Behavioral and Electrophysiological Evidence of aRight Hemisphere Bias for the Influence of Negative

Emotion on Higher Cognition

Emiliana R. Simon-Thomas, Kemi O. Role, and Robert T. Knight

Abstract

& We examined how responses to aversive pictures affectedperformance and stimulus-locked event-related potentials(ERPs) recorded during a demanding cognitive task. Nu-meric Stroop stimuli were brief ly presented to either left orright visual hemifield (LVF and RVF, respectively) after acentrally presented aversive or neutral picture from the In-ternational Affective Picture System. Subjects indicatedwhether a quantity value from each Stroop stimulus matchedthe preceding Stroop stimulus while passively viewing thepictures. After aversive pictures, responses were more accu-

rate for LVF Stroops and less accurate for RVF Stroops.Early-latency extrastriate attention-dependent visual ERPswere enhanced for LVF Stroops. The N2 ERP was enhancedfor LVF Stroops over the right frontal and parietal scalp sites.Slow potentials (300–800 msec) recorded over the frontaland parietal regions showed enhanced picture related modu-lation and amplitude for LVF Stroops. These results suggestthat emotional responses to aversive pictures selectively fa-cilitated right hemisphere processing during higher cognitivetask performance. &

INTRODUCTION

Do negative emotional and higher executive processescontribute competitively or synergistically to humancognition? Plato’s ‘‘competitive’’ view posits that nega-tive emotions degrade the capacity for higher cognitivefunctioning; we cannot reason when we are impas-sioned. Alternatively, negative emotions may provideessential guidance for certain cognitive processes con-juring a more synergistic view. The former competitiveview is supported by the concept of interference, whichproposes that negative emotions disrupt ongoing cog-nition by consuming attention and diverting processingresources away from cognitive functioning. Neuroimag-ing data have shown an inverse relationship betweenbrain regions involved in negative emotion and thoseengaged during higher cognitive functioning, furthersupporting the competitive view (Northoff et al., 2004;Drevets & Raichle, 1998; Heller & Nitschke, 1997). Thesynergistic view, on the other hand, is supported bystudies showing that negative emotions facilitate highercognition. Here, negative emotions are considered cuesfor cognition, permitting effective responding to salientinformation (Gray, Braver, & Raichle, 2002; Perlstein,Elbert, & Stenger, 2002; Sato, Kochiyama, Yoshikawa, &Matsumura, 2001; Ito, Larsen, Smith, & Cacioppo, 1998;Stormark, Nordby, & Hugdahl, 1995). For example,

performance on a spatial working memory task showsimprovement with concurrent negative emotion induc-tion (Gray, 2001). In sum, there is no unified theory forhow the limbic and cortical structures involved in neg-ative emotional experience interact with the corticalcircuits involved in higher cognition.

The orientation of attention, a primary component ofcognition, is dependent on both cognitive and emotion-al influences. Electrophysiological techniques have de-lineated how attention, the ‘‘spotlighting’’ of neuralprocessing resources, shapes perceptual and cognitiveprocessing during many different cognitive tasks (Luck,Woodman, & Vogel, 2000; Mangun & Hillyard, 1995;Posner & Petersen, 1990). Early event-related potential(ERP) responses to visual stimuli measured over extras-triate cortex show reliable increases with attention cue-ing and with task-related rules for attention orientationand allocation (Awh, Anllo-Vento, & Hillyard, 2000; Luck,Woodman, et al., 2000; Heinze, Luck, Mangun, & Hill-yard, 1990; Luck, Heinze, Mangun, & Hillyard, 1990).Subsequent electrophysiological activity associated withstimulus evaluation, working memory, decision-making,and response preparation also show modulation withattention allocation (Monfort & Pouthas, 2003; Vogel &Luck, 2000; Garcia-Larrea & Cezanne-Bert, 1998; Gevins,Smith, McEvoy, & Yu, 1997; Picton, 1992; Rugg, Milner,Lines, & Phalp, 1987). Emotional states, emotion judg-ments, and emotional significance of stimuli also influ-ence attention-sensitive ERPs (Smith, Cacioppo, Larsen,University of California

D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 17:3, pp. 518–529

& Chartrand, 2003; Bernat, Bunce, & Shevrin, 2001; Keilet al., 2001; Sato et al., 2001; Kayser, Bruder, Tenke,Stewart, & Quitkin, 2000; Schupp et al., 2000; Pizzagalli,Regard, & Lehmann, 1999; Diedrich, Naumann, Maier,Becker, & Bartussek, 1997). The key question then ishow and where are ongoing emotional and cognitiveprocesses monitored, weighted, and integrated to me-diate the allocation of attention and processing re-sources toward optimal behavior?

