Pier Francesco Ferrari

Re-examination of Oostenbroek et al. (2016): evidence for neonatal imitation of tongue protrusion

The meaning, mechanism, and function of imitation in early infancy have been actively discussed since Meltzoff and Moores (1977) report of facial and manual imitation by human neonates. Oostenbroek etxa0al. (2016) claim to challenge the existence of early imitation and to counter all interpretations so far offered. Such claims, if true, would have implications for theories of social-cognitive development. Here we identify 11 flaws in Oostenbroek etxa0al.s experimental design that biased the results toward null effects. We requested and obtained the authors raw data. Contrary to the authors conclusions, new analyses reveal significant tongue-protrusion imitation at all four ages tested (1, 3, 6, and 9 weeks old). We explain how the authors missed this pattern and offer five recommendations for designing future experiments. Infant imitation raises fundamental issues about action representation, social learning, and brain-behavior relations. The debate about the origins and development of imitation reflects its importance to theories of developmental science.

Early rearing history influences oxytocin receptor epigenetic regulation in rhesus macaques

Significance Epigenetically programmed stress adaptation may be a conduit for informing offspring of environmental challenge. We employed ChIP-sequencing to examine effects of early environment on epigenetic regulation using hippocampal samples from macaques exposed to disruption in maternal care. We found decreased H3K4me3 binding at genes critical to behavioral stress response, the most robust being the oxytocin receptor gene (OXTR), for which we observed a corresponding decrease in RNA expression. Post hoc analysis showed that a gain-of-function OXTR SNP rescued behavioral differences in early stress-exposed subjects. Our data suggest that epigenetic down-modulation of OXTR in brain could contribute to behavioral differences observed in early stress-exposed subjects and that functional genetic variation plays a role. These could have translational implications for human psychiatric disease and personality disorders. Adaptations to stress can occur through epigenetic processes and may be a conduit for informing offspring of environmental challenge. We employed ChIP-sequencing for H3K4me3 to examine effects of early maternal deprivation (peer-rearing, PR) in archived rhesus macaque hippocampal samples (male, n = 13). Focusing on genes with roles in stress response and behavior, we assessed the effects of rearing on H3K4me3 binding by ANOVA. We found decreased H3K4me3 binding at genes critical to behavioral stress response, the most robust being the oxytocin receptor gene OXTR, for which we observed a corresponding decrease in RNA expression. Based on this finding, we performed behavioral analyses to determine whether a gain-of-function nonsynonymous OXTR SNP interacted with early stress to influence relevant behavioral stress reactivity phenotypes (n = 194), revealing that this SNP partially rescued the PR phenotype. PR infants exhibited higher levels of separation anxiety and arousal in response to social separation, but infants carrying the alternative OXTR allele did not exhibit as great a separation response. These data indicate that the oxytocin system is involved in social-separation response and suggest that epigenetic down-modulation of OXTR could contribute to behavioral differences observed in PR animals. Epigenetic changes at OXTR may represent predictive adaptive responses that could impart readiness to respond to environmental challenge or maintain proximity to a caregiver but also contribute to behavioral pathology. Our data also demonstrate that OXTR polymorphism can permit animals to partially overcome the detrimental effects of early maternal deprivation, which could have translational implications for human psychiatric disorders.

Early maternal mirroring predicts infant motor system activation during facial expression observation.

Processing facial expressions is an essential component of social interaction, especially for preverbal infants. In human adults and monkeys, this process involves the motor system, with a neural matching mechanism believed to couple self- and other-generated facial gestures. Here, we used electroencephalography to demonstrate recruitment of the human motor system during observation and execution of facial expressions in nine-month-old infants, implicating this system in facial expression processing from a very young age. Notably, examination of early video-recorded mother-infant interactions supported the common, but as yet untested, hypothesis that maternal mirroring of infant facial gestures is central to the development of a neural matching mechanism for these gestures. Specifically, the extent to which mothers mirrored infant facial expressions at two months postpartum predicted infant motor system activity during observation of the same expressions at nine months. This suggests that maternal mirroring strengthens mappings between visual and motor representations of facial gestures, which increases infant neural sensitivity to particularly relevant cues in the early social environment.

