And I think this one says it all --
http://physiologyonline.physiology.org/cgi/content/full/17/1/38
nuff said
Dana
News in Physiological Sciences, Vol. 17, No. 1, 38-42, February 2002
(c) 2002 Int. Union Physiol. Sci./Am. Physiol. Soc.
Is there a Mind? Electrophysiology of Unconscious Patients
Boris Kotchoubey1, Simone Lang1, Vladimir Bostanov1 and Niels Birbaumer2
1 Institute of Medical Psychology and Behavioral Neurobiology,
University of Tübingen, 72074 Tübingen, Germany, and
2 Department of General Psychology, University of Padua, Padua, Italy
Abstract
Event related brain potentials (ERPs) provide information about
cortical processing in severe neurological patients whose cognitive
abilities cannot be expressed in their behavior. In coma, ERPs
contribute to the prediction of the outcome. In a vegetative state,
ERPs uncover the functional state of cortical processes. The
significance of ERPs in the neurophysiological study of consciousness
is discussed.
Introduction
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
The question of whether patients who appear to be unconscious are
really without conscious experience has remained an enigma until
recently. Numerous anecdotes exist about seemingly unconscious
patients who, in fact, were able to perceive their environment (4).
One may reformulate this question in physiological terms by asking to
what extent cortical functions are preserved in neurological patients
with severe global brain injury or in other unresponsive persons. A
technique allowing us to test those covert cortical functions are
event-related brain potentials (ERPs).
ERP methodology
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
Electroencephalogram (EEG) waves time-locked to particular events,
like sensory stimulus or a patient's motor response, are referred to
as evoked potentials. They can be roughly subdivided into two classes.
Those of the first class, early, short-latency components (several
milliseconds to several tens of milliseconds after stimulus), reflect
propagation of sensory signals from receptors via ascending pathways
to the cortex. Some of them are widely used in clinical
neurophysiology (see Ref. 10). However, these short-latency waves
merely indicate whether sensory pathways are intact. They do not
convey information about cognitive processes, and thus they are
irrelevant to the issue of consciousness.
The other group of evoked potentials is referred to as ERPs. In
contrast to the short-latency waves described above, ERPs are of
cortical origin. Of special importance are ERP waves that appear
between 100 and 1000 ms after stimulus. ERPs constitute a unique,
noninvasive technique to obtain information about how the cortex
processes signals and prepares actions. In general, what is observed
when a patient performs a neuropsychological test is always a result
of many physiological processes. ERP waves are supposed to "manifest"
single components of this processing chain. The ERP method permits us
to follow stimulus processing in real time at all levels of
complexity.
ERPs can be used to study the processing of physical stimulus features
as well as the processing of semantic stimulus features (language,
meaning). Regarding the former, the most frequently used experiment is
the oddball paradigm (5) in which rare (e.g., 20%) stimuli ("targets")
are randomly inserted in a sequence of frequent (e.g., 80%) stimuli
and the subjects' task is usually to count the rare events (Figs. 1A
and 2). Similar, albeit smaller, effects are observed without the
counting instruction: the so-called passive oddball (15).
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FIGURE 1. Different types of event-related potentials (ERPs) in
normal subjects. A–C: nonverbal stimulation. A: visual oddball with 2
simple stimuli [blue, frequent (FS); red, rare RS)]. N1, P2, and N2,
common to both stimuli, were followed by large P300 to RS. B: mismatch
negativity (MMN) to nontarget (ignored) RS (red). Blue, FS. C: FS in
the relevant (red) vs. irrelevant (blue) channel reveals an additional
"processing negativity" (PN) to relevant stimuli. D–F: verbal
stimulation. D: semantic oddball. Subjects count words belonging to 1
semantic class (e.g., animals; red) and ignore words belonging to
others (blue). Counted category elicits a P3-like parietal wave with a
latency of 600 ms. E: ERPs to 2nd word in semantically related (e.g.,
chair-table; blue) or unrelated (e.g., man-day; red) word pairs.
Typical response was broad negativity to unrelated words. F: N400 wave
to words violating semantic context of sentence (red) vs. words
congruent with context (blue). Site of recording is shown as red point
on scalp. Although voltage scale is the same in all diagrams, note
different time scales. Vertical bars indicate stimulus onset.
Negativity is plotted upward in all panels.
