Advertisement

Reward elicits cognitive control over emotional distraction: Evidence from pupillometry

  • Amy T. Walsh
  • David Carmel
  • Gina M. GrimshawEmail author
Article
  • 79 Downloads

Abstract

Attention is biased toward emotional stimuli, even when they are irrelevant to current goals. Motivation, elicited by performance-contingent reward, reduces behavioural emotional distraction. In emotionally neutral contexts, reward is thought to encourage use of a proactive cognitive control strategy, altering anticipatory attentional settings to more effectively suppress distractors. The current preregistered study investigates whether a similar proactive shift occurs even when distractors are highly arousing emotional images. We monitored pupil area, an online measure of both cognitive and emotional processing, to examine how reward influences the time course of control. Participants (n = 110) identified a target letter flanking an irrelevant central image. Images were meaningless scrambles on 75% of trials; on the remaining 25%, they were intact positive (erotic), negative (mutilation), or neutral images. Half the participants received financial rewards for fast and accurate performance, while the other half received no performance-contingent reward. Emotional distraction was greater than neutral distraction, and both were attenuated by reward. Consistent with behavioural findings, pupil dilation was greater following emotional than neutral distractors, and dilation to intact distractors (regardless of valence) was decreased by reward. Although reward did not enhance tonic pupil dilation (an index of sustained proactive control), exploratory analyses showed that reward altered the time course of control—eliciting a sharp, rapid, increase in dilation immediately preceding stimulus onset (reflecting dynamic use of anticipatory control), that extended until well after stimulus offset. These findings suggest that reward alters the time course of control by encouraging proactive preparation to rapidly disengage from emotional distractors.

Keywords

Emotion Motivation Distraction Cognitive control Reward Pupillometry 

Notes

Acknowledgements

The authors would like to acknowledge contributions from Al Abenoja for technical assistance, Dr. Sanjay Manohar for sharing MATLAB code for pupillometry preprocessing analysis, Dr. Michael C. Hout for sharing code for experiment programming, Cathryn Bjarnesen for assistance with experiment planning, and Dr. Christel Devue for assistance with programming the experiment.

Our experiment preregistration (osf.io/jd96p/), materials, data, analyses, and code are available on Open Science Framework: osf.io/yhkdr

Funding

Research was supported by a grant from the Royal Society of New Zealand Marsden Fund (VUW-1307) to Gina Grimshaw and David Carmel. Findings were reported at the meeting of the Society for Psychophysiological Research, Vienna, October, 2017. Disclosure of interest statement: The authors report no conflict of interest.

Supplementary material

13415_2018_669_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 13 kb)
13415_2018_669_MOESM2_ESM.docx (15 kb)
ESM 2 (DOCX 14 kb)

