a r t ic l e s

A central role for the lateral prefrontal cortex in

goal-directed and stimulus-driven attention
Christopher L Asplund1, J Jay Todd1,2, Andy P Snyder1 & René Marois1

Attention is the process that selects which sensory information is preferentially processed and ultimately reaches our awareness.
Attention, however, is not a unitary process; it can be captured by unexpected or salient events (stimulus driven) or it can be
deployed under voluntary control (goal directed), and these two forms of attention are implemented by largely distinct ventral
and dorsal parieto-frontal networks. For coherent behavior and awareness to emerge, stimulus-driven and goal-directed behavior
© 2010 Nature America, Inc. All rights reserved.

must ultimately interact. We found that the ventral, but not dorsal, network can account for stimulus-driven attentional limits to
conscious perception, and that stimulus-driven and goal-directed attention converge in the lateral prefrontal component of that
network. Although these results do not rule out dorsal network involvement in awareness when goal-directed task demands are
present, they point to a general role for the lateral prefrontal cortex in the control of attention and awareness.

Reading this manuscript requires attention to be voluntarily deployed, cognitive processes is necessary to capture attention exogenously but
in a ‘top-down’ fashion, to this task. As a consequence of selectively all are known to engage the dorsal attentional network1,3–6.
attending to the page, one might become oblivious to surrounding The same concern also applies to our current understanding of how
sounds and sights. However, if a fire alarm suddenly blares, this salient attention controls awareness. Both the ventral and dorsal attentional
stimulus will probably capture attention in a ‘bottom-up’ manner networks have been associated with conscious perception5,17–23, lend-
and interrupt the ongoing task so that an appropriate course of action ing support to theories of awareness in which widespread changes in
can be initiated. This simple example illustrates a fundamental aspect of brain activity accompany conscious perception17,24. However, there
attention: what ultimately reaches our awareness and guides our behavior has been no specific attempt to assess the relative contributions of the
depends on the interaction between goal-directed and stimulus- dorsal and ventral networks to the neural basis of attentional limits to
driven attention1,2. conscious perception by using tasks that dissociate between stimulus-
Although much is known about the neural mechanisms that support driven and goal-directed attentional processes. Hence, the extent to
goal-directed1,3–7 and stimulus-driven attention1,5,8–12, how these two which each of these attention networks is necessary for awareness is
forms of attention are ultimately coordinated is not yet understood. currently unclear22,23,25.
The finding that these attentional forms are supported by largely dis- We have recently developed an experimental procedure that reveals
tinct neural networks, with a dorsal network that includes the frontal a profound but fleeting deficit in visual awareness resulting from the
eye field (FEF) and superior parietal cortex1,4–7,13 supporting goal- foveal presentation of an unexpected, task-irrelevant stimulus that
directed attention and a ventral one that consists of the lateral and involves neither an overt response nor a shift in spatial attention.
inferior frontal/prefrontal cortex and the temporo-parietal junction The deficit, termed surprise-induced blindness (SiB), is triggered by
(TPJ) underlying stimulus-driven attention1,3,8,9,12,13, has further com- an event that is absent from the observer’s goal-directed attentional
plicated the issue. As a result, several hypotheses have been proposed set and is not under the observer’s initial control26. As such, the
to explain how these two forms of attention might be coordinated: procedure represents a powerful way to assess whether stimulus-
through an interaction between the ventral and dorsal networks1, driven attentional limits to conscious perception can arise within the
across the dorsal14,15 or ventral5 attention network, or in the anterior ventral attention network in the absence of dorsal network involve-
component of the ventral network16. However, many of these proposals ment. Moreover, because the unexpected event ultimately affects the
are based on studies that used tasks that conflate stimulus-driven and goal-directed task of detecting a target, SiB experiments are also well
goal-directed attention, thereby making it difficult to determine the suited to reveal the neural mechanisms by which stimulus-driven
relative contributions of bottom-up and top-down neural processes attention affects goal-directed behavior.
to task performance. For example, the brain mechanisms of stimulus-
driven attention cannot easily be dissociated from those of goal-directed RESULTS
behavior if the stimulus-driven attention task involves spatial shifts of We scanned 30 participants while they were searching for a target
attention, goal-oriented processes, or motor responses, as none of these in a rapid serial visual presentation (RSVP) stream of distractor

1Department of Psychology, Vanderbilt Vision Research Center, Vanderbilt University, Nashville, Tennessee, USA. 2Department of Psychology, University of Chicago,
Chicago, Illinois, USA. Correspondence should be addressed to C.L.A. ([email protected]) or R.M. ([email protected]).

