All smoke and mirror neurons?

Photo by Flickr user Mike_in_Kboro. Click for sourceNew Scientist has a tantalising snippet reporting on a shortly to be released and potentially important new study challenging the idea of ‘mirror neurons’.

Mirror neurons fire both when we perform an action and when we see someone else doing it. The theory is that by simulating action even when watching an act, the neurons allow us to recognise and understand other people’s actions and intentions…

However, Alfonso Caramazza at Harvard University and colleagues say their research suggests this theory is flawed.

Neurons that encounter repeated stimulus reduce their successive response, a process called adaptation. If mirror neurons existed in the activated part of the brain, reasoned Caramazza, adaptation should be triggered by both observation and performance.

To test the theory, his team asked 12 volunteers to watch videos of hand gestures and, when instructed, to mimic the action. However, fMRI scans of the participants’ brains showed that the neurons only adapted when gestures were observed then enacted, but not the other way around.

Caramazza says the finding overturns the core theory of mirror neurons that activation is a precursor to recognition and understanding of an action. If after executing an act, “you need to activate the same neurons to recognise the act, then those neurons should have adapted,” he says.

The study is to appear in the Proceedings of the National Academy of Sciences and apparently is embargoed so the full text is not yet available, although it should appear here when it is.

The announcement is interesting because using adaptation is a novel way of testing ‘mirror neurons’ and the lead researcher, Alfonso Caramazza, is known for a long series of influential neuropsychology studies.

He has a reputation for being a sober and considered scientist so it will be interesting to see if the final study is really the challenge to mirror neurons as it seems.

Although the hype has subsided a little, the years following the initial reports saw these now famous neurons being used to explain everything from language, to empathy, to why we love art.

We’re now in a period where we’re taking, if you’ll excuse the pun, a somewhat more reflective look at the topic and developing more nuanced theories about how this brain system functions.

UPDATE: Grabbed from the comments. Looks like this paper might have the potential to cause a ruckus. A comment from mirror neuron researcher Marco Iacoboni:

Caramazza‚Äôs paper is seriously flawed. The technique of fMRI adaptation seemed very promising ten years ago, but careful studies on its neurophysiological correlates have demonstrated that its findings are uninterpretable. Indeed, Caramazza‚Äôs manuscript has been around for many years and nobody wanted to publish it. Caramazza managed to publish with an old trick that only PNAS allows: he handed it personally to a friend of his. The paper is basically unrefereed (this is what it means ‚ÄòEdited by…‚Äô under its title).

Link to NewSci on ‘Role of mirror neurons may need a rethink’.

10 Comments

  1. Posted May 27, 2009 at 3:06 pm | Permalink

    Caramazza‚Äôs paper is seriously flawed. The technique of fMRI adaptation seemed very promising ten years ago, but careful studies on its neurophysiological correlates have demonstrated that its findings are uninterpretable. Indeed, Caramazza‚Äôs manuscript has been around for many years and nobody wanted to publish it. Caramazza managed to publish with an old trick that only PNAS allows: he handed it personally to a friend of his. The paper is basically unrefereed (this is what it means ‚ÄòEdited by…‚Äô under its title).

  2. Posted May 28, 2009 at 12:20 am | Permalink

    Of course, most of the ‘direct’ evidence for mirror neurons in humans comes from studies showing that the same fMRI voxels are activated by observed and executed actions. How interpretable is that, given that a single voxel may contain several hundred thousand neurons? Fundamentally, you need to get beyond such primitive designs if you really want to directly test the existence of mirror neurons in humans. fMRI adaptation isn’t perfect, but the technique is certainly far from ‘uninterpretable’. However, we really need adaptation designs in the single unit studies in order to avoid comparing across species, designs (adaptation vs direct response) and methods (neurophys vs fMRI) all at once.
    Note that this is not the first study to use fMRI adaptation to study mirror neurons – see Chong et al in Current Biology 2008 – http://dx.doi.org/10.1016/j.cub.2008.08.068
    Amusingly, these authors find the opposite pattern as Caramazza et al appear to have found – adaptation crosses over from executed to observed actions in IPL, but not the other way around. This makes little sense for a canonical mirror neuron representation. It’s a little unclear so far which area Caramazza et al studied, however.
    Dinstein et al, also failed to find execution-observation cross-over using multivariate pattern analysis, so the effect is not an artefact of fMRI adaptation as such – http://www.jneurosci.org/cgi/content/abstract/28/44/11231
    Basically, if you want to compare the similarity of representations in humans (and this is indeed the only way to address the mirror neuron hypothesis), your only current options are fMRI adaptation and multivariate pattern analysis. They both come with their limitations, but if neither method succeeds in producing evidence for a mirror neuron representation, one has to begin to wonder how such an elusive representation can play such a key role in nigh on all human social cognitive processing, as Iacoboni and colleagues like to suggest.
    See also a recent review by Hikock (2008): http://www.mitpressjournals.org/doi/abs/10.1162/jocn.2009.21189

  3. Posted May 28, 2009 at 6:12 am | Permalink

    What phineasgage says is wrong. Both multivariate pattern analysis and fMRI adaptation have serious intepretational limitations, see Bartels, Logothetis and Moutoussis, “fMRI and its interpretation: an illustration on directional selectivity in area V5/MT” Trends in Neurosciences 2008; 31: 444-453. In short: the fMRI signal is influenced by three factors: the action potentials of neurons (what Caramazza was after in his study), the local field potential (an index of synaptic input), and global modulatory factors. The only reasonable way for fMRI to make inferences on action potentials is to have all these parameters correlating with each other. Traditional subtraction designs most likely do that (I don’t have space here to explain why), adaptation paradigms by definition don’t do that because they change synaptic efficacy, which is invariably associated with a decoupling between action potentials and local field potential. When action potentials and local field potential do not correlate, the fMRI signal correlates with the local field potential, not the action potential. This means that Caramazza is not imaging action potentials. And guess what? Mirror neurons are defined by patterns of action potential activity. I hope this helps understanding the issues.

