NeuroImage 70 (2013) 268–277

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Neural correlates of attentional deployment within unpleasant pictures

Jamie Ferri ⁎, Joseph Schmidt, Greg Hajcak, Turhan CanliDepartment of Psychology, Stony Brook University, Stony Brook, NY, USA

⁎ Corresponding author at: Department of PsychologyBrook, NY 11794-2500, USA. Fax: +1 631 632 7876.

E-mail address: jamie.ferri@stonybrook.edu (J. Ferri

1053-8119/$ – see front matter © 2012 Elsevier Inc. Allhttp://dx.doi.org/10.1016/j.neuroimage.2012.12.030

a b s t r a c t

a r t i c l e i n f o

Article history:Accepted 17 December 2012Available online 25 December 2012

Keywords:AttentionEmotionAttentional deploymentfMRIIAPS

Attentional deployment is an emotion regulation strategy that involves shifting attentional focus towardsor away from particular aspects of emotional stimuli. Previous studies have highlighted the prevalence ofattentional deployment and demonstrated that it can have a significant impact on brain activity and behavior.However, little is known about the neural correlates of this strategy. The goal of the present studies was toexamine the effect of attentional deployment on neural activity by directing attention tomore or less arousingportions of unpleasant images. In Studies 1 and 2, participants passively viewed counterbalanced blocks ofunpleasant images without a focus, unpleasant images with an arousing focus, unpleasant images with anon-arousing focus, neutral images without a focus, and neutral images with a non-arousing focus for4000 ms each. In Study 2, eye-tracking data were collected on all participants during image acquisition. Inboth studies, affect ratings following each block indicated that participants felt significantly less negativeaffect after viewing unpleasant images with a non-arousing focus compared to unpleasant images with anarousing focus. In both studies, the unpleasant non-arousing focus condition compared to the unpleasantarousing focus condition was associated with increased activity in frontal and parietal regions implicated ininhibitory control and visual attention. In Study 2, the unpleasant non-arousing focus condition comparedto the unpleasant arousing focus condition was associated with reduced activity in the amygdala and visualcortex. Collectively these data suggest that attending to a non-arousing portion of an unpleasant image success-fully reduces subjective negative affect and recruits fronto-parietal networks implicated in inhibitory control.Moreover, when ensuring task compliance by monitoring eye movements, attentional deployment modulatesamygdala activity.

© 2012 Elsevier Inc. All rights reserved.

Introduction

Compared to neutral stimuli, emotional stimuli are detected faster(Öhman et al., 2001; Vuilleumier and Schwartz, 2001) andhold attentionmore efficiently (Lang et al., 1997). However, it is not always adaptive toattend to emotional information; involuntary attention to task-irrelevantemotional stimuli can slow reaction times and decrease accuracy(MacNamara and Hajcak, 2009; Vuilleumier et al., 2001). Indeed, beingtoo attentive to negative information represents a cognitive vulnerabilityfor psychopathologies such as anxiety and depression (Bar-Haim et al.,2007; Joormann, 2009).

People are capable of exerting control over reflexive responses toemotional stimuli by using a number of emotion regulation techniques.Attentional deployment, for example, is a strategy that involves shiftingattention towards or away from affective stimuli in the interest of anemotional goal (Gross, 1998; Gross and Thompson, 2007). Attentionaldeployment is one of the earliest emotion regulation strategies toemerge in development: very young children use distraction to delay

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gratification (Mischel andAyduk, 2011), and even grade school childrenare aware that changes in attention can change the way they feel(Harris and Lipian, 1989). The use of attentional deployment continuesbeyond childhood; adults shift attention away from negative parts ofimages to reduce negative affect even without instruction to do so(van Reekum et al., 2007; Xing, 2006). Older adults in particular seemto divert gaze away from negative information and towards positiveinformation in the interest of regulating mood (Isaacowitz et al., 2006,2009; Mather and Carstensen, 2005). Individuals who are able tosuccessfully deploy attention away from negative, or towards positive,information appear to experience both improved mood and decreasedfrustration with difficult tasks (Johnson, 2009; Urry, 2010). These datasuggest that attentional deployment is an effective strategy to regulateemotional response that emerges early and persists throughout thelifespan.

Previous studies have also shown that attentional deployment canhave a dramatic impact on brain activity. A number of studies haveexamined the late positive potential (LPP), a centro-parietal event-related potential that is larger for emotional compared to neutralstimuli (Cuthbert et al., 2000; Schupp et al., 2000). To examine theimpact of attentional deployment on the LPP, Dunning and Hajcak(2009) asked participants to passively view unpleasant and neutralimages for 3 seconds, after which a circle was presented to direct

269J. Ferri et al. / NeuroImage 70 (2013) 268–277

participants to either an arousing or a non-arousing portion of an un-pleasant image, or to a non-arousing portion of a neutral image. TheLPP was larger in response to emotional images both during the passiveviewing period and when attention was directed towards the arousingportion of the image, but not when attention was directed to anon-arousing portion of the same unpleasant image. In another study,Hajcak et al. (2009) found that using a tone, rather than a visual cue,to direct participants to an arousing or non-arousing portion of an un-pleasant image produced an analogous effect—the LPP was reliably re-duced when participants were instructed to attend to a non-arousingportion of unpleasant images. These findings are in concert with thosereporting reduced LPP magnitude during cognitive reappraisal—a strat-egy that involves changing themeaning of emotional situations or stim-uli in order to change emotional significance (Foti and Hajcak, 2008;Hajcak and Nieuwenhuis, 2006; MacNamara et al., 2009). This suggeststhat attentional deployment, even in the absence of a goal to intention-allymodify emotional experience, can function to reduce neural indicesof attention to emotion.