References

  1. Armstrong, R. A. (2014). When to use the Bonferroni correction. Ophthalmic and Physiological Optics, 34(5), 502–508. doi: https://doi.org/10.1111/opo.12131 CrossRefPubMedGoogle Scholar
  2. Beatty, J., & Lucero-Wagoner, B. (2000). The pupillary system. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (pp. 142–162). New York, NY: Cambridge University Press.Google Scholar
  3. Botvinick, M., & Braver, T. (2015). Motivation and cognitive control: From behaviour to neural mechanism. Annual Review of Psychology, 66(1), 83–113. doi: https://doi.org/10.1146/annurev-psych-010814-015044 CrossRefPubMedGoogle Scholar
  4. Bouret, S., & Richmond, B. J. (2015). Sensitivity of locus coeruleus neurons to reward value for goal-directed actions. Journal of Neuroscience, 35(9), 4005–4014. doi: https://doi.org/10.1523/JNEUROSCI.4553-14.2015 CrossRefPubMedGoogle Scholar
  5. Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45(4), 602–607. doi: https://doi.org/10.1111/j.1469-8986.2008.00654.x CrossRefPubMedPubMedCentralGoogle Scholar
  6. Braver, T. S. (2012). The variable nature of cognitive control: A dual mechanisms framework. Trends in Cognitive Sciences, 16(2), 106–113. doi: https://doi.org/10.1016/j.tics.2011.12.010 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Braver, T. S., Gray, J. R., & Burgess, G. C. (2007). Explaining the many varieties of working memory variation: Dual mechanisms of cognitive control. In A. R. A. Conway, C. Jarrold, M. J. Kane, A. Miyake, & J. N. Towse (Eds.), Variation in working memory (pp. 76–106). Oxford, UK: Oxford University Press.Google Scholar
  8. Braver, T. S., Paxton, J. L., Locke, H. S., & Barch, D. M. (2009). Flexible neural mechanisms of cognitive control within human prefrontal cortex. Proceedings of the National Academy of Sciences, 106(18), 7351–7356. doi: https://doi.org/10.1073/pnas.0808187106 CrossRefGoogle Scholar
  9. Brisson, J., Mainville, M., Mailloux, D., Beaulieu, C., Serres, J., & Sirois, S. (2013). Pupil diameter measurement errors as a function of gaze direction in corneal reflection eyetrackers. Behaviour Research Methods, 45(4), 1322–1331. doi: https://doi.org/10.3758/s13428-013-0327-0 CrossRefGoogle Scholar
  10. Brosch, T., Pourtois, G., Sander, D., & Vuilleumier, P. (2011). Additive effects of emotional, endogenous, and exogenous attention: Behavioural and electrophysiological evidence. Neuropsychologia, 49(7), 1779–1787. doi: https://doi.org/10.1016/j.neuropsychologia.2011.02.056 CrossRefPubMedGoogle Scholar
  11. Bruyer, R., & Brysbaert, M. (2011). Combining speed and accuracy in cognitive psychology: Is the inverse efficiency score (IES) a better dependent variable than the mean reaction time (RT) and the percentage of errors (PE)?. Psychologica Belgica, 51(1), 5–13. doi: https://doi.org/10.5334/pb-51-1-5 CrossRefGoogle Scholar
  12. Bugg, J. M., & Crump, M. J. (2012). In support of a distinction between voluntary and stimulus-driven control: A review of the literature on proportion congruent effects. Frontiers in Psychology, 3, 367. doi: https://doi.org/10.3389/fpsyg.2012.00367 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Carver, C. S., & White, T. L. (1994). Behavioural inhibition, behavioural activation, and affective responses to impending reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology, 67(2), 319. doi: https://doi.org/10.1037/0022-3514.67.2.319 CrossRefGoogle Scholar
  14. Chatham, C. H., Frank, M. J., & Munakata, Y. (2009). Pupillometric and behavioural markers of a developmental shift in the temporal dynamics of cognitive control. Proceedings of the National Academy of Sciences, 106(14), 5529–5533. doi: https://doi.org/10.1073/pnas.0810002106 CrossRefGoogle Scholar
