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Opinion

How do emotion and motivation direct


executive control?
Luiz Pessoa
Department of Psychological and Brain Sciences, Indiana University, 1101 E10th Street, Bloomington, IN 47505, USA
Open access under CC BY-NC-ND license.

Emotion and motivation have crucial roles in determin- of behavior [4,5]. To understand the flow of information
ing human behavior. Yet, how they interact with cogni- processing more widely, in addition to the role of percep-
tive control functions is less understood. Here, the basic tual competition, it is crucial to understand the impact of
elements of a conceptual framework for understanding executive control functions on item processing. Executive
how they interact are introduced. More broadly, the control involves a host of ‘adjustment processes’, including
‘dual competition’ framework proposes that emotion perceptual selection, detection and resolution of conflict,
and motivation affect both perceptual and executive and maintenance of contextual information. Executive
competition. In particular, the anterior cingulate cortex control is not unitary, and different mechanisms can have
is hypothesized to be engaged in attentional/effortful their own limited processing capacities or resources [6,7].
control mechanisms and to interact with several other Neuropsychological research also supports the dissociation
brain structures, including the amygdala and nucleus of executive functions, consistent with the fractionation of
accumbens, in integrating affectively significant signals the central executive [8–10]. The exact fractionation of
with control signals in prefrontal cortex. An implication executive functions is subject to debate, but probably
of the proposal is that emotion and motivation can either involves at least three functions [11,12]: inhibition, shifting
enhance or impair behavioral performance depending on and updating. Crucially, ample evidence indicates some
how they interact with control functions. unity of executive functions as well, consistent with the
notion that mechanisms are shared across functions
Perceptual and executive competition [12,13]. This ‘capacity sharing’ has important implications
Although the impact of affective significance (see Glossary) for the understanding of human information processing –
on behavioral performance is well documented [1], in gen- because it leads to ‘executive competition’. Here, it is
eral, the mechanisms by which this impact is manifested proposed that subcomponents of executive control are
remain poorly understood. And, whereas some progress mutually interacting, such that resources devoted to one
has been made concerning the interactions between component will detract from those available to other com-
emotion and specific cognitive processes [2,3], important ponents. For instance, if resources required to carry out
gaps still remain. Crucially, relatively little is known about behavioral inhibition are partly shared with those needed
the role of affective significance in ‘executive control’ func- during shifting, an individual needing to withhold respond-
tions. Here, our goal is to propose a conceptual framework ing in a trial might exhibit an increased switching cost if
that describes how affective significance impacts the flow of
information processing in the brain, with a particular aim
at understating how it can either enhance or impair beha- Glossary
vioral performance according to the situation at hand.
Affective significance: affectively significant items are those that have either
Items laden with affective significance include those that negative or positive value to the organism.
involve threat (e.g. via pairing with mild shock) and reward Dprime: perceptual sensitivity measure that takes into account both ‘hits’ (e.g.
(e.g. via pairing with cash). The framework thus attempts correct, target-present trials) and ‘false alarms’ (incorrect, target-absent trials).
Dprime scores effectively discount for elevated numbers of false alarms and
to describe how both emotion and motivation interact with are independent of response criterion.
executive control to determine behavioral outcome – in Emotion: emotion and motivation (see later) are closely linked concepts as
contrast with proposals that focus on either threat or both depend on the relationship between the organism and its environment
(e.g. positive–negative, approach–withdrawal).
reward processing. Here, it is suggested that both emotion Executive control: set of functions, typically believed to depend on the frontal
and motivation signals are integrated with executive func- cortex (and probably the parietal cortex), which are needed when non-routine
tions so as to effectively incorporate value into the unfold- behaviors are called for – namely, when ‘control’ is required. These functions
are thought to confer behavioral flexibility and context-dependency to complex
ing of behavior. The proposed framework is referred to as behaviors.
the ‘dual competition’ model to reflect the suggestion that Motivation: commonly defined as what makes one work to obtain a reward or
to avoid punishment. In the case of emotion (see earlier), the emphasis might
affective significance influences competition at both the
be on the evaluative aspect of the organism–environment relationship,
perceptual and executive levels – and because the impact is whereas in the case of motivation it might be on how the organism acts in a
caused by both emotion and motivation. given situation.
Resources: specific information processing mechanisms (e.g. inhibition) have
According to many proposals of attention, objects com- their own limited processing capacities or resources. Given the limited capacity
pete for limited perceptual processing capacity and control of mental resources, performance is impaired if demands are greater than
available capacity. In addition to having their own specific resources, executive
functions are proposed to share a common resource pool.
Corresponding author: Pessoa, L. (lpessoa@indiana.edu).