Nevertheless, relatively little is known about the specific brainstructures and networks involved in attentional deployment. It isestimated that the LPP reflects activity in fronto-parietal attentionnetworks (Moratti et al., 2004) and some have suggested it may alsoreflect indirect activity from the amygdala (Lang and Bradley, 2010),however the exact neural sources of the LPP are unknown. While it isclear that the LPP is reduced following attentional deployment, it isnot clear what changes in brain activity support this reduction.Although fMRI would be an ideal avenue to explore the neural corre-lates of attentional deployment, thus far, the majority of fMRI studiesof emotion regulation have focused on cognitive reappraisal. The neuralsystems associatedwith this strategy have been extensively studied andhave culminated in a model suggesting that successful emotion regula-tion relies on interactions between prefrontal regions associated withcognitive control, and limbic regions such as the amygdala whichhave been associated with response to emotion (Ochsner and Gross,2008).

In addition to prefrontal and limbic regions, many emotion regula-tion studies also report increased activations in regions related to visualattention and inhibitory control, such as the superior parietal lobule andthe precuneus (Hopfinger et al., 2000; Pessoa et al., 2003). As fronto-parietal regions are critical for visuospatial attention and visual control,van Reekum et al. (2007) reasoned that activation in these regionsmight reflect shifts in gaze to achieve emotion regulatory goals eventhough participants were instructed to use cognitive strategies such asreappraisal. Changes in subject emotional experience due to cognitivereappraisal should occur as a result of changes in appraisal, ratherthan changes in attention. Using eye-tracking, van Reekum and col-leagues found that when participants were instructed to use cognitivereappraisal to increase or decrease their emotional response to unpleas-ant pictures, they spent more or less time, respectively, looking at themost arousing portions of these images. Further, when participantswere instructed to decrease negative emotion using cognitive reappraisal,the amount of time spent looking at arousing portions of the images pre-dicted a significant amount of variation in neural activity, including up to35% in the amygdala, and as much as 75% in other regions often reportedin emotion regulation studies such as the middle frontal gyrus, theprecentral gyrus, and the cuneus (van Reekum et al., 2007). Thus, atten-tional deployment may account for some, but not all, of the variance inneural activity associated with cognitive reappraisal. Indeed, subsequentstudies have shown that cognitive reappraisal results in reduced auto-nomic arousal and subjective affect even when gaze is held constant(Urry, 2010). However, these findings highlight the importance of atten-tional deployment as an emotion regulation strategy and inspire ques-tions regarding the underlying neural mechanisms.

The goal of the present studywas to examine the effect of attentionaldeployment on neural activation and subjective affect while partici-pants viewed unpleasant and neutral images in the absence of a

regulatory goal. In Study 1, we collected eye-tracking data from a subsetof participants (5 of 41) during scanning to assess task compliance. InStudy 2, we collected eye-tracking data from all participants of a secondindependent cohort (n=47). We avoided any explicit instruction tomodify emotional state in an effort to understand the impact of visualattention alone on neural activation and affect. While previous studieshave independently demonstrated that attentional deployment canhave a significant impact on brain activity and behavior, the neuralcorrelates of attentional deployment are not well understood, and itremains unknown whether successful attentional deployment relieson the same well-defined circuits as cognitive reappraisal. As previousstudies have reported that attentional deployment during cognitivereappraisal accounts for at least someof the variance in activity in limbicas well as fronto-parietal regions (van Reekum et al., 2007), we hypoth-esized that these regions would also be involved in attentional deploy-ment in the absence of other explicit regulatory goals (i.e. cognitivereappraisal). Specifically, we hypothesized that directing gaze to anon-arousing, compared to an arousing, portion of a unpleasant imagewould result in reduced activation in areas of the brain implicated inemotional processing, including the amygdala, and correspondingincreases in fronto-parietal regions associated with top-down atten-tional control. We also collected subjective ratings of negative affectduring the course of the experiment in both studies. We predictedthat participants would report reduced negative affect during unpleas-ant non-arousing compared to unpleasant arousing focus trials, and thatunpleasant arousing focus trials would not differ from unpleasant trialswithout a focus.

Study 1

Materials and methods

ParticipantsForty-one healthy adults (22 females) with a mean age of 22.29

and no history of neurological or psychological illness were recruitedto participate in the study. Participants self-identified as 53.7%Caucasian,31.7% Asian, 9.8% African American, and 4.8% “Other.” The study wasapproved by The Committees on Research Involving Human Subjectsat Stony Brook University. All participants provided informed consentand received payment for their participation. Participants were nativeEnglish speakers who had normal or corrected-to-normal vision andno history of neurological or psychiatric diagnoses.

