Attention

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Neuron. Author manuscript; available in PMC 2016 October 07.
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Published in final edited form as:

Neuron. 2015 October 7; 88(1): 127–144. doi:10.1016/j.neuron.2015.09.017.
From behavior to neural dynamics: An integrated theory of

attention
Timothy J. Buschman and Sabine Kastner
Princeton Neuroscience Institute, Department of Psychology, Princeton University, Princeton, NJ
08544
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Abstract
The brain has a limited capacity and therefore needs mechanisms to selectively enhance the
information most relevant to one’s current behavior. We refer to these mechanisms as ‘attention’.
Attention acts by increasing the strength of selected neural representations and preferentially
routing them through the brain’s large-scale network. This is a critical component of cognition and
therefore has been a central topic in cognitive neuroscience. Here we review a diverse literature
that has studied attention at the level of behavior, networks, circuits and neurons. We then
integrate these disparate results into a unified theory of attention.
Introduction
Over 125 years ago, William James defined attention as the “taking possession by the mind
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… of one out of what seem simultaneously possible objects or trains of thought” (James,
1890). James’ intuitive understanding of attention is remarkably close to our modern
definition: attention is the selective prioritization of the neural representations that are most
relevant to one’s current behavioral goals. Such prioritization is necessary because the brain
is a limited capacity information system. Representations of external stimuli and internal
thoughts compete for access to these limited processing resources, and attention helps to
resolve that competition in favor of the information that is currently task-relevant.
Attention research has been central to the fields of cognitive neuroscience, psychology and
systems neurophysiology. This has led to the discovery of a large number of attention effects
at each of these levels of observation. In the first three sections, we briefly review this
literature, highlighting key insights at the behavioral, network, and neuronal levels. Our goal
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for this review is to integrate these disparate findings into a single unified framework, which
we outline in the fourth section.
We should note that we will largely constrain our review to visual attention, as it has been
the best studied. We acknowledge the importance of extending our understanding to other
Correspondence to: TJB ([email protected]) and SK ([email protected]).

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Buschman and Kastner Page 2
sensory modalities and to interactions between modalities and we hope the knowledge
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gained from understanding visual attention will reveal principles of neural processing that
may be fundamental to cognition more generally.
Furthermore, even though attention is often studied in isolation, a mechanism that prioritizes
task-relevant information will likely interface with many cognitive domains such as action
control and decision making, motivation and emotions, memories at different time scales,
and awareness. We will review our current knowledge of some of these interactions in the
last section. Understanding the interaction of selective attention with other cognitive
domains will ultimately lay the foundation for reaching a cohesive understanding of the
general principles of cognition and their associated neural mechanisms (2014).
Behavioral effects - Building blocks and shifting concepts

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Classical attention paradigms

The two most commonly used paradigms to study visual attention are visual spatial orienting
(Posner et al., 1980) and visual search (Treisman and Gelade, 1980).
In spatial orienting tasks, subjects are instructed by a predictive cue to direct attention to a
particular spatial location where they must detect or discriminate a target stimulus. The
classic finding is that subjects benefit from the cue as they respond faster and more
accurately to stimuli occurring at the cued location than to stimuli occurring at other
locations. This facilitation comes at the expense of other objects in the visual environment,
reflecting the competitive nature of attention.
While orienting tasks typically involve only a single target stimulus, visual search tasks
more closely relate to our everyday experience, where we typically face cluttered scenes. In
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search tasks, subjects are given an array of stimuli and asked to find a particular target
stimulus defined by one or more features in the array (e.g. find the green ‘T’ in an array of
green and blue ‘T’s and ‘L’s; see Figure 1A). Hence, in visual search, the selection process
is informed by features of the target (i.e. feature-based attention), which then guides spatial
attention.
Performance on visual search tasks is affected by how many features the target shares with
other stimuli in the array. If the target has a unique feature, such as being of different color
from the distracters, the search is completed quickly and effortlessly, regardless of the
number of elements in the array. This phenomenon is known as ‘pop-out’ or efficient
(parallel) search. However, just by changing the distractors in the search array, the search for
the same target can be made much more difficult. For example, if the target is defined by a
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conjunction of features that each are shared by distracters (as in Figure 1A), search time
increases as a function of the number of elements in the array. This is known as inefficient
search and the increase in search times is thought to reflect a serial target search, which is
mediated by a spatial ‘spotlight’ mechanism that can shift from location-to-location about
every 50 ms (Buschman and Miller, 2009; Wolfe et al., 2011). However, under some
circumstances, only a subset of the array needs to be searched. Simple features, such as
color, can be used to guide search to just those elements that share a particular target feature

(Wolfe et al., 1989). Search difficulty also depends on the similarity of the target to the
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distracters and to the dissimilarity of the distracters to each other (Duncan and Humphreys,
1989).
The results of studies using classical attention paradigms have shaped our current theoretical
concepts and have been foundational for investigations at the neural level that we will
review below. However, attention mechanisms have evolved to function in real-world
scenarios. Recently, there has been a growing number of studies that have asked whether the
knowledge and concepts gained from simplified laboratory conditions translate to more
ecologically relevant situations.
Real-world visual search

An important first step to investigate attentional prioritization under more naturalistic
conditions has been to study the selection of categorical object information from natural
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scenes (for an in depth review, see Peelen and Kastner, 2014). In daily life, we select
meaningful objects from meaningful scenes such as looking for cars when crossing a street.
What would be the behavioral prediction for detecting a car in the scene of Figure 1B based
on classic search paradigms? Typical scenes contain dozens of distracter objects with highly
variable appearance, and there is not one feature that uniquely defines a target. Based on
classical attention theories one would predict a long response time reflecting a particularly
inefficient search. However, the opposite is the case. The detection of familiar object
categories in scenes is extremely rapid (Thorpe et al., 1996) and search is highly efficient –
adding additional items to a scene has little cost (Wolfe et al., 2011). Furthermore, one can
accurately perform such real-world search tasks while simultaneously performing a second,
demanding attention task at fixation (Figure 1C; Li et al., 2002). This suggests that real-
world search of object categories does not require focused spatial attention.
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Neuroimaging studies in humans have begun to investigate the neural basis of real-world
search by having subjects detect the presence of objects from a target category in briefly
presented photographs (Peelen and Kastner, 2011; Peelen et al., 2009), or short movie
segments (Çukur et al., 2013). It was found that the pattern of neural activity in object-
selective cortex evoked by the scenes fully depended on task-relevance: target objects
embedded in natural scenes were only represented when one was actively searching for
them. Responses in many parts of the brain increased with the appearance of a stimulus in
the target category, or a semantically similar category, suggesting that category-based
attention may have widespread influences on brain activity. Together, these results provide
neural evidence that the attentional selection mechanism that biases the processing of scenes
acts at the level of natural categories. Future work is needed to extend our traditional
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concepts of attention to incorporate mechanisms that are optimized for naturalistic

conditions. Key to this will be the development of appropriate paradigms in animal models
in order to study the underlying neural mechanisms in greater detail.
Rhythmic properties of selective attention

Classic attention theories (Posner et al., 1980; Treisman and Gelade, 1980) propose a unique
and indivisible ‘spotlight’ of attention that highlights a selected item. To process an entire

scene, this spotlight was thought to be continuously moving from location-to-location,

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shifting at a rate of approximately 20 Hz (Wolfe et al., 2011). Previous studies suggested

that this shifting may be regular, moving the spotlight of attention in a rhythmic fashion
around a visual scene (Buschman and Miller, 2009). Surprisingly, recent evidence shows
that even when this spotlight is sustained at one location, it is not static, but rather appears to
flash rhythmically. Using EEG, Busch and VanRullen (2010) demonstrated that the
detection of a visual target at threshold was systematically related to the phase of an ongoing
theta oscillation (~7 Hz). This phase-behavior relationship was contingent on the allocation
of attentional resources following a cue and was absent at other locations in the visual field.
The cue served not only to guide the deployment of attention, but caused the timing of the
high- and low-excitability states of the oscillation to align across trials (see also Lakatos et
al., 2009). Thus, it appears that the selection mechanism periodically samples the attended
location, with the degree of selection fluctuating with the phase of the neural rhythm.
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Intriguingly, recent behavioral studies suggest that there may be at least two concurrent
spatial mechanisms: the first is the ‘classic’ focusing of attention at a selected location,
while the second mechanism rhythmically monitors other locations outside this focus
(Figure 1C; Fiebelkorn et al., 2013; Landau and Fries, 2012). Such rhythmic monitoring of
other locations and objects may be an important mechanism for flexibly gating the
reallocation of attentional resources. It is important to note that the rhythmic monitoring
appears to be an automatic process that is distinct from voluntarily splitting or dividing
attentional resources across multiple locations. Together, these findings suggest that
selective attention falls into the class of rhythmic behaviors and is a highly dynamic and
flexible resource. The neural basis of the rhythmic properties of selective attention is unclear
and awaits future investigation.
Studies based on careful observations of behavior have provided the foundation not only for
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theoretical accounts of selective visual processing, but also for the investigations that are
aimed at revealing its underlying neural mechanisms, as we will discuss next.
Network effects – from functional anatomy to dynamic connectivity

