Neural Networks 19 (2006) 254–271 www.elsevier.com/locate/neunet 2006 Special issue Mirror neurons and imitation: A computationally guided review Erhan Oztop a,b,*, Mitsuo Kawato a,b, Michael Arbib c a JST-ICORP Computational Brain Project, Kyoto, Japan b ATR, Computational Neuroscience Laboratories, 2-2-2 Hikaridai Seika-cho, Soraku-gun, Kyoto 619-0288, Japan c Computer Science, Neuroscience and USC Brain Project, University of Southern California, Los Angeles, CA 90089-2520, USA Abstract Neurophysiology reveals the properties of individual mirror neurons in the macaque while brain imaging reveals the presence of ‘mirror systems’ (not individual neurons) in the human. Current conceptual models attribute high level functions such as action understanding, imitation, and language to mirror neurons. However, only the first of these three functions is well-developed in monkeys. We thus distinguish current opinions (conceptual models) on mirror neuron function from more detailed computational models. We assess the strengths and weaknesses of current computational models in addressing the data and speculations on mirror neurons (macaque) and mirror systems (human). In particular, our mirror neuron system (MNS), mental state inference (MSI) and modular selection and identification for control (MOSAIC) models are analyzed in more detail. Conceptual models often overlook the computational requirements for posited functions, while too many computational models adopt the erroneous hypothesis that mirror neurons are interchangeable with imitation ability. Our meta-analysis underlines the gap between conceptual and computational models and points out the research effort required from both sides to reduce this gap. q 2006 Elsevier Ltd. All rights reserved. Keywords: Mirror neuron; Action understanding; Imitation; Language; Computational model 1. Introduction to be transitive, i.e. to involve action upon an object and apply even to an object just recently hidden from view (e.g. Umilta Many neurons in the ventral premotor area F5 in macaque et al., 2001). monkeys show activity in correlation with the grasp1 type It is not possible to find individual mirror neurons in humans being executed (Rizzolatti, 1988). A subpopulation of these since electrophysiology is only possible in very rare cases and neurons, the mirror neurons (MNs), exhibit multi-modal at specific brain sites in humans. Therefore, one usually talks properties responding to the observation of goal directed about a ‘mirror region’ or a ‘mirror system’ for grasping movements performed by another monkey or an experimenter identified by brain imaging (PET, fMRI, MEG, etc.). Other (e.g. precision or power grasping) for grasps more or less regions of the brain may support mirror systems for other congruent with those associated with the motor activity of the classes of actions. An increasing number of human brain neuron (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; mapping studies now refer to a mirror system (although not all Rizzolatti, Fadiga, Gallese, & Fogassi, 1996). The same area are conclusive). Collectively these data indicate that action includes auditory mirror neurons (Kohler et al., 2002) that observation activates certain regions involved in the execution respond not only to the view but also to the sound of actions of actions of the same class. However, in contrast to monkeys, with typical sounds (e.g. breaking a peanut, tearing paper). intransitive actions have also been shown to activate motor The actions associated with mirror neurons in the monkey seem regions in humans. The existence of a (transitive and intransitive) mirror system in the human brain has also been supported by behavioral experiments illustrating the so-called * Corresponding author. Address: Department of Cognitive Neuroscience, ‘motor interference’ effect where observation of a movement ATR, Computational Neuroscience Laboratories, 2-2-2 Hikaridai Seika-cho, degrades the performance of a concurrently executed incon- Soraku-gun, Kyoto 619-0288, Japan. Tel.: C81 774 95 1215; fax: C81 774 95 1236. gruent movement (Brass, Bekkering, Wohlschlager, & Prinz, E-mail address: [email protected] (E. Oztop). 