StimuliSixty unpleasant and forty neutral images from the International

Affective Picture System (Lang et al., 2008) were selected for thisstudy. Normative ratings (Lang et al., 2005) indicated that unpleasantimages were less pleasant (M=2.28, SD=1.47) than neutral images(M=5.14, SD=1.28), and that unpleasant images were morearousing (M=6.05, SD=2.25) than neutral images (M=2.91, SD=1.92); higher numbers indicate higher self-reported pleasantnessand arousal.

Stimuli were presented in a counterbalanced block design. Twentyunpleasant and twenty neutral pictures were presented withoutmodification. For the remaining images, attention was directed to asmaller portion of the image by placing a blue circle over that portion.These images were taken from a set of stimuli created by Dunning andHajcak (2009), along with 20 additional neutral images. For the neutralpictures, the blue circle was always placed over a non-arousing, butvisually complex portion of the picture. For the unpleasant pictures,the blue circle was either placed over an arousing or non-arousingportion of the image. The procedure for selecting areas of focus isoutlined byDunning andHajcak (2009). Thereforewe had 5 conditions:neutral images with no focus, neutral images with a non-arousingfocus, unpleasant images with no focus, unpleasant images with anarousing focus, and unpleasant images with a non-arousing focus.

270 J. Ferri et al. / NeuroImage 70 (2013) 268–277

Each participant viewed the same set of IAPS images; however, to en-sure that differences between conditions were not due to the specificimages selected for a given condition, pictures were counterbalancedacross subjects such that each unpleasant picture appeared in the nofocus, non-arousing focus, and arousing focus condition an equal num-ber of times across subjects. For example, the set of images used for theunpleasant arousing focus condition for the first subject would be usedfor the unpleasant non-arousing focus condition for the second subjectbymoving the location of the circle. Similarly, the neutral pictures werecounterbalanced so that they appeared in the no focus or focus condi-tions an equal number of times across subjects. The order of blockswas counterbalanced for each subject so that one condition did notfollow another more than once during an experimental session. Imageswithin each block were presented in a random order and were neverrepeated. No picture was presented in more than one condition for agiven subject. Stimuli were presented in 2 runs of 10 blocks each.

The task for the first 36 subjects was presented using E-Prime 2(Psychology Software Tools, Inc., version 2). For the remaining fivesubjects, we re-programmed the experiment using Experiment Buildersoftware package (SR Research Ltd, version 1.10.165) in order to collecteye-tracking data during image acquisition. The experimental designfor the eye-tracking version of the experiment was identical to that ofthe original experiment. Stimuli for both versions of the task werepresented using an MRI-compatible 60 Hz projector with a 1024×768resolution which back-projected stimuli onto a mirror attached to thehead coil.

ProcedureParticipants were instructed to passively view sets of images and

then rate their negative affect following each set of images. Participantswere told that for some sets of images theywould be instructed to freelyview the images, while for other sets they would be asked to focus theireyes and attention only on the part of the picture within the blue circle.

Each trial began with a 5-second instruction to either “look freelyat the following images” for no focus blocks, or to “look only at thepart of the image within the blue circle” for focus blocks. Participantsthen viewed five pictures presented for 4 seconds each. Participantswere then given 5 seconds to rate the intensity of their negative affecton a scale from one to four, with one being “not intense at all” and fourbeing “very intense” using a four button custom built MRI-compatibleresponse box. Fixation crosses were then presented in the center of thescreen on a 10% to 50% saturated grey background, which alternatedevery 4 seconds for 20 seconds total. A schematic of the design can beseen in Fig. 1.

Fig. 1. Depiction of a neutral non-arousing focus block followed by a neutral no focus block. Eon the contents of the blue circle or to freely view the following set of images. This was fol5000 ms to rate the intensity of their negative affect on a scale of 1 to 4. Finally, participants

Eye-Tracking data acquisition and analysisEye position was sampled at 1000 Hz, using a long-range mounted

EyeLink 1000 eye-tracker with default saccade detection settings. Eachrun of trials beganwith a thirteen-point calibration routine used tomapeye position to screen coordinates. Calibrations were not consideredacceptable until the average errorwas less than 0.49° and themaximumerror was less than 0.99°.

Data analysis was conducted off-line using the DataViewer softwarepackage (SR Research Ltd, version 1.11.1). The regions within the focuscircles were defined as interest areas (IAs) and cumulative fixationduration (dwell time) within these regions was computed. Groupmeans for the eye data were obtained by first averaging fixation dataacross images within each block, then across blocks and finally acrossparticipants.

fMRI data acquisition and analysisA 3 Tesla Siemens TrioTim whole body scanner (Siemens Medical,

Erlangen, Germany) with a 12 channel head coil was used to acquire400 T2 star-weighted whole-brain volumes with an EPI sequence foranalysis of BOLD signal. The following parameters were used: TR=2500 ms, TE=30 ms, flip angle=90°, matrix dimensions=64×64,FOV=256, 256 mm, slices=34, aligned to the AC-PC, slice thickness=4 mm, slice acquisition=interleaved, gap=0.

