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Invited Conference

MEASURING ATTENTION IN NEUROPSYCHOLOGICAL DIAGNOSIS AND


REHABILITATION
M. Rosario Rueda#*, Jin Fan* & Michael I. Posner#*,
#University of Oregon, Eugene and *Sackler Institute, Weill Medical College of
Cornell University
ABSTRACT
We have developed a simple computerized Attention Network Test (ANT) as a way
of quickly measuring the efficiency of the orienting, alerting and executive networks
involved in attention to the external environment and internal thoughts. The test involves
responding to a central arrow by pressing one key if it points left and another if it points
right. Flankers of the target can be congruent or incongruent and the difference provides a
measure of the time to resolve conflict (executive attention). Cues prior to the target serve
as warning signals (alerting) and as a cue to the target location (orienting). In normal
adults the three resulting networks have separate anatomy and the network scores are for
the most part independent. We have developed a version of the ANT for children as
young as four years old and we think it will be easily used by a variety of patient
populations. This test and previous measures employing parts of the ANT have proven
useful for the purpose of diagnosis and we believe will be helpful in measuring the effects
of rehabilitation. In this paper we outline the ANT results with normals, and illustrate its
use with various patient populations.
Background
Functional neuroimaging has allowed many cognitive tasks to be analyzed in terms of
the brain areas they activate. Studies of attention have been among the most often
examined in this way. Data from different domains have supported the presence of three
brain networks that contribute to the cognitive concept of attention. These networks carry
out the functions of alerting, orienting and executive control [1,2]. The three brain
networks have been shown to differ in their functional anatomy, the circuitry of their
component operations and the neurochemical modulators that influence their efficiency
[2]. Alerting is defined as achieving and maintaining a state of high sensitivity to
incoming stimuli; orienting is the selection of information from sensory input; and
executive control is defined as involving the mechanisms for resolving conflict among
thoughts, feelings and responses.
The alerting system has been associated with frontal and parietal regions particularly
of the right hemisphere. An effective way to vary alertness has been to use warning
signals prior to targets. The influence of warning signals on the level of alertness is
thought to be due to modulation of neural activity by the norepinephrine system. Studies
with primates have provided strong evidence of a double dissociation that relates

norepinephrine to the alerting network and acetylcholine to the orienting network [3, 4].
The same result has been observed in rats [4, 5].
Orienting involves aligning attention with a source of sensory signals. This may be
overt as in eye movements or may occur covertly without any movement. The orienting
system for visual events has been associated with posterior brain areas including the
superior parietal lobe and temporal parietal junction and, in addition, the frontal eye
fields. Orienting can be manipulated by presenting a cue indicating where in space a
person should attend, thereby directing attention to the cued location [6]. Event related
functional magnetic resonance imaging (fMRI) studies have suggested that the superior
parietal lobe is associated with orienting following the presentation of a cue [7]. The
superior parietal lobe in humans is closely related to the lateral intraparietal area (LIP) in
monkeys, which is known to produce eye movements [8]. When a target occurs at an
uncued location and attention has to be disengaged and moved to a new location, there is
activity in the temporal parietal junction [7]. Lesions of the parietal lobe and superior
temporal lobe have been consistently related to difficulties in orienting [9]. In addition,
pharmacological studies carried out with animals that have been trained to use cues to
direct attention to targets have shown the cholinergic system to modulate covert orienting
responses [5, 10].
Executive control of attention is required in situations that involve planning, error
detection, novelty and difficult processing or conflict situations in which overcoming
habitual actions are needed. The function of the conflict network seems to be modulated
by the dopaminergic system [1]. Executive functions are often studied by tasks that
involve conflict, such as various versions of the Stroop task. In the Stroop task subjects
must respond to the ink color (e.g. red) of a word while ignoring the color word name
(e.g. blue). Resolving conflict in the Stroop task activates midline frontal areas (anterior
cingulate) and lateral prefrontal cortex [11, 12]. There is evidence for the activation of
this network in tasks involving conflict between a central target and surrounding flankers
when these are incongruent with the target and suggest a different and inappropriate
response [13, 14, 15]. Studies of adults using the flanker task with arrows have shown
activation of the anterior cingulate and lateral prefrontal areas that are common to other
conflict tasks [16]. Imaging studies carried out with tasks designed to analyze different
operations involved in executive attention indicate that lateral areas of the prefrontal
cortex are involved in representing specific information over time, while medial areas are
more related to the detection and monitoring of conflict [12, 13, 14, 17]. Fractionating the
functional contributions of different areas within the executive attention network is
important for a better understanding of the psychopathology of the system since
particular disabilities may be related to specific component operations of cognitive
control [18, 15].
The ANT Task
To study individual differences in these networks we have developed an attention
network test (ANT). This task examines the efficiency of the three brain networks we
have discussed above [19]. The ANT procedure and the reaction times (RT) subtractions