Received 16 September 2009; accepted 29 January 2010; published online 7 March 2010; corrected online 14 March 2010 (details online); doi:10.1038/nn.2509

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 a r t ic l e s

Figure 1 SiB experiment (Experiment 1). (a) Trial design. Participants

searched for a target letter in a rapid serial visual presentation (RSVP)
a b 100 Surprise-1 trial Surprise trial
G
stream of distractor letters. In a small proportion of trials (surprise trials), Target

Group target detection rate (%)

a surprise face stimulus was shown before the target. (b) Group target X 80
detection performance. Black bars represent accuracy in surprise trials, and Y
gray bars represent accuracy in trials immediately preceding the surprise 60
trials (surprise-1). Dashed line corresponds to the average target hit rate for Surprise K
stimulus
search trials (target only). Dotted line corresponds to the false alarm rate. 40

e
m
Ti
B 20

items (Fig. 1a). Unannounced to the participants, a salient but task- D

0
irrelevant stimulus occurred 330 ms before the target in a small pro- 1 2 3 4 5 6

portion of trials (surprise trials), causing SiB (Fig. 1b). Specifically, Surprise stimulus presentation number

group target detection performance differed across the surprise

stimuli presentations (Cochran’s Q4 = 30.3, P < 0.0001; see Online testing whether the response pattern mirrored the behavioral per-
Methods), with target detection worse following the first surprise trial formance. Specifically, because presentations of rare, task-irrelevant
(SS1) than after SS3–SS6 (sign tests, P’s < 0.040; see Online Methods), stimuli are known to increase neural activity8–10,27 and because SiB
and worse after SS2 than after SS5 or SS6 (P’s < 0.027). In SS3–SS6, was only observed for the first pair of surprise stimuli (SS1+2), we
performance was comparable to search trials (trials without surprise predicted that this pair would cause a greater BOLD response than the
stimuli, for which the target detection rate was 90.4%; Fig. 1b). Target- two subsequent pairs (SS3+4 and SS5+6) of surprise stimuli (the time
detection performance in the trials immediately preceding the first courses from each consecutive pair of surprise stimuli were averaged
© 2010 Nature America, Inc. All rights reserved.

two surprise trials was far better than in the respective surprise trials to improve statistical power; see Online Methods).
(sign tests, P’s < 0.0001; Fig. 1b), indicating that SiB does not result A statistical parametric map (SPM) revealed several brain areas that
from an initial difficulty with the target detection task. Rather, the were recruited more during surprise than during search trials (Table 1,
finding that unexpected, task-irrelevant stimuli triggered a profound Fig. 2 and Supplementary Fig. 1). Several of these areas showed invari-
but short-lived impairment in target detection that was essentially ant BOLD responses across the six surprise stimuli presentations, most
dissipated by the third surprise stimulus presentation is consistent notably the fusiform gyrus in visual cortex, suggesting that SiB might be
with a stimulus-driven, attention-based origin for this deficit26. a primarily central phenomenon that occurs at later stages than visual
information processing. Correspondingly, the only two regions that
Neural correlates of SiB demonstrated a BOLD response that quickly habituated after the first
To identify the neural substrates that underlie stimulus-driven two surprise stimulus presentations were in association cortex (Fig. 2):
attentional limits to conscious perception, we first isolated the brain the inferior frontal junction (IFJ), located in the posterior aspect of the
regions that were sensitive to the surprise stimuli, irrespective of presen­ inferior frontal sulcus (parts of Brodmann areas 9, 44, 6), and the temporo-­
tation number (see Online Methods). We then examined the BOLD parietal junction (TPJ), at the intersection of the superior temporal
(blood-oxygen-level dependent) signal from these brain regions, gyrus, supramarginal gyrus and superior temporal sulcus (parts of
Brodmann areas 40, 22, 39). For these two
brain regions, in both hemispheres, the peak
Table 1 Anatomical location and statistical assessment of activation for the ROIs isolated
response to SS1+2 was higher than the response
from surprise trials in Experiment 1 (surprise trial–search trial contrast)
to the two other SS pairs (two-tailed paired
Talairach coordinates SS1+2 vs. SS3+4 vs. SS1+2 vs.
Region Hemi (x, y, z) SS3+4 (t) SS5+6 (t) SS5+6 (t)
t tests, t29’s > 2.05, P’s < 0.049), whereas the
peak responses to SS3+4 and SS5+6 were indis-
TPJ Right 46, −56, 27 2.11* 1.07 2.76*
TPJ Left −49, −56, 23 2.35* 1.30 2.86* tinguishable (t29’s < 1.30, P’s > 0.20; Fig. 2).
IFJ Right 37, 5, 29 2.72* −0.37 2.05* Thus, the IFJ and TPJ exhibited an activity
IFJ Left −40, 8, 25 2.46* 0.05 2.18* pattern that mirrored the magnitude of SiB.
FG Right 30, −44, −11 0.42 −0.92 −0.53 This activity modulation was caused by the
FG Left −32, −51, −10 1.05 −0.70 0.05
IFG Right 40, 19, 13 0.75 0.30 1.09
surprise stimuli, not the perceived absence
IFG Left −48, 19, 7 −0.57 0.77 0.19 of a target, which co-varies with SiB, because
OFC Right 34, 27, −10 −0.22 −0.19 −0.53 the peak responses in target-absent trials and
OFC Left −37, 26, −8 0.27 0.15 0.40 search trials (see Online Methods) were indis-
Pulvinar Bilateral −7/9, −27, 1 1.46 0.71 1.83
tinguishable (two-tailed paired t tests, t29’s
PG Right 32, −3, −13 −0.09 −0.70 −0.80
STG Right 33, 12, −27 0.95 0.07 1.26 < 1.17, P’s > 0.25). No other brain regions
MTS Left −51, 2, −12 −0.17 −0.28 −0.36 showed an SiB-like pattern of activation, as an
SFG Right 13, 24, 49 0.49 0.74 0.90 additional SPM that directly contrasted SS1+2
Amygdala/SLEA Right 16, −9, −8 1.58 −0.17 1.26 with SS3+4 and SS5+6 demonstrated.
The three rightmost columns list the t-values resulting from paired t-tests of the given surprise stimulus pairs. Together, these results indicate that the
Amygdala/SLEA, amygdala and sublenticular extended amygdale; FG, fusiform gyrus (Brodmann area 37);
IFG, inferior frontal gyrus (Brodmann areas 44, 45); IFJ, inferior frontal junction (Brodmann areas 9, 44, 6); presentation of unexpected, task-irrelevant
MTS, middle temporal sulcus (Brodmann area 21); OFC, orbitofrontal cortex (Brodmann area 47); PG, parahippocam- stimuli activates a large network of cortical
pal gyrus; SFG, superior frontal gyrus (Brodmann area 8); STG, superior temporal gyrus (Brodmann area 38)45; TPJ,
temporo-parietal junction (Brodmann areas 39, 40, 22). With the exception of the IFJ and TPJ, none of these brain
and subcortical regions, but only a subset of
regions showed activation differences between any of the three surprise stimulus pairs (all P’s > 0.1), although the this network in the frontal/prefrontal and
amygdala/SLEA and pulvinar showed non-significant trends for greater SS1+2 activation relative to the two other temporo-parietal cortex shows a rapid BOLD
SS pairs. Note that the TPJ foci are anatomically distinct from, and superior to, regions of the superior temporal
46
sulcus involved in processing facial expressions and eye gaze . response adaptation that is commensurate
*P < 0.05. with the behavioral performance. This subset

