Mirror neurons, the representation of word meaning, and the foot of the third left frontal convolution Greig de Zubicaray a, * , Natasha Postle b , Katie McMahon a , Matthew Meredith a , Roderick Ashton b a Functional MRI Laboratory, Centre for Magnetic Resonance, University of Queensland, Brisbane, Qld. 4072, Australia b School of Psychology, University of Queensland, Brisbane, Qld., Australia article info Article history: Accepted 29 September 2008 Available online xxxx Keywords: Broca’s area Language comprehension Mirror neurons Action observation Imitation Semantics Phonology abstract Previous neuroimaging research has attempted to demonstrate a preferential involvement of the human mirror neuron system (MNS) in the comprehension of effector-related action word (verb) meanings. These studies have assumed that Broca’s area (or Brodmann’s area 44) is the homologue of a monkey pre- motor area (F5) containing mouth and hand mirror neurons, and that action word meanings are shared with the mirror system due to a proposed link between speech and gestural communication. In an fMRI experiment, we investigated whether Broca’s area shows mirror activity solely for effectors implicated in the MNS. Next, we examined the responses of empirically determined mirror areas during a language perception task comprising effector-specific action words, unrelated words and nonwords. We found overlapping activity for observation and execution of actions with all effectors studied, i.e., including the foot, despite there being no evidence of foot mirror neurons in the monkey or human brain. These ‘‘mirror” areas showed equivalent responses for action words, unrelated words and nonwords, with all of these stimuli showing increased responses relative to visual character strings. Our results support alternative explanations attributing mirror activity in Broca’s area to covert verbalisation or hierarchical linearisation, and provide no evidence that the MNS makes a preferential contribution to comprehending action word meanings. Ó 2008 Elsevier Inc. All rights reserved. 1. Introduction At the foot of the third left frontal convolution of the human cerebral cortex is a region whose role in language remains contro- versial almost a century and a half after it was first proposed. This region, called Broca’s area after the French neurologist who first proposed a role for it in articulate speech, is now referred to more generally in terms of its cytoarchitecture as Brodmann’s area 44 (BA44; sometimes referred to as encompassing areas 44 and 45; Hagoort, 2005). Theoretical perspectives of Broca’s area have changed considerably in recent years, informed by the results of neuroimaging studies indicating BA44 is active when subjects observe actions performed by both the mouth and hand (e.g., Baumgaertner, Buccino, Lange, McNamara, & Binkofski, 2007; Binkofski et al., 2000; Buccino, Binkofski, & Riggio, 2004a; Buccino et al., 2004b; Iacoboni et al., 1999; Molnar-Szakacs, Iacoboni, Koski, & Mazziotta, 2005; Nishitani & Hari, 2002; for reviews, see Binkofski & Buccino, 2006; Iacoboni, 2005; Nishitani, Schurmann, Amunts, & Hari, 2005; Rizzolatti & Craighero, 2004). The neuroim- aging investigations of the visuomotor properties of human BA44 were prompted by comparative neuroanatomy studies revealing it to have apparently similar cytoarchitectonic characteristics to premotor area F5 in the macaque monkey (Nelissen, Luppino, Vanduffel, Rizzolatti, & Orban, 2005; but see Petrides, 2005; for a critique of this evidence, see Toni, de Lange, Noordzij, & Hagoort, 2008). As area F5 contains a class of visuomotor neurons (called mirror neurons) that respond congruently when goal-directed mouth or hand actions are both observed and executed, some authors have proposed that it (and its putative human homologue BA44) might transform visual information into knowledge coded at an abstract level, i.e., it might be involved in understanding the ac- tion meaning (Nishitani et al., 2005; Rizzolatti & Craighero, 2004). A corollary to this theory is that the mirror neuron system (MNS) in Broca’s area might represent a mechanism linking speech and ges- tural communication (Arbib, 2005; Gallese & Lakoff, 2005; Gentil- ucci & Corballis, 2006; Nishitani et al., 2005; Rizzolatti & Arbib, 1998). At least two alternative explanations have been proposed for the activity elicited in BA44 when actions are observed. The first is referred to as the ‘‘verbalization hypothesis” (see Buccino et al., 2001; Grèzes & Decety, 2001; Iacoboni, 2005; Iacoboni & Dapretto, 2006). This explanation acknowledges a role for Broca’s area in speech production and proposes that the activity reflects an internal verbalization of the observed actions; similar to the activity detected during verbally instructed motor preparation 0093-934X/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.bandl.2008.09.011 * Corresponding author. Fax: +61 7 3365 3833. E-mail address: greig.dezubicaray@cmr.uq.edu.au (G. de Zubicaray). Brain and Language xxx (2008) xxx–xxx Contents lists available at ScienceDirect Brain and Language journal homepage: www.elsevier.com/locate/b&l ARTICLE IN PRESS Please cite this article in press as: de Zubicaray, G., et al. Mirror neurons, the representation of word meaning, and the foot ... Brain and Language (2008), doi:10.1016/j.bandl.2008.09.011