Divergent effects of oxytocin on eye contact in bonobos and chimpanzees

Brooks, James; Kano, Fumihiro; Sato, Yutaro; Yeow, Hanling; Morimura, Naruki; Nagasawa, Miho; Kikusui, Takefumi; Yamamoto, Shinya

doi:10.1016/j.psyneuen.2020.105119

Cited by 34 publications

(43 citation statements)

References 73 publications

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“…In a comparative study, individual differences in RJA that were observed in male chimpanzees were associated with the DupB+_ DupB −/− polymorphism of the AVPR1A arginine vasopressin receptor gene ( 255 ). Additionally, the intranasal administration of oxytocin increased eye contact in bonobos, but decreased it in chimpanzees ( 256 ). These findings suggest that comparative primate studies provide important animal models for developmental research on the mechanism processes involved in social attention symptoms in ASD ( 250 ).…”

Section: The Neurogenetics Of Social Attentionmentioning

confidence: 99%

The Bidirectional Social-Cognitive Mechanisms of the Social-Attention Symptoms of Autism

Mundy

Bullen

2022

Front. Psychiatry

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Differences in social attention development begin to be apparent in the 6th to 12th month of development in children with Autism Spectrum Disorder (ASD) and theoretically reflect important elements of its neurodevelopmental endophenotype. This paper examines alternative conceptual views of these early social attention symptoms and hypotheses about the mechanisms involved in their development. One model emphasizes mechanism involved in the spontaneous allocation of attention to faces, or social orienting. Alternatively, another model emphasizes mechanisms involved in the coordination of attention with other people, or joint attention, and the socially bi-directional nature of its development. This model raises the possibility that atypical responses of children to the attention or the gaze of a social partner directed toward themselves may be as important in the development of social attention symptoms as differences in the development of social orienting. Another model holds that symptoms of social attention may be important to early development, but may not impact older individuals with ASD. The alterative model is that the social attention symptoms in infancy (social orienting and joint attention), and social cognitive symptoms in childhood and adulthood share common neurodevelopmental substrates. Therefore, differences in early social attention and later social cognition constitute a developmentally continuous axis of symptom presentation in ASD. However, symptoms in older individuals may be best measured with in vivo measures of efficiency of social attention and social cognition in social interactions rather than the accuracy of response on analog tests used in measures with younger children. Finally, a third model suggests that the social attention symptoms may not truly be a symptom of ASD. Rather, they may be best conceptualized as stemming from differences domain general attention and motivation mechanisms. The alternative argued for here that infant social attention symptoms meet all the criteria of a unique dimension of the phenotype of ASD and the bi-directional phenomena involved in social attention cannot be fully explained in terms of domain general aspects of attention development.

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Section: The Neurogenetics Of Social Attentionmentioning

confidence: 99%

The Bidirectional Social-Cognitive Mechanisms of the Social-Attention Symptoms of Autism

Mundy

Bullen

2022

Front. Psychiatry

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“…We carefully considered the safety of the oxytocin administration as in previous studies. Again, we based this decision on the fact that 1) oxytocin is often administered to human children and adults, 2) oxytocin is active for only a short period of time following administration, 3) oxytocin is naturally produced in bonobos and chimpanzees following relevant behaviors [7,8] , and 4) no previous studies administering oxytocin intranasally to chimpanzees or bonobos reported any agonistic interaction [24][25][26]. All female bonobos were taking birth control and thus no bonobos were pregnant at any time during the course of this experiment.…”

Section: Methodsmentioning

confidence: 99%

“…Given recent progresses in this line of research, it is worthwhile to test whether oxytocin promotes key social behaviours related to social bonding in Pan , particularly in bonobos using the updated methods of oxytocin administration. Therefore, this study administered nebulized oxytocin or saline placebo to a whole group of female bonobos following the methods employed in Brooks et al [26] and subsequently observed the change in their gross interactive behavior, including grooming and GG-rubbing, as well as other noninteractive behaviours during their free interaction. As mentioned, the biobehavioural feedback loop hypothesis suggests that an oxytocin positive feedback loop has evolved to support Pan social bonding, and in particular we predicted that oxytocin would promote social grooming, which is known to be released through social grooming in wild chimpanzees [7].…”

