Yet another post on RC's much cited paper -- 517 citations so far, according to Google Scholar.
Mirror Neurons in Humans
As we all know, direct evidence for the existence of MNs in humans is completely lacking because you can't record from single cells in humans all that readily. But let's not get hung up on this technicality, and grant that such cells probably exist. So assuming this, RC point out that human MNs are different from monkey MNs, in two ways:
1. The human mirror system does not require the presence of an object-directed action. It will respond to meaningless intransitive gestures.
2. The human mirror system, in addition to its assumed function in action understanding, also supports imitation.
I have no problem with the idea that a system might change from one species to the next, so I don't object to the idea that the mirror system might be different in humans. But it does mean that important properties found in MNs in monkeys, such as the fact that they don't seem to be involved in boring old movement preparation, can't automatically be generalized to humans. You've got to do the experiments.
Another general point worth making is that when we think in terms of evolution, we have to remember that human mirror neurons did not evolve from macaque mirror neurons. Rather the behavior of human mirror neurons (assuming they exist) and macaque mirror neurons evolved from neurons of some type that existed in our most recent common ancestor, which lived about 25 million years ago. It is therefore a mistake to think of the human "mirror system" as evolving from macaque mirror neurons.
Where is the human mirror system? According to RC, the "core" of it is "the rostral art of the inferior parietal lobule and the lower part of the precentral gyrus plus the posterior part of the inferior frontal gyrus" (p. 176). This is based on a number of studies cited on page 176. A good discussion of anatomy follows on the next page or so. Worth reading for sure.
On page 179, RC discuss an interesting fMRI study by Buccino et al. (2004, JoCN, 16-1-14). Subjects watched video clips of silent mouth actions performed by humans, monkeys, and dogs. There were two types of actions: biting, and oral communicative gestures (speech, lip smacking, and barking for human, monkey, and dogs, respectively). Biting activated the inferior parietal lobule, pars opercularis and precentral gyrus independent of species (some slight hemispheric asymmetries were found though). Communicative gestures yielded a different pattern: Speech and lip smacking activated the pars opercularis, whereas barking "did not produce any frontal lobe activation" (p. 179).
You know what I'm going to say. Presumably, subjects in this study understood the barking actions. Yet this was achieved without the activation of the mirror system. Mirror neurons, therefore, are not necessary for action understanding.
RC have a different spin. "Actions belonging to the motor repertoire of the observer are mapped on his/her motor system. Actions that do not belong to this repertoire do not excite the motor system of the observer and appear to be recognized essentially on a visual basis without motor involvement. It is likely that these two different ways of recognizing actions have two different psychological counterparts. In the first case the motor 'resonance' translates the visual experience into an internal 'personal knowledge'... whereas this lacking in the second case" (p. 179).
Ok, so following this reasoning, mirror neurons are not the basis of action understanding, because that can be achieved "on a visual basis without motor involvement", but instead are the basis of "internal knowledge" of an action. In other words, they are the neural correlate of the psychological experience, "hey, I can do that too!" I wonder if mirror neurons would be as popular as they are if their discoverers claimed that they were the neural basis of "internal knowledge" of perceived actions, rather than the neural basis of action understanding.
Notice now, that we have a double-dissociation between action understanding and mirror system activity in humans. The mirror system can be activated during the perception of actions that are meaningless (and therefore don't lead to understanding), and action understanding can be achieved without activation of the mirror system (viewing a barking dog).
Incidentally, the same double-dissociation has long been documented in the aphasia literature, and in a more forceful fashion. Severe Broca's aphasics can understand speech in the absence of a frontal mirror system, whereas patients with transcortical sensory aphasia (or better yet, the syndrome reported by Geschwind as "isolation of the speech area") can imitate speech quite well indicating an intact mirror system, but without the ability to comprehend it.