Attention, Neural Basis of 1
Attention, Neural Basis of
Peter De Weerd, University of Arizona, Tucson, Arizona, USA
CONTENTS
Introduction
Paradigms of attention in experimental psychology
Attention, the ability to selectively process sensory
information, is generated by the modulation of sens-
ory processes by frontoparietal neural networks.
INTRODUCTION
The neural basis of attention resides in the ability of
structures in the brain representing the behavioral
relevance of stimuli to alter sensory processing, so
that relevant stimuli are processed effectively and
irrelevant ones are ignored. Attention, however, is
not a unitary cognitive ability. Attention can alter
the sensory processing of stimuli in all sensory
systems. In addition, there are different kinds of
attention which are related to specific behavioral
requirements in different cognitive tasks. Thus,
depending on the cognitive task one faces, and the
sensory systems involved, different neural net-
works in the brain will become active during atten-
tional operations.
Definitions of Attention
At the end of the nineteenth century the psycholo-
gist William James described attention as a ‘concen-
tration of consciousness’, with the purpose of
‘withdrawing from some things in order to deal
effectively with others’. An experimental demon-
stration of that idea was given by Hermann von
Helmholtz in 1894. He filled a large screen with
letters, which were spread too widely to be read
at once without moving the eyes. During a brief
illumination of the screen with a flash of light,
which made it impossible to use eye movements
to explore the screen, he measured the number of
letters that could be read. Only a few letters (up to
about five) could be read during each flash. Inter-
estingly, the letters that could be read were not
necessarily located at the center of gaze. Letters in
any region of the screen away from the center of
gaze could be read if the region of interest was
selected in advance. This experiment demonstrates
Introductory article
A cognitive neuroscience approach to attention
Conclusion
several aspects of attention which are still being
investigated today: the dissociation of directed at-
tention from eye gaze (‘covert’ attention), the se-
lective nature of attention, and the limited capacity
of attention.
The experiment of Helmholtz indicates that the
ability to selectively attend to information is an
answer to limitations in sensory information pro-
cessing. The ability to select information also
avoids our behavior being determined by the
strength of random stimuli in our environment.
Behavior otherwise would inevitably become un-
coordinated and chaotic. Hence, the ability to select
information is crucial, because it allows us to will-
fully give precedence to behaviorally relevant in-
formation, at the cost of irrelevant information. The
‘grabbing’ of attention by powerful stimuli is re-
ferred to as ‘bottom up’ (exogenous) attention, and
the intentional selection of behaviorally relevant
stimuli is referred to as ‘top down’ (endogenous)
attention.
There are different kinds of top-down attention.
Selective attention, the main topic discussed here,
is the ability to detect or discriminate relevant stim-
uli (targets) in the presence of competing irrelevant
stimuli (distracters). Selective attention is required
to find a familiar face in a crowd at a party. A
second attentive process is vigilance: the ability to
orient attention and respond to randomly occur-
ring, relevant events in the environment over an
extended period. A guard who is keeping an eye on
the entrance of a building, monitoring for suspi-
cious activity throughout the night, is carrying out
a vigilance task. In addition, it has been proposed
that there are attentional functions that maintain
‘executive control’ over goal-directed behavior
and thought processes. Executive control functions
are especially important when stimuli contain con-
flicting information. The onset of reading of the
word ‘green’ will be faster when the word is
printed in green than when it is printed in red, a
phenomenon known as the Stroop effect. Applying
2 Attention, Neural Basis of
a level of analysis to a stimulus that contains con-
flicting information, appropriate for the required
behavioral response, is a function of executive pro-
cesses.
Circuits of Selective Attention in the
Visual System
The ability to attend to a stimulus is best under-
stood as an emergent property of the functional
architecture of sensory systems. This concept will
be explored within the context of the visual system
(Figure 1).
