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Neuron. 2008 May 8; 58(3): 306324.

The Reorienting System of the Human Brain: From Environment

to Theory of Mind

Maurizio Corbetta1,2,3,4,*, Gaurav Patel2,3, and Gordon L. Shulman1,4,*

1 Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA
2 Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA
3 Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, MO
63110, USA

Abstract
Survival can depend on the ability to change a current course of action to respond to potentially
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advantageous or threatening stimuli. This reorienting response involves the coordinated action of
a right hemisphere dominant ventral frontoparietal network that interrupts and resets ongoing activity
and a dorsal frontoparietal network specialized for selecting and linking stimuli and responses. At
rest, each network is distinct and internally correlated, but when attention is focused, the ventral
network is suppressed to prevent reorienting to distracting events. These different patterns of
recruitment may reflect inputs to the ventral attention network from the locus coeruleus/
norepinephrine system. While originally conceptualized as a system for redirecting attention from
one object to another, recent evidence suggests a more general role in switching between networks,
which may explain recent evidence of its involvement in functions such as social cognition.

Introduction
To safely navigate the environment, survive, and reproduce, animals and people must rapidly
select sensory information that is relevant to their goals (e.g., routes, food, mates). They must
also quickly redirect their attention and change their course of action when faced with novel,
potentially threatening, or rewarding stimuli. The complex set of adjustments in response to
novel and unexpected stimuli is defined here as a reorienting response. Reorienting may occur
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between two environmental stimuli, such as when we orient to the siren of an ambulance while
reading a newspaper, or between an internally directed activity and the environment, as when
the same siren interrupts a train of thought. While several autonomic and motor responses can
be triggered by novel sensory stimuli through subcortical reflexes that are largely automatic
and unconscious (the orienting reflex; Sokolov, 1963), more recent work indicates that this
adaptive behavior involves a complex interaction between cortical systems specialized for the
selection of sensory information. A dorsal frontoparietal (or dorsal attention) network enables
the selection of sensory stimuli based on internal goals or expectations (goal-driven attention)
and links them to appropriate motor responses. A ventral frontoparietal (or ventral attention)
network detects salient and behaviorally relevant stimuli in the environment, especially when
unattended (stimulus-driven attention). These systems dynamically interact during normal
perception to determine where and what we attend to. In this paper, we review evidence from
neuroimaging, neuropsychology, and neurophysiology on the role of these two networks,
particularly the ventral network, in the reorienting response.

*Correspondence: [email protected] (M.C.), [email protected] (G.L.S.).

4These authors have contributed equally to this work.
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The Psychology of Attention to Environmental Stimuli

Psychological theories of attention are often concerned with simple behavioral goals, such as
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finding an object with particular features (Treisman and Gelade, 1980; Wolfe, 1994) or at a
particular location (Eriksen and Hoffman, 1974; Posner, 1980) and responding to it in an
appropriate manner (Hommel, 2000). This form of selection is labeled goal-driven or
endogenous to emphasize the internal or top-down signals that guide perception through a
dynamic interaction with sensory or bottom-up information. The biased-competition model of
attention, for example, proposes that objects in a visual scene compete for access to visual
short-term memory and that the competition is biased by top-down signals that promote access
of behaviorally relevant objects (Desimone and Duncan, 1995). These top-down signals,
characterized as working memory (e.g., Downing, 2000; but see Woodman and Luck, 2007),
long-term memory (Moores et al., 2003), or action related (Craighero et al., 2002; Rosenbaum,
1991), interact with sensory (bottom-up) signals produced by objects in the visual scene,
enabling the desired object to be selectively perceived and entered into memory at the expense
of unimportant objects (Bundesen, 1990; Wolfe, 1994). For instance, Figure 1A shows a
student who focuses on his computer desktop while writing his thesis and ignores surrounding
objects and people.

Adaptive behavior, however, also requires that we respond to objects that are outside the current
focus of attention, i.e., that do not match current settings for selecting stimuli and responses.
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The object we are looking for may appear with different features than we expected or at a
different location. More importantly, a new object may appear that requires a completely
different course of action. While the student looks at the computer screen, a colleague may ask
a question (Figure 1B), or while a monkey searches for food, a predator may appear. Moreover,
we may be presented with new events requiring a response while we are engaged in internally
directed activities that do not involve an interaction with the environment. Someone may
distract us while we are considering the meaning of a sentence in the thesis we are writing, or
a monkey may quickly react to the appearance of a predator while grooming or eating.

Reorienting to new objects may occur reflexively, based on their high sensory salience (Jonides
and Yantis, 1988), particularly when we do not have a specific task to do (Pashler and Harris,
2001), but distinctive objects attract attention more effectively when they are also behaviorally
relevant (Yantis and Egeth, 1999), either because they match our current goals or because of
long-term memory associations that signal their importance, as when we hear the phone ringing
or the siren of an ambulance. In fact, the degree to which a distinctive but entirely irrelevant
object can attract our attention, so-called exogenous attention, is controversial (Folk et al.,
1992; Gibson and Kelsey, 1998; Jonides, 1981; Posner and Cohen, 1984; Theeuwes and
Burger, 1998; Yantis and Egeth, 1999). In some cases, shifts of attention to a distinctive
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stimulus can be part of a task goal (Bacon and Egeth, 1994), as when someone tries to detect
any salient object appearing in a visual scene. In other cases, distinctive but irrelevant objects
may share a specific feature with our current goal, as when we notice someone wearing a red
sweater while looking for a friend with a red hat (Folk et al., 1992; Gibson and Kelsey,
1998).

A Neuroanatomical Model of Attention: Dorsal and Ventral Attention

Networks
Several lines of evidence indicate that two cortico-cortical neural systems are involved in
attending to environmental stimuli (Corbetta and Shulman, 2002). A dorsal frontoparietal
network, whose core regions include dorsal parietal cortex, particularly intraparietal sulcus
(IPS) and superior parietal lobule (SPL), and dorsal frontal cortex along the precentral sulcus,
near or at the frontal eye field (FEF) (Figure 2A, blue areas), embodies the top-down control

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mechanism proposed by biased competition and related theories (Bundesen, 1990; Desimone
and Duncan, 1995; Wolfe, 1994). The dorsal system generates and maintains endogenous
signals based on current goals and preexisting information about likely contingencies and sends
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out top-down signals that bias the processing of appropriate stimulus features and locations in
sensory cortex. This conclusion is based on evidence that the dorsal network is preactivated
by the expectation of seeing an object at a particular location or with certain features (e.g.,
movement in a specific direction) (Corbetta et al., 2000; Hopfinger et al., 2000; Kastner et al.,
1999; Shulman et al., 1999), by the preparation of a specific response (Astafiev et al., 2003;
Connolly et al., 2002), or by the short-term memory of a visual scene (LaBar et al., 1999;
Pessoa et al., 2002). The dorsal system is also involved in linking relevant stimuli to responses,
as it is modulated when people change their motor plan for an object (Rushworth et al.,
2001). Under some conditions, the preparatory activation of the dorsal frontoparietal network
extends to visual cortex, presumably reflecting the top-down modulation of sensory
representations (Giesbrecht et al., 2006; Hopfinger et al., 2000; Kastner et al., 1999; Serences
et al., 2004; Silver et al., 2007; Sylvester et al., 2007) (Figure 1A). Accordingly, anticipatory
activity may predict performance to subsequent targets (Giesbrecht et al., 2006; Pessoa and
Padmala, 2005; Sapir et al., 2005; Sylvester et al., 2007). Finally, recent studies show that
electrical or magnetic stimulation of FEF or IPS leads to a retinotopically specific modulation
of visual areas and parallel improvement of perception at corresponding locations of the visual
field (Moore and Armstrong, 2003; Ruff et al., 2006, 2007).
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A second system, the ventral frontoparietal network, is not activated by expectations or task
preparation but responds along with the dorsal network when behaviorally relevant objects (or
targets) are detected (Corbetta et al., 2000). Both dorsal and ventral networks are also activated
during reorienting, with enhanced responses during the detection of targets that appear at
unattended locations. For example, enhanced responses are observed when subjects are cued
to expect a target at one location but it unexpectedly appears at another (i.e., invalid targets
in the Posner spatial cueing paradigm) (Arrington et al., 2000; Corbetta et al., 2000; Kincade
et al., 2005; Macaluso et al., 2002; Vossel et al., 2006) or when a target appears infrequently,
as in oddball paradigms (Bledowski et al., 2004; Braver et al., 2001; Linden et al., 1999;
Marois et al., 2000; McCarthy et al., 1997; Stevens et al., 2005) (Figure 1B). Core regions of
the ventral network include temporoparietal junction (TPJ) cortex (anatomically, TPJ is more
strictly defined as the cortex at the intersection of the posterior end of the STS, the inferior
parietal lobule, and the lateral occipital cortex), defined as the posterior sector of the superior
temporal sulcus (STS) and gyrus (STG) and the ventral part of the supramarginal gyrus (SMG)
and ventral frontal cortex (VFC), including parts of middle frontal gyrus (MFG), inferior frontal
gyrus (IFG), frontal operculum, and anterior insula (Figure 2A, orange regions). An early
theory of how the two networks interact (Corbetta and Shulman, 2002) proposed that when
attention is reoriented to a new source of information (stimulus-driven reorienting), output
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from the ventral network interrupts (as a circuit breaker) ongoing selection in the dorsal
network, which in turn shifts attention toward the novel object of interest.