160 1364-6613 ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2009.01.006 Available online 13 March 2009
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Opinion Trends in Cognitive Sciences Vol.13 No.4

Figure 1. Dual competition model framework. Affective significance impacts the flow of information processing both in a (a) ‘stimulus-driven’ (note fearful face paired with
shock as input) and a (b) ‘state-dependent’ fashion based on motivational manipulations (note neutral face input). In both cases competition is suggested to occur at the
perceptual and executive levels. Arrows denote functional pathways that do not necessarily map one-to-one to specific anatomical connections. Individual differences in
state and/or trait anxiety and sensitivity to reward are expected to modulate the impact of affective significance on information processing.

she is asked in close temporal succession to switch between frontal cortex (PFC) (see later). In this manner, the modu-
tasks (e.g. Ref. [14]). lation of executive control eventually affects visual
It is hypothesized that affective significance determines processing [17] (Figure 1a, arrow 4).
the flow of information processing in at least two general The impact of an emotion-laden stimulus on behavior
ways: in a ‘stimulus-driven’ and a ‘state-dependent’ man- crucially depends on how it affects the flow of executive
ner. functions. It is hypothesized that this will depend on the
level of threat, which, accordingly, will determine if
Stimulus-driven effects emotional content enhances or impairs behavioral per-
Emotion-laden stimuli include those involving emotional formance. When emotional content is low in threat, proces-
expressions or affective scenes, in addition to originally sing is biased in favor of the emotional item (Figure 2a) –
neutral items that might have acquired affective signifi- this situation also extends to positive stimuli [18] (Box 1).
cance by previous pairing with aversive events (e.g. pairing In particular, the spatial locus of the emotional item is
with mild shock). It is hypothesized that affective signifi- privileged, possibly because items that are low in threat
cance impacts both perceptual competition and executive are somewhat ambiguous and so might attract further
control (Figure 1a). Perceptual competition, which takes attention as part of additional information gathering
place in visual cortex, is affected because emotional content [19]. In this manner, emotional content enhances target
enhances sensory representations of emotional items processing with relatively minor effects on irrelevant
(Figure 1a, arrow 1), which is well documented in human stimuli and other executive functions that might be needed
visual cortex [1]. Such enhancement depends, at least in (e.g. if task switching is involved). Thus, in the low-threat
part, on output connections from the amygdala, which is case, although emotional items are prioritized, the impact
known to project to multiple levels of visual cortex, in- on behavior is modest – in this sense, it can be said that a
cluding the primary visual cortex [15]. ‘soft’ prioritization occurs. Because the effect on perform-
Executive control is affected by emotional content ance is relatively weak, behavioral findings can be difficult
because; firstly, strengthened sensory representations will to replicate and might be observed only in high-anxious
receive prioritized attention (Figure 1a, arrow 2). For individuals (e.g. Ref. [20]). Furthermore, whereas low-
example, items with increased visual responses can direct threat emotional stimuli comprise a privileged stimulus
spatial attention towards those locations – this will occur category, their processing is highly dynamic and depends
as long as sufficient processing resources are available [16]. on the interplay of a host of factors that sculpt the associ-
Secondly, executive control is modulated because affective ated neural responses, including attention, task context,
information might be directly conveyed to control struc- awareness and perceptual interpretation [21].
tures (Figure 1a, arrow 3). For instance, amygdala outputs When emotional content is high in threat, resources are
might convey the significance of an item via connections diverted towards the processing of the item. The mobiliz-
with anterior cingulate cortex (ACC) territories, which ation of the resources is more extreme, and the effects on
might help direct attention towards the location of the behavior considerably more dramatic [22,23]. In this case,
emotional item via connections with the dorsolateral pre- the main impact on behavior comes from the recruitment of

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Opinion Trends in Cognitive Sciences Vol.13 No.4

Figure 2. Executive control and competition are viewed as involving multiple mechanisms, or resources. Larger unfilled ellipses represent executive control; smaller shapes
represent processing resources. (a) When threat level is low, affective significance enhances the processing of the item. Other executive functions are not strongly impacted
(smaller ellipses). (b–d) Processes are hypothesized to share resources, here called common-pool resources (smaller ellipses in bright blue), such that the engagement of
one will detract from the processing of the other. Common-pool resources are proposed to be necessary for general functions of attentional/effortful control. (b) High-threat
emotion-laden stimuli will typically recruit common-pool resources that allow their processing to be prioritized, which will detract from other mechanisms sharing those
resources (see intersections indicated in bright blue). (c) High threat will also trigger specific executive functions to handle the challenges to the organism, as indicated by
the arrows emanating from attentional/effortful control. For instance, ‘updating’ might be needed to refresh the contents of working memory, ‘shifting’ might be recruited to
switch the current task set and ‘inhibition’ could be called for to cancel previously planned actions. (d) State-dependent affective significance, such as reward, is
hypothesized to have two main effects on executive function. Firstly, motivation fine-tunes executive functions that are important for the task at hand (represented by the
change of shape of the updating function; see green arrow). Secondly, motivation can rearrange the allocation of common-pool resources (bright blue ellipse; see orange
arrow), thereby affecting other executive resources.

