Behavioral and Electrophysiological Evidence of a Right … · 2011-04-29 · Behavioral and...

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

amp 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 StroopsEarly-latency extrastriate attention-dependent visual ERPswere enhanced for LVF Stroops The N2 ERP was enhancedfor LVF Stroops over the right frontal and parietal scalp sitesSlow potentials (300ndash800 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 amp

INTRODUCTION

Do negative emotional and higher executive processescontribute competitively or synergistically to humancognition Platorsquos lsquolsquocompetitiversquorsquo 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 2004Drevets amp Raichle 1998 Heller amp 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 amp Raichle 2002 PerlsteinElbert amp Stenger 2002 Sato Kochiyama Yoshikawa ampMatsumura 2001 Ito Larsen Smith amp Cacioppo 1998Stormark Nordby amp 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 lsquolsquospotlightingrsquorsquo of neuralprocessing resources shapes perceptual and cognitiveprocessing during many different cognitive tasks (LuckWoodman amp Vogel 2000 Mangun amp Hillyard 1995Posner amp 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 amp Hillyard 2000 LuckWoodman et al 2000 Heinze Luck Mangun amp Hill-yard 1990 Luck Heinze Mangun amp Hillyard 1990)Subsequent electrophysiological activity associated withstimulus evaluation working memory decision-makingand response preparation also show modulation withattention allocation (Monfort amp Pouthas 2003 Vogel ampLuck 2000 Garcia-Larrea amp Cezanne-Bert 1998 GevinsSmith McEvoy amp Yu 1997 Picton 1992 Rugg MilnerLines amp Phalp 1987) Emotional states emotion judg-ments and emotional significance of stimuli also influ-ence attention-sensitive ERPs (Smith Cacioppo LarsenUniversity of California

D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 173 pp 518ndash529

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

amp 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 StroopsEarly-latency extrastriate attention-dependent visual ERPswere enhanced for LVF Stroops The N2 ERP was enhancedfor LVF Stroops over the right frontal and parietal scalp sitesSlow potentials (300ndash800 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 amp

INTRODUCTION

Do negative emotional and higher executive processescontribute competitively or synergistically to humancognition Platorsquos lsquolsquocompetitiversquorsquo 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 2004Drevets amp Raichle 1998 Heller amp 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 amp Raichle 2002 PerlsteinElbert amp Stenger 2002 Sato Kochiyama Yoshikawa ampMatsumura 2001 Ito Larsen Smith amp Cacioppo 1998Stormark Nordby amp 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 lsquolsquospotlightingrsquorsquo of neuralprocessing resources shapes perceptual and cognitiveprocessing during many different cognitive tasks (LuckWoodman amp Vogel 2000 Mangun amp Hillyard 1995Posner amp 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 amp Hillyard 2000 LuckWoodman et al 2000 Heinze Luck Mangun amp Hill-yard 1990 Luck Heinze Mangun amp Hillyard 1990)Subsequent electrophysiological activity associated withstimulus evaluation working memory decision-makingand response preparation also show modulation withattention allocation (Monfort amp Pouthas 2003 Vogel ampLuck 2000 Garcia-Larrea amp Cezanne-Bert 1998 GevinsSmith McEvoy amp Yu 1997 Picton 1992 Rugg MilnerLines amp Phalp 1987) Emotional states emotion judg-ments and emotional significance of stimuli also influ-ence attention-sensitive ERPs (Smith Cacioppo LarsenUniversity of California

D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 173 pp 518ndash529

amp Chartrand 2003 Bernat Bunce amp Shevrin 2001 Keilet al 2001 Sato et al 2001 Kayser Bruder TenkeStewart amp Quitkin 2000 Schupp et al 2000 PizzagalliRegard amp Lehmann 1999 Diedrich Naumann MaierBecker amp 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 amp Knight 2000 StormarkHugdahl amp Posner 1999 Van Strien amp Luipen 1999Stormark Nordby et al 1995 Van Strien amp Heijt 1995Van Strien amp 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 amp 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 Lupienrsquos 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(eg fear aversion) emotions and that the left hemi-sphere may play a greater role in approach-relatedemotion (eg joy) (Adolphs Jansari amp Tranel 2001