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0.6 Left IFJ t 0.6 Right IFJ Figure 2 SiB experiment (Experiment 1) SPM.
Percent signal change

Surprise stimulus pairs

0.4 8.00 0.4 Brain regions showing rapid attenuation of
1+2
0.2 3+4 0.2 surprise stimulus-related activation. The SPM
5+6 highlights brain regions that responded to all six
0 0
3.71 surprise trials (see Online Methods), specifically
–0.2 –0.2
qFDR < 0.05 the IFJs (Talairach coordinates45 37, 5, 29 and
–0.4 –0.4
–4 0 4 8 12
−40, 8, 25) and TPJs (Talairach coordinates 46,
–4 0 4 8 12
Time from surprise stimulus (s)
−56, 27 and −49, −56, 23). The time courses
illustrate the brain regions from the SPM that
showed greater activity in the first pair of Surprise
0.6
Left TPJ Right TPJ trials than in the two other pairs of surprise trials.
0.6
The surprise stimulus appears at approximately
0.4 0.4
time zero. Error bars represent s.e.m.
0.2 0.2
0 0
–0.2 –0.2 Online Methods and Fig. 3b), while activity
–0.4 z = 24 –0.4
within each of these two pairs did not differ
–4 0 4 8 12 –4 0 4 8 12 (all P’s > 0.55). These results were obtained
regardless of whether the IFJ and TPJ ROIs
of brain regions is anatomically consistent with areas previously were defined exactly as the IPS and FEF ROIs or on the basis of the
implicated in novelty processing8,9,11,27–30, attentional orienting to group-level surprise trial ROIs (Tables 1 and 2).
sensory events31,32 and, most notably, to the core components of the Thus, the ROI analysis revealed that the dorsal network is activated
© 2010 Nature America, Inc. All rights reserved.

