r Human Brain Mapping 31:1446–1457 (2010) r

Emotional Imagery: Assessing Pleasure andArousal in the Brain’s Reward Circuitry

Vincent D. Costa, Peter J. Lang*, Dean Sabatinelli, Francesco Versace, andMargaret 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 nucleusaccumbens (NAc) and medial prefrontal cortex (mPFC), whereas amygdala activity is modulated bythe emotional intensity of appetitive and aversive cues. This study sought to determine patterns offunctional activation and connectivity among these regions during narrative emotional imagery. Usingevent-related fMRI, we investigate activation of these structures when participants vividly imaginepleasant, neutral, and unpleasant scenes. Results indicate that pleasant imagery selectively activatesNAc and mPFC, whereas amygdala activation was enhanced during both pleasant and unpleasant im-agery. 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 NAcand mPFC was evident throughout imagery, regardless of hedonic content, while correlated activationof the amygdala with NAc and mPFC was specific to imagining pleasant scenes. These findings pro-vide strong evidence that pleasurable text-driven imagery engages a core appetitive circuit, includingNAc, mPFC, and the amygdala. Hum Brain Mapp 31:1446–1457, 2010. VC 2010 Wiley-Liss, Inc.

Keywords: liking; mental imagery; mesocorticolimbic; script-driven imagery; psychophysiologicalinteraction; ventral striatum; ventral medial prefrontal cortex

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INTRODUCTION

Reading an exciting novel or listening to an engagingstory can prompt vivid imagery of the described eventsand reported feelings of intense emotion. Research hasrepeatedly confirmed this phenomenon and demonstratedthat text-driven imagery prompts heightened autonomicand 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]. Perhapsbecause the evocation of vivid fear imagery has been animportant method in the psychological treatment of pho-bias and anxiety [Lang, 1977; Wolpe, 1958], clinical studiesthat utilize narrative imagery for symptom provocation[Cuthbert et al., 2003; Lang and McTeague, 2009;McTeague et al., 2009; Orr et al., 1993] have mainlyassessed reactivity during aversive imagery. This emphasisalso characterizes related neuroimaging research [Brittonet al., 2005; Dougherty et al., 1999; Shin et al., 2000; Sinhaet al., 2004] that consistently reports increased activation

Additional Supporting Information may be found in the onlineversion of this article.

Contract grant sponsor: National Institute of Mental Health;Contract grant number: P50 MH 72850 [to the Center for theStudy of Emotion and Attention (CSEA), University of Florida,Gainesville, FL]; Contract grant sponsor: National Institute ofMental Health; Contract grant number: F31 MH080551 (NationalResearch 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 atthe University of Texas, Houston, Texas, USA.

*Correspondence to: Peter J. Lang, NIMH Center for the Study ofEmotion and Attention, University of Florida, P.O. Box 112766,Gainesville, Florida 32611, USA. E-mail: langp@phhp.ufl.edu

Received for publication 17 June 2009; Revised 4 September 2009;Accepted 19 October 2009

DOI: 10.1002/hbm.20948Published online 2 February 2010 in Wiley Online Library(wileyonlinelibrary.com).

VC 2010 Wiley-Liss, Inc.

in the brain’s aversive system [Lang and Davis, 2006],including the amygdala and related paralimbic regions.

While research on emotional perception and learningclearly indicates that the amygdala encodes the emotionalintensity of both appetitive and aversive stimuli [Baxterand Murray, 2002; Davis and Whalen, 2001; McGaugh,2004; Zald, 2003], there is debate as to whether NAc acti-vation is driven by the pleasantness of a stimulus or itssalience [Berridge et al., 2009]. Evidence from studies ofpleasant visual perception [Aharon et al., 2001; Sabatinelliet al., 2007] and reward processing [Breiter et al., 2001;Cooper and Knutson, 2007; Knutson et al., 2005] indicatesthat the nucleus accumbens (NAc) and medial prefrontalcortex (mPFC) are selectively activated for pleasurablestimuli that are readily discerned. On the other hand,based on studies using a wide variety of populations,paradigms, and procedures, there is also evidence thatNAc activity increases in response to both pain and pleas-ure [Leknes and Tracey, 2008]. This raises the question ofwhether mesolimbic activation during narrative emotionalimagery will reflect the hedonic valence or the salience(emotional arousal) of the imagined scenes.

Consistent with the view that imagery and perception ofemotional stimuli engage similar motivational circuitry[Lang, 1979, 1994], narrative imagery of drug cravingheightened regional cerebral blood flow (rCBF) in NAcand amygdala in cocaine-dependent men and women[Kilts et al., 2001, 2004], and imagery of pleasant sexualencounters/athletic success increased rCBF in ventral pal-lidum (an efferent target of NAc) in men [Rauch et al.,1999]. Yet because prior studies have not examined NAcactivation during both pleasant and unpleasant imagery, itremains plausible that unpleasant imagery could alsoprompt increased activation of NAc, consistent with a sali-ence 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], ifimagining prototypical pleasant scenes uniquely activatesmesolimbic reward circuitry in healthy males and females,whether amygdala activation is found when imaginingboth pleasant and unpleasant scenes, and how functionalconnectivity among these three regions varies withhedonic content.

It is hypothesized that relative to neutral and unpleasantscenes, imagining pleasurable scenes will selectively acti-vate NAc and mPFC, whereas compared to neutral im-agery, processing arousing emotional content—pleasant orunpleasant—will heighten amygdala activation. We alsoexamined the relationship between signal change in theseregions and participants’ ratings of pleasure and emotionalarousal for the imagined scenes. Based on prior findingsduring 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 posi-tively with signal change in NAc and mPFC, while emo-tional arousal ratings should correlate positively withamygdala activity.

NAc and mPFC heavily innervate one another [Ongurand Price, 2000] and each region receives amygdala affer-ents [Friedman et al., 2002]. If these anatomical connec-tions support a circuit underlying appetitive processing,functional connectivity among these structures is expectedto vary with hedonic content. Predicated on the hypothe-sized sensitivity of NAc and mPFC to pleasure, temporalcovariation of mesolimbic activation is anticipated duringpleasant imagery and possibly overall. Because of theamygdala’s sensitivity to emotional arousal, its functionalconnectivity with structures specifically sensitive to pleas-ure will reflect appetitive arousal. This suggests that func-tional connectivity of the amygdala with NAc or mPFC orboth will occur only when imagining pleasant contents.