Davidson Ekman Saron Senulis amp Friesen 1990 Da-vidson Mednick Moss Saron amp Schaffer 1987) Bothversions of the valence hypothesis the lsquolsquoright hemi-sphere emotionrsquorsquo and the lsquolsquoleft hemisphere approachversus right hemisphere withdrawal emotionrsquorsquo are sup-ported if the evidence is divided into studies that requireidentification of emotion expression versus studies thatinvolve experienced emotions respectively (Van Strienamp Van Beek 2000 Ley amp 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(448) =98 p lt 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 lt 01) Negative PANASscores also showed a main effect of time F(448) = 98p lt 001 Planned comparison showed that the nega-tive affect score increased significantly after starting thetask ( p lt 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 accuracyHowever there was a VF PV interaction F(112) =

Simon-Thomas Role and Knight 519






RESULTS

Subjective Ratings


Performance

Response Times


Accuracy



805 p lt 05 Responses to LVF Stroops that followedaversive pictures were more accurate than responsesto LVF Stroops that followed neutral pictures (428 plusmn044 vs 344 plusmn 035 p lt 05) or to responses toRVF Stroops that followed aversive pictures (428 plusmn044 vs 338 plusmn 041 p lt 05) Responses to RVFStroops were more accurate after neutral than afteraversive pictures (40 plusmn 041 vs 338 plusmn 041) althoughthis difference did not reach significance ( p = 2)(Figure 1)

Electrophysiology

Stroop Stimulus-Locked ERPs Early Components

The amplitude of early visual components (P1N1)measured from electrodes over contralateral extrastri-ate cortex (LVF PO8 RVF PO7) showed no maineffects of VF or PV or significant interactions Howeveran 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 P1N1 magnitudewas greater for LVF Stroops over right extrastriateelectrodes than for RVF Stroops over left extrastriateelectrodes F(112) = 81 p lt 05 Planned t test com-parisons showed that this VF effect was significantfor both aversive and neutral picture trials ( p lt 05

for both) with enhanced right extrastriate activity forall stimuli Post callosal transfer the N1 measured onelectrodes over ipsilateral extrastriate cortex (LVF PO7RVF PO8) across a 180- to 220-msec window showeda VF PV interaction F(112) = 553 p lt 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(111) = 77p lt 05 (one subject was excluded from this analysisdue to excessive artifact on the measured electrodes)Frontal N2 amplitude increased for LVF StroopsPlanned follow-up t test comparisons showed that thisVF effect was significant in the aversive picture condi-tion ( p lt 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(112) = 536 p lt 05 Planned t test com-parisons showed that the parietal N2 increase for LVFstimuli was also only significant in the aversive picturecondition ( p lt 05 vs p = 66 for neutral condition)(Figure 3)

Stroop Stimulus-Locked ERPs Slow Potentials

Sustained slow potential (SP) shifts (300ndash800 msec)showed condition-related differences over right frontaland bilateral parietal regions Focused measures ofSP amplitude shifts from right frontal (Afz AF4 450ndash800 msec) and left and right parietalndashoccipital electrodes(left CP3 P3 PO3 right CP4 P4 PO4 300ndash800 msec)were analyzed to probe the effects of negative emotionand hemisphere on SPs Over right frontal electrodesa negative-going SP showed a PV VF interactionF(111) = 70 p lt 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 lt 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(112) = 1471lt 005 Planned t test comparisons showed that thisdifference was significant for LVF versus RVF aversiveand LVF versus RVF neutral picture trials ( p lt 05 forboth) Left parietal SP amplitude also showed decreasedamplitude for aversive picture trials F(112) = 601p lt 05 Planned t test comparisons showed that thiseffect was significant for LVF Stroops (aversive lt 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 lt 05 for all comparisons)

520 Journal of Cognitive Neuroscience Volume 17 Number 3


Electrophysiology











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 P1N1 is enhanced for LVF Stroops ( p lt 05) Postcallosal N1

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





tral p lt 05) and not for RVF Stroops ( p = 1) Overthe right parietal cortex a positive-going SP showed amain effect of PV F(112) = 555 p lt 05 and a VF PVinteraction F(112) = 538 p lt 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)






neutral picture trials for LVF Stroops ( p lt 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 tasknegative 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 emotionndashcognition 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 lt 001 and

p lt 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 lt 05)Over the left parietal cortex SP amplitude was decreased for RVF

Stroops relative to LVF Stroops ( p lt 05)



