B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

ava i l ab l e a t www.sc i enced i rec t . com

www.e l sev i e r. com/ l oca te /b ra in res

Research Report

Valence interacts with the early ERP old/new effect and arousalwith the sustained ERP old/new effect for affective pictures

Jan W. Van Strien⁎, Sandra J.E. Langeslag, Nadja J. Strekalova,Liselotte Gootjes, Ingmar H.A. Franken

Erasmus Affective Neuroscience Lab, Institute of Psychology, Erasmus University, Rotterdam, The Netherlands

A R T I C L E I N F O

⁎ Corresponding author. Institute of PsycholoE-mail address: vanstrien@fsw.eur.nl (J.W

0006-8993/$ – see front matter © 2008 Elsevidoi:10.1016/j.brainres.2008.11.027

A B S T R A C T

Article history:Accepted 6 November 2008Available online 18 November 2008

To examine whether valence and arousal influence recognition memory during earlyautomatic or during more sustained processes, event-related brain potentials (ERPs) of 21womenwere recordedwhile theymade old/new judgments in a continuous recognition taskwith pictures from the International Affective Picture System. The pictures were presentedtwice and differed in emotional valence and arousal. The P1 peak and four time windowswere investigated: 200–300 ms, 300–400 ms, 400–600 ms, and 750–1000 ms after stimulusonset. There was a robust old/new effect starting in the 200–300 ms epoch and lasting alltime windows. The valence effect was mainly present in the P1 peak and the 200–400 msepoch, whereas the arousal effect was found in the 300–1000 ms epoch. ExploratorysLORETA analyses dissociated valence-dependent ventromedial prefrontal activity andarousal-dependent occipital activity in the 350–380 ms time window. Valence interactedwith the 200–400 ms old/new effect at central and frontal sites. Arousal interacted with the750–1000 ms old/new effect at posterior sites. It is concluded that valence influences fastrecognition memory, while arousal may influence sustained encoding.

© 2008 Elsevier B.V. All rights reserved.

Keywords:Recognition memoryERP old/new effectValenceArousalAffective picture

1. Introduction

People remember eventswith a high emotional impact usuallybetter than events without such an impact. Emotions influ-encememory at various stages ofmemory processingwith theamygdala allegedly playing an important role in encoding,consolidation, and retrieval of emotional information (LaBarand Cabeza, 2006). Emotions can be parsed according to twoorthogonal dimensions: valence and arousal. Both dimensionsmay enhance memory, but through different neural pro-cesses. Employing functional MRI (fMRI) and behavioralstudies, Kensinger and Corkin (2004) concluded that memoryenhancement for arousing information occurs automatically

gy, Erasmus University Ro. Van Strien).

er B.V. All rights reserved

and is primarily mediated by an amygdalar-hippocampalnetwork, whereas memory enhancement for valenced infor-mation appears to rely on controlled encoding processesmediated by a prefrontal cortex-hippocampal network.

As the Kensinger and Corkin study demonstrated distinctneural encoding processes for valence and arousal, it remainsunclear whether distinct neural retrieval processes exist forthese two dimensions. The utilization of event-related poten-tials (ERPs) offers the opportunity to examine both automaticand controlled memory retrieval processes and, unlike fMRIstudies, allows the precise measurement of the time course ofcortical activation such as the onset of valence or arousal-mediated processes. ERP recognition studies employ either a

tterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands.

.

224 B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

study-test procedure in which a study phase is followed by atest phase where studied items have to be recognized from alist of targets and distracters, or a continuous recognitionparadigm in which ‘new’ (=first presentation) and ‘old’(=second presentation) items are intermixed. With bothparadigms, the correct identification of studied or repeateditems (i.e., as ‘old’ stimuli) is associated with an increasedpositivity of the ERP waveform starting about 300 ms afterstimulus onset. This ERP repetition or old/new effect com-prises an early mid-frontal component (time window 300 to500 ms, often interpreted as an attenuation of the N400, seeRugg, 1995), a later parietal component (time window 500 to800 ms), and a sustained right frontal component. With thestudy-test procedure, the early mid-frontal old/new effect isthought to reflect familiarity (i.e. recognition without retrievalof details), whereas the later parietal old/new effect is thoughtto reflect recollection (i.e. recognition with the retrieval ofassociated details, see Curran et al., 2006; Rugg and Curran,2007). The sustained right frontal component is considered toreflect postretrieval processes (Allan et al., 1998; Ally andBudson, 2007).

With the continuous recognition procedure, the lagbetween the first and second presentation of a word isconsiderably shorter than with the study-test procedure. Inaddition, the continuous recognition procedure involvesalternating encoding and retrieval, whereas the study-testprocedure separates encoding and retrieval. For these reasons,a dual-process explanation in terms of familiarity vs. recollec-tion distinctionmay be less applicable to the earlymid-frontaland later parietal old/new effects in a continuous recognitionparadigm. Using an extended continuous word recognitionparadigm in which each item was repeated nine times, VanStrien et al. (2005) demonstrated that the positivity of the laterparietal component increased linearly with the number ofrepetitions, which suggests that this component reflects agraded recognition process depending on the strength of thememory trace. By contrast, the early old/new effect was notaffected by the number of repetitions. This may indicate that,with continuous recognition, the early old/new effect reflectsan automatic matching process that is not dependent onmemory strength. Interestingly, the early old/new effect inVan Strien et al.'s study was observed at mid-parietal ratherthan mid-frontal electrode positions. In another continuousword recognition study, Van Strien et al. (2007) found that thisearly parietal old/new effect was much larger with immediatethan with delayed repetitions. It is therefore likely that withcontinuous recognition, the early old/new effect reflectsimplicit memory rather than familiarity. This notion is inconcordance with Rugg and colleagues (Rugg et al., 1998; Ruggand Curran, 2007), who also proposed that the early parietalold/new effect is a neural correlate of implicit memoryprocesses.

Various studies investigated the impact of emotion on ERPold/new effects. Employing a continuous recognition proce-dure, Dietrich et al. (2001) found larger late (450–650 ms)parietal old/new effects for negative and positive wordscompared to neutral ones. With a study-test procedure,Inaba et al. (2005) found better recognition and larger lateparietal old/new effects for negative words when compared topositive and neutral words. Likewise, Maratos and Rugg (2001)

found larger parietal old/new effects when words had beenstudied in negative vs. neutral sentences. However, otherstudy-test procedures demonstrated that the late parietal old/new effect was largely unaffected by emotional valence(Windmann and Kutas, 2001) or was smaller for negativecompared to neutral words (Maratos et al., 2000).

Concerning the late onsetting frontal old/new effect,Graham and Cabeza (2001) using faces in a study-testprocedure, found a left lateralized late (750–1250 ms) frontaleffect for happy faces, but a right lateralized frontal effect forneutral faces. In contrast, Johansson et al. (2004) found a latebilateral frontal old/new effect (700–1000 ms), which was notaffected by facial expression.

