This week in our Mirror Neuron course we looked over some papers in the apraxia literature, which seemed to hold the promise of providing evidence in support of the MN theory of action understanding. Specifically, based on some of the abstracts, I thought we would find (i) that disorders to gesture production would be strongly associated with disorders of gesture understanding, and (ii) that damage to the frontal (putative) mirror neuron system should be associated with these production/comprehension disorders.
Instead, and despite the conclusions of some of the authors, the papers we read made a pretty decent case against the MN theory of action understanding.
First of all, it is very clear that deficits in gesture production/imitation dissociate from the ability to comprehend gestures. For example, Table 4 of Tessari et al. 2007 (Brain, 130:1111-26) shows data that includes eight (8) patients (out of a sample of 32 left hemisphere patients), who are performing at 60% correct or less on action imitation, while recognizing actions at 90% or better. Case 27, is a dramatic example, with only 10% correct imitations of meaningful actions and 100% correct on action recognition. It's possible, though, that imitation deficits in such cases result from some relatively peripheral motor control mechanism that is outside the mirror system proper. This is reasonable, but then I have to wonder whether data from say, motor evoked potentials, which are touted as strong evidence for the mirror system (and which might be considered rather peripheral!), should now be discounted for being peripheral to the mirror system. In other words, you can't point to a very peripheral response like MEPs and call it evidence for mirror neurons, and then turn around and explain imitation deficits caused by (non-M1) cortical damage as arising from systems that are peripheral to the mirror system.
In other, other words, it's time to be explicit about what components of the motor system are part of the mirror system. As it stands, "mirror neuron theory" is effectively untestable because any result just gets folded into the mythology: humans show "mirror" responses for pantomimed gestures (unlike macaque F5 cells)? That's because humans are more sophisticated than monkeys. The STS responds just as selectively (more so!) to perceived actions than F5? That's because it inherits its mirror properties from the real mirror system. Passive viewing of non-action stimuli (rectangles with dots in them) activates the mirror system? That's because of motor imagery associated with the non-action stimuli. Mirror neuron theorizing is starting to remind me of one of those house-of-mirrors attractions at the county fair: Mirrors everywhere, but mostly reflecting nothing.
But I digress... Let's focus on the two papers that seem to make the best case for action understanding deficits associated with lesions to the inferior frontal gyrus.
Saygin et al. studied the ability of aphasic patients to understand action-related pictures. Ok, not exactly action understanding (pictures are static), but let's assume that these pictures induced action percepts/concepts. Subjects viewed actions with the object of the action removed, such as a boy licking an ice cream cone, but with no ice cream cone in his hand. Subjects then had to pick the matching object out of an array of two pictured objects which included the target (ice cream cone) and a distractor. Distractors included (on different trials) semantically related items (cake), "affordance" related items (a bouquet of flowers which is held in a similar manner but not normally licked), or an unrelated item (rooster). A matched verbal version of the task was also administered in which subjects read sentence fragments ("He is licking the _____") and had to pick the correct picture, as above.
The results were quite interesting: (i) performance on the two task was completely uncorrelated (after the one outlier patient was removed), showing that action understanding is domain-specific. (ii) lesion analysis revealed that deficits on the pictorial task were correlated with lesions in the inferior frontal gyrus, whereas deficits on the linguistic task were correlated with a different distribution of lesions that was more posterior and involved the anterior temporal lobe (interesting for other reasons). So both behavioral and brain data show these two tasks dissociate, and pictorial action understanding is associated with the frontal "mirror system." The results were interpreted as support for the mirror neuron theory of action understanding.
But this is an odd theoretical position. Apparently, the ability to understand actions generally, is dependent on the sensory signals that access that action-concept information. That is, having a deficit in the ability to understand actions from action depictions, does not prevent you from accessing action-concepts via a verbal route. Put another way, damage to your mirror neuron system (the frontal lesions associated with pictorial action understanding deficits) leaves action-concepts (action understanding) intact, as evidenced by the fact that you can access them via another input route. Therefore, the representation of action meaning (the understanding part) is not in the motor representation, but is somewhere else. At most the motor system may facilitate access to the meaning of actions. But these data show that the semantics of action is NOT inherent to the motor system. Alternatively, the correlation with frontal lobe structures for this action understanding task, may have more to do with making complex inferences from static ambiguous pictures (have a look at the sample stimulus item in the paper -- the "licking boy" could just as easily be smiling real big, or have a fat lip).
Enough for now. I'll comment in the next post on the strongest evidence we've seen so far for the MN theory of action understanding. (Turns out its not so strong.)