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Human Brain Mapping 31:1446–1457 (2010)
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Emotional Imagery: Assessing Pleasure and
Arousal in the Brain’s Reward Circuitry
Vincent D. Costa, Peter J. Lang*, Dean Sabatinelli, Francesco Versace, and
Margaret M. Bradley
NIMH Center for the Study of Emotion and Attention, University of Florida, Gainesville, Florida
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Abstract: Research on emotional perception and learning indicates appetitive cues engage nucleus
accumbens (NAc) and medial prefrontal cortex (mPFC), whereas amygdala activity is modulated by
the emotional intensity of appetitive and aversive cues. This study sought to determine patterns of
functional activation and connectivity among these regions during narrative emotional imagery. Using
event-related fMRI, we investigate activation of these structures when participants vividly imagine
pleasant, neutral, and unpleasant scenes. Results indicate that pleasant imagery selectively activates
NAc and mPFC, whereas amygdala activation was enhanced during both pleasant and unpleasant imagery. NAc and mPFC activity were each correlated with the rated pleasure of the imagined scenes,
while amygdala activity was correlated with rated emotional arousal. Functional connectivity of NAc
and mPFC was evident throughout imagery, regardless of hedonic content, while correlated activation
of the amygdala with NAc and mPFC was specific to imagining pleasant scenes. These findings provide strong evidence that pleasurable text-driven imagery engages a core appetitive circuit, including
NAc, mPFC, and the amygdala. Hum Brain Mapp 31:1446–1457, 2010. VC 2010 Wiley-Liss, Inc.
Key words: liking; mental imagery; mesocorticolimbic; script-driven imagery; psychophysiological
interaction; ventral striatum; ventral medial prefrontal cortex
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INTRODUCTION
Additional Supporting Information may be found in the online
version of this article.
Contract grant sponsor: National Institute of Mental Health;
Contract grant number: P50 MH 72850 [to the Center for the
Study of Emotion and Attention (CSEA), University of Florida,
Gainesville, FL]; Contract grant sponsor: National Institute of
Mental Health; Contract grant number: F31 MH080551 (National
Research Service Award to Vincent D. Costa).
Dean Sabatinellli is currently at University of Georgia, Athens,
Georgia, USA.
Francesco Versace is currently at MD Anderson Cancer Center at
the University of Texas, Houston, Texas, USA.
*Correspondence to: Peter J. Lang, NIMH Center for the Study of
Emotion and Attention, University of Florida, P.O. Box 112766,
Gainesville, Florida 32611, USA. E-mail: [email protected]
Received for publication 17 June 2009; Revised 4 September 2009;
Accepted 19 October 2009
DOI: 10.1002/hbm.20948
Published online 2 February 2010 in Wiley Online Library
(wileyonlinelibrary.com).
C 2010 Wiley-Liss, Inc.
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Reading an exciting novel or listening to an engaging
story can prompt vivid imagery of the described events
and reported feelings of intense emotion. Research has
repeatedly confirmed this phenomenon and demonstrated
that text-driven imagery prompts heightened autonomic
and somatic reactions consistent with affective engagement
[Cuthbert et al., 2003; Lang and McTeague, 2009;
McTeague et al., 2009; Orr et al., 1993; Vrana et al., 1986;
Vrana and Lang, 1990; Witvliet and Vrana, 1995]. Perhaps
because the evocation of vivid fear imagery has been an
important method in the psychological treatment of phobias and anxiety [Lang, 1977; Wolpe, 1958], clinical studies
that utilize narrative imagery for symptom provocation
[Cuthbert et al., 2003; Lang and McTeague, 2009;
McTeague et al., 2009; Orr et al., 1993] have mainly
assessed reactivity during aversive imagery. This emphasis
also characterizes related neuroimaging research [Britton
et al., 2005; Dougherty et al., 1999; Shin et al., 2000; Sinha
et al., 2004] that consistently reports increased activation
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Emotional Imagery Activates Reward Circuits
in the brain’s aversive system [Lang and Davis, 2006],
including the amygdala and related paralimbic regions.
While research on emotional perception and learning
clearly indicates that the amygdala encodes the emotional
intensity of both appetitive and aversive stimuli [Baxter
and Murray, 2002; Davis and Whalen, 2001; McGaugh,
2004; Zald, 2003], there is debate as to whether NAc activation is driven by the pleasantness of a stimulus or its
salience [Berridge et al., 2009]. Evidence from studies of
pleasant visual perception [Aharon et al., 2001; Sabatinelli
et al., 2007] and reward processing [Breiter et al., 2001;
Cooper and Knutson, 2007; Knutson et al., 2005] indicates
that the nucleus accumbens (NAc) and medial prefrontal
cortex (mPFC) are selectively activated for pleasurable
stimuli that are readily discerned. On the other hand,
based on studies using a wide variety of populations,
paradigms, and procedures, there is also evidence that
NAc activity increases in response to both pain and pleasure [Leknes and Tracey, 2008]. This raises the question of
whether mesolimbic activation during narrative emotional
imagery will reflect the hedonic valence or the salience
(emotional arousal) of the imagined scenes.