Old/new effects appear to be modulated by emotion, butless is known about the particular roles of the valence andarousal dimensions. Whereas fMRI studies have sought todisentangle the influence of the arousal and valence dimen-sions, none of the above ERP old/new studies have done so.There is evidence that the time courses of ERP valence andarousal effects differ, with valence effects emerging earlierthan arousal effects. Unpleasant pictures typically producelarger P1 peak amplitudes (around 100 ms after stimulusonset) than pleasant and neutral ones, which may indicatethat unpleasant valence in particular attracts early visualattention (see Olofsson et al., 2008). Gainotti et al. (2008)presented high and low arousal pleasant and unpleasantwords (experiment 1) and pictures (experiment 2) andrecorded the ERP. Their ERP microstate analyses revealedthat valence effects occurred from 118 ms onwards for wordsand from 142 ms onwards for pictures, while arousal effectsoccurred from 266 ms onwards for words and from 302 msonwards for pictures. The authors concluded that in bothexperiments information about valence was processed beforeinformation about arousal.

In the present ERP study, we examined old/new effects inresponse to affective pictures by means of a continuousrecognition task. We used affective pictures rather thanwords, because these pictures will have more arousingcapacity than words (Keil, 2006). We employed an orthogonaldesign to study the influence of emotion on recognition, witharousal and valence as independent factors. In this way, thedifferential contributions of these dimensions to the ERP old/new effect and the time courses of these contributions (early/automatic or late/controlled) can be established. Givenprevious ERP research, we expected larger old/new effects foremotional than for neutral pictures. Given the evidence thatvalence effects emerge earlier than arousal effects (e.g.,Gianotti et al., 2008; Olofsson et al., 2008), we expected thatvalence would influence the early ERP old/new effect, whereasarousal would influence the late ERP old/new effect.

2. Results

2.1. Behavioral data

The overall mean accuracy was 96.3%. The overall meandiscrimination index equaled .954 (sd=.032) and the overallmean response bias equaled .486 (sd=.098). One-way (emo-tion) ANOVAs on the discrimination and bias measures

1 A preliminary analysis of the old/new effect, with the datacollapsed across all five emotion conditions (i.e., including theneutral condition) yielded ANOVA results that were highlycomparable with the results reported in Section 2.3.

Fig. 1 – Grand-average ERPs (n=21) from selected electrodes for ‘new’ pictures (black lines) vs ‘old’ pictures (gray lines) andspherical-spline interpolated scalp distributions of the old/new effect (‘old’ minus ‘new’ pictures).

225B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

yielded no significant effects. A two-way (old/new×emotion)ANOVA on the latency data showed significant main effectsfor old/new, F(1,20)=32.01, pb .001, with latencies to repeti-tions (M=747 ms) being shorter than to first presentations(M=799 ms), and emotion, F(4,80)=17.41, ɛ=.808, pb .001.Compared to neutral pictures (M=753 ms), mean latencieswere longer for high arousal pleasant (M=782 ms, pb .001),high arousal unpleasant (M=796 ms, pb .001), and low arousalunpleasant pictures (M=772 ms, p=.003), but not for lowarousal pleasant (M=762 ms, p=.113). A three-way (old/new×valence×arousal) ANOVA revealed additional maineffects of valence and arousal. Pleasant pictures (M=772 ms)evoked shorter latencies than unpleasant pictures(M=784 ms), F(1,20)=10.20, p=.005, and low arousing pictures(M=767 ms) evoked shorter latencies than high arousingpictures (M=789 ms), F(1,20)=34.80, pb .001.

2.2. Event-related potentials

The ERP analyses were conducted in two parts. First, toexamine the topography and temporal dynamics of the ERPold/new, valence, and arousal effects, we computed regionalaverages (three electrodes per average, see Experimentalprocedures) for each time window in a three-by-three grid(left anterior, midline anterior, right anterior, left central,midline central, right central, left posterior, midline posterior,and right posterior). We tested the main old/new, valence and

arousal effects and their interactions with topography (caud-ality, laterality) by means of separate ANOVAs for each timewindow. To examine the effect of valence and arousal on theearly visual processing, we also analyzed the P1 amplitude atOz. The results of these ANOVAs are given in Section 2.3 forthe old/new effects and in Section 2.4 for the emotion effects.

Second, to further explore the modulation of the old/neweffect by arousal and valence, we computed three largerregional averages (seven electrodes per average) along themidline axis (anterior, central, posterior) and tested theinteractions of old/new, valence, arousal, and caudality (seeSection 2.5). The choice of the three midline clusters wasbased on the topography of the interaction effects: theemotional modulation of the old/new effect was present atwidespread medial regions.

2.3. Old/new effects1

Fig. 1 shows the grand-average ERPs at selected electrodes for‘new’ vs. ‘old’ pictures and the topographic voltage maps ofthe main old/new effects for all four time windows. The ERP

Table 1 – ANOVA main and interaction effects of Old/new for each time window

df 200–300 ms 300–400 ms 400–600 ms 750–1000 ms

F ɛ p F ɛ p F ɛ p F ɛ p

Old/new 1,20 19.55 1.000 b .001 36.55 1.000 b .001 32.77 1.000 b .001 .56 1.000 ns.Old/new×caudality 2,40 4.95 .579 .032 16.74 .574 b .001 3.88 .617 .052 4.54 .564 .040Old/new×laterality 2,40 12.00 .967 b .001 19.95 .853 b .001 15.25 .983 b .001 3.10 .993 .057Old/new×caudality×laterality 2,40 8.08 .711 b .001 4.44 .688 .009 9.73 .740 b .001 15.52 .713 b .001

226 B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

was more positive going for ‘old’ than for ‘new’ pictures from200 ms onward. The ANOVAs yielded significant interactionsof old/new, caudality and laterality for the 200–300, 300–400,and 400–600 ms time windows in addition to main old/neweffects and the lower order interactions (see Table 1). Thesethree-way interactions reflect the topographic distributions ofthe old/new effects. From Fig. 1, it can be seen that that theold/new effect was largest in the 300–600 ms time window,with the early (300–400 ms) old/new effects having a fronto-central maximum and the late (400–600 ms) old/new effecthaving a widespread distribution with a rightward centralmaximum. The 200–300 ms old/new effect showed a topo-graphic distribution that is comparable to the 300–400 mseffect, but with the exclusion of the most frontal electrodes.For the 750–1000ms time window, there was also a significantthree-way interaction of old/new, caudality and laterality, inaddition to the interaction of old/new and caudality. Thetopographic voltage map indicates that the 750–1000 ms old/new effect was restricted to right anterior sites.

2.4. Emotion effects

2.4.1. Valence effectsWe first tested the P1 amplitude at Oz. There was a robustvalence effect for the P1 peak. Pleasant pictures resulted insignificantly higher P1 amplitudes than unpleasant pictures(see Fig. 2), F(1,20)=9.32, p=.006.

