Attention and its disorders
Darren R Gitelman
Cognitive Neurology and Alzheimer’s Disease Center, Departments of Neurology, and Radiology,
Northwestern University Medical School, Chicago, and VA Healthcare System Lakeside Division,
Chicago, Illinois, USA
Correspondence to:
Darren R Gitelman MD,
Northwestern University
Medical School, 320 E
Superior St, Searle 11-470,
Chicago, IL 60611, USA
British Medical Bulletin 2003; 65: 21–34
DOI 10.1093/bmb/ldg65.021
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This chapter focuses on the clinical aspects of attention including anatomy,
cognitive neuropsychology, disorders, and functional imaging evidence for the
role of attention in cognition. Particular emphasis is given to selected aspects of
visual attention. Imaging studies discussed are primarily functional magnetic
resonance imaging (fMRI) and positron emission tomography (PET). In addition,
some evidence will be provided from the time-honoured clinical method of
lesion studies.
Numerous cognitive processes come into play as one reads this chapter. In
fact, it takes little introspection to realize the necessity for visual, language,
working memory, and declarative memory (among other) systems in the
reading process. Perhaps this chapter will contradict or confirm a cherished
scientific belief, thus bringing limbic systems into play. However, the
proper operation of all these systems would not be possible without a
function that allowed the appropriate selection of stimuli, maintenance of
concentration, and interactions with space and time. That cognitive
function is attention. Indeed, it could be argued that while most other
cognitive systems can operate somewhat independently of one another (e.g.
patients with aphasia can still see just as well and patients with pure
amnesia can still speak) none of them could function at anywhere near
normal levels without the appropriate attentional interactions. Without
attention, coherent thought itself would be impossible.
The focus of this chapter will be on the clinical aspects of attention
including anatomy, cognitive neuropsychology, disorders, and
functional imaging evidence for the role of attention in cognition.
However, as the short space allotted to this chapter allows only a brief
overview of this domain, the discussion will be focused primarily on
selected aspects of visual attention. The interested reader should see the
references for additional information. The imaging studies discussed in
this chapter primarily fall into the domain of functional magnetic
resonance imaging (fMRI) and positron emission tomography (PET). In
addition, some evidence will be provided from the time-honoured
clinical method of lesion studies.
 The British Council 2003
Imaging neuroscience: clinical frontiers for diagnosis and management

Definition
Attention has been defined in many ways over the years, yet none of the
definitions has improved substantially on the one given by William
James in 1890. In his book, The Principles of Psychology, James stated1:
It [attention] is the taking possession by the mind, in clear and vivid form, of one

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out of what seem several simultaneously possible objects or trains of thought.
Focalization, concentration, of consciousness are of its essence. It implies
withdrawal from some things in order to deal effectively with others, and is a
condition which has a real opposite in the confused, dazed, scatterbrained state.

In this one paragraph, James provided both a definition of attention

and a remarkably prescient description of one type of attentional deficit,
that of a confusional state. As James’s statement implies, and recent
research has demonstrated, attention results in the preferential
processing of various types of cognitive information. For example,
attentional enhancement can be demonstrated for objects in the
environment, for actions, for perception of our own internal states, for
thoughts, for space and for time2–5. The multidimensional nature of
attention has led theorists to wonder whether the concept of attention is
well-conceived, i.e. whether it refers to a single or clearly definable set
of functions3,6. The approach taken in this chapter is that while attention
is not a unitary concept, it does represent a cohesive set of processes,
which serve to enhance sensory, motor and cognitive processing.

Attentional components
Figure 1 presents a schematic for the basic organization and anatomy of
attention. Each of these levels will be discussed in turn. Any discussion
of attention must first comment on the relationship between attention
and arousal since the terms appear so closely related. It seems logical, for
example, that an organism with impaired arousal would also have
impaired attention. The reverse, however, is not necessarily true as
normally alert individuals can show attentional deficits2. Furthermore,
states of hyperarousal (e.g. pain and fear) may interfere with proper
attentional functioning.
The core of the arousal system includes the mesencephalic reticular
formation and portions of the thalamus (reticular and intralaminar nuclei).
Together, these regions comprise one part of the ascending reticular
activating system (ARAS). The other components of this system of a series
of brainstem (substantia nigra, ventral tegmental area, raphe nuclei, and
locus coeruleus) and basal forebrain nuclei2. Activity in the ARAS results in
a wakeful state, desynchronizes the electroencephalogram, and modulates

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 Attention and its disorders

Top-down
attentional modulation
Frontal, parietal & limbic cortices

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Bottom-up
attentional competition
Visual, auditory, & somatosensory
association cortices + others?