attentional/effortful control that is required to prioritize functions (see also Refs. [24–26]). Because high-threat is
the processing of high-threat information (Figure 2b) – expected to recruit such ‘common-pool resources’, it will
thus, ‘hard’ prioritization occurs. In particular, atten- impair other executive functions that are reliant on them,
tional/effortful control is envisaged as involving processing including inhibition, shifting and updating. For instance,
resources that are strongly shared by several executive in a recent study, performance during response inhibition
was compromised when participants viewed high- versus
Box 1. Positive and other stimuli low-arousing pictures [27]. Specifically, emotional scenes
preceding both go and stop stimuli increased the stop-
In the main text, the effects of emotional content on information
processing are discussed in terms of threat level because they
signal reaction time, a measure of the temporal evolution
provide the clearest example of cognitive-emotional interactions in of inhibitory processes (see also Ref. [28]). The processing of
which both perceptual and executive competition are needed to threat typically will require further actions and, in
explain how affectively potent information impacts behavior (e.g. addition to the consumption of common resources, could
see Figure 3c,d in main text). However, the framework should be involve the triggering of multiple mechanisms that are
generalized to consider other stimulus classes, including high-
intensity perceptual stimuli (including items high in arousal but of
specific to the task at hand (Figure 2c).
neutral valence [60]), novel and erotic stimuli. In these cases, Although the notion of resources has at times been
stimulus-driven effects might function as in the low threat situation, viewed as vague [29] (but see Ref. [30]), one approach to
although stronger effects might be generated by items of suffi- understanding resource consumption could be to probe the
ciently high arousal (e.g. Ref. [61]). In other words, high-arousal
correspondence of brain sites that are sensitive to specific
items can command a form of ‘hard prioritization’ (see main text)
such that processing resources needed by executive functions are experimental conditions. It is particularly instructive, for
devoted to their processing, thereby impairing task performance in instance, to observe the overlap between attentional
a manner analogous to that shown in Figure 2b (in the main text). In manipulations and those that are sensitive to higher levels
particular, exposure to erotica enhances visual responses [62] and of threat. The ‘attentional network’ has been extensively
can interfere with ongoing tasks [63,64]. Interestingly, during the
researched and is believed to involve fronto-parietal
viewing of these items, both the amygdala and the ventral striatum
are strongly recruited, in addition to the ACC [65]. Because these regions, including the middle frontal gyrus (MFG), ACC,
regions are key nodes of the scheme proposed in Figure 4 (in the inferior frontal gyrus (IFG) and anterior insula [31,32]. To
main text), the interaction between the processing of erotic stimuli assess brain regions that are sensitive to high levels of
and cognitive function might function in a manner closely related to threat, the activation sites of the contrast of CS+ (i.e.
that proposed here for threat-related information.
stimuli paired with an unconditioned stimulus) versus

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Opinion Trends in Cognitive Sciences Vol.13 No.4

