflects a functional mechanism where fast and automatic attention allocation to emotional information can aid humans in threatening situations by fostering fast actions (11, 12).
Experimentally, this has, for example, been demonstrated with the dot-probe task. Previous dot-probe studies have shown that emotional signals induce a bias in spatial attention, in that participants respond faster to a presented dot (the target, henceforth, "probe") when it appears at the location of a previously presented emotion compared with neutral stimulus (13-17). Although in humans a bias toward threatening compared with neutral stimuli is most commonly observed, some studies also report increased attention toward positive versus neutral stimuli (18-21). Other research has shown that there are marked individual differences in biases and that these are, for example, modulated by mood (22, 23). From an evolutionary perspective, it is most adaptive to be able to quickly attend to relevant stimuli, whether those are threats in the environment or an affiliative signal from an individual who could provide support and care (24, 25).
Most primates spend their lives in social groups. To prevent conflicts, they keep close track of others' behaviors, emotions, and social debts. For example, chimpanzees remember who groomed whom for long periods of time (26). In the chimpanzee, but also in the rarely studied bonobo, grooming is a major social activity and a means by which animals living in proximity may bond and reinforce social structures. It is also used as a form of reconciliation and a means of conflict resolution. Despite their general similarities and close phylogenetic relationship, bonobos, chimpanzees, and humans show clear differences in their social behavior. Although chimpanzee and human societies are dominated by males and encounters between different groups frequently result in violence and sometimes the killing of conspecifics (27-29), bonobo society is controlled by females and aggression is usually prevented through nonconceptive sexual behavior, grooming, and play (30-33). Compared with chimpanzees, bonobos live in more predictable environments with low seasonality and stable food availability, which is why they have a lower degree of fission-fusion and which, next to the peace-keeping role of the females, may also explain the lower rates of competition (31).
Bonobos have rich personalities and share most of their traits with humans and chimpanzees, suggesting these were also present in their common ancestor (34). From early age on, bonobos are sensitive to others' emotions, which is demonstrated by their ability to provide appropriate consolatory behaviors after conflicts (35), a skill individuals with more effective self-regulation capabilities excel in particularly (35), but which is also demonstrated by more automatic behavior, including yawn contagion, an index of empathy (36, 37).
Bonobos' personality characteristics and complex social emotional behavior have rarely been studied experimentally, but the conclusions that can be drawn from the few studies available are in line with the conclusions from observational research, described above. It has for example been demonstrated that great apes, bonobos included, can reliably recognize human emotions (38) and experiments with chimpanzees show that they are also sensitive to the emotions of conspecifics (39-42). By using an experimental cofeeding set-up, it has been shown that bonobos are more tolerant than chimpanzees (43; but see ref. 44). In addition, an eye-tracking study demonstrated that bonobos make more eye contact than chimpanzees (45). Finally, in a risky decision game, bonobos showed more risk-aversion than chimpanzees (46, 47).
The present study investigates emotional attention in the bonobo. [Although the usage of the adjective "emotion" is debated when it concerns animals, this term is used in dot-probe studies in humans. To be able to portray commonalities and differences with the human literature, we feel that using the same adjective is appropriate. We are also aware that at this point we cannot tell what bonobo-emotions are, and we therefore have to rely on observational work and on research into human and chimpanzee expressions. The term "emotional attention" is therefore used when attention is directed toward an emotional expression, but also when directed toward scenes showing emotion regulatory behaviors (Methods).] For this purpose, four bonobos completed a dot-probe task during which emotional and neutral pictures of unfamiliar bonobos and control animals were being presented on a touch-screen (Fig. 1). Per individual, the task was spread out over 13 sessions with 25 trials each (Methods and Table S1). Given their highly social nature, we predicted that bonobos would show heightened attention toward the pictures showing emotional compared with neutral bonobos. In addition, as bonobos are known to be less aggressive than chimpanzees and humans, and spend a lot of time on positive social behaviors&emdash;such as play, sex, and grooming&emdash;we predicted seeing this reflected in a specific attentional bias toward these more affiliative or protective behaviors than to signals of distress.
Bonobos spend their lives in large social groups and for their survival have to rely on that group and its members. Observational research has shown that bonobos are very social and can adequately regulate their own and group members' emotions, thereby often preventing conflicts from arising or solving them quickly. The present study is, to our knowledge, the first to experimentally demonstrate that bonobos, like humans, have heightened attention for emotional compared with neutral signals of conspecifics. With aid of the dot-probe task, a paradigm designed for testing attentional biases in humans, we here demonstrate that bonobos have an attentional bias toward the emotions of others. Most interestingly, bonobos were particularly drawn toward scenes showing other bonobos that were yawning, mating, or grooming, but not toward scenes depicting distressed bonobos, bonobos pant-hooting, playing, or handling food compared with neutral scenes. In addition to an attentional bias towards emotions, Kumbuka showed more nose wipes - a behavior indicating edginess, motivational ambivalence, or frustration (48, 49) - on trials where the probe was located on the side of the emotional compared with the neutral picture. We will now discuss the most attended emotional behaviors in more detail, and the putative drivers of their saliency.