Although both attentional networks have been most extensively investigated in vision, the
available evidence indicates a supramodal function (Driver and Spence, 1998; Macaluso et al.,
2002). The ventral network (right TPJ, right IFG) registers salient events in the environment
not only in the visual but also in the auditory and tactile modalities (Downar et al., 2000), and
similar dorsal and ventral parietal and frontal regions are modulated by reorienting to invalid
targets (Arrington et al., 2000; Corbetta et al., 2000; Giessing et al., 2006; Kincade et al.,
2005; Macaluso et al., 2002; Mayer et al., 2006; Vossel et al., 2006) or by oddballs (Braver et
al., 2001; Kiehl et al., 2001; Linden et al., 1999; Marois et al., 2000) in different modalities.

The sections below review in more detail recent work on these networks, particularly the ventral
network, including: (1) the functional-anatomical independence of each network, (2) the

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importance of behavioral relevance rather than sensory salience in driving the ventral network,
(3) whether the output of the ventral network initiates a reorienting response and how the dorsal
and ventral networks interact, (4) how the functions of the ventral network may generalize
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beyond perception and action to include memory and social cognition, and finally (5) the
emerging link between activity in the ventral network and the output of the locus coeruleus-
norepinephrine system (LC-NE), as recently outlined by neurocomputational theories (Aston-
Jones and Cohen, 2005; Bouret and Sara, 2005; Dayan and Yu, 2006; Yu and Dayan, 2005).

We do not consider in this discussion the relationship between cortical and subcortical regions
involved in the control of attention. There is strong evidence that subcortical structures like
the superior colliculus are involved in stimulus-driven but also goal-driven attention (Bell et
al., 2004; Fecteau et al., 2004; Rafal et al., 1988; Sapir et al., 1999). The pulvinar nucleus of
the thalamus has been proposed as a gateway structure that funnels top-down biases from
parietal areas into visual cortex (Petersen et al., 1987; Shipp, 2004).

The Dorsal and Ventral Attention Systems Form Separate Functional-

Anatomical Networks
A basic question is the degree to which different regions in each putative system cohere as a
functional-anatomical network. The hypothesis of two attention networks, originally based on
the patterns of activation under different task conditions (Corbetta and Shulman, 2002), has
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been strongly supported by studies of interareal correlation of low-frequency (<0.1 Hz)

fluctuations of the spontaneous (not task-evoked) BOLD signal over time, called functional
connectivity by MRI (fcMRI) (Biswal et al., 1995). Several groups have reported a number of
fcMRI networks (e.g., visual, auditory, somatomotor, default, attention) (Biswal et al., 1995;
Fox et al., 2005b, 2006a; Fransson, 2005; Greicius et al., 2003; Mantini et al., 2007), which
are related to the underlying anatomical connectivity (Vincent et al., 2007) and replay at rest
the patterns of functional activation evoked by behavioral tasks (Fox et al., 2005b, 2006a;
Greicius et al., 2003; Hampson et al., 2002; Vincent et al., 2007). In other words, brain regions
that are commonly recruited during a task are anatomically connected and maintain in the
resting state (in the absence of any stimulation) a significant degree of temporal coherence in
their spontaneous activity. Furthermore, there is growing evidence that the integrity and
strength of spontaneous functional connectivity are behaviorally significant (Hampson et al.,
2006; Seeley et al., 2007; He et al., 2007b). For instance, breakdown of interhemispheric
functional connectivity in posterior parietal cortex correlates in a group of patients with post-
stroke neglect with their visuospatial deficits (He et al., 2007a; see below).

Regions that putatively belong to the dorsal and ventral attention systems, based on their
consistent activation in the Posner cueing paradigm to spatial cues and unattended targets,
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respectively, also show significant interregional correlation at rest (Fox et al., 2006b) or during
an active task with the mean task signal removed (He et al., 2007a) (see Figure 3). There is a
remarkable similarity between the dorsal parietal and frontal regions identified by a meta-
analysis of task-evoked activation studies (Figure 2) and those showing high resting-state
correlations (Figure 3). Similar results are found for ventral frontoparietal regions coactivated
during stimulus-driven orienting (Fox et al., 2006a; He et al., 2007a). Moreover, the right
hemispheric bias observed in the ventral attention network in several activation studies
(Arrington et al., 2000; Corbetta et al., 2000; Downar et al., 2000) is mirrored in fcMRI (Fox
et al., 2006a; He et al., 2007a) (compare ventral network in Figures 2 and 3).

While segregation between dorsal and ventral attention networks is nearly complete,
spontaneous activity in right posterior MFG correlates with both networks (Figure 3),
indicating that right MFG may contain intermixed neuronal populations respectively connected
with dorsal or ventral regions (Fox et al., 2006a). This result raises the possibility that ventral

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and dorsal networks do not directly interact but are principally linked through prefrontal cortex
(Fox et al., 2006a). This link is also supported by results obtained in neglect subjects showing
that the functional disconnection of MFG with dorsal parietal cortex is responsible for abnormal
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stimulus selection (see below and He et al., 2007a) (wire diagram, Figure 2B). The functional
segregation of the two networks in the absence of a task may allow their flexible recruitment
during active behavior. For example, while dorsal regions are active following the presentation
of an instructive cue, ventral regions are not recruited or are even suppressed (Shulman et al.,
2003;Todd et al., 2005). However, following the presentation of a target, both ventral and
dorsal regions respond briskly (Corbetta et al., 2000;Hampshire et al., 2007;Shulman et al.,
1999,2003). In summary, the correspondence between activation and connectivity analyses
provides strong evidence for separate dorsal and ventral attention networks forming distinct
functional systems.

The Ventral Network Is Activated by Important Stimuli that Reorient Attention

While reorienting to an object can be driven by salience and behavioral relevance, relevance
is the critical factor that determines whether an object activates the ventral network (Downar
et al., 2001). The ventral network might be considered a prime candidate for mediating
orienting to salient but unimportant stimuli, i.e., exogenous attention (Posner and Cohen,
1984), because under passive conditions it is highly responsive to distinctive sensory events
in all modalities (Downar et al., 2000). But this hypothesis has now been tested and rejected
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(Kincade et al., 2005). Kincade and colleagues separated the BOLD activity produced by an
uninformative but salient peripheral cue, a red square in an array of green squares, from the
activity produced by discriminating a subsequent rotated T or L (Figure 4A). In control
conditions, subjects were presented with a neutral display of randomly intermixed color squares
or a foveal cue that oriented attention voluntarily. Exogenous cues (the red square) did not
activate the ventral network (Figure 4A), even though performance was better at that location,
indicating that these cues were effective in generating a shift of attention. In contrast, the dorsal
network (IPS/SPL and FEF) showed stronger activation for exogenous than neutral cues
(Figure 4A), although the strongest recruitment was recorded for endogenous cues (data not
shown). Many other studies have measured activations in exogenous orienting paradigms that
have combined activations during the cue and target periods (Kim et al., 1999; Lepsien and
Pollmann, 2002; Mayer et al., 2006; Peelen et al., 2004; Rosen et al., 1999). Although these
studies are more difficult to interpret, they indicate that the ventral network is not recruited by
orienting to uninformative but salient cues presented before a target appears (see Peelen et al.,
2004, for an exception). Similarly, de Fockert and colleagues showed that uninformative but
salient distracters that attract attention did not activate the ventral system (de Fockert et al.,
2004) (Figure 4B), although they did activate the dorsal system. The overall conclusion is that
exogenous orienting recruits the same dorsal frontoparietal network that is responsible for
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directing attention based on goals or expectations.