versus safe faces were observed in several of the same


fronto-parietal regions. To further test the idea that
additional processing resources were recruited during
the viewing of threatening stimuli (relative to safe), in a
new analysis, we correlated evoked fMRI responses in the
regions modulated by attentional load with behavioral
accuracy during the task. As illustrated in Figure 3d,
the higher the ACC recruitment during the threat con-
dition, the worse the behavioral performance (relative to
the safe condition; p < 0.05). Interestingly, a similar pat-
tern of results was observed in multiple regions, including
MFG, IFG and anterior insula, in addition to superior
parietal lobule (although the exact spatial overlap between
attentional load and threat effects varied slightly for these
regions). Consistent with the increased processing of
shock-paired stimuli, such stimuli exhibited increased
behavioral priming and fMRI repetition effects relative
to unpaired faces during a subsequent implicit-memory
task [33]. These findings indicate that consumption of
processing resources engaged by task-irrelevant threat
faces (as indicated via, e.g. ACC responses) impaired per-
Figure 3. Processing resources and threat. Summary of results from 34 positron formance on the main task.
emission tomography (PET) and fMRI studies of conditioning from 1995 to 2008,
illustrating the coordinates provided for the contrast of threat (CS+) versus safe
Overall, interactions between high threat processing
(CS-). (a) Activation peaks that were observed in the ACC, or nearby cortex, are and executive functions are proposed to take place via at
shown in green for right hemisphere results and red for left hemisphere results (all least three types of neural mechanisms (Figure 4). Firstly,
coordinates were projected onto a midline view for display purposes). (b) Results
for the right lateral surface are shown on an inflated surface to reveal multiple PFC
it is hypothesized that threat processing engages atten-
sites, including ones that are not on the surface. These included the middle frontal tional/effortful control mechanisms in the ACC and, in
gyrus, inferior frontal gyrus and anterior insula (note that the surface inflation particular, the dorsal site observed in the previous analysis
‘pushed up’ some of the activation sites relative to their standard anatomical
positions). (c) Subjects viewed an array of letters superimposed on task-irrelevant
(see inset in Figure 3d) – in contrast to more rostral sites
faces and were asked to report whether or not the target letter X was present [33]. [34]. The ACC is important for integrating inputs from
During the low attentional load condition shown here, the target appeared among multiple sources, including affective and motivational
a uniform array of distractors (’pop-out’ condition). During the high attentional
load condition (not shown), a non-uniform array of letters was employed (search inputs [35,36] – and in this respect works in close coopera-
condition). During the threat condition, faces were previously paired with mild tion with the anterior insula and OFC [37]. The ACC has
electrical shock, whereas safe stimuli were never paired with shock. (d) Differential also been suggested to be involved in conflict detection,
responses to task-irrelevant threat and safe faces were inversely correlated with
behavioral performance, suggesting that the processing of threat captured error likelihood processing and error monitoring, and helps
processing resources needed for task execution as a function of threat-related determine the benefits and costs of acting. It is suggested
responses. Results are shown for a region of interest in the ACC that was defined in
here that ACC engagement during threat will impair
terms of a separate contrast of high versus low attentional load (shown in the
inset). Data reanalyzed from Ref. [33]. executive function because common-pool resources that
are required to prioritize threat processing are taken up.
Secondly, threat also recruits multiple PFC sites that are
CS- (i.e. stimuli never followed by an unconditioned involved in specific executive functions (Figure 4, green
stimulus) of 34 aversive conditioning studies were arrows). This recruitment is suggested to depend, at least
reviewed here. In addition to the amygdala, several frontal in part, on the ACC, whose signals are known to influence
activation sites were consistently reported, including
MFG, ACC, IFG and anterior insula (Figure 3a,b). Thus,
it seems that high-threat processing engages key nodes of
the attentional network, consistent with the notion that it
is linked to resource consumption.
It is possible to further operationalize resource con-
sumption by linking observed evoked functional magnetic
resonance imaging (fMRI) responses and behavioral per-
formance. For instance, in a recent experiment [33], sub-
jects performed a search task under low and high
attentional demands (Figure 3c), which were contrasted
to determine brain sites sensitive to the availability of
processing resources. Differential responses (high versus
low) were observed in several fronto-parietal regions com- Figure 4. Effects of threat and motivation on executive function. Key brain regions
monly associated with the attentional network, including mediating the interactions between emotion and/or motivation with executive
the ones previously listed. In the same study, subjects were control function. Both types of interaction are hypothesized to depend on the
anterior cingulate cortex (ACC). Abbreviations: DLPFC, dorsolateral PFC; IFG,
also shown task-irrelevant threat and safe faces inferior frontal gyrus; LC, locus coeruleus; Nacc, nucleus accumbens; OFC,
(Figure 3c). Interestingly, increased responses to threat orbitofrontal cortex; VTA, ventral tegmental area.

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Opinion Trends in Cognitive Sciences Vol.13 No.4

