Pier Francesco Ferrari

During pregnancy fetuses are responsive to the external environment, specifically to maternal stimulation. During this period, brain circuits develop to prepare neonates to respond appropriately. The detailed behavioral analysis of fetus’ mouth movements in response to mothers’ speech may reveal important aspects of their sensorimotor and affective skills; however, to date, no studies have investigated this response. Given that newborns at birth are capable of responding with matched behaviors to the social signals emitted by the caregiver, we hypothesize that such precocious responses could emerge in the prenatal period by exploiting infants’ sensitivity to their mother’s voice. By means of a two-dimensional (2D) ultrasonography, we assessed whether fetuses at 25 weeks of gestation, showed a congruent mouth motor response to maternal acoustic stimulation. Mothers were asked to provide different stimuli, each characterized by a different acoustic output (e.g. chewing, yawning, nursery rhymes, etc.) and we recorded the behavioral responses of 29 fetuses. We found that, when mothers sang the syllable LA in a nursery rhyme, fetuses significantly increased mouth openings. Other stimuli provided by the mother did not produce other significant changes in fetus’ behavior. This finding suggests that fetuses are sensitive only to specific maternal vocalizations (LA) and that fetal matched responses are rudimentary signs of early mirroring behaviors that become functional in the postnatal period. In conclusion, fetuses seem to be predisposed to respond selectively to specific maternal stimuli. We propose that such responses may play a role in the development of behavioral and emotional attunement with their mothers long before birth.

A fundamental issue in cognitive neuroscience is how the brain encodes the actions and intentions of others. The discovery of an action-production-perception mechanism underpinning such a capacity advanced our knowledge of how these processes occur; however, no study has examined how the early postnatal environment may shape action-production-perception. Here, we examined the effects of social experience on action-production-perception in 3-day-old rhesus macaques that were raised either with or without their biological mothers. We measured the neonatal imitation skills and brain electrical activity responses, while infants produced and observed facial gestures. We hypothesized that early social experiences may shape brain activity, as assessed via electroencephalogram suppression in the α band (5-7 Hz in infants, known as the mu rhythm) during action observation, and lead to more proficient imitation skills. Consistent with this hypothesis, the infants reared by their mothers were more likely to imitate lipsmacking (LS) - a natural, affiliative gesture - and exhibited greater mu rhythm desynchronization while viewing LS gestures than the nursery-reared infants. These effects were not found in response to tongue protrusion, a meaningless gesture, or a nonsocial control. These data suggest that socially enriched early experiences in the first days after birth increase brain sensitivity to socially relevant actions.

Le concept d’évolution tourne autour de la reproduction. Le moment de l’accouchement est probablement le plus critique de tout le processus reproductif puisque en quelques heures la vie de la mère comme de l’enfant peut être sérieusement menacée. Du point de vue de l’évolution, de nombreuses pressions sélectives en compétition doivent avoir donné forme au déroulement de l’accouchement afin de minimiser les risques et de maximiser la probabilité de survie de la mère et de l’enfant et, à la longue, de l’espèce. Malgré son extrême importance, nous savons bien peu de choses à propos du processus de naissance dans l’ordre des primates, à l’exception de l’homme ("Homo sapiens"). Nous avons filmé trois accouchements de bonobos ("Pan paniscus"), un dans le parc primates d’Apenheul (Pays-Bas) et deux à La Vallée des Singes (France). Durant toutes les phases de l’accouchement, les mères sont restées dans leurs groupes sociaux et étaient libres de se déplacer à l’intérieur comme à l’extérieur de leurs enclos. Cela nous a permis de décrire en détail et de quantifier temporellement les comportements des mères, tout comme les interactions entre les autres membres du groupe pendant les différentes phases de l’accouchement. Les autres femelles du groupe sont restées auprès des parturientes et ont démontré envers elles de nombreux comportements affiliatifs en créant une sorte de barrière protective. La placentophagie a été observée dans chaque cas et, dans un d’entre eux, le placenta a été partagé avec les autres femelles. Les premières interactions entre mère et enfant ont principalement consisté dans le nettoyage du poil et des contacts affiliatifs entre le nouveau-né et les autres membres du groupe ont également été observés. Les comportements observés prouvent encore une fois la puissance des liens entre femelles bonobos, qui forment une unité compacte autour d’une femelle homologue en difficulté.

Neonatal imitation should not exclusively be considered at the population-level; instead, we propose that inconsistent findings regarding its occurrence result from important individual differences in imitative responses. We also highlight what we consider to be a false dichotomy of genetic versus learning accounts of the development of mirror neurons, and instead suggest a more parsimonious epigenetic perspective.

Here, we tested hypotheses about the potential functions of yawning based on its intensity and social contexts. Due to their spectrum intensity of yawns (covered teeth/YW1; uncovered teeth/YW2; uncovered gums/YW3), geladas are a good model species for this purpose. We suggest that yawns of different intensity can bear different information according to the performer, the context and the behavioural pattern temporally associated to the yawn event. YW3, mainly performed by high ranking males during periods of high social tension, was frequently associated with an auditory component and often accompanied by scratching (a measure of anxiety). YW1 and YW2, preferentially performed by females, were frequently associated to lip smacking, an affiliative display. In conclusion, even though a clear-cut functional distinction of geladas' yawn intensity is difficult, YW1 and YW2 seem to be more linked to affiliative social interactions; whereas, YW3 seems to be more linked to agonistic and tension situations.

One of the key questions in understanding human morality is how central are emotions in influencing our decisions and in our moral judgments. Theoretical work has proposed that empathy could play an important role in guiding our tendencies to behave altruistically or selfishly. Neurosciences suggest that one of the core elements of empathic behaviour in human and nonhuman primates is the capacity to internally mimic the behaviour of others, through the activation of shared motor representations. Part of the neural circuits involves parietal and premotor cortical regions (mirror system), in conjunction with other areas, such as the insula and the anterior cingulate cortex. Together with this embodied neural mechanism, there is a cognitive route in which individuals can evaluate the social situation without necessary sharing the emotional state of others. For example, several brain areas of the prefrontal cortex track the effects of one’s own behaviour and of the value of one’s own actions in social contexts. It is here proposed that, moral cognition could emerge as the consequence of the activity of emotional processing brain networks, probably involving mirror mechanisms, and of brain regions that, through abstract-inferential processing, evaluate the social context and the value of actions in terms of abstract representations. A comparative-based approach to the neurobiology of social relations and decision-making may explain how complex mental faculties, such as moral judgments, have their foundations in brain networks endowed with functions related to emotional and abstract-evaluation processing of goods. It is proposed that in primate evolution these brain circuits have been co-opted in the social domain to integrate mechanisms of self-reward, estimation of negative outcomes, with emotional engagement.