Attentional orienting towards emotion: P2 and N400 ERP effects

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Neuropsychologia 49 (2011) 3121–3129 Contents lists available at ScienceDirect Neuropsychologia jo u rn al hom epa ge : www.elsevier.com/locate/neuropsychologia Attentional orienting towards emotion: P2 and N400 ERP effects Philipp Kanske a,b,, Jan Plitschka c , Sonja A. Kotz a a Max Planck Institute for Human Cognitive and Brain Sciences, Neurocognition of Rhythm in Communication Group, Leipzig, Germany b Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Mannheim, Germany c Bonn-Aachen International Center for Information Technology B-IT, Algorithmic Bioinformatics Group, Rheinische Friedrich-Wilhelms-Universität Bonn, Germany a r t i c l e i n f o Article history: Received 3 December 2010 Received in revised form 7 July 2011 Accepted 18 July 2011 Available online 23 July 2011 Keywords: EEG Event related potentials Emotion Linguistics Semantics Social cognition a b s t r a c t Attention can be oriented to different spatial locations yielding faster processing of attended compared to unattended stimuli. Similarly attention can be oriented to a semantic category such as “animals” or “tools”. Words from the attended category will also be recognized faster than words from an unattended category. Here, we asked whether it is possible to orient attention to an emotional category, for example, “negative emotional stimuli”. Furthermore, we investigated which mechanisms facilitate processing of attended stimuli. In an attentional orienting paradigm in which cues are informative with regard to the spatial location, semantic category, or emotional category of subsequent target words, we found attention effects in all three cue conditions. Words at attended locations or of the attended semantic or emotional category were responded to faster than unattended categories. While spatial attention acted upon early visual processing and amplified occipital N1-P2 potentials, semantic cues modulated the N400 amplitude indexing semantic processing. Emotional cues also yielded an N400 modulation; however, in addition, a left anterior P2 effect was observed. The data clearly show that attention can be oriented to emotional categories. Emotional orienting yields facilitated processing of an attended emotional category through the modulation of early and late word processing stages. © 2011 Elsevier Ltd. All rights reserved. 1. Introduction Human communication relies on the fast detection of others’ emotional states as these are highly predictive with regard to future behavior. Anger, for example, may result in an attack, while a neutral state may signal safety. Therefore, emotional stimuli are not only processed faster than neutral stimuli (Carretie, Hinojosa, Martin-Loeches, Mercado, & Tapia, 2004; Kanske & Kotz, 2007; Ortigue et al., 2004), but also attract attention (e.g. to their spa- tial location, see Stormark, Nordby, & Hugdahl, 1995; or in visual image processing, see Schupp et al., 2007). However, it is unclear whether attention can also be oriented in advance to signals of oth- ers’ emotional states. Thus, we asked whether non-emotional cues can lead to an active orienting of attention to the emotional quality of a stimulus. We investigated emotional orienting in a Posner-type cueing paradigm and compared it to spatial and semantic cueing effects (Cristescu & Nobre, 2008). Orienting of attention refers to the mechanisms that select infor- mation. It has primarily been investigated with perceptual features Corresponding author at: Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Square J5, 68159 Mannheim, Germany. Tel.: +49 621 1703 6307; fax: +49 621 1703 6305. E-mail addresses: [email protected], [email protected] (P. Kanske). in vision, mainly in visual spatial processing. Classic experimen- tal paradigms include visual search (Treisman & Gelade, 1980) and cueing tasks (Posner, 1980). In the latter, a cue that informs the participant about the spatial location of an upcoming tar- get is presented prior to that target. The modulatory influence of attention on stimulus processing can then be studied when com- paring targets that are preceded by valid and invalid cues. Reaction times (RT) to validly cued targets are typically shorter than those to invalidly cued target sites (Posner, 1980). This indicates that visual spatial attention is oriented according to cue information, facilitating the processing of subsequent target stimuli. In event- related potentials (ERP) this facilitated processing is reflected in an amplification of early visual potentials over occipital electrodes. P1 and N1 amplitudes are enhanced for attended stimuli (Hillyard & Anllo-Vento, 1998); however, there are also reports of P2 modula- tions (Eason, 1981; Gomez, Vazquez, Vaquero, Lopez-Mendoza, & Cardoso, 1998; Hillyard & Mangun, 1986; Maenoa, Gjinia, Iraminaa, Etob, & Ueno, 2004; Shedden & Nordgaard, 2001; van Voorhis & Hillyard, 1977). Only a few studies have investigated whether attention can also select information that is not sensory-perceptual, but post- perceptual. Recently, Cristescu and Nobre (2008) and Cristescu, Devlin, and Nobre (2006) proposed a version of the classical cueing paradigm that tests orienting of attention to the semantic cate- gory of a stimulus. Participants performed a lexical decision task. Prior to the words, an abstract cue symbol was presented that 0028-3932/$ see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.07.022