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FIGURE 2. A–E: varieties of ERPs in an oddball paradigm (with 2
musical tones) in severely brain-damaged patients. A: lack of cortical
response in patient with hypoxic brain injury. B: distinct ERP
consisting of the P1, N1, and P2 components (but without any
differentiation between standards and targets) in a patient with head
trauma. C: cortical negativity in response to rare targets (here in
patient with multiple subcortical strokes) is regarded as superficial
differentiation between 2 stimuli. D: positive wave with frontal
maximum and peak latency of 250–300 ms (P3a) may be conceived of as a
manifestation of orienting response to rare tones (another patient
with severe head injury). E: normal response pattern, here recorded in
patient with "locked-in syndrome" caused by a pontine stroke. F:
well-preserved P600 response to semantic oddball task in a young
female patient who remained almost unresponsive for 1 year after a
massive hemorrhage in all ventricles that followed a seemingly
successful tumorectomy.
Sometimes, both frequent and rare stimuli are presented via two
sensory channels (e.g., the right and left ears). Only the rare
stimuli in one of the channels (the relevant channel) serve as
targets; stimuli in the other channel should be ignored. This paradigm
has allowed researchers to identify several robust ERP phenomena,
which are best studied by using a subtraction technique (17). Thus the
subtraction of the ERP to frequent stimuli in the irrelevant channel
from those to frequent stimuli in the relevant channel reveals a
negative wave, sometimes called "processing negativity," which starts
as early as 50–150 ms after stimulus presentation. In the auditory
modality, the subtraction "rare minus frequent" within the irrelevant
channel results in a "mismatch negativity" (MMN; Ref. 17). Finally,
the difference between rare targets and nontargets in the relevant
channel is dominated by a large parietal wave with a latency of
350–500 ms; this wave, referred to as P3b or P300, is often preceded
by a brief negativity (N2; Fig. 1).
The second type of cognitive analysis, the processing of semantic
input, is frequently assessed by means of sentences that either end in
a semantically correct fashion or have inappropriate endings (14). The
final words contradicting the semantic context elicit a large parietal
negative wave (N400). Alternatively, the semantic context can be
construed by using pairs of words that are either strongly associated
or unrelated to each other (2). Oddball techniques can also be used
for assessment of semantic comprehension. For example, subjects are
presented words of different semantic classes. Words belonging to one
of these classes should be counted, the other words ignored. Like in
oddball tasks with tones, the rare targets elicit a parietal P300 wave
but with a longer latency.
The negative waves recorded on the scalp are most probably a result of
summation of numerous excitatory postsynaptic potentials in the apical
dendrites of cortical units (layers I and II) and thus reflect
threshold lowering of pyramidal neurons and their preparation for
future activity. The positive waves are supposed to result from
depolarization processes in deeper cortical layers and thus to reflect
the actual work of underlying cortical areas, i.e., the consumption of
the resources prepared during the preceding negativity phase.
Some ERP-based inferences are related to the contemporary knowledge
about the functional meaning of particular waves. For instance, a
frontal P3a wave in oddball (Fig. 2D) is interpreted as reflecting
more shallow stimulus processing compared with a parietal P3b (Fig.
2E), since P3a is usually regarded as a rather automatic phenomenon.
Although much evidence has been accumulated to support this
interpretation, these notions of the parietal versus frontal varieties
of P3 may change with future research. But this hypothetical knowledge
can nevertheless lead to inferences that are impossible if only a
behavioral response is recorded.
In other instances, interpretation of clinical ERP research is
theory-free. Thus when a patient should count words belonging to a
particular class, a P3 response to these words proves the patient's
ability for semantic classification regardless of what the exact
functional meaning of this P300 might be. This is because a
classification process is conditio sine qua non a differential brain
response; if the patient were unable to classify, no P300 to a
particular word class could appear (Figs. 1D and 2F).
Evoked potentials and ERPs in coma
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
Coma is the most severe disorder of the functions of the central
nervous system, resulting usually from a dysfunction of midbrain
structures regulating wakefulness. Coma is always an acute state
indicating an ongoing pathological process caused, e.g., by trauma,
anoxia, inflammation, or hemorrhage.
Short-latency evoked potentials (<50 ms) are frequently used for the
prediction of the outcome from coma. Characteristically, they show a
very low rate of false negative predictions (i.e., most patients
missing these waves show a negative outcome, e.g., death). On the
other hand, the rate of false positive predictions is high (i.e.,
well-preserved brain waves are recorded in patients who have a bad
clinical prognosis). Clearly, because these early waves reflect rather
primitive processing operations, their being intact only indicates
that simple sensory processes are possible; in this sense, they can
overestimate the patient's state.