Consistent with the view that imagery and perception of
emotional stimuli engage similar motivational circuitry
[Lang, 1979, 1994], narrative imagery of drug craving
heightened regional cerebral blood flow (rCBF) in NAc
and amygdala in cocaine-dependent men and women
[Kilts et al., 2001, 2004], and imagery of pleasant sexual
encounters/athletic success increased rCBF in ventral pallidum (an efferent target of NAc) in men [Rauch et al.,
1999]. Yet because prior studies have not examined NAc
activation during both pleasant and unpleasant imagery, it
remains plausible that unpleasant imagery could also
prompt increased activation of NAc, consistent with a salience account. The novel aim of this study is to determine,
using a well-founded imagery procedure [Cuthbert et al.,
2003; Lang and McTeague, 2009; McTeague et al., 2009], if
imagining prototypical pleasant scenes uniquely activates
mesolimbic reward circuitry in healthy males and females,
whether amygdala activation is found when imagining
both pleasant and unpleasant scenes, and how functional
connectivity among these three regions varies with
hedonic content.
It is hypothesized that relative to neutral and unpleasant
scenes, imagining pleasurable scenes will selectively activate NAc and mPFC, whereas compared to neutral imagery, processing arousing emotional content—pleasant or
unpleasant—will heighten amygdala activation. We also
examined the relationship between signal change in these
regions and participants’ ratings of pleasure and emotional
arousal for the imagined scenes. Based on prior findings
during emotional perception [Anderson et al., 2003;
Cloutier et al., 2008; Knutson et al., 2005; Sabatinelli et al.,
2005, 2007], pleasure ratings are expected to correlate positively with signal change in NAc and mPFC, while emotional arousal ratings should correlate positively with
amygdala activity.
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NAc and mPFC heavily innervate one another [Ongur
and Price, 2000] and each region receives amygdala afferents [Friedman et al., 2002]. If these anatomical connections support a circuit underlying appetitive processing,
functional connectivity among these structures is expected
to vary with hedonic content. Predicated on the hypothesized sensitivity of NAc and mPFC to pleasure, temporal
covariation of mesolimbic activation is anticipated during
pleasant imagery and possibly overall. Because of the
amygdala’s sensitivity to emotional arousal, its functional
connectivity with structures specifically sensitive to pleasure will reflect appetitive arousal. This suggests that functional connectivity of the amygdala with NAc or mPFC or
both will occur only when imagining pleasant contents.
MATERIALS AND METHODS
Participants
Thirty-two students (16 women, mean age ¼ 19.1, SD ¼
1.5) from introductory psychology courses participated for
course credit or for $20. Participants were right-handed,
had normal visual acuity, and reported no history of claustrophobia, psychopathology, or neurological insult in a telephone interview. Informed consent was obtained as
stipulated by the institutional review board. Three participants were excluded due to excessive head motion or technical errors, resulting in a final sample of 29 participants.
Materials and Design
Forty-two narratives were selected from the Affective
Norms of English Text [ANET; Bradley and Lang, 2007;
see Supporting Information Table S2 for a full listing]
based on standardized ratings of pleasure and arousal and
were categorized as pleasant (e.g., winning the lottery; n ¼
12), neutral (e.g., reading the newspaper; n ¼ 6), or
unpleasant (e.g., a car accident; n ¼ 24).1 Prior to scanning,
participants briefly read and imagined each scene and
rated their experience of pleasure and arousal using
graphic Self-Assessment Manikin scales [Bradley and
Lang, 1994; Lang, 1980]. Texts were written to be read in
12 s and their presentation counterbalanced so that no
more than two trials of the same hedonic content occurred
in succession. Multivariate comparison of sentence properties indicated that emotional and neutral sentences did not
differ in word, syllable, or character counts [F(6,74) ¼ 1.95,
ns].
The imagery procedure consisted of 42 trials. Each trial
began with visual presentation of a text for 12 s, backward
1
The additional 12 unpleasant scenes described specific fear-relevant
scenarios (dental and snake fear) and were included in the design to
allow future comparisons with clinical populations. Analyses that
excluded these categories yielded the same pattern of results.
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Costa et al.
projected onto a monitor (640 " 480 pixel resolution) situated behind the participant’s head, and viewed using a
head-coil mounted mirror (IFIS-SA, Invivo, Orlando, FL).
The visual offset of the text signaled participants to continue imagining the scene they had just read. Twelve seconds later, a brief (400 ms) change in the color of the
screen, perceptible as a flash, signaled that imagery should
end and was followed by a fixed 12-s intertrial interval.
