The Role of the Superior Temporal Sulcus and the Mirror Neuron System in Imitation

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The Role of the Superior Temporal Sulcus and the Mirror Neuron System in Imitation r Human Brain Mapping 31:1316–1326 (2010) r The Role of the Superior Temporal Sulcus and the Mirror Neuron System in Imitation Pascal Molenberghs,* Christopher Brander, Jason B. Mattingley, and Ross Cunnington The University of Queensland, Queensland Brain Institute & School of Psychology, St Lucia, Queensland, Australia r r Abstract: It has been suggested that in humans the mirror neuron system provides a neural substrate for imitation behaviour, but the relative contributions of different brain regions to the imitation of manual actions is still a matter of debate. To investigate the role of the mirror neuron system in imita- tion we used fMRI to examine patterns of neural activity under four different conditions: passive ob- servation of a pantomimed action (e.g., hammering a nail); (2) imitation of an observed action; (3) execution of an action in response to a word cue; and (4) self-selected execution of an action. A net- work of cortical areas, including the left supramarginal gyrus, left superior parietal lobule, left dorsal premotor area and bilateral superior temporal sulcus (STS), was significantly active across all four con- ditions. Crucially, within this network the STS bilaterally was the only region in which activity was significantly greater for action imitation than for the passive observation and execution conditions. We suggest that the role of the STS in imitation is not merely to passively register observed biological motion, but rather to actively represent visuomotor correspondences between one’s own actions and the actions of others. Hum Brain Mapp 31:1316–1326, 2010. VC 2010 Wiley-Liss, Inc. Key words: fMRI; imitation; mirror neuron system r r INTRODUCTION ror neurons are visuomotor neurons that fire both when an action is performed and when a similar or identical Motor imitation involves observing the action of another action is passively observed [Rizzolatti and Craighero, individual and matching one’s own movements to those 2004]. A mirror system or network in the human brain actions being observed [Decety et al., 2002]. Imitation has should therefore be defined by its common activation dur- been suggested to rely on the mirror neuron system [Brass ing passive observation of action and during execution of and Heyes, 2005; Buccino et al., 2004; Heyes, 2001; Iaco- actions without visual stimulation [Chong et al., 2008]. If boni, 2005; Iacoboni and Dapretto, 2006; Rizzolatti, 2005; such a mirror network is the basis for imitation, then imi- Rizzolatti et al., 2001; Rizzolatti and Craighero, 2004]. Mir- tation should rely on the same areas that are commonly recruited for action observation and execution. Previous brain imaging studies that have investigated imitation, Contract grant sponsor: National Health and Medical Research however, have not examined the overlap or conjunction Council of Australia (NHMRC). between action observation, execution, and imitation. *Correspondence to: Pascal Molenberghs, The University of Therefore, the relative roles of different brain regions Queensland, Queensland Brain Institute, St Lucia, Queensland within an action observation/execution network during 4072, Australia. E-mail: [email protected] imitation remain unknown. The aim of the present study Received for publication 3 February 2009; Revised 7 September 2009; Accepted 7 October 2009 was to independently identify the brain regions that DOI: 10.1002/hbm.20938 respond to both observation and execution of movements Published online 19 January 2010 in Wiley Online Library (both word-cued and self-selected) and to investigate the (wileyonlinelibrary.com). differential role of these regions during imitation. VC 2010 Wiley-Liss, Inc. r Superior Temporal Sulcus and Mirror Neuron System r Mirror neurons were first observed using microelectrode Assuming a similar mirror neuron network exists in recordings of single neurons in area F5 of the monkey pre- humans and monkeys, the question remains whether this motor cortex [di Pellegrino et al., 1992; Gallese et al., 1996; network supports imitation. The fact that monkeys appear Rizzolatti et al., 1996a] and later also in the PF/PFG com- to be relatively poor imitators [Visalberghi and Fragaszy, plex within the inferior parietal cortex [Fogassi and Lup- 2001; Whiten and Ham, 1992] suggests that imitation is not pino, 2005; Fogassi et al., 2005; Gallese et al., 2002]. the primary function of the nonhuman mirror neuron sys- Neurons in the superior temporal sulcus (STS) also tem. Iacoboni and Dapretto [2006] have suggested a ‘‘core respond to the passive observation of actions [Jellema circuit’’ for imitation that includes three regions. Two of et al., 2000; Perrett et al., 1989], but they have not gener- these regions form part of the mirror neuron network: the ally been considered to form part of the mirror-neuron posterior inferior frontal gyrus (IFG) plus adjacent ventral network because they do not appear to be endowed premotor cortex (PMC), and the rostral part of the inferior with motor properties [Rizzolatti