Standard preprocessing procedures were performed in SPM8starting with slice time correction, followed by realignment for motioncorrection, normalization to standard Montreal Neurological Institutespace, and spatial smoothing using a Gaussian kernel with 8 mmFWHM. First level single subject SPMs were created for each subjectfrom a model that specified the onset of each condition, the ratingperiod and the instruction period. At the second level, random effectsanalyses were conducted to test for statistical differences between con-ditions of interest using contrasts created for each individual at the firstlevel. A height threshold set to FDR .05 was used to correct for multiplecomparisons. We report only those peak activations that are significantat less than p=.025, FDR corrected, with an extent size larger than 10voxels.

In order to assess differences in brain activity as a result of eyemove-ments being explicitly monitored we compared the five eye-trackingsubjects to five random non-eye-tracking subjects for each of ourmain contrasts. There were no significant differences in brain activityon any of the contrasts (unpleasant no focus compared to neutral nofocus, focus compared to no focus, or unpleasant non-arousing focuscompared to unpleasant arousing focus) at our significance threshold,or at thresholds as low as p=.01, uncorrected.

ach block began with a 5000 ms instruction screen indicating if the subject was to focuslowed by the presentation of 5 images for 4000 ms each. Participants were then givensaw fixations presented on grey backgrounds for 20,000 ms (Font size is not to scale).

Table 1Means (and standard deviations) for average dwell time and percent dwell time (dwell time in IA/total dwell time−time to first fixation in IA) in the interest area (IA) per image(4000 ms presentation) in Study 1 (n=5).

UnpleasantNo focus(no visible IA)

Unpleasant arousing focus UnpleasantNon-arousing focus

NeutralNo focus(no visible IA)

NeutralNon-arousing focus

Dwell time (ms) Arousing: 1136.74 (496.18); non-arousing: 126.38 (24.00) 2800.43 (382.80) 2774.68 (281.67) 434.48 (170.46) 3085.68 (343.55)Dwell time (%) Arousing: 41%; non-arousing: 4% 82% 87% 17% 90%

Table 3Peak activations for the unpleasant non-arousing focus compared to unpleasant arousingfocus conditions in Study 1 (n=41).

Region BA ClusterSize

Talairachcoordinates

T Z

R supramarG 40 1900 57 −41 37 6.43 5.30L SOG 19 −34 −72 28 5.78 4.90L precuneus 19 −18 −76 42 5.73 4.87

R MidFG 9 1712 34 33 30 6.19 5.16R MidFG/R cingG 32 14 14 42 5.33 4.60R MidFG 6 18 7 57 5.29 4.58

L insula 13 141 −30 23 1 4.42 3.97L insula 13 −42 12 5 4.07 3.70

R MTG 21 41 65 −24 −11 4.34 3.91R MTG, TPJ 21 65 −43 −3 2.72 2.59

L MidFG 9 255 −30 29 34 4.22 3.81L SFG 10 −34 47 14 3.88 3.55L MidFG 11 −38 50 −11 3.71 3.42

L Cblm 293 −42 −56 −29 4.10 3.73L Cblm −34 −56 −26 3.77 3.47L Cblm −26 −58 −2 3.52 3.27

R parahippG 19 62 30 −47 −6 3.80 3.49

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Results

Manipulation checks

Did participants stay within the focus regions as instructed? Means andstandard deviations for dwell time and percent dwell time arepresented in Table 1. During focus trials, participants complied withtask instructions to focus on the contents of the blue circle, spendingbetween 82% and 90% of total dwell time within the blue circle.During free viewing of unpleasant images, even though there wereno circles directing attention to any portion of the image, participantsspent significantly more time looking in the areas where the arousingfocus region would be compared to where the non-arousing focusregion would be, t (4)=4.63, p=.01.

Areas associated with viewing unpleasant images. The whole brainanalysis for the simple effect of emotion (unpleasant no focus greaterthan neutral no focus) on the BOLD response revealed clusters ofactivation in occipital, frontal, limbic, and parietal regions. In frontalregions, the unpleasant no focus condition resulted in significantlygreater activations in bilateral superior frontal gyrus (BA8/9) andbilateral middle frontal gyrus (BA 6/46). There was significantly greateractivity in the left amygdala.Within parietal regions, greater activationswere seen in bilateral precuneus (BA 7), bilateral postcentral gyrus, andthe inferior parietal lobe (BA 40). Table 1 in the supplemental materialsidentifies significant regions associated with this contrast.

Areas associated with focusing. The effect of overall focus (unpleasantarousing focus+unpleasant non-arousing focus+neutral non-arousingfocus greater than unpleasant no focus+neutral no focus) revealed alarge cluster of activation that covered themajority of frontal and parietalregions, with peak activations in the precuneus (BA 7), the superiorparietal lobe (BA 7), and the inferior parietal lobe (BA 40). This clusterextended into frontal regions including the middle frontal gyrus (BA 6/9/10) and the anterior cingulate (BA 32). These activations are listed inTable 2 of the supplemental materials.

Hypothesis testing

Did focusing on a non-arousing portion of an unpleasant image reducenegative affect? Means and standard deviations for affect ratings arepresented in Table 2. Participants reported feeling less negative affectfollowing the unpleasant non-arousing focus condition compared toboth the unpleasant arousing focus, t (40)=8.96, pb .001, and theunpleasant no focus conditions, t (40)=9.44, pb .001. Participants alsoreported feeling more negative affect following the unpleasant non-arousing focus condition compared to both the neutral non-arousing

Table 2Means (and standard deviations) for ratings of negative affect intensity (1 being “notintense at all” and 4 being “very intense”) following each condition in Study 1 (n=41).