After the experiment, participants rated the overall difficulty of imagining the presented scenes (1 ¼ very difficult
to 9 ¼ not difficult at all). On average participants
reported little difficulty in completing the imagery task
(mean difficulty rating ¼ 6.78, SD ¼ 1.13).
Procedure
After entering the scanner, participants were instructed
to silently read each text as it appeared and to continue to
imagine their active involvement in the described event,
until a brief change in the color of the screen alerted the
participant to stop imagining. Except during text presentations, participants were told to maintain their gaze on a
fixation cross presented at the center of the monitor.
Data Acquisition and Analysis
A T1-weighted anatomical volume was acquired using a
Siemens 3T Allegra MR scanner. A total of 506 functional
volumes (50 coronal slices, 2.5 mm thick, 0.5 mm gap)
were collected using a T2*-weighted echo planar imaging
sequence (3 s TR, 35 ms TE, 160 mm FOV, 64 " 64 acquisition matrix).
Functional data were slice-time adjusted, motion-corrected, spatially smoothed (5-mm FWHM Gaussian kernel), and converted to percent blood oxygen leveldependent (BOLD) signal change using the Analysis of
Functional Neuroimages software [Cox, 1996]. A multiple
linear regression (MLM) model deconvolved hemodynamic responses for the three hedonic contents as a linear
combination of eight uniform B-spline basis functions.
This generated a time series of beta coefficients at each
voxel equaling the length of a single trial (24 s), beginning
with text presentation and extending through the imagery
period. Additional regressors modeled motion residuals
and baseline drift. Resultant time series were spatially normalized [Talariach and Tournoux, 1988] and resampled to
a 2.5 mm isotropic voxel size.
Using participants’ average percent BOLD signal change
during imagery following text presentation, three mixed
effects ANOVAs identified voxels with greater activation
during pleasant compared to neutral imagery, unpleasant
compared to neutral imagery, and pleasant compared to
unpleasant imagery. Nonparametric permutation tests were
computed following recommended guidelines [Nichols and
Holmes, 2002] to determine critical t-statistic values for each
contrast that corrected for multiple comparisons across the
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volume. In each permutation test, labels coding hedonic content were randomly reassigned within participants and
checked for independence from previous permutation
orders. A t-statistic was then generated at each voxel and a
Gaussian function fit to their distribution over the entire
brain. The value of the t-statistic at the 99.9 percentile of the
fitted Gaussian distribution was selected to form a permutation distribution based on 10,000 randomizations. The resulting absolute thresholds that corrected for multiple
comparisons at P < 0.05 were t ¼ 3.71 (P < 0.0008 uncorrected) when contrasting pleasant to neutral imagery, t ¼
4.07 (P < 0.0003 uncorrected) when contrasting unpleasant
to neutral imagery, and t ¼ 4.2 (P < 0.0002 uncorrected)
when contrasting pleasant to unpleasant imagery.
Functional regions of interest (ROI) for NAc and mPFC
were based on cluster locations identified in the group
contrast of pleasant compared to neutral imagery and for
the amygdala based on the conjoined group contrasts of
pleasant and unpleasant compared to neutral imagery. Average BOLD activity was extracted for each ROI from a
109 ll volume within the area of interest and surrounding
a significant peak activation (P < 0.05 uncorrected) in each
participants’ spatially normalized contrast maps. Assuming that imagery begins as a text is read, we analyzed
BOLD activity in an early window, during the 12-s text
presentation, and at a later 12-s window when text was no
longer on the screen. Mean BOLD signal change for each
window was deviated from a baseline immediately prior
to text presentation and then exported for ANOVA analyses. These included time period and hedonic content as
within-participant factors and gender as a between-participant factor. Sphericity violations and all pairwise comparisons were controlled using the Greenhouse-Geisser and
Bonferroni corrections, respectively.
To examine correlations of NAc, mPFC, and amygdala activity with pleasure and arousal ratings, the imagined texts
were ranked from low (1) to high (42) according to their
rated pleasantness or arousal, for each participant. Mean
group pleasure ratings were used to resolve ties when texts
were rated as equally pleasant, and mean group arousal ratings used when texts were rated as equally arousing. Mean
BOLD signal change in the postpresentation time window
in NAc, mPFC, and amygdala at each rank was correlated
with ranked pleasure or arousal ratings to test predictions
regarding regional sensitivities to rated pleasure or emotional arousal. Correlations were similarly computed for
each participant and categorized as either exceeding significance (r > 0.26, df ¼ 42, one-tailed P < 0.05) or not.