and Craighero, 2004]. parietal lobule (IPL). The third region, the posterior part of Early brain imaging studies that compared brain activity the superior temporal sulcus (STS), is outside of the mirror during perceived and executed actions [Decety et al., neuron system. Iacoboni and coworkers [Iacoboni, 2005; 1997; Iacoboni et al., 2001; Rizzolatti et al., 1996b] sug- Iacoboni et al., 2001; Iacoboni and Dapretto, 2006] have sug- gested that an analogous frontoparietal mirror neuron gested that the main function of the STS is to provide visual system exists in humans. Since then, many studies using input to the mirror neuron system and to allow matching TMS, EEG, MEG, PET and fMRI have confirmed these between sensory predictions of imitative motor plans and a early results. It is widely believed that Brodmann area visual description of observed actions. 44, in the posterior inferior frontal gyrus (IFG), is the Apart from these three regions, other studies examining human mirror-equivalent of monkey area F5 and that imitation have reported involvement of the superior parie- the rostral inferior parietal lobule (IPL) is the human tal lobule [Chaminade et al., 2002; Iacoboni et al., 1999; mirror-equivalent of area PF/PFG (for reviews, see Fab- Jackson et al., 2006; Koski et al., 2003; Vogt et al., 2007; bri-Destro and Rizzolatti [2008], Iacoboni and Dapretto Williams et al., 2007] and dorsal premotor area [Aziz- [2006], Rizzolatti [2005], Rizzolatti et al. [2001], and Riz- Zadeh et al., 2006; Buccino et al., 2004; Gre`zes et al., 2003; zolatti and Craighero [2004]). However, it has been sug- Koski et al., 2002, 2003; Vogt et al., 2007; Williams et al., gested that the evidence for a circuit in humans with 2007]. The study of Gazzola and Keysers [2009] also identi- ‘‘mirror’’ properties analogous to those observed in fied these regions as overlapping for observation and exe- monkeys is relatively weak [Decety and Gre`zes, 1999; cution of movement; however, the function of these areas Dinstein et al., 2008; Gre`zes and Decety, 2001; Turella for imitation and their relationship with the mirror net- et al., 2009]. One issue is that, in humans, there appear to be work are still not clear. many more areas that exhibit ‘‘mirror’’ properties based on In the current study, we aimed to examine the roles of their common activation during observation and execution mirror network areas in imitation. As noted earlier, most of action—including the ventral and dorsal premotor cortex, of the studies that have investigated the mirror system in the supplementary and presupplementary motor areas, the humans have not included the necessary conditions to superior parietal lobule, and the intraparietal region—than test for mirror properties as defined by the original sin- would be expected based on the original monkey studies gle-cell work in monkeys [Dinstein et al., 2008; Gazzola [Gazzola and Keysers, 2009; Turella et al., 2009]. If mirror and Keysers, 2009; Turella et al., 2009]. Instead of simply areas in humans are truly widespread throughout the cor- comparing levels of activity between the different condi- tex, the explanatory power of a ‘‘mirror system’’ with tions, as in typical fMRI studies, we specifically used a unique functional properties is diminished. A further issue conjunction analysis to identify areas commonly active is that most brain imaging studies have examined neural ac- during all conditions of passive observation, execution, tivity for just a single condition at a time—passive observa- and imitation of action. Another problem with previous tion, execution, or imitation—rather than testing for regions investigations is that they have typically involved visual of overlap between all conditions, which a strict definition of stimulationinboththeobservationandexecutioncondi- the mirror system requires [Fabbri-Destro and Rizzolatti, tions, thus potentially yielding vision-related activity in 2008]. A recent study by Gazzola and Keysers [2009] both. A true mirror area should be active during execu- directly tested for common areas of activation for tion conditions without visual stimulation [Dinstein et al., observed and executed actions in humans. They found 2007]. In our fMRI study, participants were required to reliable overlap in two regions in which mirror neurons observe, imitate, and execute actions—in the latter condi- have been found in monkeys: (1) the ventral premotor tion in the absence of any visual stimuli. Two separate area (BA 6/44) and (2) the inferior parietal cortex (area execution conditions were examined: participants either PF). In addition, however, they observed reliable overlap selected an appropriate action on the basis of a word-cue, in the dorsal premotor cortex, supplementary motor area, or they self-selected an action pseudorandomly from a middle cingulate, middle temporal gyrus, somatosensory learned set. During word-cued execution, visual and lan- cortex, and superior parietal lobule. guage areas of the brain should be active, whereas during r 1317 r r Molenberghs et al. r self-selected execution working memory and response Experimental Design selection areas should be involved [Cunnington et al., 2002].
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