Transcript of Attentional orienting towards emotion: P2 and N400 ERP effects

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Neuropsychologia 49 (2011) 3121– 3129

Contents lists available at ScienceDirect

Neuropsychologia

jo u rn al hom epa ge : www.elsev ier .com/ locate /neuropsychologia

ttentional orienting towards emotion: P2 and N400 ERP effects

hilipp Kanskea,b,∗, Jan Plitschkac, Sonja A. Kotza

Max Planck Institute for Human Cognitive and Brain Sciences, Neurocognition of Rhythm in Communication Group, Leipzig, GermanyDepartment of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Mannheim, GermanyBonn-Aachen International Center for Information Technology B-IT, Algorithmic Bioinformatics Group, Rheinische Friedrich-Wilhelms-Universität Bonn, Germany

r t i c l e i n f o

rticle history:eceived 3 December 2010eceived in revised form 7 July 2011ccepted 18 July 2011vailable online 23 July 2011

eywords:EGvent related potentials

a b s t r a c t

Attention can be oriented to different spatial locations yielding faster processing of attended comparedto unattended stimuli. Similarly attention can be oriented to a semantic category such as “animals” or“tools”. Words from the attended category will also be recognized faster than words from an unattendedcategory. Here, we asked whether it is possible to orient attention to an emotional category, for example,“negative emotional stimuli”. Furthermore, we investigated which mechanisms facilitate processing ofattended stimuli. In an attentional orienting paradigm in which cues are informative with regard to thespatial location, semantic category, or emotional category of subsequent target words, we found attentioneffects in all three cue conditions. Words at attended locations or of the attended semantic or emotional

motioninguisticsemanticsocial cognition

category were responded to faster than unattended categories. While spatial attention acted upon earlyvisual processing and amplified occipital N1-P2 potentials, semantic cues modulated the N400 amplitudeindexing semantic processing. Emotional cues also yielded an N400 modulation; however, in addition, aleft anterior P2 effect was observed. The data clearly show that attention can be oriented to emotionalcategories. Emotional orienting yields facilitated processing of an attended emotional category through

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the modulation of early a

. Introduction

Human communication relies on the fast detection of others’motional states as these are highly predictive with regard to futureehavior. Anger, for example, may result in an attack, while aeutral state may signal safety. Therefore, emotional stimuli areot only processed faster than neutral stimuli (Carretie, Hinojosa,artin-Loeches, Mercado, & Tapia, 2004; Kanske & Kotz, 2007;rtigue et al., 2004), but also attract attention (e.g. to their spa-

ial location, see Stormark, Nordby, & Hugdahl, 1995; or in visualmage processing, see Schupp et al., 2007). However, it is unclear

hether attention can also be oriented in advance to signals of oth-rs’ emotional states. Thus, we asked whether non-emotional cuesan lead to an active orienting of attention to the emotional qualityf a stimulus. We investigated emotional orienting in a Posner-typeueing paradigm and compared it to spatial and semantic cueing

ffects (Cristescu & Nobre, 2008).

Orienting of attention refers to the mechanisms that select infor-ation. It has primarily been investigated with perceptual features

∗ Corresponding author at: Department of Cognitive and Clinical Neuroscience,entral Institute of Mental Health, Square J5, 68159 Mannheim, Germany.el.: +49 621 1703 6307; fax: +49 621 1703 6305.

E-mail addresses: [email protected], [email protected]. Kanske).

028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2011.07.022

te word processing stages.© 2011 Elsevier Ltd. All rights reserved.

in vision, mainly in visual spatial processing. Classic experimen-tal paradigms include visual search (Treisman & Gelade, 1980)and cueing tasks (Posner, 1980). In the latter, a cue that informsthe participant about the spatial location of an upcoming tar-get is presented prior to that target. The modulatory influence ofattention on stimulus processing can then be studied when com-paring targets that are preceded by valid and invalid cues. Reactiontimes (RT) to validly cued targets are typically shorter than thoseto invalidly cued target sites (Posner, 1980). This indicates thatvisual spatial attention is oriented according to cue information,facilitating the processing of subsequent target stimuli. In event-related potentials (ERP) this facilitated processing is reflected in anamplification of early visual potentials over occipital electrodes. P1and N1 amplitudes are enhanced for attended stimuli (Hillyard &Anllo-Vento, 1998); however, there are also reports of P2 modula-tions (Eason, 1981; Gomez, Vazquez, Vaquero, Lopez-Mendoza, &Cardoso, 1998; Hillyard & Mangun, 1986; Maenoa, Gjinia, Iraminaa,Etob, & Ueno, 2004; Shedden & Nordgaard, 2001; van Voorhis &Hillyard, 1977).

