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Vigilant Attention
Ian H Robertson and Hugh Garavan
Department of Psychology and Institute of Neuroscience
Trinity College Dublin, Ireland
Robertson IH and Garavan H (2004) Vigilant Attention. In M. S. Gazzaniga The Cognitive
Neurosciences, 3rd edition. Michael S. Gazzaniga Editor-in-Chief. MIT Press November 2004, 563578.
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Abstract
When train drivers pass through warning or stop signals – as they do many thousands of
times per day throughout the world – this is an example, we argue, of an inefficiency in
the functioning of a right hemispheric, fronto-parietal attention system for ‘vigilant
attention’. Closely linked to Posner’s notion of the ‘alerting’ system, vigilant attention is
distinct from Posner’s other two functionally and anatomically distinct supramodal
attentional systems – selection and control respectively. We review evidence for the
validity of this 3-factor typology of attention, and clarify the frequently articulated
misconception that ‘vigilance’ and ‘sustained attention’ are defined by time-on-task
decrements over extended periods of test performance, as originally proposed by
Mackworth. Rather, we show that vigilant attention involves a half-life measured in
seconds rather than minutes, and is most sensitively measured in situations where routine
action cycles are under way. We further show evidence of how everyday action error
propensities link to specific functional brain activation patterns and how Attention Deficit
Disorder can be an excellent model system for malfunctioning of this system. We end by
demonstrating the possibilities for rehabilitation of this system.
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A neglected dimension of attention
At 24 minutes past 5 on the 8th August 1996, the 17.04 train from London’s Euston
Station to Milton Keynes passed through a red signal near Watford Junction and
ploughed into an empty goods train, killing just one person - Ruth Holland - associate
editor of the British Medical Journal and a close colleague of the first author of this
chapter.
The driver of the train, Peter Afford, was later cleared of criminal charges for having
passed the red signal; the court accepted his defence that trees and bushes had obscured
the signal. He also told the court that he could not remember seeing two early warning
signals that would have told him to expect a red light at the next signal point.
Signals passed at danger (SPAD) is the most common cause of accidents on railways
(Edkins and Pollock, 1997) and imperfectly sustained attention is by far the major factor
in these errors. Every day, thousands of signals are passed at danger by train drivers
worldwide, but thankfully only a small number result in tragedy – partly through good
fortune and partly through the presence in some railway systems of other backup safety
measures. This type of error is classified as a skill-based slip that typically occurs during
routine action sequences (Reason, 1992). The job of driving a train is typically routine,
stopping at stations and travelling sections of track that the driver has passed many times
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before. Familiar surroundings and well-practised sequences of actions minimise the need
for effortful attention on the part of the driver.
The focus of the current chapter is that type of attentional control that is crucially
required for error-free performance of this type of task. This type of attention is linked to
a number of hitherto ambiguously defined concepts such as vigilance, alertness, sustained
attention and arousal. We will use the term ‘vigilant attention’ to characterise this in the
present chapter. Among the first studies of vigilant attention to be carried out were those
by Mackworth and his colleagues at the MRC Applied Psychology Unit in Cambridge,
UK. These were particularly inspired by the problems encountered by operators of the
recently developed radar, who had to maintain attention to a small, dim and mostly
unchanging screen, for rare but crucially important events – enemy or about-to-collide
aircraft. This research concluded that it was often difficult to pull human observers off
ceiling on this type of vigilance task and that errors, when they did occur, were only
observed over relatively long time periods approaching – usually more than 30 minutes
(Mackworth, 1968; Mackworth, 1950).
The difficulty in finding sensitive measures of vigilant attention, as demonstrated by
these contemporary measures, may have been one factor that led to its relative neglect for
the next 30 years, in comparison, that is, to the burgeoning research in other major
aspects of attention linked to selection, working memory and switching. A second reason
for its demise as a major subject of research may have been the loss of confidence in the
unitary nature of its sister process – arousal. The classic studies of Moruzzi and Magoun
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(Moruzzi and Magoun, 1949) suggesting the existence of a single arousal-modulating
reticular formation gave way to evidence for the existence of multiple ascending
pathways from subcortical nuclei, each linked to different neurotransmitters and different
cortical innervation (Olszewski and Baxter, 1982).
The resurrection of vigilant attention as an important dimension of attention is due
largely to the work of Michael Posner (Posner and Boies, 1971) and Raja Parasuraman
(Parasuraman, 1983) with the onset of human functional brain imaging providing a major
boost to the validity of their typologies of attention (Posner and Peterson, 1990). Posner
and colleagues suggested the existence of three main functionally and anatomically
distinct types of supramodal attentional control systems - selection, orientation and
alertness. This was somewhat different from Posner and Boies earlier typology –
selection, capacity and alertness, but close to Parasuraman’s typology of selection,
control and vigilance (Parasuraman, 1998). The important aspect of these typographies,
however, is the clear distinction between attention as selection/management of goals in
working memory on the one hand versus attention as vigilant attention linked to alertness
on the other. It is the latter of these two dimensions that we focus on in the current
chapter.
The restless brain: Why doing little is so hard
If vigilance is such a fundamental dimension of attention, why is it relatively difficult to
show decrements on standard vigilance tasks in normal human adults? Mackworth’s
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would-be radar operators in a darkened room often performed normally for an hour or
longer before they began to show the vigilance decrement that was seen to be the
hallmark of this attentional system. Even in people with traumatic brain injury and
consequently impaired frontal lobe/attentional deficits, marginal decrements could only
be observed in sustained attention when the visual stimuli were heavily perceptually
degraded (Parasuraman et al., 1991).