  15. Chevalier, N., Martis, S. B., Curran, T., & Munakata, Y. (2015). Metacognitive processes in executive control development: The case of reactive and proactive control. Journal of Cognitive Neuroscience, 27(6), 1125–1136. doi: https://doi.org/10.1162/jocn_a_00782 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chiew, K. S., & Braver, T. S. (2013). Temporal dynamics of motivation-cognitive control interactions revealed by high-resolution pupillometry. Frontiers in Psychology, 4, 15. doi: https://doi.org/10.3389/fpsyg.2013.00015 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chiew, K. S., & Braver, T. S. (2014). Dissociable influences of reward motivation and positive emotion on cognitive control. Cognitive, Affective, & Behavioural Neuroscience, 14(2), 509–529. doi: https://doi.org/10.3758/s13415-014-0280-0 CrossRefGoogle Scholar
  18. Cohen, N., Moyal, N., & Henik, A. (2015). Executive control suppresses pupillary responses to aversive stimuli. Biological Psychology, 112, 1–11. doi: https://doi.org/10.1016/j.biopsycho.2015.09.006 CrossRefPubMedGoogle Scholar
  19. Coull, J. T., Büchel, C., Friston, K. J., & Frith, C. D. (1999). Noradrenergically mediated plasticity in a human attentional neuronal network. NeuroImage, 10(6), 705–715. doi: https://doi.org/10.1006/nimg.1999.0513 CrossRefPubMedGoogle Scholar
  20. Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioural, and biomedical sciences. Behaviour Research Methods, 39, 175–191. doi: https://doi.org/10.3758/BF03193146 CrossRefGoogle Scholar
  21. Fröber, K., & Dreisbach, G. (2014). The differential influences of positive affect, random reward, and performance-contingent reward on cognitive control. Cognitive, Affective & Behavioural Neuroscience, 14(2), 530–547. doi: https://doi.org/10.3758/s13415-014-0259-x CrossRefGoogle Scholar
  22. Fröber, K., & Dreisbach, G. (2016). How performance (non-)contingent reward modulates cognitive control. Acta Psychologica, 168, 65–77. doi: https://doi.org/10.1016/j.actpsy.2016.04.008 CrossRefPubMedGoogle Scholar
  23. Geng, J. J. (2014). Attentional mechanisms of distractor suppression. Current Directions in Psychological Science, 23(2), 147–153. doi: https://doi.org/10.1177/0963721414525780 CrossRefGoogle Scholar
  24. Grimshaw, G. M., Kranz, L. S., Carmel, D., Moody, R. E., & Devue, C. (2018). Contrasting reactive and proactive control of emotional distraction. Emotion. doi: https://doi.org/10.1037/emo000033
  25. Gupta, R., Hur, Y. J., & Lavie, N. (2016). Distracted by pleasure: Effects of positive versus negative valence on emotional capture under load. Emotion, 16(3), 328–337. doi: https://doi.org/10.1037/emo0000112 CrossRefPubMedGoogle Scholar
  26. Hefer, C., & Dreisbach, G. (2016). The motivational modulation of proactive control in a modified version of the AX-continuous performance task: Evidence from cue-based and prime-based preparation. Motivation Science; Washington, 2(2), 116–134. doi: https://doi.org/10.1037/mot0000034
  27. Heitz, R. P., Schrock, J. C., Payne, T. W., & Engle, R. W. (2008). Effects of incentive on working memory capacity: Behavioural and pupillometric data. Psychophysiology, 45(1), 119–129. doi: https://doi.org/10.1111/j.1469-8986.2007.00605.x PubMedGoogle Scholar
  28. Henderson, R. R., Bradley, M. M., & Lang, P. J. (2014). Modulation of the initial light reflex during affective picture viewing. Psychophysiology, 51(9), 815–818. doi: https://doi.org/10.1111/psyp.12236 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jackson, I., & Sirois, S. (2009). Infant cognition: Going full factorial with pupil dilation. Developmental Science, 12(4), 670–679. doi: https://doi.org/10.1111/j.1467-7687.2008.00805.x CrossRefPubMedGoogle Scholar
  30. Jones, N. P., Siegle, G. J., & Mandell, D. (2015). Motivational and emotional influences on cognitive control in depression: A pupillometry study. Cognitive, Affective, & Behavioural Neuroscience, 15(2), 263–275. doi: https://doi.org/10.3758/s13415-014-0323-6 CrossRefGoogle Scholar
  31. Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89(1), 221–234. doi: https://doi.org/10.1016/j.neuron.2015.11.028 CrossRefPubMedGoogle Scholar
