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1 3 Exp Brain Res DOI 10.1007/s00221-014-3870-8 RESEARCH ARTICLE Task relevance regulates the interaction between reward expectation and emotion Ping Wei · Guanlan Kang Received: 23 October 2013 / Accepted: 3 February 2014 © Springer-Verlag Berlin Heidelberg 2014 Introduction The ability to monitor and adjust one’s behavior accord- ing to the current task goal is vital for human cognitive function. It has been demonstrated recently that moti- vational factors (e.g., food, monetary incentive) have a strong influence on task performance by increasing task concentration and engagement (see Chelazzi et al. 2013; Chiew and Braver 2011; Pessoa 2009; Pessoa and Engel- mann 2010 for reviews). For example, when subjects were informed by an explicit cue or instructions that they would receive a monetary reward that is contingent upon their performance in a visual search task, their detection of a rarely appearing target improved (Navalpakkam et al. 2009). Although many studies have demonstrated the effect of monetary incentives on performance in cognitive tasks such as spatial orienting (Baines et al. 2011; Small et al. 2005; Theeuwes and Belopolsky 2012), attentional blink (Bijleveld et al. 2011), attentional capture (Hickey et al. 2010a, b, 2011; Kiss et al. 2009; Locke and Braver 2008; Wang et al. 2013), and conflict control (Krebs et al. 2010; Padmala and Pessoa 2011), little is known about the impact of motivational cues on the processing of emo- tional stimuli. Motivation and emotion are highly related concepts within the domain of affect since most of the goals we pur- sued in daily life are emotionally meaningful (Berridge and Robinson 2003; Chiew and Braver 2011; Lang and Bradley 2010; Rolls 2002). That is, we are motivated to obtain out- comes that are pleasurable and to avoid outcomes that are aversive. It has been suggested that motivation and emotion may share common processing mechanisms and may oper- ate in highly similar ways (Baxter and Murray 2002; Pes- soa 2009). Neuroimaging studies have demonstrated that imagining a pleasant scene (Costa et al. 2010) or viewing Abstract In the present study, we investigated the impact of reward expectation on the processing of emotional facial expression using a cue-target paradigm. A cue indicat- ing the reward condition of each trial (incentive vs. non- incentive) was followed by the presentation of a picture of an emotional face, the target. Participants were asked to discriminate the emotional expression of the target face in Experiment 1, to discriminate the gender of the target face in Experiment 2, and to judge a number superimposed on the center of the target face as even or odd in Experiment 3, rendering the emotional expression of the target face as task relevant in Experiment 1 but task irrelevant in Experi- ments 2 and 3. Faster reaction times (RTs) were observed in the monetary incentive condition than in the non-incentive condition, demonstrating the effect of reward on facilitating task concentration. Moreover, the reward effect (i.e., RTs in non-incentive conditions versus incentive conditions) was larger for emotional faces than for neutral faces when emo- tional expression was task relevant but not when it was task irrelevant. The findings suggest that top-down incentive motivation biased attentional processing toward task-rel- evant stimuli, and that task relevance played an important role in regulating the influence of reward expectation on the processing of emotional stimuli. Keywords Reward · Emotion · Facial expression · Happy · Anger P. Wei (*) · G. Kang Beijing Key Laboratory of Learning and Cognition, Department of Psychology, Capital Normal University, Beijing 100048, China e-mail: [email protected] G. Kang Department of Psychology, Center for Brain and Cognition Sciences, Peking University, Beijing 100871, China

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Page 1: Task relevance regulates the interaction between reward expectation and emotion

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Exp Brain ResDOI 10.1007/s00221-014-3870-8

REsEaRch aRtIclE

Task relevance regulates the interaction between reward expectation and emotion

Ping Wei · Guanlan Kang

Received: 23 October 2013 / accepted: 3 February 2014 © springer-Verlag Berlin heidelberg 2014

Introduction

the ability to monitor and adjust one’s behavior accord-ing to the current task goal is vital for human cognitive function. It has been demonstrated recently that moti-vational factors (e.g., food, monetary incentive) have a strong influence on task performance by increasing task concentration and engagement (see chelazzi et al. 2013; chiew and Braver 2011; Pessoa 2009; Pessoa and Engel-mann 2010 for reviews). For example, when subjects were informed by an explicit cue or instructions that they would receive a monetary reward that is contingent upon their performance in a visual search task, their detection of a rarely appearing target improved (Navalpakkam et al. 2009). although many studies have demonstrated the effect of monetary incentives on performance in cognitive tasks such as spatial orienting (Baines et al. 2011; small et al. 2005; theeuwes and Belopolsky 2012), attentional blink (Bijleveld et al. 2011), attentional capture (hickey et al. 2010a, b, 2011; Kiss et al. 2009; locke and Braver 2008; Wang et al. 2013), and conflict control (Krebs et al. 2010; Padmala and Pessoa 2011), little is known about the impact of motivational cues on the processing of emo-tional stimuli.