Conversely, the ventral network is well activated by stimuli that are important, even if they are
not very distinctive. Indovina and Macaluso (2007), for example, showed that unattended
targets of low salience activated regions in both dorsal (FEF, precuneus) and ventral (IFG and
anterior insula) attention networks, in line with previous results (Arrington et al., 2000;
Corbetta et al., 2000; Macaluso et al., 2002), to a much greater degree than highly salient but
irrelevant distracters (see Figure 4C). Finally, the ventral network is activated by irrelevant
objects when they are similar to a target object. Serences et al. (2005) asked subjects to
categorize red foveal letters interspersed among a rapid, successive series of colored foveal
letters (rapid serial visual presentation, or RSVP) while peripheral distracter letters were
occasionally presented in the target color (red) or in a nontarget color (green) (Figure 4D). This
situation is analogous to when we look in a crowd for a friend wearing a red sweater and notice
people wearing red but not green clothes (contingent orienting; Folk et al., 1992). TPJ

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activation was only observed for the red distracters (Figure 4D), consistent with the hypothesis
that the ventral network responds mainly to stimuli thought to be behaviorally relevant (see
also Downar et al., 2001).
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In summary, the ventral network is not activated by orienting to distinctive but unimportant
stimuli (exogenous orienting), except perhaps in the special case where subjects do not have
an ongoing task, but does underlie reorienting to environmental stimuli based on their task
relevance. An important conclusion from these neuroimaging studies is that the psychological
distinction between exogenous and endogenous orienting (Jonides, 1981) may not map onto
different neural systems. Rather, a more fundamental distinction appears to be between systems
involved in orienting, both exogenous and goal-driven, i.e., the dorsal attention system, and
those involved in stimulus-driven reorienting, i.e., the ventral and dorsal attention systems.

Preventing Activation of the Ventral Network by Unimportant Objects

The poor response of the ventral network to distinctive but unimportant objects when a person
focuses on a task prevents shifts of attention that could interfere with task performance. Two
studies have now shown that this poor response may be due to suppression of the ventral
network by a sustained top-down signal.

In one study, subjects saw a rapid stream of letters (RSVP) and were instructed to look for an
occasional digit (Figure 5A) (Shulman et al., 2003). Prior to the point at which the digit was
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detected, while subjects were still searching the letter displays, the ventral network (bilateral
TPJ, R MFG, and R IFG) showed a sustained deactivation (Figure 5C, green-blue voxels).
These deactivated regions overlapped regions that showed increased positive responses to
unattended targets in a separate experiment, indicating that the deactivation occurred within
ventral regions involved in stimulus-driven reorienting. Shulman and colleagues (Shulman et
al., 2003) suggested that the suppression of activity prevented an inappropriate response to
irrelevant stimuli. Because targets still triggered a robust positive response, however, activity
in the ventral network appeared to have been gated by task relevance or filtered, with only
targets passing the filter. Stronger filtering appeared to correlate with better performance,
because the average deactivation in right TPJ was significantly larger on trials in which the
subsequent target was detected than missed (Shulman et al., 2007) (Figure 5A).

In a second study (Todd et al., 2005), subjects remembered a set of objects in a visual display,
and following a blank retention interval, decided whether any of the objects were present in a
new display (Figure 5B). The larger the number of objects the subject had to remember (the
memory load), the more R TPJ was deactivated during the retention interval. The authors
separately showed that higher memory loads resulted in poorer detection of a novel unattended
stimulus, suggesting that high memory loads suppress activity in R TPJ and prevent stimulus-
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driven reorienting (Todd et al., 2005). Together, these studies indicate that when subjects focus
on a task, signals for task relevance (filtering in Figure 2B) deactivate TPJ, preventing
reorienting to unimportant objects.

Source of Signals that Restrict Ventral Activation to Important Objects

The source of signals for task relevance may be the dorsal network (IPS, FEF), which shows
strong anticipatory activity when people expect to see an object at a particular location or with
particular features (Corbetta et al., 2000; Kastner et al., 1999). In the previous RSVP
experiment, IPS and FEF were each one of the few regions in the brain that showed sustained
activation to distracters prior to target detection (Shulman et al., 2003) (Figures 5A and 5C).
These sustained signals may have filtered the input to the ventral network (blue arrows in Figure
5C; filtering signal in Figure 2B).

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Another possible source of top-down signals is prefrontal cortex (Desimone and Duncan,
1995; Miller and Cohen, 2001). Resting-state analyses suggest that R MFG may link dorsal
and ventral networks (Fox et al., 2006a), possibly funneling top-down biases from the dorsal
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network onto the ventral network (Figure 5C and 2B). R MFG is probably not the source
because it showed sustained deactivation along with R TPJ and R IFG (Figure 5C). However,
sustained increases were observed in anterior cingulate and anterior insula (Shulman et al.,
2003), which have been postulated to form the core of a network for cognitive control
(Dosenbach et al., 2006) (orange arrows in Figure 5C). The influence from these cortical
regions may be direct through cortico-cortical interactions or indirectly via subcortical loops.
In the last section, we relate the pattern of activity in TPJ, including filtering signals, to the
output of the LC-NE, which receives input from the anterior cingulate and the anterior insula
(Aston-Jones and Cohen, 2005; Ongur et al., 2003).

If prefrontal cortex is the source or the conduit of these modulations onto TPJ, then poor top-
down control of stimulus-driven reorienting should be evident after prefrontal lesions. Chao
and Knight (1995) reported that patients with unilateral dorsolateral prefrontal cortex (DLPFC)
lesions showed markedly decreased performance in an auditory match-to-sample task due to
irrelevant distracter tones presented during the retention interval. Loss of prefrontal inputs may
have decreased top-down control over TPJ, resulting in inappropriate reorienting to distracting
stimuli (see also Ro et al., 1998; Snow and Mattingley, 2006).
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In summary, only environmental stimuli that are behaviorally relevant trigger the ventral
network. The ventral network response is suppressed when irrelevant stimuli are presented,
even if they are distinctive, reflecting a filtering signal that gates sensory responses by
behavioral relevance. The source of the filtering signal may be the dorsal network or other
parts of prefrontal cortex, either directly or indirectly via subcortical loops.

Do Signals from the Ventral Network Initiate Reorienting?

Above, we discussed the inputs to the ventral system that ensure it is mainly activated by
behaviorally important stimuli. Next, we consider how the output from this system affects
activity in other neural systems and behavior. One possibility is that, when an important
stimulus appears outside the current focus of attention, fast-latency signals from the ventral
network initiate reorienting by sending a circuit-breaking or interrupt signal to dorsal regions,
which change the locus of attention (Corbetta and Shulman, 2002).

The dorsal network contains the neural machinery for directing attention and the eyes to sensory
stimuli appearing at unexpected locations, with spatially selective responses to contralateral
stimuli and responses to movements of attention or the eyes (Beauchamp et al., 2001; Corbetta
et al., 1998, 1993; Nobre et al., 1997; Schluppeck et al., 2005; Sereno et al., 2001; Sweeney et
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al., 1996; Sylvester et al., 2007). In contrast, group-averaged studies of ventral regions (TPJ,
VFC) have not found spatially selective responses during reorienting (Corbetta et al., 2002;
Macaluso et al., 2002; Macaluso and Patria, 2007). Similarly, mapping studies in individuals
have only reported weak spatially selective responses near or within the ventral network in
parts of MFG (Hagler and Sereno, 2006; Jack et al., 2007) and superior temporal gyrus (STG)
(Jack et al., 2007). The weak evidence for spatial selectivity in the ventral network suggests
that spatial reorienting is not mediated solely by that network but involves joint activation of
dorsal and ventral regions.