MATERIALS AND METHODS

Participants

Thirty-two students (16 women, mean age ! 19.1, SD !1.5) from introductory psychology courses participated forcourse credit or for $20. Participants were right-handed,had normal visual acuity, and reported no history of claus-trophobia, psychopathology, or neurological insult in a tel-ephone interview. Informed consent was obtained asstipulated by the institutional review board. Three partici-pants were excluded due to excessive head motion or tech-nical errors, resulting in a final sample of 29 participants.

Materials and Design

Forty-two narratives were selected from the AffectiveNorms 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 andwere categorized as pleasant (e.g., winning the lottery; n !12), neutral (e.g., reading the newspaper; n ! 6), orunpleasant (e.g., a car accident; n ! 24).1 Prior to scanning,participants briefly read and imagined each scene andrated their experience of pleasure and arousal usinggraphic Self-Assessment Manikin scales [Bradley andLang, 1994; Lang, 1980]. Texts were written to be read in12 s and their presentation counterbalanced so that nomore than two trials of the same hedonic content occurredin succession. Multivariate comparison of sentence proper-ties indicated that emotional and neutral sentences did notdiffer in word, syllable, or character counts [F(6,74) ! 1.95,ns].

The imagery procedure consisted of 42 trials. Each trialbegan with visual presentation of a text for 12 s, backward

1The additional 12 unpleasant scenes described specific fear-relevantscenarios (dental and snake fear) and were included in the design toallow future comparisons with clinical populations. Analyses thatexcluded these categories yielded the same pattern of results.

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projected onto a monitor (640 " 480 pixel resolution) situ-ated behind the participant’s head, and viewed using ahead-coil mounted mirror (IFIS-SA, Invivo, Orlando, FL).The visual offset of the text signaled participants to con-tinue imagining the scene they had just read. Twelve sec-onds later, a brief (400 ms) change in the color of thescreen, perceptible as a flash, signaled that imagery shouldend and was followed by a fixed 12-s intertrial interval.After the experiment, participants rated the overall diffi-culty of imagining the presented scenes (1 ! very difficultto 9 ! not difficult at all). On average participantsreported little difficulty in completing the imagery task(mean difficulty rating ! 6.78, SD ! 1.13).

Procedure

After entering the scanner, participants were instructedto silently read each text as it appeared and to continue toimagine their active involvement in the described event,until a brief change in the color of the screen alerted theparticipant to stop imagining. Except during text presenta-tions, participants were told to maintain their gaze on afixation cross presented at the center of the monitor.

Data Acquisition and Analysis

A T1-weighted anatomical volume was acquired using aSiemens 3T Allegra MR scanner. A total of 506 functionalvolumes (50 coronal slices, 2.5 mm thick, 0.5 mm gap)were collected using a T2*-weighted echo planar imagingsequence (3 s TR, 35 ms TE, 160 mm FOV, 64 " 64 acquisi-tion matrix).

Functional data were slice-time adjusted, motion-cor-rected, spatially smoothed (5-mm FWHM Gaussian ker-nel), and converted to percent blood oxygen level-dependent (BOLD) signal change using the Analysis ofFunctional Neuroimages software [Cox, 1996]. A multiplelinear regression (MLM) model deconvolved hemody-namic responses for the three hedonic contents as a linearcombination of eight uniform B-spline basis functions.This generated a time series of beta coefficients at eachvoxel equaling the length of a single trial (24 s), beginningwith text presentation and extending through the imageryperiod. Additional regressors modeled motion residualsand baseline drift. Resultant time series were spatially nor-malized [Talariach and Tournoux, 1988] and resampled toa 2.5 mm isotropic voxel size.

Using participants’ average percent BOLD signal changeduring imagery following text presentation, three mixedeffects ANOVAs identified voxels with greater activationduring pleasant compared to neutral imagery, unpleasantcompared to neutral imagery, and pleasant compared tounpleasant imagery. Nonparametric permutation tests werecomputed following recommended guidelines [Nichols andHolmes, 2002] to determine critical t-statistic values for eachcontrast that corrected for multiple comparisons across the

volume. In each permutation test, labels coding hedonic con-tent were randomly reassigned within participants andchecked for independence from previous permutationorders. A t-statistic was then generated at each voxel and aGaussian function fit to their distribution over the entirebrain. The value of the t-statistic at the 99.9 percentile of thefitted Gaussian distribution was selected to form a permuta-tion distribution based on 10,000 randomizations. The result-ing absolute thresholds that corrected for multiplecomparisons at P < 0.05 were t ! 3.71 (P < 0.0008 uncor-rected) when contrasting pleasant to neutral imagery, t !4.07 (P < 0.0003 uncorrected) when contrasting unpleasantto neutral imagery, and t ! 4.2 (P < 0.0002 uncorrected)when contrasting pleasant to unpleasant imagery.

Functional regions of interest (ROI) for NAc and mPFCwere based on cluster locations identified in the groupcontrast of pleasant compared to neutral imagery and forthe amygdala based on the conjoined group contrasts ofpleasant and unpleasant compared to neutral imagery. Av-erage BOLD activity was extracted for each ROI from a109 ll volume within the area of interest and surroundinga significant peak activation (P < 0.05 uncorrected) in eachparticipants’ spatially normalized contrast maps. Assum-ing that imagery begins as a text is read, we analyzedBOLD activity in an early window, during the 12-s textpresentation, and at a later 12-s window when text was nolonger on the screen. Mean BOLD signal change for eachwindow was deviated from a baseline immediately priorto text presentation and then exported for ANOVA analy-ses. These included time period and hedonic content aswithin-participant factors and gender as a between-partici-pant factor. Sphericity violations and all pairwise compari-sons were controlled using the Greenhouse-Geisser andBonferroni corrections, respectively.

