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Smiling faces and cash bonuses: Exploring common affective coding across positive and negative emotional and motivational stimuli using fMRI

  • Haeme R. P. Park
  • Mariam Kostandyan
  • C. Nico Boehler
  • Ruth M. Krebs
Article

Abstract

Although it is clear that emotional and motivational manipulations yield a strong influence on cognition and behaviour, these domains have mostly been investigated in independent research lines. Therefore, it remains poorly understood how far these affective manipulations overlap in terms of their underlying neural activations, especially in light of previous findings that suggest a shared valence mechanism across multiple affective processing domains (e.g., monetary incentives, primary rewards, emotional events). This is particularly interesting considering the commonality between emotional and motivational constructs in terms of their basic affective nature (positive vs. negative), but dissociations in terms of instrumentality, in that only reward-related stimuli are typically associated with performance-contingent outcomes. Here, we aimed to examine potential common neural processes triggered by emotional and motivational stimuli in matched tasks within participants using functional magnetic resonance imaging (fMRI). Across tasks, we found shared valence effects in the ventromedial prefrontal cortex and left inferior frontal gyrus (part of dorsolateral prefrontal cortex), with increased activity for positive and negative stimuli, respectively. Despite this commonality, emotion and reward tasks featured differential behavioural patterns in that negative valence effects (performance costs) were exclusive to emotional stimuli, while positive valence effects (performance benefits) were only observed for reward-related stimuli. Overall, our data suggest a common affective coding mechanism across different task domains and support the idea that monetary incentives entail signed basic valence signals, above and beyond the instruction to perform both gain and loss trials as accurately as possible to maximise the outcome.

Keywords

Emotion Motivation Reward Saliency Affect fMRI 

Notes

Acknowledgements

This study was supported by a starting grant of the European Research Council (ERC) under the Horizon 2020 framework (Grant No. 636110 awarded to R.M.K.).

Supplementary material

13415_2018_587_MOESM1_ESM.docx (1.1 mb)
ESM 1 (DOCX 1107 kb)