The bonobos that were tested in the present study showed the strongest attentional bias toward pictures of yawning bonobos. Yawning is an evolutionarily old behavior that is widespread among vertebrates. Although there is a scientific debate about the exact function, different studies have demonstrated a social signaling function. There is convincing evidence that yawning serves a thermoregulatory function (i.e., it cools the brain back to homeostasis). It is thought that by cooling the brain, yawning induces vigilance, which is why it is evolutionary adaptive for the whole group to pick up or mimic this behavior (50). Yawning indeed is very contagious in many social species, including bonobos, and its effect is even stronger when the observed yawners are kin or friends or of higher rank (36, 37, 51). Research has shown the involvement of the mirror neuron system during contagious yawning and supports the premise of a connection between this system and higher cognitive empathic functions, including mentalizing. Hence, it has been suggested that contagious yawning is based on a functional substrate of empathy (52).
It is possible that as a sign of threat, bonobos' attention was caught by the display of canines (which are less impressive compared with the chimpanzee). However, after close inspection of the different pictures and their associated reaction times, we can conclude that this is unlikely. First, the pictures where the canines were most visible did not attract more attention than the pictures where they were less visible. Second, the canines were also visible during fear grimaces, which did not attract attention more than did neutral images.
Touch is a powerful tool for communicating positive emotions. Human and nonhuman primates use social touch for maintenance and reinforcement of social structures (53). Most primate species communicate affection and reduce group tension by means of so-called grooming, the act of tidying or cleaning one another's body or appearance. Grooming is regarded as a service given by one individual that confers benefits to the recipient in terms of hygiene and has possible calming effects (54). Grooming is a recipe for social support and releases oxytocin in both the groomer and groomed (55). Bonobos keep close track of who groomed whom, reciprocate grooming, and distribute their grooming according to the rank of the receivers (56). Given that grooming plays such a prominent role in bonobo society, it is not surprising that their attention was drawn toward scenes showing this behavior.
The third category that attracted bonobos' attention were pictures showing scenes with bonobos involved in sexual behavior. In humans, sexual frequency has been found to be a strong positive predictor of general wellbeing and of the quality of the social relationship (57). Sexual activity plays an even bigger role in bonobo society. In bonobos, sex is being used as a form of greeting, a means of forming social bonds, conflict resolution, and postconflict reconciliation. Bonobos are the only nonhuman animal to have been observed engaging in face-to-face genital sex, tongue kissing, and oral sex (58). Bonobos do not form permanent monogamous sexual relationships with individual partners and do not discriminate in their sexual behavior by sex or age (with the possible exception of abstaining from sexual activity between mothers and their adult sons). When bonobos find a new food source or feeding ground, the increased excitement will usually lead to communal sexual activity, presumably decreasing tension and encouraging peaceful feeding (58). The attentional bias for sexual images as observed in our study reflects the high frequency and importance of this behavior in their daily lives.
Despite their great genetic similarity, bonobos' behavior is strikingly different from that of chimpanzees. Whereas males are the dominant sex in the chimpanzee, bonobo society is female-dominant. Remarkably, like humans, chimpanzees make war with rivaling groups and do not take kindly to strangers. In stark contrast, bonobos live in friendly and tolerant societies and, although they sometimes hunt smaller animals for consumption, never kill one of their own (9, 31, 32). Intriguingly, bonobos prefer to share food and mate with strangers than with acquaintances (33). The social and emotional differences between the two species of Pan are reflected in the anatomy of the brain. A neuroimaging study comparing both species showed that bonobos not only have more gray matter in the amygdala and insula, regions involved in perceiving emotions in self and others, they also have a larger pathway linking the amygdala with the anterior cingulate cortex, which is implicated in top-down control of aggressive impulses (59). The results are in line with earlier work showing that bonobos have more Von Economo neurons, which are involved in social cognition, in the anterior cingulate cortex than chimpanzees, and showed a pattern that closely resembled that seen in humans (59_-61).