The primary visual area (V1) receives retinal in-
formation through the lateral geniculate nucleus, a
l
ieta Fro
Par
ce
ital
cip
MT ip ar
Oc
lu
V1
V4
la
TEO
io
TE sts
Tem
por
al
Figure 1. A neural network for attention in the primate
brain. Shown is a lateral view of the brain of a rhesus
macaque, with the back of the brain towards the left.
Dotted arrows correspond to the boundaries between
occipital, temporal, parietal, and frontal lobes. White
labels indicate visual areas, white arrows indicate ana-
tomical pathways. Visual area V1 gives rise to a ventrally
directed pathway which includes V2 (buried in the
lunate sulcus), V4, and areas in the temporal lobe (TEO
and TE). It also gives rise to a dorsally directed pathway
which includes V3 (buried in the lunate sulcus), MT
(buried inside the superior temporal sulcus), and areas
in the parietal lobe. There is cross-talk between areas
belonging to these two visual processing pathways (e.g.
double arrow between V4 and MT). Roughly 40 visual
areas have been described, and only a few are indicated
here. Projections from parietal and temporal lobes to-
wards the prefrontal region of the frontal lobe retain a
significant degree of segregation. Forward projections
(white arrows) from one to the next area are always
returned by backward projections (not shown). ar, arcu-
ate sulcus; ce, central sulcus; io, inferior occipital sulcus;
ip, intraparietal sulcus; la, lateral sulcus; lu, lunate
sulcus; p, principal sulcus; sts, superior temporal sulcus.
relay station in the thalamus. Following lesion and
anatomical studies in the monkey, Ungerleider and
Mishkin proposed in 1982 that forward projections
from V1 give rise to two visual processing streams.
One is directed ventrally to the temporal lobe, and
is involved in the analysis of objects (ventral path-
way, or ‘what?’ pathway). The other one is directed
dorsally to the parietal lobe, and is involved in the
analysis of locations of objects relative to each other
and relative to the observer (dorsal pathway, or
‘where?’ pathway). A relative segregation between
ventral and dorsal streams is maintained in their
projections to the prefrontal cortex in the frontal
lobe (Figure 1). Prefrontal cortex is involved in the
maintenance and manipulation of information in
working memory, response selection and a variety
of executive processes.
Each of the two processing streams is composed
of a number of areas, which are hierarchically or-
ganized. Lower-order areas (closer to V1) each con-
nta
l
tain an orderly retinotopic map of the environment,
and are composed of neurons with small receptive
fields (RFs), which process simple aspects of the
stimulus, such as the orientation of edges. Higher-
p order areas do not show retinotopy, their neurons
have large RFs, and they process complex aspects
of the stimulus, such as its shape. Owing to this
hierarchical organization, lesions at low levels
result in severe sensory deficits, while lesions at
intermediate and higher levels leave elementary
sensory processes intact and interfere in more
subtle ways with visual processing. Lesions at
higher levels of the ventral stream induce a dis-
order in visual object recognition that is referred
to as ‘agnosia’. Parietal damage causes severe
spatial deficits. Because these lesion effects reflect
at least in part attention deficits, they are discussed
in the following section.
When we look at an object it is automatically
perceived as a whole, with a particular location,
color, shape, and orientation. Because different
aspects of a stimulus are processed in a distributed
manner in different cortical regions, this raises the
question of how the different features of a stimulus
are combined in order to generate a holistic percep-
tion. This question is referred to as the ‘binding’
problem, and the quest for a solution to that prob-
lem is intimately related to the quest to understand
mechanisms of selective attention. A fundamental
insight that will help to resolve both issues is the
fact that the separation of the different processing
streams is only relative: at various levels in the
system, there are anatomical connections between
pathways that permit cross-talk. Furthermore,
feedforward projections are returned by feedback
 Attention, Neural Basis of 3

projections. Hence, neural activity in a given area
can be modulated by activity in other areas or
structures to which it is connected. These modula-
tory influences are a functional property that re-
flects the structural layout of the system, which is
crucial to understanding attention and other cogni-
tive abilities.