Motivation and emotion are highly related concepts within the domain of affect since most of the goals we pur-sued in daily life are emotionally meaningful (Berridge and Robinson 2003; chiew and Braver 2011; lang and Bradley 2010; Rolls 2002). that is, we are motivated to obtain out-comes that are pleasurable and to avoid outcomes that are aversive. It has been suggested that motivation and emotion may share common processing mechanisms and may oper-ate in highly similar ways (Baxter and Murray 2002; Pes-soa 2009). Neuroimaging studies have demonstrated that imagining a pleasant scene (costa et al. 2010) or viewing

Abstract In the present study, we investigated the impact of reward expectation on the processing of emotional facial expression using a cue-target paradigm. a cue indicat-ing the reward condition of each trial (incentive vs. non-incentive) was followed by the presentation of a picture of an emotional face, the target. Participants were asked to discriminate the emotional expression of the target face in Experiment 1, to discriminate the gender of the target face in Experiment 2, and to judge a number superimposed on the center of the target face as even or odd in Experiment 3, rendering the emotional expression of the target face as task relevant in Experiment 1 but task irrelevant in Experi-ments 2 and 3. Faster reaction times (Rts) were observed in the monetary incentive condition than in the non-incentive condition, demonstrating the effect of reward on facilitating task concentration. Moreover, the reward effect (i.e., Rts in non-incentive conditions versus incentive conditions) was larger for emotional faces than for neutral faces when emo-tional expression was task relevant but not when it was task irrelevant. the findings suggest that top-down incentive motivation biased attentional processing toward task-rel-evant stimuli, and that task relevance played an important role in regulating the influence of reward expectation on the processing of emotional stimuli.

Keywords Reward · Emotion · Facial expression · happy · anger

P. Wei (*) · G. Kang Beijing Key laboratory of learning and cognition, Department of Psychology, capital Normal University, Beijing 100048, chinae-mail: [email protected]

G. Kang Department of Psychology, center for Brain and cognition sciences, Peking University, Beijing 100871, china

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a loved one’s picture (aron et al. 2005) activates reward circuitry in the human brain. additionally, tsukiura and cabeza (2008) found that memory of face-name associa-tions was enhanced for smiling faces relative to faces with a neutral expression. they concluded that smiling faces were recognized as a socially rewarding signal, resulting in enhancement of performance in the task.

although the above studies pointed to correlations and potentially shared brain mechanisms for reward and emo-tion, especially positive emotion, they did not manipulate or investigate the impact of reward directly on the pro-cessing of emotional stimuli. two recent studies tested the effects of explicit manipulations of the emotional content of task stimuli and a monetary reward on memory encod-ing in human subjects to investigate the brain mechanisms involved in the interaction between reward and emotional experience in memory formation processes (shigemune et al. 2010; Wittmann et al. 2008). In the first study, Witt-mann et al. (2008) asked participants to perform an inci-dental memory encoding task in which they were presented with negative, neutral, or positive pictures and then asked to decide whether there were people on these pictures or not. Before each trial, a cue indicated whether task perfor-mance in the trial would be rewarded. the subjects showed better subsequent recollection of the stimuli that were associated with a pre-trial cue indicating a performance-based reward than the stimuli that were not associated with a reward. Moreover, the corrected hit rate was higher for positive rewarded pictures than for positive unrewarded pictures, but the corrected hit rate for rewarded pictures did not differ from the hit rate for unrewarded pictures for negative and neutral pictures. the functional magnetic res-onance imaging (fMRI) data showed an enhancement of reward-related activity in the ventral striatum with presen-tation of emotionally positive but not emotionally negative stimuli. the results suggested that the reward system may only interact with memory formation of positive emotional stimuli. In a subsequent study, shigemune et al. (2010) investigated the brain mechanisms of intentional encod-ing of negative or neutral emotional pictures under high and low reward conditions. their imaging results showed enhanced activation of the right hippocampus as a main effect of emotion and a main effect of reward, suggest-ing that the right hippocampus may integrate the effects of emotional processing (in the amygdala) and monetary reward processing (in the orbitofrontal cortex) on episodic memory encoding.

