Observational Learning of New Movement Sequences Is Reflected in Fronto-Parietal Coherence Jurjen van der Helden1,2*., Hein T. van Schie3., Christiaan Rombouts2 1 Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands, 2 Department of Cognitive Psychology and Ergonomics, University of Twente, Enschede, The Netherlands, 3 Behavioural Science Institute, Radboud University Nijmegen, Nijmegen, The Netherlands Abstract Mankind is unique in her ability for observational learning, i.e. the transmission of acquired knowledge and behavioral repertoire through observation of others’ actions. In the present study we used electrophysiological measures to investigate brain mechanisms of observational learning. Analysis investigated the possible functional coupling between occipital (alpha) and motor (mu) rhythms operating in the 10Hz frequency range for translating ‘‘seeing’’ into ‘‘doing’’. Subjects observed movement sequences consisting of six consecutive left or right hand button presses directed at one of two target- buttons for subsequent imitation. Each movement sequence was presented four times, intervened by short pause intervals for sequence rehearsal. During a control task subjects observed the same movement sequences without a requirement for subsequent reproduction. Although both alpha and mu rhythms desynchronized during the imitation task relative to the control task, modulations in alpha and mu power were found to be largely independent from each other over time, arguing against a functional coupling of alpha and mu generators during observational learning. This independence was furthermore reflected in the absence of coherence between occipital and motor electrodes overlaying alpha and mu generators. Instead, coherence analysis revealed a pair of symmetric fronto-parietal networks, one over the left and one over the right hemisphere, reflecting stronger coherence during observation of movements than during pauses. Individual differences in fronto-parietal coherence were furthermore found to predict imitation accuracy. The properties of these networks, i.e. their fronto-parietal distribution, their ipsilateral organization and their sensitivity to the observation of movements, match closely with the known properties of the mirror neuron system (MNS) as studied in the macaque brain. These results indicate a functional dissociation between higher order areas for observational learning (i.e. parts of the MNS as reflected in 10Hz coherence measures) and peripheral structures (i.e. lateral occipital gyrus for alpha; central sulcus for mu) that provide low-level support for observation and motor imagery of action sequences. Citation: van der Helden J, van Schie HT, Rombouts C (2010) Observational Learning of New Movement Sequences Is Reflected in Fronto-Parietal Coherence. PLoS ONE 5(12): e14482. doi:10.1371/journal.pone.0014482 Editor: Clayton T. Dickson, University of Alberta, Canada Received July 21, 2010; Accepted December 10, 2010; Published December 31, 2010 Copyright: 2010 van der Helden et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: HvS was supported by the European Union Integrated Project JAST (Joint Action Science and Technology), grant FP6-IST2-003747. 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. * E-mail: J.vanderHelden@donders.ru.nl . These authors contributed equally to this work. Introduction Many behavioural skills that humans establish during their life are acquired through observational learning. An important neurophys- iological principle that has been hypothesized to underlie observa- tional learning and imitation is motor resonance, i.e. the automatic activation of motor representations during action observation. Neuroimaging experiments in humans and single cell studies in macaques have investigated the neurophysiological basis of motor resonance during action observation [1]. In particular, motor resonance has been described as a basic property of mirror neurons, a selection of motor neurons in monkey higher-order premotor and parietal areas that are activated in a comparable manner during action execution and during the observation of a similar action by another individual [2,3]. At a larger scale neuroimaging experiments in humans confirm the existence of a mirror neuron system in man comprised of the inferior frontal gyrus, and the inferior parietal lobe supporting both action observation [4] and imitation [5,6]. The mirror neuron system (MNS) has been shown to be activated to a stronger extent if observers view movements that they already have in their repertoire. Calvo-Merino and others [7,8] for instance found that the MNS of dancers that observed dancing movements in the fMRI scanner, responded more strongly if these movements were part of their dancing routine. Orgs and others [9] showed that dancing experience was correlated with motor resonance, reflected in mu- and beta- suppression in the dancer’s electroencephalogram (EEG), when they observed a familiar dance movement. Recent findings from van Elk and others [10] further extend these findings to the domain of natural motor development. In their study, EEG was recorded from 14- to 16-month old infants during observation of videos showing other infants crawling and walking. EEG mu- and beta-suppression was found strongly related to the infant’s own motor experience, suggesting that already early in life an individuals’ action experience determines how the actions of others are processed. Whereas the above studies convincingly showed effects of motor experience to influence the observation of actions by others, involvement of the human MNS in the reverse direction, i.e. during the acquisition of a new action repertoire, has until recently PLoS ONE | www.plosone.org 1 December 2010 | Volume 5 | Issue 12 | e14482