used to measure the efficiency of each network is shown in Figure 1. Subtracting RTs
obtained in the double cue condition from RT in the no cue condition gives a measure of
alerting due to a warning signal. Subtracting RTs to targets at the cued location (spatial
cue) from trials using a central cue gives a measure of orienting. Subtracting congruent
from incongruent target trials provides a measure of conflict. The data provide three
numbers that represent the skill of each individual in the alerting, orienting and executive
networks.
INSERT FIGURE 1 APPROXIMATELY HERE
The ANT has some useful properties as a measure of attentional efficiency. It does
not use language stimuli so it can be used with children, speakers of any language and
patients unable to read or special populations. In about 20 minutes the test provides a
measure of the efficiency of the alerting, orienting and conflict networks with reasonable
reliability, in addition to overall RT and error rates. Measuring the three networks scores
in the same test also allows assessment of possible patterns of interactions between them.
We do not exclude the possibility that certain psychopathologies or brain-injured patients
would have a dysfunction on the way the attentional networks interact.
In a sample of 40 normal persons we found the network scores to be reliable over two
successive presentations. In addition, we found no correlation among the three network
scores. An analysis of the reaction times found in this task shows large main effects for
cueing and for the type of target, but only two small but significant interactions [19].
They both involve very small reductions in conflict when either no warning cue is
provided or when the cue is at the location of the target. The latter interaction is to be
expected because the effective eccentricity of flankers is increased when attention is
specifically on the central arrow. The first finding appears to arise because with no
warning the subject is generally slow and some conflict resolution may occur during the
longer overall RT. This effect also appears to be responsible for a small but significant
negative correlation between alerting and conflict (r=-.18; p<.01) when we examine a
larger sample of more than 200 people who have taken the ANT [20].
Recently, the ANT scores have been used as a phenotype to assay the heritability of
each attentional function with a sample of 26 pairs of MZ and DZ twins [21]. In
accordance with their neuroanatomical and behavioral independence, the three attentional
networks also showed different heritability indexes. Despite the small scale of the study,
the executive network scores showed significant correlation (r=.73) between the MZ
twins, this correlation was also significant, although weaker, for the alerting scores
(r=.46), while the orienting network showed no evidence of heritability.
Interpreting the ANT scores
Although we use subtraction of reactions times in the ANT as a measure of the
efficiency of the networks, interpretation of the efficiency of the various networks
between groups needs to be made with the full range of reaction time and accuracy data
in mind. In general larger differences between incongruent and congruent RTs mean

more difficulty in resolving conflict. This is straightforward if errors differences are in