Section: Introductionmentioning

confidence: 99%

Testing the effect of oxytocin on social grooming in bonobos

Brooks

Kano

Yeow

et al. 2021

Preprint

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Oxytocin has attracted research attention due to its role in promoting social bonding. One notable recent hypothesis is the biobehavioral feedback loop, which posits that the oxytocin system has evolved to support the formation and maintenance of social bonds through a positive feedback loop, where oxytocin promotes social behaviours which then cause oxytocin release themselves. In the two Pan species, humans’ closest relatives, oxytocin is known to be released following key behaviours related to social bonding, such as social grooming in chimpanzees and female-female sexual behaviour in bonobos. However, no experimental evidence has demonstrated that oxytocin promotes such socio-positive behaviours. To test this, we administered nebulized oxytocin or saline placebo to a group of female bonobos and subsequently observed the change in their gross behavior during free interaction. We found that bonobos groomed other group members significantly more frequently in the oxytocin compared to placebo condition. Other behavioural measures did not largely differ between conditions, except for a nonsignificant trend for reduction in abnormal regurgitation/reingestion behaviour. Overall, we found that oxytocin promoted socio-positive interaction in bonobos, providing support for the biobehavioural feedback loop hypothesis of oxytocin in bonobo social evolution.

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“…For example, research has revealed genetic variants that affect cooperative social behaviors in dogs, and administration of exogenous oxytocin also enhances these behaviors (Persson et al, 2017). Recent research on the effects of exogenous administration of oxytocin in great apes suggests that oxytocin may facilitate social interaction more in bonobos than chimpanzees (Brooks et al, 2021). A large body of experimental work has demonstrated that oxytocin strongly influences various aspects of social and cooperative behavior in humans including trust of others and cooperation in economic games (e.g., Neto et al, 2020; Theodoridou et al, 2009).…”

Section: Purpose Of the Studymentioning

confidence: 99%

Concordant evidence for positive selection on genes related to self-domestication in bonobos and early humans.

Summers¹

2023

Evolutionary Behavioral Sciences

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The domestication syndrome refers to a suite of traits characteristic of domesticated animals, including neotenic aspects of morphology and behavior, increased docility, and reduced reactive aggression. The term self-domestication refers to a process governed by social selection against reactive aggression within species, with effects parallel to those of selection for tameness. There are several recent hypotheses concerning the mechanisms of human self-domestication. It has also recently been hypothesized that bonobos have undergone a process of self-domestication after diverging from their common ancestor with chimpanzees. Here we investigate independent patterns of selection on bonobos (relative to chimpanzees) and humans (relative to Neanderthals) in genes associated with domestication in previous research. We used the Great Apes selection browser and the Neanderthal-human selection browser (in the UCSC Genome Browser) to compare concordant patterns of selection (at the level of gene region and peak selection regions), in a set of 9 genes, to 50 genes found to be under positive selection in bonobos in a prior survey. In terms of concordance, we found that the vasopressin receptor, avpr1b, was ranked first in the peak region and second in the gene region, the oxytocin receptor, oxtr, was ranked second in peak region and sixth in gene region, the serotonin receptor, htr1f, was ranked third in gene region, and the gtf2i gene was found to be ranked ninth for peak region. We argue that our results provide preliminary molecular evolutionary support for parallel patterns of positive selection on genes associated with self-domestication in bonobos and humans.

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Divergent effects of oxytocin on eye contact in bonobos and chimpanzees

Cited by 34 publications

References 73 publications

The Bidirectional Social-Cognitive Mechanisms of the Social-Attention Symptoms of Autism

The Bidirectional Social-Cognitive Mechanisms of the Social-Attention Symptoms of Autism

Testing the effect of oxytocin on social grooming in bonobos

Concordant evidence for positive selection on genes related to self-domestication in bonobos and early humans.

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