Reports of interaction between elicited emotions andattention or cognition suggest that negative emotionaffects cognition differently in the two cerebral hemi-spheres (Hartikainen, Ogawa, & Knight, 2000; Stormark,Hugdahl, & Posner, 1999; Van Strien & Luipen, 1999;Stormark, Nordby, et al., 1995; Van Strien & Heijt, 1995;Van Strien & Morpurgo, 1992). Hartikainen et al. (2000)found that presentation of a brief aversive picture priorto a simple target event delayed detection responsetimes (RTs) for the LVF (right hemisphere) targets. Theyproposed that the emotional stimuli preferentially en-gaged the right hemisphere, interfering with subse-quent target detection. In contrast, Van Strien andMorpurgo (1992) reported improved performance forright hemisphere targets that followed aversive emo-tional stimuli, which they interpreted as emotionalpriming of the right hemisphere that facilitated ensuingcognitive processing. Although both implicate the righthemisphere in negative emotional processing, severalfactors may account for the apparent contradiction be-tween their behavioral findings. First, the intensity of theemotion elicited by the emotion-eliciting stimuli wasqualitatively different. Hartikainen et al. used disturbingpictures whereas Van Strien and Lupien used negativeemotion words. Second, the length of time between theemotion eliciting stimulus and the cognitive stimulus wasdifferent, affecting both the intensity of the emotionalresponse and the stage of the cognitive process engagedduring the task (Codispoti, Bradley, & Lang, 2001). Forinstance, emotions may influence early perceptual pro-cesses differently from later evaluative, decision, andmemory-related processes (Dolan, 2002). Third, theremay have been a difference in hemispheric dominancefor the cognitive processes engaged during the tasks. VanStrien and Lupien’s use of emotionally laden words mayhave confounded the hemispheric influence of the neg-ative emotion. However, the observation that the righthemisphere is more influenced by negative emotion evo-cation and concurrent cognitive processing is consistentwith the valence hypothesis positing that the righthemisphere is more involved with emotion processing(Derryberry, 1990).

Further studies of emotion laterality have modifiedthe valence hypothesis, suggesting that the right hemi-sphere is dominant for processing withdrawal-related(e.g., fear, aversion) emotions and that the left hemi-sphere may play a greater role in approach-relatedemotion (e.g., joy) (Adolphs, Jansari, & Tranel, 2001;

Davidson, Ekman, Saron, Senulis, & Friesen, 1990; Da-vidson, Mednick, Moss, Saron, & Schaffer, 1987). Bothversions of the valence hypothesis, the ‘‘right hemi-sphere emotion’’ and the ‘‘left hemisphere approachversus right hemisphere withdrawal emotion’’ are sup-ported if the evidence is divided into studies that requireidentification of emotion expression versus studies thatinvolve experienced emotions, respectively (Van Strien& Van Beek, 2000; Ley & Strauss, 1986).

Here, we examined performance and electrophysio-logical activity during a higher cognitive task that pro-moted lateralized visual processing while presentingtask-irrelevant, negative emotion eliciting pictures. Aver-sive pictures were presented for approximately 1 sec toinitiate an emotional response immediately precedingvisual presentation of cognitive task stimuli. The taskinvolved a numeric Stroop with a one-back workingmemory load to engage higher cognitive processes in-cluding cognitive control, response inhibition, andworking memory. Stroops were presented to unilateralvisual hemifields (left and right visual hemifields, orLVF and RVF, respectively) to directly investigate hemi-spheric specificity for the influence of bilaterally initi-ated negative emotional processes on higher cognitivetask related processing. Task performance and Stroopstimulus-locked ERPs provided millisecond resolutionmeasurements of the influence that negative emotionalexperience can have on electrophysiological indices ofattention and cognitive processing.

