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The light's on, but is anybody home?

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To put this into everyday terms, imagine your morning commute. You settle into your car, turn on the news and you're immediately immersed in the latest presidential scandal. In what seems only seconds later, you find yourself at work. You have no specific awareness of having made the 10-mile drive. Nevertheless, if you had been wearing a portable fMRI helmet, your scan would have shown various areas of brain lighting up as your brain successively processed a wide variety of inputs that you may or may not remember having heard or seen. You may consider making turns or applying the brakes as intentional actions, but in fact your unconscious mind was making intentional and deliberate choices while the conscious "you" was on autopilot.

When judging a patient's degree of personal awareness and ability to make willful decisions, it's important to distinguish between choices that can only be made consciously (such as consistently choosing to blink once for yes or twice for no) and choices that might be more reflexive and occur outside of consciousness. In short, we need to know if a choice is truly deliberate or merely the unconscious activation of neural circuitry.

So is it possible that this young woman's fMRI scans are not reflective of conscious intention and choice? Maybe her injury destroyed her ability to make unconscious thoughts conscious, but left her auditory pathways and subconscious processing mechanisms sufficiently intact to "hear" and respond to the researchers' questions.

Although it's too early to draw definitive conclusions, several recent fMRI studies point in this direction. In the March 2007 Journal of Neurology, Chinese researchers have studied the ability of unconscious patients to recognize their own names. Of seven persistent vegetative patients presented with a familiar voice saying their name (the same technique used when asking unconscious young women to relax), three showed activation of the primary auditory cortex and two also activated higher order association areas in the temporal lobe. So, are we to conclude that such patients are secretly conscious, or are they merely unconsciously registering recognition of their own names? And how would we know?

Imagine being at a cocktail party. You are intently talking to one person; all other conversations are mercifully tuned out. Suddenly you are aware that someone across the room has mentioned your name. Neural circuitry previously trained to recognize your name did what it was trained to do; the conscious "you" neither willed this activation nor asked to be notified when your name came up. Seen in this light, the Chinese researchers elegantly demonstrate how extensive areas of brain specific for language processing can be activated in unconscious patients. The study does not tell us whether these patients were actually aware of hearing their names, nor does it tell us that this processing was consciously willed.

These studies may be the earliest fMRI demonstrations of how much cognition actually occurs at a purely unconscious level. Indeed, Nicholas Schiff of Cornell Medical School, who specializes in disorders of impaired consciousness, has repeatedly cautioned that preservation of isolated neural networks (like name recognition) shouldn't be construed as representing conscious awareness; rather, such activity might be seen as evidence for parts of the brain operating outside of awareness.

Back to the young woman imagining playing tennis. Since the appearance of the preliminary version of the study in Science in 2006, there has been a flurry of criticisms, ranging from how to construct a study that can separate out conscious choice from more automatic unconscious processing, to the larger question of whether the fMRI is capable of confirming the presence of consciousness. The authors haven't budged.

On his Web site, the lead author, Cambridge neuroscientist Adrian Owen, has expanded his conclusion by suggesting that the performance of these mental tasks might be a way that non-communicative patients "may be able to use their residual cognitive capabilities to communicate their thoughts to those around them by modulating their own neural activity." Imagine being the young woman's parent and reading that just maybe your unconscious daughter could communicate with you, if only science could perfect the proper techniques.

The dream of technology clarifying personal experience carries a huge moral burden. I've lived through the era when the electro-encephalogram (EEG) was correlated with everything from borderline personality to impulsive, even homicidal behavior. In criminal trials, EEGs were commonly flaunted as evidence for diminished capacity. Patients without clinical seizures were treated with major league anticonvulsants simply because they had minor brain-wave irregularities. With time and experience, enthusiasm for the specificity of EEGs subsided; the neurological community learned that a wide variety of "irregular" findings might be nothing more than the far ends of the distribution of normal findings.

Now the new fair-haired kid on the neurological block is the fMRI. The underlying principle of fMRIs is fairly straightforward. Areas of brain that are active need more oxygen; this increased oxygen use is reflected as hot spots on the scan. But fMRI accuracy, reliability and interpretations remain debatable, especially when it comes to studying complex mental activities with relatively primitive and indirect measurements of blood flow. At best, the fMRI is the physiological equivalent of an aerial photograph of a house. It can tell you which rooms are lighted, even the amount of electricity being used in any room, but it cannot tell you what is going on in a lighted room, or even if anyone is home and is aware of the light.

Despite numerous discussions of technical limitations -- the April 2005 Scientific American article "Fact or Phrenology" is an excellent overview -- the fMRI has captured the popular imagination big time. In 2006, there were 1,500 fMRI articles in professional journals. Some studies have been meticulous and provide superb insights into brain function. Others have been trivial, if not downright silly, such as why consumers might prefer Coke to Pepsi, or how fMRI can conclusively determine if you are lying. There are those that border on science fiction, such as German neuroscientist John-Dylan Haynes' suggestion that one day the computer should be able to read minds. "Every thought is associated with a characteristic pattern of activation in the brain. By training a computer to recognize these patterns, it becomes possible to read a person's thoughts from patterns of their cerebral activity."

My primary concern isn't with the variable quality of fMRI studies; we are all aware that science proceeds via fits and starts, the good and the bad sorted out over time. For me, the problem is one of ethical responsibility to patients and their families. And there is the issue of social responsibility. Science doesn't exist in a vacuum; I would hate to see such preliminary and controversial studies cited as evidence for otherwise untenable or extreme social policies.

Perhaps Owen and his colleagues are correct and this unfortunate woman has fleeting moments of consciousness and is trying to communicate her thoughts. But perhaps the study shows nothing more than preserved bits of neural machinery capable of making unconscious choices. There cannot be a definitive conclusion until we understand every aspect of brain function and have demonstrated precisely what neural states correspond to specific conscious experiences. Until this mythical time arrives, pronouncements of fMRI confirmation of consciousness aren't science; they are bald speculations and should be so labeled.

Scientists dealing with human lives have the obligation to heed the Hippocratic Oath: primum non nocerum. Above all, do no harm. The study by Owen and co. provides provocative insights into the degree of residual cognitive processes that can be preserved in a clinically unconscious patient. That is enough. Whether this unfortunate young woman has elements of consciousness lurking beneath her unresponsive behavior is not a question that can be answered through technology.

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About the writer

Robert Burton, M.D., is the former chief of neurology at Mount Zion-UCSF Hospital and the author of "On Being Certain: Believing You Are Right Even When You're Not" (St. Martin's Press, February 2008).

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