In the primate brain, attentional selection is mediated by a large-scale network of regions,
including the frontal, parietal, temporal and occipital cortex as well as thalamic and
midbrain regions (Corbetta and Shulman, 2002; Ungerleider and Kastner, 2000). In this
section, we will review the functional anatomy of the primate attention network, and its
major dissociations of function. We will particularly focus on dynamic network interactions
that ultimately drive the selection process and its associated specific behavior. This is not a
perceptual deficit as subjects will respond if competing stimuli from the unaffected
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hemifield are removed.
Defining the visual attention network

Early evidence that attentional selection involves a distributed large-scale network comes
from neuropsychological studies of human patients showing that unilateral brain lesions,
especially of higher-order cortex, may cause impairment in spatially directing attention to
the contralateral hemifield. This syndrome is known as visuospatial hemineglect. In severe
cases, patients suffering from neglect will completely disregard the visual hemifield

contralateral to the side of the lesion (e.g. Bisiach and Vallar, 1988). This leads to deficits in
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everyday behaviors; patients will read from only one side of a book, apply make-up to only
one half of their face, or eat from only one side of a plate.
Visuospatial neglect may follow unilateral lesions at different sites, including most
frequently the temporo-parietal junction (Mort et al., 2003) and superior temporal cortex
(e.g. Karnath et al., 2001). Neglect is also, but less frequently observed following damage of
the frontal lobe (e.g. Damasio et al., 1980), the anterior cingulate cortex (e.g. Janer and
Pardo, 1991), other sites in parietal cortex such as the superior parietal lobule (Kenzie et al.,
2015), the basal ganglia (e.g. Damasio et al., 1980), and the thalamus, in particular the
pulvinar (e.g. Karnath et al., 2002). The syndrome is not confined to cortical lesions, but can
also result from white matter lesions that affect structural connections between nodes of the
attention network (Lunven et al., 2015). Importantly, neglect occurs more often with right-
sided lesions than with left-sided lesions, which has been taken as evidence for a specialized
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role of the right hemisphere in attentional selection. This observed hemispheric asymmetry
led to the ‘hemispatial’ theory which proposes that the right hemisphere directs attention to
both visual hemifields, whereas the left hemisphere directs attention to the right visual field
only (Heilman and Van Den Abell, 1980). Thus, while left hemispheric damage can be
compensated for by the right hemisphere, such compensation will not be possible with right
hemispheric damage, thereby resulting in neglect of the left visual field.
Human neuroimaging studies of the intact brain have provided a more detailed account of
the neuroanatomy of the attention network. When subjects attend to a location in space in
anticipation of the appearance of a stimulus, neural signals increase in a fronto-parietal
network consisting of regions within the superior parietal lobule (SPL), the intraparietal
sulcus (IPS), the frontal eye field (FEF), and the supplementary eye field (SEF; see Figure
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2A for full map). This dorsal fronto-parietal attention network has been implicated in many
visuospatial tasks, regardless of whether target stimuli were detected, discriminated or
tracked in visual space (Ungerleider and Kastner, 2000) and regardless of whether the task
required spatial attention, spatial working memory, or planning saccades (Jerde et al., 2012).
The fronto-parietal attention network is also activated when subjects select non-spatial
information. In studies of feature-based attention, similar activations have been found when
subjects shift attention from one feature to another (e.g. from color to direction of motion in
a display of colored, moving dots; (Greenberg et al., 2010), or when subjects shift attention
between two spatially overlapping objects and perform object-based selections (Serences et
al., 2004). Together, these studies suggest that the fronto-parietal network is a ‘domain-
general’ controller without much functional specialization. However, it is not clear whether
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distributed subpopulations within this network subserve specific functions needed for
space-, feature-, or object-based attentional control. The different neural mechanisms
associated with the different selection modes (as described below in our theory section) may
suggest such a functional organization.
It is important to note that the fronto-parietal network consists of a large number of

topographically organized areas that coordinate their functional operations (Figure 2A).
Thus far, nine topographically organized areas have been found in posterior parietal and

frontal cortex, each containing a continuous representation of the contralateral visual field
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(for review, Silver and Kastner, 2009). The delineation of topographic organization in
higher-order cortex in individual subjects has permitted a more systematic study of the
dorsal attention network in the human brain.
In line with the topographic organization, spatial attention increased responses more
strongly when directed contra- rather than ipsilaterally (Szczepanski et al., 2010), thus
generating a contralateral spatial biasing signal in each topographic region. The sum of the
biasing signals across areas was of similar magnitude across the two hemispheres,
suggesting a balanced spatial control system in the intact brain. Thus, visual space within a
hemifield appears to be largely controlled by the contralateral hemisphere, contradicting the
hemspatial theory of attention control. Instead, these studies have provided evidence for an
alternative model of neglect, first proposed by Kinsbourne (1977). According to this
‘interhemispheric competition account’, spatial attention uses an opponent processor control
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system, in which each hemisphere directs attention towards the contralateral visual field. In
an intact system, the two hemispheric processors are balanced through mutual reciprocal
inhibition, possibly through direct callosal connections, or through cortico-subcortical
interactions of parietal cortex and superior colliculus. The interhemispheric competition
account of attention control has received further empirical support in transcranial magnetic
stimulation studies showing that attentional biasing signals can be altered in predictable
ways by perturbing the frontoparietal control system (Szczepanski and Kastner, 2013).
While Kinsbourne’s original model was not able to account for the right hemispheric
dominance observed with the neglect syndrome, the functional brain imaging studies in the
intact brain have shown several asymmetries in the strengths of attentional biasing signals
across the nodes of the dorsal attention network (Sczcepanski et al., 2010). These
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asymmetries can theoretically account for the observed right hemispheric dominance.
Further support for the Kinsbourne model comes from clinical studies in patients suffering
from hemi-neglect following a stroke to the right superior temporal cortex, who show
reduced activity in the right relative to the left dorsal parietal attention network, even though
these brain regions are structurally intact (Corbetta et al., 2005). Thus, the attentional
deficits observed in these patients may be explained by a distal impact of the lesion. This
results in an imbalance of attentional biasing signals generated by each hemisphere and,
thus, an imbalance in the ability to control contralateral space. This imbalance is also
accompanied by a breakdown of functional connectivity within the dorsal network between
the two hemispheres (He et al., 2007).
Functional dissociations of the network

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Thus far we have highlighted the distributed nature of attentional processing, which is
mediated by the strongly interconnected anatomy of the brain, thereby ensuring that any
information is quickly shared between regions. In this framework, computations and
behavior do not arise from a single brain region but rather emerge through interactions
between regions. However, this does not imply that each brain region does exactly the same
computation. There are important functional dissociations that can be drawn between
regions.

One broad functional dissociation that has been made is that higher-order fronto-parietal
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cortex acts as the ‘source’ of modulatory attention-related signals that are fed back to
sensory cortex. This dissociation was observed in early human neuroimaging studies
showing that when attention was directed to the location of an upcoming stimulus, activity
in frontal and parietal cortex was sustained relative to activity in visual cortex, reflecting the
attentional operations of the task and not sensory processing (Figure 2C; Kastner et al.,
1999). To understand the different contributions of frontal and parietal cortex in controlling
attention, we will now turn to electrophysiological studies in non-human primates.
The large-scale fronto-parietal attention network seen in humans is generally conserved in