Regarding the later components, Fig. 3 shows the grand-average ERPs at selected electrodes for pleasant and unplea-

Fig. 2 – The P1 peak at Oz for unpleasant (black lines) vs.pleasant (gray lines) pictures.

sant pictures and the topographic voltage maps of the mainvalence effects for all time windows. For the 200–300 and 300–400 time windows, we found a significant main effect ofvalence. In both time windows, the three-way interaction ofold/new, caudality and laterality was significant in addition tothe lower order interactions (see upper part of Table 2). Thevalence effects were most prominent at right anterior sites(see Fig. 3), with pleasant pictures resulting in more positiveamplitudes in comparison to unpleasant pictures. For the 400–600 ms time window, the three-way interaction was alsosignificant but only in addition to the interaction of valenceand caudality. The topographic voltage map indicates that the400–600 ms valence effect was confined to the right anteriorregion. For the 750–1000 ms time window, a significantinteraction of valence and caudality was found. Inspection ofthe data revealed that the 750–1000 ms valence effect wasinverted (unpleasant pictures resulted in more positive goingamplitudes than pleasant pictures) at posterior sites.

2.4.2. Arousal effectsArousal did not modulate the P1 peak (Fb .30). Fig. 4 shows thegrand-average ERPs at selected electrodes for high and lowarousal pictures and the topographic voltagemaps of themainarousal effects for all time windows. For the 200–300 ms timewindow, no significant main arousal effect or interactions ofarousal with caudality and laterality were found (see middlepart of Table 2). For the 300–400 ms time window, theinteraction of arousal and caudality was significant in addi-tion to a main arousal effect. The topographic voltage mapsshow that high arousing pictures resulted in more positiveamplitudes relative to low arousing pictures, and that thisarousal effect was largest at posterior sites. For the 400–600mstime window the ANOVA yielded a significant interaction ofarousal and laterality, in addition to a significantmain arousaleffect. The 400–600 ms arousal effect had a widespreaddistribution with a midline maximum. For the 750–1000 mstime window, the interaction of arousal, caudality, andlaterality was significant, in addition to a significant interac-tion of arousal and laterality, and a main arousal effect. The750–1000 ms arousal effect had a widespread and leftwarddistribution across the central region.

2.4.3. Interaction of valence and arousalFor the P1 peak at Oz, no interaction of valence and arousalwas found (Fb .55). For the 200–300ms timewindow, there wasa significant four-way interaction of valence, arousal, caud-ality, and laterality in addition to a significant two-wayinteraction of valence and arousal, and a significant three-way interaction of valence, arousal, and laterality (see lower

Fig. 3 – Grand-average ERPs (n=21) from selected electrodes for unpleasant pictures (black lines) vs. pleasant pictures(gray lines) and spherical-spline interpolated scalp distributions of the valence effect (pleasant minus unpleasant pictures).

227B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

part of Table 2). Separate valence×arousal ANOVAs on eachcluster revealed significant interactions of valence andarousal at the right anterior cluster (p=.009), the midlinecentral cluster (p=.026) and the right central cluster (p=.020).At these clusters, the valence effect (i.e. more positive-goingwaveforms for pleasant pictures) was larger for low than forhigh arousing pictures. For the 300–400 ms time window, thethree-way interaction of valence, arousal, and laterality wassignificant, in addition to a significant interaction of valence

Table 2 – ANOVA main and interaction effects of valence and a

df 200–300 ms

F ɛ p

Valence 1,20 11.89 1.000 .003Valence×caudality 2,40 4.49 .571 .041Valence×laterality 2,40 4.90 .735 .023Valence×caudality×laterality 2,40 8.62 .780 b .001

Arousal 1,20 .51 1.000 ns.Arousal×caudality 2,40 .94 .733 ns.Arousal×laterality 2,40 1.78 .869 ns.Arousal×caudality×laterality 2,40 1.81 .793 ns.

Valence×arousal 1,20 4.46 1.000 .048Valence×arousal×caudality 2,40 .50 .649 ns.Valence×arousal×laterality 2,40 3.38 .999 .044Valence×arousal×caudality×laterality 2,40 3.24 .777 .026

and arousal. Separate valence×arousal ANOVAs on left,midline, and right clusters revealed significant interactionsof valence and arousal across midline (p= .040) and left(p=.010) clusters. At these clusters, the valence effect againwas larger for low than for high arousing pictures. For the 400–600ms time-window, the valence effect tended to be larger forlow compared to high arousing pictures across all clusters,while for the 750–1000 ms time window, no interaction ofvalence and arousal was found.

rousal for each time window

300–400 ms 400–600 ms 750–1000 ms

F ɛ p F ɛ p F ɛ p

9.53 1.000 .006 2.06 1.000 ns. .02 1.000 ns.4.78 .587 .034 7.75 .662 .006 6.85 .620 .0115.50 .757 .015 1.58 .807 ns. .16 .894 ns.7.12 .738 b .001 9.17 .792 b .001 .45 .658 ns.

10.20 1.000 .005 5.95 1.000 .024 6.65 1.000 .0187.91 .666 .005 .36 .628 ns. .67 .658 ns.3.22 .966 .053 16.23 .905 b .001 6.60 .876 .0051.09 .591 ns. 2.21 .649 ns. 7.25 .775 b .001

4.66 1.000 .043 4.40 1.000 .049 .18 1.000 ns..90 .621 ns. .51 .560 ns. .31 .590 ns.

4.33 .877 .025 1.64 .878 ns. 1.39 .822 ns.1.74 .758 ns. 2.68 .685 ns. 1.20 .505 ns.

Fig. 4 – Grand-average ERPs (n=21) from selected electrodes for low arousal pictures (black lines) vs high arousal pictures(gray lines) and spherical-spline interpolated scalp distributions of the arousal effect (high minus low arousal pictures).

Fig. 5 – Spherical-spline interpolated scalp distributions of the old/new effect (‘old’ minus ‘new’) for unpleasant and pleasantpictures in the 200–300 ms and 300–400 ms time window and the corresponding mean old/new effects at anterior, centraland posterior regions.

228 B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

Fig. 7 – The old/new effect in the 750–1000 ms time windowat Pz for low arousal pictures (solid black line = ‘new’, dottedblack line = ‘old’) and high arousal pictures (solid gray line =‘new’, dotted gray line = ‘old’). The arrow indicates thesustained positivity for new high arousal pictures.

229B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

2.5. Effects of valence and arousal on old/new

2.5.1. Interaction of old/new and valenceFor the 200–300 ms time window, there was a significantinteraction of old/new, valence, and caudality, F(2,40)=4.60,ɛ= .678, p= .031. For the 300–400 ms time window, thisinteraction was also significant, F(2, 40)=4.19, ɛ=.660, p=.041.Fig. 5 displays the topographic distribution of the 200–300 msand 300–400 ms old/new effect for pleasant and unpleasantpictures. The early old/new effect was more robust and morefrontal for unpleasant compared to pleasant pictures. Post hoccontrasts revealed that in the 200–300 ms time window, thefrontal regions, when compared to central regions, showedsmaller old/new effects for pleasant pictures (p=.042). Forunpleasant pictures, the frontal and central regions showedcomparable old/new effects. In the 300–400 ms time window,post hoc contrasts yielded no significant differences betweenthe frontal and central old/new effects. Fig. 6 illustrates theold/new effect at Fz for pleasant and unpleasant pictures. Theold/new effect was larger for unpleasant than for pleasantpictures and this was due to a larger valence effect for newcompared to old pictures.

For the 400–600 ms and 750–1000 ms time windows, nosignificant interactions of old/new, valence, and caudalitywere found.