activity in other brain regions and to modulate cognitive, (Figure 2d, green arrow) – as opposed to general effects,
motor and visceral responses [35]. For instance, the ACC such as arousal. Recent behavioral results are consistent
might engage the MFG, which is important in the manip- with this notion. For instance, motivation affected both the
ulation of information, among other important functions. orienting and reorienting of attention, and the impact was
In this manner, additional specific processing resources evident during both exogenous [47] and endogenous tasks
are diverted to the processing of threat information (J. B. Engelmann et al., unpublished*). Observed effects
(Figure 4, orange regions). Thirdly, threat affects executive were specific, such that detection sensitivity (i.e. dprime)
functions by inducing state changes that are implemented increased as a function of absolute incentive level. In
via ascending systems [38,39] (Figure 4, red arrows). parallel with improvements in behavioral performance,
The neural interactions described previously indicate fMRI responses in visual cortex also increased as a function
that the effects of affective significance on behavioral of absolute incentive level. Therefore, the findings indicate
performance will typically depend on multiple factors. that elevated motivation leads to improved efficiency in
For example, emotional content will enhance stimulus- orienting and reorienting of attention and that one mech-
driven processing in a way that could enhance or impair anism by which attention and motivation interact involves
task performance. An important dimension in determining the enhancement of attention during motivationally sali-
the impact of affective significance on information proces- ent conditions – resulting in the boosting of responses in
sing is task relevance. Specifically, an emotion-laden item occipitotemporal visual regions engaged by the task at
that is task relevant will often improve behavioral per- hand (Figure 1b, arrow 4) (see also Refs [45,46,48,49]).
formance because additional processing resources will Secondly, motivation is proposed to recalibrate the allo-
typically be devoted to it (relative to neutral). At the same cation of processing resources available to executive func-
time, a task irrelevant emotional item will usually impair tions, to maximize potential reward. Because of capacity
performance because resources will be taken away from sharing, such reallocation is suggested to impact not only
the main task. As described, another important dimension target functions directly associated with rewarded beha-
of emotional information corresponds to the level of threat. viors but also other processes that share some of the same
On the one hand, emotional items that are relatively low in processing resources (Figure 2d, orange arrow). In this
threat will benefit from sensory enhancement, which might manner, motivation could affect executive function in a
improve, for instance, reaction time when the item is task way that is actually deleterious to behavioral performance.
relevant. On the other hand, emotional items that are For instance, in a recent study, participants who were
relatively high in threat will lead to enhanced sensory rewarded for accurate and fast performance on go trials
enhancement but, crucially, will also divert processing of a stop-signal task exhibited impaired inhibitory per-
resources away from other mechanisms. Thus, in many formance as evidenced by prolonged stop-signal reaction
tasks, items that are high in threat will impair behavioral time (S. Padmala and L. Pessoa, unpublishedy). One
performance even though sensory processing is enhanced. possibility is that, to maximize reward, participants
The impairment will be typically observed when the item is enhanced attention to the go stimulus, leaving fewer
task irrelevant, especially in high-anxious individuals [26]. resources to process the stop stimulus (see Ref. [50]). In
this sense, incentives can be viewed as reallocating
State-dependent effects resources to prioritize the processing of the rewarded
State-dependent effects on executive control depend on function in a way that is similar to that discussed for
general factors such as mood and anxiety [40]. This section threat processing.
focuses instead on a less explored source of state-depend- As in the case of threat processing, it is hypothesized
ent effects on executive function involving reward-related that motivation influences executive function by engaging
manipulations of motivation. the ACC, partly via influences from the ventral striatum
A wealth of non-human and human studies has and OFC (Figure 4). As before, it is hypothesized that
described brain regions that are involved in the repres- motivation-related ACC recruitment has an important role
entation of reward [41]. However, how motivation impacts in controlling the operations of other brain regions, so as to
other brain regions that contribute to improving beha- maximize utility (i.e. maximize reward or minimize pun-
vioral performance has received less attention. In humans, ishment); see Figure 4, green arrows. For instance, the
important steps in attempting to fill in this gap have been dorsolateral PFC might be recruited to resolve conflict in a
taken in recent years. For instance, Locke and Braver [42] way that increases utility. Motivation also affects execu-
showed that incentives modulated task performance, tive functions by inducing state changes that are imple-
potentially by altering the control strategy employed by mented via ascending systems – again, in a way that is
participants. Neuroimaging data indicated that the reward parallel to threat (Figure 4, red arrows). For instance,
condition was associated with a sustained increase in incentives affect responses in the locus coeruleus (LC),
parietal and PFC regions of the right hemisphere (see also which regulates norepinephrine function, and also modu-
Refs [43–46]). late dopaminergic function. LC phasic firing often tracks
It is hypothesized that motivation, like threat, impacts *
J. B. Engelmann et al. (2009). Combined effects of attention and motivation on
both perceptual competition and executive control visual task performance: transient and sustained motivational effects. Frontiers in
(Figure 1b). Furthermore, motivation has two main effects Human Neuroscience (submitted).
y
on executive function. Firstly, reward will lead to the S. Padmala and L. Pessoa. Motivation and inhibitory control: reward delays
response inhibition and decreases responses in inferior frontal cortex. Paper/poster
sharpening of executive functions. Crucially, reward is presentation at the 38th Annual Meeting of the Society for Neuroscience, Washington,
suggested to have specific influences on cognitive function D.C., 2008.