The mu-rhythm can mirror: insights from experimental design, and looking past the controversy

Author(s): Bowman, Lindsay C; Bakermans-Kranenburg, Marian J; Yoo, Kathryn H; Cannon, Erin N; Vanderwert, Ross E; Ferrari, Pier F; van IJzendoorn, Marinus H; Fox, Nathan A

High-Ranking Geladas Protect and Comfort Others After Conflicts

Post-conflict affiliation is a mechanism favored by natural selection to manage conflicts in animal groups thus avoiding group disruption. Triadic affiliation towards the victim can reduce the likelihood of redirection (benefits to third-parties) and protect and provide comfort to the victim by reducing its post-conflict anxiety (benefits to victims). Here, we test specific hypotheses on the potential functions of triadic affiliation in Theropithecus gelada, a primate species living in complex multi-level societies. Our results show that higher-ranking geladas provided more spontaneous triadic affiliation than lower-ranking subjects and that these contacts significantly reduced the likelihood of further aggression on the victim. Spontaneous triadic affiliation significantly reduced the victim’s anxiety (measured by scratching), although it was not biased towards kin or friends. In conclusion, triadic affiliation in geladas seems to be a strategy available to high-ranking subjects to reduce the social tension generated by a conflict. Although this interpretation is the most parsimonious one, it cannot be totally excluded that third parties could also be affected by the negative emotional state of the victim thus increasing a third party’s motivation to provide comfort. Therefore, the debate on the linkage between third-party affiliation and emotional contagion in monkeys remains to be resolved.

Eliciting imitation in early infancy

We (Meltzoff etxa0al., 2018) described how Oostenbroek etxa0al.s (2016) design likely dampened infant imitation. In their commentary, Oostenbroek etxa0al. (in press) argue that our points are post hoc. It is important for readers to know that they are not. Our paper re-stated best practices described in published papers. Based on the literature, the design used by Oostenbroek etxa0al. (2016) would be predicted to dampen infant imitation. This article is protected by copyright. All rights reserved.

The role of the motor system in action understanding and communication: Evidence from human infants and non-human primates

There is growing evidence that activation of the motor system during observation of actions, a phenomenon first observed in non-human primates, underlies action understanding and even communication. This review (a) examines the evidence on motor system activity as an underlying neural correlate of action understanding; (b) reviews the theoretical and empirical work linking action understanding and the development of communication, with a specific focus on the role that gestures play as an intermediary; and (c) discusses the research on and existing opportunities for understanding the link between the motor system and communication in both humans and non-human primates, through the lens of action perception. Bringing together findings and perspectives from developmental social cognition in both humans and non-human primates and applying recent neuroscientific perspectives will help to elucidate the processes underlying the ability to understand and communicate with others.