2.5.2. Interaction of old/new and arousalFor the 200–300 ms, 300–400 ms, and 400–600 ms timewindows, no significant interactions of old/new and arousalor old/new, arousal, and caudality were found. For the 750–1000 ms time window, the interaction of arousal and old/newwas significant, F(1,20)=5.95, p=.024, with low arousal picturesresulting in a regular old/new effect (new: M=1.26 μV; old:M=1.91 μV) and high arousal pictures resulting in an inverseold/new effect (new: M=2.84 μV; old: M=2.32 μV). Althoughthe interaction of old/new, arousal and caudality was notsignificant (p=.111), single electrode analyses revealed aspecific cluster of posterior electrodes with significant old/new×arousal interactions at P3, Pz, P4, PO3, PO4, O1, Oz, O2(all p'sb .006). Further, a separate ANOVA for the posterior

Fig. 6 – The old/new effects in the 200–300 ms and 300–400 ms time windows at Fz for unpleasant pictures (solidblack line = ‘new’, dotted black line = ‘old’) and pleasantpictures (solid gray line = ‘new’, dotted gray line = ‘old’).

cluster yielded a robust interaction of old/new and arousal,F(1,20)=19.02, pb .001, with low arousal pictures resulting ina small old/new effect (new: M=− .47 μV; old: M=− .13 μV)and high arousal pictures resulting in an clear inverse old/new effect (new: M=1.22 μV; old: M=− .25 μV). Fig. 7 illus-trates the inverse old/new effect at Pz. The first presenta-tion of high arousal pictures resulted in a large positiveamplitude for the 750–1000 ms time window, while thesecond presentation of high arousal pictures was lesspositive going. The first presentation of low arousal picturesresulted in a relatively small positive amplitude, while thesecond presentation of low arousal pictures wasmore positivegoing.

2.5.3. Interaction of old/new, valence, and arousalFor none of the four time windows, the interaction of old/new,valence, and arousal, or of old/new, valence, arousal, andcaudality was statistically significant (all Fsb .35).

2.6. Exploratory sLORETA analyses

In the 300–400 ms time window, the topographic scalpdistributions displayed a more anterior effect of valence anda more posterior effect of arousal. Because there is convergingevidence that valence and arousal are processed by distinctneural systems, with valence-specific activations occurring inthe prefrontal cortex and arousal-dependent responses occur-ring in the amygdala and probably in the cortical sensory areas(e.g., Bradley et al., 2003; Vuilleumier and Driver, 2007), weexplored the possible cortical sources of the ERP valence andarousal effects in the 350–380 ms time window by means ofexploratory sLORETA analysis (Pascual-Marqui, 2002). ThesLORETA analyses were conducted on the grand-averagedERP difference waves (average reference) of pleasant minusunpleasant pictures and of high minus low arousal pictures.The sLORETA solution for the ERP valence effect yieldedmaximum current density at the vicinity of the ventromedialprefrontal cortex (see upper part of (Fig. 8). The sLORETA

Fig. 8 – sLORETA solution for the grand-averaged ERP difference wave of the valence effect (pleasant minus unpleasant, upperpart) and arousal effect (high minus low, lower part) in the 350–380 ms time window.

230 B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

solution for the ERP arousal effect yielded maximum currentdensity at the visual areas (see lower part of Fig. 8).2

3. Discussion

3.1. Behavioral data

Latencies to ‘old’ pictures were shorter than latencies to ‘new’pictures. This outcome is consistent with behavioral data ofother old/new studies employing pictures (e.g., Guo et al.,2007; Schloerscheidt and Rugg, 1997), but opposite to beha-vioral data of old/new studies employing words (e.g., Fried-man, 1990; Van Strien et al., 2005). Van Strien et al. (2007)found that in a relatively easy task condition with highaccuracy (massed repetitions), RTs were faster for ‘old’ thanfor ‘new’ words. In a more difficult task condition with loweraccuracy (spaced repetitions), RTs were slower for ‘old’ thanfor ‘new’ words. In the present study, accuracy was high,suggesting that the continuous picture recognition was a

2 For the 350–380 ms valence effect, dipole source modelingusing BESA 5.1 (MEGIS Software, Germany) with two symmetric(bilateral) dipoles in the prefrontal region and a single dipole inthe right posterior cingulate cortex yielded a residual variance of4.29%. For the 350–380 ms arousal effect, a dipole source modelwith two single dipoles in the medial extrastriate visual cortex(cuneus, Brodman area 18) yielded a residual variance of 5.88%.

rather easy task (i.e., required little retrieval effort) thatresulted in fast recognition of ‘old’ items.

Latencies were longer to emotional pictures than to neutralpictures, with responses to unpleasant pictures being slowerthan to pleasant pictures, and responses to high arousal

Fig. 9 – Scatterplot of the normative female valence andarousal ratings (range 1–9) of the selected stimuli from theInternational Affective Picture System.

231B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

pictures being slower that to low arousal pictures. Evidently,the affective content interfered with old/new decisions.Affective content did not influence recognition accuracy,probably because the recognition task was easy to perform.Affective content did not influence response bias either, whichis discordant with old/new studies that reported a recognitionbias for negative emotional stimuli. Withwords, amore liberalresponse bias to negative than to neutral words has beenreported (Maratos et al., 2000;WindmannandKutas, 2001), andwith faces a more liberal response bias to negative than topositive expressions (Johansson et al., 2004). Such a tendencytomakemore ‘old’ responses to negative vs. neutral or positivestimulimay serve an adaptive function (WindmannandKutas,2001) related to processing potential threat. The absence ofsuch a response bias in the present research may be aconsequence of the type of emotional stimuli that was used.Negative words may show more semantic overlap andnegative facial expressionsmore feature overlap thannegativepictures andhencewords and facesmay result in a recognitionbias for negative emotions, whereas pictures may not.

3.2. Event-related potentials

3.2.1. ERP old/new effectsOld/new effects emerged from 200 ms after stimulus onsetonwards, with an early fronto-central effect, a later parietaleffect and a sustained right frontal effect. This sequence is inagreement with other ERP old/new studies (e.g., Allan et al.,1998). The fronto-central topography of the early old/neweffect may indicate that early recognition was less implicitthan in the Van Strien et al. (2005; 2007) studies, whichemployed words and found an early parietal old/new effect(cf., Rugg et al., 1998). The 400–600 ms parietal effect had awidespread centroparietal distribution that wasmaximal overright central regions. This rightward distribution may be aconsequence of the use of pictorial stimuli, as with words, leftlate parietal old/new effects have been reported (e.g., Maratoset al., 2000; Wilding and Rugg, 1996). There is evidence thatboth the hippocampus and the parietal cortex are involved inthe parietal old/new effect (Curran et al., 2006) and that the leftand right hippocampi are differentially involved in verbal andnonverbal memory (Golby et al., 2001). Asymmetric parietalold/new effects might thus reflect the lateralization ofmaterial-specific recollection processes, although differencesin task demands between study-test procedures and contin-uous recognition tasks could affect the extent of thesehemispheric asymmetries (Rugg et al., 1997).