PARADIGMS OF ATTENTION IN
EXPERIMENTAL PSYCHOLOGY
Before explaining how modulation of activity
creates the cognitive ability of attention, it is im-
portant to review the different paradigms psych-
ologists have used to investigate attention. These
paradigms have led to a precise characterization of
attentional behavior, and have become the corner-
stone of most experiments on attention in the broad
field of cognitive neuroscience (Figure 2).
Spatial Cueing
The spatial cueing paradigm was developed by
Posner and colleagues to measure the effects of
directed attention (Figure 2(a)). Participants are in-
structed to keep their eyes on a central fixation
cross presented on a computer monitor, and to
covertly attend to a location in the left or right
half of the screen, indicated by an arrow close to
the fixation cross (the cue). The cue is followed in
time by a target (e.g., a small square) briefly pre-
sented away from fixation. The target can be pre-
sented in the cued location (valid cue), or in a
minority of cases in a location in the other half of
the screen (invalid cue). Participants have to make
a button response as soon as they detect the target.
On trials in which the target is preceded by a valid
cue, response times are shorter (about 250 ms) than
on trials in which the target is preceded by an
invalid cue (about 300 ms). These results support
the idea of a ‘focus of attention’. After a valid cue,
participants move their focus of attention to the
expected location in anticipation of target presenta-
tion, and target detection benefits from the pres-
ence of attention at the cued location. After an
invalid cue, attention moves to the invalid location,
and the target is presented outside the focus of
attention. The associated cost, an increased reaction
time, may be due to the reorienting of the atten-
tional focus to the target.
The reorienting of attention to a location in re-
sponse to a cue is controlled by the participant, and

Cue Target Cue Target

Valid

+ + + +
Invalid

+ + + +

(a) (b)

Search Conjunction search Pop-out

+ + +

(c) (d)

Figure 2. Paradigms in attention research. (a, b) Spatial cueing paradigms. (a) The top two panels show a symbolic cue
(arrow) close to a fixation spot (cross) on a computer monitor (gray rectangle) which validly predicts the location of the
target (square), presented briefly after offset of the cue. The bottom two panels show target presentation after an
invalid cue. When cues are valid on most trials, attention is shifted to the cued location in anticipation of target
presentation, and this speeds up responses to the target. (b) Valid (top row) and invalid (bottom row) cueing of
attention by a physical stimulus. Even if half of the cues are invalid (rendering the cue unpredictive of target location),
the cue has specific attention effects on targets presented in the cued location. (c, d) Search paradigms. (c) Searching for
a target among distracters is slow and time-consuming when the target is similar to the distracters (left panel), or if the
target is defined by a conjunction of features on more than a single stimulus dimension (right panel). (d) Search is fast
and seemingly effortless (pop-out) when the target differs from distracters on a single dimension, and when the
difference is large.
4 Attention, Neural Basis of
this type of cueing is referred to as endogenous
cueing (‘top down’ attention). On the other hand,
attention is often automatically oriented to new
stimuli. When a student enters class late, it is
almost inevitable that everybody turns attention
to the latecomer. This exogenous cueing effect
(‘bottom up’ attention) has been investigated in a
variation of the spatial cueing paradigm (Figure
2(b)). In this variation, small cues are presented in
random locations on the computer screen while the
participant fixates a small cross in the middle of
the screen. The cue location is unpredictive for the
location of the subsequently presented target
stimulus. Nevertheless, the cue affects processing
of the target if the target happens to be presented in
the location of the preceding cue. This effect
depends upon the time interval between the cue
and target presentation. A target that follows a cue
within 250 ms will be responded to with a de-
creased reaction time, while a target lagging behind
the cue by more than about 300 ms will be re-
sponded to with an increased reaction time, com-
pared with target presentations not preceded by
a cue.
