Attentional capture by Pavlovian reward-signalling distractors in visual search persists when rewards are removed

Autoři: Poppy Watson aff001;  Daniel Pearson aff001;  Steven B. Most aff001;  Jan Theeuwes aff002;  Reinout W. Wiers aff003;  Mike E. Le Pelley aff001
Působiště autorů: School of Psychology, UNSW, Sydney, Australia aff001;  Department of Experimental and Applied Psychology, Vrije Universiteit, Amsterdam, The Netherlands aff002;  Department of Psychology, University of Amsterdam, Amsterdam, The Netherlands aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226284


Existing research indicates that learning about the Pavlovian ‘signal value’ of stimuli can induce attentional biases: findings suggest that our attentional system prioritises detection of stimuli that have previously signalled availability of high reward. These findings potentially provide a human analogue of sign-tracking behaviour previously reported in studies of non-human animals. Here we examine a visual search task that has been developed to demonstrate the Pavlovian influence of reward on attention, in which the critical reward-signalling stimuli are never explicit targets of search. This procedure has previously yielded robust effects of reward on attention; however it remains unclear whether this pattern reflects a persistent and automatic bias in attentional capture based on prior experience of stimulus–reward pairings, or whether it results from participants strategically attending to reward-signalling distractors because they provide useful information about reward magnitude. To investigate this issue, in the current study participants initially completed a rewarded visual search task, in which colours of distractor stimuli signalled availability of high or low reward. Participants then completed a test phase in which rewards were no longer available, such that distractor colours no longer provided useful information on reward availability. Performance during the initial rewarded phase was impaired by the presence of a distractor signalling availability of high relative to low reward. Crucially, the magnitude of this reward-related distraction effect did not reduce in the subsequent unrewarded test phase. This suggests that participants’ experience of differences in reward value signalled by distractor stimuli in this task can induce persistent biases in the extent to which these stimuli involuntarily capture attention, even when they are entirely task-irrelevant.

Klíčová slova:

Analysis of variance – Animal behavior – Attention – Behavior – Behavioral addiction – Cognitive psychology – Human performance – Learning


1. Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002;3(3):201–15. doi: 10.1038/nrn755 11994752

2. Yantis S. Goal-directed and stimulus-driven determinants of attentional control. In: Monsell S, Driver J, editors. Attention and Performance XVIII. Cambridge, MA: MIT Press; 2000. p. 73–103.

3. Anderson BA. The attention habit: How reward learning shapes attentional selection. Ann Ny Acad Sci. 2016;1369(The Year in Cognitive Neuroscience):24–39. doi: 10.1111/nyas.12957 26595376

4. Failing M, Theeuwes J. Selection history: How reward modulates selectivity of visual attention. Psychonomic Bulletin & Review. 2018;25(2):514–38. doi: 10.3758/s13423-017-1380-y 28986770

5. Le Pelley ME, Mitchell CJ, Beesley T, George DN, Wills AJ. Attention and associative learning in humans: An integrative review. Psychol Bull. 2016;142(10):1111–40. doi: 10.1037/bul0000064 27504933.

6. Watson P, Pearson D, Wiers RW, Le Pelley ME. Prioritizing pleasure and pain: Attentional capture by reward-related and punishment-related stimuli. Curr Opin Behav Sci. 2019;26:107–13. doi: 10.1016/j.cobeha.2018.12.002

7. Anderson BA, Laurent PA, Yantis S. Value-driven attentional capture. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(25):10367–71. doi: 10.1073/pnas.1104047108 21646524

8. Della Libera C, Chelazzi L. Learning to attend and to ignore is a matter of gains and losses. Psychological Science. 2009;20(6):778–84. doi: 10.1111/j.1467-9280.2009.02360.x 19422618

9. Hickey C, Chelazzi L, Theeuwes J. Reward changes salience in human vision via the anterior cingulate. J Neurosci. 2010;30(33):11096–103. doi: 10.1523/JNEUROSCI.1026-10.2010 20720117

10. Le Pelley ME, Pearson D, Griffiths O, Beesley T. When goals conflict with values: Counterproductive attentional and oculomotor capture by reward-related stimuli. Journal of Experimental Psychology: General. 2015;144(1):158–71. doi: 10.1037/xge0000037 25420117

11. Le Pelley ME, Seabrooke T, Kennedy BL, Pearson D, Most SB. Miss it and miss out: Counterproductive nonspatial attentional capture by task-irrelevant, value-related stimuli. Attention, Perception, & Psychophysics. 2017;79(6):1628–42. doi: 10.3758/s13414-017-1346-1 28584955

12. Peck CJ, Jangraw DC, Suzuki M, Efem R, Gottlieb J. Reward modulates attention independently of action value in posterior parietal cortex. J Neurosci. 2009;29(36):11182–91. doi: 10.1523/JNEUROSCI.1929-09.2009 19741125

13. Theeuwes J. Perceptual selectivity for color and form. Perception & Psychophysics. 1992;51(6):599–606. doi: 10.3758/Bf03211656 1620571

14. Albertella L, Copeland J, Pearson D, Watson P, Wiers RW, Le Pelley ME. Selective attention moderates the relationship between attentional capture by signals of nondrug reward and illicit drug use. Drug Alcohol Depen. 2017;175:99–105. doi: 10.1016/j.drugalcdep.2017.01.041 28411561.