non-human primates. For spatial selection, important parts of the network include frontal
cortex (lateral prefrontal, lPFC, and the frontal eye fields, FEF) as well as a region within
the intraparietal sulcus (lateral intraparietal area, LIP). In addition, a recent neuroimaging
study has shown evidence for a role of medial posterior parietal cortex including areas V6
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and V6A in mediating dynamic shifts of attention across the visual field (Premereur et al.,
2015). Shifts in attention are reflected in single neuron responses in all of these regions (e.g.
FEF, Bichot and Schall, 1999; LIP, Bisley and Goldberg, 2003).
What then distinguishes these regions? To answer this question, Buschman and Miller
(2007) used large-scale, multiple electrode recording techniques to simultaneously record
the activity of neurons in lPFC, FEF, and LIP. They found that, when a monkey’s attention
was externally captured by a salient stimulus (i.e. by a ‘pop-out’ stimulus, see above), this
was reflected first in LIP neurons and then in FEF neurons, suggesting a flow of information
from parietal to frontal cortex. In contrast, when attention was internally directed by the
memory of the target stimulus (i.e. during a conjunction search), such voluntary control of
attention originated in frontal cortex, and information flowed back to parietal cortex. Similar
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results have recently been found in humans (Li et al., 2010).
These results suggest that frontal and parietal cortex play different roles in guiding attention.
First, parietal cortex (LIP) encodes a ‘saliency’ map of the visual scene, encoding which
locations in space are of potentially high significance. Such saliency is largely defined by
the properties of the stimuli. Consistent with this model, LIP neurons will respond to a
highly salient, transiently flashed stimulus (Bisley and Goldberg, 2006) and encode the
saliency of stimuli in a visual scene (Arcizet et al., 2011). In contrast, neurons in frontal
cortex carry information about task-relevant stimuli, not necessarily the most salient
stimulus (Hasegawa et al., 2000). Furthermore, inactivating lateral PFC disrupts tasks
requiring top-down, internal direction of attention (Iba and Sawaguchi, 2003).
Further evidence that prefrontal cortex is the source of top-down signals comes from the
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work of Moore and colleagues, who found that electrical stimulation of the frontal eye fields
(FEF) can induce attention-like effects. Stimulation of FEF increases the animal’s
behavioral discriminability at the location of the FEF receptive fields, as if attentional
resources had been directed there (Moore and Fallah, 2004). Furthermore, attention-like
effects were observed in V4 neurons whose receptive fields overlapped with the stimulated
FEF neurons (Figure 2D; Moore and Armstrong, 2003). Causal manipulations in humans

using TMS have corroborated these findings by showing qualitatively similar effects (Ruff
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et al., 2006).
Dynamic functional connectivity

Despite these functional dissociations, it is clear that the fronto-parietal network works as a
cohesive unit to direct attention based on a multitude of factors. This then raises the question
– how can one network dynamically adapt to changing requirements as the situation or goals
change? More globally, how might the fronto-parietal network induce attention by biasing
connections throughout the brain? This isn’t likely due to anatomical changes; changes in
behavior simply happen too quickly. Instead, changes in the effective connectivity between
interconnected regions allows for the large-scale network to adapt as needed.
Changing the synchrony of neurons is one mechanism that may modulate effective
connectivity. Theoretical and experimental work has shown that increasing the synchrony of
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inputs into a single neuron has a super-additive effect (Azouz and Gray, 2000; Salinas and
Sejnowski, 2001). Therefore, modulating the synchrony of a population of neurons will
dynamically change their downstream impact. Therefore, one way to increase the strength of
an attended stimulus would be to increase the synchrony of neurons representing that
stimulus. Early experimental support for such a model came from the somatosensory
system, where Steinmetz and colleagues (2000) found that attending to tactile stimuli
increased the synchrony of neurons. Studies on visual attention showed that neural
synchrony increased in a highly specific way, that is, attention increased the high-frequency
(40–80 Hz) synchronous oscillations and decreased the low-frequency (<10 Hz) oscillations
in populations of neurons representing the attended location (Fries et al., 2001; Womelsdorf
et al., 2006a).
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In addition to boosting the effectiveness of local neuronal populations, increasing synchrony

between brain regions may also change inter-areal effective connectivity. As we detail
below in the section on an integrated theory of attention, oscillations in population activity
likely reflect the ebb-and-flow of inhibition in a local network. Therefore, aligning such
oscillations across regions could ensure that populations of neurons in inter-connected
regions will be in a co-excitable state, which is one possible way to boost effective
connectivity (Figure 3A; Bressler, 1996; Fries, 2005). There is growing evidence for such a
model (Buschman and Miller, 2007; Gregoriou et al., 2009a; Saalmann et al., 2007; Siegel et
al., 2008). In particular, a recent study by Fries and colleagues demonstrated that synchrony
between regions can be highly selective, acting on a single visual object (Bosman et al.,
2012). By recording simultaneously from populations of V1 neurons with receptive fields
encompassing one of two stimuli as well as from V4 neurons whose receptive field
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overlapped both stimuli (Figure 3B, middle), they showed that, when attention was directed
to a single stimulus, gamma-band oscillations were selectively synchronized between V4
and only those V1 neurons that encoded the attended stimulus location (Figure 3B, left and
right).
These effects of synchronization are not limited to visual cortex or specifically to the gamma
frequency band. Buschman and Miller (2007) found that synchrony between prefrontal and
parietal cortex differed depending on whether attention was being externally captured by a

salient stimulus or internally directed based on a remembered target (Figure 3C). When
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attention was externally captured and information flowed in a bottom-up manner (from
parietal cortex to prefrontal cortex), synchrony was observed at gamma-band frequencies
(the same frequency found in visual cortex). In contrast, when attention was internally
controlled, and information flowed ‘top-down’ from prefrontal to parietal cortex, synchrony
between prefrontal and parietal cortex was at a lower-frequency ‘beta’ band. These results
suggest that attention modulates synchrony between brain regions in order to guide
information flow between regions in a task-specific manner. Furthermore, these results
provided the first evidence that specific frequency bands might serve specific purposes:
beta-band oscillations may increase ‘top-down’ signaling while gamma-band oscillations
increase ‘bottom-up signals.
Importantly, communication in cortical large-scale networks is not only mediated through

cortico-cortical interactions, but also through thalamo-cortical interactions. In particular,
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there is growing evidence that the pulvinar, the largest nucleus in the primate thalamus,
plays a key role in attention. The pulvinar is considered a higher-order thalamic nucleus,
because it forms input-output loops almost exclusively with the cortex, thereby forming
cortico-thalamo-cortical pathways. As a general principle, directly connected cortical areas
will be indirectly connected via the pulvinar (Jones, 2001; Shipp, 2003). This indirect
connectivity may be used to facilitate information transfer between cortical areas. During
spatial selection, increased synchrony of slow frequency oscillations in the alpha band
between two interconnected visual cortical areas (V4 and TEO) resulted from pulvino-
cortical rather than cortico-cortical communication (Figure 3D; Saalmann et al., 2012). In
addition, these slow oscillations were coupled to higher frequency oscillations in the gamma
band in each cortical region. Such cross-frequency coupling may be an effective mechanism
for coordinating long-range communication across a network, with lower frequency
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oscillations controlling the excitability of local neural populations in order to facilitate the
coupling of higher frequency oscillations (Canolty et al., 2006; Lakatos et al., 2008). This
mechanism may provide a bridge between cortico-cortical and thalamo-cortical mechanisms
for large-scale communication. These studies have begun to provide a mechanistic
framework for behavioral observations showing that pulvinar lesions or inactivations impair
orienting responses and the exploration of visual space (Ward et al., 2002; Wilke et al.,
2010).
Thus far, we have highlighted the dynamic nature of attention. Behaviorally, attention can
be internally or externally controlled and even when ‘statically’ maintained, it vacillates
between locations. This is reflected in the dynamic nature of attentional signals across the
fronto-parietal network, including recent evidence that synchrony within and between brain
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regions may sculpt information flow. Next, we discuss how attention acts on the sensory
representations themselves.
Neuronal effects – from single neurons to populations

When attention is allocated to a spatial location, feature, or object, its neural representation
is enhanced relative to when attending elsewhere. This enhancement occurs in many

different ways, ranging from changes in the responses of single neurons to changes in the
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dynamics of populations of neurons.
Spatial attention enhances neural responses

In one of the first studies probing attention effects in the primate brain, it was reported that
directing spatial attention into the receptive field of a single parietal cortex neuron increased
its response to a stimulus (Bushnell et al., 1981). Since then, studies in monkeys and humans
have shown that spatial attention increases neural responses to a selected stimulus across
many levels of processing. This includes cortical visual areas, such as V1, V2, V4, MT,
MST, and IT (e.g. Chelazzi et al., 1993; Luck et al., 1997; Spitzer et al., 1988; Treue and
Maunsell, 1999), as well as subcortical regions such as the lateral geniculate nucleus,
pulvinar, reticular nucleus of the thalamus, and superior colliculus (McAlonan et al., 2006;
O’Connor et al., 2002; Zénon and Krauzlis, 2012). The magnitude of the spatial attention
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effect increases along the cortical hierarchy, reaching its strongest effect in associative
regions, such as prefrontal and parietal cortex (Rainer et al., 1998). Similarly, spatial
attention effects seem to occur first in higher cortical regions and then cascade backwards
(Buffalo et al., 2010). However, spatial attention does not simply increase the response rate
of neurons but also increases a neuron’s sensitivity to stimuli. For example, spatial attention
shifts the contrast-response function of single neurons in V4 and MT such that a neuron is
more sensitive to low contrast stimuli (Figure 4A, Martínez-Trujillo and Treue, 2002;
Reynolds et al., 2000). By increasing the neuronal sensitivity the perceived contrast of a
stimulus can be increased due to attentional allocation, thus improving behavioral
performance (Carrasco et al., 2004).
Attending to features
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As noted above, attention can not only be directed to a specific location, but also to a
stimulus feature. Such featural attention influences single neuron responses in much the
same way as spatial attention, increasing the sensitivity of neurons that respond
preferentially to stimuli matching the sought-after feature (in V1 and V4, Haenny and
Schiller, 1988; in MT, Treue and Trujillo, 1999). Similar results have been reported in
human neuroimaging studies (Saenz et al., 2002). Selection of a desired feature also
suppresses neurons with response properties of differing selectivity (Martinez-Trujillo and
Treue, 2004) and increases baseline activity in feature-specific ways even when no stimulus
is present (Serences and Boynton, 2007).
Attention changes population codes

