Wired to Be Social: The Ontogeny of Human Interaction

Citation: Castiello U, Becchio C, Zoia S, Nelini C, Sartori L, et al. ( Wired to Be Social: The Ontogeny of Human Interaction Umberto Castiello 0 Cristina Becchio 0 Stefania Zoia 0 Cristian Nelini 0 Luisa Sartori 0 Laura Blason 0 Giuseppina D'Ottavio 0 Maria Bulgheroni 0 Vittorio Gallese 0 Aldo Rustichini, University of Minnesota, United States of America 0 1 Department of General Psychology, University of Padova , Padova , Italy , 2 Department of Psychology, Centre for Cognitive Science, University of Turin , Turin , Italy , 3 Child Neurology and Psychiatry Unit, Department of Paediatrics, Institute of Child Health IRCCS , Burlo Garofolo, Trieste , Italy , 4 Unit for Prenatal Diagnosis, Department of Obstetrics and Gynaecology, Institute of Child Health IRCCS , Burlo Garofolo, Trieste , Italy , 5 Department of Neuroscience, University of Parma and IIT (Italian Institute of Technology), Section of Parma , Parma , Italy Background: Newborns come into the world wired to socially interact. Is a propensity to socially oriented action already present before birth? Twin pregnancies provide a unique opportunity to investigate the social pre-wiring hypothesis. Although various types of inter-twins contact have been demonstrated starting from the 11th week of gestation, no study has so far investigated the critical question whether intra-pair contact is the result of motor planning rather then the accidental outcome of spatial proximity. Methodology/Principal Findings: Kinematic profiles of movements in five pairs of twin foetuses were studied by using four-dimensional ultrasonography during two separate recording sessions carried out at the 14th and 18th week of gestation. We demonstrate that by the 14th week of gestation twin foetuses do not only display movements directed towards the uterine wall and self-directed movements, but also movements specifically aimed at the co-twin, the proportion of which increases between the 14th and 18th gestational week. Kinematic analysis revealed that movement duration was longer and deceleration time was prolonged for other-directed movements compared to movements directed towards the uterine wall. Similar kinematic profiles were observed for movements directed towards the co-twin and selfdirected movements aimed at the eye-region, i.e. the most delicate region of the body. Conclusions/Significance: We conclude that performance of movements towards the co-twin is not accidental: already starting from the 14th week of gestation twin foetuses execute movements specifically aimed at the co-twin. - Funding: This work was supported by grant R.C. 44/03 of the Institute of Child Health IRCCS, Burlo Garofolo, Trieste, Italy and by the Ministero Italiano dell Universite e della Ricerca. C.B. was supported by a grant from the Regione Piemonte, Bando Scienze Umane e Sociali 2008, L.R. n. 4/2006. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. One-to-one interactions are the cradle of social cognition. Infants do not develop social understanding by merely watching other people at a distance. Rather, they learn by engaging in reciprocal exchanges with others [17]. Even hours after birth, newborns have been found to show preparedness for social interaction that, among other things, is expressed in their imitation of facial gestures [8,9]. Altogether such evidence indicates that newborns come into the world wired to socially interact. But, is a propensity to interact with others demonstrable before birth? Twin pregnancies provide a unique opportunity to investigate the social pre-wiring hypothesis. Unlike ordinary siblings, twins share a most important environment the uterus. If a predisposition towards social interaction is present before birth, one may expect twin foetuses to engage in some form of interaction. Although inter-twin contact has been demonstrated starting from the 11th week of gestation [10], no study has so far investigated the critical question of whether twin foetuses plan and execute movements directed towards each other. Put differently, whether intra-pair contact is the result of motor planning rather then the accidental outcome of spatial proximity. Whilst twins are initially too distant and their movements too weak to reach one another, with advancing gestational age contact between them becomes possible and soon almost inevitable. From the 11th week onwards, different patterns of inter-twin contact such as head to head, head to arm and arm to head contact are observed [10]. It is, however, between the 15th and 22nd week that intra-pair contact becomes a constant and increasing feature of all twin pregnancies [1113]. Whereas inter-twin contact is well established, little is known about the organization of movements bringing twins in touch. The motor behaviour of foetuses has traditionally been described in terms of reflexes rather than actions [14]. Although reflexes serve important functions, they are stereotyped, elicited and once launched run their predetermined course. This signifies, for instance, that reflexes are not goal directed, are not subject to learning and do not adjust to future states in a prospective fashion [14]. In contrast with the idea that foetuses only display reflexes, Zoia and colleagues [15] recently demonstrated kinematic adaptation to the somatosensory properties of the target in 22week-old single foetuses. Three types of hand movements were Junior High School Junior High School Junior High School Notes. SES social economical status, BMI body mass index, BP blood pressure, AF amniotic fluid. doi:10.1371/journal.pone.0013199.t001 directed movements, including hand to the back and hand to the head of the co-twin. We employed three analyses in order to explore whether the organization of foetal movements differed depending on the nature of the executed movement. The first analysis compared the incidence of each type of movement at the two gestational periods. The trend in the incidence of motor activities is considered to directly reflect developmental and maturational processes of the foetal central nervous system [2022]. If specific movement patterns underlie other-directed movements, the trend in the incidence of other-directed movements might be expected to be dissociated from that of movements directed towards ones own body or outer-directed movements. The second analysis compared the kinematic profiles of the different categories of movements. Based on the social prewiring hypothesis, we predicted that the kinematic pattern of other-directed movements would be different from the kinematic pattern of those movements directed towards ones own body or outer-directed movements. Finally, the third analysis employed a comparison of self-directed movements towards the mouth and the eye region, and movements directed towards the sibling (...truncated)