RESULTS

Subjective Ratings

There was a main effect of time on positive PANAS(Positive and Negative Affect Scale) scores, F(4,48) =9.8, p < .001; they decreased throughout the experi-ment. Planned comparison between the baseline andpost-task PANAS scores showed that the initial drop wassignificant across subjects ( p < .01). Negative PANASscores also showed a main effect of time, F(4,48) = 9.8,p < .001. Planned comparison showed that the nega-tive affect score increased significantly after starting thetask ( p < .005). Subsequent negative affect scores de-creased throughout the experiment.

Performance

Response Times

There were no main effects of visual field (VF), picturevalence (PV), or interaction effects on RTs.

Accuracy

There were no main effects of VF or PV on accuracy.However, there was a VF � PV interaction, F(1,12) =

Simon-Thomas, Role, and Knight 519

8.05, p < .05. Responses to LVF Stroops that followedaversive pictures were more accurate than responsesto LVF Stroops that followed neutral pictures (4.28 ±0.44 vs. 3.44 ± 0.35, p < .05) or to responses toRVF Stroops that followed aversive pictures (4.28 ±0.44 vs. 3.38 ± 0.41, p < .05). Responses to RVFStroops were more accurate after neutral than afteraversive pictures (4.0 ± 0.41 vs. 3.38 ± 0.41), althoughthis difference did not reach significance ( p = .2)(Figure 1).

Electrophysiology

Stroop Stimulus-Locked ERPs: Early Components

The amplitude of early visual components (P1/N1)measured from electrodes over contralateral extrastri-ate cortex (LVF: PO8, RVF: PO7) showed no maineffects of VF or PV or significant interactions. However,an alternate measure of extrastriate attention mod-ulation indexed by a root mean square calculationacross a 50- to 200-msec window (representative ofthe magnitude of the P1 and N1 component com-plex) showed a main effect of VF. P1/N1 magnitudewas greater for LVF Stroops over right extrastriateelectrodes than for RVF Stroops over left extrastriateelectrodes, F(1,12) = 8.1, p < .05. Planned t test com-parisons showed that this VF effect was significantfor both aversive and neutral picture trials ( p < .05

for both) with enhanced right extrastriate activity forall stimuli. Post callosal transfer, the N1 measured onelectrodes over ipsilateral extrastriate cortex (LVF: PO7,RVF: PO8) across a 180- to 220-msec window showeda VF � PV interaction, F(1,12) = 5.53, p < .05. Callosal-dependent N1 amplitude was selectively diminishedfor RVF (left hemisphere) Stroops that followed aver-sive pictures. Planned comparisons revealed no sig-nificant differences between group means (Figure 2Aand B).

The N2 component, measured at right frontal elec-trodes (FP2, AFz, AF4, and AF8) between 150 and250 msec, showed a main effect of VF, F(1,11) = 7.7,p < .05 (one subject was excluded from this analysisdue to excessive artifact on the measured electrodes).Frontal N2 amplitude increased for LVF Stroops.Planned follow-up t test comparisons showed that thisVF effect was significant in the aversive picture condi-tion ( p < .001) and not in the neutral picture condition( p = .13). Measured from right parietal electrodes(PO4 and P6) over the same time window, the N2component was selectively increased for LVF Stroopsthat followed aversive pictures evidenced by a VF � PVinteraction, F(1,12) = 5.36, p < .05. Planned t test com-parisons showed that the parietal N2 increase for LVFstimuli was also only significant in the aversive picturecondition ( p < .05 vs. p = .66 for neutral condition)(Figure 3).

Stroop Stimulus-Locked ERPs: Slow Potentials

Sustained slow potential (SP) shifts (300–800 msec)showed condition-related differences over right frontaland bilateral parietal regions. Focused measures ofSP amplitude shifts from right frontal (Afz, AF4: 450–800 msec) and left and right parietal–occipital electrodes(left: CP3, P3, PO3; right: CP4, P4, PO4, 300–800 msec)were analyzed to probe the effects of negative emotionand hemisphere on SPs. Over right frontal electrodes,a negative-going SP showed a PV � VF interaction,F(1,11) = 7.0, p < .05; SP amplitude was greater forLVF Stroops during aversive picture trials. Planned t testcomparisons showed a trend for increased SP amplitudefor LVF Stroops after aversive versus neutral pictures( p < .07) and no differences between aversive versusneutral picture-preceded RVF Stroops ( p = .5). Over left-parietal cortex, a positive-going SP showed main effectsof VF and PV. Left-parietal SP amplitude was greaterfor LVF Stroops than for RVF Stroops, F(1,12) = 14.71< .005. Planned t test comparisons showed that thisdifference was significant for LVF versus RVF aversiveand LVF versus RVF neutral picture trials ( p < .05 forboth). Left parietal SP amplitude also showed decreasedamplitude for aversive picture trials, F(1,12) = 6.01,p < .05. Planned t test comparisons showed that thiseffect was significant for LVF Stroops (aversive < neu-