Although many of the effects of attention are observed at the level of single neurons, they
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also impact representations at the population level. For example, increasing the sensitivity of
selected neurons will lead to an increase in the selectivity of the entire population. In
addition, attention also acts to directly change the way information is represented in
populations of neurons. One way that attention improves the encoding of information in a
neuronal population is by decreasing noise correlations (Cohen and Maunsell, 2009;
Mitchell et al., 2009). Noise correlations measure the degree to which neurons share
uninformative signals that vary from trial-to-trial. Since each neuron has a limited
bandwidth, correlations in their signal reduces the information carrying capacity of the

population as a whole. This is perhaps most easily seen in the extreme: if each neuron
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carried the same signal, then the amount of information carried by the entire population
would be the same as by any one neuron. Therefore, by reducing noise correlations,
attention can significantly increase the information capacity of the population (Figure 4B).
However, not all correlations have a negative impact. As noted above, attention increases
the synchrony of selected populations of neurons, particularly at high frequencies (~40–50
Hz, Fries et al., 2001; Figure 4C). This is thought to boost the transmission of information
from the selected population (see above). It is important to note that such temporal
synchrony is orthogonal to noise correlations: information is carried in the pattern of firing
across a population of neurons, and redundancy in that population (such as in the case of
noise correlations) reduces the information capacity of a network; synchrony is local
coincidence in time and ensures the temporal precision of the firing pattern in order to drive
downstream neurons. Exactly how such synchrony arises remains unknown (although we
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propose one theory in the Model section below). However, it may be under top-down
control. For example, microstimulation of FEF induces high-frequency oscillations in
parietal cortex in a topographic manner (Premereur et al., 2012).
Attention resolves competition

Thus far we have largely discussed how attention impacts the representation of isolated
stimuli. However, as emphasized in the Introduction, the need for attention is greatest when
multiple stimuli are present and thus there is competition among stimuli for neural
representation. In a now classic experiment, Moran and Desimone demonstrated how
competition is resolved within single V4 neurons (Moran and Desimone, 1985). When two
stimuli were simultaneously presented in the receptive field of a V4 neuron they competed
with one another, reducing the overall response of the neuron (Figure 4D, purple line).
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However, this effect was counteracted by attention: when attention was directed to one of
the two stimuli in the receptive field, the neuron responded as if only the attended stimulus
was presented (Figure 4D, pink dashed line). Similar results have been found in MT and
MST (Treue and Maunsell, 1999), and corroborating evidence has been obtained in human
neuroimaging studies (reviewed in Beck and Kastner, 2009). Biasing the competition
between stimuli can also be conceived as a shift in a neuron’s selectivity: spatial attention
collapses the receptive field of neurons towards the attended location (Connor et al., 1997;
Womelsdorf et al., 2006b) while featural attention shifts the tuning curve of neurons toward
an attended feature (David et al., 2008; Martinez-Trujillo and Treue, 2004).
As reviewed here, there is strong evidence that attention impacts neural representations in
several different ways. Models of attention typically focus on an individual aspect of these
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effects. However, an integrated understanding of attention will require a unified theoretical

framework that captures these diverse effects. Next, we outline a theory that attempts to
build such an integrated understanding.
A unified framework for selective attention

As we have reviewed thus far, attention is a complex, multi-faceted, phenomenon with a
large and diverse number of associated effects, both in the way attention impacts sensory

representations as well as how attentional resources are allocated in space and time. Many
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different theories have been proposed that capture specific components of these attention
effects. However, an integrated model of attention has yet to be developed. Here we outline
a theoretical framework that builds upon several existing models of attention with a focus on
integrating the disparate physiological findings reviewed above.
Basic assertions
Before we detail our theory of attention we will briefly outline three basic assertions upon
which our theory is built:
i. Sensory cortex learns to represent visual objects; these embedded representations

are then used during perception.
ii. Normalization of responses is a fundamental aspect of neural processing in the

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cortex.
iii. Oscillations largely reflect rhythmic fluctuations in inhibitory tone in a neural

network.
Here, we will first explain the evidence for each assertion and, where possible, propose
underlying neural circuit mechanisms. Then, we describe how these three broad
observations can be combined with top-down attention signals to explain the large body of
neurophysiological findings associated with attention.
Our first assertion states that sensory cortex encodes and represents visual objects (Figure
5A). Although this review is focused on visual attention, it is important to consider the
computations used by sensory cortex to support perception given that visual attention affects
sensory processing. Although classical models assumed that these representations were the
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result of fine-tuned wiring (Hubel and Wiesel, 1959), more recent theoretical and
experimental work suggests that these representations are learned through experience. With
the help of simple unsupervised learning rules a ‘dictionary’ can be learnt that captures the
statistical regularities in the world (Simoncelli and Olshausen, 2001). At the level of primary
visual cortex, such learning results in gabor-like representations (Olshausen and Field,
1996); in higher-order cortex, it likely generalizes to ‘object’-like properties (e.g. co-
linearity of line segments, correlation of movement, parts of complex objects, etc). In
support of this model, experiments that ‘re-wired’ auditory cortex to receive visual inputs
led to neurons in auditory cortex with tuning properties that matched visual cortex (Sharma
et al., 2000). In other words, the selectivity of the neurons were not defined by a
developmental plan, but rather neurons learned the representations that best captured the
variability in their inputs.
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Importantly, embedding object-based representations will ensure that the system is tolerant
to noise as any input will be transformed by the learned object dictionary: signals that match
an expected pattern will be boosted while signals that are orthogonal to representations in
the dictionary will be ignored. As the dictionary has been trained to optimally represent the
world, this means the system will, in effect, perform pattern completion, settling on nearby
‘known’ representations, even when provided with a noisy input. As we detail below, this

will be crucial for allowing broad, unspecific attention signals to become selective based on
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the combination of a learned dictionary and the current sensory drive.
Our second assertion is that response normalization is fundamental to cortical function

(Figure 5B). Responses in cortex are normalized such that a constant level of overall activity
in a region is maintained. For example, the response of V1 neurons to multiple stimuli of
varying constrasts closely fits the predictions of a normalization model (Busse et al., 2009).
The exact neural mechanisms responsible for normalizing responses remain unknown,
although several possibilities have been discussed (for review, see Carandini and Heeger,
2012). In particular, one account that fits well with other observed effects of attention is that
divisive normalization is the result of lateral inhibition within a cortical region (Figure 5B;
Lee et al., 2012; Wilson et al., 2012; but also see Nassi et al., 2014 for a role for feedback).
Normalization is thought to be important for cortical functioning for several reasons. First,
by bounding the overall activity level, normalization may reduce the risk of pathologically
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high levels of excitation. Second, normalization acts to sparsify responses in a cortical

region, possibly contributing to the formation of the optimal, sparse, responses described
above (Schwartz and Simoncelli, 2001). Finally, as we detail below, a wide range of the
attention effects reviewed above have been modeled as the result of attention modulating the
gain of normalization (Reynolds and Heeger, 2009; Reynolds et al., 1999).
Our third assertion is that oscillations reflect rhythmic fluctuations in inhibition (Figure 5C
and 5D). Rhythmic fluctuations in neural activity are observed throughout the brain across a
wide variety of frequency bands (for review, see Buzsaki, 2006). The exact neural
mechanisms that produce oscillatory activity in the brain remain unknown; however, there is
a general consensus that inhibitory interneurons play a key role in the generation of rhythms.
For example, blockade of GABA receptors reduces the high-frequency oscillations
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commonly modulated by attention in the cortex (Hasenstaub et al., 2005). Furthermore,

optogenetic stimulation of parvalbumin-positive inhibitory interneurons preferentially
generates high-frequency gamma oscillations (Cardin et al., 2009). These results suggest
that oscillations in the brain reflect the ebb-and-flow of cortical excitability as inhibition is
rhythmically modulated.
Outline of the theory

We propose that many of the diverse neurophysiological findings associated with attention
can be explained by combining our three basic assertions with the mechanisms of top-down
attentional selection reviewed in the section on network level effects. In particular, we
propose interactions between excitatory pyramidal neurons and inhibitory interneurons are
central to the mechanism supporting normalization and in the generation of synchronous
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oscillations. In brief, we propose that attention works through a cascade of effects:
1. Attention can either be a) automatically grabbed by salient stimuli or b) guided by

task representations in frontal and parietal regions to specific spatial locations or
features.