Arousal mechanisms
Ascending reticular
activating system

Fig. 1 Graphical representation of the main psychological and anatomical aspects of

attention. In the case of bottom-up attentional competition, other anatomical regions
might include those involved with motor planing (e.g. premotor cortex), time intervals or
thoughts, though this has not been shown. Adapted from Mesulam2 with permission from
Oxford University Press.

neuronal responsivity7. Changes in the state of arousal will thus clearly

influence cortical and subcortical areas involved with attention. The
opposite relationship is also true and changes in the attentional state of
an organism can influence the activity in the ARAS. For example,
Kinomura and colleagues demonstrated the influence of attention on
ARAS activity by using PET to compare regional cerebral blood flow
(rCBF) when subjects were awake but resting versus when they were
engaged in attentionally demanding tasks. During the state of high
attention, rCBF increased markedly in the mesencephalic tegmentum
and the intralaminar nuclei of the thalamus (among other regions)
confirming the hypothesized influence8. Figure 2 shows the activations
in the thalamus and mesencephalic tegmentum.
In keeping with the multidimensional nature of attention, several
different varieties have been identified. This situation is no different than
in other cognitive domains. For example, memory processing has been
divided into declarative, episodic, implicit, etc subgroups, while in the
language domain there are fluent and non-fluent aphasias among other
distinctions. The taxonomy of attentional divisions has tended to be
confusing, however, as it has often depended on what is being attended
to. For example, the term selective attention can refer to the selection of
objects, their attributes, or a portion of space.

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Fig. 2 Increased rCBF during tasks requiring a high attentional load. On the left, the arrow points to increased rCBF
in the intralaminar thalamic nuclei. On the right, the arrow points to activation in the mesencephalic tegmentum.
Adapted from Kinomura et al8 with permission from the American Association for the Advancement of Science.

Selective attention is one of the most studied aspects of attention and is

the aspect of attention most often referred to when discussing the brain’s
limited processing capacity and the need to select particular targets among
multiple stimulus streams. What exactly an organism is selecting will
depend on the task being performed. Selection can encompass many
domains, and evidence has accumulated for both object and space based
attentional selections9,10. Divided attention involves monitoring of several
stimuli at once. Vigilance refers to the sustained aspects of attention.
Vigilant behaviour can include both sustaining attention to a particular
stimulus over time or to the detection of and response to any unpredictable
or rare event11,12. Finally, the controlled aspects of attention refer to
behaviour in which attention to one activity is stopped so that attention
can be directed to another stimulus.

Anatomical and behavioural models

One set of cognitive models has postulated that various aspects of
attention act in a top-down manner to bias preferentially the processing
of stimuli. As illustrated in Figure 1, top-down refers to the influences of
heteromodal (posterior parietal and prefrontal) and limbic cortical areas
on unimodal visual, auditory and somatosensory cortices in order to
modulate the processing of stimuli based on the cognitive and
motivational preferences of the organism2. Top-down models of attention
have also been conceived as a type of mental spotlight, which enhances

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Fig. 3 Anatomical models for top-down attentional control. (A) Model adapted from Mesulam16 with permission
from Wiley. (B) Model adapted from Posner and colleagues5 with permission from MIT Press.

processing of the illuminated (i.e. selected) item13,14. Two main anatomical

models have emerged for this organization of attention. Although the
model developed by Mesulam comes from a more anatomical viewpoint,
and that of Posner stresses the particular psychological operations
involved, both models bear a remarkable similarity in the hypothesized
brain regions and cognitive processes (Fig. 3).
Mesulam’s model is characterized by each of the main cortical regions
containing a high-level abstract map of the world: a sensory-
representational map in the parietal cortex, a motor-exploratory-map in
the premotor cortex/frontal eye fields, and a limbic-motivational map in
the cingulate cortex and possibly insula. This anatomical organization
was based primarily on tract tracing studies in primates and behavioural
studies of patients with neglect (see Mesulam15,16 for references).
The model proposed by Posner and colleagues focuses on the cognitive
operations performed by each of the regions. Thus, the posterior
attentional network is responsible for moving the focus of attention.
This operation includes disengaging attention from its current target
(controlled by the parietal cortex), moving attention to a new target
(controlled by the superior colliculus) and engaging attention at the new
target (controlled by the pulvinar). The anterior attentional network is
involved with detecting salient events and preparing motor responses.
Finally, the vigilance network is in charge of sustaining attention and
maintaining a state of alertness17.
Both Mesulam’s and Posner’s models were initially intended to explain
the spatial aspects of attention and not the interaction of attention with
particular object features. In his 1981 article, Mesulam himself noted
that his theory did not account for all aspects of attention15. In addition,