Only a few studies have investigated whether attention canalso select information that is not sensory-perceptual, but post-perceptual. Recently, Cristescu and Nobre (2008) and Cristescu,

Devlin, and Nobre (2006) proposed a version of the classical cueingparadigm that tests orienting of attention to the semantic cate-gory of a stimulus. Participants performed a lexical decision task.Prior to the words, an abstract cue symbol was presented that

3122 P. Kanske et al. / Neuropsycholo

Fig. 1. Cueing task with spatial, semantic, and emotional cueing conditions. Thecues validly (80%) or invalidly (20%) predicted the location, semantic category, orem

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A trial sequence is displayed in Fig. 1. First, a cue was presented in the center

motional connotation of subsequent target words. Participants identified the gram-atical gender of the target words.

as informative with regard to the semantic category of the tar-et word, which could either be an animal or a tool word. Validues led to shorter RTs in the lexical decision task. This behavioralffect was accompanied by a reduction of the N400 potential, anndex of semantic analysis and integration (Kutas & Federmeier,000). A similar behavioral result in spatial and semantic orienting

s thus achieved through distinct mechanisms that modify differ-nt levels of stimulus analysis (Cristescu & Nobre, 2008). Analysis ofue-related activity in fMRI revealed a similar fronto-parietal net-ork for spatial and semantic orienting and additional activations

or semantic orienting including left hemisphere areas involvedn semantic analysis of words, such as the inferior frontal cortexCristescu et al., 2006).

The semantic orienting task (Cristescu & Nobre, 2008; Cristescut al., 2006) can be adapted to the current question of whetherttention can be oriented to the emotional quality of a target stim-lus. Accelerated processing of a stimulus that is preceded by anbstract cue validly predicting whether the stimulus is emotionalr neutral would indicate that attention can select emotional cate-ories similarly to selecting spatial locations. To test this possibilitye extended the attentional orienting paradigm by including (1)

patially informative cues, (2) semantically informative cues, and3) emotionally informative cues (see Fig. 1). The same abstract cueymbols were used in the three conditions; however, their meaningiffered. Spatial cues predicted the location of the target to the rightr left of a fixation point. Comparable to Cristescu and Nobre (2008),he semantic cues predicted whether the target words belonged tohe category “animals” or “tools”. In the emotional orienting con-ition, the cues predicted the emotional connotation of the targetords. Negative (e.g., tumor, corpse, jail) and neutral words (e.g.,ea, belly, dam) were presented. The design thus largely resemblesriming studies in which, for example, semantically related wordsre presented (Rugg, 1985). The prime word is expected to activateandidates in a semantic network, which then ease the processingnd integration of subsequently presented target words. The criti-al difference in the present design is that prime words are replacedy abstract cue symbols that may only pre-activate a certain num-er of network candidates if attention is voluntarily and activelyriented towards them.

In addition to the question whether it is possible to orient atten-ion to a stimulus’ emotional characteristics, we asked which stagesf emotional word processing would be modulated by attention,.e. can be pre-activated. To this end, we also recorded ERPs duringhe task. With reference to the semantic orienting task (Cristescu &

obre, 2008) it seems likely to expect an N400 effect. Stimuli of onemotional category (e.g., hatred, bomb, terror) also group semanti-ally (Bradley & Lang, 1994; Moore, Romney, Hsia, & Rusch, 1999;