Figure 1. Mean task performance accuracy (d0) showed a VF � PV

interaction: Accuracy increased for LVF aversive Stroops and decreased

for RVF aversive Stroops ( p < .05 for all comparisons).

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Figure 2. (A) LVF Stroop-locked ERP waveforms for aversive (bold line) and neutral (thin line) picture trials. (B) RVF Stroop-locked ERPwaveforms for aversive (bold line) and neutral (thin line) picture trials. P1/N1 is enhanced for LVF Stroops ( p < .05). Postcallosal N1

amplitude for RVF Stroops following aversive pictures (bold line) is selectively decreased over right extrastriate cortex (PO8) ( p < .05).

Simon-Thomas, Role, and Knight 521

tral: p < .05) and not for RVF Stroops ( p = .1). Overthe right parietal cortex, a positive-going SP showed amain effect of PV, F(1,12) = 5.55, p < .05, and a VF � PVinteraction, F(1,12) = 5.38, p < .05. Like the left parietal

SP, right parietal SP amplitude was decreased duringaversive versus neutral picture trials. Planned t testcomparisons showed that this decrease was primarilydue to a difference in amplitude between aversive and

Figure 2. (continued)

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neutral picture trials for LVF Stroops ( p < .01, p = .3 forRVF) (Figure 4).

DISCUSSION

Behavior

Changes in PANAS subjective ratings suggest that thepictures from the International Affective Picture System(IAPS) elicited negative emotional feelings in subjects(Lang, 1999). After two blocks of the task, subjects iden-tified significantly more with negative terms and lesswith positive terms, indicating that they felt worse afterstarting the task. With further repetitions of the task,negative and positive self-ratings both decreased gradu-ally throughout the experiment. PANAS scores indicatethat the pictures elicited stronger emotional responsesduring the first blocks of the experiment, which mighthave revealed more intense emotion–cognition interac-tions. We present data from the entire experiment sincethere were insufficient numbers of events in individualtask blocks to compute reliable ERPs necessary toexamine condition-related differences in ERP compo-nents. The overall pattern in PANAS ratings, a sharpincrease in negative ratings and decrease in positiveratings followed by smaller shifts toward less negativeand less positive ratings, may be explained by several

Figure 3. Scalp topographic

maps of the difference in

amplitude between aversive

and neutral preceded Stroopspresented to the LVF and RVF

depict the increased right

frontal and parietal N2 for LVF

Stroops that follow aversivepictures ( p < .001 and

p < .05 respectively).

Figure 4. Scalp topographic maps of frontal and parietal slow waves.

For LVF Stroops frontal SP amplitude increased and parietal SP

amplitude decreased bilaterally during aversive picture trials ( p < .05).Over the left parietal cortex, SP amplitude was decreased for RVF

Stroops relative to LVF Stroops ( p < .05).

Simon-Thomas, Role, and Knight 523

factors. After the initial distress subjects’ emotionalresponses may have habituated with repetition of thepictures (Phan, Liberzon, Welsh, Britton, & Taylor,2003), or subjects’ may have regulated their subjectiveexperience in response to the task-irrelevant pictures.

The aversive pictures used in this study were in-tended to elicit negative emotional feelings whilethe neutral pictures served as control visual stimuli.The possibility that emotional processing related tothe negative pictures was tonic, diffusing into neutralpicture trials, is present for our task and potentiallyblurred observable differences between negative andneutral picture trials. For this reason, positive emotioneliciting pictures were excluded from this study, despitethe inherent value that a positive emotion conditionwould have provided to our understanding of emotion–cognition interaction. Intermixing a positive-emotioneliciting condition with the negative and neutral con-ditions would have diluted the rapid event-related emo-tion induction process and worsened the overlapbetween emotion eliciting conditions.