DISCUSSION

Behavior















factors After the initial distress subjectsrsquo emotionalresponses may have habituated with repetition of thepictures (Phan Liberzon Welsh Britton amp Taylor2003) or subjectsrsquo 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 stimuliThe 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 emotionndashcognition 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 subjectsrsquo negative emotionalresponses facilitated cognitive task processing in theright hemisphere and may have reduced task process-ing in the left hemisphere This pattern of emotionndashcognition interaction is consistent with two existingtheories related to emotional and cognitive processingin the brain The valence hypothesis (Davidson amp Irwin1999) 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 ampPetersen 1990 Friedman Polson Dafoe amp Gaskill1982 Hellige Cox amp 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 thelsquolsquocompetitiversquorsquo and the lsquolsquosynergisticrsquorsquo view of emotionndashcognition 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 consideredIn Hartikainen et alrsquos 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 presentationsDifference 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 StormarkField Hugdahl and Horowitz (1997) found that shorterintervals between emotion cues and stimuli causedinterference while longer intervals produced facilitationFinally Hartikainen et alrsquos 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 parametersand 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 globallocal perception (Evert amp 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 amp 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 amp Hillyard 1995)









Electrophysiology



Visual extrastriate activity (N1) showed diminished am-plitude for RVF stimuli that followed aversive picturesN1 amplitude is thought to index prefrontal and pari-etal modulation of early sensory processing (BarceloSuwazono amp Knight 2000) typically evidenced by in-creases with attention allocation For example improvedstimulus discrimination after attention cueing corre-lates with increased N1 amplitude (Vogel amp Luck2000) 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 cortexndashanterior cingulate network (Nieuwenhuis Yeung vanden Wildenberg amp Ridderinkhof 2003 Bokura Yama-guchi amp Kobayashi 2001) The Stroop element to thetask used in this study invoked conflict-monitoringprocesses The right frontalndashparietal N2 enhancementfor aversive-picture-preceded LVF Stroops suggests thatthe right hemispherersquos response to the demands of thecognitive task was enhanced when stimuli followedaversive pictures

Frontal and parietal SPs (450ndash800 and 300ndash800 msecrespectively) 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 frontalndashparietal network engagementwith increased task-related effort or working-memorydemand (Monfort amp Pouthas 2003 Pelosi Slade Blum-hardt amp Sharma 2000 Rama et al 1997) Decreasedamplitude of the parietal P300 (300ndash600 msec) a com-ponent that falls within the range of the SP has alsobeen related to subjective ratings of increased difficultyincreased working memory load and increased recruit-ment of frontal lobe structures to carry out task pro-cesses during working memory intervals (McEvoySmith amp Gevins 1998) Paradoxically increased parietalP300 amplitude is also related to prefrontally mediatedincreased allocation of attention and processing re-sources toward stimuli that present increased saliencesuch as novel irregularunexpected or motivationallysignificant stimuli (Soltani amp 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 hemispherersquos functional facilitation by thenegative emotion elicitation Over both left and rightparietal electrodes SP amplitude was decreased forStroops that followed aversive versus neutral picturesmainly 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 demandtherefore increasing frontal engagement in the frontalndashparietal 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 hemisphereNeurophysiological indices of visual feature analysisworking 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 informationFrontal SPs were enhanced for stimuli presented tothe right hemisphere and showed enhanced sensitivityto concurrent emotion manipulation These findings arein accord with Grayrsquos (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







Conclusions



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 andor anhourly honorarium

Electroencephalogram

Electroencephalograms (EEGs 01- to 100-Hz band-width 256 samples per second) were recorded from60 scalp electrodes located in standard 1010 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 1ndash5 instances of an integer between 1 and 5Half of the stimuli were lsquolsquocongruentrsquorsquo meaning that theinteger used was the same as the number of instances(ie 333) and half were lsquolsquoincongruentrsquorsquo (ie 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 thelsquolsquomatchrsquorsquo or lsquolsquononmatchrsquorsquo 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 scenesNeutral 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-jectrsquos 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 538 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 558and 758 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


METHODS

Subjects




Electrooculogram


Task





Procedure








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 subjectsSubjects 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 recordingWhen 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 amp 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 stimuliExperimenters 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 taskalternating between congruent and incongruent blocksAfter 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 24 6 and 8 task blocks) within-subjects repeated mea-sures ANOVAs GreenhousendashGeisser-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-subjectsrepeated measures ANOVA Because the task required alsquolsquomatchrsquorsquo or lsquolsquono-matchrsquorsquo 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 subjectrsquos 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-ThomasHelen Wills Neuroscience Institute University of CaliforniaBerkeley 132 Barker Hall MC3190 CA 94720-3190 or via e-mailemilianasocratesberkeleyedu