Functional connectivity analyses [Friston et al., 1997]
assessed temporal correlations of NAc, mPFC, and amygdala BOLD activity when imagining emotional and neutral
scenes. For each participant, BOLD time series extracted
from each ROI were mean detrended and segmented to
include activity in the post-presentation time window,
where effects of hedonic content were maximal. To represent the time-varying interaction of BOLD activity and
each imagined scenes’ hedonic content, these time series
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Emotional Imagery Activates Reward Circuits
TABLE I. Mean pleasure and emotional arousal ratings
for the imagined texts
Hedonic content
Pleasant
Neutral
Unpleasant
Pleasure
Arousal
8.25 (0.55)
6.75 (1.03)
2.78 (0.79)
7.24 (1.20)
3.23 (1.37)
6.67 (1.07)
Values in parentheses indicate standard deviations.
were weighted by an equal length vector coding a contrast
of pleasant versus unpleasant imagery. Iteratively specifying NAc, mPFC, or amygdala as the target ROI, the actual
and weighted BOLD time series of the remaining two seed
ROIs were entered as regressors in a MLM model predicting target ROI activity. This yielded two sets of correlation
coefficients that described overall and valence-dependent
functional connectivity of the target and seed regions.
Signed correlation coefficients for each participant were
transformed to z statistics using Fisher’s z-transformation
and analyzed at the group level using a one-sample t-test
to determine if average correlation values differed from
zero. Coactivation was further assessed, by averaging over
participants’ baseline-deviated BOLD activity in NAc,
mPFC, and amygdala for each text at each of the four time
points following text presentations. Where indicated, correlation coefficients were then separately evaluated by
hedonic content and compared to determine if they significantly differed from one another.
RESULTS
Imagery Ratings
Table I lists mean pleasure and emotional arousal ratings when imagining each scene. Pleasure ratings indicated that compared to neutral scenes, pleasant scenes
were rated as more pleasant, while unpleasant scenes
were rated as more unpleasant [F(2,58) ¼ 372, P <
0.0001, g2 ¼ 0.93]. Both pleasant and unpleasant scenes
were rated as more emotionally arousing than neutral
scenes [F(2,58) ¼ 106, P < 0.0001, g2 ¼ 0.79] and did not
differ in rated arousal.
Volume Analyses
A set of volume analyses, corrected for multiple comparisons at P < 0.05, identified regions activated during either
pleasant or unpleasant imagery compared to neutral imagery and during pleasant compared to unpleasant imagery
(Table II; see Supporting Information Table S1 for a complete list of activated regions). As illustrated in Figure 1,
greater activation was evident in NAc (Fig. 1A) and mPFC
(Fig. 1B) during imagery of pleasant, compared to neutral
texts. A contrast of pleasant and unpleasant imagery reinforced activation patterns found when contrasting pleasant
and neutral imagery—specifically increased activation of
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ventral mPFC2 and NAc (Table II). There were no significant
differences in activation of NAc or ventral mPFC when
comparing unpleasant to neutral imagery.
Examination of the event-related time course of groupaveraged BOLD signal change for each region (Fig. 1D,E)
indicated an increase in activity for pleasant scenes beginning during text presentation and that was selectively sustained during imagery, whereas during presentation of
neutral and unpleasant texts, a signal decrease was
obtained that reached a minimum during imagery.
Selective activation of NAc and mPFC for pleasant imagery contrasted with the heightened amygdala activation
occurring during imagery of either pleasant or unpleasant
scenes, compared to neutral scenes (Fig. 1C represents the
conjunction of these contrasts). Increased BOLD activity
that was initiated during text presentation was subsequently maintained during imagery of emotional texts, but
decreased when imagining neutral scenes (Fig. 1F). There
were no significant differences in activation of the amygdala for the contrasts of pleasant and unpleasant imagery.
ROI Analyses
NAc and mPFC
Modulation of NAc activity by hedonic content was significant in the individually sampled analysis of mean
BOLD signal change [F(2,54) ¼ 17.24, P < 0.0001, g2 ¼
0.13]. These effects were consistent across men and
women. Pairwise analyses indicated larger signal increases
in NAc both during text presentation [t(28) ¼ 3.85, P <
0.005] and subsequent imagery [t(28) ¼ 7.05, P < 0.0001]
for pleasant, compared to unpleasant, scenes. When compared to neutral scenes, pleasant scenes elicited heightened NAc activity during text presentation [t(28) ¼ 4.93, P
< 0.0001], whereas activity prompted by unpleasant and
neutral scenes did not differ at either time [Valence "
Time, F(2,54) ¼ 9.93, P < 0.0001, g2 ¼ 0.02].
Mean signal change in mPFC also was significantly
modulated by hedonic content [F(2,54) ¼ 26.99, P < 0.0001,
g2 ¼ 0.35]. Pleasant scenes evoked greater signal increases
in mPFC compared to unpleasant scenes, both during text
presentation [t(28) ¼ 5.65, P < 0.0001] and subsequent imagery [t(28) ¼ 8.62, P < 0.0001]. Following text presentation,
subsequent imagery of pleasant scenes evoked larger signal
increases than neutral scenes [t(28) ¼ 4.74, P < 0.0001],
whereas unpleasant, compared to neutral, scenes prompted
significantly larger decreases in mPFC both during text presentation [t(28) ¼ 3.17, P < 0.05] and during subsequent
2
Activation of mPFC for the contrast of pleasant imagery versus
unpleasant imagery was decidedly more ventral with respect to the
frontal pole—overlapping BA 10/11—than that observed when contrasting pleasant and neutral imagery. It was also distinct from a
smaller, dorsal cluster of increased activation in mPFC (BA 8) present when comparing both pleasant and unpleasant to neutral imagery (see Supporting Information Table S2).