2. The pattern-completion nature of sensory cortex sharpens the broad top-down

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attentional bias, restricting it to perceptually relevant representations. Interactions

with bottom-up sensory drive will emphasize specific objects.
3. Interneuron-mediated lateral inhibition normalizes activity and, thus, suppresses

competing stimuli. This results in increased sensitivity and decreased noise
correlations.
4. Lateral inhibition also leads to the generation of high-frequency synchronous

oscillations within a cortical region. Inter-areal synchronization follows as these
local oscillations synchronize along with the propagation of a bottom-up sensory
drive. Both forms of synchrony act to further boost selected representations.
5. Further build-up of inhibition acts to ‘reset’ the network, thereby restarting the
process. This reset allows the network to avoid being captured by a single stimulus
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and allows a positive-only selection mechanism to move over time.
As we detail next, many of the effects observed at the neural level can be explained through
this cascade. In addition to noting neurophysiological observations, we will also highlight
some of the theoretical models on which our unified framework is built.
Step #1: Direction of attention—Attention is controlled in one of two ways. First,

attention can be captured by stimuli that are inherently salient based on their physical
properties (such as their brightness, contrast, speed, etc) or other factors such as their
associated valence. As noted above, saliency maps capture the saliency of all objects in a
visual scene, allowing attention to be directed to stimuli in their rank order of salience (Itti
and Koch, 2001).
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Second, attention can be guided towards stimuli that are relevant to one’s current task. Our
ability to focus our attention in such a manner is remarkably flexible: we can attend to
different spatial locations, with seemingly different ‘zoom’ levels, as well as to both simple
and complex features (i.e. ‘red things’ and ‘cars’). As reviewed above, such attention
templates are ‘top-down’; originating in prefrontal and parietal cortex and influencing
sensory cortex both through direct descending projections (e.g. from FEF to V4; Figure 6A)
as well as through a backwards cascade (e.g. from PFC to IT to V4, etc; Figure 6B).
Step #2: From broad to precise top-down modulation—This then presents a

conundrum: what neural mechanisms would allow for both the flexibility and specificity of
attentional modulation? One hypothesis is that there are specific anatomical connections that
support all possible selections that could be desired. Under this model, every form of
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attentional selection would need a physiological correlate. For example, top-down spatial
attention projections would have to be distributed across different spatial locations as well as
across different spatial scales. Although this remains a possibility, current anatomical and
physiological support for this model is limited (Anderson et al., 2011). Instead, we argue
that broad, non-specific top-down signals are shaped by the local circuitry and activity in
sensory cortex (Duncan et al., 1997).

The pattern-completion nature of sensory cortex (Assertion #1) means that non-specific
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inputs will be transformed into something that ‘makes sense’ to the network. In other words,
any energy input to the circuit that is orthogonal to its inherent representations will be
discarded while energy along its learned representations will be maintained. This effect will
be further amplified when the circuit is already receiving (and processing) bottom-up inputs.
In this case, sensory drive has activated a sub-set of possible activity states for the network –
moving away from these would require a strong overriding input. Instead, attention is
modulatory and therefore has the greatest impact on those representations that are already
active in the network.
To demonstrate this effect, we can imagine a simplified case where attention is being
directed to a spatial location with two competing neurons that respond to either circular or
square stimuli. Attending to this location without visual stimulation will broadly boost both
representations (note that representations not embedded in our network, such as triangular
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stimuli, will not be boosted as our simplified network does not encode them). However, if
our spatial location begins receiving circular visual input this same attention signal will only
be effective in increasing the activity of the ‘circle’ neuron as the ‘square’ neuron will be
suppressed (either in a bottom-up manner or through competition with the circle neuron).
Featural selection would work in a similar way: attending to a ‘car’ will emphasize car-
components, such as circular wheels. These would be automatically selected in a top-down
cascade (as seen in Figure 6B). Again, interactions with bottom-up sensory drive would
collapse that selection to a particular exemplar of a category (i.e. a BMW vs. a Ford).
Generalizing from this simplified example, our theory will make a prediction how attention
selects objects. As noted above in our first assertion, the visual system has learned the
statistical regularities of objects and has embedded this knowledge in the connections of a
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distributed network (Figure 5A). Therefore, applying attention to any part of the object
representation will cause the boosting signal to spread throughout the object. This prediction
has extensive experimental support. First, attention to an object automatically selects all
components of an object (Duncan, 1984; Egly et al., 1994; Siegel et al., 2015). In addition,
recent work suggests that attention will automatically extend to other stimuli that follow
Gestalt object rules (e.g. collinearity, Wannig et al., 2011). Furthermore, spatially attending
to a stimulus will also boost the representation of objects with similar features across the
visual field (McAdams and Maunsell, 2000; Treue and Trujillo, 1999).
Together, these results provide experimental support for a model in which top-down
attention is broad and non-specific and only becomes focused through interactions with the
anatomical connectivity embedded in sensory cortex and the bottom-up sensory drive.
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Step #3: Biasing competition through normalization—As reviewed above, there is

evidence that attention resolves competition between stimuli in a way that boosts selected
representations while suppressing unselected ones. This finding was captured in the highly
influential ‘biased competition’ theory of attention (Desimone and Duncan, 1995). In brief,
the model proposes that stimuli are constantly competing with one another for greater
representation; attention acts to bias this competition, allowing the selected stimulus to
‘win’.

Competition between stimuli is likely the result of the normalization process described in
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our second assertion (Reynolds et al., 1999). Recent work by Reynolds and Heeger (2009)
showed that integrating a normalization model with attentional biasing mechanism, captures
a wide variety of attentional effects. First, they were able to explain how spatial attention
can increase the contrast gain of neurons (Reynolds et al., 2000), the response gain
(Williford and Maunsell, 2006), or multiplicatively scale responses (McAdams and
Maunsell, 2000). Second, they captured the sharpening of tuning curves with featural
attention (David et al., 2008; Martinez-Trujillo and Treue, 2004). Finally, like the biased
competition model, the normalization model of attention also predicts the response to
multiple stimuli in a single receptive field (Moran and Desimone, 1985).
Lateral inhibition carried out by inhibitory interneurons is a candidate mechanism that may
instantiate the normalization computation (Figure 5B). If so, one would expect significant
attentional modulation of the inhibitory neurons that are computing the normalization signal.
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Indeed, attention has a much larger impact on the responses of putative inhibitory
interneurons compared to putative pyramidal cells (Mitchell et al., 2007). Direct evidence
for top-down targeting of inhibitory interneurons comes from a recent study showing that
long-range projections from cingulate cortex to visual cortex in mice increase center-
surround modulation via local inhibitory interneuron circuits (Zhang et al., 2014).
We propose that a model that centers on lateral inhibition has the potential to explain a
diverse set of attention effects. For example, as noted by Reynolds and Heeger, such
recurrent models of normalization may capture the temporal dynamics of attention effects
(namely the lack of an attention effect on the visual transient) or the alterations of the size
and center of receptive fields. Lateral inhibition has also been shown to increase the sparsity
of neural representations (Schwartz and Simoncelli, 2001). As sparser signals are more
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likely to be independent to one another, this will lead to a reduction in noise correlations (as
observed; Cohen and Maunsell, 2009).
Step #4: Synchrony is rhythmic inhibition—In addition to computing the

normalization effect, lateral inhibition may also underlie synchronous oscillations (Figure
5C and 5D). As reviewed above, attention modulates local synchrony, possibly to increase
the gain of a selected neural representation (Tiesinga et al., 2004) or to boost the
transmission of information from one region to the next (Fries, 2005). However, such
models that explain effects on synchronous firing in local populations are often separated
from those that explain other effects of attention on single neurons. We propose a unifying
mechanism relying on lateral inhibition: namely, that the same attentional modulation of
inhibitory interneurons that leads to normalization also increases synchronous high-
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frequency oscillations.
Such a model makes several predictions about the nature of synchronous oscillations in
cortex. First, it predicts high-frequency oscillations are generated by local inhibitory
interneurons. As noted in our third assertion, a large body of modeling work suggests that
this is true, either due to interactions between interneurons directly (so called “ING” models;
Wang and Buzsáki, 1996) or between inhibitory interneurons and excitatory pyramidal
neurons (so called “PING” networks; Börgers and Kopell, 2005). Furthermore, optogenetic

stimulation of inhibitory interneurons produces high-frequency oscillations (Cardin et al.,