Responding to infrequent target versus inhibiting ongoing behaviour
Why should train drivers frequently miss danger signals while participants in vigilance
experiments show such good performance? A possible answer to this question may be
that, unlike the radar operators who must make a response to rare targets, train drivers
must inhibit their ongoing behaviour in the context of a rare target – namely a red or
warning signal. When required to make a response, the presentation of the rare target can
facilitate performance insofar as (a) the default response in a task such as this is not to
respond thereby providing time to detect the target and make the appropriate response
and (b) the presentation of the rare target can itself serve to orient attention to its
presence. Contrast this with the circumstance in which people must inhibit responding to
rare stimuli. Here, the ongoing default behaviour (responding, or in the case of the train
driver, to keep driving forward) is opposite to the desired response (i.e., interrupt the
default behaviour). Furthermore, the ongoing behaviour which engages the person in
well-practiced behaviours can create the illusion that the person is attentively engaged in
the task at hand. However, the automatic quality of the behaviour can be deceptive as it,
in fact, requires little vigilant attention. Consequently, the commission error might be
committed before the person can countermand it or, as in the train driver, without the
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person even noticing that the countermand was required. This distinction between
responding and inhibiting also rests on whether the vigilant attention for the task must be
generated endogenously or is supported by exogenous task demands, an important issue
that will be addressed later.
This distinction can be seen clearly when you compare frontally- and attentionallyimpaired traumatic brain injury patients with controls on a task that requires detection of
rare targets with one which requires inhibition of response to rare targets – the latter
being more closely analogous to the train driver situation (Robertson et al., 1997a). In
this study, controls and traumatic brain injured patients made statistically
indistinguishable numbers of errors when they had to detect rare (11%) targets ascending or descending trios of digits (eg 234 or 987 in an otherwise random stream of
one-per-second digits). Yet the frontally-impaired patients did show significant
impairment – twice the error rate of controls – on a task where they had to withhold a
response to the number 3, also appearing 11% of the time in the same stream of randomly
appearing digits (Sustained Attention to Response Task – SART). We believe these
deficits result from a dynamic interaction between inhibitory abilities and vigilant
attention as becomes apparent when we made the sequence of digits entirely predictable –
1,2,3,4,5,6,7,8,9,1,2,3 … etc. Whereas normal controls make only occasional errors on
this task, TBI patients have considerable difficulty and in one study made more than 7 out
of 25 errors – 28% - despite there being a totally predictable sequence leading up to the
target letter (Manly et al., in press-b)(see figure 1). Here, the inability to withhold
responding is likely due to an inability to maintain a sufficient level of arousal and a
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sufficiently strong representation of the task goals (“don’t respond to 3”): when vigilant
attention is poor, the patient defaults to the frequent response. Later we will expand on
these two central components of vigilant attention, arousal and goal representation.
Figure 1 about here
Exogenous versus endogenous modulation of vigilant attention
As we will discuss later in the section on arousal, vigilant attention can be impaired
through administration of drugs – for instance clonidine - that inhibit noradrenaline
release. One study, for example (Smith and Nutt, 1996), confirmed that noradrenaline
suppression in humans led to vigilant attention lapses but they also showed that this effect
was much attenuated when the participants were exposed to loud white noise while
performing the task. This suggests that external stimuli can induce ‘bottom-up’ or
exogenous modulation of the cortical systems for vigilant attention. Coull and her
colleagues confirmed that this is indeed the case (Coull et al., 1995b); (Coull et al.,
1995a), showing that clonidine-induced noradrenergic suppression impaired vigilant
attention performance much more when the task was familiar than when it was
unfamiliar. Furthermore, other research by Arnsten and Contant ((Arnsten and Contant,
1992)) showed that the clonidine affected delayed response performance during a delay
period less when a distractor was interpolated in the delay period than when the period
was free of distractors. This apparently paradoxical effect where the deleterious effect of
a drug is reduced by making the task more difficult is a key finding in understanding how
the vigilant attention system might function. What these findings suggest is that this
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system can be engaged by both endogenous and exogenous means; furthermore, where
exogenous activation takes place, we argue, this considerably reduces the demands on the
endogenous components of the system. But do exogenous and endogenous input activate
the system in the same way? One of our recent studies suggest that this may not be the
case.
In a recent fMRI study of the SART (O'Connor et al., in press-b) we showed that,
compared to a rest period, the standard SART (press to digits, except to randomly
appearing, 11% frequency, 3’s) showed precisely the right fronto-parietal activation that
we would predict as being needed for a task that placed demands on the vigilant attention
system. We had previously shown, however, that performance on SART and on other
tasks requiring vigilant attention could be much enhanced by presenting non-informative
auditory arousing tones randomly during task performance (Manly et al., 2002; Manly et
al., in press-a). On the basis of these data, we predicted that these exogenous stimuli
externally activated vigilant attention, hence reducing the demands on the endogenous
components of that system that we argue are based in the right hemisphere fronto-parietal
system. What we in fact found was that presenting alerting tones during SART did
eliminate the right frontal activation, but did not eliminate the right parietal activation. In
other words, it seems as if the parietal component of the right hemisphere vigilant
attention system may be a common pathway for both endogenous and exogenous routes,
while the right frontal element may be particularly linked to endogenous activation. We
have also shown that increasing the task demand in the SART paradoxically reduces the
proportional number of errors of commission. When the inhibit target is relatively rare –
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11% - proportionately more errors are made than when the target is more common – 25%
- and the proportional error rate declines linearly as the target rate increases to 50%
(Manly et al., 1999) (see figure 2a). Furthermore, self-reported proneness to everyday
attentional slips - such as forgetting why one has walked into a room (as measured by the
cognitive failures questionnaire (Broadbent et al., 1982)- are significantly related to the
proportion of errors made on the 11% target frequency SART, but not where the targets
are more frequent (see figure 2b) (Manly et al., 1999). We interpret these effects as being
due to the repeated targets in the higher frequency condition providing increased
exogenous support for the task through repeated activation of the “inhibit response”
motor action and goal representation. We believe that one feature of tasks sensitive to the
vigilance system is that this type of exogenous support is absent or relatively weak and
consequently the vigilance system must be maintained endogenously, a function for
which the right prefrontal areas appear especially important.
Figure 2 a and b about here
Attention and Arousal
What is ‘arousal’?
