icu_imageThe tragic case of Terri Schiavo has focused national attention on questions of conscious awareness and the brain. How can we tell whether a brain-damaged individual is aware? What is the difference between brain death and persistent vegetative state, given that the capacity for conscious awareness is permanently lost in both? Can functional brain imaging be used to detect consciousness in patients whose neurological impairments prevent them from communicating with us?

Knowledge of the relations among conscious awareness, brain and behavior is crucial for deciding whether patients like Terri Schiavo have a mental life. If the family had agreed on whether she was aware of the people and events in her surroundings, they would probably have agreed on the many other issues that divided them and divided the nation as a whole.

Until recently, a patient’s behavior was the one source of evidence we could use to infer their mental state. Now functional neuroimaging has been brought into the mix. Both sources of evidence are trickier to interpret than they appear at first.

Some observers of Terri Schiavo found her behavior indicative of conscious awareness and intentionality. One observer, writing on the website wrote: “I was pleasantly surprised to observe Terri’s purposeful and varied behaviors… I never imagined Terri would be so active, curious, and purposeful. She watched people intently, obviously was attempting to communicate with each one in various ways and with various facial expressions and sounds. ” For me, watching Terri Schiavo in the website videos, it was difficult not feel I was seeing a person interacting with others and aware of her surroundings.

However, clinical and experimental neuroscience have taught us some surprising things about the range of behaviors that can emerge from a decorticate brain. Such behaviors include orienting with eye and head movements toward sights and sounds, generating facial expressions, and producing nonverbal vocalizations that have meaning for us, if not the person producing them, such as cries and laughter. In light of this, we must interpret the behavior seen in the videos cautiously and with a measure of skepticism.

The most natural interpretation for the behaviors we see on the video is not the only interpretation. For example, when a dozing Terri is loudly ordered to “open your eyes!”and does so, does that mean she understood what was said? Or would she have done the same thing if roused with an equally loud order to “open your mouth!” or “stand on your head!”

Humans are hardwired to interpret the behavior of others in terms of mental states. In the psychology literature this tendency is part of a suite of abilities termed “Theory of Mind” (ToM) and in most situations we apply our ToM automatically, without weighing alternative reasons for the behavior. For a particularly striking demonstration of this fact about ourselves, consider the typical response to the robot Kismet. Kismet is part of a research effort at the MIT Artificial Intelligence Lab to design machines that interact socially with humans. Kismet has been programmed to gaze at humans who approach it, orient to salient objects moving within its field of view, pull back avoidantly if an object is thrust forward at it, and so on. People attribute all manner of cognitive and emotional states to this robot on the basis of a fairly small set of simple behaviors, and have been known to become quite attached to it. And this is a contraption made of metal and plastic, not a human being! My point is emphatically not to liken Terri Schiavo to Kismet, but rather to suggest a similarity in our reactions to the woman and the robot.

Given that Terri Schiavo cannot demonstrate understanding or awareness by speaking or gesturing in any way, what can we conclude about her mental life? Is she a person trapped in a body that can no longer speak or act purposefully? Or does her absence of communicative behavior indicate an absence of consciousness? The neurological taxonomy of states of consciousness, which includes her diagnosis of Persistent Vegetative State (PVS) provides a helpful starting point for discussion. The following is excerpted from Bradley et al.’s Neurology in Clinical Practice (Butterworth-Heinemann, 2003):

“Several different behavioral states may appear similar to coma

[a state of total unarousability] or may be confused with it…

“In the locked-in syndrome…; patients are alert and aware of their environment but…voluntarily able only to move their eyes vertically, or blink, or both. The locked-in syndrome is most often observed as a consequence of pontine infarction [i.e. stroke in the pons, a structure through which motor impulses must pass]…

“In the persistent vegetative state, patients have lost cognitive neurological function but retain vegetative or noncognitive neurological function such as cardiac action, respiration, and maintenance of blood pressure… This state follows coma and is characterized by the absence of cognitive function or awareness if the environment, despite a preserved sleep-wake cycle. Spontaneous movements may occur and the eyes may open in response to external stimuli, but the patient does not speak or obey commands… The diagnosis of PVS should be made cautiously and only after extended periods of observation.

“The term minimally conscious state [MCS] is distinguished from coma and persistent vegetative state by the preservation of discernible behavioral evidence of consciousness… The diagnosis is established by the presence of one or more of the following behaviors: (1) ability to follow simple commands, (2) gestural or verbal yes/no responses, (3) intelligible verbalization, or (4) purposeful behaviors that are contingent upon and relevant to the external environment.”

The preponderance of medical opinion is that Terri Schiavo was in a PVS. However the line between PVS and MCS is fuzzy, and for what it is worth, rare anecdotal evidence hinted at occasional awareness.

Recent functional brain imaging results have added a new twist to the treatment of PVS. Brain imaging is potentially helpful in understanding the mental life of neurological patients. Behavior is an imperfect measure of cognitive state in anyone, but especially in neurological patients whose verbal and motor systems may be damaged or disconnected from cognitive systems. Brain imaging offers seemingly more direct access to the workings of cognitive areas of the brain. However, at this point in the development of functional brain imaging, the meaning of different patterns of brain activity is not well understood.

