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Neural coding of behavioral relevance in parietal cortex
John A Assad
Flexible control of behavior requires the selective processing of
task-relevant sensory information and the appropriate linkage of
sensory input to action. A great deal of evidence suggests a
central role for the parietal cortex in these functions. Recent
results from neurophysiological studies in non-human primates
and neuroimaging experiments in humans illuminate the
importance of parietal cortex for attention, and suggest how
parietal neurons might allow the dynamic representation of
behaviorally relevant information.
Addresses
Department of Neurobiology, Harvard Medical School, 220 Longwood
Avenue, Boston, MA 02115, USA
e-mail: [email protected]
Current Opinion in Neurobiology 2003, 13:194–197
This review comes from a themed issue on
Cognitive neuroscience
Edited by Brian Wandell and Anthony Movshon
0959-4388/03/$ – see front matter
ß 2003 Elsevier Science Ltd. All rights reserved.
DOI 10.1016/S0959-4388(03)00045-X
Abbreviations
fMRI functional magnetic resonance imaging
IPS
intraparietal sulcus
LIP
lateral intraparietal area
MST medial superior temporal area
MT
middle temporal area
RF
receptive field
VIP
ventral intraparietal area
Introduction
It could be argued that a general function of the cerebral
cortex is to facilitate the association of sensory input with
particular behaviors. This implies that relevant information is first selectively extracted from the sensory scene,
and then linked to actions in a manner appropriate to the
demands of the task at hand. For example, under different circumstances we can selectively attend to specific
attributes of a visual scene — say red objects — yet
respond to them differently, such as by reaching to
acquire a ripe apple in a tree or by extending a foot to
apply the brakes in response to a stoplight.
Decades of neuropsychological research point to a role of
the parietal cortex in these processes, particularly in
visually guided behaviors. Patients with parietal lesions
are not blind per se, but they have deficits in their
representation of and their attention to the spatial attributes of their visual surroundings, and in their use of
Current Opinion in Neurobiology 2003, 13:194–197
visual information to guide movements of the body [1–3].
Physiological studies in non-human primates and neuroimaging studies in human subjects [4] have confirmed that
individual parietal neurons and cortical areas are activated
during spatial, attentional, and visuomotor behaviors.
Mountcastle and co-workers [5] were the first to identify
neurons throughout the monkey parietal lobe that were
activated by a host of visually guided behaviors of the
eyes or hands. Later studies identified parietal activity
that was related to attention to or salience of particular
locations [6–8], and the intention to make eye or hand
movements to those locations [9,10]. In addition, many
neurons in parietal areas in the monkey are sensitive to
spatial attributes of visual stimuli, such as the direction of
motion [11–13], and are likely to contribute to the initiation or maintenance of behaviors made to acquire moving
targets, such as pursuit eye movements [14,15].
The purpose of this review is to discuss recent findings
that expand our understanding of the role of parietal
cortex in encoding behavioral relevance. New experiments have addressed how attention modulates parietal
responses, how physiological modulation by attention
relates to behavioral enhancement, and how non-spatial
information can be dynamically represented depending
on the demands of the task.
Parietal mechanisms of attention revealed by
single-unit studies
Some of the most detailed experiments on the neuronal
mechanisms of attention in the parietal pathway have
been carried out in the middle temporal area (MT) and
the medial superior temporal area (MST) of the monkey.
MT and MST contain a preponderance of neurons that
are selective for the direction of moving stimuli within
their receptive fields (RF). Treue and Maunsell [16,17]
were the first to show that the direction-selective
responses of many MT and MST neurons were modulated by attention. Neuronal responses to stimuli moving
within the RF are generally larger when the animal
attends to the location of the RF. Attentional effects
are not solely restricted to attended locations, however
[18,19]. For example, if an animal attends to a stimulus
moving in a particular direction, neuronal responses to a
second stimulus can be enhanced if that stimulus moves
in the same direction as the attended stimulus [18].