The present study showed that bonobos have heightened attention toward conspecifics' yawns, grooming, and sexual behaviors. Based on the results of the present study, can these behaviors be interpreted as emotional behaviors? Heightened attention as measured via shorter reaction times in the dot-probe task has in the human literature been widely interpreted as an emotional bias. Can we then draw the same conclusion for bonobos? For the following reasons, we indeed think we can. First, reaction times of all four subjects reflected an attentional bias toward conspecifics' emotional behaviors. Second, the scenes that were rated by four experts as being emotionally intense for bonobos, especially grabbed bonobo's attention most. Third, one subject showed more nose wipes following trials where she had to approach emotional compared with neutral scenes. A nose wipe is considered a sign of edginess, motivational ambivalence, or frustration (48, 49).
To conclude, bonobos' attention is quickly captured by the emotional expressions of others. Interestingly, this attentional bias was strongest for affiliative behaviors (grooming and mating) and behaviors that are highly contagious (yawning) and not significant for scenes depicting distress. The results suggest that protective and affiliative behaviors are pivotal in bonobo society and therefore prioritized.
Darwin CR (1872) The Expression of the Emotions in Man and Animals (John Murray, London)
Spoor JR, Kelly JR (2004) The evolutionary significance of affect in groups: Communication and group bonding. Group Process Intergroup Relat 7(4):398-412
de Waal FB (2008) Putting the altruism back into altruism: The evolution of empathy. Annu Rev Psychol 59:279-300
Phelps EA, Ling S, Carrasco M (2006) Emotion facilitates perception and potentiates the perceptual benefits of attention. Psychol Sci 17(4):292-299
Schupp HT, Junghöfer M, Weike AI, Hamm AO (2003) Attention and emotion: An ERP analysis of facilitated emotional stimulus processing. Neuroreport 14(8):1107-1110
Vuilleumier P (2005) How brains beware: Neural mechanisms of emotional attention. Trends Cogn Sci 9(12):585-594
Panksepp J (1998) Affective Neuroscience: The Foundation of Human and Animal Emotions (Oxford Univ Press, New
Anderson DJ, Adolphs R (2014) A framework for studying emotions across species. Cell 157(1):187-200
de Waal FBM (2014) The Bonobo and the Atheist: In Search of Humanism Among the Primates (Norton & Company, New York)
Lang PJ, Bradley MM, Cuthbert BN (1998) Emotion, motivation, and anxiety: Brain mechanisms and psychophysiology. Biol Psychiatry 44(12):1248-1263
Frijda NH (2010) Impulsive action and motivation. Biol Psychol 84(3):570-579
LeDoux JE (1995) Emotion: Clues from the brain. Annu Rev Psychol 46:209-235
Williams JM, Mathews A, MacLeod C (1996) The emotional Stroop task and psychopathology. Psychol Bull 120(1):3-24
Bradley B, et al. (1997) Attentional biases for emotional faces. Cogn Emotion 11(1):25-42
Carlson JM, Reinke KS (2008) Masked fearful faces modulate the orienting of covert spatial attention. Emotion 8(4):522-529
Holmes A, Green S, Vuilleumier P (2005) The involvement of distinct visual channels in rapid attention towards fearful facial expressions. Cogn Emotion 19(6):899-922
de Valk JM, Wijnen JG, Kret ME (2015) Anger fosters action. Fast responses in a motor task involving approach movements toward angry faces and bodies. Front Psychol 6:1240
Vuilleumier P, Schwartz S (2001) Emotional facial expressions capture attention. Neurology 56(2):153-158
Tamietto M, et al. (2005) Effects of emotional face cueing on line bisection in neglect: A single case study. Neurocase 11(6):399-404
Williams MA, Mattingley JB (2004) Unconscious perception of non-threatening facial emotion in parietal extinction. Exp Brain Res 154(4):403-406
Flaisch T, Schupp HT, Renner B, Junghöfer M (2009) Neural systems of visual attention responding to emotional gestures. Neuroimage 45(4):1339-1346
Rowe G, Hirsh JB, Anderson AK (2007) Positive affect increases the breadth of attentional selection. Proc Natl Acad Sci USA 104(1):383-388
Derryberry D, Tucker DM (1994) in The Heart's Eye: Emotional Influences in Perception and Attention, eds Niedenthal PM, Kitayama S (Academic, San Diego), pp 167-196
Todd RM, Cunningham WA, Anderson AK, Thompson E (2012) Affect-biased attention as emotion regulation. Trends Cogn Sci 16(7):365-372
Anderson BA, Laurent PA, Yantis S (2011) Value-driven attentional capture. Proc Natl Acad Sci USA 108(25):10367-10371