  4. Tom
    Posted May 28, 2009 at 2:33 pm | Permalink

    iacoboni says “Caramazza managed to publish with an old trick that only PNAS allows: he handed it personally to a friend of his. The paper is basically unrefereed (this is what it means ‚ÄòEdited by…‚Äô under its title).”
    This completely wrong. ‘Edited by…’ after the title just tells you the name of the member editor. All PNAS papers are peer reviewed, but there are two submission routes. If it says ‘Communicated by…’ then it means it was submitted by a member (either on their own or someone else’s behalf) who has obtained reviews before submission. This pretty much guarantees acceptance, I imagine. Alternatively, if the paper is a ‘Direct submission’ (which most are these days, including Caramazza’s last PNAS paper) this means it will have been considered by the editorial board, then fully and anonymously peer reviewed, just like with any other journal. Wait until you know what route it was submitted under (and maybe even read the thing) before you start trashing it.

  5. Posted May 28, 2009 at 2:59 pm | Permalink

    In the past, there used to be three ways of submitting papers to PNAS. Direct submission did not mean ‘submitted as any other journal.’ Track II meant submitted ‘as any other journal.’ Caramazza’s paper is not defined as Track II. In the past, direct submission meant that Caramazza contacted Smith and Smith accepted to function as an Editor. ‘Communicated by’ meant that a member submit his or her own paper. However, I just checked the website http://www.pnas.org/ and the description of the submission procedure is changed a bit. It’s not clear to me if Tom is correct, but definitely there is no mention of Track II anymore, so he may be right. In this case, my apologies to Caramazza and the readers of this blog. However, the scientific problems of the paper remain. See also Sawamura et al, Neuron 2006; 49: 307-318.

  6. Ross Cunnington
    Posted May 29, 2009 at 1:29 am | Permalink

    This study of Caramazza, finding adaptation effects when observing and then execution actions, sounds exciting. I will be very interested to see the full paper.
    As mentioned in the earlier post, we also found fMRI adaptation in the IPL when participants first executed actions then observed the same actions (Chong, et al, 2008, Current Biology) – replicated in two separate studies. Interestingly, Caramazza’s result, as reported here, seems to be the other way around.
    Of course, for true mirror neurons we would expect neural adaption no matter what order actions are observed/executed. Across the two studies, it now seems that there may be evidence for this (although without seeing Caramazza’s full paper, we should be cautious about passing judgement).

  7. ah
    Posted May 30, 2009 at 2:55 pm | Permalink

    It is not clear to me why Marco is making such an important distinction between measuring action potentials and measuring local field potentials. Different neuroimaging techniques (fMRI, MEG, EEG) measure slightly different things but we are able to deal with that. All these techniques measure the correlates of neural processing (of slightly different forms), and I think we do not yet have the luxury of being fussy. None of the methods are perfect (see Friston et al, NeuroImage 1996 for limits of fMRI subtraction), so I see no reason to dismiss the repetition suppression or multivariate methods out of hand.
    As for the question of whether mirror neurons really exist in humans, well, probably. I think the question of what they might mean for social cognition is more important.
    Antonia Hamilton
    (disclosure – I have several repetition suppression papers published).

  8. gob
    Posted June 3, 2009 at 7:12 pm | Permalink

    It is interesting that Dr. Iacoboni is critical of a PNAS submission track that he himself appears to have used.

    http://www.pnas.org/content/98/24/13995.abstract

  9. Posted June 8, 2009 at 4:12 am | Permalink

    gob – The paper you link to does not have the same submission method as Caramazza’s.
    Caramazza’s: “Edited by Edward E. Smith, Columbia University, New York, NY, and approved April 24, 2009 (received for review February 28, 2009)”; “This article is a PNAS Direct Submission.”
    Your link: “Communicated by James M. Sprague, University of Pennsylvania School of Medicine, Philadelphia, PA (received for review August 9, 2001)”; no equivalent of the ‘direct submission’
    I know nothing of PNAS’ submission tracks and thus make no claim as to what these mean; I am just pointing out that they’re clearly different.

  10. gob
    Posted July 7, 2009 at 1:42 am | Permalink

    I am referring to Iacoboni’s criticism that “Caramazza managed to publish with an old trick that only PNAS allows: he handed it personally to a friend of his.”
    Yes, the two tracks are different, but it is the “Communicated By” track which actually describes what Iacaboni is criticizing, and that is the one that he, not Caramazza, has used (at least for the papers in question). See Tom’s post above, and the PNAS website. If nothing else, this is a nice clinic on PNAS submission tracks, and on how not to criticize a paper.


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