Arousal has been defined as ‘…some level of non-specific neuronal excitability deriving
from the structures formerly known as the reticular formation but now generally referred
to as specific chemically defined or thalamic systems that innervate the forebrain’
(Robbins and Everitt, 1995). This definition rescues the concept of arousal from doubts
about its unitary nature that followed the original identification of this function with the
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reticular formation (Moruzzi and Magoun, 1949). This identification was based in part on
the finding that electrical stimulation of this subcortical region elicited behavioural
arousal and EEG desychronisation characteristic of the alert state. Furthermore, lesions to
this region caused coma, and these and other findings led to the concept of the midbrain
reticular formation and associated structures as a key system for regulating cortical
arousal. Subsequent research however showed that a number of neuroanatomically and
neurochemically distinct systems projected to various parts of the cortex from different
subcortical nuclei including the cholinergic basal forebrain, the noradrenergic locus
coeruleus, the dopaminergic median forebrain bundle and the serotinergic dorsal raphe
nucleus. Understandably, confidence in a single construct of ‘cortical arousal’ was
considerably weakened by these findings (Olszewski and Baxter, 1982).
Human functional brain imaging helped revive the flagging concept of arousal as a useful
explanatory heuristic. Kinomura, Paus and their colleagues identified the midbrain
reticular formation and the intralaminar and other thalamic nuclei with arousal
(Kinomura et al., 1996; Paus et al., 1997). Both Paus (Paus et al., 1997) and Critchley
(Critchley et al., 2001; Critchley et al., 2002) have proposed that the anterior cingulate
plays a key role in regulating arousal in response to task demands, thereby providing
neuroanatomical guidance on how the vigilant attention system might interface with
subcortical arousal mechanisms. The extensive connectivity between fronto-parietal
areas and the cingulate may enable the communication between these two systems.
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Electrophysiological measures have also continued to generate data that confirm the
utililty of – for heuristic purposes at least – accepting the existence of arousal as a viable
concept. In the Paus et al PET study cited earlier, for instance, the decline in sustained
attention over time was associated not only with a decline in metabolic activity in the
right hemisphere cortical and subcortical regions already described, it was also correlated
with an increase in low-frequency activity in the EEG spectrum. A further study (Makeig
and Jung, 1995) showed that vigilance errors were linked to short-term changes in the
EEG spectrum, and these changes correlated with concurrent changes in level of
performance on a sustained auditory detection task. This author concluded: "…the onedimensional relationship between detection performance and the EEG spectrum confirms
quantitatively the intuitive assumption that minute-scale changes in behavioral alertness
during drowsiness are predominantly linked to changes in global brain dynamics along a
single dimension of psychophysiological arousal" (p 213).
While it is outwith the scope of this chapter to review the neurochemistry of arousal, a
number of authors ((Berridge and Waterhouse, 2003; Posner and Peterson, 1990; Usher et
al., 1999)) make a strong case for a particularly close linkage between vigilant attention
on the one hand, and the activity of the noradrenergic system on the other. Animal
research shows, for instance, that locus coerulus activity is higher when animals are
observed as being behaviourally alert (Aston-Jones et al., 1991). Furthermore the
appearance of a low-probability target among foils leads to increased LC activity and
widespread noradrenergic release (Berridge and Waterhouse, 2003). As will be seen
below, the relationship is likely more complex than this, but the evidence of a close
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linkage between noradrenergic activity and vigilant behaviour is strong. This is
particularly true given the evidence, cited earlier, that in humans, reducing noradrenaline
release through clonidine administration results in the sorts of attentional lapses
characteristic of states of poor alertness/sustained attention (Smith and Nutt, 1996). There
is some evidence also that noradrenaline may have a stronger right than left hemisphere
innervation (Oke et al., 1978; Robinson, 1979), giving further support to a particularly
close relationship between the vigilant attention system and noradrenaline activity.
While the cholinergic system is also involved in vigilant attention (Sarter et al., 2001) it
is the evidence for noradrenergic right hemispheric lateralisation combined with the clear
right hemisphere dominance for vigilant attention that lead many authors to postulate a
particular linkage between noradrenaline and vigilant attention.
Links between Attention and Arousal
In 1908, Robert Yerkes and John Dodson studied the effects of different degrees of
arousal (by varying degree of shock) in mice on their ability to learn discriminations
between the luminance of two compartments (Yerkes and Dodson, 1908). They found
that where lightness levels were easily discriminated, the mice performed better at high
levels of arousal, whereas difficult light discriminations were best learned at low levels of
arousal. On the basis of these experiments, they formulated the Yerkes-Dodson law. This
law proposed that any task will have an optimal level of arousal below and beyond which
performance will decline; this optimal level is lower in challenging tasks than in routine
tasks, they hypothesised. Similarly, Donald Broadbent showed that stress can improve
performance on routine, non-demanding tasks, but the same levels of stress can impair
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performance on more complex and demanding tasks (Broadbent, 1971). These classical
psychological studies suggesting an interaction between arousal levels, optimal
performance, and degree of challenge in a task mesh well with the notion of exogenous
modulation of arousal as previously discussed. It also suggests, however, that the
relationship between the system for vigilant attention and arousal may not be a simple
one of mutual facilitation, and a number of other more recent studies support such a view.
Progress has been made in identifying the neuroanatomical basis for this attention-arousal
coupling. For example, locus coeruleus (LC) activity has been show to correlate closely
with behavioural performance where monkeys have to detect relatively rare (20%
probability) visual targets among foils, but optimal performance was achieved not at
maximum levels of locus coeruleus activity, but rather at intermediate levels (Usher et
al., 1999). Increased tonic LC noradrenergic activity was linked to decreased reponsivity
of LC neurons to target stimuli, as well as to poor behavioural performance. These
authors proposed that high tonic LC activity offers a mechanism for sampling new
stimuli and behaviours by decreasing attentional selectivity and increasing the
behavioural responsiveness to unexpected or novel stimuli. Intermediate levels of tonic
LC activity, on the other hand, allow the optimising of performance in a stable
environment. In a comprehensive review of catecholamine modulation of prefrontal
cognitive function, Arnsten showed that many studies have confirmed the findings of
Usher et al, in showing a Yerkes-Dodson type inverted-U relationship between levels of
noradrenalin release on the one hand, and behavioural performance on the other (Arnsten,
1998). She also concludes that different neuropsychiatric conditions may reveal
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impairment in executive control of complex behaviours for reasons of either deficient or
excessive levels of noradrenaline respectively.