Gomes CM, Mundry R, Boesch C (2009) Long-term reciprocation of grooming in wild West African chimpanzees. Proc Biol Sci 276(1657):699-706
Wilson ML, et al. (2014) Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature
Mitani JC, Watts DP, Amsler SJ (2010) Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr Biol 20(12):R507-R508
Bingham PM (2000) Human evolution and human history: A complete theory. Evol Anthropol 9(6):248-257
de Waal FBM (1990) Sociosexual behavior used for tension regulation in all age and sex combinations among bonobos. Pedophilia, ed Fierman JR (Springer, New York), pp 378-393
Furuichi T (2011) Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20(4):131-142
Hare B, Wobber V, Wrangham R (2012) The self-domestication hypothesis: Evolution of bonobo psychology is due to selection against aggression. Anim Behav 83(3):573-585
Tan J, Hare B (2013) Bonobos share with strangers. PLoS One 8(1):e51922
Weiss A, et al. (2015) Personality in bonobos. Psychol Sci 26(9):1430-1439
Clay Z, de Waal FB (2013) Bonobos respond to distress in others: Consolation across the age spectrum. PLoS One 8(1):e55206
Palagi E, Norscia I, Demuru E (2014) Yawn contagion in humans and bonobos: Emotional affinity matters more than species. PeerJ 2:e519
Demuru E, Palagi E (2012) In bonobos yawn contagion is higher among kin and friends. PLoS One 7(11):e49613
Buttelmann D, Call J, Tomasello M (2009) Do great apes use emotional expressions to infer desires? Dev Sci 12(5):688-698
Kret ME, Tomonaga M, Matsuzawa T (2014) Chimpanzees and humans mimic pupil-size of conspecifics. PLoS One 9(8):e104886
Izumi A, Kojima S (2004) Matching vocalizations to vocalizing faces in a chimpanzee (Pan troglodytes). Anim Cogn 7(3):179-184
Parr LA (2003) The discrimination of faces and their emotional content by chimpanzees (Pan troglodytes). Ann N Y Acad Sci 1000:56-78
Kano F, Tanaka M, Tomonaga M (2008) Enhanced recognition of emotional stimuli in the chimpanzee (Pan troglodytes). Anim Cogn 11(3):517-524
Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17(7):619-623
Herrmann E, Tomasello M (2006) Apes' and children's understanding of cooperative and competitive motives in a communicative situation. Dev Sci 9(5):518-529
Adachi I, Kuwahata H, Fujita K, Tomonaga M, Matsuzawa T (2009) Plasticity of ability to form cross-modal representations in infant Japanese macaques. Dev Sci 12(3):446-452
Haun DB, Nawroth C, Call J (2011) Great apes' risk-taking strategies in a decision making task. PLoS One 6(12):e28801
Rosati AG, Hare B (2013) Chimpanzees and bonobos exhibit emotional responses to decision outcomes. PLoS One 8(5):e63058
Aureli F, de Waal FB (1997) Inhibition of social behavior in chimpanzees under high-density conditions. Am J Primatol 41(3):213-228
Leavens DA, Aureli F, Hopkins WD (2004) Behavioral evidence for the cutaneous expression of emotion in a chimpanzee
Gallup AC (2011) Why do we yawn? Primitive versus derived features. Neurosci Biobehav Rev 35(3):765-769
Massen JJM, Vermunt DA, Sterck EHM (2012) Male yawning is more contagious than female yawning among chimpanzees (Pan troglodytes). PLoS One 7(7):e40697
Haker H, Kawohl W, Herwig U, Rössler W (2013) Mirror neuron activity during contagious yawning&emdash;An fMRI study. Brain Imaging Behav 7(1):28-34
Suvilehto JT, Glerean E, Dunbar RIM, Hari R, Nummenmaa L (2015) Topography of social touching depends on emotional bonds between humans. Proc Natl Acad Sci USA 112(45):13811-13816
de Waal FB (1997) The Chimpanzee's service economy: Food for grooming. Evol Hum Behav 18(6):375-386
Crockford C, et al. (2013) Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proc Biol Sci 280(1755):20122765
Vervaecke H, de Vries H, van Elsacker L (2000) The pivotal role of rank in grooming and support behavior in a captive group of bonobos (Pan paniscus). Behaviour 137(11):1463-1485
Heiman JR, et al. (2011) Sexual satisfaction and relationship happiness in midlife and older couples in five countries. Arch Sex Behav 40(4):741-753
Manson JH, Perry S, Parish AR (1997) Nonconceptive sexual behavior in bonobos and capuchins. Int J Primatol 18(5):767-786
Rilling JK, et al. (2011) Differences between chimpanzees and bonobos in neural systems supporting social cognition. Soc Cogn Affect Neurosci 7(4):369-379
Nimchinsky EA, et al. (1999) A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 96(9):5268-5273
Parr LA, Waller BM, Fugate J (2005) Emotional communication in primates: implications for neurobiology. Curr Opin Neurobiol 15(6):716-720