Abstract
The current study used event-related potentials (ERPs) to examine the ability of task demand in modulating the effect of reward association on the processing of emotional faces. In the learning phase, a high or low reward probability was paired with male or female facial photos of angry, happy, or neutral expressions. Then, in the test phase, task demand was manipulated by asking participants to discriminate the emotionality or the gender of the pre-learned face with no reward at stake. The ERP results in the test phase revealed that the fronto-central N1 (60–100 ms) and the VPP (160–210 ms) components were sensitive to the interaction between reward and emotion, in that the differences between the mean amplitudes for high- and low-reward conditions were significantly larger in the neutral face and angry face conditions than in the happy face condition. Moreover, reward association and task demand showed a significant interaction over the right hemisphere for the N170 component (140–180 ms), with amplitude difference between high- and low-reward conditions being larger in the emotion task than that in the gender task. The later N2pc component exhibited an interaction between task demand and emotionality, in that happy faces elicited larger N2pc difference waves than angry and neutral faces did in the emotion task, but neutral faces elicited larger N2pc difference waves than angry faces did in the gender task. The N2pc effect aligned with behavioral performance. These results suggest that reward association acts as an ‘emotional tagging’ to imbue neutral or angry faces with motivational significance at early time windows. Task demand functions in a top-down way to modulate the deployment of attentional resources at the later attentional selection stage, but does not affect the early automatic processing of either emotion or reward association.
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The data presented in this study are available on request from the corresponding author on reasonable request.
References
Anderson BA (2013) A value-driven mechanism of attentional selection. J Vis 13. https://doi.org/10.1167/13.3.7
Anderson BA, Folk CL (2010) Variations in the magnitude of attentional capture: testing a two-process model. Atten Percept Psychophys 72:342–352. https://doi.org/10.3758/APP.72.2.342
Awh E, Belopolsky AV, Theeuwes J (2012) Top-down versus bottom-up attentional control: a failed theoretical dichotomy. Trends Cogn Sci 16:437–443. https://doi.org/10.1016/j.tics.2012.06.010
Baluch F, Itti L (2011) Mechanisms of top-down attention. Trends Neurosci 34:210–224. https://doi.org/10.1016/j.tins.2011.02.003
Bentin S, Allison T, Puce A, Perez E, McCarthy G (1996) Electrophysiological studies of Face Perception in humans. J Cogn Neurosci 8:551–565. https://doi.org/10.1162/jocn.1996.8.6.551
Bourgeois A, Chelazzi L, Vuilleumier P (2016) How motivation and reward learning modulate selective attention. Prog Brain Res 229:325–342. https://doi.org/10.1016/bs.pbr.2016.06.004
Calvo MG, Beltrán D (2014) Brain lateralization of holistic versus analytic processing of emotional facial expressions. NeuroImage 92:237–247. https://doi.org/10.1016/j.neuroimage.2014.01.048
Calvo MG, Beltran D, Fernandez-Martin A (2014a) Processing of facial expressions in peripheral vision: neurophysiological evidence. Biol Psychol 100:60–70. https://doi.org/10.1016/j.biopsycho.2014.05.007
Calvo MG, Fernández-Martín A, Nummenmaa L (2014b) Facial expression recognition in peripheral versus central vision: role of the eyes and the mouth. Psychol Res 78:180–195. https://doi.org/10.1007/s00426-013-0492-x
Calvo MG, Nummenmaa L (2016) Perceptual and affective mechanisms in facial expression recognition: an integrative review. Cogn Emot 30:1081–1106. https://doi.org/10.1080/02699931.2015.1049124
Chen N, Wei P (2019) Reward association alters brain responses to emotional stimuli: ERP evidence. Int J Psychophysiol 135:21–32. https://doi.org/10.1016/j.ijpsycho.2018.11.001
Chen NX, Wei P (2023) Reward history modulates the Processing of Task-Irrelevant Emotional faces in a demanding Task. Brain Sci 13. https://doi.org/10.3390/brainsci13060874