gia 49 (2011) 3121– 3129

Romney, Moore, & Rusch, 1997; Wierzbicka, 1992). Consequently,comparable to semantic priming, an N400 has been observed inemotional priming (Steinbeis & Koelsch, 2009). Interestingly, emo-tional words also modulate ERPs in much earlier time-windows.Frequently, effects are observed in the P2 time-window (Begleiter& Platz, 1969; Begleiter, Projesz, & Garazzo, 1979; Bernat, Bunce,& Shevrin, 2001; Herbert, Kissler, Junghöfer, Peyk, & Rockstroh,2006; Schapkin, Gusev, & Kuhl, 2000). For example, Kanske andKotz (2007) observed a larger P2 amplitude for positive emo-tional than neutral words in a lexical decision task, however, anumber of studies have also observed other early emotion effects(Herbert, Junghöfer, & Kissler, 2008; Hofmann, Kuchinke, Tamm,Vo, & Jacobs, 2009; Ortigue et al., 2004; Schacht & Sommer, 2009;Scott, O’Donnell, Leuthold, & Sereno, 2009; for reviews Kissler,Assadollahi, & Herbert, 2006; Kotz & Paulmann, 2011). Theseearly emotion effects have often been interpreted as indicatingrapid attention capture by emotional words (Herbert et al., 2008)or rudimentary semantic stimulus classification (Kissler, Herbert,Winkler, & Junghofer, 2009). Also, there is mixed evidence regard-ing the automaticity of these early effects. In a study directlycontrasting different tasks, Begleiter et al. (1979) found early emo-tion effects only in an affective evaluation task, but not in aletter-identification condition. This would suggest that early ERPeffects are only elicited when participants focus on judging theemotional connotation of presented words. Independent of theexact nature of these early emotion effects, if they represent anemotional word processing stage that can be selected by attention,than there should be ERP effects prior to the N400, potentially inthe P2 time-window.

In summary, our hypotheses are: (1) attentional orientingeffects in RTs in all three cueing conditions (spatial, semantic, emo-tional). (2) An amplification of early visual potentials over occipitalelectrodes in the spatial orienting condition. (3) Modulation of theN400 in the semantic orienting condition (see Cristescu & Nobre,2008). (4) Similarly, an N400 modulation is expected in the emo-tional orienting condition. Here, an effect may also show in anearlier time window (e.g., the P2; Kanske & Kotz, 2007).

2. Methods

2.1. Participants

Twenty-five participants (13 females) volunteered for the experiment. All werenative speakers of German and right-handed according to the Edinburgh Handed-ness Inventory (Oldfield, 1971). Three participants (2 females) were excluded dueto increased error rates (more than 40% in at least one condition). Data from twofurther participants (2 females) could not be analyzed due to severe artifacts. Theremaining 20 participants had a mean age of 24.8 years (SD 3.0) and a handed-ness laterality quotient of 96.0 (SD 6.4). All reported normal or corrected-to-normalvision.

2.2. Stimuli

To assess orienting of attention to semantic and to emotional categories, twoword lists were constructed (see Supplement 1 for a complete stimulus list). Thelist for the semantic task contained 32 concrete animal and 32 tool words. Theemotional word list included 32 negative emotional and 32 neutral words, whichdiffered significantly in valence and arousal ratings, but not in rated concreteness(see Table 1). The ratings were taken from a previous rating study with 32 partici-pants (16 females). The word groups did not differ in number of letters and numberof syllables. Also, the words were controlled for frequency of usage according to theWortschatzlexikon of the University of Leipzig (http://wortschatz.uni-leipzig.de/;Biemann, Bordag, Heyer, Quasthoff, & Wolf, 2004). All words were German nouns,half of which were of male gender (“der”), and the other half of female gender (“die”).

2.3. Task and procedure

of the screen, followed by a target word in either the right or the left hemifield.Participants decided whether the target word required the article “der” or “die”.However, the cue contained different types of information in the different runs ofthe experiment. (1) In the spatial orienting condition, the cue predicted the location

P. Kanske et al. / Neuropsychologia 49 (2011) 3121– 3129 3123

Table 1Psycholinguistic parameters of the selected words. Means and standard deviations (in parentheses) are given.

Frequency # of letters # of syllables Valence Arousal Concreteness

Semantic Animals 13.69 (1.64) 5.41 (1.27) 1.94 (0.56) – – –Wordlist Tools 14.47 (1.59) 5.72 (1.20) 1.94 (0.35) – – –

Emotional Neutral 13.47 (2.36) 6.00 (1.08) 1.84 (0.37) 5.18 (0.20) 2.56 (0.66) 4.63 (2.25)1

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difference between valid and invalid cues did not reach significance(semantic cues: F(1,19) = 3.27, p > .05; emotional cues: F(1,19) = 0.0,p > .10; spatial cues, semantic wordlist: F(1,19) = 12.39, p < .01; spa-tial cues, emotional wordlist: F(1,19) = 11.49, p < .01).