REFERENCES

Adolphs R Jansari A amp Tranel D (2001) Hemisphericperception of emotional valence from facial expressionsNeuropsychology 15 516ndash524

Awh E Anllo-Vento L amp Hillyard S A (2000) The role ofspatial selective attention in working memory for locationsEvidence from event-related potentials Journal of CognitiveNeuroscience 12 840ndash847

Barcelo F Suwazono S amp Knight R T (2000) Prefrontalmodulation of visual processing in humans NatureNeuroscience 3 399ndash403

Bernat E Bunce S amp Shevrin H (2001) Event-relatedpotentials differentiate positive and negative moodadjectives during both supraliminal and subliminal visualprocessing International Journal of Psychophysiology42 11ndash34




Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES






Bokura H Yamaguchi S amp Kobayashi S (2001)Electrophysiological correlates for response inhibitionin a gonogo task Clinical Neurophysiology 1122224ndash2232

Codispoti M Bradley M M amp Lang P J (2001) Affectivereactions to briefly presented pictures Psychophysiology38 474ndash478

Davidson R J Ekman P Saron C D Senulis J A ampFriesen W V (1990) Approachndashwithdrawal and cerebralasymmetry Emotional expression and brain physiologyJournal of Personality and Social Psychology 58 330ndash341

Davidson R J amp Irwin W (1999) The functionalneuroanatomy of emotion and affective style Trends inCognitive Neurosciences 3 11ndash21

Davidson R J Mednick D Moss E Saron C ampSchaffer C E (1987) Ratings of emotion in faces areinfluenced by the visual field to which stimuli arepresented Brain and Cognition 6 403ndash411

Derryberry D (1990) Right hemisphere sensitivity tofeedback Neuropsychologia 28 1261ndash1271

Diedrich O Naumann E Maier S Becker G ampBartussek D (1997) A frontal positive slow wave inthe ERP associated with emotional slides Journal ofPsychophysiology 11 71ndash84

Dolan R J (2002) Emotion cognition and behavior Science298 1191ndash1194

Drevets W C amp Raichle M E (1998) Reciprocal suppressionof regional cerebral blood flow during emotional versushigher cognitive processes Implications for interactionsbetween emotion and cognition Cognition amp Emotion 12353ndash385

Evert D L amp Kmen M (2003) Hemispheric asymmetriesfor global and local processing as a function of stimulusexposure duration Brain and Cognition 51 115ndash142

Evert D L McGlinchey-Berroth R Verfaellie M ampMilberg W P (2003) Hemispheric asymmetries forselective attention apparent only with increased taskdemands in healthy participants Brain and Cognition53 34ndash41

Friedman A Polson M C Dafoe C G amp Gaskill S J(1982) Dividing attention within and between hemispheresTesting a multiple resources approach to limited-capacityinformation processing Journal of ExperimentalPsychology Human Perception and Performance 8625ndash650

Garcia-Larrea L amp Cezanne-Bert G (1998) P3 positive slowwave and working memory load A study on the functionalcorrelates of slow wave activity Electroencephalographyand Clinical Neurophysiology 108 260ndash273

Gevins A Smith M McEvoy L amp Yu D (1997)High-resolution EEG mapping of cortical activationrelated to working memory Effects of task difficulty typeof processing and practice Cerebral Cortex 7 374ndash385

Gray J Braver T amp Raichle M (2002) Integration ofemotion and cognition in the lateral prefrontal cortexProceedings of the National Academy of Sciences USA 994115ndash4120

Gray J R (2001) Emotional modulation of cognitive controlApproachndashwithdrawal states double-dissociate spatial fromverbal two-back task performance Journal of ExperimentalPsychology 130 436ndash452

Hartikainen K M Ogawa K H amp Knight R T (2000)Transient interference of right hemispheric function due toautomatic emotional processing Neuropsychologia 381576ndash1580

Heinze H J Luck S J Mangun G R amp Hillyard S A (1990)Visual event-related potentials index focused attentionwithin bilateral stimulus arrays I Evidence for early

selection Electroencephalography and ClinicalNeurophysiology 75 511ndash527

Heller W amp Nitschke J B (1997) Regional brain activity inemotion A framework for understanding cognition indepression Cognition amp Emotion 11 637ndash661