Thus, the mere presentation of a stimulus in a
given location can attract attention to that location
for a limited time. After that time, attention is dis-
engaged from the stimulus location, and a re-
orientation of attention to the same location is
suppressed. This effect is referred to as ‘inhibition
of return’. It is important that attention can be
attracted easily to unexpected but significant
events in the environment, but it is equally import-
ant that attention then can be freed from that event
to make it available for new, potentially important
stimuli. If there were no easy disengagement of
attention, attention could get stuck to a stimulus,
and new incoming stimuli might go unnoticed. The
brief period during which attention is engaged in
the processing of a particular stimulus, and during
which limited or no attention is available for the
processing of new stimuli, is often referred to as the
‘attentional blink’.
Search Paradigms
The metaphor of a ‘focus of attention’ has also been
used to explain performance in visual search tasks,
a second major paradigm to study attention. In a
search task, participants are presented with dis-
plays filled with distracter stimuli, which may or
may not contain a specific target. Participants are
instructed to respond with a button press as soon as
they find the target, or to press another button to
indicate its absence. Performance is assessed by
measuring the time required to find the target as a
function of the number of distracters in the display.
The resulting plot is referred to as a ‘search curve’.
A typical experiment suggesting serial search
would show an increase in search time by about
30 ms per item.
Search performance becomes dependent on the
number of distracters in the display when the
target is difficult to distinguish from the distracters
(Figure 2(c)). An example of such a search display
is one in which the target is a line element slightly
tilted away from vertical, surrounded by vertical
distracters. Another example is one in which the
target is defined by a conjunction of features: the
target could be a vertical red line, surrounded by
horizontal red, vertical green, and horizontal green
lines. The latter task (conjunction search) is difficult
because different properties of the objects have to
be analyzed and combined before it can be deter-
mined whether the object matches the target being
searched. The time-consuming nature of these
types of search suggests that a focus of attention is
continually relocated during search to scan items in
the display serially, and in the case of conjunction
search also suggests that focal attention plays a role
in solving the binding problem.
While search displays have been used to demon-
strate serial search, ‘pop-out’ displays have been
used to demonstrate the existence of ‘parallel
search’. In pop-out displays, the target (e.g. a hori-
zontal line) differs strongly from the surrounding
distracters (e.g. vertical lines) and the time required
to detect the target appears independent from the
number of distracters (Figure 2(d)). The identifica-
tion of a target in pop-out displays is often con-
sidered to occur ‘preattentively’, or to result from a
parallel attentional operation.
A COGNITIVE NEUROSCIENCE
APPROACH TO ATTENTION
While the experimental paradigms introduced
above characterize important aspects of attentional
behavior, they do not address the important ques-
tion of how modulations of sensory processes pro-
duce attentive behavior. Recent neurophysiological
findings have brought us closer to an answer.
Findings in the Temporal Lobe
In a series of ground-breaking recording studies,
Desimone and colleagues flashed pairs of stim-
uli inside the RF of single neurons of temporal
lobe areas V2, V4, and TE in monkeys trained
to identify one of the stimuli and ignore the other.

The neurons’ responses were determined by the
attended stimulus (target), while the influence from
unattended stimuli inside the RF upon the neurons’
responses was greatly attenuated (Figure 3). In the
period during which the monkeys were waiting for
Sensory
Sensory interaction
+ F+ +
Cell 1
S1
S2
+ + +
Cell 2
(a)
Cell 1
Response
Cell 2
Sensory Sensory
(b) interaction
Figure 3. Elimination of sensory interaction (competi-
tion) by attention. (a) Different configurations of stimuli
and covert attention inside the receptive fields (RF) of
two cells (cell 1 and 2). The monkey fixates a cross (F)
while covertly attending (arrow) or ignoring stimuli
away from fixation placed in the RF of cells 1 or 2,
whose activity is recorded. The RFs of cell 1 and 2 are
shown as the light and dark gray squares, respectively.
Stimuli are symbolized by small white (S1) or black (S2)
squares. (b) Pattern of responses illustrating competition
and effects of attention. For cell 1, stimulus S1 is more
effective than S2 (response to S2 alone not shown). Be-
cause stimuli compete for control over the firing rate of
the cell, the addition of the less effective stimulus (S2) to
the more effective stimulus (S1) drives the response
down (sensory interaction). That suppressive effect is
eliminated when attention is covertly directed to S1
(arrow in A). Cell 1 now responds as if only S1 were
present in its RF, despite the presence of S2 in the RF.