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Opinion Trends in Cognitive Sciences Vol.13 No.4

Box 2. Questions for future research research has attempted to investigate how motivation
directly interacts with executive function. The goal of the
 Can the dual competition framework be extended to other sensory
modalities? The answer seems to be in the affirmative, at least for dual competition framework is to propose basic elements of a
auditory stimuli [66]. conceptual framework with which to understand how both
 Can positive stimuli ever lead to a ‘hard’ prioritization of emotion and motivation are integrated with executive con-
processing that is comparable to that of threat? In at least one trol. An important implication of the proposal is that
case, we failed to observe comparable effects [61].
emotion and motivation can either enhance or impair beha-
 Is the impact of higher levels of threat the same across distinct
executive functions? For instance, does an affectively potent item vioral performance depending on how they interact with key
impair conflict processing and behavioral inhibition to a similar control functions. Carefully characterizing how emotion and
extent? motivation can be beneficial or deleterious to behavior (e.g.
 Can the model be extended to a broader range of motivational as in drug addiction) constitutes a great challenge for future
states, including thirst, hunger and sexual drive?
 Should executive functions be viewed as tied to specific regions
research (Box 2).
or are they better conceptualized as engaging specific networks of
brain regions [67]? Acknowledgements
I would like to thank Todd Braver, Josh Brown, Greg Hajcak, Seung-Lark
Lim, Leticia Oliveira, Srikanth Padmala, Mirtes Pereira and the
anonymous reviewers for their insightful feedback on earlier versions of
task-relevant processes, such as target stimuli, but not the manuscript. I am indebted to Seung-Lark Lim for the review of
task-irrelevant items, such as distractors (see Ref. [51]). activation sites shown in Figures 3a,b and for the data analysis shown in
These and other findings have led to the suggestion that Figure 3d. Finally, I thank Andrew Bauer and Srikanth Padmala for
the LC is responsive to ongoing evaluations of task utility assistance with figures. The author’s work is partly funded by the
National Institute of Mental Health (R01 MH071589).
provided by input from frontal structures [51].
The notion that motivation interacts with executive References
functions to meet current behavioral demands and oppor- 1 Vuilleumier, P. (2005) How brains beware: neural mechanisms of
tunities is well supported by animal studies of reward, too. emotional attention. Trends Cogn. Sci. 9, 585–594
2 Phelps, E.A. (2006) Emotion and cognition: insights from studies of the
For instance, Redgrave and colleagues [52,53] have pro-
human amygdala. Annu. Rev. Psychol. 57, 27–53
posed that the dopamine response, and consequently the 3 Pessoa, L. (2008) On the relationship between emotion and cognition.
related striatal function, might be viewed as providing a Nat. Rev. Neurosci. 9, 148–158
signal that facilitates the reallocation of limited behavioral 4 Desimone, R. and Duncan, J. (1995) Neural mechanisms of selective
and cognitive processing capacity towards unexpected attention. Annu. Rev. Neurosci. 18, 193–222
5 Pashler, H. (1998) The Psychology of Attention. MIT Press
events of behavioral significance, including rewarding
6 Kahneman, D. (1973) Attention and Effort. Prentice-Hall
ones. These and other results (e.g. Refs [54,55]) are con- 7 Norman, D.A. (1975) On data-limited and resource-limited processes.
sistent with the notion that striatal activation drives the Cognit. Psychol. 7, 44–64
reallocation of available resources to process salient events 8 Norman, D.A. and Shallice, T. (1986) Attention to action: willed and
whose processing is then prioritized – instead of simply automatic control of behavior. In Consciousness and Self-Regulation
(Davidson, R.J. et al., eds), pp. 1–18, Plenum
providing a ‘reward signal’. 9 Baddeley, A. (2003) Working memory: looking back and looking
Above, interactions between emotion and motivation forward. Nat. Rev. Neurosci. 4, 829–839
with executive functions were discussed in terms of 10 Stuss, D.T. and Knight, R.T., eds (2002) Principles of Frontal Lobe
stimulus-driven and state-dependent effects, respectively. Function, Oxford University Press
However, these two types of effects were not meant to 11 Smith, E.E. and Jonides, J.J. (1999) Neurosicence – storage and
executive processes in the frontal lobes. Science 283, 1657–1661
diagnostically capture the differences between emotion 12 Miyake, A. et al. (2000) The unity and diversity of executive functions
and motivation. For instance, when one is hungry (i.e. in and their contributions to complex ‘Frontal Lobe’ tasks: a latent
a motivational state of hunger), food items are salient and variable analysis. Cognit. Psychol. 41, 49–100
can direct attention in a stimulus-related fashion [46]. 13 Duncan, J. et al. (1996) Intelligence and the frontal lobe:
the organization of goal-directed behavior. Cognit. Psychol. 30, 257–
Conversely, anxiety might be thought of as an emotional
303
state of sustained threat, and leads to state-dependent 14 Verbruggen, F. et al. (2004) The interaction between stop signal
effects [56], too. Finally, in general, emotion and motiv- inhibition and distractor interference in the flanker and Stroop task.
ation are broad constructs and here, for brevity, we focus on Acta Psychol. (Amst.) 116, 21–37
threat and reward processing only (Box 1). 15 Amaral, D.G. et al. (1992) Anatomical organization of the primate
amygdaloid complex. In The Amygdala: Neurobiological Aspects of
Emotion, Memory, and Mental Dysfunction (Aggleton, J., ed.), pp. 1–
Conclusions 66, Wiley-Liss
The proposed framework of how emotion and motivation 16 Pessoa, L. (2005) To what extent are emotional visual stimuli processed
interact with executive functions draws upon several ideas without attention and awareness? Curr. Opin. Neurobiol. 15, 188–196
in the literature, including biased competition [4] and 17 Egner, T. and Hirsch, J. (2005) Cognitive control mechanisms resolve
conflict through cortical amplification of task-relevant information.
resource theory [6,7,30,57] – see also Braver et al. [58] Nat. Neurosci. 8, 1784–1790
and Robbins et al. [59] for complementary proposals. A 18 Brosch, T. et al. (2008) Beyond fear: rapid spatial orienting toward
considerable body of work has investigated how emotional positive emotional stimuli. Psychol. Sci. 19, 362–370
stimuli are prioritized in terms of attentional processes [1]. 19 Whalen, P.J. (1998) Fear, vigilance, and ambiguity: initial
However, less research has been devoted to understanding neuroimaging studies of the human amygdala. Curr. Dir. Psychol.
Sci. 7, 177–188
the integration of emotional information and executive 20 Fox, E. et al. (2001) Do threatening stimuli draw or hold
control. Likewise, a large amount of literature has con- visual attention in subclinical anxiety? J. Exp. Psychol. Gen. 130,
sidered the neural substrates of reward [41]. Again, less 681–700