anatomically, the amygdala is strongly associated with the processing of visual emotional stimuli (Britton et al. 2006; hariri et al. 2002; Phan et al. 2004; Zald 2003). It has close connections with brain areas that have been iden-tified as being involved in the processing of reward stimuli,

including the ventral striatum (alheid 2003; McDonald 1998) and the substantia nigra/ventral tegmental area (sN/Vta, Price and haber 1981), suggesting a strong reciprocal influence between reward and emotion (Baxter and Murray 2002). these functional and anatomical find-ings raise the possibility that reward (e.g., monetary com-pensation) may have a direct influence on the processing of emotional stimuli.

It is noteworthy that the emotional content of target pic-tures in the aforementioned two studies was task irrelevant given that the aims were to investigate whether emotional processing occurs automatically and unintentionally. some studies have emphasized the specific ability of emotional, especially negative, stimuli to capture subjects’ attention regardless of its task relevance (e.g., hodsoll et al. 2011). For example, subjects show delayed response times (Rts) to the ink color of negative words relative to that of neutral words in the emotional stroop paradigm (compton et al. 2003; Etkin et al. 2006; han et al. 2013). however, other recent behavioral and neurocognitive evidence suggests that emotionally distracting stimuli may create interference only when they are relevant to the task (lichtenstein-Vidne et al. 2012; Okon-singer et al. 2013; Vogt et al. 2013), sug-gesting that participants can ignore task-irrelevant emotion-ally charged distractions to a certain extent. since the role of monetary reward in facilitating task performance was accomplished by improving concentration upon the task-relevant aspect of the stimuli, it is of theoretical impor-tance to investigate the impact of monetary reward on the processing of emotional stimuli of different task-relevance statuses.

the goal of the present study was to manipulate mon-etary incentives and the task relevance of emotional facial expressions to determine the influence of incentive on the processing of emotional stimuli. We employed a cue-target paradigm (Fig. 1) in which the cue indicated whether the trial was incentivized or not and the target was a picture of a face with an emotionally positive, neutral, or nega-tive expression. Participants were asked to discriminate the emotional expression of the target picture in Experi-ment 1, to discriminate the gender of the emotional face in Experiment 2, and to discriminate whether a digital number superimposed on the center of the face was even or odd in Experiment 3. thus, the emotional expression of the target was task relevant in Experiment 1 but task irrel-evant in Experiments 2 and 3. Participants were rewarded for fast and correct responses in the incentivized condi-tion. We hypothesized that monetary incentive would ben-efit performance by decreasing Rts in general in all three tasks. Moreover, we hypothesized that reward expectation may impact facilitation of processing differently with posi-tive versus negative facial expression targets and may do

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so only when the emotional facial expressions are task relevant.

Methods

Participants

Independent groups of undergraduate and graduate stu-dents participated in Experiment 1 (N = 18, 16 females, 18–23 years of age), Experiment 2 (N = 19, 16 females, 20–25 years of age), and Experiment 3 (N = 20, 18 females, 19–27 years of age). all 57 participants were right-handed with normal or corrected-to-normal vision and had no known cognitive or neurological disorders. Data from one participant in Experiment 2 and two participants in Experiment 3 were discarded due to excessive error rates (>20 %). this study was approved by the Ethics commit-tee of the Department of Psychology at capital Normal University, and all participants gave informed consent prior to the experiments in accordance with the Declaration of helsinki.

Design and materials

a 2 × 3 within-participant factorial design was used for each experiment, with the first factor being the trial type (incen-tive or non-incentive) and the second factor being the emo-tional expression of the target face (happy, neutral, or angry). the stimuli consisted of 90 pictures from the chinese Facial affective Picture system (cFaPs) whose valence and arousal levels were rated on a 9-point likert scale (Wang and luo 2005). the cFaPs was chosen to avoid the cultural bias seen when the International affective Picture system was used with chinese participants (huang and luo 2004). the stimulus series included 30 positive (happy) faces, 30 neutral (calm) faces, and 30 negative (angry) faces, with 15 male and 15 female faces in each condition. Positive and negative stimuli were matched according to arousal level and did not differ significantly in their arousing character [mean (M) ± standard deviation (sD): positive = 6.2 ± 0.75; nega-tive = 6.0 ± 1.10]. the three categories of pictures differed significantly from one another in their normative valence rat-ing [M ± sD: positive = 6.6 ± 0.47; neutral = 4.6 ± 0.21; negative = 2.9 ± 0.39, p < .001]. Each picture occupied a