Hellige J B Cox P J amp Litvac L (1979) Informationprocessing in the cerebral hemispheres Selectivehemispheric activation and capacity limitations Journalof Experimental Psychology General 108 251ndash279

Ito T A Larsen J T Smith K amp Cacioppo J T (1998)Negative information weighs more heavily on the brainThe negativity bias in evaluative categorizations Journalof Personality and Social Psychology 75 887ndash900

Kayser J Bruder G E Tenke C E Stewart J E Quitkin F M(2000) Event-related potentials (ERPs) to hemifieldpresentations of emotional stimuli Differences betweendepressed patients and healthy adults in P3 amplitude andasymmetry International Journal of Psychophysiology 36211ndash236

Keil A Muller M Gruber T Wienbruch C Stolarova Mamp Elbert T (2001) Effects of emotional arousal in thecerebral hemispheres A study of oscillatory brain activityand event related potentials Clinical Neurophysiology112 2057ndash2068

Lang P J (1999) The International Affective Picture SystemGainesville FL NIMH Center for the Study of Emotion andAttention University of Florida

Ley R G amp Strauss E (1986) Hemispheric asymmetries inthe perception of facial expressions by normals In R Bruyer(Ed) The neuropsychology of face perception and facialexpression (pp 269ndash289) Hillsdale NJ Erlbaum

Luck S Woodman G amp Vogel E (2000) Event-relatedpotential studies of attention Trends in Cognitive Sciences4 432ndash440

Luck S J Heinze H J Mangun G R amp Hillyard S A (1990)Visual event-related potentials index focused attentionwithin bilateral stimulus arrays II Functional dissociationof P1 and N1 components Electroencephalography andClinical Neurophysiology 75 528ndash542

Mangun G R amp Hillyard S A (1995) Mechanismsand models of selective attention In M D Rugg ampM G Coles (Eds) Electrophysiology of mind Eventrelated potentials and cognition (pp 40ndash85) New YorkOxford University Press

McEvoy L K Smith M E amp Gevins A (1998) Dynamiccortical networks of verbal and spatial working memoryEffects of memory load and task practice Cerebral Cortex8 563ndash574

Monfort V amp Pouthas V (2003) Effects of workingmemory demands on frontal slow waves in time-intervalreproduction tasks in humans Neuroscience Letters 343195ndash199

Nieuwenhuis S Yeung N van den Wildenberg W ampRidderinkhof K R (2003) Electrophysiological correlatesof anterior cingulate function in a gono-go task Effects ofresponse conflict and trial type frequency CognitiveAffective and Behavioral Neuroscience 3 17ndash26

Northoff G Heinzel A Bermpohl F Niese R Pfennig APascual-Leone A amp Schlaug G (2004) Reciprocalmodulation and attenuation in the prefrontal cortex AnfMRI study on emotionalndashcognitive interaction HumanBrain Mapping 21 202ndash212

Pelosi L Slade T Blumhardt L D amp Sharma V K (2000)Working memory dysfunction in major depression Anevent-related potential study Clinical Neurophysiology111 1531ndash1543

Perlstein W M Elbert T amp Stenger V A (2002) Dissociationin human prefrontal cortex of affective influences on






































working memory-related activity Proceedings of theNational Academy of Sciences USA 99 1736ndash1741

Phan K L Liberzon I Welsh R C Britton J C ampTaylor S F (2003) Habituation of rostral anteriorcingulate cortex to repeated emotionally salient picturesNeuropsychopharmacology 28 1344ndash1350

Picton T W (1992) The P300 wave of the humanevent-related potential Journal of ClinicalNeurophysiology 9 456ndash479

Pizzagalli D Regard M amp Lehmann D (1999) Rapidemotional face processing in the human right and leftbrain hemispheres An ERP study NeuroReport 102691ndash2698

Posner M I amp Petersen S E (1990) The attention systemof the human brain Annual Review of Neuroscience 1325ndash42

Rama P Kesseli K Reinikainen K Kekoni JHamalainen H amp Carlson S (1997) Visuospatialmnemonic load modulates event-related slow potentialsNeuroReport 8 871ndash876

Rodway P Wright L amp Hardie S (2003) The valence-specificlaterality effect in free viewing conditions The influenceof sex handedness and response bias Brain andCognition 53 452ndash463