3.2.2. ERP valence effectsP1 amplitude at Oz was larger in response to pleasant stimulithan in response to unpleasant stimuli. The P1 reflects earlyvisual processing and is sensitive to physical stimuluscharacteristics and attentional manipulations. Most studieson affective picture processing have found that unpleasantpictures evoke larger P1 amplitudes than pleasant or neutralpictures (see for review, Olofsson et al., 2008), which mayindicate that unpleasant stimuli catch more attention. Thismay serve an adaptive function (to look where the danger is,e.g., Crawford and Cacioppo, 2002) but it can be argued thatunder certain circumstances, pleasant or rewarding stimuli

also have adaptive value. Consistent, with our finding, arecent ERP studywith unfiltered and spatial-frequency filteredaffective pictures found larger occipital P1 amplitudes forunfiltered pleasant pictures than for unfiltered neutralpictures (Alorda et al., 2007). Yet, it remains possible that ourpleasant pictures differed from our unpleasant pictures inphysical characteristics such brightness or visual complexity,thus evoking the P1 valence effect.

Robust valence effects were found in the 200–300 ms and300–400ms timewindows at right anterior sites, with pleasantpictures eliciting a larger positive-going deflection thanunpleasant pictures. This outcome is consistent with otherERP studies that examined valence effects. Cuthbert et al.(2000) also foundmore positive ERP wave forms in response topleasant compared to unpleasant IAPS pictures, but in a longertime window (300–700 ms). This longer lasting valence effectmay have been a consequence of the much longer exposuretimes of the emotional stimuli (6 s) in their study as comparedto our study (500 ms). Delplanque et al. (2006) found similarvalence effects but only in a later time window (439–630 ms—P3b). In their study, pictures were presented for 750ms and theparticipants had to give valence ratings during the presenta-tions, which possibly modulated the P3b.

Cuthbert et al. (2000) explained their valence effect as aconsequence of autonomic arousal. Although in their studypleasant and unpleasant picture were rated equal in arousal,pleasant pictures did evoke greater skin conductanceresponses. In the current study, we had no independentphysiological measures of arousal, such as skin conductance,to confirm the orthogonality of valence and arousal, but wefound clear temporal and topographic dissociations betweenvalence and arousal effects (see Figs. 3 and 4). The arousaleffect was absent in the 200–300 ms time window, and waslocated posteriorly in the 300–400ms time window. Therefore,our valence effects cannot be explained as a result ofdifferences in the arousal qualities of the pleasant andunpleasant stimuli. When matched for arousal, functionalimaging data reveal no differences in amygdala activation forpleasant and unpleasant pictures (Garavan et al., 2001).Neuropsychological theories of emotion assume a differentialcortical processing of pleasant and unpleasant stimuli, inparticular in the prefrontal cortex (Borod et al., 2001). Withpleasant and unpleasant words, Herrington et al. (2005) foundmore dorsolateral prefrontal fMRI activity for pleasant than forunpleasant words, in particular on the left side. With pictures,Dolcos et al. (2004) found a similar valence-dependent hemi-sphere-specific activation in the dorsolateral prefrontal cortexand an additional selective activation of ventromedial pre-frontal cortex in response to pleasant pictures. Further,Sabatinelli et al. (2007) demonstrated that pleasant picturesgave rise to activations in the nucleus accumbens and themedial prefrontal cortex, whereas equally arousing unplea-sant pictures did not. These structures, which are part of thehuman brain reward system, thus appeared to be sensitive tovalence in particular, and not to arousal. The present ERPvalence effect may reflect these intrinsic valence differencesin prefrontal emotional processing. The exploratory sLORETAanalysis on the valence effect supports this notion, with themaximum current density of this effect being localized in theventromedial prefrontal cortex.

232 B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

3.2.3. ERP arousal effectsUnlike valence, arousal did not affect the P1 and 200–300 mstime window. There is converging evidence that the early ERPvalence effects (b300 ms) reflect selective attention processes,whereas ERP arousal effects (N300 ms) reflects later motiva-tional (encoding) processes (Olofsson et al., 2008). For the latertime windows (300–1000 ms), arousal effects were robust andlong lasting, with midline maxima spreading from a moreposterior location in the 300–400 ms time window to a morecentral location in the later time windows. Such a positive-going wave for arousing visual stimuli has been reportedfrequently (e.g., Cuthbert et al., 2000; Schupp et al., 2004b) andhas been interpreted as reflecting sustained motivated atten-tion (Schupp et al., 2004a). The 300–400 ms ERP arousal effectmay reflect increased posterior activity as a result fromprojections from the amygdala to the visual cortex (Bradleyet al., 2003). The exploratory sLORETA analysis that weemployed in the present study suggests that in the 350–380 ms time window the ERP arousal effect is mainly localizedin the visual cortex. Increased activity in the visual cortexmaylead to better memory encoding for arousing pictures.

3.2.4. ERP valence×arousal effectsAlthough there was no main arousal or arousal by topographyeffect in the 200–300 ms time window, arousal interacted withthe early (200–300 ms) valence effect, which was larger for lowarousing than for high arousing pictures at right anterior,midline central, and right central clusters. Arousal alsointeracted with the 300–400 ms valence effect at midline andright clusters. These interactions may reflect the co-activity ofdissociable neural systems for arousal and valence, but theexact nature of ERP valence and arousal interactions awaitsfurther assessment as ERP studies with an orthogonalvalence×arousal design are scarce (Gianotti et al., 2008; seealso, Olofsson et al., 2008).

3.2.5. Interaction of the ERP old/new effect with valenceand arousalValence interacted with the early old/new effect. Unpleasantpictures elicited amore pronounced andmore frontal early old/new effect than did pleasant pictures. Inspection of thewaveforms revealed that the larger old/new effect for unplea-sant pictures was primarily due to a larger valence effect fornew than for old pictures. It is doubtful whether the reducedvalence effect for old pictures is a consequence of rapidhabituation. Previous research demonstrated that arousalhabituates rapidly but that valence effects remain relativelyintact acrossmultiple picture repetitions (Codispoti et al., 2006).

Valence did not interact with the 400–600 ms parietal oldnew effect or the 750–1000 ms late frontal old/new effect. Thelack of an interaction of old/new and valence for the 400–600 ms time window is at variance with old/new studies thatemployed words or faces. With words, several studies havereported modulation of the parietal old/new effect by valence(Dietrich et al., 2001; Inaba et al., 2005; Maratos and Rugg,2001), although the absence of emotional modulation has alsobeen reported (Windmann and Kutas, 2001). With faces,Johansson et al. (2004) found that negative facial expressionsmodulated the parietal old/new effect, but not the late frontalold/new effect. For the late frontal old/new effect, Graham and

Cabeza (Graham and Cabeza, 2001) found a left lateralizedeffect for happy faces compared to a right lateralized effect forneutral faces. In the present study however, the valence effectin response to emotional pictures disappeared for the mostpart before the onset of the parietal old/new effect around400 ms, and this may explain the lack old/new effects laterthan 400 ms.