Fig. 1 a Example of trial sequence in Experiments 1 and 2. the task in Experiment 1 was to discriminate the emotional expression of the target face, while the task in Experiment 2 was to discriminate the gender of the target face. b Example target facial stimulus used in

Experiment 3, with the same trial sequence as in Experiments 1 and 2 and the task being to judge the number superimposed on the face as even or odd

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visual angle of 4.93° (horizontally) × 5.99° (vertically) viewed at a distance of 65 cm.

Procedures

the presentation of stimuli and recording of Rts and error rates were controlled by Presentation software (http://nbs.neuro-bs.com/). Participants were seated in a dimly lit and sound-attenuated room. at the start of each trial (Fig. 1a), a white fixation cross (visual angle, 0.4° × 0.4°) appeared at the center of the black screen for 500 ms, fol-lowed by an incentive cue, ¥, or non-incentive cue, # (vis-ual angle, 2.3° × 2.3°) for 800 ms. after a variable cue-target interval (ctI) of 500–1,000 ms, the target stimulus (visual angle, 4.93° × 5.99°) was presented for 300 ms. the purpose of using variable ctIs was to prevent partici-pants from forming time-based expectations for the target.

In Experiment 1, participants were instructed to record whether the target stimulus conveyed a happy, neutral, or angry expression as quickly and accurately as possible using three response buttons (left, down, and right direc-tional keys on the computer keyboard) under the right index finger, right middle finger, and right ring finger, respectively. the assignment of response buttons to the target facial expressions (happy, neutral, and angry) was counter-balanced over participants.

In Experiment 2, the trial sequence and the presenta-tion of stimuli were the same as in Experiment 1, except that participants were instructed to record the gender of the face as quickly and accurately as possible by pressing the left button of the computer mouse for male face and the right button for female face. the target faces were the same as in Experiment 1. In Experiment 3, a number (ran-domly selected from zero to nine) measuring 0.6° × 0.7° in visual angle was presented over the nose area of the target face stimulus (see Fig. 1b). Participants were instructed to respond to the number as quickly and accurately as possi-ble by pressing the left button of the computer mouse for odd numbers and the right button for even numbers. the assignments of the response buttons were also counter-bal-anced over participants in Experiments 2 and 3.

after each target stimulus was displayed, the fixa-tion point was shown again until the participant entered a response (maximum, 1,500 ms), followed by the presen-tation of a feedback stimulus for 500 ms. For non-incen-tive trials, a filled gray circle feedback stimulus indicated a correct response and an empty gray circle indicated an incorrect response. For incentive trials, a picture of one chinese Yuan coin was presented following responses that were correct and faster than the baseline Rt (deter-mined in the practice session, see below), a filled gray cir-cle was presented following responses that were correct but slower than the baseline Rt, and an empty gray circle

was presented following incorrect responses as in the non-incentive trials. the fixation point was then presented for the inter-trial interval (1,000–1,500 ms).

the experiment series had 480 trials in total, with each experimental condition having 80 trials. all experimental trials were divided into four sessions, with each session consisted of 120 trials (and each condition having 20 trials) in pseudo-randomized order.

Participants received 24 practice trials before the experiment. During the practice phase, participants were informed that the cue pictures were task irrelevant and were asked to ignore them. they were required to respond as quickly and accurately as possible to the corresponding tar-get stimuli in each experiment. there were only correct and false feedbacks (no coin feedback) during the practice ses-sion. the filled or empty gray circle was presented to indi-cate a right or wrong response, respectively. the averaged reaction time for each participant during the practice phase was used as that participant’s baseline Rt.

after the practice session, participants were informed of the meaning of the cue picture and the presentation rule of the coin feedback in the formal experiment. they were informed that they would gain an additional 10 chinese Yuan in reward if they managed to get the coin feedback in >75 % of the total incentive trials (240 trials).