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Costa et al.
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TABLE II. Mesocorticolimbic regions activated for contrasts of emotional imagery
Region
Unpleasant > Neutral
L Amygdala
R Amygdala
Pleasant > Neutral
L Amygdala
R Amygdala
L Medial prefrontal cortex (BA 10)
L Nucleus accumbens
R Nucleus accumbens
Pleasant > Unpleasant
L Medial prefrontal cortex (BA 10)
L Nucleus accumbens
lla
x
y
z
tb
156
63
#22
30
#6
#4
#10
#12
4.51
4.27
562
63
1,969
189
78
#21
18
#6
#10
10
#2
#6
58
8
6
#10
#10
16
#6
#8
5.86
4.30
4.29
3.72
4.16
2,047
172
0
#7
55
5
#2
#9
6.26
5.80
L, left; R, right.
Cluster size computed using 2.5-mm3 voxel.
b
Significant at P < 0.05 corrected.
a
imagery [t(28) ¼ 3.18, P < 0.05; Valence " Time, F(2,54) ¼
11.09, P < 0.0001, g2 ¼ 0.04].
Amygdala
Mean signal change in the amygdala was significantly
modulated by emotional arousal [F(2,54) ¼ 30.56, P <
0.0001, g2 ¼ 0.25]. Imagining either pleasant [t(28) ¼ 6.69,
P < 0.0001] or unpleasant scenes [t(28) ¼ 5.9, P < 0.0001]
resulted in increased signal change, compared to neutral
scenes. Heightened amygdala activation for emotional
scenes was confined to imagery following text presentation
[Valence " Time, F(2,54) ¼ 51.47, P < 0.0001, g2 ¼ 0.22].
There were no differences in amygdala activity between
pleasant and unpleasant scenes and no gender effects.
Ratings of Emotional Experience and BOLD
For each participant, scenes were ranked based on pleasure ratings from least to most pleasurable. The proportion
of a priori pleasant, neutral, and unpleasant texts comprising each rank is depicted by the pie charts in Figure 2.
NAc and mPFC
A positive curvilinear trend strongly related mean BOLD
signal change during imagery to ranked pleasure ratings for
NAc [r ¼ 0.75, F(2,39) ¼ 25.3, P < 0.0001; Fig. 2A] and
mPFC [r ¼ 0.82, F(2,39) ¼ 39.23, P < 0.0001; Fig. 2B].3 Posi3
Correlations of similar size between NAc and mPFC activity and pleasure ratings were obtained when using mean pleasure ratings at each
rank [NAc: r = 0.71, F(2,39) = 20.66, P > 0.0001; mPFc: r = 0.81, F(2,39) =
39.95, P > 0.0001], or when using mean pleasure ratings for each imagined scene [NAc: r = 0.72, F(2,39) = 21.15, P > 0.0001; mPFc: r = 0.85,
F(2,39) = 21.15, P > 0.0001]. Likewise correlation between amygdala activation and arousal ratings were of similar magnitude when using either
mean arousal ratings at each rank [r = 0.46, F(1,40) = 12.83, P > 0.001] or
mean arousal ratings for each imagined scene [r = 0.46, F(1,40) = 12.21, P
> 0.005].
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tive curvilinear trends fit NAc activity in 79% of participants
and were significant in 48% of the sample, and fit mPFC activity in 83% of participants, reaching significance in 55% of
the sample. Pleasure rankings were also linearly related to
mean signal change in each region [NAc: r ¼ 0.72, F(1,40) ¼
43.9, P < 0.001; mPFC: r ¼ 0.76, F(1,40) ¼ 58, P < 0.0001],
although a quadratic fit accounted for slightly, but significantly, more variance [NAc: F(1,39) ¼ 3.36, P < 0.05; mPFC:
F(1,39) ¼ 9.03, P < 0.005]. When scenes were ranked by
rated emotional arousal, there was no significant correlation
with signal change in NAc (r ¼ 0.16, ns) or mPFC (r ¼ 0.26,
ns).
Amygdala
BOLD signal change in the amygdala during imagery
was unrelated to rankings based on pleasure ratings (r ¼
0.07, ns), but increased linearly when scenes were ranked
according to participants’ arousal ratings from least to
most arousing [r ¼ 0.44, F(1,40) ¼ 8.9, P < 0.005]. A positive linear trend between arousal rankings and increased
amygdala activity was evident in 68% of participants and
significant in 25% of the sample.