References

  1. Bartra, O., McGuire, J. T., & Kable, J. W. (2013). The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. NeuroImage, 76, 412–427.  https://doi.org/10.1016/j.neuroimage.2013.02.063 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Belopolsky, A. V., Devue, C., & Theeuwes, J. (2011). Angry faces hold the eyes. Visual Cognition, 19(1), 27–36.  https://doi.org/10.1080/13506285.2010.536186 CrossRefGoogle Scholar
  3. Bradley, M. M. (2000). Emotion and motivation. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (pp. 602–642). New York, NY: Cambridge University Press.Google Scholar
  4. Brett, M., Anton, J.-L., Valabregue, R., & Poline, J.-B. (2002). Region of interest analysis using an SPM toolbox. Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2–6, Sendai, Japan. Available on CD-ROM in NeuroImage, 16(2), abstract 497.Google Scholar
  5. Brodeur, M. B., Guérard, K., & Bouras, M. (2014). Bank of Standardized Stimuli (BOSS) Phase II: 930 new normative photos. PLOS ONE, 9(9), e106953.  https://doi.org/10.1371/journal.pone.0106953 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010). Dopamine in motivational control: Rewarding, aversive, and alerting. Neuron, 68, 815–834.  https://doi.org/10.1016/j.neuron.2010.11.022 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bunzeck, N., & Düzel, E. (2006). Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron, 51(3), 369–379.CrossRefPubMedGoogle Scholar
  8. Burgdorf, J., & Panksepp, J. (2006). The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews, 30, 173–187.  https://doi.org/10.1016/j.neubiorev.2005.06.001 CrossRefPubMedGoogle Scholar
  9. Chib, V. S., Rangel, A., Shimojo, S., & O’Doherty, J. P. (2009). Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. The Journal of Neuroscience, 29(39), 12315–12320.  https://doi.org/10.1523/JNEUROSCI.2575-09.2009 CrossRefPubMedGoogle Scholar
  10. Chiew, K. S., & Braver, T. S. (2014). Dissociable influences of reward motivation and positive emotion on cognitive control. Cognitive, Affective, & Behavioral Neuroscience, 14, 509–529.  https://doi.org/10.3758/s13415-014-0280-0 CrossRefGoogle Scholar
  11. Clithero, J. A., & Rangel, A. (2014). Informatic parcellation of the network involved in the computation of subjective value. Social Cognitive and Affective Neuroscience, 9(9), 1289–1302.  https://doi.org/10.1093/scan/nst106 CrossRefPubMedGoogle Scholar
  12. Dreisbach, G. (2006). How positive affect modulates cognitive control: The costs and benefits of reduced maintenance capability. Brain and Cognition, 60(1), 11–19.  https://doi.org/10.1016/j.bandc.2005.08.003 CrossRefPubMedGoogle Scholar
  13. Eastwood, J. D., Smilek, D., & Merikle, P. M. (2003). Negative facial expression captures attention and disrupts performance. Perception & Psychophysics, 65(3), 352–358.  https://doi.org/10.3758/BF03194566 CrossRefGoogle Scholar
  14. Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles K. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage, 25(4), 1325–1335.CrossRefPubMedGoogle Scholar
  15. Engelmann, J. B., Damaraju, E., Padmala, S., & Pessoa, L. (2009). Combined effects of attention and motivation on visual task performance: transient and sustained motivational effects. Frontiers in Human Neuroscience, 3, 4.  https://doi.org/10.3389/neuro.09.004.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fischer, H., Wright, C. I., Whalen, P. J., McInerney, S. C., Shin, L. M., & Rauch, S. L. (2003). Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study. Brain Research Bulletin, 59(5), 387–392.  https://doi.org/10.1016/S0361-9230(02)00940-1 CrossRefPubMedGoogle Scholar
  17. FitzGerald, T. H., Seymour, B., & Dolan, R. J. (2009). The role of human orbitorontal cortex in value comparison for incommensurable objects. The Journal of Neuroscience, 29(26), 8388–8395.  https://doi.org/10.1523/JNEUROSCI.0717-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fox, E., Russo, R., & Dutton, K. (2002). Attentional bias for threat: Evidence for delayed disengagement from emotional faces. Cognition & Emotion, 16(3), 355–379.  https://doi.org/10.1080/02699930143000527 CrossRefGoogle Scholar