The study mentioned earlier by Paus and colleagues (Paus, Zatorre, Hofle, Caramanos,
Gotman, Petrides et al., 1997) demonstrated the inter-relatedness of attention and arousal.
To recap, in this study healthy participants were asked to perform a simple vigilance task
for around 60 min. Every 10 min, regional cerebral blood flow and EEG were measured.
Significant reductions in blood flow were observed in subcortical structures, the
thalamus, substantia innominata and putamen, and in right hemisphere cortical areas,
including frontal and parietal cortex. These were interpreted by the authors as a
subcortical arousal system and right cortical attentional system, respectively. Increases in
low theta activity, associated with reduction in arousal, were also observed on the EEG as
the task progressed. Despite the reduction in blood flow in the right hemisphere based
“attentional” and subcortical “arousal” networks, the number of successful target
detections did not significantly decline over the hour of the task. This was interpreted as
reflecting a need for active attentional engagement early on in the task which declined as
target detection became increasingly automatic. Results such as these suggest that the
term “sustained attention” may be somewhat inappropriately applied to situations which
clearly require sustained performance but which may actually make relatively limited
demands on what might be termed vigilant attention. This distinction is perhaps best
captured by consideration of whether “maintaining” responsivity to an arbitrary but
overlearned stimulus such as one’s own name requires anything approaching an active
maintenance of attention at all.
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Such a conclusion would be supported by Coull et al (Coull et al., 1996) who also found
declines in thalamic and right fronto-parietal perfusion over an 18 minute task period in
which participants had to respond whenever any letter appeared on the screen, and these
stimuli appeared on average every 20 seconds, with a range of 10-30 seconds. In contrast,
when the task was made a relatively difficult selective attention task by requiring
participants to respond only to red B's interspersed among red and blue B's and G's , no
significant decline in the right frontal and parietal cortices was observed. This is in line
with the earlier arguments about the effects of exogenous demand on vigilant attention,
and suggests that this right fronto-parietal system for vigilant attention is - in part at least
- a system needed to maintain alert and reasonably accurate responding in the absence of
strong external demands or stimuli that otherwise 'support' alert responding.
Assuming this to be the case, then a major role of the right fronto-parietal system is to
modulate arousal, particularly where that arousal is not externally generated by task
demand or stimulus. As mentioned earlier, the anterior cingulate may serve on the
interface between cognition and emotion and may serve as a conduit by which the right
prefrontal-parietal system modulates arousal levels.
This appearance of a functional wood from out of the neurochemical trees allows us to
begin to develop the concept of a broad mesencephalic arousal system operating in
concert with a predominantly right hemisphere fronto-parietal vigilant attention system.
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What distinct contributions the right prefrontal and right parietal structures might make to
vigilant attention is the topic to which we will next turn.
Fronto-parietal interactions in vigilant attention
The right dorsolateral prefrontal and inferior parietal cortices of the right hemisphere
have been widely implicated in vigilant attention, as we have demonstrated over the last
several pages. One possibility is that the right prefrontal cortex may have a particular role
in the endogenous components of this system, while the inferior parietal cortex may be
commonly activated by both endogenous and exogenous pathways. We have shown that
the effects of exogenous alerting stimuli on performance on the SART, described earlier
(O'Connor et al., in press-a) were to reduce neuronal activity in the right prefrontal
cortex, but not in the right inferior parietal cortex. A recent meta-analysis of error-related
activations (n=44) from a number of our event-related GO/NOGO response inhibition
tasks similar in structure to the SART has revealed robust right inferior parietal lobule
activation that correlated negatively with the numbers of errors subjects committed. We
have consistently seen this parietal area and right dorsolateral prefrontal cortex coactivated during response inhibition (Garavan et al., 1999; 2002). The presence of the
parietal activation for both errors and successful inhibitions suggests that it has a more
general attentional role in processing the salient NOGO stimuli and not in response
inhibition per se, while the negative correlation suggests that greater activation here is
associated with better performance. The right prefrontal area is probably critical to the
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response selection process itself (Garavan et al., 2002; Garavan et al., 1999) (Rowe et al.,
2000).
Combined, these disparate findings suggest that the right inferior parietal cortex has a
role in the routine, semi-automatic maintenance of sustained vigilant responding, whereas
the right dorsolateral prefrontal cortex has a more "executive" role in maintaining the
vigilant state. One hypothesis for what this executive role involves might be to
engage/initiate the vigilant state based on a dynamic assessment of the optimal arousal
level to match performance to task demands. This implies that the monitoring of either
one's endogenous arousal levels or of one's performance is information crucial for the
functioning of the vigilant attention system. This monitoring function might be
performed by the right prefrontal area itself with, for example, inputs from relevant
midline structures that detect errors or response conflict ((Dehaene et al., 1994)
(Botvinick et al., 2001)). Alternatively, if these other structures perform the monitoring
function themselves, then the right prefrontal cortex's role would be to modulate arousal
levels based on their outputs. Either way, it would seem to be the case that vigilant
attention operates in an interactive way with other executive functions, a topic that we
will turn to next.
Relationship between vigilant attention and other executive systems
We conceive of the right parietal-prefrontal network and its interactions with the
midbrain arousal systems as the circuitry by which vigilant attention is maintained. This
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circuitry can be “turned up” endogenously or with exogenous support. Within this
system, we believe that the prefrontal cortex plays a central role in maintaining and
monitoring optimal arousal levels to match current task demands. Although we can
conceive of this system as somewhat independent and autonomous, in order to be
responsive to changing tasks demands, changing performance levels, or changing
physiological resources such as might be depleted by fatigue, monitoring processes must
be tightly coupled with, or intrinsic to, its functioning. In addition, this system works in
the service of current task goals and close interaction between it and goal representations
are to be expected. Consequently, the type of attentional control that has been the focus
of this chapter need not be isolated from the other aspects of attention linked to selection,
working memory and switching that were mentioned at the beginning of this chapter.