To examine correlations of NAc, mPFC, and amygdala ac-tivity with pleasure and arousal ratings, the imagined textswere ranked from low (1) to high (42) according to theirrated pleasantness or arousal, for each participant. Meangroup pleasure ratings were used to resolve ties when textswere rated as equally pleasant, and mean group arousal rat-ings used when texts were rated as equally arousing. MeanBOLD signal change in the postpresentation time windowin NAc, mPFC, and amygdala at each rank was correlatedwith ranked pleasure or arousal ratings to test predictionsregarding regional sensitivities to rated pleasure or emo-tional arousal. Correlations were similarly computed foreach participant and categorized as either exceeding signifi-cance (r > 0.26, df ! 42, one-tailed P < 0.05) or not.

Functional connectivity analyses [Friston et al., 1997]assessed temporal correlations of NAc, mPFC, and amyg-dala BOLD activity when imagining emotional and neutralscenes. For each participant, BOLD time series extractedfrom each ROI were mean detrended and segmented toinclude activity in the post-presentation time window,where effects of hedonic content were maximal. To repre-sent the time-varying interaction of BOLD activity andeach imagined scenes’ hedonic content, these time series

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were weighted by an equal length vector coding a contrastof pleasant versus unpleasant imagery. Iteratively specify-ing NAc, mPFC, or amygdala as the target ROI, the actualand weighted BOLD time series of the remaining two seedROIs were entered as regressors in a MLM model predict-ing target ROI activity. This yielded two sets of correlationcoefficients that described overall and valence-dependentfunctional connectivity of the target and seed regions.Signed correlation coefficients for each participant weretransformed to z statistics using Fisher’s z-transformationand analyzed at the group level using a one-sample t-testto determine if average correlation values differed fromzero. Coactivation was further assessed, by averaging overparticipants’ baseline-deviated BOLD activity in NAc,mPFC, and amygdala for each text at each of the four timepoints following text presentations. Where indicated, cor-relation coefficients were then separately evaluated byhedonic content and compared to determine if they signifi-cantly differed from one another.

RESULTS

Imagery Ratings

Table I lists mean pleasure and emotional arousal rat-ings when imagining each scene. Pleasure ratings indi-cated that compared to neutral scenes, pleasant sceneswere rated as more pleasant, while unpleasant sceneswere rated as more unpleasant [F(2,58) ! 372, P <0.0001, g2 ! 0.93]. Both pleasant and unpleasant sceneswere rated as more emotionally arousing than neutralscenes [F(2,58) ! 106, P < 0.0001, g2 ! 0.79] and did notdiffer in rated arousal.

Volume Analyses

A set of volume analyses, corrected for multiple compari-sons at P < 0.05, identified regions activated during eitherpleasant or unpleasant imagery compared to neutral im-agery and during pleasant compared to unpleasant imagery(Table II; see Supporting Information Table S1 for a com-plete 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 neutraltexts. A contrast of pleasant and unpleasant imagery rein-forced activation patterns found when contrasting pleasantand neutral imagery—specifically increased activation of

ventral mPFC2 and NAc (Table II). There were no significantdifferences in activation of NAc or ventral mPFC whencomparing unpleasant to neutral imagery.

Examination of the event-related time course of group-averaged BOLD signal change for each region (Fig. 1D,E)indicated an increase in activity for pleasant scenes begin-ning during text presentation and that was selectively sus-tained during imagery, whereas during presentation ofneutral and unpleasant texts, a signal decrease wasobtained that reached a minimum during imagery.

Selective activation of NAc and mPFC for pleasant im-agery contrasted with the heightened amygdala activationoccurring during imagery of either pleasant or unpleasantscenes, compared to neutral scenes (Fig. 1C represents theconjunction of these contrasts). Increased BOLD activitythat was initiated during text presentation was subse-quently maintained during imagery of emotional texts, butdecreased when imagining neutral scenes (Fig. 1F). Therewere no significant differences in activation of the amyg-dala for the contrasts of pleasant and unpleasant imagery.

ROI Analyses

NAc and mPFC

Modulation of NAc activity by hedonic content was sig-nificant in the individually sampled analysis of meanBOLD signal change [F(2,54) ! 17.24, P < 0.0001, g2 !0.13]. These effects were consistent across men andwomen. Pairwise analyses indicated larger signal increasesin NAc both during text presentation [t(28) ! 3.85, P <0.005] and subsequent imagery [t(28) ! 7.05, P < 0.0001]for pleasant, compared to unpleasant, scenes. When com-pared to neutral scenes, pleasant scenes elicited height-ened NAc activity during text presentation [t(28) ! 4.93, P< 0.0001], whereas activity prompted by unpleasant andneutral scenes did not differ at either time [Valence "Time, F(2,54) ! 9.93, P < 0.0001, g2 ! 0.02].

Mean signal change in mPFC also was significantlymodulated by hedonic content [F(2,54) ! 26.99, P < 0.0001,g2 ! 0.35]. Pleasant scenes evoked greater signal increasesin mPFC compared to unpleasant scenes, both during textpresentation [t(28) ! 5.65, P < 0.0001] and subsequent im-agery [t(28) ! 8.62, P < 0.0001]. Following text presentation,subsequent imagery of pleasant scenes evoked larger signalincreases than neutral scenes [t(28) ! 4.74, P < 0.0001],whereas unpleasant, compared to neutral, scenes promptedsignificantly larger decreases in mPFC both during text pre-sentation [t(28) ! 3.17, P < 0.05] and during subsequent

TABLE I. Mean pleasure and emotional arousal ratingsfor the imagined texts

Hedonic content Pleasure Arousal

Pleasant 8.25 (0.55) 7.24 (1.20)Neutral 6.75 (1.03) 3.23 (1.37)Unpleasant 2.78 (0.79) 6.67 (1.07)

Values in parentheses indicate standard deviations.

2Activation of mPFC for the contrast of pleasant imagery versusunpleasant imagery was decidedly more ventral with respect to thefrontal pole—overlapping BA 10/11—than that observed when con-trasting pleasant and neutral imagery. It was also distinct from asmaller, dorsal cluster of increased activation in mPFC (BA 8) pres-ent when comparing both pleasant and unpleasant to neutral im-agery (see Supporting Information Table S2).