UnpleasantNo focus

UnpleasantArousingfocus

UnpleasantNon-arousingfocus

NeutralNo focus

NeutralNon-arousingfocus

Affect Rating 3.18 (.84) 3.22 (.77) 2.11 (.75) 1.05 (.28) 1.07 (.30)

focus t (40)=8.9, pb .001 and the neutral no focus conditions t (40)=9.06, pb .001. Therewere no significant differences between the unpleas-ant no focus and unpleasant arousing focus conditions, t (40)=− .47,p=.64, or the neutral no focus and neutral non-arousing focus condi-tions, t (40)=− .91, p=.37.

Was focusing on an arousing portion of an unpleasant image (compared toa non-arousing portion) associated with increased amygdala activation?There was no difference in amygdala activation between the unpleasantarousing focus condition and the unpleasant non-arousing focus condi-tion. No regions of the brain were more active for the unpleasant arous-ing focus compared to the unpleasant non-arousing focus condition atp>.05, FDR corrected.

Was focusing on a non-arousing portion of anunpleasant image (comparedto an arousing portion) associated with increased frontal and parietalactivity? Focusing on an unpleasant non-arousing region, compared toan arousing region produced significantly greater activations inparietal regions including the supramarginal gyrus (BA 40), the cuneus,the precuneus (BA 7), as well as greater activation in frontal regionsincluding the inferior frontal gyrus (BA 47), the middle frontal gyrus(BA 10), the superior frontal gyrus (BA 9), the precentral gyrus (BA 6)and the cingulate gyrus (BA 32). These activations are presented inTable 3 and Fig. 2.

Overall findings from Study 1 indicated that attention to a non-arousing, compared to an arousing, portion of an unpleasant image

R parahippG 36 30 −39 −10 3.63 3.35L MTG 21 11 −65 −31 −7 3.31 3.09

L MTG 21 −65 −43 −3 2.96 2.80R thalamus 55 14 −19 18 3.22 3.01

R thalamus 10 −12 2 3.09 2.91R lentiform nucleus, putamen 26 −8 2 2.75 2.61

R supramarG 40 1900 57 −41 37 6.43 5.30

Peak activations from random effects analysis are listed with a threshold of pb .025,FDR corrected, and cluster filter of 10 contiguous voxels. BA=Brodmann's area, R=right, L=left, supramarG=supramarginal gyrus, SOG=superior occipital gyrus,MFG=middle frontal gyrus, cingG=cingulate gyrus, MTG=middle temporal gyrus,SFG=superior frontal gyrus, Cblm=cerebellum, parahippG=prahippocampal gyrus.

Fig. 2. Regions of the brain more active for unpleasant non-arousing focus compared to unpleasant arousing focus in Study 1.

272 J. Ferri et al. / NeuroImage 70 (2013) 268–277

was associated with reduced negative affect and increased activationsin frontal and parietal regions associated with cognitive control. How-ever, contrary to our hypothesis, we did not observe a reduction inamygdala activity for this contrast. To ensure that individual differencesin task compliance and viewing patterns were not contributing to thislack of difference, we ran a second study using the same task with anadditional fifty-one individuals, all with eye-tracking data. In Study 2we sought to replicate the findings of Study 1 and to investigate anysystematic differences resulting the collection of eye-tracking data onall individuals.

Study 2

Materials and methods

ParticipantsFifty-one healthy adults with no history of neurological or psycho-

logical illness were recruited to participate in Study 2. No participants

from Study 1 participated in Study 2. Four subjects were excludedfrom analysis as a result of spending less than 50% of dwell time in theinterest area on neutral trials with a non-arousing focus. One of thesesubjects reported intentionally looking off screen to avoid unpleasantstimuli, while the remaining subjects closed their eyes for large portionsof blocks of all types due to self-reported sleepiness. The final data setincluded 47 participants (25 females) with a mean age of 21.57. Partici-pants self-identified as 57.4% Caucasian, 19.1% Latino/a, 17% Asian, 4.3%African American, and 1% “Other.” The study was approved by TheCommittees on Research Involving Human Subjects at Stony BrookUniversity. All participants provided informed consent and receivedpayment for their participation. Participants were native Englishspeakers who had normal or corrected to normal vision and no historyof neurological or psychiatric diagnoses.

Stimuli, procedure, data acquisition and data analysisThe stimuli and procedure for Study 2 were largely identical to

Study 1 with the following exceptions. In Study 2, the images within

Table 4Means (and standard deviations) for dwell time and percent dwell time (dwell time in IA/total dwell time−time to first fixation in IA) in the interest area (IA) per image (4000 mspresentation) in Study 2 (n=47).

UnpleasantNo focus(no IA visible)

Unpleasant arousing focus UnpleasantNon-arousing focus

NeutralNo focus (no IA visible)

NeutralNon-arousingfocus

Dwell time (ms) Arousing: 1410.39 (282.53); non-arousing: 202.39 (115.04) 3312.09 (283.77) 3168.30 (331.49) 447.24 (132.65) 3317.24 (304.56)Dwell time (%) Arousing: 47%; non-arousing: 5% 96% 97% 18% 99%

Table 6Peak activations for the unpleasant arousing focus greater than unpleasant non-arousingfocus conditions in Study 2 (n=47).