Wordlist Negative 13.47 (2.53) 5.50 (1.14)

f the target words (both, the semantic and the emotional word list were presentedn this condition). (2) In the semantic orienting condition (using the semantic wordist), the cue was informative with regard to a semantic category (animal or tool),nd (3) in the emotional orienting condition (using the emotional word list), the cueredicted the emotional category of the target words (negative or neutral). The cueas valid in 80% of all trials, and predicted the wrong location or category in 20% of

he trials.The timing of events in a trial was as follows: a fixation dot was presented for

variable duration (1250–1750 ms) followed by the cue (100 ms). After an inter-al of 1100–1500 ms, the target appeared for 150 ms on the screen. Participantsad to respond within 2000 ms. Feedback was presented for 1000 ms before a newrial started. The feedback consisted of the word “falsch” (wrong) for erroneous and

issed responses, and of the RT in ms for correct responses. The assignment of theue symbols “×” and “+” to a certain location or category was counterbalanced acrossarticipants. There were two experimental sessions, which were at least seven dayspart. Each session included (1) a spatial orienting task with one wordlist (e.g., spa-ial orienting with the semantic list consisting of animal and tool words) and (2) theemantic or emotional orienting task with the other wordlist (e.g., emotional ori-nting with the emotional wordlist consisting of negative and neutral words). Therder of sessions and tasks was counterbalanced across participants. Each word wasresented twice in the invalid cueing condition (once in the left and once in the rightemifield), and eight times in the valid condition to have 20% invalid and 80% validrials. Thus, there were 320 trials in each task, which were split into 4 blocks withhort breaks in between. Stimuli were presented on a computer screen in white on alack background. The words were presented in upper case 3◦ of visual angle to the

eft or right of fixation. The computer monitor was positioned 100 cm in front of thearticipants’ eyes. Participants responded with a right- or left-hand button press.ssignment of the responses (the articles “der” and “die”) to the response hands wasounterbalanced.

A practice block was presented before the experiment with longer stimulusresentation and response times to help the participants adjust to the task. Prioro this practice, to ensure that participants correctly understood the target wordategories, they also (1) produced items for each category or (2) sorted presentedords into the categories (either with or without a prior cue).

.4. EEG recording

Ag–AgCl electrodes were used to record the EEG from 64 scalp positionsccording to the international 10-20 system, see Fig. 2 (Jasper, 1958). Vertical eyeovements were registered with two electrodes positioned above and below the

ight eye. The horizontal electrooculograms were recorded with lateral electrodesrom both eyes. The ground electrode was located on the sternum. Data were refer-nced to the left mastoid, and the right mastoid was actively recorded. Impedancesere below 5 k� for all recordings. Brain vision professional recorder software byrain Products GmbH and the corresponding amplifier Brainamps were used. Sam-ling rate was 500 Hz. Data were stored on hard disk and were filtered online with

bandpass between DC and 250 Hz. Further filtering was only done for graphicalisplay (14 Hz lowpass filter). Data were re-referenced offline to the average of bothastoids.

.5. Data analysis

EEG data were analyzed with the software package EEP (ERP Evaluation Pack-ge EEP 3.2, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig,ermany). Epochs of 1000 ms after stimulus onset were computed according to a00 ms pre-stimulus baseline. All trials were visually inspected for artifacts. An auto-atic rejection of trials exceeding 30 �V for the two eye channels and 40 �V for CZ

nd PZ within a sliding window of 200 ms was additionally applied. Trials were aver-ged for each condition and participant and for each condition across participantsgrand average). After visual inspection of the grand averages and a time-line analy-is with 50 ms time windows, three time windows were chosen for further analysis.hese time windows represent the following deflections: N1-P2 amplitude differ-nce was computed between 140 and 255 ms over occipital electrodes O1, OZ, and

2 to obtain a measure of early visual processing. Here, we analyzed the ampli-

ude difference in accordance with previous attention studies (e.g., Eason, 1981;oldorff, Hansen, & Hillyard, 1987). The frontal P2 was computed as mean ampli-

ude between 190 and 290 ms and for the N400 between 460 and 590 ms. Channelsere grouped into four regions of interest (ROI) with 9 electrodes each (see Fig. 2).

.81 (0.40) 2.32 (0.28) 6.40 (0.69) 5.39 (2.13)

For the statistical analyses of both the behavioral and the EEG data, the softwarepackage SAS (SAS Copyright© SAS Institute Inc., Cary, NC, USA) was used. Repeatedmeasures ANOVAs including validity (valid and invalid cues) and cue type (spatial,semantic, emotional) were computed for the behavioral data. The analysis of theEEG data additionally included the factors region (anterior and posterior) as wellas hemisphere (left and right). Additionally, we compared processing of emotionalto neutral words by calculating repeated measures ANOVAs including the word’semotional quality (negative and neutral) and cue validity (valid and invalid) in theemotional orienting task. The mean numbers of averaged trials per condition arereported in Supplement 2.