The nature of the relationship between goal state representation and vigilance is,
however, not very well understood. It may be the case that the goal state (e.g., take the
train safely from station A to station B) may call upon the vigilant attention system to
ensure the goal is attained in the circumstances already described in which exogenous
support is minimal. However, if the goal can be actively maintained in a focus of
attention within working memory (Garavan, 1998) then this may, in fact, reduce reliance
on the vigilance system. For example, inhibiting a response to the number 3 in the SART
task is quite easy if you have just refreshed that rule, perhaps by subvocally re-iterating to
yourself that you must not respond to 3's (indeed, we have demonstrated in patients with
impaired fronto-parietal function that precisely this type of verbal regulation can
compensate for sub-optimal vigilance (Robertson et al., 1995). Inhibiting to the 3
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becomes difficult - and reliant on the vigilant attention system - if the "inhibit to 3" goal
is no longer prominent but, instead, has been allowed to decay. A number of lines of
evidence implicate left prefrontal areas in this type of goal maintenance (Brass and
Cramon, 2002; Frith and Dolan, 1996; Garavan, 1998; MacDonald et al., 2000; Ruchsow
et al., 2002) which implies inter-hemispheric interaction between goal representations
and vigilant attention.
Combined, this conceptualisation of vigilant attention and its interaction with goal
representations provides a basis for different types of attentional impairment. First, the
subcortical arousal or cortical vigilant attention systems - the "machinery" of attention might be damaged leading to gross vigilance impairments that may not be easily
amenable to rehabilitation. Second, the functioning of the task goal system and/or its
interaction with the vigilance systems may be compromised. That is, while the
machinery (i.e., the ability to attend) may be intact, the mechanisms by which this
machinery is mustered in the service of task goals might be compromised. Patients who
can muster sufficient attentional resources with exogenous support (e.g., cueing, phasic
alerting) but have difficulty doing so without this support may have this second type of
dysfunction.
We can perhaps gain an insight into the interactions between vigilant attention and other
executive functions by observing the processes involved in preparing for an attentionally
demanding task. A predictive cue that warns of an impending task involves the
endogenous activation of a vigilant state. We have recently shown that the areas
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activated in anticipation of a response inhibition include right prefrontal and parietal
cortex (Hester et al., under review). This may reflect either engagement of the vigilant
attention system or, given that these areas were necessary for the subsequent inhibition,
may reflect preparatory activation of task-specific areas. Left prefrontal cortex was also
activated following the cue which we believe reflects task set re-activation as described
above. Furthermore, what uniquely distinguished a successful preparation from an
unsuccessful one (i.e., despite the cue, a commission error was made) was the
deactivation of midline prefrontal areas that are thought to be involved in the monitoring
of internal emotional states (Gusnard et al., 2001). The deactivation of task inappropriate
areas confirms a finding of similar deactivations underlying good performance in a Rapid
Visual Information Processing task (Lawrence et al., in press). Together, these additional
processes, the preparatory activation of task relevant areas and deactivation of task
inappropriate areas, may serve as additional attentional mechanisms that obviate reliance
on the vigilant attentional system.
The notion that vigilant attention is linked to deactivation of inappropriate areas raises the
question as to whether inhibition can be regarded as one means by which vigilant
attention is maintained: in the case of the London train driver, for instance, the ability to
detect the yellow warning signals may have been predicated on the ability to inhibit non
task-relevant cognitions, emotions and perceptions. While not synonymous, vigilant
attention and inhibition may be strongly overlapping functions both functionally and
anatomically, which would explain the very strong similarity in activation patterns for
vigilant attention and inhibitory tasks. Figure 3 shows activation associated with
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GO/NOGO response inhibition based on a meta-analysis of 58 subjects (Garavan and
Hester, in preparation). Robust event-related activation in the right dorsolateral
prefrontal and right inferior parietal lobule parallels tonic activation patterns observed for
vigilance tasks. The speculation follows that vigilant attention might be conceptualised as
a continuous inhibition of task irrelevances. Also shown on the figure is a more ventral
activation on the right inferior frontal gyrus. Inhibition-related activation in this inferior
region was significantly greater in those subjects scoring higher on the cognitive failures
questionnaire that we described above as correlating with SART performance. The region
in question in figure three also shows a correlation between inhibition-related activation
and age, suggesting that this structure is used more both by highly absentminded and
older people (Garavan and Hester, in preparation). Furthermore, older subjects also
showed significantly greater left prefrontal activation than younger subjects, consistent
with an age-related increased dependence on the left hemisphere task-set re-activation
mechanism. While the relationship between vigilant attention and inhibition must be
investigated further, these results offer encouragement in the search for the
neuroanatomical bases for these executive functions and their relationship to normal
individual variability and pathological disturbance.
Figure 3 about here
Attention Deficit Hyperactivity Disorder
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Robertson and Garavan
23
Attention Deficit Hyperactivity Disorder is a complex condition with a number of
different subtypes, and a range of associated cognitive and motivational impairments
(Castellanos and Tannock, 2002). What is interesting about this disorder in the context of
the current chapter is the fact that the Inattentive subtype of the disorder includes a
profile of impaired sustained attention, absent-mindedness, distractibility and action slips
that are extremely close to the pattern of adult behaviour we have described in this
chapter as being linked to a deficient vigilant attention system. Bearing in mind this
similarity in behaviour patterns, and without wishing to ignore the abnormalities in other
brain regions such as the caudate nucleus and the vermis of the cerebellum that have been
identified in ADHD, it is of considerable interest that there are also abnormalities in the
right frontal lobe – particularly in the underlying white matter (Castellanos et al., 1996) –
in ADHD. Furthermore, we have also shown that, compared to IQ-matched controls,
children with ADHD are impaired on sustained but not selective attention performance
(Manly et al., 2001).
The remarkable responsiveness of these attentional deficits in ADHD to methylphenidate
or amphetamine (Solanto et al., 2001) – drugs that potentiate noradrenergic as well as
dopaminergic release – also links the vigilant attention system and its arousal-modulating
role to this clinical syndrome. This is particularly true given the EEG evidence of low
tonic arousal as manifested by high theta power in the EEG spectrum (Bresnahan and
Barry, 2002). We have recently shown that the fixed sequence SART that discriminated
traumatic brain injured patients from controls so well, also discriminates between ADHD
and controls (Connell et al., in preparation). Furthermore, tests of vigilant attention in a
23
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24
children’s battery of attention consistently discriminate ADHD participants from controls
in a way that selective attention tests do not (Manly et al., 2001).