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Durston AJ, Itier RJ (2021) The early processing of fearful and happy facial expressions is independent of task demands - support from mass univariate analyses. Brain Res 1765:147505. https://doi.org/10.1016/j.brainres.2021.147505
Eimer M (1996) The N2pc component as an indicator of attentional selectivity. Electroencephalogr Clin Neurophysiol 99:225–234. https://doi.org/10.1016/0013-4694(96)95711-9
Eimer M (2000) Effects of face inversion on the structural encoding and recognition of faces. Evidence from event-related brain potentials. Brain Res Cogn Brain Res 10:145–158. https://doi.org/10.1016/s0926-6410(00)00038-0
Eimer M, Holmes A (2002) An ERP study on the time course of emotional face processing. NeuroReport 13:427–431. https://doi.org/10.1097/00001756-200203250-00013
Eimer M, Holmes A (2007) Event-related brain potential correlates of emotional face processing. Neuropsychologia 45:15–31. https://doi.org/10.1016/j.neuropsychologia.2006.04.022
Faul F, Erdfelder E, Buchner A, Lang AG (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41:1149–1160. https://doi.org/10.3758/brm.41.4.1149
Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10:382–390. https://doi.org/10.1016/j.tics.2006.06.011
Feldmann-Wüstefeld T, Schmidt-Daffy M, Schubö A (2011) Neural evidence for the threat detection advantage: differential attention allocation to angry and happy faces. Psychophysiology 48:697–707. https://doi.org/10.1111/j.1469-8986.2010.01130.x
Foti D, Hajcak G, Dien J (2009) Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. Psychophysiology 46:521–530. https://doi.org/10.1111/j.1469-8986.2009.00796.x
George N, Jemel B, Fiori N, Chaby L, Renault B (2005) Electrophysiological correlates of facial decision: insights from upright and upside-down Mooney-face perception. Brain Res Cogn Brain Res 24:663–673. https://doi.org/10.1016/j.cogbrainres.2005.03.017
Gupta R, Hur YJ, Lavie N (2016) Distracted by pleasure: effects of positive versus negative valence on emotional capture under load. Emotion 16:328–337. https://doi.org/10.1037/emo0000112
Hammerschmidt W, Sennhenn-Reulen H, Schacht A (2017) Associated motivational salience impacts early sensory processing of human faces. NeuroImage 156:466–474. https://doi.org/10.1016/j.neuroimage.2017.04.032
Hammerschmidt W, Kagan I, Kulke L, Schacht A (2018a) Implicit reward associations impact face processing: time-resolved evidence from event-related brain potentials and pupil dilations. NeuroImage 179:557–569. https://doi.org/10.1016/j.neuroimage.2018.06.055
Hammerschmidt W, Kulke L, Broering C, Schacht A (2018b) Money or smiles: independent ERP effects of associated monetary reward and happy faces. PLoS ONE 13:e0206142. https://doi.org/10.1371/journal.pone.0206142
Hickey C, Chelazzi L, Theeuwes J (2010a) Reward changes salience in human vision via the anterior cingulate. J Neurosci 30:11096–11103. https://doi.org/10.1523/JNEUROSCI.1026-10.2010
Hickey C, Chelazzi L, Theeuwes J (2010b) Reward guides vision when it’s your thing: trait reward-seeking in reward-mediated visual priming. PLoS ONE 5:e14087. https://doi.org/10.1371/journal.pone.0014087
Hickey C, Chelazzi L, Theeuwes J (2011) Reward has a residual impact on target selection in visual search, but not on the suppression of distractors. Vis Cogn 19:117–128. https://doi.org/10.1080/13506285.2010.503946
Holmes A, Bradley BP, Kragh Nielsen M, Mogg K (2009) Attentional selectivity for emotional faces: evidence from human electrophysiology. Psychophysiology 46:62–68. https://doi.org/10.1111/j.1469-8986.2008.00750.x
Hu K, Padmala S, Pessoa L (2013) Interactions between reward and threat during visual processing. Neuropsychologia 51:1763–1772. https://doi.org/10.1016/j.neuropsychologia.2013.05.025
Hudson A, Durston AJ, McCrackin SD, Itier RJ (2021) Emotion, gender and gaze discrimination tasks do not differentially Impact the neural Processing of Angry or Happy Facial Expressions-a Mass Univariate ERP Analysis. Brain Topogr 34:813–833. https://doi.org/10.1007/s10548-021-00873-x
Jia Y, Cui L, Pollmann S, Wei P (2021) The interactive effects of reward expectation and emotional interference on cognitive conflict control: an ERP study. Physiol Behav 234:113369. https://doi.org/10.1016/j.physbeh.2021.113369