  19. Fröber, K., & Dreisbach, G. (2014). The differential influences of positive affect, random reward, and performance-contingent reward on cognitive control. Cognitive, Affective, & Behavioral Neuroscience, 14, 530–547.  https://doi.org/10.3758/s13415-014-0259-x CrossRefGoogle Scholar
  20. Glover, G. H., Li, T. Q., & Ress, D. (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magnetic Resonance in Medicine, 44(1), 162–167.  https://doi.org/10.1002/1522-2594(200007)44 CrossRefPubMedGoogle Scholar
  21. Grill-Spector, K., & Sayres, R. (2008). Object recognition. Current Directions in Psychological Science, 17(2), 73–79.CrossRefGoogle Scholar
  22. Guillory, S. A., & Bujarski, K. A. (2014). Exploring emotions using invasive methods: Review of 60 years of human intracranial electrophysiology. Social Cognitive and Affective Neuroscience, 9(12), 1880–1889.  https://doi.org/10.1093/scan/nsu002 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Guitart-Masip, M., Huys, Q. J. N., Fuentemilla, L., Dayan, P., Duzel, E., & Dolan, R.J. (2012). Go and no-go learning in reward and punishment: Interactions between affect and effect. NeuroImage, 62(1), 154–166.  https://doi.org/10.1016/j.neuroimage.2012.04.024 CrossRefPubMedGoogle Scholar
  24. Hinrichs, H., Scholz, M., Tempelmann, C., Woldorff, M. G., Dale, A. M., & Heinze, H. J. (2000). Deconvolution of event-related fMRI responses in fast-rate experimental designs: Tracking amplitude variations. Journal of Cognitive Neuroscience, 12(Suppl 2), 76–89.  https://doi.org/10.1162/089892900564082 CrossRefPubMedGoogle Scholar
  25. Horvitz, J. C. (2000). Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience, 96(4), 651–656.  https://doi.org/10.1016/S0306-4522(00)00019-1 CrossRefPubMedGoogle Scholar
  26. Iacovella, V., & Hasson, U. (2011). The relationship between BOLD signal and autonomic nervous system functions: Implications for processing of “physiological noise”. Magnetic Resonance Imaging, 29(10), 1338–1345.  https://doi.org/10.1016/j.mri.2011.03.006 CrossRefPubMedGoogle Scholar
  27. JASP Team (2017). JASP (Version 0.8.2)[Computer software]. Available at: https://jasp-stats.org/.
  28. Jeffreys, H. (1961). Theory of probability (3rd ed.). Oxford, UK: Oxford University Press.Google Scholar
  29. Kanske, P., & Kotz, S. A. (2011). Emotion speeds up conflict resolution: A new role for the ventral anterior cingulate cortex? Cerebral Cortex, 21(4), 911–919.  https://doi.org/10.1093/cercor/bhq157 CrossRefPubMedGoogle Scholar
  30. Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. The Journal of Neuroscience, 17(11), 4302–4311.Google Scholar
  31. Kasper, L., Bollmann, S., Diaconescu, A.O., Hutton, C., Heinzle, J., Iglesias, S.,… Pruessmann, K. P. (2017). The PhysIO Toolbox for modeling physiological noise in fMRI data. Journal of Neuroscience Methods, 276, 56–72.  https://doi.org/10.1016/j.jneumeth.2016.10.019 CrossRefPubMedGoogle Scholar
  32. Knutson, B., Katovich, K., & Suri, G. (2014). Inferring affect from fMRI data. Trends in Cognitive Sciences, 18(8), 422–428.  https://doi.org/10.1016/j.tics.2014.04.006 CrossRefPubMedGoogle Scholar
  33. Kobayashi, S., Nomoto, K., Watanabe, M., Hikosaka, O., Schultz, W., & Sakagami, M. (2006). Influences of rewarding and aversive outcomes on activity in macaque lateral prefrontal cortex. Neuron, 51(6), 861–870.CrossRefPubMedGoogle Scholar
  34. Kohn, N., Eickhoff, S. B., Scheller, M., Laird, A. R., Fox, P. T., & Habel, U. (2014). Neural network of cognitive emotion regulation—An ALE meta-analysis and MACM analysis. NeuroImage, 87, 345–355.  https://doi.org/10.1016/j.neuroimage.2013.11.001 CrossRefPubMedGoogle Scholar
  35. Krebs, R. M., Boehler, C. N., Roberts, K. C., Song, A. W., & Woldorff, M. G. (2012). The involvement of the dopaminergic midbrain and cortico-striatal-thalamic circuits in the integration of reward prospect and attentional task demands. Cerebral Cortex, 22, 607–615.  https://doi.org/10.1093/cercor/bhr134 CrossRefPubMedGoogle Scholar