To summarise, important aspects of the ADHD syndrome may constitute an important
manifestation of deficits of the vigilant attention system, and therefore progress that has
been made towards rehabilitation deficits in this system may potentially be applicable to
ADHD: it is to this final question that we turn now.
Rehabilitation and Vigilant Attention
The ability to sustain vigilant attention seems to be an important factor in determining
recovery of motor and other function following stroke (Ben-Yishay et al., 1968; BlancGarin, 1994). Furthermore we have shown that motor recovery following stroke over a 2year period was significantly predicted by measures of sustained attention taken 2 months
after right hemisphere stroke. Specifically, the ability to sustain attention to a tone
counting task (a validated measure of sustained attention related to right frontal function
(Wilkins et al., 1987)) at two months post-stroke predicted not only everyday life
function 2 years later, but also the functional dexterity of the left hand in a pegboard task
(Robertson et al., 1997b).
24
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25
Impairment in sustained attention may also be a key factor in the development of the
disabling condition unilateral spatial neglect – a relatively common consequence of right
hemisphere stroke (Husain and Rorden, 2003; Robertson, 2001). Apart from the disabling
consequences of impaired vigilant attention itself, it is likely that impairments in this
system have more wide-ranging consequences for recovery from brain damage and the
learning that underpins rehabilitation effects (Robertson and Murre, 1999).
It is possible to enhance vigilant attention both in the short term through exogenous
means (Manly et al., 2002; Manly et al., in press-a) and also over longer periods by
training patients endogenously to implement metacognitive, verbally-regulated strategies
(Robertson et al., 1995). We have further shown that short-term exogenous activation of
the vigilant attention and arousal systems can temporarily alleviate neglect-induced
spatial bias (Robertson et al., 1998). Similar methods have now been incorporated as an
element in a more comprehensive and successful system of rehabilitation for executive
problems following frontal lobe damage (Levine et al., 2000).
Conclusions
When you have driven your train a hundred times through a light that was always green,
it is all too easy for the brain to miss the yellow light that appears on the 101st journey and to let the train-driving motor programme run on, unsupervised - occasionally to
catastrophe. If that yellow light is detected, the accelerator handle released, and the train
slowed down in preparation to stop at the next light, it is thanks to the right hemisphere of
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the brain, and in particular the right dorsolateral prefrontal and inferior parietal cortices –
working in concert with thalamic and mesencephalic circuits. Repeated, unchallenging
stimuli in the context of highly practiced actions diminish arousal, dull sensory
responsiveness and blunt vigilant oversight of one’s actions and environment. The
reciprocal action of a right hemisphere cortical network on the one hand, and a
subcortical arousal network on the other, has evolved to protect against such a potentially
dangerous diminution of awareness and monitoring. Because so much of what we do is
practised and automatic, this system is needed throughout our waking day. The next time
you walk into a room, scratch your head and wonder - ‘now why did I come in here?’ –
you are witnessing a minor inefficiency of this system.
Bibliography
Arnsten AFT. Catecholamine modulation of prefrontal cortical cognitive function. Trends
in Cognitive Sciences 1998; 2: 436-447.
Arnsten AFT, Contant TA. Alpha-2 adrenergic agonists decrease distractibility in aged
monkeys performing the delayed response task. Psychopharmacology 1992; 108:
159-169.
Aston-Jones G, Chiang C, Alexinsky T. Discharge of noradrenergic locus coeruleus
neurons in behaving rats and monkeys suggests a role in vigilance. In: Barnes CD
and Pompeiano O, editors. Progress in Brain Research. Vol 88. Amsterdam:
Elsevier Science, 1991: 501-520.
Ben-Yishay Y, Diller L, Gerstman L, Haas A. The relationship between impersistence,
intellectual function and outcome of rehabilitation in patients with left
hemiplegia. Neurology 1968; 18: 852-861.
26
Robertson and Garavan
27
Berridge CW, Waterhouse BD. The locus-coeruleus-noradrenergic system: modulation of
behavioral state and state-dependent cognitive processes. Brain Research Reviews
2003; 42: 33-84.
Blanc-Garin J. Patterns of recovery from hemiplegia following stroke.
Neuropsychological Rehabilitation 1994; 4: 359-385.
Botvinick MW, Carter CS, Braver TS, Barch DM, Cohen JD. Conflict monitoring and
cognitive control. Psychological Review 2001; 108: 624-652.
Brass M, Cramon DYv. The role of the frontal cortex in task preparation. Cerebral Cortex
2002; 12: 908-914.
Bresnahan SM, Barry RJ. Specificity of quantitative EEG analysis in adults with attention
deficit hyperactivity disorder. Psychiatry Research 2002; 112: 133-144.
Broadbent DB, Cooper PF, FitzGerald P, Parkes KR. The Cognitive Failures
Questionnaire (CFQ) and its correlates. British Journal of Clinical Psychology
1982; 21: 1-16.
Broadbent DE. Decision and stress. London: Academic Press, 1971.
Castellanos FX, Giedd JN, Marsh WL, Hamburger SD, Vaituzis AC, Dickstein DP, et al.
Quantitative brain magnetic-resonance-imaging in attention-deficit hyperactivity
disorder. Archives of General Psychiatry 1996; 53: 607-616.
Castellanos FX, Tannock R. Neuroscience of attention-deficit/hyperactivity disorder: the
search for endophenotypes. Nature Reviews Neuroscience 2002; 3: 617-628.
Connell R, Bellgrove M, Robertson IH. Vigilant attention in ADHD. in preparation.
Coull JT, Frackowiak RSJ, Frith CD. Monitoring for target objects: activation of right
frontal and parietal cortices with increasing time on task. Neuropsychologia 1998;
36: 1325-1334.
Coull JT, Frith CD, Frackowiak RSJ, Grasby PM. A fronto-parietal network for rapid
visual information-processing: A PET study of sustained attention and working
memory. Neuropsychologia 1996; 34: 1085-1095.
Coull JT, Middelton HC, Robbins TW, Sahakian BJ. Differential effects of of clonidine,
haloperidol, diazepam and tryptophan depletion on focused attention and
attentional search. Psychopharmacology 1995a; 121: 222-230.