A much publicized article in the journal Neurology used fMRI to document cortical responses to speech in patients who were in a minimally conscious state (MCS). This result, reported on the front page of the New York Times, was seized upon by some as evidence that Terri Schiavo may have retained more awareness than her behavior suggested. There are two problems with this conclusion.

The first problem is that the patients in this study were in a MCS, not a PVS. What is known about brain activity in PVS? A few studies have shown that the primary sensory cortices of PVS patients respond to touch and sound but higher-level cortices associated with cognition are not reliably activated. However, one PVS patient imaged with PET showed more cortical activation in response to a story told by his mother than to nonsense words.

The second problem is that brain activation, even activation that discriminates between meaningful stimulation and nonsense, does not imply awareness. The cognitive neuroscience literature contains a number of studies in which people’s awareness of stimuli was manipulated while brain activity was measured. In studies with healthy normal participants, awareness of visual stimuli was eliminated by the use of brief, subliminal presentations. In studies with neurological patients, a phenomenon called “extinction” was used to control awareness of the stimuli; visual stimuli on one side of space are extinguished (not consciously perceived) when another stimulus is presented simultaneously on the other side of space. These studies have shown that stimuli can activate relevant regions of cortex even when people are unaware of the stimulus. This is consistent with the idea that the brain activity underlying perception is graded, ranging from nonexistent to the levels of activity observed in normal conscious perception, and that conscious awareness of external events accompanies only the higher end of that range.

The bottom line is that we have two windows through which to look for an answer to the question of conscious awareness in brain-damaged patients, and while neither is crystal clear, both are useful. The first is extended behavioral observation (as opposed to snippets of video), undertaken with an awareness of our susceptibility to the “Kismet” phenomenon. The other is functional neuroimaging, interpreted cautiously and with an awareness of how much remains to be learned about activation-cognition correlations in damaged brains.

Martha J. Farah

Alkire, M. T., A. G. Hudetz, and G. Tononi. 2008. Consciousness and anesthesia. Science 322: 876–880.

Andrews, K. 1996. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. British Medical Journal 313 (7048): 13-16.

*Dehaene, S., Naccache, L., Le ClecéH. G., Koechlin, E., Mueller, M., Dehaene-Lambertz, G., van de Moortele, P.F., Le Bihan, D. 1998. Imaging unconsious semantic priming. Nature 395 (6702): 597-600.

Eisenberg, J. fMRI and its Impact on Surrogate End of Life Decision Making. Neuroethics, 2008.

Elliott, C. (2001). Attitudes, souls and persons: children with severe neurological impairment. In C. Elliott (Ed.),Slow cures and bad philosophers: essays in Wittgenstein, medicine and bioethics (pp. 89–102). Durham (NC): Duke University Press.

Farah, M. 2009. Neuroethics and the problem of other minds: implications of neuroscience for the moral status of brain-damaged patients and nonhuman animals. Neuroethics 1: 9–18

Farah, M and Heberlein, A. , ‘Response to Open Peer Commentaries on “Personhood and Neuroscience: Naturalizing or Nihilating?”: Getting Personal’, The American Journal of Bioethics, 7:1.

* Fins, J.J. 2005. Rethinking disorders of consciousness: new research and its implications Hastings Center Report 35 (2), 22-24.

Fins JJ, Illes J, Bernat JL, Hirsch J, Laureys S, Murphy E. Neuroimaging and disorders of consciousness: envisioning an ethical research agenda. Am J Bioeth 2008; 8: 37–46.

* Giacino, J.T. 2003. Disorders of consciousness in coma, stupor, and minimally responsive states. Behavioral Neurology and Neuropsychology (2nd Ed.): 337-345.

* de Jong, B.M., Willemsen, A.T., Paans, A.M. 1997. Regional cerebral blood flow changes related to affective speech presentation in persistent vegetative state. Clinical Neurology and Neurosurgery 99 (3): 213-216.

Laureys, S. (2005). Death, unconsciousness and the brain. Nature Reviews Neuroscience, 6, 899-909.

Laureys, S. (2005) The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 9, 556–559

Laureys S., Owen, A,M., Schiff, N.D. 2004. Brain function in coma, vegetative state, and related disorders. Lancet Neurology 3 (9): 537-546.

Munakata Y. 2001. Graded representationsin behavioral dissociations. Trends in Cognitive Sciences, 5 (7): 309-315.

NINDS Coma and Persistent Vegetative State Information Page

Owen, A.M., Coleman, M.R., Boly, M., Davis, M.H., Laureys, S., Pickard, J.D., 2006. Detecting awareness in the vegetative state. Science 313, 1402.

*The multi-society task force on PVS. 1994. Medical Aspects of the Persistent Vegetative State (1). New England Journal of Medicine,330: 1499-1508.

Rees, G., Kreiman, G., Koch, C. 2002. Neural correlates of consciousness in humans. Nature Reviews Neuroscience 3 (4): 261-270.

*Schiff, N.D., Rodriguez-Moreno, D., Kamal, A., Kim, K.H., Giacino, J.T., Plum, F., Hirsch, J. 2005. fMRI reveals large-scale network activation in minimally conscious patients. Neurology 64 (3): 514-523.