the same direction, but interpretation is complex if one group shows larger RT
differences while the other group shows larger error differences. In this case, different
conflict scores could reflect different strategies of approaching the task instead of
differences in the ability to resolve conflict. A more conservative individual (or group)
who opts for being accurate will mainly produce slow responses in the incongruent
situation in which the probability of committing an error is higher. This approach results
in an increased conflict RT score.
Larger alerting numbers generally arise when one group has difficulty in maintaining
alertness without a cue. This is clearly the case in right parietal strokes. Younger subjects
also show more difficulty when no cue warns them of a trial. However, in some cases
larger numbers might arise because one group uses a cue more efficiently, perhaps by
increased effort. In that case larger RT differences between no cue and double cue may
not indicate less efficient performance. Taking into account RT and errors rates for each
condition helps to interpret the scores and examine possible differences in strategies
between groups.
The case of orienting is complex because in the ANT we do not vary probabilities in a
way which can give a measure of the time to disengage from a clearly attended location.
We generally assume that larger orienting times arise because of a difficulty in
disengaging from the central cue, but of course no target occurs there. Disengagement
difficulties would implicate a deficit of the type found in parietal patients. However, it is
also possible that through effort more efficient use may be made of the peripheral cue in
which case larger number could indicate improved orienting. A careful analysis of all of
the data is needed to make a judgment about the efficiency of each network. One helpful
approach to this question is to examine how attentional networks change with age.
Development
We have developed a child version of the ANT task. In previous work we found that
children work best when there is a story and when there is clear feedback on their
performance [22]. In the child version of the ANT five colorful fish replaced the arrows
that typically appear in the flanker task. We invite the children to help us make the
middle fish happy by pressing a button corresponding to the direction in which it is
swimming. Visual feedback (the middle fish smiles and some bubbles come out of its
mouth) and auditory feedback (a woohoo sound) is provided when the response has
been successful. In each trial, the flanker fish are swimming in the same (congruent) or
opposite (incongruent) direction as the center fish. As in the adult version, different types
of cues are presented before the fish so the efficiency of the three attentional networks
can be assayed using the same subtractions explained before.
Using the child ANT we have assayed the developmental course of the attentional
networks [23]. As in the adult data, the child study also revealed independence between
the three networks scores. Table 1 shows the networks scores of five groups of children
between 6 and 10 years of age and a group of adults as measured by the child ANT.

Overall performance measures (RT and accuracy) are fundamental to interpreting the
network scores specially when comparing populations with differences in overall reaction
time and accuracy.
INSERT TABLE 1 APPROXIMATELY HERE
Developmental studies such the one summarized in Table 1 involve large differences
in overall RT and accuracy. Despite this common decline in RT, each network shows a
different developmental course. There is a significant improvement in conflict resolution
at age seven compared to younger children, but a remarkable stability in both RT and
accuracy conflict scores from the age seven to adulthood. The alerting scores show some
improvement in late childhood and continued development between ten year olds and
adults. Finally, the orienting score was similar to adult levels at the age of six.
Application
Although the attention network test itself is new there are already substantial results
using components of the task to study the various disorders discussed below.
Stroke
Parietal lesions often show neglect of the side of space opposite the lesion. Patients
with right and left parietal lesions have been studied extensively by use of a cued
detection task similar to the orienting part of the ANT [24]. Lesions of the right and left
parietal lobe, most often from stroke produce a deficit in orienting attention to the side of
space opposite the lesion. In addition right but not left parietal patients have shown a
deficit in maintaining the alert state [25]. These findings have fit well with neuroimaging
results which have shown a role for the superior parietal lobe in voluntary shifts of
attention toward the opposite side of space and of the temporal parietal junction in
involuntary shifts when targets occur at unattended locations [26].
There have been a number of efforts to study rehabilitation based upon ideas that
have arisen in these studies. For example, Ladavas, Menghini and Umilta [27] have
studied the use of central cues to compensate for patients who have had parietal damage
and peripheral cues to aid those with central damage and has shown that building upon
the remaining function provides greater success than the reverse. Robertson [28] has
attempted to compensate for right parietal damage by use of subsidiary cues that maintain
the alert state in these patients. Again this provided some support for the loss of alertness
specific to right parietal patients.
Alzheimer
Some patients with Alzheimers disease have a difficulty in finding their way around.
This led Parasurman to test whether these patients might also show a deficit in the ability
to orient to visual locations, in a manner analogous to what is found in neglect patients. In
one study [29] it was found that early Alzheimer patients were similar to normals in
responding to peripheral cues to attend to targets, but had greater than normal difficulty in

