Everybody's a Neurocritic!

It was fashionable and socially acceptable last week to criticize fMRI after Nikos Logothetis, one of the leading experts on the origin of the BOLD (Blood-Oxygen-Level Dependent) signal, published a high-profile article in Nature on What we can do and what we cannot do with fMRI:

Functional MRI is an excellent tool for formulating intelligent, data-based hypotheses, but only in certain special cases can it be really useful for unambiguously selecting one of them, or for explaining the detailed neural mechanisms underlying the studied cognitive capacities. In the vast majority of cases, it is the combination of fMRI with other techniques and the parallel use of animal models that will be the most effective strategy for understanding brain function.

He defends modularity¹ (although not exactly of the Fodorian variety), critiques the assumption of pure insertion², and points out the shortcomings of adaptation³ designs.

The 14 page Supplementary Information is comprehensive as well, covering topics such as MRI and fMRI Principles, Single and Multiple Unit Activity vs. Local Field Potentials, and Spatial Specificity, all documented by 112 references.

Finally, Logothetis has some sharp words not only for the fMRI pollyannas among us, but also for the naysayers (lest we get too dismissive):

Its popular fascination is reflected in countless articles in the press speculating on potential applications, and seeming to indicate that with fMRI we can read minds better than direct tests of behaviour itself. Unsurprisingly, criticism has been just as vigorous, both among scientists and the public. In fact, fMRI is not and will never be a mind reader, as some of the proponents of decoding-based methods suggest, nor is it a worthless and non-informative 'neophrenology' that is condemned to fail, as has been occasionally argued.

But what I really want to discuss here is a News Focus item in the 13 June 2008 issue of Science.

NEUROIMAGING: Growing Pains for fMRI

Greg Miller

As the use of functional magnetic resonance imaging has exploded, some researchers say the field could use a dose of rigor. Will new experimental approaches come to the rescue?

Science has never published an unrigorous fMRI paper? Let's look at the 23 May 2008 edition of "This Week in Science - Editor summaries of this week's papers."

Kindness or Fairness?

It's easy to propose that allocations of scarce resources should provide the greatest benefit to a group as a whole and be as fair as possible to individual members of the group, but what should be done when both aims cannot be optimized simultaneously? Hsu et al. (p. 1092... see the 9 May news story by Miller) use functional brain imaging, not to resolve these dilemmas, but to probe the underlying cognitive and emotional processes supporting one view (favoring equity, for instance) versus the other (maximizing the good). Brain regions involved in encoding reward relate also to calculations of total benefit, whereas the balancing of equity and utility seems to be the province of the insula, which connects with emotion-processing neural systems. Thus, judgments of fairness derive from emotion-based preferences, rather than those of pure reason.

Reverse inference anyone? See papers by Aguirre (2003) and Poldrack (2006). What did The Neurocritic say about the right and the good and the insula?

[The insula]'s a pretty large area. Besides being crowned the "seat of emotional reactions" (whatever that means), portions of the insula have been associated with interoceptive awareness, visceral sensation, pain, autonomic control, and taste, among other things... a lot of other things. Do a search of the BrainMap database using just two of the many insular foci reported by the Caltech researchers and you'll see activations related to action execution, speech, attention, language, explicit memory, working memory, and audition.

The 9 May news story by Miller mentions the 2001 Science paper on moral judgment and emotion (Greene et al., 2001).⁴ In that paper, the authors

reported that the medial frontal gyrus and other brain regions linked to emotion become more active when people contemplate "personal" moral dilemmas--such as shoving the man onto the trolley tracks or removing a man's organs against his will to save five transplant recipients--compared with when they weigh impersonal moral dilemmas--such as flipping a switch to save the workers or declaring bogus business expenses on a tax return.

Besides the medial frontal gyrus [BA 9/10, which did not replicate in Experiement 2], what were these other brain regions linked to emotion? Did they include the insula? No, they did not. They included the posterior cingulate gyrus (which has some grounding in reality) and the L and R angular gyri (which does not⁵).

Ironically, the 13 June story by Miller interviewed Russell Poldrack on the infamous New York Times Op-Ed piece (and the moral judgment paper):

Neuroimagers gone wild

What irked Poldrack and others most about the Times's op-ed was the way the authors inferred particular mental states from the activation of particular brain regions: Activity in the anterior cingulate cortex indicated mixed feelings about Hillary Clinton, for example, whereas amygdala activation indicated "voter anxiety" about Republican candidate Mitt Romney.