Data analysis

Incorrect responses were excluded from the Rt analysis, and Rts more than three standard deviations above or below the mean in each experimental condition for each participant were discarded as “outliers.” analyses of variance (aNO-Vas) were conducted on Rt data, with trial type (incen-tive vs. non-incentive) and target facial expression (happy, neutral, vs. angry) serving as within-participants factors, followed by Bonferroni-corrected pairwise comparisons. the effect of the reward incentive was computed for each target facial expression as the difference between incen-tive trial Rts and non-incentive trial Rts, and the resultant values were subjected to planned pairwise comparisons. an aNOVa of the reward effect was conducted with target emotion (happy, neutral, or angry) as the within-participant factor and the experiment (1, 2, or 3) as the between-partici-pant factor. a one-way aNOVa with emotion as the within-participant factor was performed for each experiment. all statistical analyses were performed using sPss software. In all cases, a p < .05 was considered significant.

Results

Mean Rts and response error rates in each experimen-tal condition are reported in table 1 and Fig. 2 for each

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experiment. In accordance with the exclusionary crite-rion stated in the Methods, 1.2, 1.1, and 1.3 % of the total data points in Experiments 1, 2, and 3, respectively, were excluded as outliers.

Experiment 1

an aNOVa of Rts revealed a main effect of trial type [F(1, 17) = 34.85, p < .001], with participants having faster Rts to incentive trials (M = 583 ms) than to non-incentive trials (M = 637 ms), as well as a main effect of target facial expression [F(2, 34) = 25.74, p < .001]. Bonferroni-corrected pairwise comparisons revealed that happy-face Rts (M = 565 ms) were faster than neutral-face Rts (M = 639 ms) and angry-face Rts (M = 627 ms; both p < .001), but there was no difference between neutral- and angry-face Rts (p > .1). Importantly, the interaction between trial type and target facial expression was signifi-cant [F(2, 34) = 6.22, p < .01].

Planned pairwise comparisons showed that the incen-tive effect was significantly larger for happy-face targets (p < .005) and for angry-face targets (p < .05) than for

neutral-face targets. the incentive effect was not different between angry- and happy-face targets [t(17) < 1].

analyses of error rates revealed a significant main effect of target facial expression [F(2, 34) = 16.11, p < .001]. Bonferroni-corrected pairwise comparisons showed that participants made more errors in the neutral-face (8.3 %) and angry-face (11.7 %) conditions than in the happy-face condition (4.3 %; both p < .05). No other effects or interac-tions reached significance.

Experiment 2

a 2 (trial type: incentive, non-incentive) × 3 (target facial expression: happy, neutral, angry) aNOVa of Rts revealed a main effect of trial type [F(1, 17) = 14.27, p < .005], with participants posting faster Rts in incentive trials (M = 475 ms) than in non-incentive trials (M = 532 ms), as well as a main effect of target facial expression [F(2, 34) = 36.16, p < .001]. Bonferroni-corrected pairwise comparisons showed that Rts in the happy-face condi-tion (M = 491 ms) were significantly faster than Rts in the angry-face condition (M = 503 ms; p < .001), and Rts

Table 1 Mean reaction times (ms) and error rates (%) with standard errors in parentheses in terms of the experimental conditions for each experiment

Incentive Non-incentive

happy Neutral angry happy Neutral angry

Experiment 1 Rts (sE) 533 (14) 620 (17) 597 (13) 597 (11) 657 (16) 657 (15)

Error rates (sE) 4.0 (0.7) 8.6 (1.4) 11.6 (1.8) 4.7 (0.6) 7.9 (1.2) 11.7 (1.8)

Experiment 2 Rts (sE) 463 (13) 485 (14) 476 (12) 519 (20) 543 (23) 533 (20)

Error rates (sE) 7.2 (0.9) 10.5 (1.0) 9.0 (0.8) 6.9 (1.0) 11.0 (1.0) 7.2 (0.9)

Experiment 3 Rts (sE) 526 (17) 518 (16) 527 (20) 556 (17) 557 (18) 558 (17)

Error rates (sE) 8.6 (0.9) 9.0 (0.9) 9.2 (1.0) 7.6 (1.0) 6.2 (0.9) 7.0 (1.0)

Fig. 2 Rts (ms) with standard errors in terms of the experimental conditions for each experiment. the letter (a, b, or c in white square) in the middle of each emotional condition refers to the effect of tar-get facial expression, with Rts increasing in alphabetic order and the same letters indicating similar effects of emotional expression within

each experiment. the number on top of each emotional condition refers to the magnitude of the reward effect, with reward effect mag-nitude increasing along with numerical order and the same numbers indicating similar reward effects within each experiment