The situation changes when we pass to ERPs. To date, five large
studies on patients in coma have been carried out, and all of them
used ERPs recorded in a passive oddball paradigm with simple sine
tones (6–8, 10, 16). In sum, these studies yielded two main results.
First, the ability of the cortex to differentiate between frequent and
rare events could be detected in many coma patients (an estimate of
30–50%). Second, when ERP findings are compared with the outcome of
coma, the rate of false positive predictions is very low, sometimes
equal to zero, whereas the rate of false negative predictions (i.e.,
the outcome is better than predicted on the basis of ERP data) is
high, the only exception being a study of 20 anoxic coma patients in
which a false positive rate of 50% was found (16). Furthermore, ERP
components related to more complex cognitive processes (i.e., MMN or
P3) yield a higher false negative rate and a lower false positive rate
than components such as N1 and P2 reflecting the first cortical
reaction to a stimulus.
This indicates that ERP tests are biased to underestimate patients'
cognitive abilities. Different factors can contribute to this
underestimation. First, ERP components are also occasionally absent in
a few healthy subjects; hence, although the presence of a particular
ERP effect always suggests the presence of the corresponding function,
its absence does not prove the lack of this function. Second, many
neurological patients have considerable fluctuations of arousal, and a
neurophysiological test may be carried out at the moment of arousal
decrement; some time earlier or later the same patient would
demonstrate a better outcome. Third, a test run may last too long, and
its result may be negative not because the patient cannot distinguish
between the presented stimulus categories but because he or she cannot
concentrate for this time period. Fourth, the technique of ERP
averaging implies that the particular brain wave not only occurs but
is also time-locked throughout testing; a large latency jitter may
lead to the disappearance of the wave in the average although it was
present in most single trials. Fifth, statistical tests performed to
confirm the existence of the wave are generally biased to retain the
null hypothesis (H0, which reads that the patient does not distinguish
between the presented stimuli) until it is very improbable. This means
that the conventional statistics, with their reasonable conservatism,
are directed against the patient. At present, therefore, the ERP test
data should probably be treated as the lowest limit of the patient's
capabilities, even though these data show that many more patients are
capable of higher cortical information processing at different levels
than may appear to be the case on the basis of clinical-behavioral
observations.
"Waking coma" is not coma
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
Some patients surviving coma pass to another condition called the
vegetative state (VS). In contrast to coma, midbrain functions are
largely preserved in VS, which is manifested in a preserved
sleep-wakefulness cycle. Also, subcortical reflexes to simple stimuli
like flash or sound are preserved. However, all cortical functions
are, by definition, completely lacking (13), which gave rise to the
description of VS as "waking coma." Another important difference from
coma is that VS can exist both as an acute pathological state
(transition from coma to another syndrome) and as a residual condition
after a brain disease has already done its work, leaving a mass of
destroyed cortical neurons.
These differences determine different strategies in ERP studies. The
diagnosis of coma, with its almost complete nonreactivity, is usually
simple, and the critical issue, addressed by ERP studies, is that of
prognosis. In contrast, the diagnosis of VS sometimes requires very
subtle differentiation between subcortical and cortical, "simple" and
"complex" responses, resulting in a high diagnostic error rate (1, 3).
Particularly difficult may be the differentiation from "locked-in
syndrome," in which (usually after a stroke in the anterior part of
the pons cerebri or as a result of degeneration of motor neurons in
the motor cortex and/or spinal cord) a patient becomes completely or
almost completely paralyzed. Although cognitive functions can largely
remain intact in this condition, the patient cannot express these
functions due to the lack of motor control (18). The difficulty of
differentiation between the two states is further enlarged by the fact
that there are numerous transitional conditions between VS and
locked-in-syndrome. In this case, the prognosis, therapy, and
rehabilitation measures depend on the correctness of the diagnosis.
ERPs in VS
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
In contrast to coma, ERPs have only sporadically been used for
assessment of cognitive abilities in VS. One of these studies (20)
used several procedures addressing different levels of processing
complexity. No ERP response was obtained in 11 out of 43 patients with
"definite VS" but in only 1 of 23 patients qualified as "questionable
VS." In another recent study (9), the N1 and MMN ERP components were
recorded in response to changes in complex tonal patterns (e.g., the
change from oboe to clarinet) in 10 nonresponsive postcomatose
patients (probably in VS). Eight out of ten patients showed no clear
cortical wave. These data left some doubt as to whether consistent ERP
responses can be recorded in VS at all.