Thus, attention eliminates competitive effects caused by
behaviorally irrelevant stimuli. In cell 2, stimulus S2 is
more effective than S1, and adding S2 to S1 in the RF
increases the response compared with the response
obtained with S1 alone. Attention to the less effective
stimulus S1 will screen out the effect of the more effective
stimulus S2, resulting in a decreased response. Thus,
whether attention will increase or decrease the activity
of a given neuron depends upon the selectivity of the
neuron for the stimuli in its RF.
Attention, Neural Basis of 5
the presentation of each stimulus pair, increased
baseline activity was observed compared with the
spontaneous firing rate. Depending on the task,
increased baseline activity might represent the in-
struction to the monkey to attend in a particular
location, or to expect a stimulus of a given identity,
and it might facilitate processing of the target
stimulus.
These data provide a neural foundation for the
Attention
behavioral finding that target stimuli are processed
more efficiently than nonattended distracters. In
1995, Duncan and Desimone proposed a ‘biased
competition’ model of attention to account for
these findings. In this model, objects presented
simultaneously in the visual field compete with
each other for control over the firing rate of cells
within whose RF they are presented. The competi-
tion is decided in favor of stimuli that receive a
biasing signal which can be generated ‘bottom up’
(by a salient stimulus) or ‘top down’ (by an instruc-
tion to identify a particular target among distrac-
ters, or to monitor objects in a particular location).
The increased spontaneous activity reported
during attention tasks may be a correlate of such a
biasing signal. Thus, the process of attention is
viewed as a biased competition between popula-
Attention tions of cells representing different objects or loca-
tions (Figure 4).
In agreement with the idea that temporal lobe
areas are important for attention, cortical lesions
of monkey areas V4 and TEO in the temporal lobe
cause an inability to discriminate properties of
target objects surrounded by distracters, especially
when the target is weak (e.g. smaller or dimmer
than the distracters). Without distracters, deficits in
discriminating the target are absent or limited.
These lesion deficits in the monkey resemble
agnosia, a neurological syndrome found after
occipitotemporal damage in humans. Humans
with agnosia have trouble recognizing visually pre-
sented objects embedded in a complex scene, or
visually presented complex objects consisting of
multiple parts; yet simple stimuli presented by
themselves can be discriminated with great accur-
acy. These general characteristics of agnosia sug-
gest that attention deficits contribute to the
syndrome. In the terminology of Duncan and Desi-
mone, agnosia may reflect, at least in part, a failure
of biased competition, because of damage to the
substrate in which the competition takes place.
Findings in the Parietal Lobe
The description of attention as a process of biased
competition leads to the question: where does the
6 Attention, Neural Basis of
Frontoparietal Temporal lobe
network S1 > S2
C
Bias
S1 S2
(Target) (Distracter)
Competition
Figure 4. Competition in the temporal lobe is biased by
signals generated in a frontoparietal network. Cell C
receives input from a population of cells coding S1, and
another population of cells coding S2. Each population
provides a mixture of excitatory and inhibitory inputs to
cell C. The balance of excitatory and inhibitory inputs
to C provided by each population determines the size of
C’s response to S1 and S2 presented alone in C’s RF. The
response to S1 and S2 presented together in C’s RF is
determined by the total balance of all excitatory and
inhibitory inputs from both populations taken together
(competition). When one of these two stimuli (e.g. S1) is
made behaviorally relevant (a target), and is therefore
attended to, a biasing signal renders inputs from cells
coding the target more efficient compared with the dis-
tracter. As a result, C’s activity will reflect the balance of
excitatory and inhibitory inputs provided by S1 alone,
rather than the balance of excitatory and inhibitory
inputs provided together by the two stimuli in the RF,
and S1 wins a competition with S2 for control over the
firing rate of cell C (S1 > S2). ‘Bottom up’ stimulus-driven
bias can have effects similar to ‘top down’ bias generated
in a frontoparietal network. This formalization of biased
competition theory was first proposed by Reynolds and
Desimone in 1999.