165
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For personal use only. No other uses without permission. Copyright ©2017. Elsevier Inc. All rights reserved.
Opinion Trends in Cognitive Sciences Vol.13 No.4

21 Ohman, A. (2002) Automaticity and the amygdala: nonconscious 45 Small, D.M. et al. (2005) Monetary incentives enhance processing in
responses to emotional faces. Curr. Dir. Psychol. Sci. 11, 62–66 brain regions mediating top-down control of attention. Cereb. Cortex
22 Panksepp, J. (1998) Affective Neuroscience: The Foundations of Human 15, 1855–1865
and Animal Emotions. Oxford University Press 46 Mohanty, A. et al. (2008) The spatial attention network interacts with
23 Lang, P.J. et al. (2000) Fear and anxiety: animal models and human limbic and monoaminergic systems to modulate motivation-induced
cognitive psychophysiology. J. Affect. Disord. 61, 137–159 attention shifts. Cereb. Cortex 18, 2604–2613
24 Mathews, A. and Mackinstosh, B. (1998) A cognitive model of selective 47 Engelmann, J.B. and Pessoa, L. (2007) Motivation sharpens exogenous
processing in anxiety. Cognit. Ther. Res. 22, 539–560 spatial attention. Emotion 7, 668–674
25 Eysenck, M.W. et al. (2007) Anxiety and cognitive performance: 48 Serences, J.T. (2008) Value-based modulations in human visual cortex.
attentional control theory. Emotion 7, 336–353 Neuron 60, 1169–1181
26 Bishop, S.J. (2007) Neurocognitive mechanisms of anxiety: an 49 Della Libera, C. and Chelazzi, L. (2006) Visual selective attention and
integrative account. Trends Cogn. Sci. 11, 307–316 the effects of monetary rewards. Psychol. Sci. 17, 222–227
27 Verbruggen, F. and De Houwer, J. (2007) Do emotional stimuli 50 Boehler, C.N. et al. (2008) Sensory MEG responses predict successful
interfere with response inhibition? Evidence from the stop signal and failed inhibition in a stop-signal task. Cereb. Cortex 19, 134–
paradigm. Cogn. Emotion 21, 391–403 145
28 Blair, K.S. et al. (2007) Modulation of emotion by cognition and 51 Aston-Jones, G. and Cohen, J.D. (2005) An integrative theory of locus
cognition by emotion. Neuroimage 35, 430–440 coeruleus-norepinephrine function: adaptive gain and optimal
29 Navon, D. (1984) Resources–A theoretical soup stone? Psychol. Rev. 91, performance. Annu. Rev. Neurosci. 28, 403–450
216–234 52 Redgrave, P. et al. (1999) Is the short-latency dopamine response too
30 Park, S. et al. (2007) Concurrent working memory load can facilitate short to signal reward error? Trends Neurosci. 22, 146–151
selective attention: evidence for specialized load. J. Exp. Psychol. Hum. 53 Redgrave, P. and Gurney, K. (2006) The short-latency dopamine signal:
Percept. Perform. 33, 1062–1075 a role in discovering novel actions? Nat. Rev. Neurosci. 7, 967–975
31 Kastner, S. and Ungerleider, L.G. (2000) Mechanisms of visual 54 Horvitz, J.C. (2000) Mesolimbocortical and nigrostriatal dopamine
attention in the human cortex. Annu. Rev. Neurosci. 23, 315–341 responses to salient non-reward events. Neuroscience 96, 651–656
32 Corbetta, M. and Shulman, G.L. (2002) Control of goal-directed and 55 Zink, C.F. et al. (2004) Human striatal responses to monetary reward
stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 depend on saliency. Neuron 42, 509–517
33 Lim, S.L. et al. (2008) Affective learning modulates spatial competition 56 Grillon, C. (2008) Models and mechanisms of anxiety: evidence from
