Expertise in action observation: recent neuroimaging findings and future perspectives

INTRODUCTION In everyday life, we continuously interact with other individuals. Understanding actions of other people, i.e., the ability to distinguish between different actions, such as passing over vs. threatening someone with a knife, has been crucial for the survival of our species and is a fundamental capability for our social interactions. Neuroimaging studies investigated the neural substrates subtending action perception using a variety of techniques, ranging from univariate analysis of fMRI data (Brass et al., 2007; Gazzola et al., 2007; De Lange et al., 2008; Gazzola and Keysers, 2009; Turella et al., 2009a, 2012; Wurm et al., 2011; Wurm and Schubotz, 2012; Wurm et al., 2012; Lingnau and Petris, 2013), to fMRI repetition suppression (Dinstein et al., 2007; Chong et al., 2008; Lingnau et al., 2009; Kilner et al., 2009) and multivoxel pattern analysis (MVPA; Dinstein et al., 2008a; Oosterhof et al., 2010, 2012). These studies reported the consistent recruitment of a number of regions, generally assumed as pertaining to two different networks, typically referred to as the action observation network (AON) and the mentalizing system (Figure 1A). Both networks have been advocated to be involved in action understanding (Brass et al., 2007; De Lange et al., 2008; Van Overwalle, 2009; Van Overwalle and Baetens, 2009; Wurm et al., 2011), but their precise roles and their causal involvement are strongly debated (Dinstein et al., 2008b; Mahon and Caramazza, 2008; Hickok, 2009; Turella et al., 2009b; Rizzolatti and Sinigaglia, 2010). In homology with monkey neurophysiological studies, three regions have been proposed to form the human AON (Rizzolatti and Craighero, 2004; Rizzolatti and Sinigaglia, 2010; see Figure 1A). This “core” AON was defined as comprising (i) the ventral premotor cortex (PMV) together with the posterior part of the inferior frontal gyrus (pIFG), (ii) the anterior inferior parietal lobule (aIPL) and (iii) the superior temporal sulcus (STS). Human neuroimaging studies suggested the recruitment of several additional areas that were incorporated in an “extended” version of the AON (Gazzola and Keysers, 2009; Caspers et al., 2010; see Figure 1A). The mentalizing system has been identified in human neuroimaging studies investigating social cognition tasks, such as intention and beliefs attribution about the self or others, while observing actionrelated stimuli (Van Overwalle, 2009). The regions consistently assigned to this network are the medial prefrontal cortex (mPFC) and the temporo-parietal junction (TPJ) (Figure 1A), and less often also the precuneus and the posterior cingulate cortex (Amodio and Frith, 2006; Brass et al., 2007; De Lange et al., 2008; Van Overwalle, 2009; Van Overwalle and Baetens, 2009). The first description of the involvement of sensorimotor regions during action perception started with the discovery of mirror neurons in the ventral premotor cortex in macaque monkeys (Di Pellegrino et al., 1992). These visuomotor neurons responded both while the monkey executed or observed similar actions and were later described also within the monkey inferior parietal lobule (Fogassi et al., 2005). Note that both regions also contain neurons with motor-only and visual-only properties (Gallese et al., 1996, 2002). Following their discovery, motor theories of action understanding proposed that mirror neurons might provide the basis for a matching mechanism between what we observe and what we can perform allowing the understanding of observed actions in motoric terms (Rizzolatti et al., 2001). Even if this hypothesis is strongly debated (Jacob and Jeannerod, 2005; Mahon and Caramazza, 2008; Hickok, 2009, 2013), a similar homologue mechanism has been proposed to exist in the human AON (Rizzolatti et al., 2001; Rizzolatti and Craighero, 2004; Rizzolatti and Sinigaglia, 2010). In this brief overview, we will first describe previous fMRI studies that investigated how motor experience affects activation within the AON, and to which degree these studies allow drawing conclusions about the role of this network in action understanding. As the majority of the studies investigated only the AON and given the limited scope of this Opinion, we will focus on this network, even if our considerations might also hold true for other areas. We will then try to delineate how future studies might exploit motor expertise as a tool for gaining insights into the neural basis of action understanding.