Region BA Cluster size Talairach coordinates T Z

L IOG 17 851 −18 −91 −6 10.55 7.48R IOG 17 22 −91 1 8.88 6.74L Cblm −33 −78 −16 6.85 5.66

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each block were no longer presented in a random order. Instead, im-ages were carefully balanced such that the average distance betweenthe centers of interest areas across condition types did not differ. Thiswas to ensure that a difference in the distance that participants movedtheir eyes to reach the focus areas between unpleasant arousing focusand unpleasant non-arousing focus would not impact observed differ-ences in brain activity for this contrast. In addition, we no longerpresented the fixation crosses on alternating grey backgrounds. Instead,we calculated the mean luminance of all affective pictures and set boththe instruction screens and the fixation background to this value. Thiswas done to minimize changes in pupil diameter as a function ofchanges in luminance, which can impact eye-tracking accuracy. Finally,we asked subjects to fixate on the center of the blue circle so that smallerrors in eye tracking would not result in fixations being recorded asoutside of the interest area.

The data acquisition and analysis procedures for Study 2 wereidentical to those listed for the eye-tracking portion of Study 1 withone exception. In order to correct for drift during the course of theexperiment, due to changes in pupil size in response to changing lumi-nance levels and emotional content, we enable a drift correction proce-dure that allowed us to re-calibrate the eye-tracker to the center of thescreen during the presentation of fixation crosses. In addition to thedata acquisition and analysis procedure described in Study 1, in Study2 we also used the AAL atlas (Tzourio-Mazoyer et al., 2002) in WFUPickatlas (Maldjian et al., 2003) to create a bilateral amygdala mask inorder to conduct an ROI analysis of amygdala activity.

Results

Manipulation checks

Did participants stay within the focus regions as instructed? Means andstandard deviations for dwell time and percent dwell time arepresented in Table 4. As in Study 1, during focus trials, participantscomplied with task instructions to focus on the contents of the bluecircle, spending between 96% and 99% of total dwell time within theblue circle. During free viewing of unpleasant images participantsagain spent significantly more time looking in the areas where thearousing focus region would be compared to where the non-arousing region would be, t (46)=23.67, p=.001.

Areas associated with viewing unpleasant images. Replicating Study 1,the whole brain analysis revealed activations in the occipital, frontaland parietal regions. Overlapping regions of activation included thefusiform gyrus, the middle and superior frontal gyrus in the prefrontal

Table 5Means (and standard deviations) for ratings of negative affect intensity (1 being “notintense at all” and 4 being “very intense”) following each condition in Study 2 (n=47).

Unpleasantno focus

Unpleasantarousingfocus

Unpleasantnon-arousingfocus

Neutralno focus

Neutralnon-arousingfocus

Affect rating 3.09 (.65) 3.16 (.63) 2.43 (.74) 1.14 (.27) 1.15 (.29)

cortex, and the postcentral gyrus in the parietal lobe. Table 3 of thesupplemental materials list significant activations associated withthis contrast. An ROI analysis using a mask for bilateral amygdalarevealed significant peaks in both the right and left amygdala. Coordi-nates are listed at the bottom of Table 3.

Areas associated with focusing. As in Study 1, the effect of overall focus(unpleasant arousing focus+unpleasant non-arousing focus+neutralnon-arousing focus greater than unpleasant no focus and neutral nofocus) revealed several large clusters of activation covering frontaland parietal regions in Study 2. Peak activations echoed those inStudy 1 and included the inferior parietal lobe (BA 40), and the middlefrontal gyrus (BA 6). These activations are presented in Table 4 of thesupplemental materials.

Hypothesis testing

Did focusing on a non-arousing portion of an unpleasant image reducenegative affect? Means and standard deviations for affect ratings arepresented in Table 5. Replicating Study 1, participants rated their nega-tive affect during the unpleasant non-arousing focus condition as signif-icantly less than both the unpleasant arousing focus, t (46)=8.21,pb .001, and the unpleasant no focus conditions, t (46)=6.79, pb .001.Participants also rated affect following the unpleasant non-arousingfocus condition as significantly more negative than both the neutralnon-arousing focus t (46)=11.69, pb .001 and the neutral no focus con-ditions, t (46)=23.02, pb .001. There were no significant differencesbetween the unpleasant no focus and unpleasant arousing focus condi-tions, t (46)=.97, p=.34, or the neutral no focus and neutral non-arousing focus conditions, t (46)=.26, p=.80.

Was focusing on an arousing portion of an unpleasant image (compared toa non-arousing portion) associated with increased amygdala activation?Contrary to Study 1, in Study 2, focusing on an arousing portion of anunpleasant image compared to a non-arousing portion of an unpleas-ant image resulted in significantly greater activations in the inferior

L insula 13 26 −36 −3 16 5.52 4.01L amygdala 11 −21 −11 −9 4.22 3.86L IPL 40 29 −55 −24 34 3.73 3.47

L postCG 2 −58 −27 39 4.74 4.26L postCG 2 −55 −24 50 3.53 3.30

L IPL 40 15 −36 −39 49 3.60 3.36L FG 37 14 −40 −48 −17 4.14 3.80

Peak activations from random effects analysis are listed with a threshold of pb .025,FDR corrected, and cluster filter of 10 contiguous voxels. BA=Brodmann's area, R=right, L=left, IOG=inferior occipital gyrus, Cblm=cerebellum, IPL=inferior parietallobe, postCG=postcentral gyrus, FG=fusiform gyrus.