Functional Connectivity
NAc and mPFC
The mean temporal correlation between activation in
NAc and mPFC when imagining scenes following text presentation was significant [r ¼ 0.27, t(28) ¼ 8.10, P <
0.0001, g2 ¼ 0.7], indicating their overall functional connectivity. Figure 3A presents the covariation of signal
change in NAc and mPFC, averaged across participants
for each time point in the imagery interval following text
presentation for each scene. Signal change in each region
was highly correlated overall (r ¼ 0.71, P < 0.0001). Also
shown is the distribution of signed correlation values
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Emotional Imagery Activates Reward Circuits
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Figure 1.
Increased activation of NAc (A) and mPFC (B) was obtained with text presentation and continuing through subsequent imduring pleasant, compared to neutral, imagery, whereas amygdala agery in NAc (D), mPFC (E), and the amygdala (F). Talairach
activity (C) was increased during both pleasant and unpleasant, coordinates are based on coronal slice selection. Error bars repcompared to neutral, imagery. Event-related signal change is resent 95% confidence intervals [Loftus and Masson, 1994].
plotted for pleasant, neutral, and unpleasant scenes beginning
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Costa et al.
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when this same relationship was assessed in each participant (Fig. 3B). A positive linear correlation between NAc
and mPFC activity during imagery was present in 86% of
participants and was significant in 76% of the sample.
When the covariation of mean BOLD signal change in
NAc and mPFC was separately assessed by hedonic content, correlation coefficients when imagining pleasant (r ¼
0.57; Z ¼ 2.92, P < 0.005) or unpleasant (r ¼ 0.36; Z ¼
2.04, P < 0.05) scenes were larger than when imagining
neutral scenes (r ¼ #0.12), but did not differ from one
another (Z ¼ 1.54, ns).
Amygdala
Functional connectivity of the amygdala with NAc and
mPFC was heightened during pleasant, compared to neutral or unpleasant imagery. A significant temporal correlation across individuals was found in the BOLD time series
between amygdala and NAc [t(28) ¼ 2.65, P ¼ 0.01, g2 ¼
0.19] and between the amygdala and mPFC [t(28) ¼ 2.24,
P < 0.05, g2 ¼ 0.15] when the latter time series was linearly weighted by the a priori valence of the imagined
scene. Figure 4 illustrates the covariation of the BOLD activity in amygdala with activity in NAc (A) and mPFC (B)
during imagery of each scene—for the four time points following text presentation—separately assessed by hedonic
content. Correlation of signal change in amygdala and
NAc was larger during pleasant imagery (r ¼ 0.51) compared to neutral (r ¼ #0.04; Z ¼ 2.24, P < 0.05) or
unpleasant (r ¼ 0.03; Z ¼ 2.86, P < 0.005) imagery. Correlation of signal change in amygdala and mPFC was also
larger during pleasant imagery (r ¼ 0.59) compared to
neutral (r ¼ #0.01; Z ¼ 2.62, P < 0.01) or unpleasant (r ¼
0.11; Z ¼ 3.14, P < 0.005) imagery.
DISCUSSION
Narrative Emotional Imagery Engages
Motivational Centers
Figure 2.
Pleasure ratings correlate with mesolimbic BOLD activity during
imagery. Scenes were rank ordered by each participant’s pleasure ratings and plotted against the mean signal change in NAc
and mPFC at each rank. Pie charts depict the proportion of the
a priori selected pleasant, neutral, and unpleasant texts at each
rank [based on ANET standardized ratings; Bradley and Lang,
2007].
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Imagining pleasant events strongly activated NAc and
mPFC, compared to imagining unpleasant or neutral
scenes. Selective activation of these structures developed
over time as participants continued to imagine the pleasant events they had just read. Activation of NAc and
mPFC also showed a positive, graded response that correlated highly with pleasure ratings for the imagined texts.
These results suggest a central role for NAc and mPFC in
processing pleasurable events that is consistent across
stimulus media, showing the same pattern of activation
during pleasant imagery as previously observed in
research assessing human reactions to tangible appetitive
cues [Breiter et al., 1997, 2001; Knutson et al., 2005] or
when viewing arousing pleasant pictures [Sabatinelli et al.,
2007]. Peak activation coordinates reported here for pleasant imagery (NAc: $10, 7, #7; mPFC: #6, 58, 16) are very
close to those we reported previously [Sabatinelli et al.,
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Emotional Imagery Activates Reward Circuits
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Figure 3.
Functional connectivity of NAc and mPFC during imagery. The distribution of the correlation between NAc and mPFC activity
mean BOLD signal change during imagery in each region, aver- for each participant during imagery (r > 0.16. is significant; 0 <
aged over participants for each of the four time points following r < 0.16 is not significant, and r < 0 are in the unpredicted
text presentation for pleasant (blue), neutral (green), or unpleas- direction). [Color figure can be viewed in the online issue,
ant (red) scenes (A). The adjacent panel (B) shows the ordered which is available at wileyonlinelibrary.com.]