Jonas J, Jacques C, Liu-Shuang J, Brissart H, Colnat-Coulbois S, Maillard L, Rossion B (2016) A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials. Proc Natl Acad Sci U S A 113:E4088–4097. https://doi.org/10.1073/pnas.1522033113
Kiss M, Driver J, Eimer M (2009) Reward priority of visual target singletons modulates event-related potential signatures of attentional selection. Psychol Sci 20:245–251. https://doi.org/10.1111/j.1467-9280.2009.02281.x
Krebs RM, Boehler CN, Woldorff MG (2010) The influence of reward associations on conflict processing in the Stroop task. Cognition 117:341–347. https://doi.org/10.1016/j.cognition.2010.08.018
Lochy A, de Heering A, Rossion B (2019) The non-linear development of the right hemispheric specialization for human face perception. Neuropsychologia 126:10–19. https://doi.org/10.1016/j.neuropsychologia.2017.06.029
Luck SJ (2005) Ten simple rules for designing ERP experiments. Event-related potentials: A methods handbook 262083337
Luck SJ (2006) The Operation of Attention–Millisecond by Millisecond–Over the First Half Second
Luck SJ, Hillyard SA (1994) Electrophysiological correlates of feature analysis during visual search. Psychophysiology 31:291–308. https://doi.org/10.1111/j.1469-8986.1994.tb02218.x
Luo W, Feng W, He W, Wang NY, Luo YJ (2010) Three stages of facial expression processing: ERP study with rapid serial visual presentation. NeuroImage 49:1857–1867. https://doi.org/10.1016/j.neuroimage.2009.09.018
Marini F, Marzi T, Viggiano MP (2011) Wanted! The effects of reward on face recognition: electrophysiological correlates. Cogn Affect Behav Neurosci 11:627–643. https://doi.org/10.3758/s13415-011-0057-7
Müller-Bardorff M, Schulz C, Peterburs J, Bruchmann M, Mothes-Lasch M, Miltner W, Straube T (2016) Effects of emotional intensity under perceptual load: an event-related potentials (ERPs) study. Biol Psychol 117:141–149. https://doi.org/10.1016/j.biopsycho.2016.03.006
Nummenmaa L, Calvo MG (2015) Dissociation between recognition and detection advantage for facial expressions: a meta-analysis. Emotion 15:243–256. https://doi.org/10.1037/emo0000042
Palermo R, Rhodes G (2007) Are you always on my mind? A review of how face perception and attention interact. Neuropsychologia 45:75–92. https://doi.org/10.1016/j.neuropsychologia.2006.04.025
Park HRP, Kostandyan M, Boehler CN, Krebs RM (2019) Winning smiles: signalling reward by overlapping and non-overlapping emotional valence differentially affects performance and neural activity. Neuropsychologia 122:28–37. https://doi.org/10.1016/j.neuropsychologia.2018.11.018
Paul K, Pourtois G (2017) Mood congruent tuning of reward expectation in positive mood: evidence from FRN and theta modulations. Soc Cogn Affect Neurosci 12:765–774
Paul K, Pourtois G, Harmon-Jones E (2020) Modulatory effects of positive mood and approach motivation on reward processing: two sides of the same coin? Cognitive. Affect Behav Neurosci 20:236–249
Pessoa L (2015) Multiple influences of reward on perception and attention. Vis Cogn 23:272–290. https://doi.org/10.1080/13506285.2014.974729
Ping W, Guanlan K, Jinhong D, Chunyan G (2014) Monetary incentives modulate the processing of emotional facial expressions: an ERP study. Acta Physiol Sinica 46:437
Pollmann S, Estocinova J, Sommer S, Chelazzi L, Zinke W (2016) Neural structures involved in visual search guidance by reward-enhanced contextual cueing of the target location. NeuroImage 124:887–897. https://doi.org/10.1016/j.neuroimage.2015.09.040
Raymond JE, O’Brien JL (2009) Selective visual attention and motivation: the consequences of value learning in an attentional blink task. Psychol Sci 20:981–988. https://doi.org/10.1111/j.1467-9280.2009.02391.x
Rossi V, Vanlessen N, Bayer M, Grass A, Pourtois G, Schacht A (2017) Motivational salience modulates early visual cortex responses across Task Sets. J Cogn Neurosci 29:968–979. https://doi.org/10.1162/jocn_a_01093
Rossion B (2014) Understanding face perception by means of human electrophysiology. Trends Cogn Sci 18:310–318. https://doi.org/10.1016/j.tics.2014.02.013
Rossion B, Joyce CA, Cottrell GW, Tarr MJ (2003) Early lateralization and orientation tuning for face, word, and object processing in the visual cortex. NeuroImage 20:1609–1624. https://doi.org/10.1016/j.neuroimage.2003.07.010