using central cues to voluntarily shift attention to an expected location. The Alzheimers
patients also showed reductions in cerebral blood flow in the superior parietal cortex,
which correlated with the extent of deficit in their orienting behavior.
More recently, Greenwood [30] found that asymptomatic persons with the APOE4
gene, which is related to early Alzheimers, show similar abnormalities as the patients.
These and related results suggest that damage to a particular brain area will produce
similar effects on component operations even when they arise from very different
disorders.
Autism
Another disorder that involves the orienting system is Autism [31, 32]. It is well
know that autistic persons do not normally orient to faces. However, in preliminary work,
Rodier has shown difficulty in orienting in tasks that involve non-social stimuli as in the
ANT. Similar deficits in the ability to disengage and move attention have been reported
in autism in relation to abnormal development of the cerebellum [31]. We do not know if
this abnormality is due only to cerebellar deficits since many of the patients also show
parietal abnormalities as well. Rodier [32] has some evidence that the abnormalities
found in autism might relate to a gene associated with migration of cells in early
development.
ADHD
Many theories of ADHD have suggested a deficit in executive functions. However,
in early work using a spatial orienting task the most compelling deficit appeared to be a
difficulty in maintaining the alert state in the absence of a warning signal [33]. This
difficulty might arise from right hemisphere damage which has also been reported to be a
feature in many studies of ADHD. More recent studies of the full ANT have also shown
problems with alerting, mostly due to the inability to hold the alert state when no warning
signal was used. In one study [34], the full ANT was used to attempt to discriminate the
inattentive subtype from normals and the combined subtype. The alerting network best
distinguished the different forms of ADHD.
Neuroimaging studies however have generally shown right frontal, cingulate and
basal ganglia deficits [35]. These results are more closely related to executive attention
deficits. Since right frontal areas have been related both to problems with the alert state
and with inhibitory control there could be links between the orienting studies and these
imaging studies, but that remains to be established.
Schizophrenia
A number of years ago we tested never medicated schizophrenic patients with a cued
detection task similar to the orienting part of the ANT. At rest, these subjects had shown
a focal decrease in cerebral blood flow in the left globus palidus [36] a part of the basal
ganglia with close ties to the anterior cingulate. The subjects showed a deficit in orienting
similar to what we had shown for left parietal patients [36]. When their visual attention
was engaged they had difficulty in shifting attention to the right visual field. However,
they also showed deficits in conflict tasks particularly when they had to rely on a

language cue. We concluded that the overall pattern of their behavior was most consistent
with a deficit in the anterior cingulate and basal ganglia, which are parts of a frontally
based executive attention system. First break schizophrenic subjects often have been
shown to have left hemisphere deficits and there have been many reports of anterior
cingulate and basal ganglia deficits in patients with schizophrenia [37]. Although the
executive attention system in general and the anterior cingulate in particular has often
been shown to be active in orienting tasks, we do not know the exact link between the
executive attention and orienting network.
Closed Head Injury
From studies of rehabilitation of closed head injury patients, Strum [38] has suggested
that we may view attention networks as hierarchical with alerting as being required
before it is possible to remediate higher networks. However, in our work with the ANT
we have generally found a great deal of independence between the networks among
normal persons. In a study of rehabilitation we used attention process therapy as a
treatment and a neuropsychological course as a control group [39]. We found that
executive networks were both the most impaired by the multiple lesions in these patients
and the most likely to show the differential training effects of attention process therapy
[39]. In some cases, improvement in executive attention did depend upon the level of
alertness, with patients showing the highest level of alertness being the most likely to
show improvement.
Closed head injury patients seemed to have the greatest difficulty in high-level tasks
involving executive attention such as paced serial addition and Stroop [39]. We found
that they also had difficulties in anticipation based upon cues, a function often related to
frontal lobe impairment. The ANT task would be a good one with this population in
differentiating the types of attentional impairment that might be present and helping to
design an appropriate remediation perhaps using the Strum guidelines [38].
Borderline Personality
Borderline personality disorder is characterized by very great liability of affect and
difficulty in interpersonal relations. In some cases patients are suicidal or involved in
self-mutilation. Because this diagnosis has been studied largely by psychoanalysts it
might at first be thought of as a pour candidate for a specific pathophysiology involving
attentional networks. However, in our study of these patients with the ANT we did find a
deficit specific to the executive attention network in compared to normals and although
not significant, greater than what was found in control groups matched on the
temperamental variables of negative affect and effortful control [40].
Preliminary imaging results suggested overgeneralization of responding in the
amygdala and reduced responding in the anterior cingulate and related midline frontal
areas [41]. Preliminary analysis suggested that patients with higher effortful control and
lower conflict scores on the ANT were the most likely to show the effects of therapy.
This study is ongoing so it will be another year before it will be possible to relate specific
aspects of the psychoanalytic and cognitive-behavioral therapies to differences of the
ANT and in brain scanning.