Coull JT, Middleton HC, Robbins TW, Sahakian BJ. Clonidine and diazepam have
differential effects on tests of attention and learning. Psychopharmacology 1995b;
120: 322-332.
Critchley HD, Melmed RN, Featherstone E, Mathias CJ, Dolan RJ. Brain activity during
biofeedback relaxation: A functional neuroimaging investigation. Brain 2001;
124: 1003-1012.
Critchley HD, Melmed RN, Featherstone RN, Mathias CJ, Dolan RJ. Volitional control
of autonomic arousal: A functional magnetic resonance study. NeuroImage 2002;
16: 909-919.
Dehaene S, Posner MI, Tucker DM. Localization of a neural system for error detection
and compensation. Psychological Science 1994; 5: 303-305.
Edkins G, Pollock C. The influence of sustained attention on railway accidents. Accident
Analysis and Prevention 1997; 29: 533-539.
Frith C, Dolan R. The role of the prefrontal cortex in higher cognitive functions.
Cognitive Brain Research 1996; 5: 175-181.
27
Robertson and Garavan
28
Garavan H. Serial attention within working memory. Memory & Cognition 1998; 26:
263-276.
Garavan H, Hester R. Individual differences in executive control: A Meta analysis of four
event-related fMRI studies using the GO/NOGO task.. in preparation.
Garavan H, Ross TJ, Murphy K, Roche RAP, Stein EA. Dissociable executive functions
in the dynamic control of behaviour: Inhibition, error detection and correction.
NeuroImage 2002; 17: 1820-1829.
Garavan H, Ross TJ, Stein EA. Right hemispheric dominance of inhibitory control: an
event-related fMRI study. Proceedings of the National Academy of Sciences,
USA 1999; 96: 8301-8306.
Gusnard DA, Akbudak E, Shulman GL, Raichle ME. Medial prefrontal cortex and selfreferential mental activity: relation to a default mode of brain function.
Proceedings of the National Academy of Sciences, USA 2001; 98: 4259-64.
Hester R, Fassbender C, Garavan H. Individual differences in error processing: A review
and meta-analysis of three event-related fMRI studies using the GO/NOGO task..
under review.
Hester R, Murphy K, Foxe DM, Foxe J, Garavan. H. Predicting success: The effect of
pre-target cueing on inhibition performance. under review.
Husain M, Rorden C. Non-spatially lateralized mechanisms in hemispatial neglect.
Nature Reviews Neuroscience 2003; 4: 26-36.
Johannsen P, Jakobsen J, Bruhn P, Hansen SB, Gee A, Stødkilde-Jørgensen H, et al.
Cortical sites of sustained and divided attention in normal elderly humans.
NeuroImage 1997; 6: 145-155.
Kinomura S, Larsson J, Gulyas B, Roland PE. Activation by attention of the human
reticular formation and thalamic intralaminar nuclei. Science 1996; 271: 512-515.
Lawrence N, Ross T, Hoffman R, Garavan H, Stein EA. Activation and deactivation
during the rapid visual information processing task: an fMRI study. Journal of
Cognitive Neuroscience in press.
Levine B, Robertson I, Clare L, Carter G, Hong J, Wilson BA, et al. Rehabilitation of
executive functioning: An experimental-clinical validation of Goal Management
Training. Journal of the International Neuropsychological Society 2000.
MacDonald AW, Cohen JD, Stenger A, Carter CS. Dissociating the role of the
dorsolateral prefrontal and anterior cingulate cortex in cognitive control-1838.
Science 2000; 288: 1835-1838.
Mackworth JF. Vigilance, arousal and habituation. Psychological Review 1968; 75: 308322.
Mackworth NH. Researches in the measurement of human performance. In: Sinaiko HA,
editor. Selected papers on human factors in the design and use of control systems.
Dover: Dover Publications, 1950.
Makeig S, Jung T-P. Changes in alertness are a principle component of variance in the
EEG spectrum. NeuroReport 1995; 7: 213-216.
Manly T, Anderson V, Nimmo-Smith I, Turner A, Watson P, Robertson IH. The
differential assessment of children's attention: The Test of Everyday Attention for
Children (TEA-Ch), normative sample and ADHD performance. Journal of Child
Psychology and Psychiatry 2001; 42: 1-10.
28
Robertson and Garavan
29
Manly T, Hawkins K, Evans J, Woldt K, Robertson IH. Rehabilitation of Executive
Function: Facilitation of effective goal management on complex tasks using
periodic auditory alerts. Neuropsychologia 2002; 40: 271-281.
Manly T, Heutink J, Davison B, Gaynord B, Greenfield E, Parr A, et al. An electronic
knot in the handkerchief: 'Content free cueing' and the maintenance of attentive
control. Neuropsychological Rehabilitation in press-a.
Manly T, Owen AM, McAvinue L, Datta A, Lewis GA, Scott SK, et al. Enhancing the
sensitivity of a sustained attention task to frontal damage. Convergent clinical and
functional imaging evidence. Neurocase in press-b.
Manly T, Robertson IH, Galloway M, Hawkins K. The absent mind: Further
investigations of sustained attention to response. Neuropsychologia 1999; 37:
661-670.
McDonald S, Bennett KMB, Chambers H, Castiello U. Covert orienting and focusing of
attention in children with attention deficit hyperactivity disorder.
Neuropsychologia 1999; 37: 345-356.
Moruzzi G, Magoun HW. Brainstem reticular formation and activation of the EEG.
Electroencephalography and Clinical Neurophysiology 1949; 1: 455-473.
O'Connor C, Manly T, Robertson IH, Hevenor SJ, Levine B. Endogenous vs. exogenous
engagement of sustained attention: an fMRI study. The Clinical
Neuropsychologist in press-a.
O'Connor C, Manly T, Robertson IH, Hevenor SJ, Levine B. Endogenous vs. exogenous
engagement of sustained attention: an fMRI study. The Clinical
Neuropsychologist in press-b.
Oke A, Keller R, Mefford I, Adams R. Lateralization of norepinephrine in human
thalamus. Science 1978; 200: 1411-1413.