3. Results

3.1. Behavioral results

Validly cued targets were reacted to faster than invalidly cuedtargets (see Fig. 3; F(1,19) = 39.73, p < .0001). Validity interacted sig-nificantly with cue type (F(3,57) = 4.64, p < .01). Follow-up analysesyielded shorter RTs for valid compared to invalid trials for eachcue type; however, the effect was stronger for spatial cues (seman-tic cues: F(1,19) = 11.11, p < .01; emotional cues: F(1,19) = 12.15,p < .01; spatial cues, semantic wordlist: F(1,19) = 13.10, p < .001;spatial cues, emotional wordlist: F(1,19) = 25.71, p < .0001).

Accuracy was higher following a valid compared to an invalidcue (see Fig. 3; F(1,19) = 24.02, p < .0001). Validity interacted signif-icantly with cue type (F(3,57) = 5.30, p < .01), indicating that validlycued targets were responded to more accurately in the spatial cue-ing condition, but not in the semantic or emotional cues, where the

Fig. 2. Electrode positions and regions of interest (ROI) in gray. For the analysis ofearly visual potentials, the black encircled electrodes were included.

3124 P. Kanske et al. / Neuropsycholo

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ig. 3. Reaction times (A) and the percentage of trials correctly responded to (B)re displayed for the spatial, semantic, and emotional cueing conditions for the twoordlists (semantic and emotional). Means and S.E.M. are given.

.2. Electrophysiological results

.2.1. Occipital N1-P2We observed a modulation of the N1-P2 amplitude differ-

nce between 140 and 255 ms over occipital electrodes. Forpatially valid cues, the amplitude difference was enlarged com-ared to spatially invalid cues (see Fig. 4; spatial cues, semanticordlist F(1,19) = 7.21, p < .01; spatial cues, emotional wordlist:

(1,19) = 7.63, p < .01). There was no significant difference foremantic and emotional cues.

.2.2. Frontal P2Between 190 and 290 ms after word onset there was an inter-

ction of validity and cue type with hemisphere and region (seeig. 5; F(1,19) = 7.02, p < .01). This interaction indicated an enlarged2 amplitude for emotionally valid compared to invalid cues overeft anterior electrodes (F(1,19) = 4.49, p < .05). No such effect wasresent for any of the other cue types. There were no differencesetween negative and neutral words.

.2.3. N400In the specified N400 time window between 460 and 590 ms,

e found a significant validity by cue type interaction that wasroadly distributed (see Fig. 5; F(1,19) = 11.41, p < .01). For theemantic cues, a validity effect was present over all electrodes,ndicating larger amplitudes for invalid compared to valid cuesF(1,19) = 6.27, p < .05). For emotional cues, we observed an inter-ction of validity and region (F(1,19) = 6.44, p < .05). Emotionallyalid cues yielded reduced N400 amplitudes, but only over ante-ior sites (F(1,19) = 5.99, p < .05). Spatially informative cues alsoodulated the N400 amplitude; in the opposite direction, how-

ver. Here, valid cues elicited larger N400 amplitudes compared tonvalid cues (semantic wordlist: F(1,19) = 12.12, p < .01; emotional

ordlist: F(1,19) = 6.21, p < .05).

In the emotional orienting condition we also observed a signif-

cant effect of the emotional word quality (F(1,19) = 4.88, p < .05)nd an interaction of validity and emotion (F(1,19) = 4.63, p < .05).n the valid condition, emotional words elicited larger N400 ampli-

gia 49 (2011) 3121– 3129

tudes than neutral words (see Fig. 6; F(1,19) = 16.91, p < .001). Thisdifference was not significant in the invalid condition.

4. Discussion

The present study yields new insights into the mechanisms ofattentional orienting. It is the first to show that attention can beactively oriented to the emotional quality of a word. We presenteddifferent types of cues that (1) predict the spatial location, (2) thesemantic category, and (3) the emotional category of subsequentlypresented target words. For each cue type validly cued words wereresponded to faster than invalidly cued words. The ERP data showthat this orienting effect results from the modulation of differ-ent stimulus processing stages. While spatial orienting enhancesamplitudes of early visual potentials, semantic orienting yields anincreased N400. Orienting to the emotional category of a word alsoincreases the N400 amplitude, but also a left anterior P2.

A large number of studies have shown that attention can beoriented to perceptual features such as spatial location or color(Hillyard & Anllo-Vento, 1998; Posner, 1980; Treisman & Gelade,1980). Cristescu and Nobre (2008) showed that the semantic cate-gory of a word can also be selected by attention yielding speededprocessing of these words. The main question we addressed herewas whether attention can be oriented to the emotional status ofword stimuli. The present data clearly show that attention can beoriented to emotion. Abstract cues that predict the emotional cate-gory of a target word speed up word processing if the prediction isvalid and slow down word processing if invalid. The size of thiseffect is smaller than the spatial orienting effect, but compara-ble to semantic orienting (for a similar spatial/semantic orientingdifference see Cristescu & Nobre, 2008). This demonstrates thatparticipants build up expectations of the emotional target wordcategory based on non-emotional cues. This is a highly adaptiveprocess for human communication as it ensures the rapid predic-tion of others’ emotional states via all available cues.