There is little evidence, however, that short-latency responses in the ventral attention network
precede those in dorsal areas and trigger a reorienting response. Within dorsal parietal and
frontal sites, EEG- or MEG-based estimates of visual response latency to targets for an eye
movement vary between 130 and 170 ms (Evdokimidis et al., 2001; McDowell et al., 2005;
Sestieri et al., 2008). Within ventral sites in TPJ and IFG, the response to targets is thought to

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be indexed by the P300 potential, with a latency of 300400 ms, considerably longer than the
dorsal latencies (Bledowski et al., 2004; Daffner et al., 2003; Knight et al., 1989; Menon et al.,
1997; Yamaguchi and Knight, 1991a). Unfortunately, P300 and eye movement paradigms are
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difficult to compare. There have been a number of ERP/MEG studies of spatial reorienting,
but the results are ambiguous in relation to the relative latency of dorsal and ventral parietal
regions (Luck et al., 1994; Mangun and Hillyard, 1991). Invalid targets that follow a voluntary
cue to shift attention increase a late-positive deflection (230400 ms) at central, parietal, and
occipital sites that might correspond to P300 (Mangun and Hillyard, 1991). At temporal
electrodes ipsilateral to the target (Hopfinger and Ries, 2005), invalid targets that follow an
uninformative (exogenous) cue produce a negative-going deflection in the range of 200250
ms, preceding a separate P300. Although this latter paradigm involved noninformative cues,
the ERP component was sensitive to several task-contingent factors, reflecting top-down
signals (Hopfinger and Ries, 2005).

Overall, the latency of visual responses to salient behaviorally relevant visual stimuli is, if
anything, shorter in dorsal parietal than in ventral parietal areas, but definitive studies have not
been conducted. In awake behaving monkeys, neural responses to visual stimuli in lateral
intraparietal area (LIP), the putative homolog of human IPS/SPL, show a very rapid
nonselective volley (~50 ms) followed by slower oscillations (100200 ms) that are modulated
by spatial attention (Bisley et al., 2004). In more ventral parietal cortex, in correspondence
with area 7A, which shows modulation by unattended stimuli (Constantinidis and Steinmetz,
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2001; Robinson et al., 1995) and salient oddball stimuli during simple fixation (Constantinidis
and Steinmetz, 2005), similar to the ventral attention network, average response are about 100
ms (typical range 70200 ms; Constandidinis personal communication). No direct comparison
on the same task has been carried out, however. Reorienting of attention to a behaviorally
relevant and salient stimulus outside of the current focus is probably initiated in dorsal
frontoparietal cortex in conjunction with subcortical structures (e.g., superior colliculus).
Ventral system activity during reorienting may reflect slower adjustments necessary to
complete or carry out a complex reorienting response that involves shifts in task sets,
expectations, reward contingencies, and arousal.

Do Signals from the Ventral Network Influence Reorienting and the Dorsal
Network?
While the latency data from electrophysiological studies are ambiguous on whether ventral
network activity triggers dorsal activity during reorienting, transcranial magnetic stimulation
studies (TMS) nonetheless support a key role for ventral regions in reorienting attention and
detecting targets in conjunction with dorsal frontoparietal regions (IPS, FEF). An extensive
discussion of TMS studies of visuospatial attention is beyond the scope of this review, but
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some conclusions can be drawn from the extant literature. First, interference with regions in
inferior parietal cortex (TPJ, SMG, AG) disrupts visual target detection and reorienting
(Chambers et al., 2004a; Ellison et al., 2004; Meister et al., 2006). Second, disruption has been
demonstrated for stimulation latencies ranging from 90120 ms (Chambers et al., 2004a) to
200300 ms following target onset (Chambers et al., 2004a; Ellison et al., 2004; Meister et al.,
2006). Early interference effects may reflect disruption of a signal that disengages attention
from its current location and initiates reorienting (Chambers et al., 2004a). Third, the regions
in inferior parietal cortex that show effects of TMS depend on the task: R TPJ during detection
of bilateral stimuli (Meister et al., 2006), angular but not supra-marginal gyrus (SMG) during
reorienting in an exogenous cueing paradigm (Chambers et al., 2004a), SMG during reorienting
in an endogenous cueing paradigm (Chambers et al., 2004b), and STG during visual search
(Ellison et al., 2004). Fourth, a larger set of studies has reported effects of TMS in FEF or
posterior parietal cortex (PPC) on detection, search, and orienting (Fuggetta et al., 2006;
Grosbras and Paus, 2002; Muggleton et al., 2003; OShea et al., 2004; Taylor et al., 2007; Thut

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et al., 2005). Overall, in agreement with the imaging evidence showing that dorsal and ventral
networks are coactivated during target detection and stimulus-driven reorienting (Corbetta et
al., 2002; Giessing et al., 2006; Kincade et al., 2005; Marois et al., 2000), TMS of both ventral
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and dorsal regions affects reorienting, detection, and search.

We have reported direct evidence for an interaction between the two networks in fMRI studies
of stroke patients with spatial neglect. Spatial neglect is a syndrome characterized by a bias to
attend and respond to objects on the contralesional side and is observed more frequently after
right than left hemisphere strokes (Heilman et al., 1987b; Mesulam, 1999). Lesions that cause
neglect are typically localized in ventral frontal or temporoparietal cortex and underlying white
matter (Husain and Kennard, 1996; Karnath et al., 2004; Mort et al., 2003; Vallar and Perani,
1987). We recently demonstrated that the spatial bias of neglect depends on a physiological
imbalance between left and right dorsal parietal cortex (IPS/SPL), which is caused by structural
and physiological abnormalities in the ventral attention network (Corbetta et al., 2005; He et
al., 2007a). The inter-hemispheric imbalance in IPS/SPL is evident both during spatial attention
tasks, with a significant relationship between left-side neglect and hyperactivation of left
parietal cortex, and in measures of functional connectivity at rest. For instance, Figure 6A
shows BOLD time series collected from a stroke patient who suffered extensive damage to
inferior frontal, perisylvian, and TPJ cortex and showed severe left-side neglect at the acute
stage. The time series clearly show abnormal correlation of the resting BOLD signal between
left and right IPS, which is not structurally damaged. This deficit correlates across subjects
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with the severity of neglect and recovers over 9 months as neglect improves (He et al.,
2007a). Interestingly, the degree of functional impairment in dorsal parietal cortex correlates
with the degree of impaired functional connectivity in the structurally damaged ventral
network, hence demonstrating the interaction between the two networks. Notably, this
interaction involved right MFG and the white matter fibers connecting this region to dorsal
parietal cortex (He et al., 2007a), providing more support for the hypothesis that right MFG
links ventral and dorsal systems (Figure 2B).

Finally, a recent paper used a Granger Causality analysis to show an influence of ventral activity
on dorsal activity when healthy subjects passively listened to a movement from a symphony
(Sridharan et al., 2007) (Figure 6B), consistent with an interaction between the networks.
Completion of the movement activated both networks, but the ventral activation preceded the
dorsal activation (Sridharan et al., 2007). The authors suggested that the ventral network
activity marked an event boundary and influenced dorsal activity during a subsequent updating
of working memory.

In summary, TMS, neuroimaging, and lesion evidence support the hypothesis that ventral and
dorsal networks are both necessary and interact when attention is reoriented to behaviorally
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relevant environmental stimuli.

Reorienting Perceptual and Response Processes to Environmental Stimuli

Although many of the studies that have been discussed involved spatial reorienting to
environmental stimuli, we emphasized in the introduction that the ventral network mediates a
broader set of changes in response to an environmental stimulus. Unfortunately, these broader
changes involve many processes that can be difficult to isolate. For example, an early indication
that the ventral network was recruited under circumstances other than spatial reorienting came
from studies using the oddball paradigm, in which subjects detect a target presented
infrequently (10%20%, oddball) in a stream of frequent standard objects. Enhanced
responses to oddballs are observed in a set of regions that includes most consistently the
temporoparietal junction and the lateral prefrontal cortex but also dorsal regions in parietal and
frontal cortex involved in shifting attention. Because the oddball is usually defined by a

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different feature(s) than the standard, rather than by a different location (see Marois et al.,
2000, for a comparison of the two cases), the enhancement to the oddball is not related to a
spatial shift of attention.
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But the oddball paradigm combines a range of processes, making the fMRI activations difficult
to interpret. For example, a spatial or feature cue in a typical visual attention task may indicate
what object should be attended (e.g., attend to the red letter) (Broadbent, 1971; Bundesen,
1990) but not how the object should be categorized or responded to (e.g., if the letter is a
vowel, press the left key), restricting the relevant processes to those involved in stimulus
selection (Logan and Gordon, 2001). In the oddball paradigm, however, the oddball/standard
distinction indicates what response should be made, adding processes involved in categorizing
the oddball, selecting a response (whether overt or covert, go or no-go) based on the current
stimulus-response mapping, making the response, and generating signals related to
performance monitoring.