Arousal interacted with the 750–1000 ms old/new effect atposterior sites, with high arousal pictures resulting in a robustinverse old/new effect. The large positivities in the posteriorregion for new high arousal pictures may indicate sustainedvisual processing of arousing stimuli. Because this timewindow reflects both post retrieval processes (i.e. after the‘new’ vs. ‘old’ decision) and motivated attention, it can behypothesized that motivated attention results in bettersustained encoding and hence better recollection. The beha-vioral data of the present continuous recognition task did notdemonstrate any memory enhancing effects of arousal, but ina further continuous recognition study with a surprise freerecall task at the end, we found better delayed recall foremotional (high arousing) compared to neutral (low arousing)IAPS pictures (Langeslag and Van Strien, 2008).

3.2.6. GeneralizabilityIn the present study only females participated, for reasonsexplained below (see Section 4.1). There is evidence that menrespond with greater arousal to positive pictures, whilewomen respond with greater arousal to negative pictures(e.g., Lang et al., 1998). Because IAPS provides separatenormative valence and arousal ratings for men and women,such gender differences could be attenuated by using theappropriate norms when selecting pictures for a specificgender group. Nevertheless, it remains to be investigatedwhether men will show the same influences of valence andarousal on the old/new effect.

3.2.7. ConclusionsWithin the 200–400 ms time window, we demonstrated ERPvalence effects, which most probably reflect differences inprefrontal activation, and we found an interaction of valenceand the early ERP old/new effect at central and frontal sites.The arousal effect emerged around 300 ms after stimulusonset and interacted with the 750–1000 ms old/new effect atposterior sites. Exploratory sLORETA analyses dissociatedvalence-dependent ventromedial prefrontal activity and arou-sal-dependent occipital activity in the 350–380 ms timewindow. Kensinger and Corkin (2004) have proposed thatmemory enhancement for valenced information relies onencoding processes that are mediated by a prefrontal-cortex-hippocampal network, while memory enhancement forarousing information relies on processes mediated by anamygdalar-hippocampal network. Kensinger and Corkin con-sider the fronto-hippocampal network as subserving con-trolled encoding. The early old/new effect is usually thought toreflect more fast and automatic recognition (retrieval) pro-cesses. Interestingly, there is evidence that the early old/neweffect also originates from prefrontal regions (Rugg andCurran, 2007). The valence-dependent early old/new effectsmay thus be a corollary of the interaction of frontal processes.The arousal-dependent inverse old/new effect during the 750–

233B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

1000 ms time window reflects sustained processing of newhigh arousal pictures. As valence information is processedfaster than arousal information (Gianotti et al., 2008; Olofssonet al., 2008), valence primarily interacts with fast recognitionprocesses, whereas arousal most probably interacts withsustained encoding.

4. Experimental procedures

4.1. Participants

The participants were 21 healthy female students, 18 of whomwere right-handed by self-report. They had a mean age of23.7 years (range 20–30 years), had normal or corrected-to-normal vision, and participated in the experiment either asvolunteers or for course credits. In this study, we selectedwomen, because they tend to exhibit greater emotionalreactivity than men (Gross and Levenson, 1995; Hagemannet al., 1999; Van Strien and Van Beek, 2000).

4.2. Stimuli

One-hundred-sixty pictures were chosen from the Interna-tional Affective Picture System (IAPS, Lang et al., 2005). Theywere divided into five sets of 32 pictures each, selectedaccording to the normative IAPS ratings for female subjects:pleasant high arousal pictures, pleasant low arousal pictures,unpleasant high arousal pictures, unpleasant low arousalpictures, and neutral low arousal pictures. The pictures wereselected such that the distances between the emotionalsubsets in affective space were maximum. As more extremepleasant and unpleasant valence levels are typically asso-ciated with high arousal (Olofsson et al., 2008), the number ofpleasant and in particular unpleasant low arousal pictures israther limited. To optimally match the pleasant and unplea-sant stimuli on the arousal dimension, 30 of the 32 pictures ineach condition were used for further data analyses. Fig. 9shows the distribution of each emotional picture set in thetwo-dimensional valence and arousal space. For clarity,neutral pictures (mean valence=5.09; mean arousal=3.13)have been omitted from the scatterplot (see Olofsson et al.,2008, for a scatterplot of the complete IAPS picture set). In thepresent picture set, the mean arousal level of the unpleasantpictures was comparable with the mean arousal level ofpleasant pictures (4.79 vs. 5.19, p=.11). High and low arousalpictures had comparable valence levels (4.77 vs 5.40, p=.15).

4.3. Procedure

Stimuli were presented on a 17-inch high resolution PCmonitor. Neutral and emotional pictures were presented ineight consecutive blocks of 40 trials (20 ‘new’, 20 ‘old’), withneutral and emotional conditions being balanced acrossblocks. Within each block, a picture was presented twice inpseudo-random order with the number of intervening trialsbetween the first and second presentation of a given pictureranging from 2 to 36.

The sequence for each trial was: (1) the presentation of afixation cross in the center of the computer screen with a

variable duration of 400 to 600 ms, (2) the 500 ms presentationof the IAPS picture, and (3) the 1000 ms presentation of thefixation cross. The interval between the end of one trial andthe beginning of the next trail lasted 1500 ms. Each trial waseither a new picture, or a repeated picture.

Participants were seated in a sound attenuated, and dimly-lit chamber at a distance of approximately 80 cm in front of thescreen. They were told that pictures would be repeatedlypresented and that, for each presentation they had to indicatewhether the picture was new or ‘old’ (previously presented) bypressing response buttons with the left or right index fingers,respectively. To minimize eye movements, which may lead toERP-artifacts, the participants were instructed to avoid eyeblinks during stimulus presentations (fixation cross andwords). Preceding the experimental run, the participantsreceived a series of 20 practice trials (10 ‘new’ and 10 ‘old’pictures) with pictures that were not used in the experimentalseries.

4.4. EEG recording

EEG activity was recorded with a BioSemi Active-Two systemfrom 32 pin type active Ag/AgCl electrodes mounted in anelastic cap. The electrodes were positioned at Fz, Cz, Pz, Oz,FP1/2, AF3/4, F3/4, F7/8, FC1/2, FC5/6, C3/4, T7/8, CP1/2, CP5/6,P3/4, P7/8, PO3/4, and O1/2. Active electrodes were alsoattached to the left and right mastoids. Electro-oculogram(EOG) activity was recorded from active electrodes placedabove and beneath the left eye, and from electrodes at theouter canthus of each eye. An additional active electrode (CMS— common mode sense) and a passive electrode (DRL —driven right leg) were used to comprise a feedback loop foramplifier reference. The EEG and EOG signals were digitizedwith a 512 Hz sampling rate and 24-bit A/D conversion.Response latencies were recorded online along with the EEGdata.

4.5. Data analysis

4.5.1. Behavioral data analysisFor each participant and each emotion condition, accuracyand mean latency were determined. Accuracy was indexed bythe discrimination measure Pr (Snodgrass and Corwin, 1988).Pr is the measure of discrimination for a two-high-thresholdmodel of recognition memory and is used quite often inrecognition memory studies. Pr equals the probability of a hit(correct “old” decision in case of a repeated stimulus) minusthe probability of a false alarm (incorrect “old” decisions incase of a new stimulus). If Pr=0, overall accuracy is at chancelevel, while if Pr=1.0, overall accuracy is perfect. In addition toPr, the corresponding bias measure Br (Br=probability of afalse alarm/(1−Pr); scores range from 0 to 1) was calculated(corrected rates, Snodgrass & Corwin, 1988). Br scores above.50 indicate a liberal response strategy, that is, a tendencytoward “old” decisions. Latencies were computed over correcttrials.