Rugg M Milner A Lines C amp Phalp R (1987)Modulation of visual event-related potentials by spatialand non-spatial selective attention Neuropsychologia25 85ndash96

Sato W Kochiyama T Yoshikawa S amp Matsumura M(2001) Emotional expression boosts early visual processingof the face ERP recording and its decomposition byindependent component analysis NeuroReport 12709ndash714

Schupp H T Cuthbert B N Bradley M M Cacioppo J TIto T amp Lang P J (2000) Affective pictureprocessing The late positive potential is modulatedby motivational relevance Psychophysiology 37257ndash261

Smith N K Cacioppo J T Larsen J T amp Chartrand T L(2003) May I have your attention please Electrocorticalresponses to positive and negative stimuliNeuropsychologia 41 171ndash183

Soltani M amp Knight R T (2000) Neural origins of the P300Critical Reviews in Neurology 14 199ndash224

Stormark K M Field N P Hugdahl K amp Horowitz M(1997) Selective processing of visual alcohol cues inabstinent alcoholics An approach-avoidance conflictAddictive Behavior 22 509ndash519

Stormark K M Hugdahl K amp Posner M (1999) Emotionalmodulation of attention orienting A classical conditioningstudy Scandinavian Journal of Psychology 40 91ndash99

Stormark K M Nordby H amp Hugdahl K (1995) Attentionalshifts to emotionally charged cues Behavioral and ERP dataCognition and Emotion 9 507ndash523

Van Strien J W amp Heijt R (1995) Altered visual fieldasymmetries for letter naming and letter matching as aresult of concurrent presentation of threatening andnonthreatening words Brain and Cognition 29 187ndash203

Van Strien J W amp Luipen M W (1999) Hemisphericfacilitation as a result of threatening and nonthreateningwords Blocked vs mixed presentation effects and ordereffects Neuropsychologia 37 617ndash621

Van Strien J W amp Morpurgo M (1992) Oppositehemispheric activations as a result of emotionallythreatening and non-threatening words Neuropsychologia30 845ndash848

Van Strien J W amp Van Beek S (2000) Ratings of emotionin laterally presented faces Sex and handedness effectsBrain and Cognition 44 645ndash652

Vogel E K amp Luck S J (2000) The visual N1 componentas an index of a discrimination process Psychophysiology37 190ndash203

Watson D Clark L A amp Tellegen A (1988) Developmentand validation of brief measures of positive and negativeaffect The PANAS scales Journal of Personality and SocialPsychology 54 1063ndash1070





























RESULTS

Subjective Ratings


Performance

Response Times


Accuracy








RESULTS

Subjective Ratings


Performance

Response Times


Accuracy




Electrophysiology












Electrophysiology


























DISCUSSION

Behavior
















DISCUSSION

Behavior






















Electrophysiology










Electrophysiology








Conclusions








Conclusions



METHODS

Subjects




Electrooculogram


Task





Procedure








METHODS

Subjects




Electrooculogram


Task





Procedure










Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES



























































































































Electrophysiology












Electrophysiology


























DISCUSSION

Behavior
















DISCUSSION

Behavior






















Electrophysiology










Electrophysiology








Conclusions








Conclusions



METHODS

Subjects




Electrooculogram


Task





Procedure








METHODS

Subjects




Electrooculogram


Task





Procedure










Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES









































































































































DISCUSSION

Behavior
















DISCUSSION

Behavior






















Electrophysiology










Electrophysiology








Conclusions








Conclusions



METHODS

Subjects




Electrooculogram


Task





Procedure








METHODS

Subjects




Electrooculogram


Task





Procedure










Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES

































































































































Electrophysiology










Electrophysiology








Conclusions








Conclusions



METHODS

Subjects




Electrooculogram


Task





Procedure








METHODS

Subjects




Electrooculogram


Task





Procedure










Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES































































































































Conclusions








Conclusions



METHODS

Subjects




Electrooculogram


Task





Procedure








METHODS

Subjects




Electrooculogram


Task





Procedure










Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES


























































































































METHODS

Subjects




Electrooculogram


Task





Procedure








METHODS

Subjects




Electrooculogram


Task





Procedure










Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES




























































































































Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES








Data Analysis

Subjective Ratings


Performance



Electrophysiology



Acknowledgments



REFERENCES


























































































































Behavioral and Electrophysiological Evidence of a Right … · 2011-04-29 · Behavioral and...

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