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imagery [t(28) ! 3.18, P < 0.05; Valence " Time, F(2,54) !11.09, P < 0.0001, g2 ! 0.04].

Amygdala

Mean signal change in the amygdala was significantlymodulated by emotional arousal [F(2,54) ! 30.56, P <0.0001, g2 ! 0.25]. Imagining either pleasant [t(28) ! 6.69,P < 0.0001] or unpleasant scenes [t(28) ! 5.9, P < 0.0001]resulted in increased signal change, compared to neutralscenes. Heightened amygdala activation for emotionalscenes was confined to imagery following text presentation[Valence " Time, F(2,54) ! 51.47, P < 0.0001, g2 ! 0.22].There were no differences in amygdala activity betweenpleasant and unpleasant scenes and no gender effects.

Ratings of Emotional Experience and BOLD

For each participant, scenes were ranked based on pleas-ure ratings from least to most pleasurable. The proportionof a priori pleasant, neutral, and unpleasant texts compris-ing each rank is depicted by the pie charts in Figure 2.

NAc and mPFC

A positive curvilinear trend strongly related mean BOLDsignal change during imagery to ranked pleasure ratings forNAc [r ! 0.75, F(2,39) ! 25.3, P < 0.0001; Fig. 2A] andmPFC [r ! 0.82, F(2,39) ! 39.23, P < 0.0001; Fig. 2B].3 Posi-

tive curvilinear trends fit NAc activity in 79% of participantsand were significant in 48% of the sample, and fit mPFC ac-tivity in 83% of participants, reaching significance in 55% ofthe sample. Pleasure rankings were also linearly related tomean signal change in each region [NAc: r ! 0.72, F(1,40) !43.9, P < 0.001; mPFC: r ! 0.76, F(1,40) ! 58, P < 0.0001],although a quadratic fit accounted for slightly, but signifi-cantly, more variance [NAc: F(1,39) ! 3.36, P < 0.05; mPFC:F(1,39) ! 9.03, P < 0.005]. When scenes were ranked byrated emotional arousal, there was no significant correlationwith signal change in NAc (r ! 0.16, ns) or mPFC (r ! 0.26,ns).

Amygdala

BOLD signal change in the amygdala during imagerywas unrelated to rankings based on pleasure ratings (r !0.07, ns), but increased linearly when scenes were rankedaccording to participants’ arousal ratings from least tomost arousing [r ! 0.44, F(1,40) ! 8.9, P < 0.005]. A posi-tive linear trend between arousal rankings and increasedamygdala activity was evident in 68% of participants andsignificant in 25% of the sample.

Functional Connectivity

NAc and mPFC

The mean temporal correlation between activation inNAc and mPFC when imagining scenes following text pre-sentation was significant [r ! 0.27, t(28) ! 8.10, P <0.0001, g2 ! 0.7], indicating their overall functional con-nectivity. Figure 3A presents the covariation of signalchange in NAc and mPFC, averaged across participantsfor each time point in the imagery interval following textpresentation for each scene. Signal change in each regionwas highly correlated overall (r ! 0.71, P < 0.0001). Alsoshown is the distribution of signed correlation values

TABLE II. Mesocorticolimbic regions activated for contrasts of emotional imagery

Region lla x y z tb

Unpleasant > NeutralL Amygdala 156 #22 #6 #10 4.51R Amygdala 63 30 #4 #12 4.27

Pleasant > NeutralL Amygdala 562 #21 #2 #10 5.86R Amygdala 63 18 #6 #10 4.30L Medial prefrontal cortex (BA 10) 1,969 #6 58 16 4.29L Nucleus accumbens 189 #10 8 #6 3.72R Nucleus accumbens 78 10 6 #8 4.16

Pleasant > UnpleasantL Medial prefrontal cortex (BA 10) 2,047 0 55 #2 6.26L Nucleus accumbens 172 #7 5 #9 5.80

L, left; R, right.aCluster size computed using 2.5-mm3 voxel.bSignificant at P < 0.05 corrected.

3Correlations of similar size betweenNAc andmPFC activity and pleas-ure ratings were obtained when using mean pleasure ratings at eachrank [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 imag-ined 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 acti-vation and arousal ratings were of similar magnitudewhen using eithermean arousal ratings at each rank [r = 0.46, F(1,40) = 12.83, P> 0.001] ormean arousal ratings for each imagined scene [r = 0.46, F(1,40) = 12.21, P> 0.005].

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Figure 1.Increased activation of NAc (A) and mPFC (B) was obtainedduring pleasant, compared to neutral, imagery, whereas amygdalaactivity (C) was increased during both pleasant and unpleasant,compared to neutral, imagery. Event-related signal change isplotted for pleasant, neutral, and unpleasant scenes beginning

with text presentation and continuing through subsequent im-agery in NAc (D), mPFC (E), and the amygdala (F). Talairachcoordinates are based on coronal slice selection. Error bars rep-resent 95% confidence intervals [Loftus and Masson, 1994].

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when this same relationship was assessed in each partici-pant (Fig. 3B). A positive linear correlation between NAcand mPFC activity during imagery was present in 86% ofparticipants and was significant in 76% of the sample.When the covariation of mean BOLD signal change inNAc and mPFC was separately assessed by hedonic con-tent, correlation coefficients when imagining pleasant (r !0.57; Z ! 2.92, P < 0.005) or unpleasant (r ! 0.36; Z !2.04, P < 0.05) scenes were larger than when imaginingneutral scenes (r ! #0.12), but did not differ from oneanother (Z ! 1.54, ns).

Amygdala

Functional connectivity of the amygdala with NAc andmPFC was heightened during pleasant, compared to neu-tral or unpleasant imagery. A significant temporal correla-tion across individuals was found in the BOLD time seriesbetween amygdala and NAc [t(28) ! 2.65, P ! 0.01, g2 !0.19] and between the amygdala and mPFC [t(28) ! 2.24,P < 0.05, g2 ! 0.15] when the latter time series was line-arly weighted by the a priori valence of the imaginedscene. Figure 4 illustrates the covariation of the BOLD ac-tivity in amygdala with activity in NAc (A) and mPFC (B)during imagery of each scene—for the four time points fol-lowing text presentation—separately assessed by hedoniccontent. Correlation of signal change in amygdala andNAc was larger during pleasant imagery (r ! 0.51) com-pared to neutral (r ! #0.04; Z ! 2.24, P < 0.05) orunpleasant (r ! 0.03; Z ! 2.86, P < 0.005) imagery. Corre-lation of signal change in amygdala and mPFC was alsolarger during pleasant imagery (r ! 0.59) compared toneutral (r ! #0.01; Z ! 2.62, P < 0.01) or unpleasant (r !0.11; Z ! 3.14, P < 0.005) imagery.