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occipital gyrus (BA 17), the insula (BA 13) and the amygdala. Theseactivations are presented in Table 6 and Fig. 3.

Was focusing on a non-arousing portion of anunpleasant image (comparedto an arousing portion) associated with increased frontal and parietalactivity? Consistent with Study 1, in Study 2 focusing on a non-arousingportion of an unpleasant image also resulted in significantly greater acti-vations in parietal regions including the supramarginal gyrus (BA 40), aswell as widespread activation in frontal regions including the middlefrontal gyrus (BA 10) and the superior frontal gyrus (BA 9). These acti-vations are presented in Table 7 and Fig. 4.

In summary, Study 2 replicated Study 1 by demonstrating thatattention to a non-arousing, compared to an arousing, portion of anunpleasant image was again associated with reduced negative affectand increased activations in frontal and parietal regions. However, in

Fig. 3. Regions of the brain more active for unpleasant arousing f

contrast to Study 1, in Study 2 attention to a non-arousing, comparedto an arousing, portion of an unpleasant image was also associatedwith a reduction in amygdala activation.

Discussion

The purpose of this research was to examine the neural and sub-jective response associated with the deployment of visual attentionin the absence of an explicit regulatory goal. Consistent with previousfindings regarding the passive viewing of emotional images (Phan etal., 2002), we found greater activations in frontal and parietal regionsand in the amygdala in response to unpleasant compared to neutralimages in both Study 1 and Study 2. Also consistent with previousfindings in non-emotional attention paradigms, in both studies wefound increases in frontal and parietal regions during blocks in which

ocus compared to unpleasant non-arousing focus in Study 2.

Table 7Peak activations for unpleasant non-arousing focus compared to unpleasant arousingfocus conditions in Study 2 (n=47).

Region BA Cluster size Talairach coordinates T Z

R supramarG 40 2214 56 −50 28 9.78 7.16R STG 39 48 −53 30 9.21 6.90L STG 39 −48 −53 29 6.42 5.40

R MidFG 8 1220 34 25 41 6.74 5.59R SFG 10 19 49 25 5.93 5.08R SFG 10 34 49 19 5.86 5.04

L parahippG 37 78 −25 −45 −9 4.74 4.26L ITG 20 51 −55 −34 −12 4.57 4.12R MidTG 21 13 42 1 −29 4.32 3.93L SFG 10 64 −33 49 25 4.14 3.80

L SFG 10 −25 46 17 3.33 3.13L MidFG 8 136 −33 17 43 4.10 3.76

L MidFG 9 −33 29 34 3.33 3.13L MidFG 6 −44 13 46 3.05 2.89

L Cblm 56 −36 −54 −36 3.80 3.53L Cblm −40 −46 −36 3.18 3.01

Peak activations from random effects analysis are listed with a threshold of pb .025,FDR corrected, and cluster filter of 10 contiguous voxels. BA=Brodmann's area, R=right, L=left, supramarG=supramarginal gyrus, MFG=middle frontal gyrus, SFG=superior frontal gyrus, parahippG=prahippocampal gyrus. ITG=inferior temporalgyrus, MTG=middle temporal gyrus, Cblm=cerebellum.

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attention was directed to specific aspects of images (Hopfinger et al.,2000). As hypothesized, we observed increases in frontal and parietalregions when subjects directed their attention to non-arousing com-pared to arousing portions of unpleasant images. Moreover, in Study2, we observed reductions in amygdala activity for this contrast. Eyetracking results in a sub-sample of participants in Study 1 and in allparticipants in Study 2 confirmed that subjects who underwent eye-tracking generally stayed within the focus region as instructed.

Studies on emotion regulation, particularly cognitive reappraisal,have postulated that the use of cognitive control to carry out emotionregulation strategies may engage the prefrontal cortex. The prefrontalcortex, then, may exert top-down control over the amygdala, whichmodulates sensory processing of emotional information and causescorresponding reductions in subjective affect. Given that unpleasantstimuli have the capacity to automatically capture attention, deployingattention away from such stimuli may also require effortful action.Exercising visual and inhibitory control to deploy attention away fromunpleasant information may then rely on similar prefrontal regionsandmay promote similar decreases in amygdala activity and subjectivenegative affect as cognitive reappraisal.

In both of the current studies we observed widespread increases infrontal, as well as parietal, regions for the unpleasant non-arousingfocus compared to the unpleasant arousing focus condition, despitefocus being a common factor across both conditions. That is, theseregions were more active when participants had to maintain focus ina relatively non-arousing compared to an arousing region of the samepicture. Prefrontal and parietal regions are considered essential forcognitive control during effortful tasks (Matsumoto and Tanaka, 2004),and fronto-parietal networks are known to underlie visuospatial atten-tion and visual control (Corbetta and Shulman, 2002). As even task-irrelevant negative information is capable of capturing attention(Vuilleumier et al., 2001), increased activation in these regions mayreflect additional effort required to direct andmaintain attention withina non-arousing focus region in the presence of unpleasant arousinginformation. Some of the brain regions recruited as participants divertattention away from unpleasant arousing information substantiallyoverlap with regions activated during effortful emotion regulation. Spe-cifically prefrontal regions including BA 6, 8, and 9, which are postulatedto relate to the down-regulation of the amygdala, are common to bothcognitive reappraisal and attentional deployment.