2000; Kilner, Paulignan, & Blakemore, 2003; see also Sauser 1 We restrict our discussion to hand-related neurons; F5 contains mouth- & Billard, this issue, for functional models addressing this related neurons as well. phenomenon). Because of the overlapping neural substrate for 0893-6080/$ - see front matter q 2006 Elsevier Ltd. All rights reserved. action execution and observation in humans as well as other doi:10.1016/j.neunet.2006.02.002 primates, many researchers have attributed high level cognitive E. Oztop et al. / Neural Networks 19 (2006) 254–271 255 functions to MNs such as imitation (e.g. Carr, Iacoboni, yielding mirror neurons as a byproduct of the evolutionary Dubeau, Mazziotta, & Lenzi, 2003; Miall, 2003), action process (Borenstein & Ruppin, 2005); the mirror neuron understanding (e.g. Umilta et al., 2001), intention attribution system (MNS) model that can learn to ‘mirror’ via self- (Iacoboni et al., 2005) and—on the finding of a mirror system observation of grasp actions (Oztop & Arbib, 2002) and is for grasping in or near human Broca’s area—(evolution of) closely linked to macaque behavior and (somewhat more language (Rizzolatti & Arbib, 1998).2 loosely) neurophysiology; and models which are not restricted We stress that, although statements are often made about in this fashion: the mental state inference (MSI) model that mirror neurons in humans, we have data only on what might be builds on the forward model hypothesis of mirror neurons called mirror systems in humans—connected regions that are (Oztop, Wolpert, & Kawato, 2005), the modular selection and active in imaging studies both when the subject observes an identification for control (MOSAIC) model that utilizes action from some set and executes an action from that set, but multiple predictor–controller pairs (Haruno, Wolpert, & not during an appropriate set of control tasks. Brain imaging Kawato, 2001; Wolpert & Kawato, 1998), and the imitation results show that mirror regions in human may be associated architecture of Demiris and Hayes (2002) and Demiris and with imitation and language (Carr et al., 2003; Fadiga, Johnson (2003). Craighero, Buccino, & Rizzolatti, 2002; Iacoboni et al., 1999; Skipper, Nusbaum, & Small, 2005), but there are no 2. Mirror neurons and action understanding corresponding data on mirror neurons. Moreover, monkeys do not imitate (but see below) or learn language and so any Mirror neurons, when initially discovered in macaques, account of the role of mirror neurons in imitation and language were thought to be involved in action recognition (Fogassi must include an account of the evolution of the human mirror et al., 1992; Gallese et al., 1996; Rizzolatti et al., 1996) though system (Rizzolatti & Arbib, 1998) or at least the biological this laid the basis for later work ascribing a role in imitation to triggers that can unleash in monkeys a rudimentary imitation the human mirror system. Although the term ‘action under- capability that goes beyond those they normally exhibit, though standing’ was often used, the exact meaning of ‘understanding’ still being quite limited compared to those of humans as used here is not clear. It can range from ‘act according to (Kumashiro et al., 2003). We thus argue that imitation and what you see’, to ‘infer the intentions/mental states leading to language are not inherent in a macaque-like mirror system but the observed action’. In fact, the neurophysiological data instead depend on the embedding of circuitry homologous to simply show that a mirror neuron fires both when the monkey that of the macaque in more extended systems within the executes a certain action and when he observes more or less congruent actions. In these experiments, he is given no human brain. opportunity to show by his behavior that he understands the A general pitfall in conceptual modeling is that an innocent action in either of the above senses. looking phrase thrown in the description may render the model Gallese and Goldman (1998) suggested that the purpose of implausible or trivial from a computational perspective, hiding MNs is to enable an organism to detect certain mental states of the real difficulty of the problem. For example, terms like observed conspecifics via mental simulation. According to this ‘direct matching’ and ‘resonance’ are used as if they were view, mirror neurons could be the precursor of mind-reading atomic processes that allow one to build hypotheses about ability, being compatible with the simulation theory higher cognitive functions of mirror neurons (Gallese, Keysers, hypothesis.3 Again, this involves considerable extrapolation & Rizzolatti, 2004; Rizzolatti, Fogassi, & Gallese, 2001). One beyond the available data. In particular, mind-reading might must explain the cortical mechanisms which support the involve a quite separate mirror system for facial expression as several processing stages that transform retinal stimulation much as a mirror system for manual actions. Although the caused by an action observation into the mirror neuron suggestion has achieved some positive reception, no details responses. Another issue is to clarify what is encoded by the have been provided on how this could be implemented as a mirror neuron activity. Is it the motor command, the meaning computational model. (The MSI model does address this issue, or the intention of the observed action? In an