. . .

He and others argue that reverse inferences are particularly common in newer fields such as social cognitive neuroscience and neuroeconomics (not to mention neuropolitics), fields in which researchers are still trying to identify the cognitive processes underlying the behaviors they study. As an example, Poldrack points to a widely cited paper that used fMRI to investigate brain activity in subjects pondering moral dilemmas (Science, 14 September 2001, p. 2105); some of the brain regions that lit up had been linked in previous studies to emotional and "rational" cognitive processes, and the authors concluded that these two types of processes are active, to different degrees, in different types of moral judgments. But the strength of such arguments hinges on how specifically a given brain area is linked to a given mental process. Poldrack points out, for example, that some of the "emotional" brain regions in the morality study have also been connected to memory and language--a caveat that is rarely mentioned in media coverage of the work (Science, 9 May, p. 734).

So it appears that Science isn't exactly following its own advice... Granted, 14 September 2001 was a while ago, but 23 May 2008 was not.

Footnotes

¹ Logothetis views

the modular organization of many brain systems as a well established fact, and discuss only how far fMRI can go in revealing the neuronal mechanisms of behaviour by mapping different system modules and their dynamic inter-relationships. In this context the term module captures the classical local neuronal circuits repeated iteratively within a structure (for example, the columns or swirling, slab-like tangential arrangements of the neocortex), as well as the entities within which modules might be grouped by sets of dominating external connections.

² Pure insertion

asserts that a single cognitive process can be inserted into a task without affecting the remainder, an assumption that all too often is not tenable... Even if an experimental design could satisfy this assumption at the cognitive level, the assumption would be condemned to fail at the level of its neuronal instantiation owing to the highly nonlinear nature of most brain processes. To overcome this kind of problem and ensure better interpretation of the neuroimaging data it is necessary to perform a detailed task analysis to determine subtraction components and their interactions. Yet most neuroimaging studies provide no formal task analysis that would ensure that the particular cognitive process of interest is indeed being isolated by the subtraction.

³ In adaptation designs,

a stimulus is presented repeatedly with the expectation that it will eventually induce response adaptation in neurons selective for its various properties. In general, repetition of an identical stimulus does indeed produce a reduction in the fMRI signal. After adaptation, the subject is presented with a stimulus that is varied along one dimension (for example, the direction of a moving pattern or the view of a human face) and the possibility of a response rebound is examined. If the underlying neural representation is insensitive to the changes in the stimulus then the fMRI signal will be reduced, similar to the reduction produced by the repetition of identical stimuli. Alternatively, if the neurons are sensitive to the transformation, the signal will show a clear rebound to its original, pre-adaptation level.

⁴ Everyone always uses the "Trolley Problem" to illustrate a personal moral dilemma, but my favorite is actually "Smother for Dollars":

You are in hospital lounge waiting to visit a sick friend. A young man sitting next to you explains that his father is very ill. The doctors believe that he has a week to live at most. He explains further that his father has a substantial life insurance policy that expires at midnight.

If his father dies before midnight, this young man will receive a very large sum of money. He says that the money would mean a great deal to him and that no good will come from his father's living a few more days. He offers you half a million dollars to go up to his father's room and smother his father with a pillow.

Is it appropriate for you to kill this man's father in order to get money for yourself and this young man?

⁵ If you read the 17 abstracts carefully, you'll note that activation of the angular gyrus was mostly associated with things like cognition and mathematical processing, not emotion. Compare that search to the 170 papers in PubMed related to posterior cingulate and emotion.


References

Aguirre GK (2003). Functional Imaging in Behavioral Neurology and Cognitive Neuropsychology. In: T.E. Feinberg & M.J. Farah (Eds.), Behavioral Neurology and Cognitive Neuropsychology. New York: McGraw Hill.

Greene JD, Sommerville RB, Nystrom LE, Darley JM, Cohen JD. (2001). An fMRI investigation of emotional engagement in moral judgment. Science 293:2105-8.

Logothetis NK. (2008). What we can do and what we cannot do with fMRI. Nature 453:869-78.

Miller G. (2008). Neurobiology. The roots of morality. Science 320:734-7. (9 May 2008).

Miller G. (2008). Neuroimaging. Growing pains for fMRI. Science 320:1412-4 (13 June 2008).

Poldrack RA (2006). Can cognitive processes be inferred from neuroimaging data? Trends in Cognitive Sciences 10: 59-63.