2007] during pleasant picture perception (NAc: $10, 9, #2;
mPFC: #4, 39, 4), using the same MR hardware. The present results also clarify and expand on earlier findings
[Rauch et al., 1999] of increased ventral pallidum activation in men when imagining pleasant sexual encounters
and athletic success, as well as findings [Kilts et al., 2001,
2004] of increased NAc activation—although not mPFC
activation—during imagery of drug use in substance
abusers.
The finding of a pleasure-specific increase in NAc during narrative imagery contrasts with some studies suggesting that increased NAc activity is driven by stimulus
salience, rather than selectively by positive hedonic cues
(see review by Leknes and Tracy [2008]). The database
relating NAc activity to aversive stimulation is quite complex, and the modulation found appears to vary with species (human or animal), specific brain measure (e.g., single
unit activity, dopamine release, PET, fMRI, etc.), type of
aversive stimulation (pain, odor, taste, picture, image,
etc.), and processing paradigm (perception, anticipation,
classical conditioning, operant conditioning, etc.). When
considering fMRI studies with human participants, however, the data are consistent in indicating that NAc activity
does not increase when people view aversive pictures
[Meseguer et al., 2007; Phan et al., 2004; Sabatinelli et al.,
2007], are exposed to painful thermal stimulation [Becerra
r
and Borsook, 2008; Becerra et al., 2001], or process cues
signaling loss [Cooper and Knutson, 2007] or unpleasant
odors [Gottfried et al., 2001]. The present study is consistent with these, indicating reward system activation during
pleasant emotional imagery in human participants.
In fact, in the current study, BOLD activity during
unpleasant imagery prompted marked signal decreases
from baseline in both NAc and mPFC. Similar signal
decreases to unpleasant content were found in these same
structures in our previous study of picture perception
[Sabatinelli et al., 2007]. BOLD signal decreases from baseline have also been found in NAc with the onset of painful
stimulation [Aharon et al., 2006; Becerra and Borsook,
2008; Becerra et al., 2001]. Furthermore, using PET,
decreased rCBF in mPFC was observed when contrasting
traumatic and neutral imagery in patients with post-traumatic stress disorder [Britton et al., 2005; Shin et al., 2004].
Research on the neurophysiology of the BOLD signal
and rCBF [Goense and Logothetis, 2008; Logothetis et al.,
2001; Mathiesen et al., 1998] indicates that hemodynamic
measures generally reflect net excitation or inhibition of
cortical microcircuits [Logothetis, 2008]. Deactivation of
mesolimbic reward structures during unpleasant perception and imagery might represent inhibition of appetitive
circuitry. Significantly greater deactivation of mPFC during unpleasant compared to neutral imagery, along with
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Costa et al.
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Figure 4.
Pleasure-specific connectivity of the amygdala with NAc and mPFC. Scatter plots depict the correlation of mean BOLD activity during imagery (averaged over participants for each of the four
time points following text presentation) in the amygdala with NAc (A) and mPFC (B), separately
evaluated for pleasant, neutral, and unpleasant scenes.
reports that mPFC deactivation during trauma imagery is
correlated negatively with symptom severity in PTSD
patients [Shin et al., 2004], further suggests that signal
decreases in mPFC may code for aversion. However,
whether the extent of NAc deactivation generally indexes
aversive processing remains unclear as imagining neutral
scenes and viewing neutral pictures [Sabatinelli et al.,
2007] also prompt similar decreases.
As anticipated, heightened amygdala activation was
found during both pleasant and unpleasant imagery and
was positively correlated with emotional arousal ratings
for the imagined scenes. This is consistent with similar
patterns of amygdala activation found when people view
pleasant and unpleasant emotionally arousing external
stimuli [Cooper and Knutson, 2007; Sabatinelli et al., 2005,
2007; Zald, 2003], and complements extensive lesion and
electrophysiological work in animals demonstrating amyg-
r
dala involvement in both aversive [Davis and Whalen,
2001] and appetitive learning [Ambroggi et al., 2008;
Baxter and Murray, 2002].
Functional Connectivity of an Appetitive Circuit
A strong, positive temporal correlation of BOLD activity
in NAc and mPFC was evident during imagery regardless
of content, whereas activity in the amygdala was specifically correlated with activity in NAc and mPFC during
appetitive processing. Complete functional connectivity of
NAc, mPFC, and the amygdala when imagining pleasant
scenes is consistent with coactivation of these structures
when viewing appetitive pictures [Sabatinelli et al., 2007]
or processing monetary rewards [Cooper and Knutson,
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Emotional Imagery Activates Reward Circuits
2007]; as well as with evidence that intact afferents from
both the mPFC [Ishikawa et al., 2008a] and amygdala
[Ambroggi et al., 2008] are necessary for NAc neurons to
display firing patterns predictive of subsequent appetitive
behavior.