  36. Krebs, R. M., Boehler, C. N., & Woldorff, M. G. (2010). The influence of reward associations on conflict processing in the Stroop task. Cognition, 117(3), 341–347.  https://doi.org/10.1016/j.cognition.2010.08.018 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Krebs, R. M., Heipertz, D., Schuetze, H., & Düzel, E. (2011). Novelty increases the mesolimbic functional connectivity of the substantia nigra/ventral tegmental area (SN/VTA) during reward anticipation: Evidence from high-resolution fMRI. NeuroImage, 58, 647–655.  https://doi.org/10.1016/j.neuroimage.2011.06.038 CrossRefPubMedGoogle Scholar
  38. Krieglmeyer, R., Deutsch, R., De Houwer, J., & De Raedt, R. (2010). Being moved: Valence activates approach-avoidance behavior independently of evaluation and approach-avoidance intentions. Psychological Science, 21(4), 607–613.  https://doi.org/10.1177/0956797610365131 CrossRefPubMedGoogle Scholar
  39. Kringelbach, M. L. (2005). The human orbitofrontal cortex: Linking reward to hedonic experience. Nature Reviews Neuroscience, 6, 691–702.  https://doi.org/10.1038/nrn1748 CrossRefPubMedGoogle Scholar
  40. Lang, P. J., & Bradley, M. M. (2008). Appetitive and defensive motivation is the substrate of emotion. In A. J. Elliot (Ed.), Handbook of approach and avoidance motivation (pp. 51–66). New York, NY: Psychology Press.Google Scholar
  41. Levy, D. J., & Glimcher, P. W. (2011). Comparing apples and oranges: Using reward-specific and reward-general subjective value representation in the brain. The Journal of Neuroscience, 31(41), 14693–14707.  https://doi.org/10.1523/JNEUROSCI.2218-11.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Levy, D. J., & Glimcher, P. W. (2012). The root of all value: A neural common currency for choice. Current Opinion in Neurobiology, 22(6), 1027–1038.  https://doi.org/10.1016/j.conb.2012.06.001 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lindquist, K. A., Satpute, A. B., Wager, T. D., Weber, J., & Barrett, L. F. (2015). The brain basis of positive and negative affect: Evidence from a meta-analysis of the human neuroimaging literature. Cerebral Cortex, 26(5), 1910–1922.  https://doi.org/10.1093/cercor/bhv001 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lindström, B. R., & Bohlin, G. (2011). Emotion processing facilitates working memory performance. Cognition and Emotion, 25(7), 1196–1204.  https://doi.org/10.1080/02699931.2010.527703 CrossRefPubMedGoogle Scholar
  45. Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011). Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies. Neuroscience & Biobehavioral Reviews, 35(5), 1219–1236.  https://doi.org/10.1016/j.neubiorev.2010.12.012 CrossRefGoogle Scholar
  46. Locke, H. S., & Braver, T. S. (2008). Motivational influences on cognitive control: Behavior, brain activation, and individual differences. Cognitive, Affective, & Behavioral Neuroscience, 8(1), 99–112.  https://doi.org/10.3758/CABN.8.1.99 CrossRefGoogle Scholar
  47. Marsh, A. A., Ambady, N., & Kleck, R. E. (2005). The effects of fear and anger facial expressions on approach- and avoidance-related behaviors. Emotion, 5(1), 119–124.  https://doi.org/10.1037/1528-3542.5.1.119 CrossRefPubMedGoogle Scholar
  48. Matsumoto, M., & Hikosaka, O. (2009). Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature, 459, 837–842.  https://doi.org/10.1038/nature08028 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Miller, G. A., Crocker, L. D., Spielberg, J. M., Infantolino, Z. P., & Heller, W. (2013). Issues in localization of brain function: The case of lateralized frontal cortex in cognition, emotion, and psychopathology. Frontiers in Integrative Neuroscience, 7, 2.  https://doi.org/10.3389/fnint.2013.00002 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Notebaert, W., & Braem, S. (2015). Parsing the effects of reward on cognitive control. In T. S. Braver (Ed.), Motivation and cognitive control (pp. 105–122). New York, NY: Psychology Press.Google Scholar
  51. O’Doherty, J. P. (2007). Lights, camembert, action! The role of human orbitofrontal cortex in encoding stimuli, rewards, and choices. Annals of the New York Academy of Sciences, 1121, 254–272.  https://doi.org/10.1196/annals.1404.036 CrossRefPubMedGoogle Scholar
  52. Olive, D. J. (2017). Linear regression. Cham, Switzerland: Springer International Publishing.  https://doi.org/10.1007/978-3-319-55252-1 CrossRefGoogle Scholar