Not only a human affair: embracing behaviour in Theropithecus gelada

DOI: 10.1159/000354129 298 5th Congress of the European Federation for Primatology researchers usually argue that one of the distinguishing features of non-human primates’ gestures is their high degree of flexibility, which can be considered in different ways: (1) ‘means-end dissociation’, which refers to the use of a particular gesture in different functional contexts and/or several gestures for one specific context, and (2) gesture sequences which consist of combinations of two or more gestural signals. Both strategies enable non-human primates to adjust their gesture use to their partner’s behaviour and to increase the range of potential meanings that can be conveyed by combining the components of a more or less limited gestural repertoire. Because of their flexible use, however, very few gestures have a specific meaning, but their meaning is defined by the context in which they occur. Thus, in contrast to many vocalizations of non-human primates, their gestures are (1) less context-specific and do not represent functionally referential signals and, related to this, (2) gesture sequences do not represent meaningful combinations used for other functions than their single components. Therefore, I will first provide an overview of recent research on the flexible use of gestures in great apes to demonstrate how they create meaning in their interactions with others. I will then discuss how these findings relate to evidence from vocal studies with the aim to identify ‘blind spots’ and biases that currently constrain a fruitful debate about the origins of human language.Comparative studies of primate grasping and manipulative behaviours in captivity are numerous but there has been little research on hand use in the wild. Hand use during wild non-locomotor behaviours may reveal increased ranges of joint mobility or manipulative behaviours that have been previously ignored or underestimated. Manipulative behaviours in apes can strongly correlate with different habitats at the species and population level. Chimpanzees more often use tools in the wild and thus are thought to be more manipulative than gorillas. However, captive studies have demonstrated high dexterity in both taxa. We investigate hand use during manipulation (e.g. food processing, tool-use) in wild mountain gorillas (Gorilla beringei, Bwindi Impenetrable National Park, Uganda) and wild chimpanzees (Pan troglodytes verus, Tai National Park, Cote d’Ivoire). We used video data collected in the wild that included 32 gorilla (n=9 individuals) and 53 chimpanzee (n=11 individuals) instances of manipulative tasks. Digital images were extracted and analysed frame by frame. Preliminary results show that hand grips are similar between gorillas and chimpanzees during the manipulation of common food objects, such as long plant stems or branches. During the manipulation of species-specific food objects, gorillas use variable thumb-index grips during the manipulation of thistles and small plant stems, while chimpanzees use similar grips during nut-cracking. These preliminary results suggest that Bwindi mountain gorillas have similarly high dexterity as that of Tai chimpanzees despite not being tool-users. Gorillas frequently use precision grasping more to obtain small rather than large food items, which is similar to chimpanzees and other non-human primates.Previous studies have shown a positive relationship between proximity to humans or habitat fragmentation and parasitic levels in non-human primates (NHPs). However, to date few have explicitly explored links between parasite load and stress conditions. To better understand the links between parasite prevalence and NHP immune system efficiency and stress levels, faecal samples of Alouatta palliata and the critically endangered Ateles geoffroyi geoffroyi were non-invasively collected in northern Costa Rica. We investigated whether the presence of gastrointestinal parasites was related to the abundance of hormones (cortisol and testosterone). Samples were gathered across three areas differing in the frequency and diversity of human presence, i.e. around the Cano Palma Biological Station, near villages and at ecotourism sites. Two grams of each faecal sample were stored in a sugar saturated solution with 10% formalin to conserve the parasites; the remaining matter was dried to preserve DNA and steroid hormones. The samples enabled the quantification of parasites as well as testosterone and cortisol levels using ELISA as proxies of general health status and stress levels. Data on parasite abundance and hormone levels were contrasted across the two species and the three different sampling areas. Furthermore, we assessed the genetic exchange among the different groups of primates sampled. We genetically analysed the samples using 12 microsatellites previously validated by the University of Costa Rica. We verified whether transmission of parasites among the groups could be possible concomitant to the genetic exchange. This study aimed to better understand and assess the impact of human factors on NHP health and across NHPs with different socio-ecological characteristics.DOI: 10.1159/000354129 290 5th Congress of the European Federation for Primatology considerably between species for any given body size. Numerous hypotheses have been put forward to explain this variation. In recent years, we have tested predictions that flow from a framework focusing on the energetic aspects of having a large amount of the metabolically expensive brain tissue. In this talk, I will give an overview of our findings from broad comparative phylogenetic studies in mammals, and their implications for our understanding of non-human and human primate evolution. In sum, we found evidence for two pathways to increase relative brain size compared to the ancestral state. First, a species may change its lifestyle to allow for a stable increase in its total energy budget, e.g. by changing its diet. Alternatively, or in combination with the first pathway, a species may allocate more energy to the brain and less to other expensive functions such as offspring production. Ultimately, this option results in very low population growth rates even in good conditions, as found in great apes. A further increase in brain size would not be compatible with demographically viable populations in these large-brained primates. However, using comparative evidence from mammals, we demonstrate that help from non-mothers can alleviate this trade-off between reproductive effort and brain size. Nevertheless, the energetic constraints on brain size evolution will only be overcome in species that can actually benefit from enhanced cognitive abilities. While such benefits are potentially ubiquitous, we would expect them to be undermined by unavoidable mortality in some socioecological conditions, and by the difficulty of transferring knowledge across generations in some social systems. A combined test of all these considerations remains a challenge, largely due to the shortcomings of the distinct datasets, but I will present the newest data and results from our current projects.Throughout their range across Africa, chimpanzees (Pan troglodytes) are threatened with nextinction due to habitat destruction, disease and unsustainable levels of hunting and capture, in spite of being protected by national and international laws. In recent years, the bush meat and the pet trade have resulted in a significant increase in the number confiscated orphan chimpanzees. The Chimpanzee Conservation Centre (CCC), located in the High Niger National Park (HNNP), is the only Pan African Sanctuary Alliance (PASA)-accredited sanctuary caring for chimpanzee orphans in Guinea, West Africa. This sanctuary has been rehabilitating confiscated chimpanzees since 1997. With the aim of reinforcing the wild chimpanzee population of the HNNP and to enhance park protection, the CCC, in 2008, released a first group of 12 chimpanzees into the Mafou core area of the park. Five of those individuals have since settled at the release site and continue to be monitored. In August 2011, the CCC was able to re-enforce this resident group with the successful addition of 2 adult females. Post-release monitoring of these individuals involved distance monitoring using simple VHF and/or ARGOS and GPS store-on-board radio collars. Here, we present data downloaded in 2011–2012 from the GPS store-on-board collars of 2 adult males and these 2 additional adult females. These data allowed us to analyse their social dynamics, party composition, habitat preferences, day range and home range use. Our results indicate that these females integrated successfully into the resident group and that the behaviour of these wild-born released orphan chimpanzees mirrors that of wild counterparts inhabiting similar savannah dominated landscapes, suggesting that they have adapted appropriately to their release conditions.