ventral attention network1,13. by the surprise stimuli, but unlike the swift activation pattern in the
ventral network following presentations of the first two surprise
Late dorsal network activation stimuli, the dorsal network appears to respond too late (by about 3 s)
In contrast to the ventral network, the SPMs (even with a liberal for it to cause SiB. However, this conclusion depends on the dorsal
threshold of P < 0.001, uncorrected) provided no evidence for sur- activation delay reflecting a genuine late neural response rather than
prise stimulus-related activation in the core brain regions associated inherent differences in the hemodynamic properties of the ventral
with the goal-directed attention network1,13, namely the frontal eye and dorsal parieto-frontal networks. We performed a follow-up
field (FEF) and the intraparietal sulcus (IPS). To analyze the dorsal ‘spatial SiB’ experiment (Experiment 2) to distinguish between
network’s association with SiB with greater sensitivity, for each par- these possibilities. Given the role of the dorsal network in the con-
ticipant, we functionally defined regions of interest (ROIs) for the trol of visuo-spatial attention1,4,6, we predicted that the sporadic
putative FEF and IPS based on their activation in search trials, as presentations of highly salient, categor­ically distinct task-irrelevant
these regions were strongly activated by the task of searching for and stimuli in the periphery instead of in the center of the RSVP stream
responding to targets (see Online Methods, Fig. 3 and Table 2). The (Fig. 4a) would not only persist in capturing attention26 but also
anatomical locations of the resulting ROIs corresponded well to the lead to shifts of visual-spatial attention or eye movements, thereby
conventional positions of the FEF and IPS in goal-directed attention promptly recruiting the FEF and IPS in addition to the ventral network.
tasks1,3–6,12,13,16. When probed during the surprise trials, activity in Consistent with our hypothesis, we found a persistent SiB effect
these dorsal regions was greater during SS1+2 than in search trials and robust activations in both the dorsal and ventral networks
(t29’s > 2.50, P’s < 0.018 except for a marginal effect in the right FEF (Fig. 4b, and Supplementary Tables 1 and 2). Notably, there was no
at t29 = 1.79, P = 0.084) but not during subsequent pairs (Table 2). longer a delay in activation between the dorsal and ventral networks
Thus, the more sensitive ROI analysis revealed that the FEF and IPS (P’s > 0.36), in marked contrast to Experiment 1 (timing delay differ-
are also activated by the first two surprise stimulus presentations. ence across experiments: one-tailed P = 0.038; see Online Methods).
Notably, however, the time courses of activation specific to the first These results indicate that the delay in activation of the dorsal brain
pair of surprise stimuli, revealed by subtracting the underlying search- regions during the surprise trials of Experiment 1 had a neural,
related activity from the first two surprise stimulus trials (see Online not hemodynamic, origin. Additional behavioral evidence indicates
Methods), showed that the IPS and FEF responded significantly later that this delayed activation might reflect the modulation of top-down
than did the IFJ and TPJ (all pair-wise comparisons P < 0.048; see attentional settings in anticipation of post-surprise stimulus trials

Figure 3 Stimulus-driven and goal-directed

attention activity in Experiment 1. (a) Dorsal z = 45
0.6a TPJ b
IPS
0.3 c
IFJ FEF
brain regions that are active during search 0.2
Percent signal change

FEF
trials. (b) Surprise stimulus-specific waveform 0.4
0.1
in dorsal (FEF, IPS) and ventral (IFJ, TPJ)
regions of interest (ROIs) defined in individual R 0.2 0
participants (see Online Methods). Each time
course was constructed by subtracting the –0.1
0
search trial time course from the time course
IPS –0.2
for the first two surprise stimulus trials. The t 8.00
surprise stimulus appears at approximately time –0.2 –0.3
2.82 –4 0 4 8 12 16 20 0 4 8 12 16 20 24
zero. (c) Search trial activation time course qFDR < 0.05 Time from surprise stimulus (s) Time from trial onset (s)
over the same period of time as in b for the
same ROIs. Arrows mark each trial’s onset. Note that the activation pattern is cyclical, mirroring the trial structure (one trial every 8 s). The observed
hemodynamic responses in IPS, FEF and IFJ match the predicted responses for the hypothesized search-related activity (Supplementary Fig. 3).

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during the cue-related period (t5’s > 3.53, P’s < 0.017; see Online
Table 2 Average anatomical location and statistical assessment
of activation for the individually defined ROIs from search trials in Methods), as expected of brain regions involved in goal-directed
Experiment 1 (open contrast SPM) attention1,3,6 (Fig. 5b). Furthermore, the IFJ was also activated by the
Talairach coordinates SS1+2 vs. SS3+4 vs. SS5+6 vs.
cue (t5 = 2.74, P = 0.041) and at the same time as the FEF and IPS. These
Region Hemi (x, y, z) ± s.d. search (t) search (t) search (t) results were obtained regardless of whether the ROIs were defined
IPS Right 26 ± 4, −65 ± 6, 36 ± 5 2.81* 0.46 0.28 in the cueing task or in the search trials of the RSVP task, attesting
IPS Left −22 ± 4, −66 ± 6, 39 ± 6 3.45* 0.44 1.38 to the fact that the brain regions that showed goal-directed activity in
FEF Right 34 ± 4, −7 ± 3, 51 ± 5 1.79 0.51 0.63 the search trials are also involved in visuo-spatial shifts of attention.
FEF Left −32 ± 5, −8 ± 3, 51 ± 5 2.50* 1.95 0.96 We therefore conclude that IFJ supports goal-directed behavior, as it
TPJ Right 47 ± 5, −55 ± 5, 28 ± 5 4.52* 3.21* 1.65 is activated along with core members of the dorsal network during
TPJ Left −49 ± 2, −58 ± 5, 24 ± 4 5.33* 2.37* 1.73
the cue period of a classic goal-directed attention task. These con-
IFJ Right 40 ± 4, 6 ± 3, 27 ± 3 4.99* 1.67 1.06
IFJ Left −42 ± 3, 8 ± 3, 25 ± 2 5.92* 2.51* 1.12
clusions are consistent with previous reports suggesting that similar
The three rightmost columns list the t-values resulting from paired t-tests of the given brain regions are activated in other cued attention shift tasks37,38.
surprise stimulus pairs versus target-only activity. See Table 1 for abbreviations. These Together, the results of our experiments indicate that the IFJ parti­
ROI coordinates closely matched those isolated from the surprise trials (Table 1).
*P < 0.05.
cipates in both stimulus-driven and goal-directed attention. While
the pattern of IFJ activity is consistent with brain regions involved
in stimulus-driven attention during the presentation of a surprise
(Supplementary SiB RT Experiment and Supplementary Fig. 2). stimulus, its activity profile is instead more consistent with those of
Regardless of the function of this delayed dorsal response to sur- goal-directed brain regions during the search task. It follows from
prise stimulus presentations, it does not appear to be involved in these results that the IFJ should be more functionally integrated with
© 2010 Nature America, Inc. All rights reserved.