bias come from? To answer this question, we turn
briefly to a parallel line of work on attention in the
parietal cortex. Mountcastle in 1976 and Wurtz in
1982 showed that neurons in parietal cortex of the
monkey were more active when the stimulus in
their RFs was behaviorally relevant (attended)
than when it was not. Several imaging studies in
humans have now confirmed that covertly
orienting one’s attention to a stimulus or location
leads to enhanced activity in parietal cortex. Fur-
ther neurophysiological work in monkeys suggests
that the effects of behavioral relevance on parietal
activity can depend upon the type of action
planned by the monkey towards the target (e.g. an
arm versus an eye movement).
Lesions in the parietal cortex induce a complex
set of deficits in the representation of space and
action. Unilateral parietal damage leads to neglect
of the contralateral side of the body, and of stimuli
in contralateral extrapersonal space. Neurologists
often use the line bisection test to assess neglect:
patients with neglect will bisect a horizontal line
towards one end of the line, as the other part of the
line will become neglected when they look at it.
When a strong stimulus is presented on the neg-
lected side, patients can recognize the stimulus
perfectly, but when two such stimuli are presented,
one in the neglected hemifield and one in the other
hemifield, then the stimulus in the neglected hemi-
field will remain unnoticed, a phenomenon re-
ferred to as extinction. Extinction and neglect do
not always co-occur after parietal damage, indicat-
ing that both phenomena may constitute dissoci-
able syndromes after different types of parietal
damage.
Using a spatial cueing test, Posner and col-
leagues found that patients could shift attention to
the neglected hemifield when cued correctly, and
engage in attentional operations in that hemifield,
but had trouble redirecting attention from the ipsi-
lateral to the contralateral (neglected) hemifield.
It was therefore postulated that parietal lesions
induce a failure of a disengagement operation.
Other experiments suggest that the pulvinar nu-
cleus, a thalamic nucleus that provides weak but
direct projections to the parietal lobe, plays a part in
the shifting and engaging of attention.
Bilateral parietal damage leads to a constellation
of symptoms, including optic ataxia (deficit in visu-
ally guided reaching), paralysis of gaze, inattention
to peripheral stimuli, and sustained hyperattention
to single objects or locations (Balint syndrome).
Patients with this syndrome do not know where
they are, and have no idea of spatial relations be-
tween objects. However, once attention is directed
to an object, they can identify it perfectly. In pop-
out displays, their report of the presence of
the target is not influenced by the number of dis-
tracters, as in non-afflicted individuals, but they
cannot tell where the target is once it has been
reported. In conjunction search tasks, people with
Balint syndrome require extraordinary amounts
of time to find the target (about 1 s per item).
In addition, they often make ‘illusory conjunctions’
(e.g. joining the orientation of a given item with
the color of a neighboring item). These illusory
conjunctions can also be demonstrated in non-af-
flicted individuals when the search display is pre-
sented very briefly (and followed by a mask).
In both situations, there may be not enough
attention available to focus accurately on one of
the items.

A compelling account of the function of focused
attention was given in 1980 by Treisman and
Gelade in a model referred to as the ‘feature inte-
gration’ theory. According to this theory, different
elementary features in the image (e.g. color, orien-
tation, motion) are analyzed in separate feature
maps – an idea at least in part supported by physio-
logical evidence – and the read-out of activity
within single maps occurs fast and in parallel.
This would explain simple pop-out phenomena.
However, when targets have to be identified that
are defined by a combination of two or more fea-
tures, the activity in different feature maps must be
combined, which is a lengthy operation requiring
focused attention. Hence, the time-consuming
nature of conjunction search may reflect a mixture
of factors, including the disengagement, orienting,
and engagement of attention, as well as the time
required to conjoin features. Imaging data support
the idea that parietal cortex is involved in the
directing of attention to targets, in the shifting of
attention in response to both endogenous and
exogenous cues, and in conjunction search, but
not in feature search or pop-out. Since conjunction
search implies shifts of attention and conjoining of
features, parietal activity could indicate either or
both.