Several other studies suggest that the ventral network marks transitions when one behavior is
interrupted or terminated and a new behavior begins, including transitions at event boundaries
(for a general discussion of event boundaries, see Zacks et al., 2007). A similar phenomenon
appears to occur during the transition between a period of rest and a task block involving many
trials (task onset) or the transition from the task block to rest (task offset). Both block onsets
and offsets robustly and transiently activate R TPJ and VFC, but also other regions, including
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dorsal prefrontal cortex and the dorsal attention network (Dosenbach et al., 2006; Fox et al.,
2005a; Konishi et al., 2001) (Figure 7A). Even within a single trial, coactivation of dorsal and
ventral frontoparietal areas at task offset may index a readjustment or interruption of ongoing
task sets (Shulman et al., 2002). Interestingly, in this latter study, the transient signal at task
transition occurred both in dorsal frontoparietal areas that were engaged prior to the transition,
but only at the transition point in the ventral network. One interpretation is that the ventral
network signals the task transition and/or provides a reset signal. As discussed below, it is
possible that these cortical reset signals are related to similar signals identified in the LC-NE
system, which putatively allows for a shift of cortical architecture at task boundaries (Bouret
and Sara, 2005).

Overall, the above studies suggest that, whenever environmental stimuli call for a change in a
maintained task, ventral (and dorsal) attention networks are modulated at the transition point.
Interestingly, the ventral network is not recruited when people regularly switch from one task
to another over short time periods (e.g., task-switching paradigms). This form of task control
appears to involve a separate set of dorsal parietal and frontal regions (Brass and von Cramon,
2004; Braver et al., 2003; Kimberg et al., 2000; Rushworth et al., 2002).
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Reorienting from Internally Directed Processes to Environmental Objects

Stimulus-driven reorienting has mainly been discussed in the context of changing the control
of behavior from one environmental input to another, but similar reorienting mechanisms may
also be involved in shifting from a broad range of internally directed processes in order to
deal with environmental events, as when interrupting memory retrieval (did I lock the car
door?) to respond to a sudden stimulus (is that my cell phone ringing?). We hypothesize
that the ventral attention network may play a central role in this function.

Important aspects of internally directed processing, such as introspection, self-referential

thoughts, or projecting oneself into a situation (e.g., envisioning or planning ones future or
remembering ones past as in episodic memory) are thought to involve the so-called default
network (Raichle et al., 2001). This network of cortical regions is strongly deactivated during
a wide range of demanding cognitive tasks relative to a passive resting or viewing state (Binder
et al., 1999; Mazoyer et al., 2001; Shulman et al., 1997). It has been proposed that these regions

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mediate a number of default processes to which the brain returns in the absence of a task
(Raichle et al., 2001). A similar set of regions show high temporal correlation in resting-state
fcMRI (Fox et al., 2005b; Greicius et al., 2003).
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Some authors have proposed that default and dorsal attention networks represent two
fundamental axes of functional organization in the brain, with the dorsal attention network
controlling environmentally directed processes (e.g., perception and action) and the default
network controlling internally directed processes (e.g., memory, introspection) (Fox et al.,
2005b; Golland et al., 2007). This hypothesis is based on the observation that goal-directed
tasks activate the dorsal attention network and deactivate the default network. Moreover,
several fcMRI studies have reported that default activity is negatively correlated with the dorsal
network (see top panel of Figure 3; (Fox et al., 2006a; Fransson, 2005; but see Golland et al.,
2007; Nir et al., 2006). Finally, during natural vision, the posterior part of the brain is entirely
occupied either by regions that are positively correlated with the dorsal attention network or
the default network (Golland et al., 2007; Nir et al., 2006).

The hypothesis that the ventral network may function as a system to switch (reorient) between
internally and externally directed activities is based on two sets of observations. First, the
ventral network is largely segregated in terms of functional connectivity from both dorsal
attention and default networks (see Figure 3; Fox et al., 2006a). The independence in the resting
state of the ventral network from both dorsal and default networks may allow a flexible
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interaction during externally or internally directed behavior. Second, although both ventral
attention and default systems may deactivate during goal-oriented behavior, the deactivations
depend on different factors. During a perceptual task, in which subjects monitored an RSVP
stream for a single target (Shulman et al., 2003), the TPJ component of the ventral network
was deactivated only while subjects searched the stream for the target (Figure 5A), but the
angular gyrus component of the default network was deactivated as long as the RSVP stream
remained on the screen. In other words, TPJ was deactivated by the attentional component,
while the angular gyrus was deactivated by the sensory component of the task. Moreover, the
presentation of the attended target activated TPJ but not angular gyrus (see Golland et al.,
2007, for a different dissociation between anterior and posterior portions of IPL). In contrast,
when subjects searched their episodic memory for an item (an internally directed task), both
sets of regions were still deactivated, but only the angular gyrus was then activated by a positive
match in memory (Shannon and Buckner, 2004;Wheeler and Buckner, 2004). The similarity
of response profile when looking for a target in the environment or in memory raises the
possibility that the ventral attention network plays a similar role in both processes. In both
cases, filtering of the ventral attention network is necessary to protect the system from
involuntarily reorienting to environmental stimuli when resources are allocated to perceptual,
memory, or self-referential processing.
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Reorienting during Theory of Mind Cognition

An intriguing development of the last few years is that activation of right TPJ, the posterior
core of the ventral attention network, has been reported during theory of mind (ToM)
cognition, i.e., reasoning about other peoples mental states (Fletcher et al., 1995; Gallagher
and Frith, 2003). ToM cognition involves a close interaction between perceptual processes and
those involved in self-projection (Buckner and Carroll, 2007). Subjects may judge the
intentions of a person they are viewing in a movie or judge a persons intentions based on a
written description.

A recent study reported that ToM activations, measured by comparing responses to false-belief
stories and control stories involving outdated photographs, colocalized with activations from
reorienting to invalid targets in a Posner cueing task (Mitchell, 2007) (Figure 7C). Figure 7B

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shows the close correspondence between activations during attentional reorienting and social
cognition in R TPJ from a recent meta-analysis (Decety and Lamm, 2007), although there was
a tendency for the social cognition activations to extend slightly more posteriorly, perhaps into
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the default system proper.

Colocalization of activations from ToM and reorienting paradigms does not necessarily imply
a common process. First, the colocalization, while impressive, is only approximate. In addition
to the fact that fMRI activity averages over large cell populations, there may be a slightly more
posterior distribution for ToM activations. To our knowledge, the VFC component of the
ventral attention network has not been reported in studies of social cognition. Instead, social
cognition paradigms often activate, in addition to TPJ, foci in posterior cingulate and medial
prefrontal cortex that belong to the default network, which we argued above is distinct from
the ventral attention network. Perhaps a slightly more posterior location for the TPJ focus in
some ToM paradigms reflects connectivity with these default regions. Second, colocalization
may mask subtle but systematic differences in the voxelwise distributions of the activations
(Downing et al., 2007). Demonstrating that two voxelwise patterns or distributions are not
identical, however, begs the question of why both patterns occur in the same cortical tissue.
Although in principle the two distributions could reflect completely unrelated functions that
are juxtaposed, i.e., a specialized ToM module (Saxe and Powell, 2006) and a node within a
reorienting network (Corbetta and Shulman, 2002), the close anatomical correspondence may
suggest a less arbitrary relationship.
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If activations from reorienting and ToM are not completely unrelated, why might they be
linked? First, colocalization might reflect factors that are poorly controlled in either or both
paradigms. For example, ToM paradigms generally involve blocks or trials in which subjects
comprehend animations, movie sequences, or stories over an extended period. The cognitive
or working memory loads of the experimental and control stories in these ToM paradigms have
not been explicitly controlled. In several studies, the selective activation of right TPJ during
ToM conditions as compared to control conditions actually reflected a lesser deactivation (e.g.,
Figure 7C from Mitchell, 2007). Because greater memory loads produce stronger TPJ
deactivations (Todd et al., 2005), differential TPJ activity in experimental and control
conditions of ToM paradigms could reflect overall differences in memory load or task
complexity. The consistency of R TPJ activations in ToM and reorienting experiments across
very different paradigms, however, suggests that any single methodological factor may not
explain the colocalization.