PV- and VF (hemisphere)-related changes in perform-ance accuracy suggest that subjects’ negative emotionalresponses facilitated cognitive task processing in theright hemisphere, and may have reduced task process-ing in the left hemisphere. This pattern of emotion–cognition interaction is consistent with two existingtheories related to emotional and cognitive processingin the brain. The valence hypothesis (Davidson & Irwin,1999), which affords a greater role to the right hemi-sphere in the processing underlying withdrawal-relatedemotional experience and the limited-resource, hemi-sphere-specific model of cognitive processing (Posner &Petersen, 1990; Friedman, Polson, Dafoe, & Gaskill,1982; Hellige, Cox, & Litvac, 1979) support these find-ings. The aversive pictures presented across hemi-spheres may have initiated emotional processes thatprioritized the allocation of attention and processingresources toward the right hemisphere.

Our interpretation is parsimonious with both the‘‘competitive’’ and the ‘‘synergistic’’ view of emotion–cognition interaction. For the right hemisphere, thenegative emotion facilitated concurrent cognitive per-formance. For the left, it interfered. Revisiting the data ofHartikainen et al., who found right hemisphere impair-ment with negative emotion, opposite to the currentstudy, differences in task structure must be considered.In Hartikainen et al.’s tasks, pictures were flashed for150 msec, one-sixteenth the presentation time usedhere (950 msec). These different sensory experiencesmay have led to a different scale or quality of emotionelicitation and related processing. In a study evalu-ating emotional responses to varying IAPS picture pre-sentation times, Codispoti et al. (2001) suggest thatshorter picture presentations may lead to less defensiveemotion-related activation that sustained presentations.Difference in the time interval between the picture onset

and the cognitive stimulus onset, 500 msec versus1000 msec, may have also changed the interactionbetween these two processes. For example, Stormark,Field, Hugdahl, and Horowitz (1997) found that shorterintervals between emotion cues and stimuli causedinterference while longer intervals produced facilitation.Finally, Hartikainen et al.’s cognitive task used elemen-tary shape targets and involved a simple detectionprocess, while the stimuli in this study required com-plex evaluation and comparison to previous stimuli inworking memory. These differences in cognitive de-mand may also affect the interaction between elicitedemotions and cognition. Taken together, the evidencesuggests that the right hemisphere is preferentiallyengaged by negative emotional stimuli but that thenature of the behavioral manifestation depends on themethod of emotion induction, the temporal parameters,and the cognitive load of the concurrent task.

Another factor to consider is sex. Rodway, Wright, andHardie (2003) recently reported comparable valence-specific hemispheric effects in women subjects (n =42) but not men (n = 36), although all subjects ex-hibited a bias toward interpreting nonvalenced stimuliin the LVF as negative and in the RVF as positive. In ourstudy, there were too few subjects to reliably assess sexdifferences.

Finally, the cognitive task used in this study wasdesigned to avoid preferentially engaging left or righthemisphere-based functions, such as language produc-tion or global/local perception (Evert & Kmen, 2003).There is evidence, however, that the right hemi-sphere is more involved in attention mediation andarousal-related functions than the left (Evert, McGlinchey-Berroth, Verfaellie, & Milberg, 2003). The right hemi-sphere accuracy advantage observed in this experimentwas uniquely present for aversive picture trials ren-dering it unlikely that the task itself afforded a gross righthemisphere advantage. However, we cannot disentanglethe potential effects of arousal intrinsic to negative emo-tion from the effect of the negative emotion itself.

Electrophysiology

Stimulus-locked ERP components showed PV, VF, andhemisphere related modulation that conveyed a patternof unique hemispheric inf luences of negative emo-tional processing on cognition. First, early attention-dependent visual sensory processing of Stroop stimuliwas enhanced in the right hemisphere. Task stimuliwere perceptually identical for LVF and RVF presenta-tions, suggesting that the hemispheric difference in earlyextrastriate activity was related to the emotion manipu-lation. The elicited negative emotion may have causedtonic enhancement of attention toward right hemi-sphere structures as an attentional cue would in acued target detection task (Mangun & Hillyard, 1995).