Findings in the Frontal Lobe
An additional line of research that is related to the
question where the biasing signal comes from was
initiated by Fuster and Alexander in 1971. They
found that neurons recorded around the principal
sulcus in prefrontal cortex showed enhanced activ-
ity during delayed-response tasks, in which the
monkey was required to remember a previously
cued location that would become the target of a
directed action after a delay of a few seconds.
Later research has demonstrated that neurons in
prefrontal cortex can be activated during tasks
that require working memory for both location
and object identity.
Many attentional operations require working
memory. For example, while a participant looks
for a target in a search array, incoming sensory
information is matched against a template of the
target that is kept on-line in working memory.
Many physiological and imaging studies have con-
firmed that working memory and attention both
rely heavily on prefrontal cortex. Limitations on
attentional capacity, witnessed by the impossibility
of identifying more than a few targets at once, are
reminiscent of limitations to hold more than a few
stimuli in working memory.
Attention, Neural Basis of 7
Modulation of Competition in the
Occipitotemporal Lobe by a
Frontoparietal Biasing Signal
Competition in the occipitotemporal lobe
The term ‘competition’ refers to the sensory inter-
actions that take place automatically when two
stimuli S1 and S2 are placed inside a cell’s RF. If
this cell (C) receives inputs from a pool of neurons
that codes S1, and another pool that codes S2, then
the response of the cell will be determined by a
mixture of the influences of S1 and S2. Attention
biases the efficacy of one set of inputs relative to the
other set, such that the activity of the cell will reflect
preferentially the attended stimulus (Figure 4).
Cells encoding a target could enhance their influ-
ence on the activity of cell C by slightly depolarizing
their cell membranes. This enhances the probability
that these cells will generate action potentials when-
ever the target is presented in their RFs. Alterna-
tively, the pool of neurons that represents the target
may synchronize its spontaneous and stimulus-
driven activity. This enhances the probability of
coinciding spikes in the pool of neurons coding
the target. Because of the summation properties of
neurons, rate enhancements and synchronization
could both increase the control of the pool of
neurons coding the target over the activity of the
postsynaptic cell C. The pool of neurons coding the
target is thought to include neurons coding various
aspects of the stimulus, distributed in temporal lobe
areas and other parts of the brain. The synchroniza-
tion of the activity of neurons coding different
properties of an object could be a mechanism for
the binding of those object properties, a proposal
championed by Singer and colleagues.
A frontoparietal source for the biasing
signal
Where does the biasing signal come from? Alterna-
tively, what makes a stimulus behaviorally rele-
vant? A stimulus is behaviorally relevant when
there is a requirement to make a saccade to it, to
reach and grab it, and to keep it in working
memory. It is precisely under those conditions
that specific regions in parietal and frontal cortex
become active. Thus, to the extent that require-
ments in an attention task engage frontoparietal
regions, activity in those regions could bias activity
in ventral stream areas through connections be-
tween retinotopically matched regions in ventral
and frontoparietal areas.
Evidence suggests that parietal activation during
endogenous directing, shifting, and maintenance of
8 Attention, Neural Basis of
spatial attention may be controlled by the pre-
frontal cortex, while parietal activity related to ex-
ogenous cueing may be controlled by subcortical
thalamic input to the parietal cortex. From the per-
spective of a theory of binding, the bias would be
considered part of the representation of the
attended object. Indeed, a complete object repre-
sentation would consist of a synchronized ensem-
ble of neurons distributed in the frontal, parietal,
and temporal lobes, representing the object’s iden-
tity and location, and possible actions towards it.
Similarly, the appropriate binding of features (e.g.
color and orientation) in conjunction stimuli may
be related to the synchronization of activity in
neurons coding the color and orientation of those
stimuli by a common biasing signal. Thus, selective
attention, synchronization, and binding may be
intimately related.