SiB, as the FEF and IPS are activated after the events that trigger the core members of the dorsal network during goal-directed attention
perceptual deficit. but with core members of the ventral network during stimulus-
driven attention. These predictions were borne out by a functional
Interaction of goal-directed and stimulus-driven attention connectivity analysis (see Online Methods), which showed that IFJ
If the core components of the dorsal attentional network (the FEF activity was correlated positively with activity in the FEF and IPS (IFJ-
and IPS) are not responsible for SiB, then how do the surprise stimuli FEF, t29 = 9.13, P < 0.0001; IFJ-IPS, t29 = 12.19, P < 0.0001; FEF-IPS,
ultimately impair the goal-directed task of searching for and respond- t29 = 6.87, P < 0.0001), but negatively with TPJ activity (t29 = −4.27,
ing to a target? That is, how does stimulus-driven attention disrupt P = 0.00019), during the search trials. Conversely, following the
goal-directed behavior? The answer is provided by an examination presentation of a surprise stimulus, the IFJ-FEF and IFJ-IPS correla-
of the temporal dynamics of activation in the two attentional net- tions decreased (paired t test of the changes: t29 = −2.12, P = 0.043;
works during the search trials of Experiment 1. In these trials, the t29 = −2.36, P = 0.025), whereas those between IFJ and TPJ increased
FEF and IPS showed the pattern expected of brain regions associ- (t29 = 2.07, P = 0.047) and those between FEF and IPS did not
ated with goal-directed behavior, namely an activation profile that change (t29 = −1.07, P = 0.29). These connectivity results provide
tightly correlated with performing the primary search task (Fig. 3c). additional evidence that the IFJ underlies stimulus-driven and goal-
By contrast, TPJ activity was out of phase with activity in the dorsal directed attention, with its response profile and network allegiance
brain regions, showing deactivation when the others were activated depending on task demands. In that context, SiB would result from
(onset shifts of ~4 s, P’s < 0.0001; Fig. 3c), consistent with the finding the ‘bottom-up’ engagement of IFJ by the presentation of a surprise
that attention-demanding cognitive tasks are often accompanied by stimulus, thereby transiently disrupting or altering this brain
suppression of TPJ activity13,21,33–35. Notably, the time course of IFJ region’s control of the target detection task. With behavioral and
activity no longer closely followed that of its ventral network cohort, neuronal habituation to the repeated surprise stimulus presenta-
the TPJ (onset shifts of ~4 s, P’s < 0.0001), but instead closely tracked tions, the IFJ might be able to maintain its goal-oriented activity
the activation time course of the dorsal brain regions (Fig. 3c). This even in the face of task-irrelevant stimulus presentations.
IFJ activity in the search trials does not simply reflect target detec-
tion, for the same activity pattern was found in target-absent trials.
These findings suggest that the IFJ might be not only a core member
a G
b 0.6
TPJ IPS
Target IFJ FEF
of the ventral attention network that supports stimulus-driven atten-
Percent signal change

X
0.4
tion, but also functionally integrated with the dorsal network during
Y
goal-directed behavior.
Surprise K 0.2
To test the hypothesis that the IFJ ROIs identified in Experiment 2 stimulus
are important in goal-directed behavior, we carried out an additional C
e
m

0
Ti

experiment (Experiment 3) that assessed whether the IFJ is activated, B

along with the FEF and IPS, in a prototypical goal-directed atten- D
–0.2
tion task, an endogenous Posner cueing task3,36 (Fig. 5a; see Online –4 0 4 8 12 16 20
Methods). In this task, participants made a speeded response to a Time from surprise stimulus (s)

target presented at a location that was cued by the color of a central Figure 4 Spatial SiB experiment (Experiment 2). (a) Trial design.
fixation point, with the cue validly predicting the location of the The procedure was identical to that in Experiment 1 save that in a
target on 80% of the trials. The task was successful in engaging small proportion of trials, a colorful surprise stimulus was shown before
the target away from fixation (Fig. 1a). (b) Surprise stimulus-specific
goal-directed attention, evidenced by the fact that participants were
waveforms in dorsal and ventral attention network ROIs defined in
faster at detecting the target at validly cued than at invalidly cued individual participants. Time courses were constructed in the same
positions (reaction time ± s.d., 317 ± 36 ms versus 396 ± 64 ms, fashion as those in Experiment 1 (see Fig. 3b). Note that all four regions
t5 = 4.53, P = 0.0062). The dorsal brain regions were activated show an immediate response to the surprise stimulus presentations.