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in both the happy-face (p < .001) and angry-face (p < .01) conditions were significantly faster than Rts in the neutral-face condition (M = 514 ms). however, unlike Experiment 1, there was not a significant interaction between trial type and target facial expression [F(2, 34) < 1], indicating com-parable reward effect magnitudes across the different facial expression conditions.

analyses of error rates revealed a significant main effect of target facial expression [F(2, 34) = 10.87, p < .001]. Bonferroni-corrected pairwise comparisons then showed that participants made more errors in the neutral-face condition (10.7 %) than in either the angry-face con-dition (8.1 %; p < .005) or the happy-face condition (7.1 %; p < .005). No other effects or interactions reached significance.

Experiment 3

an aNOVa of Rts showed a significant main effect of trial type [F(1, 17) = 27.41, p < .001], with faster Rts being observed in incentive trials (M = 524 ms) than in non-incentive trials (M = 557 ms). there was not a signifi-cant effect of target facial expression or a significant trial type × target facial expression interaction.

analyses of error rates revealed a significant main effect of trial type [F(1, 17) = 14.00, p < .005], with more errors being committed in non-incentive trials (8.9 %) than in incentive trials (6.9 %). No other main effects or interac-tions reached significance.

Overall analysis of Rts across Experiments 1, 2, and 3

an aNOVa of the reward effect with target emotion (happy, neutral, or angry) as the within-participant factor and the experiment (1, 2, or 3) as the between-participant factor indicated that the emotional expression of the target image was not a significant main effect [F(2, 102) < 1]. however, experiment as a between-participant factor did interact with the emotion of the target picture [F(4, 102) = 4.41, p < .005], indicating that the three experi-ments yielded different reward effect patterns across the different target emotions.

a one-way aNOVa for the reward effect with emotion as the within-participant factor showed a significant main effect in Experiment 1 [F(2, 34) = 6.07, p < .01], with the reward effect being larger for happy-face targets than for neutral-face targets (p < .005), larger for angry-face targets than for neutral-face targets (p < .05), and similar between angry- and happy-face targets (p > .1). similar one-way aNOVas showed no significant effect of emotion in either Experiment 2 [F(2, 34) < 1] or Experiment 3 [F(2, 34) = 1.22, p > .1], indicating comparable reward effects for the different target emotions in Experiments 2 and 3.

Discussion

By asking participants to perform variable tasks with emo-tional facial expression stimuli under monetary incentive or non-incentive conditions, the current study demonstrated that reward generally facilitates task performance and that reward has differential impacts on the processing of emo-tional and neutral facial expressions only when the emo-tional content is task relevant. In all three of our experi-ments, there was a main effect of trial type, with faster Rts being observed under incentive conditions relative to non-incentive conditions, replicating the effect of mon-etary reward on facilitating task performance (Baines et al. 2011; Kiss et al. 2009; Krebs et al. 2010; Navalpakkam et al. 2009; Padmala and Pessoa 2011; small et al. 2005; theeuwes and Belopolsky 2012). this result is consistent with the notion that motivational incentive improves cogni-tive control or executive function (locke and Braver 2008; savine and Braver 2010) and biases the focus of selec-tive attention toward goal-directed aspects of task stimuli (Bijleveld et al. 2009; Pochon et al. 2002; Veling and aarts 2010; Waugh and Gotlib 2008).

By using an explicit recognition task on emotional expression in Experiment 1 and a gender discrimination task in Experiment 2, we found significant main effects of emotional facial expressions in both an explicit recognition task (Experiment 1) and a gender discrimination task not related to emotional expression (Experiment 2), such that happy faces were categorized faster than neutral and angry faces in both tasks. It is well documented that negative faces, such as threatening or angry faces, take attentional priority in an involuntary manner since they carry threat-related signals and are important for survival (Dimberg and Öhman 1996; Eastwood et al. 2003; Eimer and holmes 2002; Ekman 1973; Morris et al. 1998; Öhman et al. 2001; Vuilleumier and Driver 2007; Williams 2006). however, in categorization tasks where a facial expression must be con-sciously and explicitly identified, a consistent recognition advantage has been found for happy faces using behavio-ral measures (e.g., calvo and lundqvist 2008; calvo and Marrero 2009; leppänen and hietanen 2004; Palermo and coltheart 2004; tottenham et al. 2009), an eye-track-ing technique (calvo and Nummenmaa 2009), and event-related potential (ERP) recordings (calvo and Beltrán 2013; liu et al. 2013). Moreover, the recognition advantage of happy expressions is not due simply to physical stimulus factors, such as an open mouth, since they can be identified more accurately not only with open mouths and exposed teeth, but also with closed-mouth smiles (tottenham et al. 2009). Using the ERP technique, calvo and Beltrán (2013) showed that conscious expression recognition and the typi-cal happy-face advantage depend on later response selec-tion, rather than early processing of affective valence. the