DISCUSSION

Narrative Emotional Imagery EngagesMotivational Centers

Imagining pleasant events strongly activated NAc andmPFC, compared to imagining unpleasant or neutralscenes. Selective activation of these structures developedover time as participants continued to imagine the pleas-ant events they had just read. Activation of NAc andmPFC also showed a positive, graded response that corre-lated highly with pleasure ratings for the imagined texts.These results suggest a central role for NAc and mPFC inprocessing pleasurable events that is consistent acrossstimulus media, showing the same pattern of activationduring pleasant imagery as previously observed inresearch assessing human reactions to tangible appetitivecues [Breiter et al., 1997, 2001; Knutson et al., 2005] orwhen viewing arousing pleasant pictures [Sabatinelli et al.,2007]. Peak activation coordinates reported here for pleas-ant imagery (NAc: $10, 7, #7; mPFC: #6, 58, 16) are veryclose to those we reported previously [Sabatinelli et al.,

Figure 2.Pleasure ratings correlate with mesolimbic BOLD activity duringimagery. Scenes were rank ordered by each participant’s pleas-ure ratings and plotted against the mean signal change in NAcand mPFC at each rank. Pie charts depict the proportion of thea priori selected pleasant, neutral, and unpleasant texts at eachrank [based on ANET standardized ratings; Bradley and Lang,2007].

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2007] during pleasant picture perception (NAc: $10, 9, #2;mPFC: #4, 39, 4), using the same MR hardware. The pres-ent results also clarify and expand on earlier findings[Rauch et al., 1999] of increased ventral pallidum activa-tion in men when imagining pleasant sexual encountersand athletic success, as well as findings [Kilts et al., 2001,2004] of increased NAc activation—although not mPFCactivation—during imagery of drug use in substanceabusers.

The finding of a pleasure-specific increase in NAc dur-ing narrative imagery contrasts with some studies suggest-ing that increased NAc activity is driven by stimulussalience, rather than selectively by positive hedonic cues(see review by Leknes and Tracy [2008]). The databaserelating NAc activity to aversive stimulation is quite com-plex, and the modulation found appears to vary with spe-cies (human or animal), specific brain measure (e.g., singleunit activity, dopamine release, PET, fMRI, etc.), type ofaversive stimulation (pain, odor, taste, picture, image,etc.), and processing paradigm (perception, anticipation,classical conditioning, operant conditioning, etc.). Whenconsidering fMRI studies with human participants, how-ever, the data are consistent in indicating that NAc activitydoes 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

and Borsook, 2008; Becerra et al., 2001], or process cuessignaling loss [Cooper and Knutson, 2007] or unpleasantodors [Gottfried et al., 2001]. The present study is consist-ent with these, indicating reward system activation duringpleasant emotional imagery in human participants.

In fact, in the current study, BOLD activity duringunpleasant imagery prompted marked signal decreasesfrom baseline in both NAc and mPFC. Similar signaldecreases to unpleasant content were found in these samestructures in our previous study of picture perception[Sabatinelli et al., 2007]. BOLD signal decreases from base-line have also been found in NAc with the onset of painfulstimulation [Aharon et al., 2006; Becerra and Borsook,2008; Becerra et al., 2001]. Furthermore, using PET,decreased rCBF in mPFC was observed when contrastingtraumatic and neutral imagery in patients with post-trau-matic stress disorder [Britton et al., 2005; Shin et al., 2004].

Research on the neurophysiology of the BOLD signaland rCBF [Goense and Logothetis, 2008; Logothetis et al.,2001; Mathiesen et al., 1998] indicates that hemodynamicmeasures generally reflect net excitation or inhibition ofcortical microcircuits [Logothetis, 2008]. Deactivation ofmesolimbic reward structures during unpleasant percep-tion and imagery might represent inhibition of appetitivecircuitry. Significantly greater deactivation of mPFC dur-ing unpleasant compared to neutral imagery, along with

Figure 3.Functional connectivity of NAc and mPFC during imagery. Themean BOLD signal change during imagery in each region, aver-aged over participants for each of the four time points followingtext presentation for pleasant (blue), neutral (green), or unpleas-ant (red) scenes (A). The adjacent panel (B) shows the ordered

distribution of the correlation between NAc and mPFC activityfor each participant during imagery (r > 0.16. is significant; 0 <r < 0.16 is not significant, and r < 0 are in the unpredicteddirection). [Color figure can be viewed in the online issue,which is available at wileyonlinelibrary.com.]

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reports that mPFC deactivation during trauma imagery iscorrelated negatively with symptom severity in PTSDpatients [Shin et al., 2004], further suggests that signaldecreases in mPFC may code for aversion. However,whether the extent of NAc deactivation generally indexesaversive processing remains unclear as imagining neutralscenes and viewing neutral pictures [Sabatinelli et al.,2007] also prompt similar decreases.

As anticipated, heightened amygdala activation wasfound during both pleasant and unpleasant imagery andwas positively correlated with emotional arousal ratingsfor the imagined scenes. This is consistent with similarpatterns of amygdala activation found when people viewpleasant and unpleasant emotionally arousing externalstimuli [Cooper and Knutson, 2007; Sabatinelli et al., 2005,2007; Zald, 2003], and complements extensive lesion andelectrophysiological work in animals demonstrating amyg-

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 activityin NAc and mPFC was evident during imagery regardlessof content, whereas activity in the amygdala was specifi-cally correlated with activity in NAc and mPFC duringappetitive processing. Complete functional connectivity ofNAc, mPFC, and the amygdala when imagining pleasantscenes is consistent with coactivation of these structureswhen viewing appetitive pictures [Sabatinelli et al., 2007]or processing monetary rewards [Cooper and Knutson,

Figure 4.Pleasure-specific connectivity of the amygdala with NAc and mPFC. Scatter plots depict the cor-relation of mean BOLD activity during imagery (averaged over participants for each of the fourtime points following text presentation) in the amygdala with NAc (A) and mPFC (B), separatelyevaluated for pleasant, neutral, and unpleasant scenes.