Second, colocalization might reflect cognitive processes that are present in both paradigms.
For example, both reorienting and ToM paradigms often involve breaches of expectation (e.g.,
invalid cues [Arrington et al., 2000; Corbetta et al., 2000; Macaluso et al., 2002] or false-belief
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stories [Gallagher and Frith, 2003; Vogeley et al., 2001]), which appear to modulate the ventral
network. Decety and Lamm (2007) suggest that many aspects of social cognition involve a
comparison of internal predictions with actual external events, explaining the ubiquitous
presence of R TPJ activity. However, some ToM studies have included controls for this factor
(Saxe et al., 2004), and some ToM and reorienting studies have not involved manipulations of
expectation (Saxe and Powell, 2006; Serences et al., 2005).

Another possibility along these lines is that TPJ activity during ToM tasks reflects signals
linked to shifts in eye gaze or for perception or imagery of gaze. Several studies have shown
that posterior STS is activated during the perception of gaze shifts (Allison et al., 2000;
Pelphrey et al., 2003, 2004). Within a social context, activation from viewing-gaze shifts are
larger when they occur toward the viewer (mutual gaze) than when they occur away from the
viewer (averted gaze) (Figure 7D). This error signal may reflect a mismatch between our
expectation and the observed direction of another persons gaze (similar to an invalidly cued

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target) or an error signal in the inferred state of mind of the other person (a ToM signal). In
general, strong evolutionary reasons link mechanisms for shifting attention to the development
of social mechanisms for conspecific interactions in old and new world monkeys to
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mechanisms to infer others intention or ToM in higher apes and humans (Tomasello et al.,
2001). Gaze-related activations in STS, however, may not colocalize with those for reorienting
or ToM (these functions have not been assessed within the same experiment) (see Gobbini et
al., 2007, for a recent meta-analysis).

Finally, in ToM experiments, subjects continually shift between a simulation or judgment of

the other persons mind or viewpoint and processing of perceptual evidence from their own
viewpoint that supports the simulation or judgment. Interestingly, recent evidence indicates
that disruption of TPJ activity either by seizure activity or electrical stimulation can engender
a number of hallucinatory misperceptions that involve a mismatch between the perception of
the surrounding environment and ones own body. For example, subjects may feel as if they
see their body from the outside or as if the perception of their own body is not aligned with the
bodys visual representation and surrounding environment (reviewed in Blanke and Arzy,
2005). These changes in body self-perception can be manipulated experimentally
(Lenggenhager et al., 2007) and produce right TPJ activity (Arzy et al., 2006). These findings
have been interpreted by considering TPJ cortex a site of multimodal integration of
visuospatial, vestibular, and body-related signals and that the alignment of these signals
generates and maintains ones own sense of body or bodily self (Blanke and Arzy, 2005). While
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the relationship between reorienting signals in the ventral attention network and sense of body
remains to be explored, an intriguing hypothesis is that similar environmental and bodily
representations and their comparison may be co-opted for ToM interactions and that attention
signals in TPJ may be important to switch between internal, bodily, or self-perspective and
external, environmental, or others viewpoint, a key ingredient of ToM.

The Role of Expectation in Reorienting

Many of the conditions that activate the ventral network involve violating an expectation. For
example, because people prepare for expected objects, an unexpected target object is often an
unattended object, evoking stimulus-driven reorienting. Similarly, event boundaries, which
appear to activate the ventral network, may be determined by monitoring whether the sensory
input departs from a current model of ongoing behavior (Zacks et al., 2007). Discrepancies or
breaches of expectation indicate that a new behavior has occurred, marking an event boundary
and requiring the model to be updated. But activations to unexpected stimuli may also reflect
processes that are either entirely separate from reorienting or modulate reorienting. Important
objects that violate an expectation may also increase arousal, dishabituate neuronal responses
in sensory and associative areas in paradigms in which expectations are driven by stimulus
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frequency (e.g., oddball paradigms), or produce error signals that drive learning, reward, or
affective mechanisms. While, in some cases, violations of expectation may be an essential
feature of the process that drives ventral network activation, it will also be important in future
work to explicitly manipulate stimulus-driven reorienting independently from expectation.

Several neuromodulators have been linked to the detection of unexpected events, including
dopamine and norepinephrine (NE) (Dayan and Yu, 2006). Although dopaminergic responses
to unexpected stimuli are often discussed in the context of reward (Schultz, 1998; Schultz et
al., 1997) some authors have proposed that they more generally facilitate a shift of attention
to unexpected and behaviorally important stimuli (Horvitz, 2000; Redgrave et al., 1999; Zink
et al., 2003). This putative function is very similar to that proposed for the ventral attention
network, but there is no evidence of a significant dopaminergic projection to TPJ. In contrast,
there is evidence in monkey for a strong noradrenergic innervation of inferior parietal cortex
and superior temporal gyrus, possible homologs of human TPJ (Foote and Morrison, 1987;

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Morrison and Foote, 1986). Therefore, we next consider the functional relationship between
the ventral attention network and activity in the locus coeruleus (LC), the primary source of
NE.
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Links between Ventral Attention Network and Locus Coeruleus-

Norepinephrine System
The LC-NE system is a monoaminergic neuromodulatory system that originates from a small
nucleus in the dorsal pons, the locus coeruleus, projecting diffusely to the brainstem,
cerebellum, diencephalon, and neocortex. Several neurocomputational theories of the LC-NE
system activity (Aston-Jones and Cohen, 2005; Bouret and Sara, 2005; Dayan and Yu, 2006;
Yu and Dayan, 2005) bear striking resemblance to some of the ideas put forward in this review
regarding the role of the ventral attention network.

LC neurons exhibit both tonic and phasic activity modes. Tonic activity is low in an unaroused
state that facilitates sleep and disengagement from the environment (Aston-Jones and Bloom,
1981; Rajkowski et al., 1994), moderate when the organism is engaged in a focused task of
high utility and filters out irrelevant stimuli (Usher et al., 1999), and high when the organism
is not committed to a task, is exploring the environment, and there is uncertainty concerning
the proper relationship between stimuli and responses (Aston-Jones et al., 1997) (i.e.,
unexpected uncertainty). Although these transitions in tonic firing of LC neurons occur over
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seconds or minutes, decrements of tonic LC activity have been observed on a shorter timescale
in the period between a warning cue instructing the onset of a trial and a rewarded target
stimulus (Bouret and Sara, 2005). Aston-Jones and Cohen have proposed that LC-NE tonic
signals enable transitions between behavioral states (sleep, focused alert, exploratory) and that
the decrement of tonic activity from an exploratory state to a specific task state reflects the
higher utility associated with the detection of upcoming target stimuli. Accordingly, transitions
between different tonic levels are enabled by cortical inputs from prefrontal regions (anterior
cingulate, orbitofrontal cortex) that heavily project to LC and are sensitive to task context and
reward information.

The second component of LC discharge is the phasic response observed to target stimuli, which
is most strongly generated in the moderate tonic task-focused mode. Interestingly, phasic
responses of LC neurons share many similarities with the P300 target-related cortical evoked
potential, which was previously discussed in relation to the timing of the response in the ventral
attention network (Aston-Jones and Cohen, 2005; Nieuwenhuis et al., 2005). Two different yet
related theories have been proposed to explain the putative function of the LC phasic response
to targets. According to Aston-Jones and Cohen, the phasic response enhances the gain of
neural responses in the complex neural matrix involving sensory, decision, and motor regions
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and therefore speeds up behavioral responses. Importantly, the LC phasic response is thought
to be triggered by pre-frontal inputs only after the sensory evidence for a target has exceeded
a decision threshold in the relevant cortical network, i.e., it is a relatively late postdecision
signal that restricts LC activity to target stimuli (Clayton et al., 2004; Rajkowski et al., 2004),
consistent with the relatively late P300 response to target detection. Alternatively, the phasic
signal has been conceptualized as an interrupt signal (Dayan and Yu, 2006) or as a network
reset signal (Bouret and Sara, 2005) that allows the flexible configuration of a target network
once a target is detected. Bouret and Sara note that this interpretation is consistent with the role
that norepinephrine plays in much simpler organisms. For instance, in the stomatogastric
nervous system of crustacea, synchronized activity from a small number of neuromodulatory
cells can construct ex novo a functional network from neurons otherwise belonging to a
different functional network (Marder and Thirumalai, 2002; Meyrand et al., 1994; Simmers et
al., 1995). The phylogenetic stability of norepinephrine systems from crustaceans to humans
is a powerful argument for stability of function. The Aston-Jones/Cohen theory of the phasic