Smith E, Weinberg A, Moran T, Hajcak G (2013) Electrocortical responses to NIMSTIM facial expressions of emotion. Int J Psychophysiol 88:17–25. https://doi.org/10.1016/j.ijpsycho.2012.12.004
Steinberg C, Bröckelmann AK, Rehbein M, Dobel C, Junghöfer M (2013) Rapid and highly resolving associative affective learning: convergent electro- and magnetoencephalographic evidence from vision and audition. Biol Psychol 92:526–540. https://doi.org/10.1016/j.biopsycho.2012.02.009
Vuilleumier P, Pourtois G (2007) Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45:174–194. https://doi.org/10.1016/j.neuropsychologia.2006.06.003
Wang Y, Luo Y-j (2005) Standardization and Assessment of College Students’ facial expression of emotion. Chin J Clin Psych 13:396–398
Wei P, Ji L (2021) Reward expectation modulates N2pc for target selection: electrophysiological evidence. Psychophysiology 58:e13837. https://doi.org/10.1111/psyp.13837
Wei P, Kang G (2014) Task relevance regulates the interaction between reward expectation and emotion. Exp Brain Res 232:1783–1791. https://doi.org/10.1007/s00221-014-3870-8
Wei P, Kang G, Ding J, Guo C (2014) Monetary incentives modulate the processing of emotional facial expressions: an ERP study. Acta Physiol Sinica 46:437
Wentura D, Müller P, Rothermund K (2014) Attentional capture by evaluative stimuli: gain- and loss-connoting colors boost the additional-singleton effect. Psychon Bull Rev 21:701–707. https://doi.org/10.3758/s13423-013-0531-z
Williams LM, Palmer D, Liddell BJ, Song L, Gordon E (2006) The ‘when’ and ‘where’ of perceiving signals of threat versus non-threat. NeuroImage 31:458–467. https://doi.org/10.1016/j.neuroimage.2005.12.009
Wronka E, Walentowska W (2011) Attention modulates emotional expression processing. Psychophysiology 48:1047–1056. https://doi.org/10.1111/j.1469-8986.2011.01180.x
Wu L, Müller HJ, Zhou X, Wei P (2019) Differential modulations of reward expectation on implicit facial emotion processing: ERP evidence. Psychophysiology 56:e13304. https://doi.org/10.1111/psyp.13304
Yao S, Ding C, Qi S, Yang D (2014) Value associations of emotional faces can modify the anger superiority effect: behavioral and electrophysiological evidence. Soc Cogn Affect Neurosci 9:849–856. https://doi.org/10.1093/scan/nst056
Yokoyama T, Padmala S, Pessoa L (2015) Reward learning and negative emotion during rapid attentional competition. Front Psychol 6:269. https://doi.org/10.3389/fpsyg.2015.00269
Zhang D, Luo W, Luo Y (2013) Single-trial ERP analysis reveals facial expression category in a three-stage scheme. Brain Res 1512:78–88. https://doi.org/10.1016/j.brainres.2013.03.044
Zhang D, Liu Y, Wang L, Ai H, Luo Y (2017) Mechanisms for attentional modulation by threatening emotions of fear, anger, and disgust. Cogn Affect Behav Neurosci 17:198–210. https://doi.org/10.3758/s13415-016-0473-9
Zhou X, Du B, Wei Z, He W (2019) Attention capture of non-target emotional faces: an evidence from reward learning. Front Psychol 10:3004. https://doi.org/10.3389/fpsyg.2019.03004
Funding
This work was supported by the National Natural Science Foundation of China (31971030, 31470979), the Youth Beijing Scholar Project, the Support Project of High-level Teachers in Beijing Municipal Universities in the Period of 13th Five-year Plan, and the Capacity Building for Sci-Tech Innovation-Fundamental Scientific Research Funds (131-20530290058).
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Conceptualization: Ning-Xuan Chen and Ping Wei; Methodology: Ning-Xuan Chen; Validation: Ning-Xuan Chen and Ping Wei; Formal analysis: Ning-Xuan Chen; Investigation: Ning-Xuan Chen; Data curation: Ning-Xuan Chen and Ping Wei; Writing—original draft preparation: Ning-Xuan Chen; Writing—review and editing: Ning-Xuan Chen and Ping Wei; Visualization: Ning-Xuan Chen; Supervision: Ping Wei; All authors read and approved the final manuscript.
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Chen, NX., Wei, P. Task demand modulates the effects of reward learning on emotional stimuli. Cogn Neurodyn (2024). https://doi.org/10.1007/s11571-024-10082-4
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DOI: https://doi.org/10.1007/s11571-024-10082-4