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2007]; as well as with evidence that intact afferents fromboth the mPFC [Ishikawa et al., 2008a] and amygdala[Ambroggi et al., 2008] are necessary for NAc neurons todisplay firing patterns predictive of subsequent appetitivebehavior.

Functional coupling of NAc and mPFC signal changewas expected given their common sensitivity to pleasureand known neuroanatomical connectivity [Ongur andPrice, 2000]. Electrical stimulation of mPFC neurons isreported to evoke firing in NAc neurons [McGinty andGrace, 2009], and pharmacological inactivation of mPFCreduces reward-seeking behaviors and related cue-evokedfiring of NAc neurons [Ishikawa et al., 2008a]. Anotherpossibility is that linked mesolimbic function during pleas-ant imagery is attributable to coordinated dopaminerelease, as systemic injection of dopamine releasing agentsincreases BOLD activity in both NAc and mPFC [Breiteret al., 1997; Knutson and Gibbs, 2007].

Functional connectivity of the amygdala with NAc andmPFC specific to pleasant imagery fits with the demon-strated sensitivity of these regions to ratings of emotionalarousal or pleasure, respectively. Considering that signalchange in both NAc and mPFC was unrelated to ratedemotional arousal, mesolimbic connectivity with the amyg-dala during pleasant imagery suggests a pathway for spe-cifically enhancing appetitive motivation. A lack ofnegative functional connectivity between the amygdalaand reward structures during unpleasant imagery furtheremphasizes the specific involvement of this circuit inappetitive processing.

This view is supported by animal studies in which phar-macological inactivation of the basolateral amygdala fol-lowing appetitive conditioning dampened cue-evokedexcitation of NAc neurons [Ambroggi et al., 2008] andreduced reward-seeking behaviors in a dose-dependentmanner [Ishikawa et al., 2008b]. Chemical inactivation ofthe amygdala’s central nucleus following food deprivationalso reduced dopamine release in NAc and mPFC duringfood consumption [Ahn and Phillips, 2002], while opioidstimulation of the central nucleus increased appetitive andconsummatory behaviors toward reward cues [Mahler andBerridge, 2009]. Interestingly, electrical stimulation of theamygdala is additionally found to increase neuronal firingin mPFC neurons projecting to NAc [McGinty and Grace,2008] and coincident stimulation of amygdala and mPFCinputs to NAc increases neuronal firing above mPFC stim-ulation alone [McGinty and Grace, 2009]. Taken together,the functional connectivity patterns identified here implythat the NAc, mPFC, and the amygdala form an integra-tive circuit that is engaged when humans directly processpleasurable emotional content.

Limitations and New Directions

Because imagery is an inherently mental event, ques-tions can arise regarding compliance with the task during

experimentation. In this study, the palpable changes inBOLD signal in NAc, mPFC, and amygdala at the onset ofthe instructed imagery period (see Fig. 1) and their strongcovariation with emotional ratings of experienced pleasureand arousal during imagery—both within and across par-ticipants (see Fig. 2A,B)—suggest compliance with the im-agery task. Moreover, prior psychophysiological studies ofboth anxiety patients and healthy participants, using thesame instructions and many of the same texts as in thisstudy, have repeatedly confirmed that text-driven imageryprompts heightened autonomic and somatic reaction con-sistent 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 difficultyof imaging each scene, and most reported that it was aneasy task.

Future neuroimaging work should, nevertheless, assesshow connectivity of these structures during imageryrelates to the appetitive motivational gradients defined byautonomic and somatic reflex indices [Bradley et al., 2001].Another aim is to determine how depressive psychopa-thology alters appetitive circuitry. There is considerableevidence that altered connectivity of rostral anterior cingu-late (rACC) with the amygdala and prefrontal cortices hasa role in mediating symptoms in depressed patients [e.g.,Yoshimura et al., in press] and that this circuit can bemodified by cognitive therapy and pharmacological inter-ventions [DeRubeis et al., 2008]. Increased activation ofrACC during pleasant imagery was not found here withhealthy participants, suggesting that the interactionbetween the cingulate and reward circuit may be specificto depression. Comparative studies with depressedpatients during pleasant narrative imagery could clarifythis issue and perhaps confirm a mechanism throughwhich mood disorders compromise appetitive neuralprocessing.

SUMMARY

Imagining pleasant, highly appetitive events selectivelyactivated NAc and mPFC, and their activation correlatedpositively with rated pleasure of the imagined scenes. Incontrast, imagery of either pleasant or unpleasant emo-tional scenes prompted increased amygdala activation,and its activation was positively correlated with ratedemotional arousal. Functional connectivity analyses deter-mined, furthermore, that coincident activation of all threeregions—amygdala, NAc, and mPFC—occurred onlywhen participants imaged pleasant scenes. Together, thesefindings provide strong evidence that pleasant andunpleasant imagery engage different motivational cir-cuits—appetitive and aversive—paralleling previous find-ings from animal and human studies of emotionallearning and perception. Moreover, these results suggestthat the clinical use of narrative imagery might be usefully

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extended to mood disorders (e.g., depression and dysthy-mia) in which appetitive processing may be compromised.

REFERENCES

Aharon I, Etcoff N, Ariely D, Chabris CF, O’Connor E, Breiter HC(2001): Beautiful faces have variable reward value: fMRI andbehavioral evidence. Neuron 32:537–551.

Aharon I, Becerra L, Chabris CF, Borsook D (2006): Noxious heatinduces fMRI activation in two anatomically distinct clusterswithin the nucleus accumbens. Neurosci Lett 392:159–164.

Ahn S, Phillips AG (2002): Modulation by central and basolateralamygdalar nuclei of dopaminergic correlates of feeding to sati-ety in the rat nucleus accumbens and medial prefrontal cortex.J Neurosci 22:10958–10965.