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2009). Second, the model predicts that attention should target inhibitory interneurons in a
way that drives synchrony. Indeed, as noted above, experimental evidence suggests that
attention has its greatest impact on inhibitory interneurons (Mitchell et al., 2007). More
importantly, and as predicted, Vinck et al (2013) found inhibitory interneurons preferentially
synchronized with local populations (measured via LFPs), with a phase relationship that
suggested they were driving the high-frequency oscillations in LFP. Finally, according to
our model, attention will increase firing rates (particularly in inhibitory interneurons) before
increasing high-frequency oscillations. Although this has not been directly tested, there is
some experimental evidence that attention effects on firing rate precede modulations in
high-frequency oscillations in visual (Fries et al., 2008) and frontal cortex (Gregoriou et al.,
2009b).
By acting on inhibitory interneurons, attention increases local synchrony and, thus, increases
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the impact of a neuronal population on downstream brain regions (see dynamic functional
connectivity section above for details). Attention also increases synchrony between regions,
further boosting information transfer. However, if high-frequency oscillations are due to the
activation of local circuits, then how are they synchronized across different brain regions?
One possibility is that there is a controlling input that forces synchronization across regions
(and could be modulated by attention). For example, high-frequency oscillations have been
found to be coupled to low-frequency oscillations (Colgin, 2013; Schroeder and Lakatos,
2009) and so a synchronous low-frequency oscillations could organize the temporal
dynamics of higher-frequency oscillations across regions.
Alternatively, synchronization across brain regions may be a passive process that only
requires a phase reset to initially align local oscillations. This phase reset would occur with
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the onset of a strong input into the cortex, such as the appearance of a new stimulus in the
world or an eye movement moving an existing stimulus into a receptive field. The
propagation of this stimulus across brain regions (in a bottom-up manner), would then
naturally align the local oscillations across regions. This predicts an increase in high-
frequency synchrony with a strong stimulus drive, as seen following the onset of a pop-out
stimulus (as seen by Buschman and Miller, 2007).
Step #5: Rhythmic oscillations of inhibition resets the neural network—Many

of the above effects demonstrate how attention may increase synchrony to select specific
representations. However, these effects do not strictly rely on synchrony being oscillatory in
nature. Therefore, it is not clear what mechanistic function an oscillation may serve. We
propose that oscillations modulate the attractor dynamics of local cortex by periodically
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‘resetting’ the network through strong inhibition (Figure 5C and 5D).
For example, this may be crucial to disengaging attention. Suppose one deploys attention to
a stimulus, which as a consequence, ‘wins’ the competition with other stimuli through lateral
inhibition. In this way, the attended stimulus has captured the network; a state that will
persist, even if attention is released and redeployed. One possible solution to this problem
might be a strong negative, or inhibitory, signal that can counter the positive selection of
attention. In support of this model, psychophysical studies have revealed a strong ‘inhibition

of return’ (IOR) that inhibits re-selecting an already attended stimulus (Klein, 2000), an
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effect that reduces the neural representation of a previously selected stimulus (Mirpour et al.,
2009). Alternatively, oscillations in global inhibition levels may serve this same purpose:
every cycle of an oscillation effectively ‘resets’ the network, allowing a new stimulus to be
captured. Such a mechanism has the advantage of not requiring a strong top-down inhibitory
signal but rather relies on a local mechanism for generating inhibition. If true, our theory
would predict that shifts in attention should be tied to ongoing oscillations in neural activity.
Indeed, Buschman and Miller (2009) observed this effect during a visual search task. Covert
shifts in attention (measured behaviorally and electrophysiologically) were locked to
ongoing beta-band oscillations: on each cycle of the beta-band oscillation the animal
attended to a new location in space. Similar effects have been observed in humans, although
at lower frequencies (Busch and VanRullen, 2010; Fiebelkorn et al., 2013; Landau and
Fries, 2012). Similarly, overt shifts in attention (i.e. eye movements) are phase-locked to
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lower frequency oscillations (Schroeder et al., 2010).
Note that, at the behavioral level, rhythmic attention will appear as the classic inhibition of
return: stimuli are momentarily attended before being inhibited for a sustained period of
time (as they are never returned to). Indeed, studies of IOR have found the onset of
inhibition occurs around 225 ms (Klein, 2000), which is approximately the 4 Hz observed in
rhythmic fluctuations of attention (Fiebelkorn et al., 2013). However, it remains to be seen
which is the chicken and which is the egg: do oscillations structure the IOR or do we
observe rhythmic IOR as oscillations?
Networks for attentional control: Interplay of spatial and featural attention

Directing attention to space of features appears to be controlled by individual sources in the
brain. Spatial attention is likely directed by descending projections into extrastriate visual
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areas (e.g. FEF to V4 projections; Figure 6A). In contrast, featural attention is much broader,
impacting the entire visual field. Therefore, featural attention likely begins in regions with
larger receptive fields and more complex representations (Figure 6B). A ‘reverse hierarchy’
model of attention suggests selection begins at the highest, most abstract, level before
filtering down to the details of an object (Hochstein and Ahissar, 2002). Such a model
predicts the selection to begin in prefrontal/parietal cortex, where neurons represent abstract
categories (Freedman et al., 2001), and then filters backwards along the cortical hierarchy to
‘simpler’ visual areas. Surprisingly, it also predicts that the ease of feature-based visual
search should be directly related to whether the category of the sought-after stimulus is
‘natural’. Indeed, searching a cluttered natural scene for a complex object can be highly
efficient if the object is typical to our everyday experiences, as noted above (e.g. “cars”, for
review see Peelen and Kastner, 2014).
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Despite their independent sources, these two forms of attention do interact with one another.
A network view of selection suggests that such interactions are mediated through the
convergence of feature and spatial attention in visual cortex (Figure 6C). Attending to a
spatial location will select an object (or a piece of an object) at that location. This selection
will propagate up-and-down the visual hierarchy, acting to select associated representations.
In turn, the more abstract, invariant representations in higher cortical regions will lead to the

automatic selection of similar objects in the visual scene based on their featural properties.
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Indeed, psychophysical studies have shown that spatial attention can drive featural attention
(e.g. spatially attending to a single object leads to increases in attention to its properties
across the entire cortex, Summerfield et al., 2006). Conversely, featural attention can drive
spatial attention (e.g. the detection of a car in a visual scene drives spatial attention to that
location). In this way, spatial and featural attention can be flexibly combined to allow for the
dynamic nature of attention.
Future directions
We have attempted to outline a parsimonious theoretical model that captures the diversity of
attention effects on neural activity. In particular, we have focused on local cortical
interactions as these are the most prevalent connections in the brain and therefore the most
likely to impact neural processing. We have also attempted to avoid the need for precise top-
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down or controlling inputs, whether it is spatially precise (in the case of a spotlight of
attention) or temporally precise (in the case of inter-areal synchronization). As we hope is
clear, this model relies heavily on previous theoretical and experimental work. However,
despite this strong basis, a more mechanistic model is needed to test the details of our
theory.
In addition, there are many experimental details that need to be worked out. For example,
many of the observed effects of attention can be explained by modulating the excitatory/
inhibitory balance of this network, particularly by increasing the inhibitory gain in the
network. However, we are only beginning to understand how this balance is modulated in
the brain. For example, there are several (perhaps dozens) of different types of inhibitory
interneurons. Recent work is beginning to unravel the relative roles of these interneurons,
both in perception and attention (Lee et al., 2012; Wilson et al., 2012; Zhang et al., 2014)
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but future work must continue to detail the respective roles of these varied cell types.
A particularly intriguing avenue for further exploration is the role of neuromodulation in

altering the computational properties of local cortical circuitry. In particular, acetylcholine
(ACh) has been proposed to play a role in attention. Indeed, manipulating ACh receptors
changes the effect of attention on V1 neurons (Disney et al., 2007; Herrero et al., 2008).
This effect may be mediated by cholinergic midbrain regions that represent stimulus
saliency (Asadollahi et al., 2010) and are themselves modulated by prefrontal cortex (Sarter
et al., 2005).
Finally, the theory outlined here is focused on the effects of attention on perception (almost
exclusively visual perception). However, attention is just one small part of cognition and it
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is becoming increasingly clear that attention interacts heavily with other cognitive domains,
as we will review in the final section.
Attention and other cognitive processes

Attention, defined as the act of selecting task-relevant information, is a central component of
cognition. Although research on attention has been largely focused on its impact on visual
processing, there are close relationships between attention and other cognitive processes.