  32. Kahneman, D. (1973). Attention and effort (Vol. 1063). Englewood Cliffs, NJ: Prentice Hall.Google Scholar
  33. Kinner, V. L., Kuchinke, L., Dierolf, A. M., Merz, C. J., Otto, T., & Wolf, O. T. (2017). What our eyes tell us about feelings: Tracking pupillary responses during emotion regulation processes. Psychophysiology, 54(4), 508–518. doi: https://doi.org/10.1111/psyp.12816 CrossRefPubMedGoogle Scholar
  34. Laeng, B., Sirois, S., & Gredebäck, G. (2012). Pupillometry: A window to the preconscious?. Perspectives on Psychological Science, 7(1), 18–27. doi: https://doi.org/10.1177/1745691611427305 CrossRefPubMedGoogle Scholar
  35. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International Affective Picture System (IAPS): Affective ratings of pictures and instruction manual (Technical Report A-8). Gainesville: The Center for Research in Psychophysiology, University of Florida.Google Scholar
  36. LeDoux, J. (2012). Rethinking the emotional brain. Neuron, 73(4), 653–676. doi: https://doi.org/10.1016/j.neuron.2012.02.004 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Locke, H. S., & Braver, T. S. (2008). Motivational influences on cognitive control: Behaviour, brain activation, and individual differences. Cognitive, Affective, & Behavioural Neuroscience, 8(1), 99–112. doi: https://doi.org/10.3758/CABN.8.1.99 CrossRefGoogle Scholar
  38. Mathôt, S., Fabius, J., VanHeusden, E., & Van der Stigchel, S. (2017). Safe and sensible baseline correction of pupil-size data. PeerJ PrePrints. doi: https://doi.org/10.7287/peerj.preprints.2725v1
  39. Mathôt, S., & Van der Stigchel, S. (2015). New light on the mind’s eye: The pupillary light response as active vision. Current Directions in Psychological Science, 24(5), 374–378. doi: https://doi.org/10.1177/0963721415593725
  40. Mohanty, A., & Sussman, T. J. (2013). Top-down modulation of attention by emotion. Frontiers in Human Neuroscience, 7, 102. doi: https://doi.org/10.3389/fnhum.2013.00102 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mulckhuyse, M. (2018). The influence of emotional stimuli on the oculomotor system: A review of the literature. Cognitive, Affective, & Behavioural Neuroscience, 1–15. doi:https://doi.org/10.3758/s13415-018-0590-8Google Scholar
  42. Okon-Singer, H., Tzelgov, J., & Henik, A. (2007). Distinguishing between automaticity and attention in the processing of emotionally significant stimuli. Emotion, 7(1), 147–157. doi:https://doi.org/10.1037/1528-3542.7.1.147Google Scholar
  43. 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. doi: https://doi.org/10.1162/jocn_a_00011 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Padmala, S., & Pessoa, L. (2014). Motivation versus aversive processing during perception. Emotion, 14(3), 450–454. doi: https://doi.org/10.1037/a0036112 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Padmala, S., Sirbu, M., & Pessoa, L. (2017). Potential reward reduces the adverse impact of negative distractor stimuli. Social Cognitive and Affective Neuroscience, 12(9), 1402–1413. doi: https://doi.org/10.1093/scan/nsx067 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Pessoa, L. (2009). How do emotion and motivation direct executive control? Trends in Cognitive Sciences, 13(4), 160–166. doi: https://doi.org/10.1016/j.tics.2009.01.006 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pessoa, L., & Engelmann, J. B. (2010). Embedding reward signals into perception and cognition. Frontiers in Neuroscience, 4, 17. doi: https://doi.org/10.3389/fnins.2010.00017 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Pourtois, G., Schettino, A., & Vuilleumier, P. (2013). Brain mechanisms for emotional influences on perception and attention: What is magic and what is not. Biological Psychology, 92(3), 492–512. doi: https://doi.org/10.1016/j.biopsycho.2012.02.007 CrossRefPubMedGoogle Scholar
  49. Psychology Software Tools, Inc. (2012). E-Prime 2.0 [Computer software]. Retrieved from http://www.pstnet.com