Ambroggi F, Ishikawa A, Fields HL, Nicola SM (2008): Basolateralamygdala neurons facilitate reward-seeking behavior by excit-ing nucleus accumbens neurons. Neuron 59:648–651.

Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG,Glover G, Gabrieli JD, Sobel N (2003): Dissociated neural rep-resentations of intensity and valence in human olfaction. NatNeurosci 6:196–202.

Baxter MG, Murray EA (2002): The amygdala and reward. NatRev Neurosci 3:563–573.

Bradley MM, Lang PJ (1994): Measuring emotion: The self-assess-ment manikin and the semantic differential. J Behav Ther ExpPsychiatry 25:49–59.

Bradley MM, Lang PJ (2007): Affective Norms for English Text(ANET): Affective Ratings of Text and Instruction Manual.Technical Report No. D-1. Gainesville, FL: University of Flor-ida. 32 p.

Bradley MM, Codispoti M, Cuthbert BN, Lang PJ (2001): Emotionand motivation I: Defensive and appetitive reactions in pictureprocessing. Emotion 1:276–298.

Becerra L, Breiter HC, Wise R, Gonzalez RG, Borsook D (2001):Reward circuitry activation by noxious thermal stimuli. Neu-ron 32:927–946.

Becerra L, Borsook D (2008): Signal valence in the nucleus accum-bens to pain onset and offset. Eur J Pain 12:866–869.

Berridge KC, Robinson TE, Aldridge JW (2009): Dissecting compo-nents of reward: ‘Liking’, ‘wanting’, and learning. Curr OpinPharmacol 9:65–73.

Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N,Berke JD, Goodman JM, Kantor HL, Gastfriend DR, RiordenJP, Mathew RT, Rosen BR, Hyman SE (1997): Acute effects ofcocaine on human brain activity and emotion. Neuron 19:591–611.

Breiter HC, Aharon I, Khaneman D, Dale A, Shizgal P (2001):Functional imaging of neural responses to expectancy and ex-perience of monetary gains and losses. Neuron 30:618–639.

Britton JC, Phan KL, Taylor SF, Fig LM, Liberzon I (2005): Cortico-limbic blood flow in posttraumatic stress disorder duringscript-driven imagery. Biol Psychiatry 57:832–840.

Cloutier J, Heatherton TF, Whalen PJ, Kelley WM (2008): Areattractive people rewarding? Sex differences in the neural sub-strates of facial attractiveness. J Cogn Neurosci 20:941–951.

Cooper JC, Knutson B (2007): Valence and salience contribute tonucleus accumbens activation. Neuroimage 39:538–547.

Cox RW (1996): AFNI: Software for analysis and visualization offunctional magnetic resonance imaging. Comput Biomed Res29:162–173.

Cuthbert BN, Lang PJ, Strauss C, Drobes D, Patrick CJ, BradleyMM (2003): The psychophysiology of anxiety disorder: Fearmemory imagery. Psychophysiology 40:407–422.

Davis M, Whalen PJ (2001): The amygdala: Vigilance and emotion.Mol Psychiatry 6:13–34.

DeRubeis RJ, Siegle GJ, Hollon SD (2008): Cognitive therapy ver-sus medication for depression: Treatment outcomes and neuralmechanisms. Nat Rev Neurosci 9:788–796.

Dougherty DD, Shin LM, Alpert NM, Pitman RK, Orr SP, LaskoM, Macklin ML, Fischman AJ, Rauch SL (1999): Anger inhealthy men: A PET study using script-driven imagery. BiolPsychiatry 46:466–472.

Friedman DP, Aggleton JP, Saunders RC (2002): Comparison ofhippocampal, amygdala, and perirhinal projections to the nu-cleus accumbens: Combined anterograde and retrograde trac-ing study in the macaque brain. J Comp Neurol 450:345–365.

Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997):Psychophysiological and modulatory interactions in neuroi-maging. Neuroimage 6:218–229.

Goense JB, Logothetis NK (2008): Neurophysiology of the BOLDfMRI signal in awake monkeys. Curr Biol 18:631–640.

Gottfried JA, O’Doherty J, Dolan RD (2001): Appetitive and aver-sive olfactory learning in humans studied using event-relatedfunctional magnetic resonance imaging. J Neurosci Sci 22:10829–10837.

Ishikawa A, Ambroggi F, Nicola SM, Fields HL (2008a): Dorsome-dial prefrontal cortex contribution to behavioral and nucleusaccumbens neuronal responses to incentive cues. J Neurosci 28:5088–5098.

Ishikawa A, Ambroggi F, Nicola SM, Fields HL (2008b): Contribu-tions of the amygdala and medial prefrontal cortex to incentivecue responding. Neuroscience 155:573–584.

Kilts CD, Schweitzer JB, Quinn CK, Gross RE, Faber TL, Muham-mad F, Ely TD, Hoffman JM, Drexler KP (2001): Neural activ-ity related to drug craving in cocaine addiction. Arch GenPsychiatry 58:334–341.

Kilts CD, Gross RE, Schweitzer JB, Ely TD, Quinn CK, DrexlerKPG (2004): The neural correlates of cue-induced craving incocaine-dependent women. Am J Psychiatry 161:233–241.

Knutson B, Taylor J, Kaufman M, Peterson R, Glover G (2005):Distributed neural representation of expected value. J Neurosci25:4806–4812.

Knutson B, Gibbs SE (2007): Linking nucleus accumbens dopamineand blood oxygenation. Psychopharmacology 191:813–822.

Lang PJ (1977): Imagery in therapy: An information processinganalysis of fear. Behav Ther 8:862–886.

Lang PJ (1979): A bio-informational theory of emotional imagery.Psychophysiology 16:495–512.

Lang PJ (1980): Behavioral treatment and bio-behavioral assess-ment: Computer applications. In: Sidowski JB, Johnson JH,Williams TA, editors. Techonology in Mental Heath CareDelivery Systems. Norwood, New Jersey: Ablex. p 119–137.