Attention and working memory

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Working memory is the ability to hold items ‘in mind’, without relying on the external
world. Working memory plays a central role in cognition: it acts as a dynamic mental
‘workspace’ in which thoughts are processed, manipulated, and transformed. Indeed,
attention may rely on working memory workspaces to maintain the current ‘search template’
(Wolfe, 1994). Evidence for such a model comes from studies showing that attention can be
biased by the current contents of working memory (Soto et al., 2008). Furthermore, brain
regions involved in controlling attention are also strongly recruited during working memory,
particularly the fronto-parietal network (Awh and Jonides, 2001). However, the relationship
between attention and working memory is complicated. Models of working memory predict
the existence of a ‘central executive’ that controls and manipulates the contents of working
memory ‘sketchpads’ (Baddeley and Hitch, 1974). Recent studies underline the importance
of this ‘central executive’: an individual’s general intelligence correlates highly with how
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effectively the contents of working memory are controlled (Fukuda and Vogel, 2011).
Attention may be this ‘central executive’ of working memory. In support of this idea,
attention filters what enters working memory (Gazzaley, 2011) and plays a role in
maintaining items in memory (Kuo et al., 2011). Attention may also pull together the
distributed brain regions necessary to support working memory (Postle, 2006). There is also
growing evidence that the capacity limitation of working memory is due to competition in a
manner very similar to the competition observed during perception (Buschman et al., 2011),
suggesting that some of the neural mechanisms limiting perception may also be limiting
working memory. Indeed, the same brain regions involved in directing attention to external
stimuli are activated when attending to ‘internal’ stimuli (Chun et al., 2011; Nobre et al.,
2004).
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Attention and reward learning

Attention is also intricately related to reward processing. Attention is attracted to salient,
behaviorally-relevant, stimuli. Obviously, rewarding stimuli should be salient and therefore
reward signals are likely closely tied to attention signals. Recent electrophysiological
evidence has begun to tease apart the relationship between attention and reward in visual
cortex, with some early evidence for partially overlapping representations (Foley et al.,
2014). In addition, since reward information guides learning, it may aid in learning of where
to direct attention (Rombouts et al., 2015).
Attention may also be critical to learning what is rewarding in the real world. Reinforcement
learning is not efficient when a reward can be associated with too many possible sources. In
this context, attention may act to select the most likely sources and therefore limit
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reinforcement learning to this subset (Niv et al., 2015). In this way, attention can act to
guide learning towards task-relevant stimuli.
Together, these results suggest that attention, working memory, and rewards are closely
intertwined, and therefore may share many of the same underlying neural mechanisms.
Future work is needed to continue elucidating which mechanisms are shared and which are
distinct. This entwinement also highlights the integrative nature of behavior. Attention is

crucial to working memory and reward processing because both functions rely on selection
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of task-relevant stimuli. Indeed, as we review next, the selective nature of attention may
underlie cognitive control more broadly.
Attention and cognitive control

Cognitive control is our ability to guide our actions based on our task, our internal goals, and
the current context. Cognitive control is thought to operate by guiding activity throughout
the brain in a task-dependent manner (Miller and Cohen, 2001). In reality, this is just a
super-set of attention: instead of only acting upon sensory representations, cognitive control
can operate more broadly to select relevant stimulus representations, decision making
circuits, and motor planning regions (Norman and Shallice, 1986).
Indeed, there is significant overlap between the neural mechanisms supporting cognitive
control and attention. For example, similar to attention, prefrontal cortex is thought to be the
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source of cognitive control: lesions in PFC disrupt cognitive control (Barceló and Knight,
2002) and single neurons in PFC represent the current task (Wallis et al., 2001; White and
Wise, 1999). Furthermore, synchrony within prefrontal cortex carves out ensembles of task-
related neurons (Buschman et al., 2012), much like in the way attention creates synchronous
ensembles in posterior cortex.
In this light it seems that by studying attention we have been studying one specific form of
cognitive control. Therefore, it is possible that many of the neural mechanisms underlying
attention will apply more broadly. For example, cognitive control may resolve competition
between motor plans in the same way attention resolves competition between sensory
stimuli (a generalization of Figure 5B). Similarly, oscillations are observed throughout the
brain and may play a similar role in moderating cortical dynamics in any cortical region
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(Figure 5C and 5D). This would make sense from an evolutionary perspective – once the
brain solves one problem, it might as well apply the same solution to other, similar,
problems.
Conclusions
Attention research has moved from laboratory scenes to the real world at the behavioral
level, and from the single neuron to local populations and functional interactions across
large-scale networks at the neural level (see Box 1: Current status of the field). We have
outlined a unified theory of attention that begins to integrate these disparate effects. We
propose broad top-down selection signals interact with the inherent knowledge embedded in
sensory cortex and with bottom-up sensory drive. In addition, we suggest that these signals
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interact within the local cortical circuit to produce oscillatory synchrony. Such oscillations
temporally parse neural activity in a way that facilitates selection of relevant representation,
routes information through the brain, and modulates attractor dynamics of a network.

Box 1
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Current status of the field

• Attention is used to select specific representations for greater neural
representation. This resolves competition for limited neural resources.
• Attention is controlled by a distributed fronto-parietal network that acts upon

representations in sensory cortex.
• Attention increases the strength of neural responses in several different ways to

boost the attended representation, allowing it to win the competition for neural
resources.
• Attention interacts with many other cognitive domains, including learning,

short- and long-term memory, and decision making.
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Future work is needed to continue building a detailed, mechanistic, understanding of

attention (see Box 2: Future directions). Detailed circuit models of attention will require
continuing efforts to identify cell-types and quantify their role in attention. In addition, a
unified theory must account for the dynamics of attention. Studying these dynamics will
require accurately following the time-course of neural correlates of attention across large
populations of neurons throughout the brain. Such large-scale recordings will require
continued improvements in multi-electrode electrophysiology techniques and/or imaging
approaches. This appears particularly important as neural dynamics may be key to
understanding the enormous flexibility of attentional resources. Yet, the neural mechanisms
supporting these dynamics remain largely unknown. Finally, we must continue to integrate
attention with other cognitive domains. The parcellation of behavior and brain into different
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cognitive domains has yielded important insights into the neural mechanisms of many
behaviors. However, cognition emerges from the interactions of these ‘cognitive domains’;
thus, a complete understanding of cognition will require a more integrative approach.
Box 2
Future Directions
• Attention is highly dynamic; changing rapidly between locations and/or
features. These dynamics have been associated with local population
oscillations, yet the exact neural mechanisms remain unknown.
• The recruitment of network parts within the fronto-parietal network is highly

flexible, depending on changing behavioral demands. However, the neural
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mechanisms utilized to couple these parts for a given task are unknown, nor is it
clear how a network pattern produces the desired behavior.
• Attention may boost neural representations at several different levels, from

increasing single neuron responses to boosting population selectivity. However,
it is unknown how these effects interact and whether they share common circuit
mechanisms.

• Recent work has highlighted the existence of domain-specific neural networks.

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However, it remains unknown how these networks interact in order to support

the integrative nature of cognition.
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Figure 1. Behavioral studies

(A) Visual search in artificial displays versus in real-world scenes. Detecting the presence of
a green T (conjunction search) is effortful and time-consuming, such that reaction times
increase as a function of display items. (B) In contrast, detecting the presence of categorical
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object information such as ‘people’ or ‘cars’ in real-world scenes requires only a single
glance, despite the large number and variety of distracter objects. (C) The detection of
animals or vehicles in natural scenes does not require focused spatial attention. In a dual-
task paradigm, subjects performed a central discrimination task, while detecting animals in
scenes presented in the periphery. Performance is normalized to a condition when only a
single task was performed. Performance on the peripheral animal detection task was only
mildly impaired by simultaneously performing the central discrimination task. Adapted from
(Li et al., 2002). (D) Selective attention has rhythmic properties. Subjects detected the
dimming of a part of a rectangular object at a spatially cued (black line; location #1 in the
two object display depicted as an example), or at an uncued location of the same object than
the cued location (orange line; location #2), or a different object (blue line; location #3).
Accuracy is plotted as a function of the cue-target interval revealing the following rhythmic
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properties: at the cued location, detection performance fluctuated at 8Hz, whereas at the
same- and different-object locations a characteristic anti-phase relationship of a 4Hz rhythm
was observed. Adapted from (Fiebelkorn et al., 2013).