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present study went further, suggesting that this happy-face advantage exists even when the stimuli are being classified by gender and the emotional expression of the face is there-fore irrelevant to the classification task.

however, when participants were required to judge a number superimposed on the target face as even or odd in Experiment 3, the valence of the facial expressions had no impact on the participants’ Rts. this finding is consistent with previous studies showing the importance of task rel-evance in determining whether emotional stimuli capture attention or not (Eimer and holmes 2007; lichtenstein-Vidne et al. 2012; Vogt et al. 2013). For example, Eimer and holmes (2007) presented participants two vertical lines in the central visual field with two flanking fearful or neutral faces in the periphery and asked the participants either to determine the emotional valence of the face (emo-tion task) or to judge whether the two lines’ lengths were identical or different (lines task). ERP results showed that emotional faces elicited an enhanced positivity relative to neutral faces in the emotion task, but this effect was com-pletely eliminated in the lines task. In the current Experi-ment 3, although the face was presented in the center of the display, participants could focus on the number judging task without being affected by the emotional valence of the face in the background, suggesting a strong top-down bias in focusing on task-relevant aspects of stimuli.

Moreover, although the present study demonstrated con-sistent results of monetary incentive facilitating behavioral performance across different tasks, the more interesting finding is that the magnitude of the reward effect was larger with emotional faces than with neutral faces, but only when the emotionality of the faces was task relevant in Experi-ment 1. as mentioned in the Introduction, both anatomical (Britton et al. 2006; hariri et al. 2002; Phan et al. 2004; Zald 2003) and functional (shigemune et al. 2010; Witt-mann et al. 2008) evidence suggests that reward and emo-tion may have close reciprocal influences, yet the mecha-nism involved has not been resolved.

When Wittmann et al. (2008) manipulated reward status (reward, neutral) in an incidental emotional encoding task performed in an fMRI scanner, they found that reward-related activity in the ventral striatum was enhanced by concurrent presentation of emotionally positive but not emotionally negative stimuli, suggesting that the reward system and memory formation interacted only for the posi-tive stimuli. conversely, in Experiment 1, we found an enhanced reward effect for the processing of both positive and negative faces, relative to processing of neutral faces. however, there are key differences in experimental manip-ulations between our study and Wittman and colleagues’ work. they used incidental emotional encoding paradigm, in which the emotional content of the target picture was task irrelevant, whereas in our Experiment 1, the emotional

expression of the target image was task relevant. Moreover, Wittmann et al. (2008) were focused on memory processes rather than rapid categorization and discrimination. It is possible that interactions between reward and emotion pro-cessing in the ventral striatum and amygdala can be influ-enced or mediated by other brain areas responsible for task control.

the possibility that task set may play an important role in regulating the interaction between reward and emotion is supported by a recent ERP study (Kaltwasser et al. 2013) in which participants were asked to perform semantic cat-egorization of emotional and neutral words under differ-ent incentive conditions, with the emotional content of the words being task irrelevant. Independent effects of reward and the target’s emotional valence on ERPs were observed. consistent with the current behavioral study, the findings in both of these prior studies suggest that task relevance may have a strong influence on the way reward and emo-tion interact.

In conclusion, by asking participants to perform tasks on emotional face stimuli under incentivized and non-incentivized conditions, the current study demonstrated that reward generally facilitates task performance and that reward has differential impact upon the processing of emo-tional faces and neutral faces only when the emotionality of the faces was task relevant. Focusing processing prior-ity on task-defined aspects of the stimuli was manifested under monetary incentive conditions and task relevance played an important role in regulating reward-emotion interaction.

Acknowledgments this study was supported by grants from the Natural science Foundation of china (31000502, 31200790). Elec-tronic mail concerning this study should be addressed to Dr. Ping Wei, [email protected].

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