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LC-NE signal is not necessarily inconsistent with this idea, because the authors note that the
phasic signal effectively reconfigures the target cortical network from a multilayer to a single-
layer network following a decision phase but does not capture the network reset idea.
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We propose a functional relationship between signals of the LC/NE system and activity in the
ventral attention network, both in relation to behavioral transitions (tonic signals) and target
detection (phasic response). The decrease in tonic LC activity during the transition from an
exploratory state to a task-focused state may parallel the deactivation of TPJ, relative to rest,
when subjects engage in a demanding task (Shulman et al., 2003; Todd et al., 2005) (Figure
8). The Aston-Jones/Cohen theory maintains that a decrease in the tonic level of LC activity
promotes engagement on the current task and filtering of distracters, similar to the hypothesis
that the ventral attention network is deactivated under demanding conditions, reflecting a top-
down filtering signal that restricts the network response to a narrow range of task-relevant
stimuli (targets or contingent distracters). Conversely, the hypothesized broad sensitivity to
environmental stimuli during the high tonic activity/exploratory LC mode in the Aston-Jones/
Cohen model may correspond to the ability of any salient stimulus to activate TPJ during
passive viewing or no-task states (Downar et al., 2000). We reviewed evidence above that the
sources of top-down filtering signals into the ventral network are either the dorsal network
through prefrontal cortex (Figures 5C and 2B) or prefrontal regions (anterior cingulate, frontal
operculum; Figure 5C) directly or indirectly through their projection via LC. On the output
side, LC-NE neurons densely projects to inferior parietal cortex and superior temporal gyrus,
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possible homologs of human TPJ (Foote and Morrison, 1987; Morrison and Foote, 1986).
Therefore, as shown in Figure 8, the deactivation of the ventral attention network during
focused attention may be partly caused by a decrement of tonic activity in the LC/NE system.

There is also a striking similarity between the target-related response in the ventral network,
P300 potentials, and the phasic response in the LC (Table 1). All three (ventral network, P300,
LC neurons) show enhanced responses to behaviorally relevant stimuli (targets) in multiple
modalities, relative to distracters, and an enhanced response to low-frequency targets.
Detection of unattended targets (i.e., invalid targets in the Posner cueing paradigm) enhances
both TPJ activity and the amplitude of a late positive potential that may correspond to P300
(Mangun and Hillyard, 1991), while stimuli of high emotional valence modulate P300 and LC
activity. On the response output side, TPJ activity, P300, and LC activity are relatively
independent of response parameters (Astafiev et al., 2006;Clayton et al., 2004;McCarthy and
Donchin, 1981). Finally, both P300 and LC activity can be anatomically linked to TPJ. Lesions
of different parts of the ventral attention network affect different components of P300, with
TPJ damage decreasing both target- and novel-evoked P300 components and prefrontal lesions
affecting the novelty response (Yamaguchi and Knight, 1991b;Verleger et al., 1994;Daffner
et al., 2000). A recent study showed that oddball target responses in TPJ and prefrontal cortex
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were abolished by propranolol, a -adrenergic blocker drug (Strange and Dolan, 2007).

These physiological similarities point to similar functions. The hypothesis that the ventral
attention network is involved in reorienting from one task state to another, either in the
environment or between internally and externally directed activities, is very close to the
network-reset hypothesis of Bouret and Sarah. A network reset or interrupt hypothesis captures
the sensitivity of the ventral attention network to task transitions or unexpected events that may
require the dorsal network to be reconfigured (as in Figures 6B and 7A). Under these conditions,
activity in the dorsal network reflects the reconfiguration of task processes (stimulus and motor
representations) in response to the new contingency, while activity in the ventral network
facilitates rather than initiates this reset or reconfiguration process. We have already discussed
that activity in the ventral network, as indexed by the P300, may not be sufficiently fast to
initiate a reorienting response. A similar argument applies to the LC-NE system, which has a
relatively long latency to a stimulus (~100150 ms) and a slow transmission of its output to

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the cortex (~50100 ms). In the context of a nonlinear dynamic system, the highly synchronized
LC-NE activation of the ventral network may allow the dorsal network to switch to or settle
into another state more appropriate for the new environmental situation (Serences and Yantis,
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2006).

While the adaptive-gain theory of Aston-Jones and Cohen is concerned with the role of LC/
NE activity in categorization and responding to attended targets, an interrupt/reset/reorienting
framework includes other situations discussed above, such as stimulus-driven shifts of
attention, transitions between rest and an extended task period, and detection of event
boundaries.

The disruption of a reset signal may impair shifting between objects or events in the
environment and thus underlie nonlateralized attentional impairments after damage of ventral
frontal and temporoparietal cortex (Husain and Rorden, 2003), such as poorer detection or
identification of targets in both visual fields (Duncan et al., 1999; He et al., 2007a; Peers et al.,
2005), problems with vigilance (Heilman et al., 1987b; Robertson, 2001; Wilkins et al.,
1987), and an extended attentional blink (Husain et al., 1997; Shapiro et al., 2002). Moreveor,
impaired interactions between the ventral and dorsal attention network (Corbetta et al., 2005;
He et al., 2007a) produce activity imbalances in parietal spatial maps that result in a tonic
attentional bias toward the ipsilesional field. Transient increases in vigilance improve spatial
attention and perception (Robertson, 2001; Robertson et al., 1998), presumably through an
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augmentation of LC-NE output that leads to a more normal interaction between the two
networks.

Future Directions
This review of the function of the ventral attention network suggests several novel avenues for
future investigation. It is important to know the timing of the activation of ventral and dorsal
networks on timescales that are closer to the underlying neural signals and whether temporal
codes such as synchronization and coherence link widely separate neuronal populations during
selection and behavioral reorienting. The recent combination of fMRI and EEG/MEG methods,
as well as the integration of TMS/fMRI and EEG, should provide important information on
timing and causal interactions between areas. Also, the evolutionary precursors of the ventral
attention network and its right hemisphere lateralization could be uncovered by neuroimaging
and single-unit studies of primates. An ongoing and critical issue is the relationship between
different attentional functions and neuromodulatory systems, especially noradrenaline,
acetylcholine, and dopamine, for which there is already strong evidence of a role in attention
and learning. Finally, further exploration into human pathologies, both focal (e.g., stroke) and
nonfocal (e.g., traumatic brain injuries, attention-deficit disorders), using cognitive
NIH-PA Author Manuscript

neuroscience models of attention, may lead to a better theory of these debilitating conditions.

Acknowledgements
This work was supported by the J.S. McDonnell Foundation, the National Institute of Neurological Disorders and
Stroke (R01 NS48013), the National Institute of Mental Health (R01 MH71920-06), and a Marie Curie Chair European
Union (MEXC-CT-2004-006783). We thank Jan De Fockert, Emiliano Macaluso, John Serences, Ren Marois, Vinod
Menon, Devarajan Sridharan, Nikos Dosenbach, Steve Petersen, Jean Decety, Jason Mitchell, Kevin A. Pelphrey, and
Gary Aston-Jones for generously providing illustration of their results. We would like also to thank James Bisley,
Christos Constantidinis, Ron Mangun, and Joe Hopfinger for helpful discussions.

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Figure 1. Focusing Attention and Reorienting Attention Recruit Interacting Networks

(Left panel) Focusing attention on an object produces sustained activations in dorsal fronto-
parietal regions in the intraparietal sulcus, superior parietal lobule, and frontal eye fields, as
well as visual regions in occipital cortex (yellow and orange colors) but sustained deactivations
in more ventral regions in supramarginal gyrus and superior temporal gyrus (TPJ) and middle
and inferior prefrontal cortex (blue and green colors). (Right panel) When an unexpected but
important event evokes a reorienting of attention, both the dorsal regions and the formerly
deactivated ventral regions are now transiently activated.
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Figure 2. Definition of Dorsal and Ventral Networks from Activation Data and Putative
Interactions
(Top panel) Results from a meta-analysis of activation data. Regions in blue are consistently
activated by central cues, indicating where a peripheral object will subsequently appear or what
is the feature of an upcoming object. Regions in orange are consistently activated when
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attention is reoriented to an unexpected but behaviorally relevant object. (Bottom panel) Model
for the interaction of dorsal (blue) and ventral (orange) networks during stimulus-driven
reorienting. Dorsal network regions FEF and IPS send top-down biases to visual areas and via
MFG to the ventral network (filtering signal), restricting ventral activation to behaviorally
important stimuli. IPS-FEF are also important for exogenous orienting. Overall, the dorsal
network coordinates stimulus-response selection. Conversely, when a salient stimulus occurs
during stimulus-driven reorienting, the ventral network sends a reorienting signal to the dorsal
network through MFG.