during low-load attentional conditions. Neuropsychologia 46, 1267– startle studies. Psychopharmacology (Berl.) 199, 421–437
1278 57 Lavie, N. et al. (2004) Load theory of selective attention and cognitive
34 Bush, G. et al. (2000) Cognitive and emotional influences in anterior control. J. Exp. Psychol. Gen. 133, 339–354
cingulate cortex. Trends Cogn. Sci. 4, 215–222 58 Braver, T.S. et al. (2007) Explaining the many varieties of working
35 Devinsky, O. et al. (1995) Contributions of anterior cingulate cortex to memory variation: dual mechanisms of cognitive control. In Variation
behaviour. Brain 118, 279–306 in Working Memory (Conway, A.R.A. et al., eds), pp. 76–106, Oxford
36 Rushworth, M.F. et al. (2007) Functional organization of the medial University Press
frontal cortex. Curr. Opin. Neurobiol. 17, 220–227 59 Robbins, T.W. (2007) Shifting and stopping: fronto-striatal substrates,
37 Barbas, H. (1995) Anatomic basis of cognitive-emotional interactions in neurochemical modulation and clinical implications. Philos. Trans. R.
the primate prefrontal cortex. Neurosci. Biobehav. Rev. 19, 449–510 Soc. Lond. 362, 917–932
38 Heimer, L. and Van Hoesen, G.W. (2006) The limbic lobe and its output 60 Mourão-Miranda, J. et al. (2003) Contributions of emotional valence
channels: implications for emotional functions and adaptive behavior. and arousal to visual activation during emotional perception.
Neurosci. Biobehav. Rev. 30, 126–147 Neuroimage 20, 1950–1963
39 Sarter, M. and Bruno, J.P. (2000) Cortical cholinergic inputs mediating 61 Pereira, M.G. et al. (2006) Sustained and transient modulation of
arousal, attentional processing and dreaming: differential afferent performance induced by emotional picture viewing. Emotion 6, 622–
regulation of the basal forebrain by telencephalic and brainstem 634
afferents. Neuroscience 95, 933–952 62 Bradley, M.M. et al. (2003) Activation of the visual cortex in motivated
40 Eysenck, M.W. and Calvo, M.G. (1992) Anxiety and performance: the attention. Behav. Neurosci. 117, 369–380
processing efficiency theory. Cogn. Emotion 6, 409–434 63 Schupp, H.T. et al. (2007) Selective visual attention to emotion. J.
41 Schultz, W. (2000) Multiple reward signals in the brain. Nat. Rev. Neurosci. 27, 1082–1089
Neurosci. 1, 199–207 64 Most, S.B. et al. (2007) The naked truth: positive, arousing distractors
42 Locke, H.S. and Braver, T.S. (2008) Motivational influences on impair rapid target perception. Cogn. Emotion 21, 964–981
cognitive control: behavior, brain activation, and individual 65 Karama, S. et al. (2002) Areas of brain activation in males and females
differences. Cogn. Affect. Behav. Neurosci. 8, 99–112 during viewing of erotic film excerpts. Hum. Brain Mapp. 16, 1–13
43 Pochon, J.B. et al. (2002) The neural system that bridges reward and 66 Brosch, T. et al. (2008) Behold the voice of wrath: cross-modal
cognition in humans: an fMRI study. Proc. Natl. Acad. Sci. U. S. A. 99, modulation of visual attention by anger prosody. Cognition 106,
5669–5674 1497–1503
44 Gilbert, A.M. and Fiez, J.A. (2004) Integrating rewards and cognition 67 Dosenbach, N.U. et al. (2008) A dual-networks architecture of top-down
in the frontal cortex. Cogn. Affect. Behav. Neurosci. 4, 540–552 control. Trends Cogn. Sci. 12, 99–105

166
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For personal use only. No other uses without permission. Copyright ©2017. Elsevier Inc. All rights reserved.

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