Lang PJ (1994): The motivational organization of emotion: Affect-reflex connections. In: Van Goozen SHM, Van De Poll NE, Ser-geant JA, editors. Emotions: Essays on Emotion Theory. Hill-sdale, NJ: Erlbaum. pp 61–93.

Lang PJ, Davis M (2006): Emotion, motivation, and the brain:Reflex foundations in animal and human research. Prog BrainRes 156:3–34.

Lang PJ, McTeague LM (2009): The anxiety disorder spectrum:Fear imagery, physiological reactivity, and differential diagno-sis. Anxiety Stress Coping 22:5–25.

r Costa et al. r

r 1456 r

Leknes S, Tracey I (2008): A common neurobiology for pain andpleasure. Nat Rev Neurosci 9:314–320.

Loftus GR, Masson MEJ (1994): Using confidence intervals inwithin-subject designs. Psychol Bull Rev 1:476–490.

Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A(2001): Neurophysiological investigation of the basis of thefMRI signal. Nature 412:150–157.

Logothetis K (2008): What we can do and what we cannot dowith fMRI. Nature 453:869–878.

Mathiesen C, Caesar K, Akgoren N, Lauritzen M (1998): Modifica-tion of activity-dependent increases of cerebral blood flow byexcitatory synaptic activity and spikes in rat cerebellar cortex. JPhysiol 512:555–566.

Mahler SV, Berridge KC (2009): Which cue to ‘‘want?’’ Centralamygdala opioid activation enhances and focuses incentivesalience on a prepotent reward cue. J Neurosci 29:6500–6513.

McGaugh JL (2004): The amygdala modulates the consolidation ofmemories of emotionally arousing experiences. Annu RevNeurosci 27:1–28.

McGinty VB, Grace AA (2009): Timing-dependent regulation ofevoked spiking in nucleus accumbens neurons by integrationof limbic and prefrontal cortical inputs. J Neurophysiol 101:1823–1835.

McGinty VB, Grace AA (2008): Selective activation of medial pre-frontal-to-accumbens projection neurons by amygdala stimula-tion and Pavlovian conditioned stimuli. Cereb Cortex 18:1961–1972.

McTeague LM, Lang PJ, Laplante MC, Cuthbert BN, Strauss CC,Bradley MM (2009): Fearful imagery in social phobia: General-ization, comorbidity, and physiological reactivity. Biol Psychia-try 65:374–382.

Meseguer V, Romero MJ, Barros-Loscertales A, Belloch V, Bosch-Morell F, Romero J, Avila C (2007): Mapping the appetitiveand aversive systems with emotional pictures using a block-design fMRI procedure. Piscotherma 19:483–488.

Nichols TE, Holmes AP (2002): Nonparametric permutation testsfor functional neuroimaging: A primer with examples. HumBrain Mapp 15:1–25.

Ongur D, Price JL (2000): The organization of networks within theorbital and medial prefrontal cortex of rats, monkeys andhumans. Cereb Cortex 10:206–219.

Orr SP, Pitman RK, Lasko NB, Herz LR (1993): Psychophysiologicassessment of posttraumatic stress disorder imagery in WorldWar II and Korean combat veterans. J Abnorm Psychol102:152–159.

Phan KL, Taylor SF, Welsh RC, Ho S, Britton JC, Liberzon I(2004): Neural correlates of individual ratings of emotionalsalience: A trial related fMRI study. Neuroimage 21:786–780.

Rauch SL, Shin LM, Dougherty DD, Alpert NM, Orr SP, Lasko M,Macklin ML, Fischman AJ, Pitman RK (1999): Neural activa-tion during sexual and competitive arousal in healthy men.Psychiatry Res 91:1–10.

Sabatinelli D, Bradley MM, Fitzsimmons JR, Lang, PJ (2005): Paral-lel amygdala and inferotemporal activation reflect emotionalintensity and fear relevance. Neuroimage 24:1265–1270.

Sabatinelli D, Bradley MM, Lang PJ, Costa VD, Versace F (2007):Pleasure rather than salience activates human nucleus accum-bens and medial prefrontal cortex. J Neurophysiol 98:1374–1379.

Shin LM, Dougherty DD, Orr SP, Pitman RK, Lasko M, MacklinML, Alpert NM, Fischman AJ, Rauch SL (2000): Activation ofanterior paralimbic structures during guilt-related script-drivenimagery. Biol Psychiatry 48:43–50.

Shin LM, Orr SP, Carson MA, Rauch SL, Macklin ML, Lasko NB,Peters PM, Metzger LJ, Dougherty DD, Cannistraro PA, AlpertNM, Fischman AJ, Pitman RK (2004): Regional cerebral bloodflow in the amygdala and medial prefrontal cortex duringtraumatic imagery in male and female Vietnam veterans withPTSD. Arch Gen Psychiatry 61:168–176.

Sinha R, Lacadie C, Skudlarski P, Wexler BE (2004): Neural cir-cuits underlying emotional distress in humans. Ann NY AcadSci 1032:254–257.

Talairach J, Tournoux P (1998): Co-planar Stereotaxic Atlas of theHuman Brain: An Approach to Medical Cerebral Imaging.Stuttgart: Thieme. 122 p.

Vrana SR, Cuthbert BN, Lang PJ (1986): Fear imagery and textprocessing. Psychophysiology 23:247–253.

Vrana SR, Lang PJ (1990): Fear imagery and the startle probereflex. J Abnorm Psychol 99:189–197.

Witvliet CV, Vrana SR (1995): Psychophysiological responses asindices of affective dimensions. Psychophysiology 32:436–443.

Wolpe J (1958): Psychotherapy by Reciprocal Inhibition. Stanford:Stanford University Press. 239 p.

Yoshimura S, Okamoto Y, Onoda K, Matsunaga M, Ueda K,Suzuki SI, Shigetoyamawaki: Rostral anterior cingulate cortexactivity mediates the relationship between the depressivesymptoms and the medial prefrontal cortex activity. J AffectDisord (in press). doi:10.1016/j.jad.2009.06.017.

Zald D (2003): The human amygdala and the emotional evalua-tion of sensory stimuli. Brain Res Brain Res Rev 41:88–123.

r Emotional Imagery Activates Reward Circuits r

r 1457 r