We examined 34 patients with severe brain damage. All of them had
normal early acoustic evoked potentials, suggesting that primary
auditory pathways were intact. Most patients had general EEG slowing,
with prevailing rhythms of 5–7 Hz, but none exhibited dominant delta
activity. Seventeen patients were diagnosed as typical VS (i.e.,
nonresponsive); the other 17 patients showed inconsistent responses to
commands and were qualified as "minimally responsive." VS was caused
by a traumatic brain injury (15 patients), acute brain anoxia (10
patients), stroke (8 patients), and encephalitis (1 patient).
A broad range of ERP tests was employed at the patients' bedside,
including different versions of oddball and semantic match/mismatch
paradigms. In addition to visual evaluation of the ERPs by two raters
(as in Ref. 9), a statistical comparison between the two conditions in
each test (e.g., target vs. standard in oddball tasks; related vs.
unrelated words in the word pair task) was performed on the basis of a
single-trial ERP analysis (12).
According to visual inspection of ERP waveforms, 25 out of 34 patients
had a P3 wave in at least 1 of the 3 oddball tasks (sine tones: 9,
complex tones: 21; vowels: 16). Furthermore, 15 waveforms indicated
semantic differentiation in at least 1 of 3 tests (semantic oddball,
word pairs, and sentences). When more conservative criteria were used,
the corresponding numbers were 15–20 patients with a clear P3 response
to physical stimuli (sine tones: 4–6 patients; complex tones: 9–11
patients; vowels: 5–7 patients) and 10 patients who were capable of
semantic processing.
For the above-stated reasons, these figures underestimate the real
state of affairs. This means that one- to two-thirds of patients with
suspected VS were capable of cortical differentiation of physical
stimulus features and that at least 20% of these patients
differentiated semantic stimuli (i.e., their brains comprehended
language). The P3 wave was better pronounced in patients with minimal
behavioral responses than in those whose behavioral responsiveness was
completely lacking. However, even in the latter group P3 was found in
nine patients. Furthermore, no difference between the minimally
responsive and nonresponsive groups was found in semantic tests: at
least three "nonresponsive" patients did differentiate words according
to their semantic content. This result may reflect the continuity of
borders between typical and atypical VS and the difficulty of clinical
differentiation between a "lack of responses" versus "weak and
inconsistent responses" (12).
Increasing the reliability of ERP assessment
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
Whenever a reliable difference is obtained between the cortical
responses, e.g., to words versus pseudowords or to related versus
unrelated words, such difference supports the assumption that the
brain does distinguish between the corresponding stimulus classes and,
hence, is able to perform some operations necessary for perceiving and
understanding speech.
This emphasizes the importance of inferential tests for individual ERP
waveforms. If a reliable response indicates that the corresponding
function is preserved, the issue of response reliability becomes
crucial. In ERP studies of coma and VS conducted to date, this issue
has not received sufficient attention. Most researchers simply relied
on visual inspection of the waveforms (16, 20). Some check the
consistency of the visually detected waves using a cross-correlation
between independent subaverages (6) or between two consecutive
recordings (8). Others compare ERP waves with similar waves observed
in healthy subjects (11). The different methods for assessment of
whether the relevant wave was present or absent in a given patient's
waveform can explain the variability of results reported in the
literature.
Clearly, we cannot restrict ourselves to visual judgment of ERP
waveforms any longer. But the standard quantitative approach to ERP
assessment is problematic too. In this approach, component amplitudes
and/or latencies are measured within time epochs of interest that are
previously selected on the basis of visual inspection of the waveform.
This preselection biases the resulting statistical estimation. An
alternative is a multivariate approach in which the entire ERP curve
enters the statistical analysis. Most ERP paradigms used in coma and
VS entail two conditions (e.g., standards vs. targets and appropriate
vs. inappropriate words). The EEG data points in these two conditions
can be compared by means of Hotelling's T2-test.