  53. Padmala, S., & Pessoa, L. (2011). Reward reduces conflict by enhancing attentional control and biasing visual cortical processing. Journal of Cognitive Neuroscience, 23(11), 3419–3432.  https://doi.org/10.1162/jocn_a_00011 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Paul, K., Walentowska, W., Bakic, J., Dondaine, T., & Pourtois, G. (2017). Modulatory effects of happy mood on performance monitoring: Insights from error-related brain potentials. Cognitive, Affective, & Behavioral Neuroscience, 17, 106–123.  https://doi.org/10.3758/s13415-016-0466-8 CrossRefGoogle Scholar
  55. Peña-Gómez, C., Vidal-Piñeiro, D., Clemente, I. C., Pascual-Leone, Á., Bartrés-Faz, D., & Aleman, A. (2011). Down-regulation of negative emotional processing by transcranial direct current stimulation: Effects of personality characteristics. PLoS ONE, 6(7), e22812.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pessoa, L. (2009). How do emotion and motivation direct executive control? Trends in Cognitive Sciences, 13(4), 160–166.  https://doi.org/10.1016/j.tics.2009.01.006 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rolls, E. T. (2000). Précis of The brain and emotion. Behavioral and Brain Sciences, 23, 177–234.  https://doi.org/10.1017/S0140525X00512424 CrossRefPubMedGoogle Scholar
  58. Rowe, G., Hirsh, J. B., & Anderson, A. K. (2007). Positive affect increases the breadth of attentional selection. Proceedings of the National Academy of Sciences, 104(1), 383–388.  https://doi.org/10.1073/pnas.0605198104 CrossRefGoogle Scholar
  59. Rutledge, R. B., Skandali, N., Dayan, P., & Dolan, R. J. (2014). A computational and neural model of momentary subjective well-being. Proceedings of the National Academy of Sciences, 111(33), 12252–12257.  https://doi.org/10.1073/pnas.1407535111 CrossRefGoogle Scholar
  60. Rutledge, R. B., Skandali, N., Dayan, P., & Dolan, R. J. (2015). Dopaminergic modulation of decision making and subjective well-being. The Journal of Neuroscience, 35(27), 9811–9822.  https://doi.org/10.1523/JNEUROSCI.0702-15.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sarkheil, P., Goebel, R., Schneider, F., & Mathiak, K. (2013). Emotion unfolded by motion: A role for parietal lobe in decoding dynamic facial expressions. Social Cognitive and Affective Neuroscience, 8(8), 950–957.CrossRefPubMedGoogle Scholar
  62. Simon, H. A. (1959). Theories of decision-making in economics and behavioral science. The American Economic Review, 49(3), 253–283.Google Scholar
  63. Smith, D. V., Hayden, B. Y., Truong, T.-K., Song, A. W., Platt, M. L., & Huettel, S. A. (2010). Distinct value signals in anterior and posterior ventromedial prefrontal cortex. The Journal of Neuroscience, 30(7), 2490–2495.  https://doi.org/10.1523/JNEUROSCI.3319-09.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Theeuwes, J., & Van der Stigchel, S. (2006). Faces capture attention: Evidence from inhibition of return. Visual Cognition, 13(6), 657–665.  https://doi.org/10.1080/13506280500410949 CrossRefGoogle Scholar
  65. Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T.A.,… Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242–249.  https://doi.org/10.1016/j.psychres.2008.05.006 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wagenmakers, E-J. (2007). A practical solution to the pervasive problems of p values. Psychonomic Bulletin & Review, 14(5), 779–804.  https://doi.org/10.3758/BF03194105 CrossRefGoogle Scholar
  67. Wallis, J. D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annual Review of Neuroscience, 30, 31–56.  https://doi.org/10.1146/annurev.neuro.30.051606.094334 CrossRefPubMedGoogle Scholar
  68. Weaver, M. D., & Lauwereyns, J. (2011). Attentional capture and hold: The oculomotor correlates of the change detection advantage for faces. Psychological Research, 75(1), 10–23.  https://doi.org/10.1007/s00426-010-0284-5 CrossRefPubMedGoogle Scholar
  69. Wise, R. A. (2004). Dopamine, learning and motivation. Nature Reviews Neuroscience, 5, 1–12.  https://doi.org/10.1038/nrn1406 CrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Haeme R. P. Park
    • 1
  • Mariam Kostandyan
    • 1
  • C. Nico Boehler
    • 1
  • Ruth M. Krebs
    • 1
  1. 1.Department of Experimental PsychologyGhent UniversityGhentBelgium

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