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Figure 2. Fronto-parietal control of attentional selection

(A) Topographic organization of areas in human frontal and parietal cortex. Using a
memory-guided saccade task several areas with a systematic representation of the
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contralateral visual field were identified along the intraparietal sulcus (IPS0-5), adjacent
superior parietal cortex (SPL1), and in superior (FEF) and inferior aspects of precentral
cortex. Adapted from (Silver and Kastner, 2009). (B) Attention-related activations within
parietal and frontal cortex in a spatial attention task. There is significant overlap between
attention-related activations and topographic representations in higher-order cortex. Adapted
from (Szczepanski et al., 2010). (C) Time series of fMRI signals in V4 and FEF. Directing
attention to a peripheral target location in the absence of visual stimulation led to an increase
of baseline activity (textured blocks), which was followed by a further increase after the

onset of the stimuli (gray shaded blocks) in V4, but not in FEF, where the initially stronger
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baseline increase was sustained, thus reflecting the attentional operations of the task and not
sensory processing. Adapted from (Kastner et al., 1999) (D) Microstimulation of FEF
(below the threshold that evokes an eye movement) induces attention-like increases in the
spikes/s of V4 neurons with receptive fields that overlap the FEF site (black is baseline; red
with microstimulation). Adapted from (Moore and Armstrong, 2003).
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Figure 3. Attention dynamically changes the effective connectivity between brain regions
(A) Attention modulates the synchrony between different brain regions. A minor subset of
the effects of attention is outlined. Circles with letters refer to other parts of the figure. (B)
Attentional modulation is specific to selected objects: synchrony between V4 and V1 is
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specific to those regions that encode the currently attended stimulus (red for a stimulus
encoded by V1a; blue for V1b). Note that these changes in the pattern of synchrony overlay
the underlying anatomy and can occur rapidly, with each shift in attention. Adapted from
(Bosman et al., 2012). (C) There is also flexibility in the frequency of oscillations between
brain regions. Internal (top-down) direction of attention and external (bottom-up) capture of
attention emphasize different frequency bands between the same brain regions. Synchrony
between prefrontal cortex (PFC) and parietal cortex (PPC) changed frequency depending on

the type of attention. When attention was externally captured by a salient stimulus, this was
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reflected in neural activity in PPC first, followed by PFC. In addition, synchrony between
PFC and PPC was observed at high-frequencies (~45 Hz; shown as negative deflection). In
contrast, when attention was internally directed by the memory of a target stimulus (as in
visual search) neural activity was found first in PFC and then PPC and PFC-PPC synchrony
was observed at low frequencies (~25 Hz; shown as positive deflection). Adapted from
(Buschman and Miller, 2007) (D) Sub-cortical regions, such as the pulvinar, play an
important role in attention. In addition, they may act to coordinate activity across cortical
regions: attention increased low-frequency synchrony between the pulvinar and V4/TEO
(left/right, respectively), when allocated at the receptive field (RF) represented by the
recorded neurons (ATT to RF) relative to a different RF location (ATT away from RF). This
may organize higher-frequency oscillations, facilitating the establishment of synchrony
observed between cortical regions (as in B and C). Adapted from (Saalmann et al., 2012).
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Figure 4. Attention changes neural responses

(A) Attention increases the sensitivity of V4 neurons. Neurons increase their firing rate
response to stimuli of increasing contrast; even without attention (gray line). Attending to
the stimulus increases the response to stimuli at lower contrasts (black line; note leftward
shift). Data is schematized from (Reynolds et al., 2000). (B) Attention reduces noise
correlations in neural activity. Simultaneously recorded neurons often share uninformative
‘noise’ signals. This is schematized in the two model neurons below. Noise is schematized
as black letters in the encode ‘stream’, gray letters are ‘signal’. The two neurons share much
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of the same ‘noise’; reducing such noise makes the message encoded by both neurons
clearer (‘toy car’). Attention has such an effect in the brain (top figure; black line is below
gray line). Adapted from (Cohen and Maunsell, 2009). (C) Attention increases the
synchrony of selected neurons. The synchrony between individual neurons and the
population (as measured by the local field potential, LFP) increases with attention allocated
at RF (‘attended’, red) relative to away from RF (‘unattended’, blue). This effect is specific
to a ‘gamma’ oscillation at ~50 Hz (note that synchrony is reduced at low-frequency, ~10

Hz, oscillations). Adapted from (Fries et al, 2001) (D) Attention resolves competition
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between stimuli. Stimuli compete for representation in V4 neurons: the response to two
stimuli (purple) is approximately the average of the response to either stimuli when
presented alone (red, preferred, and blue, non-preferred). Attending to a single stimulus
‘rescues’ this competition, causing the neuron to respond as if only the attended stimulus
was presented (pink dashed line). Data is schematized from (Reynolds et al., 1999).
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Figure 5. Theory of local attention effects

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We propose many of the effects of attention to be due to local interactions within a cortical
region. Attentional selection interacts with bottom-up sensory drive (not shown) as well as
object representations that have been embedded within the neural network through learning
(A). Attention acts on these representations by changing interactions between excitatory
neurons (green) and local inhibitory interneurons (red). In particular, pooling of responses
by inhibitory interneurons could form the basis for normalization of excitatory responses
(B). As noted in the main text, normalization likely plays a key role in perception and
attention. Furthermore, rhythmic interactions between excitatory and inhibitory neurons is
proposed to underlie high-frequency oscillations (C), which are increased with attention.
These oscillations may play a fundamental role to temporally organize neural activity. For
example, periods of inhibition may ‘reset’ the network, allowing it to explore more than one
attractor state (details in main text).
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Figure 6. Cascades of spatial and featural attention across the visual hierarchy
The brain is a densely interconnected network and so attentional selections, whether (A)
spatial or (B) featural, propagate up and down the visual hierarchy. In this way, they will
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interact (C), allowing spatial attention to lead to selection of objects with similar features or
featural selection to drive spatial attention.
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Published in final edited form as:

From behavior to neural dynamics: An integrated theory of

Correspondence to: TJB ([email protected]) and SK ([email protected]).

Behavioral effects - Building blocks and shifting concepts

Classical attention paradigms

Neuron. Author manuscript; available in PMC 2016 October 07.

Real-world visual search

concepts of attention to incorporate mechanisms that are optimized for naturalistic

Rhythmic properties of selective attention

Neuron. Author manuscript; available in PMC 2016 October 07.

scene, this spotlight was thought to be continuously moving from location-to-location,

shifting at a rate of approximately 20 Hz (Wolfe et al., 2011). Previous studies suggested

Network effects – from functional anatomy to dynamic connectivity

hemifield are removed.

Defining the visual attention network

Neuron. Author manuscript; available in PMC 2016 October 07.

It is important to note that the fronto-parietal network consists of a large number of

Neuron. Author manuscript; available in PMC 2016 October 07.

Functional dissociations of the network

Neuron. Author manuscript; available in PMC 2016 October 07.

The large-scale fronto-parietal attention network seen in humans is generally conserved in

results have recently been found in humans (Li et al., 2010).

Neuron. Author manuscript; available in PMC 2016 October 07.

Dynamic functional connectivity

In addition to boosting the effectiveness of local neuronal populations, increasing synchrony

Neuron. Author manuscript; available in PMC 2016 October 07.

Importantly, communication in cortical large-scale networks is not only mediated through

Neuronal effects – from single neurons to populations

Neuron. Author manuscript; available in PMC 2016 October 07.

dynamics of populations of neurons.

Spatial attention enhances neural responses

Attention changes population codes

Neuron. Author manuscript; available in PMC 2016 October 07.

Attention resolves competition

effects. However, an integrated understanding of attention will require a unified theoretical

A unified framework for selective attention

Neuron. Author manuscript; available in PMC 2016 October 07.

i. Sensory cortex learns to represent visual objects; these embedded representations

ii. Normalization of responses is a fundamental aspect of neural processing in the

iii. Oscillations largely reflect rhythmic fluctuations in inhibitory tone in a neural

Neuron. Author manuscript; available in PMC 2016 October 07.

the combination of a learned dictionary and the current sensory drive.

Our second assertion is that response normalization is fundamental to cortical function

high levels of excitation. Second, normalization acts to sparsify responses in a cortical

commonly modulated by attention in the cortex (Hasenstaub et al., 2005). Furthermore,

Outline of the theory

oscillations. In brief, we propose that attention works through a cascade of effects:

1. Attention can either be a) automatically grabbed by salient stimuli or b) guided by

Neuron. Author manuscript; available in PMC 2016 October 07.

2. The pattern-completion nature of sensory cortex sharpens the broad top-down

attentional bias, restricting it to perceptually relevant representations. Interactions

3. Interneuron-mediated lateral inhibition normalizes activity and, thus, suppresses

4. Lateral inhibition also leads to the generation of high-frequency synchronous

and allows a positive-only selection mechanism to move over time.

Step #1: Direction of attention—Attention is controlled in one of two ways. First,

Step #2: From broad to precise top-down modulation—This then presents a

Neuron. Author manuscript; available in PMC 2016 October 07.

Step #3: Biasing competition through normalization—As reviewed above, there is