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Fig. 4 Regions activated by covert shifts of spatial attention. Images were acquired using fMRI. Activated regions are
significant at P < 0.05 corrected for multiple comparisons. The group performing this task ranged in age from 24–80
years demonstrating that these activations are seen consistently across the adult ageing spectrum. Key: INS, insula;
IPS, intraparietal sulcus; FEF, frontal eye fields; TOJ, temporo-occipital junction (probably includes region MT+); TPJ,
temporo-parietal junction.

only Mesulam’s model comments on how neuronal responses might be

affected by attention15.
Despite these shortcomings of these models, both accurately
characterise the cortical and subcortical brain regions associated with
top-down attentional behaviours. Numerous functional imaging studies
have confirmed and re-confirmed the involvement of these top-down
areas (posterior parietal, frontal eye field and cingulate/supplementary
motor cortices) in various aspects of attention. Tasks producing
activations in these regions include sustaining attention18, shifting
attention covertly (without eye movements)19–22, shifting attention
overtly (with eye movements)23,24, and motivational biasing of
attentional behaviour25. Figure 4 illustrates the anatomy of regions
putatively involved with the top-down aspects of attention. Note that
activation of the temporo-occipital junction (TOJ) is likely to reflect top-
down influences on the visual system, rather than being part of the top-
down system per se.
Recent attentional models have begun to incorporate the concept of
bottom-up competition among stimuli (actually their neuronal
representations) to explain the effects of various target types on
attention, the dynamic interaction between perception and attention,
and the fine focus of the attention spotlight26. A ‘biased competition’
model suggests that competition occurs at the level of the sensory
association cortices among neurons representing different objects or

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Fig. 5 Visual cortex activation during various states of attention and visual stimulation. (A) Activations during the
presentation of a right peripheral visual stimulus while the subject’s attention was engaged in another task. (B)
Significantly larger activation in V4 compared with (A), when the subject attended to the visual stimulus. (C)
Attending to the location of an expected but not visible visual stimulus also activated V4. Laterality is indicted by R
(right) in (A). Adapted from figure 3 of Kastner and Ungerleider28 with permission from Elsevier.

locations in the environment. A further modulatory signal is provided by

the top-down attentional cortical centres, which provide feedback to the
visual regions. Competitive interactions take place across the stimulus
environment in a parallel manner. Attention thus emerges as a
combination of feed-forward signals from the visual cortices (bottom-
up) and feed-back signals from the parieto-frontal-limbic network (top-
down). The combined interactions are thought to bias positively
neurons representing the attended target(s) to ‘prevail’ in their
interactions. Presumably, similar competitive interactions occur in other
sensory cortices. In addition, neurons representing unattended stimuli
are thought to be suppressed in their responses26,27.
The principles of top-down and bottom-up interactions are
demonstrated in Figure 5, which is taken from the article by Kastner and
Ungerleider28. The figure demonstrates that in the absence of attention,
a visual stimulus is still able to activate visual association cortex (Fig.
5A). In the presence of attention, activation is greater at sites such as V4,
which are connected with up-stream (top-down) cortical areas (Fig. 5B).
When visual stimulation is removed, attention still affects the baseline
activity in visual association cortex (Fig. 5C). Thus, it appears that
attention can modulate baseline neural activity in order to prepare a
specialized region for processing some type of anticipated stimulus.
Attention further modulates the response of a region when the
appropriate stimulus appears29.

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The concepts underlying the biased competition model are also

important because they illustrate that attentional interactions can take
place potentially at all levels of sensory processing. These multilevel
attentional concepts have been incorporated into many current theories
of attention2,29.

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Disorders of attention
Given the importance of attention to sensory and cognitive processing, it is
not surprising that attentional disorders are among the most common and
most devastating neurological conditions. The main attentional disorders
are confusional states, partial (domain-specific) attentional syndromes, and
hemispatial neglect.

