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The consciousness continuum
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The tragic case of Terri Schiavo focused international attention on questions of conscious awareness and the brain. If the thinking parts of a brain are destroyed, is this “brain death?” Can a brain be alive yet unconscious? How can we tell whether someone who cannot communicate with us is aware? Can functional brain imaging be used to detect cognition or awareness in severely brain-damaged patients?
Currrent accepted definitions of brain death require either the permanent loss of whole brain function or specifically the loss of brain stem function, the part of the brain which governs breathing and other vital functions. It does not apply to patients whose ability to think or feel is permanently lost as a result of damage to “higher,” presumably cortical, brain areas. However, such patients are sometimes referred to as “cortically brain dead,” which can be confusing.
Severely brain-damaged patients who are comatose rather than brain dead typically pass through or evolve into one of the following states as they emerge from coma. Determining the mental status of patients who are behaviorally nonresponsive or minimally responsive is a challenging but important goal for clinical neurology. Apart from its possible prognostic significance, it is also essential for determining our ethical obligations to them. A thinking, feeling human being requires more than custodial care.
The following taxonomy of states of consciousness after severe brain damage, excerpted from Bradley et al.’s (2003) Neurology in Clinical Practice, provides a useful starting point for discussion:
“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.”
“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]… Other causes include central pontine myelinolysis and brainstem mass lesions…
Until recently, patients’ behaviors were the primary source of evidence used to infer their mental states. Unfortunately, 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. Now functional neuroimaging is being brought into the mix, and showing a surprising level of residual cognitive functioning in patients whose behavior is consistent with PVS or MCS. However, both sources of evidence are trickier to interpret than they appear at first.
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. This has clear implications for the interpretation of patient behavior.
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! It is important to bear in mind this tendency to project mental states and intentions, and the possibility that we may do so even when the object of our projections in reality has neither.
Brain imaging offers seemingly more direct access to the workings of cognitive areas of the brain than behavior. However, at this point in the development of functional brain imaging, the meaning of different patterns of brain activity is not well understood. In particular, even in normal brains, activation of specific representations is not necessarily accompanied by awareness of the represented information.
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.
At the height of publicity over the Terri Schiavo case, Schiff, Hirsh and colleagues reported finding fMRI responses to speech in patients who were in MCS. This result was reported on the front page of the New York Times. Perhaps the most stunning result obtained by functional neuroimaging with a severely brain damaged patient was reported by Owen, Laureys and colleagues in 2006. They instructed a woman in a vegetative state to carry out various activities in her imagination, including playing tennis and walking around her home. During the half-minute intervals of imagined tennis, she activated the same movement-related area (supplementary motor area) that normal subjects do in this task, and during the home walk she activated the same place-related area (parahippocampal place area) as normal subjects. This is consistent with, in the words of the authors “her decision to cooperate… by imagining particular tasks when asked to do so represents a clear act of intention” and suggesting to the authors that “she was consciously aware of herself and her environment.”
As we learn more about the neural correlates of conscious awareness, it will undoubtedly have implications for our treatment of patients in PVS and MCS, as well as others on the “consciousness continuum” including patients with dementia, infants and nonhuman animals.
Martha J. Farah
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