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Visual extrastriate activity (N1) showed diminished am-plitude for RVF stimuli that followed aversive pictures.N1 amplitude is thought to index prefrontal and pari-etal modulation of early sensory processing (Barcelo,Suwazono, & Knight, 2000), typically evidenced by in-creases with attention allocation. For example, improvedstimulus discrimination after attention cueing corre-lates with increased N1 amplitude (Vogel & Luck,2000). The unilateral N1 attenuation observed heresuggests that information about the RVF Stroops wasnot well transferred from the left to the right hemi-sphere. This valence-related diminishment of signalpassing from the left to the right may be related to thedecreased accuracy observed in this condition.

The right frontal N2, which was increased for LVFStroops that followed aversive pictures, is associatedwith response inhibition and conflict monitoring. Thesefunctions are often attributed to an association cortex–anterior cingulate network (Nieuwenhuis, Yeung, vanden Wildenberg, & Ridderinkhof, 2003; Bokura, Yama-guchi, & Kobayashi, 2001). The Stroop element to thetask used in this study invoked conflict-monitoringprocesses. The right frontal–parietal N2 enhancementfor aversive-picture-preceded LVF Stroops suggests thatthe right hemisphere’s response to the demands of thecognitive task was enhanced when stimuli followedaversive pictures.

Frontal and parietal SPs (450–800 and 300–800 msec,respectively) also showed valence related amplitudechanges for Stroop stimuli presented to the LVF andRVF. Frontal and parietal slow-wave shifts like thoseobserved in the current study have been shown to re-f lect increased frontal–parietal network engagementwith increased task-related effort or working-memorydemand (Monfort & Pouthas, 2003; Pelosi, Slade, Blum-hardt, & Sharma, 2000; Rama et al., 1997). Decreasedamplitude of the parietal P300 (300–600 msec), a com-ponent that falls within the range of the SP, has alsobeen related to subjective ratings of increased difficulty,increased working memory load, and increased recruit-ment of frontal lobe structures to carry out task pro-cesses during working memory intervals (McEvoy,Smith, & Gevins, 1998). Paradoxically, increased parietalP300 amplitude is also related to prefrontally mediatedincreased allocation of attention and processing re-sources toward stimuli that present increased salience,such as novel, irregular/unexpected, or motivationallysignificant stimuli (Soltani & Knight, 2000).

Several modulatory factors may explain the SPchanges observed in this study since the experimentaltask both engaged working memory functions and, byassociation with affective pictures, manipulated stimulussalience. Frontally, SP amplitude was selectively in-creased over the right hemisphere for LVF Stroops thatfollowed aversive pictures. This suggests that the aver-sive picture cues enhanced right frontal involvement inmaintenance and feature comparison of stimuli pre-

sented to the right hemisphere, which may underliethe improved accuracy for LVF Stroops that followedaversive pictures. Over the parietal cortex, there wereunique PV- and VF-related changes in SP amplitude overright versus left hemisphere scalp regions. Over the leftparietal cortex, SP amplitude was reduced for RVFStroops relative to LVF Stroops. This VF-related differ-ence was not observed in the right parietal SP. Theunilateral SP amplitude reduction for RVF Stroops sug-gests that fewer processing resources were being allo-cated toward higher order processing of RVF Stroopsin the left hemisphere, which parallels our early extra-striate findings. This may reflect a generalized increasedsalience attributed to all LVF stimuli as a consequence ofthe right hemisphere’s functional facilitation by thenegative emotion elicitation. Over both left and rightparietal electrodes, SP amplitude was decreased forStroops that followed aversive versus neutral pictures,mainly if they had been presented to the LVF. Thispattern suggests that carrying out higher order process-ing of Stroops in the wake of the emotional response toaversive pictures constituted increased task demand,therefore, increasing frontal engagement in the frontal–parietal network involved in carrying out the workingmemory element of the task. Further, since the righthemisphere was more affected by the emotion in-duction, this SP shift was more pronounced for LVFStroops. Overall, the SP modulation observed here sug-gests that the right hemisphere was more involved inprocessing task stimuli and more discriminating of thedifferential demands induced by the negative versusneutral emotion conditions.