Rehabilitation
Although we have not been able to fully review the literature in this paper it is clear
that many disorders in neurology and psychiatry involve deficits of attention. Some
disorders appear primarily in orienting, others involve alerting and still others executive
control. However, it is not likely that these differences could be used for differential
diagnosis. Rather we believe the ANT could best be used to help target the direction of
therapy and to design improved therapies. We have conducted a neuroimaging study with
the ANT [42]. By use of an event related fMRI design and appropriate subtractions we
were able to show the activation of separate brain networks for the alerting, orienting and
executive attention. The ability to examine each of these networks separately before and
after therapy might help to guide the construction of the optimal therapies according to
which networks are damaged.
Both deficits that involve closed head injury and psychopathologies could be
classified according to the attentional networks involved by using the ANT prior to
therapy. The therapy could be tuned to assist in restoration of the damaged networks and
the influence of the therapy could be assayed by a post ANT. This strategy might be
combined with neuroimaging conducted while performing the ANT to examine the brain
response to therapy of each of the brain networks. This approach might in time lead to the
development of optimal therapeutic strategies for the deficits induced by different
attentional networks.
The work of Robertson and his collaborators [25, 28, 43] and Ladavas and colleagues
[27] are excellent examples of this approach in the cognitive rehabilitation of orienting
deficits in neglect patients. Patients suffering this dysfunction show a difficulty,
sometimes a complete failure, in reporting or interacting with objects in the hemispace
contralateral to the site of the lesion, usually the left hemispace since the damage is most
commonly related to the parietal, dorsolateral and frontal lobes of the right hemisphere. A
cognitive task used by Robertson to assay the attentional deficits in these patients requires
them to report when two visual stimuli are presented simultaneously. In order to be
perceived as appearing simultaneously by neglect patients the left-most stimuli has to
actually appear earlier than the right one, in some cases as earlier as 1 second. However,
this left hemisphere disadvantage is eliminated by presenting an auditory alerting tone
previously to the display of the visual stimuli [25]. This interaction between the alerting
and orienting systems in neglect has been successfully harnessed for rehabilitation
purposes. When neglect patients are trained to increase their levels of general alertness
using self-instructional methods, these patients show significant improvements in
measures of unilateral neglect and sustained alertness but no changes on other type of
cognitive tasks (like working memory tasks) [28].
As mentioned before, studies of closed head injury patients have provided evidence of
successful improvement of executive attention with a training based therapy [39]. Since
the training used auditory input and the test of improvements involved visual tasks there

was evidence of generalization. In addition, working memory training [44] has proved to
be effective for children with ADHD. Working memory involves executive systems
closely related to the executive attention network. More extensive training programs
based upon animal research for improving executive attention are currently under
development [45]. In these new studies the ANT combined with high density EEG is used
to assay the effectiveness of the training program.
In the era of Cognitive Neuroscience, non-invasive brain imaging methods are
combined with cognitive tasks to analyze the anatomy and time course of the mental
operations involved in these tasks [46]. This can lead to a better understanding of
individual differences among normal persons and of neuropsychological disorders.
Increased knowledge of the mechanisms involved in neuropsychological disorders should
help improve rehabilitation methods

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12

Figure 1. Representation of the sequence of events in each trial of the ANT task (adult
version).

ATTENTIONAL NETWORKS SUBTRACTIONS


ALERTING: RT no cue RT double cue
ORIENTING: RT central cue RT spatial cue
CONFLICT: RT incongruent RT congruent
congruent
incongruent
Fixation
Cue

*
+

+
~ 400-800
ms

Target

+
+

100 ms

400 ms
RT<1700
ms

+
no cue

*
+
*
double
cue

*
+

*
central
cue

spatial
cue

13

500 ms

Table 1. Attentional networks scores and overall performance data in function of age as
measured by the child ANT.
Attentional Networks Subtractions
Overall
Conflict
Accuracy Alerting Orienting Conflict Accuracy
15.8
79
58
115
15.6

Age
6

Overall
RT
931

833

5.7

100

62

63

0.7

806

4.9

73

63

71

-0.3

734

2.7

79

42

67

1.6

10

640

2.2

41

46

69

2.1

adults

483

1.2

30

32

61

1.6

14

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