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junction, is the site of convergence for stimulus-driven and goal-

a b 0.6 TPJ IPS directed attention, a finding that is consistent with recent resting
IFJ FEF
state functional connectivity data suggesting that this brain region

Beta weight estimates

Variable ITI
e

0.4
Tim

(3,967–9,967 ms) functionally interacts with both ventral and dorsal brain structures 16.
0.2
The IFJ has also been implicated in task-switching and cognitive
Target (33 ms)
control42,43 more generally. This brain region is therefore ideally
Variable delay 0
suited to act as the neural site of coordination for stimulus-driven
(2,000–8,000 ms)
and goal-directed attention. Moreover, the IFJ’s involvement in
–0.2
both the non-spatial and spatial SiB tasks (Experiments 1 and 2)
Cue (2,000 ms) 0 4 8 12 16 indicates that this brain region’s function generalizes across both
Time from cue onset (s)
spatial and non-spatial forms of attention. While it remains to be seen
Figure 5 Endogenous cueing task experiment (Experiment 3). (a) Trial whether all these attentional processes are mediated by the same sub-
design. A color cue predicted the location of an upcoming target, to
populations of IFJ neurons, a central role for this brain region in the
which the participant then responded in a speeded manner. (b) Cue-
related activity in dorsal and ventral attention network ROIs isolated from co-ordination of stimulus-driven and goal-directed attention across
Experiment 2 (see Online Methods). The arrow marks cue onset. ITI, both spatial and non-spatial domains resonates well with the proposal
inter-stimulus interval. that the IFJ is a critical neural substrate that underlies our limited
attentional capacities44.
DISCUSSION
Our study reveals that both functional divergence and convergence Methods
of the dorsal and ventral attentional networks underlie attention Methods and any associated references are available in the online
© 2010 Nature America, Inc. All rights reserved.

and awareness. Divergence of function between these two networks version of the paper at http://www.nature.com/natureneuroscience/.
is clearly shown by the SiB procedure, as it shows that stimulus-driven
Note: Supplementary information is available on the Nature Neuroscience website.
attentional limits to conscious perception can arise from the ven-
tral attentional network in the absence of dorsal network or visual Acknowledgments
cortex modulation. In contrast, previous neurobiological investiga- We thank B. Rogers, J. Swisher and E. Conser. This work was supported by National
tions17–22,39,40 have frequently implicated regions of both the ven- Science Foundation grant 0094992 and National Institute of Mental Health grant
R01 MH70776 (R.M.).
tral and dorsal networks in awareness. Such large-scale activation
patterns are consistent with ‘global workspace’ models that posit AUTHOR CONTRIBUTIONS
that awareness emerges from the reverberating activity of a widely C.L.A. designed and performed experiments, analyzed data, and wrote the
distributed cortical network17,22,24. The difference in activation pat- manuscript. J.J.T. and A.P.S. designed and performed experiments. R.M. designed
terns between these previous studies and the present one is prob- experiments and wrote the manuscript.
ably the result of differences in task design. Whereas previous tasks COMPETING FINANCIAL INTERESTS
have included spatial shifts of attention3,5,14,15,18,39 or covert or overt The authors declare no competing financial interests.
responses3,5,11,12,18–21,39,40 to the critical attention-capturing stimu-
lus, our task was specifically designed to exclude these components Published online at http://www.nature.com/natureneuroscience/.
Reprints and permissions information is available online at http://www.nature.com/
as they are unnecessary for exogenous attentional capture but can reprintsandpermissions/.
activate the dorsal attention network1,3–6. As such, our task shows
that the dorsal network’s contribution to conscious perception might
1. Corbetta, M. & Shulman, G.L. Control of goal-directed and stimulus-driven attention
be negligible under these controlled circumstances. This conclusion in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).
is consistent with the suggestion that awareness is not necessarily an 2. Egeth, H.E. & Yantis, S. Visual attention: control, representation, and time course.
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 ONLINE METHODS with the TPJ. Each ROI in each participant was defined as the peak voxel and
Participants in all experiments had normal or corrected-to-normal vision and significantly activated surrounding area up to 1 cm3. Anatomical landmarks (FEF
received monetary compensation. The Vanderbilt University Institutional Review at the junction of the superior frontal sulcus and precentral sulcus; IPS in the
Board approved the experimental protocol and written informed consent was intraparietal sulcus between y = −50 and y = −70; IFJ at the junction of the infe-
obtained from each participant. rior frontal sulcus and precentral sulcus; TPJ around the posterior Sylvian fissure)
SiB experiment (Experiment 1). Thirty-one right-handed individuals (12 females) were used to identify each region, consistent with earlier work3,5,13,44. We next
participated. One individual’s data were excluded owing to technical problems. extracted time courses for the surprise and search trials, creating baselines and
Participants searched for a target letter (X) in an RSVP stream of distractor averages as above. For statistical tests of amplitude, we compared the correspond-
letters (white Helvetica font, 1.8° × 1.8°, presented on a dark gray background). ing time points across a given pair of time courses using paired t-tests.
Each 8-s trial began with a 3.4-s RSVP of 31 letters randomly chosen from a set of For statistical tests of activity onset timing, we first subtracted each partici-
20 (vowels were excluded), with no letter presented twice in a row. Each stimulus pant’s search trial activity from their surprise stimulus trial activity for the first
was presented at fixation for 100 ms followed by a 10-ms inter-stimulus interval pair (SS1+SS2), leaving activation specific to deficit-causing surprise stimuli.
(ISI). Following the RSVP, a screen appeared for 2 s prompting the participants To estimate the hemodynamic response’s onset time for these subtracted time
to respond with an appropriate key press (right index finger for ‘target present’ courses, we employed a bootstrap approach50 owing to the difficulty of acquir-
and right middle finger for ‘target absent’). The response period was followed by ing reliable onset measures from each participant’s pairs of surprise stimulus
a 2.6-s ITI consisting of a white fixation cross. trials. Using linear interpolation, each participant’s time courses, for both search-
Each participant completed a single fMRI run of 40 trials. The target (present related (search trials) and surprise-related (surprise trials – search trials) activity,
on 77.5% of trials) appeared between frames 25 and 29. In six of the trials, a from each ROI were upsampled to 1-ms resolution and then smoothed with a
surprise stimulus (grayscale face, 1.8° × 1.8°, distinct for each trial) appeared Gaussian kernel (FWHM = 2 s). Thirty samples for each ROI were selected with
between frames 22 and 26 of the RSVP, 330 ms before the target (5 trials) or in replacement and averaged, a process that was repeated 10,000 times. For each
a trial with no target (1 trial). Surprise trials occurred between trials 2 and 38 of the resulting averaged samples, we computed the onset as the time when the
and were separated by a minimum of two search trials (trials with a target but time course had achieved 20% of its peak amplitude (results were similar for
© 2010 Nature America, Inc. All rights reserved.