Conclusions

Emotional responses to aversive pictures differentiallyaffected cognitive processing in the right and left cere-bral hemispheres. Performance accuracy was improvedfor task trials that involved negative emotion elicitationand stimulus presentation to the right hemisphere.Neurophysiological indices of visual feature analysis,working memory, and decision-related processing wereall enhanced in the right hemisphere. For the lefthemisphere, accuracy was reduced after aversive pic-tures and ERP components showed signs of diminishedleft-to-right callosal transfer of visual information.Frontal SPs were enhanced for stimuli presented tothe right hemisphere and showed enhanced sensitivityto concurrent emotion manipulation. These findings arein accord with Gray’s (2001) result that verbal workingmemory, putatively involving left hemisphere structureswas impaired by negative emotional processing, whileright hemisphere mediated spatial working memory wasfacilitated. In sum, the results provide behavioral andelectrophysiological evidence of a link between negativeemotional processing and the right hemisphere.

Simon-Thomas, Role, and Knight 525

METHODS

Subjects

Thirteen healthy volunteers (8 women, mean age = 21years) from the University of California-Berkeley com-munity completed this study. Subjects were prescreenedfor right-handedness, lack of past or present psychiatricor neurological disorder or injury, and lack of currentprescription or nonprescription drug use. The use ofhuman subjects was approved by the Committee for theProtection of Human Subjects at University of California-Berkeley, and informed consent was obtained prior toparticipation. Subjects earned course credit and/or anhourly honorarium.

Electroencephalogram

Electroencephalograms (EEGs, 0.1- to 100-Hz band-width; 256 samples per second) were recorded from60 scalp electrodes located in standard 10/10 electrodepositions imbedded in an elastic cap recording device(ElectroCap).

Electrooculogram

Electrodes were placed at the outer canthi of each eyeto measure horizontal eye movements. Vertical eyemovements were measured from one electrode placedon the right suborbital ridge and from FP2, an electrodelocated just above the right eyebrow. All channels werereferenced to linked mastoids. Skin impedances forreference and ground channels were brought to below5 k�. Other electrode impedances were brought tobelow 20 k�.

Task

A modified one-back working memory Stroop task wasused in this study. Stroop stimuli consisted of groups ofnumbers: 1–5 instances of an integer between 1 and 5.Half of the stimuli were ‘‘congruent,’’ meaning that theinteger used was the same as the number of instances(i.e., 333) and half were ‘‘incongruent’’ (i.e., 444). Sub-jects were instructed to detect how many instances ofan integer appeared in each stimulus, and to indicatewhether this value in each group matched this value inthe immediately preceding group (see Figure 5). Sub-jects responded to each stimulus by pressing the‘‘match’’ or ‘‘nonmatch’’ button on a button controlpanel. Before each number stimulus, a highly aversive orneutral picture from the IAPS was presented.

The IAPS pictures used in this experiment wereselected according to the normative pleasantness andarousal ratings that accompanied the IAPS set. Highlyaversive images had the lowest pleasantness and high-est arousal ratings and included gruesome scenes.Neutral images had low arousal ratings and included

ordinary people and objects. Twenty-one images ofeach type were used throughout the experiment. Pic-tures appeared in pseudorandom order (with repetitiononly after exhausting the complete set of 42 within ablock and no immediate sequential repetition of theexact same picture) between the Stroop stimuli. Eachpicture was repeated no less than three and no morethan six times during the course of an individual sub-ject’s experiment.

Task trials began with the appearance of a centralfixation cross-hair for 600 msec, followed by an IAPSpicture that remained on the screen for 950 msec. IAPSpictures occupied up to 5.38 of visual angle on bothsides of the visual midline. Fifty milliseconds after thepicture disappeared, a congruent or incongruent num-ber stimulus was presented in either the LVF or RVF for150 msec. The number stimuli occupied between 5.58and 7.58 of visual angle on either side of the visualmidline. A uniform 2250-msec response window fol-lowed offset of the number stimuli. Congruent and in-congruent number stimuli were presented separately inblocks of 63 trials. Data from the four blocks of incon-gruent number (Stroop) stimuli trials are presented here.

Procedure

Upon arrival, subjects signed consent forms and filledout a secondary screening form confirming their eligi-

Figure 5. Task specifications. A trial began with a white crosshair

at the center of the monitor. After 600 msec, the crosshair wasreplaced by an aversive or neutral picture that lasted 950 msec.