Functional coupling of NAc and mPFC signal change
was expected given their common sensitivity to pleasure
and known neuroanatomical connectivity [Ongur and
Price, 2000]. Electrical stimulation of mPFC neurons is
reported to evoke firing in NAc neurons [McGinty and
Grace, 2009], and pharmacological inactivation of mPFC
reduces reward-seeking behaviors and related cue-evoked
firing of NAc neurons [Ishikawa et al., 2008a]. Another
possibility is that linked mesolimbic function during pleasant imagery is attributable to coordinated dopamine
release, as systemic injection of dopamine releasing agents
increases BOLD activity in both NAc and mPFC [Breiter
et al., 1997; Knutson and Gibbs, 2007].
Functional connectivity of the amygdala with NAc and
mPFC specific to pleasant imagery fits with the demonstrated sensitivity of these regions to ratings of emotional
arousal or pleasure, respectively. Considering that signal
change in both NAc and mPFC was unrelated to rated
emotional arousal, mesolimbic connectivity with the amygdala during pleasant imagery suggests a pathway for specifically enhancing appetitive motivation. A lack of
negative functional connectivity between the amygdala
and reward structures during unpleasant imagery further
emphasizes the specific involvement of this circuit in
appetitive processing.
This view is supported by animal studies in which pharmacological inactivation of the basolateral amygdala following appetitive conditioning dampened cue-evoked
excitation of NAc neurons [Ambroggi et al., 2008] and
reduced reward-seeking behaviors in a dose-dependent
manner [Ishikawa et al., 2008b]. Chemical inactivation of
the amygdala’s central nucleus following food deprivation
also reduced dopamine release in NAc and mPFC during
food consumption [Ahn and Phillips, 2002], while opioid
stimulation of the central nucleus increased appetitive and
consummatory behaviors toward reward cues [Mahler and
Berridge, 2009]. Interestingly, electrical stimulation of the
amygdala is additionally found to increase neuronal firing
in mPFC neurons projecting to NAc [McGinty and Grace,
2008] and coincident stimulation of amygdala and mPFC
inputs to NAc increases neuronal firing above mPFC stimulation alone [McGinty and Grace, 2009]. Taken together,
the functional connectivity patterns identified here imply
that the NAc, mPFC, and the amygdala form an integrative circuit that is engaged when humans directly process
pleasurable emotional content.
Limitations and New Directions
Because imagery is an inherently mental event, questions can arise regarding compliance with the task during
r
r
experimentation. In this study, the palpable changes in
BOLD signal in NAc, mPFC, and amygdala at the onset of
the instructed imagery period (see Fig. 1) and their strong
covariation with emotional ratings of experienced pleasure
and arousal during imagery—both within and across participants (see Fig. 2A,B)—suggest compliance with the imagery task. Moreover, prior psychophysiological studies of
both anxiety patients and healthy participants, using the
same instructions and many of the same texts as in this
study, have repeatedly confirmed that text-driven imagery
prompts heightened autonomic and somatic reaction consistent with emotional engagement [e.g., Cuthbert et al.,
2003; Lang and McTeague, 2009; McTeague et al., 2009;
Vrana et al., 1986]. Finally, participants rated the difficulty
of imaging each scene, and most reported that it was an
easy task.
Future neuroimaging work should, nevertheless, assess
how connectivity of these structures during imagery
relates to the appetitive motivational gradients defined by
autonomic and somatic reflex indices [Bradley et al., 2001].
Another aim is to determine how depressive psychopathology alters appetitive circuitry. There is considerable
evidence that altered connectivity of rostral anterior cingulate (rACC) with the amygdala and prefrontal cortices has
a role in mediating symptoms in depressed patients [e.g.,
Yoshimura et al., in press] and that this circuit can be
modified by cognitive therapy and pharmacological interventions [DeRubeis et al., 2008]. Increased activation of
rACC during pleasant imagery was not found here with
healthy participants, suggesting that the interaction
between the cingulate and reward circuit may be specific
to depression. Comparative studies with depressed
patients during pleasant narrative imagery could clarify
this issue and perhaps confirm a mechanism through
which mood disorders compromise appetitive neural
processing.
SUMMARY
Imagining pleasant, highly appetitive events selectively
activated NAc and mPFC, and their activation correlated
positively with rated pleasure of the imagined scenes. In
contrast, imagery of either pleasant or unpleasant emotional scenes prompted increased amygdala activation,
and its activation was positively correlated with rated
emotional arousal. Functional connectivity analyses determined, furthermore, that coincident activation of all three
regions—amygdala, NAc, and mPFC—occurred only
when participants imaged pleasant scenes. Together, these
findings provide strong evidence that pleasant and
unpleasant imagery engage different motivational circuits—appetitive and aversive—paralleling previous findings from animal and human studies of emotional
learning and perception. Moreover, these results suggest
that the clinical use of narrative imagery might be usefully
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extended to mood disorders (e.g., depression and dysthymia) in which appetitive processing may be compromised.
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