Attention also generally ‘scales’ neuronal responses by
a uniform factor regardless of whether the visual stimulus
moves in a preferred or non-preferred direction for a given
neuron [18]. These results suggest that attention exerts a
multiplicative modulation of neuronal responses — an
effect that is also common to neurons in the temporal
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Parietal cortex and behavioral relevance Assad 195
visual pathways [20,21]. To test this idea further,
Martinez-Trujillo and Treue [22] examined attentional
effects in MT as a function of the luminance contrast of a
moving stimulus relative to a dark background. Increasing
stimulus contrast also tends to increase neuronal responses
in a scalar, multiplicative fashion [23]. Attention caused a
shift in the sigmoidal contrast–response function of the
neurons, implying that the neurons were most sensitive
to both attention and changing contrast at intermediate
contrast levels [22]. Thus, the mechanisms of attention
may be similar or identical to the mechanisms that determine the strength of visual stimuli.
Comparing neuronal and behavioral
effects of attention
Spatial attention confers a variety of behavioral advantages, such as decreased reaction time in visual detection
tasks [24–26]. A challenging issue has been to understand
how attentional modulation of neural activity could give
rise to the behavioral effects of attention. Cook and
Maunsell [27] have directly examined this question
by determining the attentional modulation of neuronal
responses in the MT and the ventral intraparietal area
(VIP), while simultaneously measuring the effects of
spatial attention on performance in a motion-detection
task. Monkeys had to detect a change in motion coherence in one of two spatially distinct patches of moving
dots, when they were directed in advance to attend to the
appropriate or inappropriate patch. Withdrawing attention
from the stimulus decreased the animals’ ability to detect
the change in motion coherence, and also reduced neuronal responses in MT and VIP. Interestingly, the changes
in neuronal responses in MT were generally too small to
account for the behavioral changes, whereas the changes
in VIP responses were generally stronger than expected to
explain the behavioral effect. These results suggest that
comparing the neuronal and behavioral effects of attention may be a reasonable way to gauge the importance of
parietal areas for particular visual behaviors.
Other studies have examined the link between neuronal
and behavioral modulation less directly. For example, it
has been known for a long time that a difficult task could
increase the responses of neurons, presumably by
demanding more attention to relevant stimuli [28]. Other
experiments suggest that attention can increase or
decrease responses to task-relevant stimuli depending
on the way that attention is allocated. For example,
Constantinidis and Steinmetz [29,30] recorded from parietal area 7a during a task in which monkeys had to
localize an odd-colored stimulus spot amidst an array of
spots extending inside and outside of the RF. The presence of a non-salient spot in the RF elicited little
response. If the salient spot was within the RF, the
response of neurons was much stronger and comparable
to that when a single spot was presented alone at the same
location [29]. In contrast, if the animals were cued in
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advance to attend to the same location in the RF, later
presentations at that location produced smaller responses
[30]. This suggests that parietal areas similar to 7a may be
involved in the re-direction of attention, for example by
responding to salient stimuli, but less involved in the
maintenance of attention to particular locations. Similar
results have also been reported for the lateral intraparietal
area (LIP) [31,32].
Neuroimaging studies and parietal
mechanisms of attention
Recent neuroimaging studies conducted on human subjects continue to provide evidence of the parietal lobe’s
role in encoding behavioral relevance [4,33]. Culham et al.
[34] used functional magnetic resonance imaging (fMRI)
to assess the role of different brain regions in attentional
tracking. Subjects were instructed to maintain gaze at a
fixed location while covertly tracking the position of one
or more spots moving randomly within a patch of visual
space. The number of tracked stimuli was increased to
examine whether the activity of a particular brain region
was affected by the attentional ‘load’ or rather reflected
the immediate demands of the task, such as planning eye
movements to one of the moving targets. Within the
parietal lobe, areas in the intraparietal sulcus (IPS) and
the inferior parietal lobule showed load-related changes
in metabolic activity, suggesting their involvement in the
specific attentional demands of the task. MT/MST
showed little effect of attentional load, consistent with
previous findings [35] that MT/MST is not specifically
activated by attentional tracking. Interestingly, these
results agree with those of a recent neuropsychological
study [36]. This study suggests that patients with parietal
lesions that spare the MT/MST complex are severely
impaired in attentional tracking and other high-level
motion tasks, but are not deficient in low-level motion
tasks [36].
fMRI has also been used to address the exact role of the
parietal areas in attention, in particular whether parietal
cortex is involved in maintaining attention to specific
spatial locations or rather in providing a transient signal
when attention is shifted from one location to another.