Implications for the Serial versus
Parallel Search Debate
Attentional bias signals affect sensory processing at
the earliest levels of sensory systems. This settles a
long debate between ‘early selection’ proposals (pi-
oneered by Broadbent in 1958) and other proposals
advocating ‘late selection’. Not unlike feature inte-
gration theory, early selection theory predicts that
nonattended stimuli are incompletely processed,
and that full processing of all aspects of a target
stimulus requires focusing of attention, which im-
plies that search must have a serial component.
However, strong arguments have been made
against the existence of serial search. It has been
argued that target search can be mediated by bias-
ing sensory processing towards the target every-
where in the visual field in parallel. Increases in
search time as a function of increases in the number
of distracters would merely reflect a thinner spread
of a limited amount of attention over all items in the
display.
Evidence is mounting, however, that perform-
ance in search tasks depends on a mixture of serial
and parallel operations. For instance, it has been
reported that detection of a ‘pop-out’ target is
impaired when an attention-demanding task is
carried out at fixation during stimulus presenta-
tion. This does not exclude a parallel component
in the detection of pop-out, but it does argue
against the idea that pop-out is entirely preatten-
tive. Thus, some degree of directed attention may
have a role, even in pop-out. Furthermore, per-
formance in spatial cueing tasks, designed to
reveal serial relocations of a focus of attention, is
influenced by a segmentation of visual space into
surfaces and objects, which takes place in parallel
across the field. Specifically, experiments by Driver
and colleagues show that reorienting attention to a
target location, after an invalid positional cue,
occurs faster if the invalid cue and target are both
presented within the same shape, compared with
when the target and cue are presented in different
shapes. Although those experiments are set up to
equate the distance over which attention has to be
reoriented, reorientation takes significantly longer
between than within objects. Hence, spatial atten-
tion does not operate within unsegmented space.
Findings in patients with neglect due to unilat-
eral parietal damage support this hypothesis. Neg-
lect is often described as a purely spatial imbalance
in the distribution of attentional operations be-
tween hemifields. However, experiments in a pa-
tient with right parietal damage showed that
details on the right side of an object placed in the
left (neglected) hemifield are perceived more accur-
ately than details on the left side of an object placed
in the right (normal) hemifield. The idea that par-
ietal cortex manipulates the distribution of atten-
tion in an object-driven way, rather than a purely
spatial way, is compatible with the role of parietal
cortex in representing potential actions towards
target objects.
In sum, processing of a visual scene may begin
with a fast quasiautomatic segmentation based on
parallel processes that require little attention. Sub-
sequently, attention may be distributed across this
roughly segmented scene, in ways that reflect be-
havioral demands, and which may not be exclu-
sively parallel or serial. When relevant objects are
expected in a single location, attentional resources
will be focused on that location. When switches of
attention between locations are required, this serial
redistribution of attention will be influenced by the
preceding segmentation of space. Furthermore,
when a specific target object is searched for without
knowledge of its location, a ‘top down’ parallel bias
may contribute to the identification of potential
targets, but does not exclude the possibility that
potential targets are serially inspected. Thus,
while items in a search display may not be scanned
individually, parallel processes (including auto-
matic ‘bottom up’ segmentation and parallel ‘top
down’ biases) may lead to the determination of
likely targets, which may then be inspected serially.
The exact distribution of attention in response to
task demands is controlled by executive processes.
These and similar ideas have led to various mixed
parallel–serial models of attention.

CONCLUSION
The combination of behavioral paradigms de-
veloped by psychologists and new methodological
approaches developed in the field of cognitive
neuroscience has greatly enhanced our under-
standing of attention and of the neural processes
that underlie it. Attention can be best understood as
a modulation of sensory processes driven by
regions in the brain that represent the behavioral
relevance of stimuli. These modulations ensure that
behaviorally relevant objects (or locations) in the
environment are preferentially processed at the
cost of irrelevant ones.
Further Reading
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