Fifty milliseconds after the picture offset a Stroop stimulus

was presented for 150 msec in the RVF or LVF, followed by a

2250-msec response window then the onset of crosshair for thesubsequent trial. Trials were presented in blocks of 63 trials.

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bility to be an EEG subject on that day. If all criteria weremet, they were led into a sound attenuated experimentalbooth, seated approximately 52 in. in front of a monitorand outfitted with a button control panel. Followingverbal instructions, they performed 4 blocks of a trainingversion of the experimental task. The training task wasidentical to the described experimental task, but theIAPS pictures were omitted. Training and experimentaltask block order was counterbalanced across subjects.Subjects were instructed to respond as quickly and asaccurately as possible. Experimenters gave general per-formance feedback in between completed trainingblocks. Subjects were then prepared for EEG recording.When the recording cap was in place, subjects werebriefed about basic EEG principles and encouraged notto blink excessively, tense facial muscles, clench theirjaws, or chew.

Prior to the first experimental task block, subjectswere given a PANAS (Watson, Clark, & Tellegen, 1988),with instructions to rate how accurately each of theterms on the scale described the way that they werefeeling at that moment (1 = not at all, 5 = very much).Upon completion of the PANAS, subjects received in-structions about the experimental task; it would requirethe same kinds of responses as the task that they hadjust practiced, but would include the appearance ofvarious pictures between consecutive number stimuli.Experimenters instructed subjects not to generate anyparticular response to the pictures, but just to noticethem as they continued to perform the task. Subjectsthen performed 8 blocks of the experimental task,alternating between congruent and incongruent blocks.After every two blocks were completed, subjects filledout another PANAS scale.

Data Analysis

Subjective Ratings

Subjective levels of positive and negative affect wereassessed using self-ratings on the PANAS. Across-subjectmeans for positive and negative PANAS scores weresubmitted to one factor (time: before task and after 2,4, 6, and 8 task blocks), within-subjects repeated mea-sures ANOVAs. Greenhouse–Geisser-corrected p valuesare reported for these and all subsequent analysis tocorrect for violation of the sphericity assumption.

Performance

RTs were averaged into four groups according to PVand VF of stimulus presentation. Mean RTs were sub-mitted to a two-factor (Valence � Side), within-subjects,repeated measures ANOVA. Because the task required a‘‘match’’ or ‘‘no-match’’ response, task performanceaccuracy was assessed using d0 values to minimize theinfluence of response bias on accuracy assessment. d0

Scores were averaged into the same groups as RTs, andsubmitted to the same statistical analyses.

Electrophysiology

Average ERPs locked to the presentation of the Stroopstimuli were computed from artifact-free data epochsextending from 200 msec prior to 1000 msec poststim-ulus onset. The mean signal over the 200 msec prior tostimulus onset was subtracted from each epoch toeliminate noise related to baseline amplitude shifts. Dataepochs time-locked to the Stroop stimuli were groupedaccording to PV and VF of stimulus presentation. A 20-Hzlow-pass filter was applied to ERPs prior to visual in-spection and analysis to minimize high-frequency arti-factual contributions to the signal.

ERP components that showed PV- and VF-relatedmodulation in the grand average waveforms were ex-tracted from each individual subject’s data for statisticalanalysis. Amplitudes were extracted as the mean ofamplitude values across a specified time window. ERPcomponents were measured on individual or clustersof neighboring electrodes that showed similar patternsof modulation in the grand average waveforms. Ampli-tude values from groups of electrodes were averagedtogether prior to statistical analysis. ERP componentamplitudes were submitted to a two-factor (PV � VF)within-subjects, repeated measures ANOVA. Plannedfollow-up paired t tests were carried out to explorehow differences between pairs of conditions may havecontributed to main effects and interactions.

Acknowledgments

This research was supported by NIH grant MH20006-05and NINDS grants DA14110, NS21135, PONS40813, andR21MH066737.

Reprint request should be sent to Emiliana R. Simon-Thomas,Helen Wills Neuroscience Institute, University of CaliforniaBerkeley, 132 Barker Hall, MC3190, CA 94720-3190, or via e-mail:emiliana@socrates.berkeley.edu.

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