Abstract. Mirror neurons within a monkey’s premotor area F5 fire not only when the monkey performs a certain class of actions but also when the monkey observes another monkey (or the experimenter) perform a similar action. It has thus been argued that these neurons are crucial for understanding of actions by others. We offer the hand-state hypothesis as a new explanation of the evolution of this capability: the basic functionality of the F5 mirror system is to elaborate the appropriate feedback – what we call the hand state – for opposition-space based control of manual grasping of an object. Given this functionality, the social role of the F5 mirror system in understanding the actions of others may be seen as an exaptation gained by generalizing from one’s own hand to an other’s hand. In other words, mirror neurons first evolved to augment the ‘‘canonical’’ F5 neurons (active during self-movement based on observation of an object) by providing visual feedback on ‘‘hand state,’’ relating the shape of the hand to the shape of the object. We then introduce the MNS1 (mirror neuron system 1) model of F5 and related brain regions. The existing Fagg–Arbib–Rizzolatti–Sakata model represents circuitry for visually guided grasping of objects, linking the anterior intraparietal area (AIP) with F5 canonical neurons. The MNS1 model extends the AIP visual pathway by also modeling pathways, directed toward F5 mirror neurons, which match arm– hand trajectories to the affordances and location of a potential target object. We present the basic schemas for the MNS1 model, then aggregate them into three ‘‘grand schemas’’ – visual analysis of hand state, reach and grasp, and the core mirror circuit – for each of which we present a useful implementation (a non-neural visual processing system, a multijoint 3-D kinematics simula- tor, and a learning neural network, respectively). With this implementation we show how the mirror system may learn to recognize actions already in the repertoire of the F5 canonical neurons. We show that the connec- tivity pattern of mirror neuron circuitry can be estab- lished through training, and that the resultant network can exhibit a range of novel, physiologically interesting behaviors during the process of action recognition. We train the system on the basis of final grasp but then observe the whole time course of mirror neuron activity, yielding predictions for neurophysiological experiments under conditions of spatial perturbation, altered kine- matics, and ambiguous grasp execution which highlight the importance of the timing of mirror neuron activity. 1 Introduction 1.1 The mirror neuron system for grasping The macaque inferior premotor cortex has been identi- fied as being involved in reaching and grasping move- ments (Rizzolatti et al. 1988). This region has been further partitioned into two subregions: F5, the rostral region, located along the arcuate part; and F4, the caudal part (see Fig. 1). The neurons in F4 appear to be primarily involved in the control of proximal move- ments (Gentilucci et al. 1988), whereas the neurons of F5 are involved in distal control (Rizzolatti et al. 1988). Rizzolatti et al. (1996a) and Gallese et al. (1996) discovered a subset of F5 hand cells, which they called mirror neurons. Like other F5 neurons, mirror neurons are active when the monkey performs a particular class of actions, such as grasping, manipulating, and placing. However, in addition the mirror neurons become active when the monkey observes the experimenter or another monkey performing an action. The term F5 canonical neurons is used to distinguish the F5 hand cells which do not posses the mirror property but are instead responsive to visual input concerning a suitably graspable object. The canonical neurons are indistinguishable from the mirror neurons with respect to their firing during self- action. However they are different in their visual prop- erties – they respond to object presentation and not action observation per se (Murata et al. 1997). Correspondence to: M.A. Arbib (e-mail: arbib@pollux.usc.edu) Biol. Cybern. 87, 116–140 (2002) DOI 10.1007/s00422-002-0318-1 Ó Springer-Verlag 2002 Schema design and implementation of the grasp-related mirror neuron system Erhan Oztop, Michael A. Arbib USC Brain Project, University of Southern California, Los Angeles, CA 90089-2520, USA Received: 6 August 2001 / Accepted in revised form: 5 February 2002