Confusional states

A confusional state (or delirium) is a global change in mental status

wherein the principal cognitive deficit is a change in the overall attentional
tone. It is the most common disturbance of mental status seen by
physicians. Associated symptoms can include incoherent thinking,
distractibility, perceptual disturbances including illusions or hallucinations,
dyscoordination, delusions, impaired judgement, reduced insight and
agitation. Some of these disturbances may arise because of the attentional
disorder while others may arise separately2.
Patients in a confusional state are usually disoriented and their memory
is impaired. They may appear to have mild-to-moderate associated
cognitive deficits such as an anomia, dysgraphia, dyscalculia, or
constructional difficulties2. The attentional nature of these disturbances
may become apparent if the patient is given additional assistance in a task.
For example, extra-encoding trials on memory tests may allow the patient
with a mild confusional state to overcome partially the apparent amnestic
disturbance.
Despite wide-spread cognitive disturbances, patients usually have no
lateralizing neurological signs and primary motor and sensory functions
are generally intact. When neurological signs occur, they may include a
coarse tremor, myoclonus or asterixis as an indicator of the patient’s
underlying metabolic disarray2. Focal neurological signs may be seen,
however, when the confusional state arises because of intrinsic central
nervous system disease (e.g. stroke).
The main causes of confusional states can be divided into six major
classes, which are listed in Table 1. Referring back to Figure 1, a
confusional state can involve any of the levels of the attention-arousal

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 Attention and its disorders

Table 1 Main disease classes leading to confusional states

Diagnostic class Examples and additional information

Toxic-metabolic encephalopathy Renal insufficiency, hepatic failure, sepsis, endocrine disorders,

severe anaemia, electrolyte and water-balance disorders, drug
withdrawal or intoxication

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Environmental stressors Circadian rhythm disturbances (e.g. in the intensive care unit),
immobilization, and sensory deprivation (e.g. sudden changes in
vision or hearing)

Multifocal brain lesions Meningitis, encephalitis, closed head injury, multiple strokes
(e.g. shower of emboli), and subarachnoid haemorrhage

Epilepsy Confusional states can be seen after a generalized seizure or in the

case of non-convulsive status epilepticus

Space occupying lesions Subdural haematoma

Focal brain lesions Lesions of the parahippocampal-fusiform-lingual gyri in either

cerebral hemisphere, or right-sided lesions of the posterior
parietal and inferior prefrontal cortex

system. The actual mechanisms of attentional disruptions include

multifocal disorders, strategic focal lesions, or interference with
neurotransmitter functions (particularly cholinergic). As listed in Table
1, the focal anatomical regions associated with a confusional state
include the parahippocampal-fusiform-lingual gyri in either cerebral
hemisphere, and right-sided lesions of the posterior parietal and inferior
prefrontal cortex.
There have been few functional imaging studies of patients in a
confusional state, probably because of the difficulties examining such
patients. In a study of 50 patients undergoing cardiac surgery, six were
found to have a delirium based on clinical examination30. These six and
another three patients, whose clinical diagnosis was not clear, were
found to have perfusion abnormalities by [99mTc]-HMPAO single
photon emission computed tomography (SPECT). Abnormalities were
noted in the left temporoparietal region (5 of 9 patients), right
temporoparietal region (4 of 9), frontal cortex on the left (1 of 9) or
right (3 of 9), and the right occipital cortex (2 of 9). Five of nine patients
had two or more areas of involvement. In a single patient study, a
SPECT scan demonstrated right parieto-occipital hypoperfusion in a
delirious patient2,30. These functional imaging studies are consistent with
the concept of a network of brain regions contributing to attention.
Damage to any part of this network may produce a confusional state,

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although some regions (e.g. temporoparietal cortex) appear to be more

critical than others.

Partial attentional syndromes

Attentional impairments can also present more focally as domain-

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specific or ‘partial’ attentional syndromes. These syndromes are not well
defined because partial attentional impairments tend not to present as
separately definable syndromes, rather they are manifest as reduced
performance in one or more cognitive domains. For example, changes in
visual-based attention could result in reduced detection of stimuli in the
environment, while changes in language-based attention could present
as reduced verbal fluency. In both these examples, the clinician must be
alert to the possibility of an attentional disruption rather than a visual
disorder or an aphasia, respectively.
Domain specific attention deficits have been produced in normal
individuals using tasks based on the concept of inattentional stimulus
processing. Such tasks present subjects with stimuli, which they either
attend or ignore. By examining the difference between the attend and
ignore conditions, the effects of attention on domain specific processing
can be observed. Rees and colleagues, for example, examined domain-
specific attentional effects on letter string and picture processing31. They
found that attention was able to influence, differentially, processing
within the visual system for words (left occipital activation) versus
pictures (bilateral occipitotemporal activations) even when the words
and pictures were both presented simultaneously at fixation. Attention
to words also enhanced activations throughout the language system31.