no surprise stimulus). Participants practiced search trials exclusively before the 10%). Finally, these onset values (10,000 per ROI) were compared across ROIs.
fMRI session. Feedback was given only during practice, and participants were For example, right IFJ onsets occurred before right IPS onsets for 9,977 of the
required to reach target accuracy above 80% before scanning. At no time were samples. From this count, we computed a P-value, which in the example would
participants informed about the surprise stimuli. be 0.0066, two-tailed. Interactions were computed by first subtracting the onset
To assess the effect of repeated surprise stimulus presentations, we used values for surprise-related activity from those for search-related activity and then
Cochran Q tests for categorical data of dependent samples47. We then applied comparing these differences across regions.
sign tests to determine the significance of the relevant pair-wise comparisons. As no hemispheric differences were found in any of the above analyses, and
These and all subsequently described tests were two-tailed with α at 0.05 unless to increase statistical power, we collapsed the data across hemispheres for all
otherwise noted. subsequent analyses.
Anatomical 3D high-resolution images were acquired using conventional The correlation analyses were performed on the data derived from the GLM
parameters on a 3T GE MRI system. Nineteen 7-mm-thick axial slices (0 mm skip; analyses after further processing steps had been applied. Global signal fluctuations
3.75 × 3.75 mm in-plane) were taken parallel to the anterior commissure–posterior in this dataset were removed by regressing out the time courses from a ventricu-
commissure (AC-PC) line. T2*-weighted image parameters: 25 ms echo time, 70° lar region of interest, a white matter region of interest, and the average signal
flip angle, 240 mm FOV, 64 × 64 matrix, 2,000 ms repetition time. The functional across the entire brain. Second, the data were filtered using a zero-phase forward
scan included 166 brain volumes, with the first 6 volumes discarded for signal and reverse band-pass filter (0.01 < f < 0.2 Hz). Next, we segmented the data
stabilization. Trials were presented using Psychophysics ToolBox48,49 for Matlab on from each individually defined ROI by trial, performing a percent signal change
an Apple G4 Macintosh. Stimuli were back-projected from an LCD projector onto transform on each trial as described above. Trials were then concatenated by
a screen viewed through a prism mirror by the supine participant. condition, yielding 28 points associated with surprise trials (SS1+2) and 28 points
Data analysis was performed using BrainVoyager 4.9.1, BrainVoyager QX 1.7.9 with search trials (two randomly selected trials from about 10 that were at least
(Brain Innovation), and custom Matlab software. Data preprocessing included three trials away from any surprise trials). Time courses for each ROI (collapsed
image realignment, 3D motion correction, linear trend removal and correction across hemispheres) pair of interest in each participant were then correlated by
for slice acquisition timing. Statistical parametric maps (SPMs) of BOLD activa- condition and the resulting values converted using Fisher’s z transformation. The
tion were created using a multiple regression analysis, with regressors defined correlations between regions were then tested for significance across participants
for the six surprise stimuli, search trials, and no-target trials; boxcar functions with one-sample t-tests, and the change in correlations between search and sur-
for each trial type were convolved with a canonical double-γ hemodynamic prise trials compared across participants with paired t-tests.
function (SPM2, http://www.fil.ion.ucl.ac.uk/spm) to generate each regressor.
The resulting maps from all participants were spatially smoothed with a 6-mm Spatial SiB experiment (Experiment 2). Six right-handed individuals (three
Gaussian kernel (full width at half maximum), standardized to Talairach space45, females) participated. The timing of each trial was as in Experiment 1 except
and superimposed to create composite maps. The model fit was assessed using that 29 stimuli were shown on each trial and the ISI was 17 ms. There were
t statistics, with significance determined by the false discovery rate (FDR) threshold 40 trials during each of six fMRI runs. The target (present on 80% of trials) appeared
at q < 0.05 (random-effects analysis). between frames 23 and 27. In four of the trials per run (three target-present and
For the group region of interest (ROI) analysis, the center of mass and sur- one target-absent), a surprise stimulus appeared 350 ms before the target at one of
rounding activated voxels for each activated focus were selected, up to 1 cm3. four spatial locations centered 4.2° from fixation. The surprise stimuli consisted
The time-course for each surprise trial was extracted from each ROI for each of distinct, large (6.5° × 6.5°), colorful items, each shown only once. Surprise
participant and then converted to percent signal change (baseline from the time trials occurred between trials 2 and 38, and were separated by a minimum of
point of surprise stimulus (SS) onset and two preceding points). The average three search trials. Participants practiced the search task before the fMRI session.
time courses for pairs of SS (SS1+SS2, SS3+SS4, SS5+SS6) were computed for Participants were not informed about the surprise stimuli.
each participant. For statistical tests of amplitude, we identified the time point Anatomical 3D high-resolution images were acquired using conventional
with the largest percent signal change between 6 and 8 s after surprise stimulus parameters on a 3T Philips MRI system. Thirty-three 3.5-mm thick axial slices
presentation for each SS pair for each participant, and then used paired t-tests (0.5 mm skip; 1.875 × 1.875 mm in-plane) were taken parallel to the AC–PC
for the appropriate comparisons. line. T2*-weighted image parameters: 35 ms echo time, 79° flip angle, 240 mm
For the individually-defined ROI analyses, we identified ROIs whose activity FOV, 128 × 128 matrix, 2,000 ms repetition time. There were 161 brain volumes
correlated with the performance of the primary target-detection task (SPM of per functional scan. Trials were presented using Psychophysics ToolBox48,49 for
open contrast of the predictor for search trials). Positive β-weights for the predictor Matlab on an Apple MacBook Pro, and stimuli back-projected to the participant
were associated with the FEF, IPS and IFJ, whereas negative ones were associated as in Experiment 1.