Reduced amygdala activation for the unpleasant non-arousing focuscompared to the unpleasant arousing focus condition was observed in

Study 2, but not Study 1. The design and analysis of Studies 1 and 2were identical with one major exception: eye-tracking data werecollected on all participants in Study 2, but only on a subset of fiveparticipants in Study 1. The divergent findings between these two stud-ies highlight important challenges in imaging research, as well as theadvantages of utilizing eye tracking in conjunction with fMRI. First,researchers rely on participants to stay awake and attend to presentedstimuli. However, collecting eye tracking data allowed us to excludefour participants from Study 2 who were intentionally avoiding thestimuli or who were otherwise closing their eyes for a large portion ofthe study. Despite closing eyes for extended periods of time, theseparticipants still pressed the button to rate their affect following eachblock of images. Without eye tracking, we would have no objectivemeans to remove these subjects fromanalyses. Becauseweonly collectedeye-tracking on 5 out of 41 subjects in Study 1, it is possible that non-compliance from a number of subjects in Study 1 attenuatedmore subtleeffects. Second, it is possible that simply knowing that their eye move-ments were being tracked changed the degree to which subjects com-plied with task instructions. While differences in task compliance as afunction of eye-tracking have not been explicitly examined, there issome evidence that eye-tracking alone can modify behavior to increaseadherence to perceived social norms (Risko and Kingstone, 2010). It ispossible that participants in Study 2 were more likely to consistentlystay within the circle as instructed, particularly the unpleasant non-arousing circle, when they knew their eye movements were being mon-itored. Consequently, we consider the observed amygdala and visualactivation for the unpleasant arousing focus compared to unpleasantnon-arousing focus condition in Study 2 to reflect activations when sub-jects are complying with task instructions. Study 2, therefore, providessupport for the idea that attentional deployment relies upon a similarnetwork of brain regions as cognitive reappraisal; successful regulationvia either strategy appears to involve increases in prefrontal regions asso-ciated with effortful control, as well as corresponding attenuations inamygdala activity. However, the specific relationships between prefron-tal regions and the amygdala, as well as their relationship to subjectiveaffect, may differ between emotion regulation strategies; a study directlycontrasting both strategies would be necessary in order to elucidate thecommon and uniquemechanisms associatedwith each. Finally, it cannotbe ruled out that participants may have been engaging in some form ofautomatic emotion regulation using methods other than attentionaldeployment during the viewing of images, which may have contributedto the resulting activation patterns in either study.

Future studies might also examine individual differences in atten-tional deployment success using eye-tracking; for instance, the use ofattentional deployment as an emotion regulation strategy might varyas a function of time “naturally” spent on negative information. It ispossible that subjectswhoautomatically attend to negative informationwill show quite different activation patterns during focused viewingthan subjects who automatically avoid negative information. Finally,connectivity studies would be useful in determining the ways in whichthese critical brain regions — frontal and parietal networks and theamygdala — interact to influence sensory processing and evaluation ofnegative information in the context of attentional deployment.

In conclusion, these studies suggest that deploying attention to anon-arousing portion of an unpleasant image is associated withreduced subjective negative affect, reduced amygdala activity, andincreased activity in fronto-parietal networks. This suggests that the neu-ral circuitry associated with attentional deployment may significantlyoverlap with effortful emotion regulation strategies such as cognitivereappraisal. Understanding the shared and unique neural mechanismsassociated with this commonly used strategy may be critical to under-standing the processes underlying emotion regulation as well as for un-derstanding deficits in the ability to deploy attention away fromnegativeinformation when necessary.

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.neuroimage.2012.12.030.

Fig. 4. Regions of the brain more active for unpleasant non-arousing focus compared to unpleasant arousing focus in Study 2.

276 J. Ferri et al. / NeuroImage 70 (2013) 268–277

Appendix A

Neutral IAPS images: 7950, 7705, 7700, 7595, 7560, 7550, 7491,7490, 7285, 7233, 7217, 7175, 7150, 7140, 7100, 7090, 7025, 7020,7010, 7004, 7002, 7000, 5875, 5740, 5530, 5390, 5250, 2980, 2880,2745, 2580, 2440, 2393, 2383, 2320, 2270, 2235, 2206, 2190, 2102.

Unpleasant IAPS images: 9810, 9635, 9584, 9571, 9570, 9435,9433, 9430, 9428, 9420, 9410, 9405, 9403, 9400, 9300, 9265, 9253,9252, 9040, 8480, 6831, 6571, 6570, 6560, 6555, 6550, 6415, 6370,6315, 6313, 6312, 6260, 6242, 6190, 6022, 3550, 3530, 3266, 3261,3225, 3220, 3213, 3212, 3211, 3195, 3181, 3063, 3060, 3053, 3030,3017, 3016, 3015, 3010, 3005, 2811, 2800, 2730, 2717, 2703.

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