The process that enables this effect acts upon semantic anal-ysis and integration of target words as indexed in the alteredN400 amplitude. This effect is in agreement with data from affec-tive priming (Steinbeis & Koelsch, 2009) and resembles the N400modulation in the semantic orienting condition. Thus, it reflectsthe semantic coherence among words of one emotional category(Bradley & Lang, 1994; Moore et al., 1999; Romney et al., 1997;Wierzbicka, 1992). Cues that predict an emotional category seem toactivate the related semantic network yielding facilitated integra-tion of the upcoming words that fit this category, which is reflectedin the reduced N400 amplitude (Kutas & Federmeier, 2011). Emo-tional orienting additionally acted upon earlier processing stages.We observed a modulation of a left anterior P2, which was largerfor words whose emotional category was validly predicted by thepreceding cue. The interpretation of this P2 effect is not as straight-forward as the N400 effect; however, the following suggestions canbe considered. We know from a number of studies that the ampli-tude of the P2 is, under certain conditions, sensitive to emotionalityin words (Begleiter & Platz, 1969; Begleiter et al., 1979; Bernat et al.,2001; Herbert et al., 2006; Kanske & Kotz, 2007; Schapkin et al.,2000). The most prominent suggestion is that this reflects atten-tional capturing by emotional words. Following this suggestion, thepresent data would indicate that cues signaling the emotional qual-ity of a subsequent target can boost the attention capture effect,which is reflected in an increased P2 amplitude. This “amplifica-tion” view is in line with the well-established interpretation of the

spatial attention effects on early visual potentials (Hillyard & Anllo-Vento, 1998). A second possibility is that early emotion effects in theERP reflect rudimentary semantic stimulus categorization (Kissleret al., 2009). Pre-N400 semantic effects have indeed been reported

P. Kanske et al. / Neuropsychologia 49 (2011) 3121– 3129 3125

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ig. 4. ERPs to validly and invalidly cued target words at occipital electrodes for themotional).

for an extensive review see Dien, 2009). However, this raises theuestion why the P2 effects were not observed in the semanticrienting condition in the present experiment. In consequence,motional words must represent an exceptional semantic categorys has been previously suggested (mainly, however, for emotionords denoting feeling such as “anger, love”, but not for emo-

ional words such as “catastrophe, grave” as used here; Altarriba Bauer, 2004; Altarriba, Bauer, & Benvenuto, 1999; Paivio, Yuille, Madigan, 1968). Even though the present study cannot unequiv-cally define the mechanism underlying the P2 emotion effect, theffect is clearly linked to the orienting of attention to emotion at an

arly stage of word processing.

One question that arises from this early P2 effect is whether suchn effect should have any behavioral consequences. This is difficulto answer as the semantic and emotional orienting effects did not

al, semantic, and emotional cueing conditions for the two wordlists (semantic and

differ in the RT data. However, such a direct comparison is com-plicated. It would require that semantic and emotional categories(animal vs. tool and negative vs. neutral words) are of equivalentsize and coherence. Otherwise one would, metaphorically speak-ing, compare the effects of spatial cues that orient attention tocertain locations of different size. Future research should addressthis open issue which goes beyond the question targeted in thepresent experiment.

We did not observe ERP differences prior to the N400 whendirectly contrasting negative with neutral words in the presentstudy which seems to contradict the observed P2 emotional ori-

enting effects. However, the targeted psychological mechanismsare very different. The orienting effect demonstrates that attentionoriented towards the emotional quality of a word selects charac-teristics of the word processed in the P2 (and N400) time-window,

3126 P. Kanske et al. / Neuropsychologia 49 (2011) 3121– 3129

Fig. 5. ERPs at selected electrodes and difference maps for validly and invalidly cued target words for the spatial, semantic, and emotional cueing conditions for the twowordlists (semantic and emotional).