Yantis et al. [37] directed subjects to detect a stimulus in
one of two rapid serial visual displays presented simultaneously in opposite visual hemifields. Attention was
rapidly shifted between the opposite hemifields in
response to particular stimuli appearing on the attended
side. Many extrastriate visual areas showed sustained
increases in activity for attention to the contralateral
visual field, whereas areas in the right superior and
inferior parietal lobules showed transient activation
whenever attention was reallocated. Other areas in the
left IPS showed the sustained pattern of activity for
attention to the contralateral field. These results suggest
that dynamic and static aspects of spatial attention could
be subserved by distinct parietal areas.
Current Opinion in Neurobiology 2003, 13:194–197
196 Cognitive Neuroscience
Several other recent fMRI experiments suggest a specialization of the parietal cortex in dynamic attention.
Shulman et al. [38] compared neural activity in the
parietal cortex when subjects performed either a color
or a motion match-to-sample task that were visually
identical. The left parietal cortex was selectively activated when subjects performed the motion task and
when the subjects alternated rapidly between the two
tasks, which suggests that left parietal areas might also
contribute to specifying the switching of task demands.
Task-switching signals may be localized to the lateral
portion of the IPS [39]. Attentional processes in the IPS
appear to extend to other stimulus modalities beyond
vision. For example, a positron-emission tomography
(PET) study found signals in the IPS when subjects
attended to either contralateral visual stimuli or somatosensory stimuli [40].
Dynamic representation of non-spatial
features in the parietal cortex
As described above, attentional effects are not just
restricted to the location of visual stimuli. Saenz et al.
[41] asked subjects to attend to a patch of moving dots in
one hemifield, while simultaneously viewing a second
task-irrelevant patch of moving dots in the opposite
hemifield. fMRI signals in response to the irrelevant
stimulus were larger when their movement was in the
same direction as the attended stimulus. Among extrastriate visual areas, feature-based attention was particularly strong in MT [41], a similar result to that of
experiments described above in monkey MT [18].
If attention to a non-spatial attribute (such as direction)
can ‘spread’ to an ignored stimulus, what would happen if
instead the non-spatial feature were behaviorally relevant? In particular, would the parietal cortex represent a
non-spatial feature if it were relevant for a behavior that is
known to engage parietal areas, such as an eye movement? Toth and Assad [42] examined this issue by
training monkeys to use a colored visual cue to direct a
saccadic eye movement. Neuronal responses were
recorded in the LIP. On alternate blocks of trials, the
animals used either the cue’s color or location (irrespective
of color) to direct a saccade towards or away from the
response field of the LIP neuron under study. Surprisingly, many LIP neurons responded to the cue in a
manner that was selective for the cue’s color. This was
unexpected, as dorsal visual stream neurons, including
parietal neurons, have not been reported to be selective
for color. However, the color selectivity of the LIP
neurons was only present when color was relevant to
solving the task: that is, the same neurons were not color
selective when the cue location was the task-relevant
feature — even though the task was otherwise visually
identical. Taken together, these data suggest that stimulus representations in the parietal cortex can adapt to
reflect the task’s demands.
Current Opinion in Neurobiology 2003, 13:194–197
Conclusions
Recent experiments provide a subtle and detailed view of
how neuronal activity in the parietal cortex reflects behavioral relevancy. However, many important questions
remain. A crucial issue is to gain an understanding of the
cellular mechanisms underlying attention. For example,
what can we infer about the mechanism(s) of attention
given its multiplicative, modulatory nature? Similarly,
what is the mechanistic relevance of the similarities
between attentional modulation and changing the stimulus
strength? These questions are closely entwined with the
problem of how attention is allocated. In particular, the
new data might suggest that attention reflects a local
selective transfer of information between brain areas,
rather than the oft-suggested (and rather awkward) idea
that attention is centrally ‘gated’. A related issue, especially
for animals trained by operant conditioning, is to understand the similarities and distinctions between attention
and reward mechanisms [43,44]. Finally, neuroimaging has
provided an important complement to neurophysiological
studies in animals, enabling us to understand more global
patterns of brain activity associated with attention. Future
investigations on attention should aim to provide a more
integrated view of these two experimental approaches.
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Current Opinion in Neurobiology 2003, 13:194–197