What we can do and what we cannot do with fMRI
Nikos K. Logothetis1
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Abstract
Functional magnetic resonance imaging (fMRI) is currently the mainstay of neuroimaging in cognitive neuroscience. Advances in scanner technology, image acquisition protocols, experimental design, and analysis methods promise to push forward fMRI from mere cartography to the true study of brain organization. However, fundamental questions concerning the interpretation of fMRI data abound, as the conclusions drawn often ignore the actual limitations of the methodology. Here I give an overview of the current state of fMRI, and draw on neuroimaging and physiological data to present the current understanding of the haemodynamic signals and the constraints they impose on neuroimaging data interpretation.
Magnetic resonance imaging (MRI) is the most important imaging advance since the introduction of X-rays by Conrad Röntgen in 1895. Since its introduction in the clinic in the 1980s, it has assumed a role of unparalleled importance in diagnostic medicine and more recently in basic research. In medicine, MRI is primarily used to produce structural images of organs, including the central nervous system, but it can also provide information on the physico-chemical state of tissues, their vascularization, and perfusion. Although all of these capacities have long been widely appreciated, it was the emergence of functional MRI (fMRI)-a technique for measuring haemodynamic changes after enhanced neural activity-in the early 1990s that had a real impact on basic cognitive neuroscience research. A recent database (ISI/Web of Science) query using the keywords 'fMRI' or 'functional MRI' or 'functional magnetic resonance imaging' returned over 19,000 peer-reviewed articles. Given that the first fMRI study without exogenous contrast agents was published in 1991, this corresponds to approximately 1,100 papers per year, or over 3 papers per day. This average obscures the actual rate of publications, as in 1992 there were four publications in total, increasing to about eight per day by 2007. About 43% of papers explore functional localization and/or cognitive anatomy associated with some cognitive task or stimulus-constructing statistical parametric maps from changes in haemodynamic responses from every point in the brain. Another 22% are region of interest studies examining the physiological properties of different brain structures, analogous to single-unit recordings; 8% are on neuropsychology; 5% on the properties of the fMRI signal; and the rest is on a variety of other topics including plasticity, drug action, experimental designs and analysis methods.
In humans, fMRI is used routinely not just to study sensory processing or control of action, but also to draw provocative conclusions about the neural mechanisms of cognitive capacities, ranging from recognition and memory to pondering ethical dilemmas. 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.
Perhaps the extreme positions on both sides result from a poor understanding of the actual capacities and limitations of this technology, as well as, frequently, a confusion between fMRI shortcomings and potential flaws in modelling the organizational principles of the faculties under investigation. For example, a frequently made assumption is that the mind can be subdivided into modules or parts whose activity can then be studied with fMRI. If this assumption is false, then even if the brain's architecture is modular, we would never be able to map mind modules onto brain structures, because a unified mind has no components to speak of. Even if true, the challenge remains in coming up with the correct recursive decompositions-in each of which any given cognitive capacity, however abstract, is divided into increasingly smaller functional units that are localized to specific brain parts, which in turn can be detected and studied with fMRI. This is not a neuroimaging problem but a cognitive one. Hierarchical decompositions are clearly possible within different sensory modalities and motor systems. Their mapping, which reflects the brain's functional organization, is evidently possible and certainly meaningful beyond any reasonable doubt1.
