Task-dependent and distinct roles of the temporoparietal junction and inferior frontal cortex in the control of imitation

doi:10.1093/scan/nsu148 SCAN (2015) 10,1003^1009 Task-dependent and distinct roles of the temporoparietal junction and inferior frontal cortex in the control of imitation Jeremy Hogeveen,1,2 Sukhvinder S. Obhi,3 Michael J. Banissy,4 Idalmis Santiesteban,5 Clare Press,5 Caroline Catmur,6 and Geoffrey Bird7,8 1 Cognitive Neuroscience Laboratory, Rehabilitation Institute of Chicago and 2Department of Physical Medicine and Rehabilitation, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA, 3Department of Psychology, Neuroscience & Behaviour, McMaster University, Hamilton, ON, Canada, 4Department of Psychology, Goldsmiths and 5Department of Psychological Sciences, Birkbeck College, University of London, London, UK, 6Department of Psychology, University of Surrey, Guildford, UK, and 7MRC Social, Genetic, and Developmental Psychology Centre, King’s College London and 8Institute of Cognitive Neuroscience, University College London, London, UK The control of neurological networks supporting social cognition is crucially important for social interaction. In particular, the control of imitation is directly linked to interaction quality, with impairments associated with disorders characterized by social difficulties. Previous work suggests inferior frontal cortex (IFC) and the temporoparietal junction (TPJ) are involved in controlling imitation, but the functional roles of these areas remain unclear. Here, transcranial direct current stimulation (tDCS) was used to enhance cortical excitability at IFC and the TPJ prior to the completion of three tasks: (i) a naturalistic social interaction during which increased imitation is known to improve rapport, (ii) a choice reaction time task in which imitation needs to be inhibited for successful performance and (iii) a non-imitative control task. Relative to sham stimulation, stimulating IFC improved the contextdependent control of imitationparticipants imitated more during the social interaction and less during the imitation inhibition task. In contrast, stimulating the TPJ reduced imitation in the inhibition task without affecting imitation during social interaction. Neither stimulation site affected the non-imitative control task. These data support a model in which IFC modulates imitation directly according to task demands, whereas TPJ controls taskappropriate shifts in attention toward representation of the self or the other, indirectly impacting upon imitation. Keywords: imitation; mimicry; mirror system; transcranial direct current stimulation; temporoparietal junction; inferior frontal cortex INTRODUCTION The importance of socio-cognitive ability for human health (KiecoltGlaser et al., 1984; Cohen, 1988), wealth (Lopes et al., 2006; Silk, 2007) and happiness (George et al., 1989; Kaufman et al., 2004) is now wellestablished. However, it is only recently that the importance of the topdown control of socio-cognitive networks has been realized (Frith and Frith, 2006; Satpute and Lieberman, 2006; Spengler et al., 2009; Cook et al., 2012). For example, despite the fact that the general tendency to imitate the posture (Lafrance and Broadbent, 1976), facial expressions (Neal and Chartrand, 2011) and actions (Chartrand and Bargh, 1999) of our interaction partners leads to high quality social interaction (Lakin and Chartrand, 2003), imitators dynamically modulate the degree to which they mimic others as a function of variables such as power relationships, group dynamics and relationship quality (Chartrand and Lakin, 2013). The importance of top-down control of socio-cognitive processes is evidenced by the severe social deficits seen in autism spectrum disorders (ASDs) when this control goes awry (Bird et al., 2006; Cook and Bird, 2012), and by the fact that, at least in the case of imitation, control of social cognition relies on a dedicated neural network, independent of the standard cognitive control network Received 8 April 2014; Revised 15 August 2014; Accepted 25 November 2014 Advance Access publication 5 December 2014 The authors would like to extend our thanks to Nazanin Biabani for acting as a confederate in this study, which was conducted while J.H. held a Michael Smith Foreign Study Supplement awarded by the Social Sciences and Humanities Research Council of Canada. M.J.B. is supported by the Economic and Social Research Council (ES/K00882X/1). G.B. contributed to this project while a Senior Research Fellow at the Netherlands Institute for Advanced Study in the Humanities and Social Sciences. C.C. is supported by the Economic and Social Research Council (ES/K00140X/1). S.S.O. is supported by a standard research grant from the Social Sciences and Humanities Research Council of Canada. Correspondence should be addressed to Jeremy Hogeveen, Cognitive Neuroscience Laboratory, Rehabilitation Institute of Chicago, 345 E Superior Street, Chicago, IL 60611, USA. E-mail: used to inhibit or enhance other automatic behavioral tendencies (Brass et al., 2005; Wang and Hamilton, 2012). The ability to imitate the actions of others is thought to be mediated by the human mirror neuron system (MNS), comprising portions of the inferior frontal cortex (IFC) and parietal cortex (Iacoboni et al., 1999; Decety et al., 2002; Heiser et al., 2003; Chaminade et al., 2005; Catmur et al., 2009). However, mirror neuron activity does not always produce imitation, and functional magnetic resonance imaging (fMRI) and brain stimulation studies suggest that the top-down control of the mirror system is accomplished via a network of regions including regions of the IFC (co-located with those involved in mirroring, but extending more anteriorly1; Brass et al., 2005; Catmur et al., 2009, 2011), the temporoparietal junction (TPJ; Brass et al., 2005, 2009; Santiesteban et al., 2012a; Sowden and Catmur, 2013) and medial prefrontal cortex (mPFC; Brass et al., 2005, 2009; Wang and Hamilton, in press; Wang et al., 2011). Networks mediating the control of imitation show functional and partial anatomical overlap with those supporting Theory of Mind (ToM; the ability to represent the mental states of oneself and others). For example, both the TPJ and mPFC are reliably activated in neuroimaging studies of ToM (Castelli et al., 2000; Frith and Frith, 2003; Mitchell, 2008; Van Overwalle, 2009; Zaki et al., 2010). Further, functional relationships between imitative control and ToM have been demonstrated, whereby training participants to control imitation improves their ability to take another’s visual perspective (Santiesteban et al., 2012b), while an impaired ability to control imitation is correlated with reduced ToM ability in individuals with ASD 1 Extant neuroimaging data suggests that IFC, referring to posterior portions of the inferior frontal gyrus and ventral premotor cortex, contains populations of cells with both facilitative mirror propertiesi.e. that match observed and executed representations of action (Iacoboni et al., 1999; Kilner et a (...truncated)