  50. Rajkowski, J., Majczynski, H., Clayton, E., & Aston-Jones, G. (2004). Activation of monkey locus coeruleus neurons varies with difficulty and performance in a target detection task. Journal of Neurophysiology, 92(1), 361–371. doi: https://doi.org/10.1152/jn.00673.2003 CrossRefPubMedGoogle Scholar
  51. Ramsay, J. O., & Silverman, B. W. (1997). Functional data analysis. New York, NY: Springer-Verlag.CrossRefGoogle Scholar
  52. Ramsay, J. O., & Silverman, B. W. (2005). Functional data analysis (Springer series in statistics). New York, NY: Springer.Google Scholar
  53. Rondeel, E., van Steenbergen, H., Holland, R., & van Knippenberg, A. (2015). A closer look at cognitive control: Differences in resource allocation during updating, inhibition and switching as revealed by pupillometry. Frontiers in Human Neuroscience, 9, 494. doi: https://doi.org/10.3389/fnhum.2015.00494 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Samuels, E. R., & Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic locus coeruleus: Its roles in the regulation of arousal and autonomic function Part I: principles of functional organisation. Current Neuropharmacology, 6(3), 235–253.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nature Reviews Neuroscience, 10(3), 211. doi: https://doi.org/10.1038/nrn2573 CrossRefPubMedGoogle Scholar
  56. Sirois, S., & Brisson, J. (2014). Pupillometry. Wiley Interdisciplinary Reviews: Cognitive Science, 5(6), 679–692. doi: https://doi.org/10.1002/wcs.1323 PubMedGoogle Scholar
  57. Snowden, R. J., O’Farrell, K. R., Burley, D., Erichsen, J. T., Newton, N. V., & Gray, N. S. (2016). The pupil’s response to affective pictures: Role of image duration, habituation, and viewing mode. Psychophysiology, 53(8), 1217–1223. doi: https://doi.org/10.1111/psyp.12668 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sussman, T. J., Jin, J., & Mohanty, A. (2016). Top-down and bottom-up factors in threat-related perception and attention in anxiety. Biological Psychology, 121, 160–172. doi: https://doi.org/10.1016/j.biopsycho.2016.08.006 CrossRefPubMedGoogle Scholar
  59. Theeuwes, J. (2010). Top-down and bottom-up control of visual selection. Acta Psychologica, 135(2), 77–99. doi: https://doi.org/10.1016/j.actpsy.2010.02.006 CrossRefPubMedGoogle Scholar
  60. Vanderhasselt, M. A., Remue, J., Ng, K. K., & De Raedt, R. (2014). The interplay between the anticipation and subsequent online processing of emotional stimuli as measured by pupillary dilatation: The role of cognitive reappraisal. Frontiers in Psychology, 5, 207. doi: https://doi.org/10.3389/fpsyg.2014.00207 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Walsh, A. T., Carmel, D., Harper, D., & Grimshaw, G. M. (2018). Motivation enhances control of positive and negative emotional distractions. Psychonomic Bulletin & Review, 1–7. doi: https://doi.org/10.3758/s13423-017-1414-5
  62. Willenbockel, V., Sadr, J., Fiset, D., Horne, G. O., Gosselin, F., & Tanaka, J. W. (2010). Controlling low-level image properties: The SHINE toolbox. Behaviour Research Methods, 42(3), 671–684. doi: https://doi.org/10.3758/BRM.42.3.671 CrossRefGoogle Scholar
  63. Yamaguchi, M., & Nishimura, A. (2018). Modulating proactive cognitive control by reward: Differential anticipatory effects of performance-contingent and non-contingent rewards. Psychological Research, 1–17. doi: https://doi.org/10.1007/s00426-018-1027-2
  64. Yiend, J. (2010). The effects of emotion on attention: A review of attentional processing of emotional information. Cognition and Emotion, 24(1), 3–47. doi: https://doi.org/10.1080/02699930903205698 CrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Amy T. Walsh
    • 1
  • David Carmel
    • 1
    • 2
  • Gina M. Grimshaw
    • 1
    Email author
  1. 1.School of PsychologyVictoria University of WellingtonWellingtonNew Zealand
  2. 2.Department of PsychologyUniversity of EdinburghEdinburghUK

Personalised recommendations