4.5.2. EEG data analysisOffline, the EEG signals were referenced to themathematicallylinkedmastoids and phase-shift-free filtered with a band passof 0.15 to 30 Hz (24 db/oct). Correction for horizontal and

234 B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

vertical eye movements was done employing the Gratton andColes algorithm (Gratton et al., 1983). ERP epochswith an 1100-ms durationwere extracted, beginning 100ms before stimulusonset. The ERP signals were defined relative to the mean ofthis 100 ms prestimulus baseline period. Average ERPs werecomputed for each participant and each of the following tentask conditions: first vs. second presentation of neutral, higharousal pleasant, low arousal pleasant, high arousal unplea-sant, and low arousal pictures. Epochs with incorrectresponses and epochs with a baseline-to-peak amplitudedifference larger than 75 μV on any channel were omittedfrom averaging. The mean number of valid epochs percondition ranged from 24.7 to 26.3, with a mean acrossconditions of 25.7 epochs.

After inspection of the grand-average ERP waveforms andscalp distribution, four timewindowswere selected for furtheranalyses: the windows between 200 and 300 ms and between300 and 400 ms after stimulus onset comprised the earlyfrontal old/new effect, the window between 400 and 600 mscomprised the parietal old/new effect, and the windowbetween 750 and 1000 ms comprised the right frontal old/new effect. The partition of the early old/new effect into two100 ms windows was based on visual inspection of the ERPwaveforms, which suggested that the arousal effect onlyemerged after 300 ms post stimulus (cf., Olofsson et al., 2008).The 750–1000 ms time window was chosen, because the ERold/new effect appeared to be inversed after 750 ms at certainelectrodes and conditions.

Nine regional averages were computed for each timewindow and each condition: left anterior (F3, F7, FC5), midlineanterior (AF3, Fz, AF4), right anterior (F4, F8, FC6), left central(C3, T7, CP5), midline central (FC1, Cz, FC2), right central(C4,T8, CP6), left posterior (P3, P7, PO3), midline posterior (CP1, Pz,CP2), and right posterior(P4, P8, PO4). In addition, three largermidline clusters were computed: anterior (Fp1, Fp2, AF3, AF4,F3, Fz, F4), central (FC1, FC2, C3, Cz, C4, CP1, CP2), and posterior(P3,Pz, P4, PO3, PO4, O1, O2).

To examine the effect of valence and arousal on the earlyERP components, we also measured the P1 amplitude at Oz.Inspection of the ERP data revealed that the largest P1 valenceeffect was found at this electrode site. The P1 peak wasdefined as the maximum positive value at Oz within the 60–120 ms time window.

4.5.3. Statistical analysisThe accuracy data were analyzed with a one-way analysis ofvariance (ANOVA) with emotion (high arousal pleasant, lowarousal pleasant, high arousal unpleasant, low arousalunpleasant, neutral) as the factor within subjects. Latencydata were analyzed by means of a two-way (2×5) repeated-measures ANOVA, with old/new and emotion (high arousalpleasant, low arousal pleasant, high arousal unpleasant, lowarousal unpleasant, neutral) as factors. In addition, theorthogonal effects of valence and arousal were analyzed bymeans of additional ANOVAs with valence (pleasant, unplea-sant) and arousal (high, low) as factors replacing the factoremotion.

To test the orthogonal effects of valence and arousal, theERP data were submitted to repeated measures ANOVAs withcaudality (anterior, central, posterior), laterality (left, right, if

applicable), old/new (new, old), valence (pleasant, unpleasant)and arousal (high, low) as factors. If appropriate, F-ratios weretestedwith Greenhouse–Geisser corrected degrees of freedom.

R E F E R E N C E S

Allan, K., Wilding, E.L., Rugg, M.D., 1998. Electrophysiologicalevidence for dissociable processes contributing to recollection.Acta Psychol. 98, 231–252.

Ally, B.A., Budson, A.E., 2007. The worth of pictures: using highdensity event-related potentials to understand the memorialpower of pictures and the dynamics of recognition memory.NeuroImage 35, 378–395.

Alorda, C., Serrano-Pedraza, I., Campos-Bueno, J.J.,Sierra-Vázquez, V., Montoya, P., 2007. Low spatial frequencyfiltering modulates early brain processing of affective complexpictures. Neuropsychologia 45, 3223–3233.

Borod, J.C., Zgaljardic, D., Tabert, M.H., Koff, E., 2001. Asymmetriesof emotional perception and expression in normal adults. In:Gainotti, G. (Ed.), Handbook of Neuropsychology, Volume 5:Emotional Behavior and its Disorders. Elsevier,Amsterdam, pp. 181–205.

Bradley, M.M., Sabatinelli, D., Lang, P.J., Fitzsimmons, J.R., King,W.,Desai, P., 2003. Activation of the visual cortex in motivatedattention. Behav. Neurosci. 117, 369–380.

Codispoti, M., Ferrari, V., Bradley, M.M., 2006. Repetitive pictureprocessing: autonomic and cortical correlates. Brain Res. 1068,213–220.

Crawford, L.E., Cacioppo, J.T., 2002. Learning where to look fordanger: integrating affective and spatial information. Psychol.Sci. 13, 449–453.

Curran, T., Tepe, K.L., Piatt, C., 2006. ERP explorations of dualprocesses in recognition memory. In: Zimmer, H.D.,Mecklinger, A., Lindenberger, U. (Eds.), Handbook of Bindingand Memory: Perspectives from Cognitive Neuroscience, Vol..Oxford University Press, Oxford, pp. 467–492.

Cuthbert, B.N., Schupp, H.T., Bradley, M.M., Birbaumer, N., Lang,P.J., 2000. Brain potentials in affective picture processing:covariation with autonomic arousal and affective report.Biol. Psychol. 52, 95–111.

Delplanque, S., Silvert, L., Hot, P., Rigoulot, S., Sequeira, H., 2006.Arousal and valence effects on event-related P3a and P3bduring emotional categorization. Int. J. Psychophysiol. 60,315–322.

Dietrich, D.E., Waller, C., Johannes, S., Wieringa, B.M., Emrich,H.M., Munte, T.F., 2001. Differential effects of emotionalcontent on event-related potentials in word recognitionmemory. Neuropsychobiology 43, 96–101.

Dolcos, F., LaBar, K.S., Cabeza, R., 2004. Dissociable effects ofarousal and valence on prefrontal activity indexing emotionalevaluation and subsequent memory: an event-related fMRIstudy. NeuroImage 23, 64–74.

Friedman, D., 1990. Erps during continuous recognition memoryfor words. Biol. Psychol. 30, 61–87.

Garavan, H., Pendergrass, J.C., Ross, T.J., Stein, E.A., Risinger, R.C.,2001. Amygdala response to both positively and negativelyvalenced stimuli. Neuroreport 12, 779–2783.