Figure 3 shows ERPs of two VS patients in the word pair paradigm. In
both cases, the waveforms for semantically congruent versus
incongruent words appear to differ at some locations but not at
others. It is difficult to find a particular "wave" clearly
distinguishing between the two conditions, which poses a huge problem
for a univariate test. In patient A, all attempts to test the visible
difference in the mean amplitude for several selected time windows and
electrode locations yielded nonsignificant results. In patient B, the
curves were found to differ over the frontal cortex within a
preselected interval of 480–930 ms. The multivariate T2-test performed
with wavelet-approximated data (to reduce the number of variables)
resulted in significant between-condition differences for both
patients. It should be emphasized that the analysis included an
interval of 300–812 ms, which was not selected on the basis of
previous visual inspection of the data.
View larger version (43K):
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FIGURE 3. ERPs of 2 patients in vegetative state under word pair
conditions. A pair of closely related or unrelated words is presented.
In both patients the waveforms for the related vs. unrelated words
seem to differ, but it is difficult to point at a particular component
whose presence or absence in the data should be statistically tested.
Multivariate statistics reveals significant differences in both cases.
Conclusions
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
Evidence from ERP research suggests that many patients diagnosed as in
coma or VS are able to perceive and process various aspects of their
environment, including, in some cases, semantic elements of human
speech. Although this technique still needs to be refined and is not
yet capable of exact assessment of each individual patient's
abilities, it is already clear that higher cortical functions are
preserved in many patients who cannot express their abilities in their
behavior. The identification of "consciousness" with "rational
expressive behavior" that originates in folk psychology does not hold
any longer, since people who cannot control their behavior can
nevertheless perform cognitive operations of different levels of
difficulty.
ERPs reflect widespread sequences of different cognitive operations.
Even though these operations may or may not be strongly related to
conscious experience, their presence always indicates that a brain
mechanism necessary for that operation which is required for the
attribution of significance ("understanding") is intact. An argument
that ERP differentiation between semantic stimuli does not prove the
conscious differentiation in meaning presumes a qualitative difference
between the neural substrates of conscious and unconscious processes.
This assumption does not find support in the empirical data. Rather,
conscious and unconscious processing of verbal material employs
largely overlapping brain structures, with conscious processing
probably involving more cell assemblies of the same type
simultaneously (19). The continuum between nonconscious and conscious
processing is fluid; no exact borders can be drawn. The vagueness of
these constantly moving borders does not allow conclusions, which may
imply a negative clinical bias.
Consciousness is a heterogeneous concept, both philosophically and
physiologically. Several physiological conditions in diverse brain
systems have to be fulfilled before conscious awareness is possible.
Some of these diverse physiological conditions are known, including
arousal of cortical neurons by cholinergic reticular fibers;
activation of the reticular thalamus, specific thalamic nuclei,
thalamocortical and prefrontothalamic connections; reentrant loops
between primary and secondary cortical areas; and coherent cortical
dynamic binding of cell assemblies by fast intracortical oscillations.
ERPs constitute only one of several possible windows into those
processes and areas involved in the production of conscious
experience. Thus reticular and thalamic activation would need careful
measurement of blood flow changes using positron emission tomography
(PET) and functional magnetic resonance imaging (fMRI). However, both
techniques are extremely difficult to realize for severely damaged
patients with artificial ventilation and other life support equipment,
leaving aside the ethical problems of invasive PET measurement in
patients unable to communicate. To observe perceptual grouping and
binding, localized high-frequency -band (30–100 Hz) EEG/MEG recording
would be advisable. These focused -responses show an extremely low
amplitude and require hundreds of repetitions, which, again, makes
their recording in severely damaged patients very problematic.
In addition to the highest possible time resolution, ERPs possess the
advantages of being easy to record noninvasively and unintrusively at
the patient's bedside in his/her familiar environment. In the future,
this method will be supplemented by some of the above-mentioned more
expensive and complicated technologies such as fMRI, PET, MEG, or
high-density EEG. The more measures that are used and the more
ingenious the cognitive paradigms employed, the more optimistic
judgment may be obtained concerning the information processing
capacity and the more frequently the examination of a patient in coma
or VS will yield a positive answer to the question posed in the title:
yes, there are mental functions there.
Acknowledgments
We gratefully acknowledge E. Herb, P. Maurer, G. Mezger, and D.
Schmalohr for fruitful discussions about patients with VS.
Research in our laboratory was supported by the Deutsche
Forschungsgemeinschaft and the Institut für Grenzgebiete in
Psychologie und Psychohygiene e.V. (Freiburg).
References
Top
Introduction
ERP methodology
Evoked potentials and ERPs...
"Waking coma" is not...
ERPs in VS
Increasing the reliability of...
Conclusions
References
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