The process of monitored output inhibition at layer 4 of the shared circuits model (SCM) predicts inhibitory and monitoring mechanisms at the neural level. The question that SCM leaves unresolved is whether, among these inhibitory neural mechanisms, there may be some neurons that are specialized in the inhibition and monitoring of mirroring cells. Clearly, layers 2+4 cannot be exclusively implemented by specialized inhibitory mirroring neurons. Indeed, the function of offline predictive simulation distinguishing actual from possible acts can be applied to all sorts of potential actions, including those directed at inanimate objects (say, a mug), which we plan for ourselves when we are alone (say, in our office). The neural mechanisms implementing layers 3+4, however, could be either general-purpose inhibitory mechanisms that may also be applied to the inhibition of overt copying or specialized inhibitory mechanisms for mirroring.
We have performed depth electrode recordings in the mesial wall of the human frontal cortex in patients with epilepsy undergoing pre-surgical evaluation of the foci of epilepsy (Mukamel et al. Reference Mukamel, Ekstrom, Kaplan, Iacoboni and Fried2007). From a total of 14 patients, we have recorded the activity of approximately 500 neurons located in three sectors of the mesial frontal cortex: the ventral and dorsal sectors of the anterior cingulate cortex and the pre-supplementary motor cortex (SMA)/SMA proper complex. Activity from individual human neurons was recorded while subjects were performing and observing hand-grasping actions, performing and observing facial emotional expressions, and during control conditions. Mirror neurons were defined as follows: Reliable firing-rate changes were measured during execution and during observation of hand-grasping actions or of facial emotional expressions, but not during the control conditions. We found that approximately 12% of all recorded mesial frontal neurons had mirror properties. Individual neurons with mirror properties were observed in all recording sites in the mesial frontal cortex. This suggests that mirror neurons are widespread in the human frontal lobe. Among these cells, approximately 50% were mirror neurons for hand-grasping actions, whereas the other 50% were mirror neurons for facial emotional expressions. One-third of mirror neurons had excitatory responses during both action execution and action observation. This is the most typical pattern of firing-rate changes observed in monkeys. One-third of mirror neurons, however, had inhibitory responses during both action execution and action observation. This pattern has also been occasionally observed in monkeys, but much less frequently. The remaining third of mirror neurons in the human frontal cortex had a pattern of firing-rate changes that has never been observed in monkeys, at least not so far. The large majority of mirror neurons (more than 80%) have excitatory responses during action execution and inhibitory responses during action observation. Few of these neurons have the opposite pattern, with decreased firing rate during execution and increased firing rate during observation. We call these cells super mirror neurons (Iacoboni & Dapretto Reference Iacoboni and Dapretto2006), not because they have super powers, but because they seem to have a modulatory role over activity in more “classical” frontal mirror neurons, that is, those mirroring cells located in the lateral inferior frontal cortex (Rizzolatti & Craighero Reference Rizzolatti and Craighero2004).
The mesial frontal areas we recorded from are anatomically connected with the lateral inferior frontal areas containing “classical” mirror neurons (Rizzolatti & Luppino Reference Rizzolatti and Luppino2001). The physiological properties of the mirror neurons in mesial frontal cortex and the anatomical connectivity between these areas and the lateral inferior frontal cortex containing classical mirror neurons suggest that this mesial frontal mirror neuron system has prevalently inhibitory functions, such that overt copying is inhibited. In line with other models (Iacoboni Reference Iacoboni2008), SCM suggests that this inhibition of overt copying allows the distinction between the actions of self and other. Several imaging studies that investigated the neural basis of complex self-related concepts have suggested a critical role of mesial frontal areas in implementing such concepts (e.g., Uddin et al. Reference Uddin, Iacoboni, Lange and Keenan2007; Vogeley & Fink Reference Vogeley and Fink2003). Taken together, these theoretical considerations and empirical data support the view that the practical simulative foundations of the SCM's subpersonal functional level may be used to build explicit reasoning and theoretical deliberation.
The physiological properties of the human mesial frontal mirror neurons and their widespread anatomical location support the concept of pervasive mirroring. A fundamental way of connecting with others and even defining the self is by means of mirroring people (Iacoboni Reference Iacoboni2008).