P. Kanske et al. / Neuropsychologia 49 (2011) 3121– 3129 3127

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ttpntaooateeTwana

ig. 6. ERPs at selected electrodes and difference maps to emotional and neutral woarget words.

hereby yielding facilitated processing of those words matchinghe selected features (e.g., being negative emotional when the cueredicted negative emotion). In contrast, the direct comparison ofegative and neutral words will give information about differen-ial processing of the two categories, which seems to be adaptivelydjusted to the current task demands. There is some evidence thatnly tasks requiring participants to evaluate the emotional qualityf words elicit P2 emotion effects (Begleiter et al., 1979, but seelso Bernat et al., 2001). In the present study the task was to iden-ify the grammatical gender of words. The lack of an early emotionffect may, thus, be due to these non-affective task demands. Inter-stingly, we also found a modulation of the N400 emotion effect.he N400 amplitude was reduced for negative compared to neutral

ords (see also Kanske & Kotz, 2007), however, only in valid cue tri-

ls. This suggests that the integration advantage of emotional overeutral words is abolished when integration is complicated by pre-ctivation of the wrong context (e.g., of “negative emotion” when

receded by cues either validly or invalidly predicting the emotional category of the

a neutral word is presented). In line with this interpretation, thedisappearance of the N400 effect in invalid trials is due to an ampli-tude increase for negative words, not a decrease for neutral words.A limitation regarding the contrast of negative and neutral words isthat words were repeatedly shown in the present experiment. Asrepetition priming effects have been reported for emotional, butnot neutral words, this may have influenced the comparison of thetwo (for details see Luo et al., 2004).

The present data also confirm the results of Cristescu and Nobre(2008). We replicate the behavioral facilitation effect for semanti-cally cued words and also report an N400 amplitude modulation.This is interesting as there are a number of differences between thetwo experimental designs. First, Cristescu and Nobre (2008) and

Cristescu et al. (2006) had participants perform a lexical decisiontask which required the presentation of words and pseudowords.While this is not problematic in the spatial cueing condition as spa-tial cues provide information about the location of the target and

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re, thus, applicable to words and pseudowords, semantic cues onlypply to words, as the pseudowords have no semantic meaning ando not belong to a semantic category. We therefore avoided the usef pseudowords by applying a grammatical gender decision task.econd, Cristescu and Nobre (2008) presented each word only onceo each participant. While this has the advantage that no arbitrarynon-semantic” relations of cue symbols and words can be learned,t also means that comparisons between the spatial and seman-ic cueing conditions had to be between-subject, and comparisonsetween valid and invalid conditions were between-item. For theurrent experiment, words were repeatedly presented in each con-ition, allowing within-subject and within-item comparison. Third,ristescu and Nobre (2008) only analyzed words presented in theight hemifield based on left-hemispheric dominance for word pro-essing. Nevertheless, modulatory influence of attention on wordrocessing should be the same, even if the information needs toe transferred from the right to the left hemisphere. We there-ore included all words in the present data analysis. Despite theseubstantial differences between the studies, the results largelyesemble each other, underscoring the reliability of the semanticrienting effect.

We also observed the modulation of early visual processingn the spatial orienting conditions. The amplified N1-P2 ampli-ude for attended words is in agreement with a large number ofisual attention studies (Eason, 1981; Gomez et al., 1998; Hillyard &angun, 1986; Johannes, Munte, Heinze, & Mangun, 1995; Maenoa

t al., 2004; Shedden & Nordgaard, 2001; van Voorhis & Hillyard,977). Spatial attention also influenced the N400 such that validlyued words elicited larger amplitudes. This pattern replicates pre-ious data (Cristescu & Nobre, 2008; McCarthy & Nobre, 1993) andupports the notion that spatial attention can modulate seman-ic analysis and integration of linguistic stimuli (Miniussi, Marzi, &obre, 2005). Specifically, the reduced N400 amplitude for unat-

ended words has been interpreted as showing that semanticnalysis is not automatic but depends on visual selective atten-ion (e.g., McCarthy & Nobre, 1993). The topographic maps of the400 effects in the present study may suggest that different subpro-esses generating the N400 were involved in the spatial orientingompared to the other conditions as the distributions seem to beore posterior. However, the lack of statistically significant distri-

ution differences makes it difficult to draw definite conclusionsnd renders answer to the question of specific subprocesses touture research.

To conclude, the present study clearly demonstrates that atten-ion can be actively oriented to the emotional category of upcomingord stimuli. Correct expectations about the emotionality of stim-li yield faster responses to these stimuli. Attention also operatest different processing stages. Attentional orienting to emotion wasimilar to orienting to a semantic category in the N400 response, butdditionally entailed an earlier modulation of the P2 component.his early effect indicates attentional selection of stimulus charac-eristics that are processed prior to word semantics and ensureshe rapid detection of potentially threatening situations, an evolu-ionary highly adaptive mechanism.

ppendix A. Supplementary data

Supplementary data associated with this article can be found, inhe online version, at doi:10.1016/j.neuropsychologia.2011.07.022.

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