Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements Michela Romani, a Paola Cesari, b Cosimo Urgesi, a Stefano Facchini, a and Salvatore Maria Aglioti c, T a Dipartimento di Scienze Neurologiche e della Visione, Sezione di Fisiologia Umana, Universita ` degli studi di Verona, Strada le Grazie 8, 37134, Verona, Italy b Facolta ` di Scienze Motorie, Universita ` degli studi di Verona, Via Casorati 43, Verona, Italy c Dipartimento di Psicologia, Universita ` di Roma bLa SapienzaQ and IRCCS, Fondazione Santa Lucia, Via dei Marsi 78, 00185, Roma, Italy Received 15 September 2004; revised 11 February 2005; accepted 17 February 2005 Available online 31 March 2005 Neurophysiological and neuroimaging studies in the human and the monkey brain indicate that links between action observation and execution are much tighter than previously believed. Indeed, the mere observation of movements performed by other individuals brings about a clear increase in activity in specific fronto-parietal neural networks (mirror system). Here, we report a series of four single-pulse trans- cranial magnetic stimulation studies of the motor system, which show that observation of index and little finger movements brings about a facilitation of potentials recorded from muscles that would be involved in the actual execution of the observed action. Remarkably, however, a clear representational selectivity was found also during observation of bio-mechanically impossible index or little finger movements. Thus, in movement observation tasks, the human cortico-spinal system reacts similarly to the vision of bio-mechanically possible and impossible movements but it is able to detect which muscle would be involved in the actual execution of the observed movement. Importantly, this system may be more related to coding body part movements than precisely simulating their execution. D 2005 Elsevier Inc. All rights reserved. Keywords: Action observation; Bio-mechanically impossible finger movements; TMS; Mirror systems; Body image; Cortico-spinal motor excitability Introduction It has long been thought that cortical frontal areas are involved in motor planning and execution and posterior cortical regions in the processing of sensory inputs. Recent important neurophysio- logical studies in awake monkeys have shown that neurons in cortical frontal areas are not only recruited during action execution and planning but also during observation of actions performed by other individuals (di Pellegrino et al., 1992; Gallese et al., 1996; Rizzolatti et al., 1996a). The discovery of these visuo-motor neurons, called bmirror neuronsQ, has radically changed the notion of well-separate neural substrates for sensory and motor processing by suggesting that perception and action are much more tightly linked than previously believed. Based on evidence supporting the existence of mirror systems in humans (Buccino et al., 2001; Calvo-Merino et al., 2005; Cochin et al., 1999; Grafton et al., 1996; Grezes et al., 1999; Hari et al., 1998; Iacoboni et al., 1999; Rizzolatti et al., 1996b), it has been postulated that observation– execution matching systems play an important role in a number of processes ranging from observational learning to imitation and action understanding (Rizzolatti et al., 1996a, 2001). Transcranial magnetic stimulation (TMS) studies provide evidence that action observation triggers specific facilitation of the muscles that would be involved in the actual execution of the observed movement (Fadiga et al., 1995; Strafella and Paus, 2000). This supports the notion that action execution is directly mapped onto the observer’s motor system. In keeping with this view is the finding that motor facilitation induced by observation is higher for natural than unnatural hand orientations (Maeda et al., 2002) and for live acts rather than for video-clips (Jarvelainen et al., 2001). Also interesting is the result that while observation of actions performed by virtual hands activates only lateral occipital cortices with mainly sensory functions, observation of actions performed by a real hand activates a visuo-spatial network involved in action representation (Perani et al., 2001). Relevant to the present research is that humans can bconceiveQ movements they cannot perform such as actions they have never learned, for example, very complex acrobatic exercises or impeccable tennis serves. It is even possible to try to imagine movements that can never be performed because of the constraints of human anatomy. Thus, knowing what to do does not always imply knowing how to do it. By using single-pulse TMS, we compared cortico-spinal neural activity contingent upon observa- tion of bio-mechanically possible movements, commonly per- formed and seen in daily life, and observation of similar but bio- 1053-8119/$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2005.02.027 T Corresponding author. Fax: +39 06 49917535. E-mail address: salvatoremaria.aglioti@uniroma1.it (S.M. Aglioti). Available online on ScienceDirect (www.sciencedirect.com). www.elsevier.com/locate/ynimg NeuroImage 26 (2005) 755 – 763