Gianotti, L., Faber, P., Schuler, M., Pascual-Marqui, R., Kochi, K.,Lehmann, D., 2008. First valence, then arousal: the temporaldynamics of brain electric activity evoked by emotionalstimuli. Brain Topogr. 20, 143–156.

Golby, A.J., Poldrack, R.A., Brewer, J.B., Spencer, D., Desmond, J.E.,Aron, A.P., Gabrieli, J.D.E., 2001. Material-specific lateralizationin the medial temporal lobe and prefrontal cortex duringmemory encoding. Brain 124, 1841–1854.

Graham, R., Cabeza, R., 2001. Event-related potentials ofrecognizing happy and neutral faces. Neuroreport 12, 245–248.

235B R A I N R E S E A R C H 1 2 5 1 ( 2 0 0 9 ) 2 2 3 – 2 3 5

Gratton, G., Coles, M.G., Donchin, E., 1983. A new method foroff-line removal of ocular artifact. Electroencephalogr. Clin.Neurophysiol. 55, 468–484.

Gross, J.J., Levenson, R.W., 1995. Emotion elicitation using films.Cogn. Emot. 9, 87–108.

Guo, C., Lawson, A.L., Jiang, Y., 2007. Distinct neural mechan-isms for repetition effects of visual objects. Neurosci. 149,747–759.

Hagemann, D., Naumann, E., Maier, S., Becker, G., Lürken, A.,Bartussek, D., 1999. The assessment of affective reactivityusing films: validity, reliability and sex differences. Pers.Individ. Difrer. 26, 627–639.

Herrington, J.D., Mohanty, A., Koven, N.S., Fisher, J.E., Stewart, J.L., Banich, M.T., Webb, A.G., Miller, G.A., Heller, W., 2005.Emotion-modulated performance and activity in leftdorsolateral prefrontal cortex. Emotion 5, 200–207.

Inaba, M., Nomura, M., Ohira, H., 2005. Neural evidence of effectsof emotional valence on word recognition.Int. J. Psychophysiol. 57, 165–173.

Johansson, M., Mecklinger, A., Treese, A.C., 2004. Recognitionmemory for emotional and neutral faces: an event-relatedpotential study. J. Cogn. Neurosci. 16, 1840–1853.

Keil, A., 2006. Macroscopic brain dynamics during verbal andpictorial processing of affective stimuli. In: Anders, S.,Ende, G., Junghöfer, M., Kissler, J., Wildgruber, D. (Eds.),Progress in Brain Research: Understanding Emotions, Vol.156. Elsevier Science, Boston, pp. 217–232.

Kensinger, E.A., Corkin, S., 2004. Two routes to emotional memory:distinct neural processes for valence and arousal. PNAS 101,3310–3315.

LaBar, K.S., Cabeza, R., 2006. Cognitive neuroscience of emotionalmemory. Nat. Rev. Neurosci. 7, 54–64.

Lang, P.J., Bradley, M.M., Cuthbert, B.N., 1998. Emotion, motivation,and anxiety: brain mechanisms and psychophysiology. Biol.Psychiatry 44, 1248–1263.

Lang, P.J., Bradley, M.M., Cuthbert, B.N., 2005. Internationalaffective picture sysytem (IAPS): Digitized photographs,instruction manual and affective ratings. Technical report A-6,University of Florida, Gainsville, FL.

Langeslag, S.J.E., Van Strien, J.W., 2008. Age differences in theemotional modulation of ERP old/new effects.Int. J. Psychophysiol. 70, 105–114.

Maratos, E.J., Allan, K., Rugg, M.D., 2000. Recognition memory foremotionally negative and neutral words: an ERP study.Neuropsychologia 38, 1452–1465.

Maratos, E.J., Rugg, M.D., 2001. Electrophysiological correlates ofthe retrieval of emotional and non-emotional context.J. Cognit. Neurosci. 13, 877–891.

Olofsson, J.K., Nordin, S., Sequeira, H., Polich, J., 2008. Affectivepicture processing: an integrative review of ERP findings. Biol.Psychol. 77, 247–265.

Pascual-Marqui, R.D., 2002. Standardized low-resolution brainelectromagnetic tomography (sLORETA): technical details.Methods Find. Exp. Clin. Pharmacol. 24, 5–12.

Rugg, M.D., 1995. ERP studies of memory. In: Rugg, M.D., Coles,M.H.G. (Eds.), Electrophysiology of Mind: Event-Related BrainPotentials and Cognition. Oxford University Press, pp. 133–170.

Rugg, M.D., Curran, T., 2007. Event-related potentials and recog-nition memory. Trends Cogn. Sci. 11, 251–257.

Rugg, M.D., Mark, R.E., Gilchrist, J., Roberts, R.C., 1997. ERPrepetition effects in indirect and direct tasks: effects of age andinteritem lag. Psychophysiology 34, 572–586.

Rugg, M.D., Mark, R.E., Walla, P., Schloerscheidt, A.M., Birch, C.S.,Allan, K., 1998. Dissociation of the neural correlates of implicitand explicit memory. Nature 392, 595–598.

Sabatinelli, D., Bradley, M.M., Lang, P.J., Costa, V.D., Versace, F.,2007. Pleasure rather than salience activates human nucleusaccumbens and medial prefrontal cortex. J. Neurophysiol. 98,1374–1379.

Schloerscheidt, A.M., Rugg, M.D., 1997. Recognition memory forwords and pictures: an event-related potential study. Neu-roreport 8, 3281–3284.

Schupp, H.T., Cuthbert, B.N., Bradley, M.M., Hillman, C.H., Hamm,A.O., Lang, P.J., 2004a. Brain processes in emotional perception:motivated attention. Cogn. Emot. 18, 593–611.

Schupp, H.T., Junghofer, M., Weike, A.I., Hamm, A.O., 2004b. Theselective processing of briefly presented affective pictures: anERP analysis. Psychophysiology 41, 441–449.

Snodgrass, J.G., Corwin, J., 1988. Pragmatics of measuring recog-nition memory: applications to dementia and amnesia. J. Exp.Psychol.Gen. 117, 34–50.

Van Strien, J.W., Van Beek, S., 2000. Ratings of emotion in laterallypresented faces: sex and handedness effects. Brain Cogn. 44,645–652.

Van Strien, J.W., Hagenbeek, R.E., Stam, C.J., Rombouts, S.,Barkhof, F., 2005. Changes in brain electrical activity duringextended continuous word recognition. Neuroimage 26, 952–959.

Van Strien, J.W., Verkoeijen, P.P.J.L., Van der Meer, N., Franken, I.H.A., 2007. Electrophysiological correlates of word repetitionspacing: ERP and induced band power old/new effects withmassed and spaced repetitions. Int. J. Psychophysiol. 66,205–214.

Vuilleumier, P., Driver, J., 2007. Modulation of visual processing byattention and emotion: windows on causal interactionsbetween human brain regions. Philos. Trans. R. Soc. Lond., BBiol. Sci. 362, 837–855.

Wilding, E.L., Rugg, M.D., 1996. Event-related potentials and therecognition memory exclusion task. Neuropsychologia 35,119–128.

Windmann, S., Kutas, M., 2001. Electrophysiological correlates ofemotion-induced recognition bias. J. Cogn. Neurosci. 13,577–592.