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Figure 3. Functional Connectivity Defines Separate Dorsal and Ventral Networks

(Top panel) Four dorsal frontoparietal regions from the meta-analysis of activation studies
shown in Figure 2 were used as seeds in an FC analysis of resting-state data. The map indicates
regions that showed significant positive correlations with three (red) or four (yellow) of the
seed regions. The dorsal network is largely reproduced in the resting-state FC maps. Regions
that show significant negative correlations with three (green) or four (blue) of the seed regions
are also shown and roughly reproduce the default network, possibly indicating a push-pull
relationship between the two networks. (Bottom panel) Five ventral regions from Figure 2 were
used as seeds for an FC analysis. Regions showing consistent positive correlations largely
reproduce the ventral network, but negative correlations in default regions are not observed.
The black arrow indicates that posterior MFG near the inferior frontal sulcus appears to be
connected to both networks.
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Figure 4. Ventral Network Activity Is Restricted to Task-Relevant Stimuli

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(A) Exogenous orienting does not activate TPJ. Subjects saw a color singleton (exogenous cue)
or a heterogeneous colored array (neutral cue) followed by a target (cue and cue period in light
blue). Behavioral performance was speeded when the target location matched the singleton
location, even though the cue and target locations were random. The time course of the BOLD
signal shown in the graph indicates that R FEF (see A in the surface-rendered brain) showed
a larger response for exogenous than neutral cues. In contrast, SMG showed a small
deactivation during the cue period, followed by a small activation when the cue period ended
(Kincade et al., 2005).
(B) Salient irrelevant distracters influence the dorsal, not ventral, system. Subjects categorized
the orientation of a line within a singleton shape (the circle). Salient but irrelevant singleton
color distracters that impaired behavioral performance activated dorsal region SPL (see B
in brain) rather than TPJ (de Fockert et al., 2004).
(C) Unattended stimuli only activate TPJ if they are task relevant, not if they are irrelevant,
even though they have high sensory salience. A task-relevant unattended letter activated
angular gyrus and inferior frontal gyrus (see C in brain), but no responses were seen to the
unattended but highly salient checkerboard. The angular gyrus response may reflect the
combined activation of dorsal (IPS/SPL) and TPJ regions (Indovina and Macaluso, 2007).
(D) Distracters only activate TPJ if they share features with a target, indicating a strong effect
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of task relevance. Subjects identified red foveal letters while ignoring irrelevant peripheral
letters. Peripheral letters that matched the target color interfered with performance and
activated TPJ, while non-target-colored letters had no effect (D in brain) (Serences et al.,
2005).

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Figure 5. TPJ Activity Is Suppressed during Focused Attention

(A) Subjects searched a rapid serial visual presentation (RSVP) display for a target digit. The
number of distracter frames containing only letters prior to the target frame containing the
target was varied. The graph shows the time course of activity in dorsal regions IPS and FEF
and ventral region TPJ under conditions in which the target appeared near the end of the trial.
In TPJ, a deactivation to the letter distracters was followed by an activation when the digit was
presented or the trial was terminated. Interestingly, the deactivation to the letters was
significantly greater when the subsequent digit was detected than when it was missed.
Conversely, IPS and FEF showed sustained activations during search (Shulman et al., 2003).
(B) Subjects encoded a visual display that they had to remember and then match to a probe
display. During the retention interval, TPJ showed a deactivation (purple disk in the surface-
rendered brain) that increased with the number of display items that had to be retained (Todd
et al., 2005).
(C) The statistical map shows regions with sustained activity as subjects searched through letter
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distracters in the RSVP experiment (see panel [A]), including dorsal attention regions IPS and
FEF (red/orange in surface-rendered brain) but also regions in anterior insula and anterior
cingulate that form a putative task-control network (Dosenbach et al., 2006). These regions
may send top-down signals (see arrows) to the ventral network, which showed sustained
deactivations during search (blue/green in surface-rendered brain), restricting its input to task-
relevant objects (Shulman et al., 2003).

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Figure 6. Interaction of Dorsal and Ventral Attention Networks

(A) The surface-rendered brains show the damaged right hemisphere regions (in dark gray) of
a stroke patient with spatial neglect. The bottom graph shows the time course of BOLD activity
in undamaged regions of IPS, with the green and red lines indicating, respectively, the time
series for the indicated left and right IPS regions. Time courses from these regions are shown
for a healthy subject, for the stroke patient immediately following the stroke, and for the same
patient following recovery. While the healthy subject and the recovered stroke patient show
highly correlated interhemispheric IPS activity, the same patient immediately after the stroke
shows activity that is much less correlated. Therefore, damage to ventral regions, possibly
including white matter tracts, impairs physiological interactions between undamaged dorsal
regions (He et al., 2007a).
(B) The surface-rendered brains show ventral (left) and dorsal (right) regions that are activated
when the completion of a symphonic movement is detected. The time courses indicate that
ventral activations (red lines) preceded the dorsal activations (blue lines), while a Granger
Causality analysis of these regions indicated that ventral activity predicted dorsal activity
(Sridharan et al., 2007).
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Figure 7. Common Activation of TPJ during Reorienting, Task Transitions, and Social Cognition
(A) Regions in green show transient activity at the transition between a rest period and the
onset of an extended block of trials (see time course in inset, indicating that both onsets and
offsets are often observed). Start cue activity is observed within some ventral and dorsal
regions, indicating the involvement of both networks in task transitions (Dosenbach et al.,
2006).
(B) A meta-analysis of activations across studies measuring reorienting and various aspects of
social cognition. Largely similar TPJ activity is observed across paradigms, with perhaps a
more posterior extension of activity in the social cognition paradigms (Decety and Lamm,
2007).
(C) A within-subject comparison of reorienting and ToM paradigms revealed that both
activated very similar TPJ regions (Mitchell, 2007). The bar graph shows the magnitude of the
TPJ activation in the two paradigms. A large deactivation was observed in the control false-
photograph condition with a significantly smaller deactivation in the experimental ToM
false-beliefs condition. The reorienting paradigm yielded event-related activations that were
larger during trials with invalid than valid cues. The blue and orange regions are taken from
the meta-analysis of the dorsal and ventral networks in Figure 2.
(D) Gaze perception activates superior temporal regions. The graph shows the time course of
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activity when another person makes or averts eye contact with the observer. Mutual gaze
enhances the activation (Pelphrey et al., 2004).

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Figure 8. Relationship between Activity in TPJ and Locus Coeruleus/Noradrenergic System

The surface-rendered brains show fMRI BOLD activations and deactivations relative to when
subjects are fixating in an otherwise blank field (i.e., the baseline, left panel), when searching
through letter distracters of an RSVP display (middle panel, ventral network is deactivated,
dorsal network is activated), and when detecting a digit target in the display (right panel, both
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networks are activated along with other regions) (Shulman et al., 2003). The bottom panel
shows spiking activity in monkey locus coeruleus neurons during analogous periods: an
inattentive period in which a task is poorly performed and tonic activity is high, an attentive
period in which the task is performed well and tonic activity is decreased, and target detection,
which produces a phasic increase in activity (Usher et al., 1999). The inset trace shows event-
related potentials recorded from the scalp of a human when a target is detected in a completely
separate experiment, with the large positive deflection indicating the P300.
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Table 1
Ventral Attention Network/P300/LC Activity

Inputs TPJ/VFC P300 LC Phasic

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Target > passive + + +

Multimodal response (visual, auditory, tactile) + + +
Stimulus probability (low > high) + + +
Orienting to unattended stimuli (invalid > valid) + +(IIN) ?
Orienting to contingent distracters (relevant > irrelevant) + +(IIN) ?

Output

Independence from motor/response parameters + + +

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