doi:10.1038/nn.2509 nature NEUROSCIENCE

 Data analysis was performed using BrainVoyager QX 1.11.4 (Brain Innovation) of each delay period was exponentially distributed to maximize deconvolution
and custom Matlab software. Data preprocessing, SPM generation, ROI defi- efficiency. Participants responded to the target with a speeded button press.
nition and event-related average construction were identical to the methods The next trial commenced after an ITI of 4–10 s (exponentially distributed).
in Experiment 1. Participants completed 32 trials during each of 3 runs.
We used a bootstrap analysis to test the hypothesis that the delay in dorsal One participant’s behavioral responses were not collected owing to a technical
network activity (relative to the ventral network) was significantly greater in error, and another participant performed the task incorrectly by withholding
Experiment 1 than in Experiment 2. After constructing bootstrap samples, we responses to invalidly cued targets. Behavioral data for these two individuals were
obtained the onset measures for the search-related and surprise-related activity collected during a separate session outside the scanner.
for each ROI in each experiment. To increase power, we collapsed these measures The imaging procedure was identical to that used for Experiment 2.
across hemispheres and network nodes (dorsal or ventral). We then compared After employing the same preprocessing steps used for Experiment 2,
the onset measures for Experiment 1 ((Search – Surprise)Dorsal – (Search – time courses from Experiment 2’s search task ROIs were constructed using a
Surprise)Ventral) with those for Experiment 2 (same subtractions). As the 90% deconvolution analysis. Z-transformed β-estimates, corrected for serial auto-
confidence intervals for the resulting metrics did not overlap, the comparison correlations, were derived for the 10 volumes following the cue onset and for the
was significant one-tailed at P < 0.05. 10 volumes following target onset, and individual time courses were averaged
across participants and hemispheres (Fig. 5b). To test for significant activation
Endogenous cueing task experiment (Experiment 3). After completing in each region, one-sample t-tests were performed on the average of the third
Experiment 2, the same six individuals participated in Experiment 3 during the and fourth volumes after cue onset.
same scan session.
Each trial began with a central dot (0.25° in diameter) changing from white 47. Sheskin, D.J. Handbook of Parametric and Nonparametric Statistical Procedures
to either green or blue for 2,000 ms, which indicated in which of two squares 2nd Ed. (CRC Press, Boca Raton, Florida, 2000).
(1.0° across, located 3.4° right or left of fixation) an upcoming target was likely 48. Brainard, D.H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).
49. Pelli, D.G. The VideoToolbox software for visual psychophysics: transforming
to appear (81% validity). The cue’s color-location mapping was counterbalanced
© 2010 Nature America, Inc. All rights reserved.

numbers into movies. Spat. Vis. 10, 437–442 (1997).

across participants. The target, a white dot (0.25°) that appeared inside one of the 50. Davison, A.C. & Hinkley, D.V. Bootstrap Methods and Their Application (Cambridge
boxes for 100 ms, was presented 4, 6, 8 or 10 s after the cue onset. The frequency University Press, Cambridge, 1998).

nature NEUROSCIENCE doi:10.1038/nn.2509