Hemispatial neglect

The last attentional disorder to be discussed is hemispatial neglect. This

disorder, one of the most clinically dramatic in neurology, is
characterized by the inability of the patient to orient towards, respond
to, or report on, stimuli on the contralesional side of space32. Neglect is
a multimodal deficit and may affect any or all sensory modalities, motor
behaviours or even the internal representations of memories and other
thoughts. Most often, the left hemispace is neglected, as the disorder is
more frequent and severe following right hemisphere injury.
Clinically, the patient’s head and eyes may be directed entirely towards
the ipsilesional space (usually right). When there is an accompanying
motor deficit, the patient may deny any problem with the affected limb
(anosognosia), may say they are moving the limb normally as it hangs

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 Attention and its disorders

limply at their side, or may fail to recognize the affected limb as their
own. Patients with neglect may fail to groom themselves properly on the
neglected side, or may fail to eat food on the neglected side of the dinner
plate. When reading, the patient may start towards the middle of a line
rather than on the left, for example, reading ‘your eyes’ when shown the
phrase ‘close your eyes’. It is important to note that basic sensory or
motor disorders are not part of the neglect syndrome, although they may

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be present.
The phenomenon of extinction may occur either together or separately
from neglect. Extinction is diagnosed by the patient being able to detect
stimuli presented separately to either side of space, but only detecting
one of the stimuli (usually right) when they are presented simultan-
eously. At times, the deficits associated with neglect are less dramatic
and may only be apparent when the patient is asked to perform more
specific tests such as bisecting lines or searching for targets among a set
of irrelevant stimuli.
Numerous theories have been proposed to account for the deficits in
neglect. Unfortunately, space constrains any discussion other than just a
listing of various theories and their chief proponents. Explanations have
included a distortion of internal representations (Bisiach), release of asym-
metrically opposed attentional vectors (Kinsbourne), impaired attention
towards the affected hemispace (Heilman and colleagues), impaired motor
intentional behaviour (Heilman), impaired disengagement of the
attentional focus from ipsilesional stimuli (Posner), distortion of the spatial
reference frame (Jeannerod, Karnath), multidimensional impairment of
selective attention (Mesulam), and altered premotor planning behaviours
(Rizzolatti)32,33.
Lesion sites causing neglect have been found throughout the network of
cortical and subcortical areas responsible for attention. These regions
include the posterior parietal cortex/temporoparietal junction, frontal eye
fields, cingulate and supplementary motor cortex, basal ganglia, thalamus,
midbrain and superior colliculus2. Typically, the lesions are on the right.
Only some functional imaging studies have demonstrated findings
consistent with right hemispheric dominance for attention. Some of these
studies have shown a greater number of activated regions on the right,
while others have shown a larger size of the right-sided activations19–21.
However, it can be difficult to show significant hemispheric differences in
attentional activation studies (personal observations) and the true nature of
this difference may have to await a finer analysis of the time-course of these
activations.
Only a few recent studies have been able to examine directly the
deficits of neglect and extinction with functional imaging technology.
Vuilleumier and colleagues studied a patient with neglect due to a right
parietal lesion, who had intact visual fields34. Event-related fMRI was

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used to show that non-perceived stimuli still activated the visual cortex.
When stimuli were occasionally perceived, the visual cortex activations
were expanded and activations were also seen in the left parietal cortex.
Measures of inter-regional correlations involving frontal, parietal and
visual areas also increased when the subject was aware of a stimulus.
This study confirmed both bottom-up and top-down aspects of

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attentional processing, and was consistent with the theory that attention
may be critical for conscious awareness31,34.

Conclusions
Numerous recent imaging studies have begun to reveal the multifaceted
nature of attentional behaviour and its disturbances. More importantly,
long-held theories regarding attentional contributions to perceptual
processing, motor selection and the internal choice of particular thoughts
can now be studied directly. Event-related fMRI, event-related potential
studies and newer studies with magneto-encephalography will allow
improved spatial and temporal localization of the processes underlying this
important aspect of cognition.

Key points for clinical practice

• Attentional disturbances are ubiquitous in clinical practice. However, the

multimodal and protean nature of the disturbances may make them
difficult to recognize.

• A confusional state is arguably the most important attentional disorder to

diagnose, as its presence usually indicates an underlying acute medical
condition.

• Domain-specific attentional changes must be specifically sought, through

careful cognitive testing. Identifying this class of disturbances is important
when trying to distinguish disorders within a modality versus a partial
deficit of attention. For example, in examining patients with memory
complaints, it is critical to demonstrate whether the patient has a true
amnestic disturbance versus a disorder of attention, as the anatomy and
treatment of the associated disorders may be very different.

• Hemispatial neglect should be sought particularly in patients with right

hemisphere lesions. Because of the nature of neglect, i.e. a lack of
awareness for the neglected hemispace, patients will never directly
complain of this deficit although it is frequently noted by care-givers.

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Acknowledgement

The preparation of this manuscript was supported by NIA grant

AG00940.

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