Olszewski J, Baxter D. Cytoarchitecture of the human brainstem (2nd ed). New York::
Karger, 1982.
Parasuraman R. Vigilance, arousal and the brain. In: Gale A and Edwards JA, editors.
Physiological correlates of human behaviour. London: Academic Press, 1983: 3555.
Parasuraman R. The Attentive Brain. Cambridge, MA: MIT Press, 1998.
Parasuraman R, Mutter SA, Molloy R. Sustained attention following mild closed-head
injury. Journal of Clinical and Experimental Neuropsychology 1991; 13: 789-811.
Parasuraman R, Warm J, See J. Brain systems of vigilance. In: Parasuraman R, editor.
Varieties of Attention. Cambridge, MA: MIT Press, 1998: 221-256.
Paus T, Zatorre RJ, Hofle N, Caramanos Z, Gotman J, Petrides M, et al. Time-related
changes in neural systems underlying attention and arousal during the
performance of an auditory vigilance task. Journal of Cognitive Neuroscience
1997; 9: 392-408.
Posner MI. Chronometric explorations of mind. Hillsdale, NJ: Lawrence Erlbaum, 1978.
Posner MI, Boies S. Components of attention. Psychological Review 1971; 78: 391-408.
Posner MI, Inhoff AW, Friedrich FJ. Isolating attentional systems: A cognitiveanatomical analysis. Psychobiology 1987; 15: 107-121.
Posner MI, Peterson SE. The attention system of the human brain. Annual Review of
Neuroscience 1990; 13: 25-42.
Reason J. Human Error. Cambridge: Cambridge University Press, 1992.
29
Robertson and Garavan
30
Robbins TW, Everitt BJ. Arousal systems in attention. In: Gazzaniga MS, editor. The
cognitive neurosciences. Cambridge, MA.: MIT Press, 1995: 703-720.
Robertson IH. Do we need the "Lateral" in unilateral neglect? Spatially nonselective
attention deficits in unilateral neglect and their implications for rehabilitation.
Neuroimage 2001; 14: S85-S90.
Robertson IH, Manly T, Andrade J, Baddeley BT, Yiend J. Oops!: Performance
correlates of everyday attentional failures in traumatic brain injured and normal
subjects: The Sustained Attention to Response Task (SART). Neuropsychologia
1997a; 35: 747-758.
Robertson IH, Mattingley JB, Rorden C, Driver J. Phasic alerting of neglect patients
overcomes their spatial deficit in visual awareness. Nature 1998; 395: 169-172.
Robertson IH, Murre JMJ. Rehabilitation of brain damage: Brain plasticity and principles
of guided recovery. Psychological Bulletin 1999; 125: 544-575.
Robertson IH, Ridgeway V, Greenfield E, Parr A. Motor recovery after stroke depends
on intact sustained attention: A two-year follow-up study. Neuropsychology
1997b; 11: 290-295.
Robertson IH, Tegner R, Tham K, Lo A, Nimmo-Smith I. Sustained attention training
for unilateral neglect: theoretical and rehabilitation implications. Journal of
Clinical and Experimental Neuropsychology 1995; 17: 416-430.
Robinson RG. Differential behavioral and biochemical effects of right and left
hemispheric infarction in the rat. Science 1979; 205: 707–710.
Rowe JB, Toni I, Josephs O, Frackowiak RSJ, Passingham RE. The prefrontal cortex:
Response selection or maintenance within working memory? Science 2000; 288:
1656-1660.
Ruchsow M, Grothe J, Spitzer M, Kiefer M. Human anterior cingulate coretx is activated
by negative feedback: evidence from event-related potentials in a guessing task.
Neuroscience Letters 2002; 325: 203-206.
Rueckert L, Grafman J. Sustained attention deficits in patients with right frontal lesions.
Neuropsychologia 1996; 34: 953-963.
Sarter M, Givens B, Bruno JP. The cognitive neuroscience of sustained attention: where
top-down meets bottom-up. Brain Research Reviews 2001; 35: 146-160.
Smith A, Nutt D. Noradrenaline and attention lapses. Nature 1996; 380: 291.
Solanto MV, Arnsten AFT, Castellanos FX. Stimulant Drugs and ADHD: Basic and
Clinical Neuroscience. Oxford: Oxford University Press, 2001.
Sturm W, Simone Ad, Krause BJ, Specht K, Hesselmann V, Radermacher I, et al.
Functional anatomy of intrinsic alertness: Evidence for a fronto-parietal-thalamicbrainstem network in the right hemisphere. Neuropsychologia 1999; 37: 797-805.
Usher M, Cohen JD, Servan-Schreiber D, Rajkowski J, Aston-Jones G. The role of locus
cueruleus in the regulation of cognitive performance. Science 1999; 283: 549-553.
Vandenberghe R, Gitelman R, Parrish TB, Mesulam MM. Functional specificity of
superior parietal mediation of spatial shifting. NeuroImage 2001; 14: 661-673.
Wilkins AJ, Shallice T, McCarthy R. Frontal lesions and sustained attention.
Neuropsychologia 1987; 25: 359-365.
Yamaguchi S, Tsuchiya H, Kobayashi S. Electoencephalographic activity associated with
shifts of visual attention. Brain 1994; 117: 553-562.
30
Robertson and Garavan
31
Yerkes RM, Dodson JD. The relation of strength of stimulus to rapidity of habitformation. Journal of Comparative and Neurological Psychology 1908; 18: 459482.
31
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Captions
Figure 1
Commission errors on the random versus fixed SART for traumatic brain injured versus
controls (Manly et al., in press-b) (see text).
Figure 2a
Proportional ommission errors increase as no-go target probability decreases (SART)
(Manly et al., 1999)
Figure 2b
Commission errors on 11% no-go versus 50% no-go (SART) for high and low cognitive
failure-prone subjects (Manly et al., 1999).
Figure 3
Extensive dorsolateral and parietal activation in red is shown for event-related response
inhibition. Activation in blue on the right inferior frontal gyrus was correlated with the
CFQ score suggesting a greater reliance on this right prefrontal area in those subjects
scoring highest on everyday absentmindedness (Garavan and Hester, in preparation).
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TBI Errors
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11% lure
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50% lure
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