15. Failing MF, Nissens T, Pearson D, Le Pelley ME, Theeuwes J. Oculomotor capture by stimuli that signal the availability of reward. J Neurophysiol. 2015;114(4):2316–27. doi: 10.1152/jn.00441.2015 26289464

16. Pearson D, Donkin C, Tran SC, Most SB, Le Pelley ME. Cognitive control and counterproductive oculomotor capture by reward-related stimuli. Vis Cogn. 2015;23(1–2):41–66. doi: 10.1080/13506285.2014.994252

17. Pearson D, Osborn R, Whitford TJ, Failing M, Theeuwes J, Le Pelley ME. Value-modulated oculomotor capture by task-irrelevant stimuli is a consequence of early competition on the saccade map. Attention, Perception, & Psychophysics. 2016;78:2226–40. doi: 10.3758/s13414-016-1135-2 27184056

18. Watson P, Pearson D, Chow M, Theeuwes J, Wiers RW, Most SB, et al. Capture and control: Working memory modulates attentional capture by reward-related stimuli. Psychological Science. 2019;30(8):1174–85. doi: 10.1177/0956797619855964 31268837.

19. Le Pelley ME, Pearson D, Porter A, Yee H, Luque D. Oculomotor capture is influenced by expected reward value but (maybe) not predictiveness. Quarterly Journal of Experimental Psychology. 2019;72(2):168–81. doi: 10.1080/17470218.2017.1313874 28375688

20. Anderson BA, Laurent PA, Yantis S. Learned value magnifies salience-based attentional capture. Plos One. 2011;6(11):1–6. doi: 10.1371/journal.pone.0027926 22132170

21. Flagel SB, Robinson TE. Neurobiological basis of individual variation in stimulus-reward learning. Curr Opin Behav Sci. 2017;13:178–85. doi: 10.1016/j.cobeha.2016.12.004 28670608

22. Hearst E, Jenkins HM. Sign tracking: The stimulus-reinforcer relation and directed action. Austin, TX: The Psychonomic Society; 1974.

23. Flagel SB, Akil H, Robinson TE. Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction. Neuropharmacology. 2009;56:139–48. doi: 10.1016/j.neuropharm.2008.06.027 18619474

24. Flagel SB, Watson SJ, Robinson TE, Akil H. Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology. 2007;191(3):599–607. doi: 10.1007/s00213-006-0535-8 16972103

25. Tomie A, Morrow JD, editors. The role of sign-tracking in drug addiction. Ann Arbor, MI: Michigan Publishing; 2018.

26. Tomie A, Grimes KL, Pohorecky LA. Behavioral characteristics and neurobiological substrates shared by Pavlovian sign-tracking and drug abuse. Brain Res Rev. 2008;58(1):121–35. doi: 10.1016/j.brainresrev.2007.12.003 18234349

27. Albertella L, Le Pelley ME, Chamberlain SR, Westbrook F, Fontenelle LF, Segrave R, et al. Reward-related attentional capture is associated with severity of addictive and obsessive-compulsive behaviors. Psychology of Addictive Behaviors. 2019;33(5):495–502. Epub 2019/06/21. doi: 10.1037/adb0000484 31219264

28. Albertella L, Watson P, Yücel M, Le Pelley ME. Persistence of value-modulated attentional capture is associated with risky alcohol use. Addictive Behaviors Reports. 2019;10:100195. Epub 2019/06/28. doi: 10.1016/j.abrep.2019.100195 31245528

29. Albertella L, Chamberlain SR, Le Pelley ME, Greenwood L-M, Lee R, Den Ouden L, et al. Compulsivity is measurable across distinct psychiatric symptom domains and is associated with familial risk and reward-related attentional capture. CNS Spectrums. in press.

30. Gottlieb J, Hayhoe M, Hikosaka O, Rangel A. Attention, reward, and information seeking. J Neurosci. 2014;34(46):15497–504. doi: 10.1523/JNEUROSCI.3270-14.2014 25392517

31. Anderson BA, Halpern M. On the value-dependence of value-driven attentional capture. Attention, Perception, & Psychophysics. 2017;79(4):1001–11. doi: 10.3758/s13414-017-1289-6 28176215

32. Le Pelley ME, Watson P, Pearson D, Abeywickrama RS, Most SB. Winners and losers: Reward and punishment produce biases in temporal selection. Journal of Experimental Psychology: Learning, Memory, & Cognition. 2019;45:822–33. doi: 10.1037/xlm0000612 29985032

33. Brainard DH. The psychophysics toolbox. Spatial Vision. 1997;10(4):433–6. doi: 10.1163/156856897x00357 9176952

34. Kleiner M, Brainard DH, Pelli DG. What’s new in Psychtoolbox-3? Perception. 2007;36:ECVP Abstract Supplement.

35. Pelli DG. The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision. 1997;10(4):437–42. doi: 10.1163/156856897x00366 9176953

36. JASP Team. JASP. 0.8.5 ed2018.

37. Jeffreys H. Theory of probability. Oxford, UK: Oxford University Press; 1961.

38. Morey RD. Confidence intervals from normalized data: A correction to Cousineau (2005). Tutorial in Quantitative Methods for Psychology. 2008;4(2):61–4.

39. Mine C, Saiki J. Task-irrelevant stimulus-reward association induces value-driven attentional capture. Attention, Perception, & Psychophysics. 2015. doi: 10.3758/s13414-015-0894-5 25893470

40. Saunders BT, Robinson TE. Individual variation in resisting temptation: Implications for addiction. Neuroscience and Biobehavioral Reviews. 2013;37(9):1955–75. doi: 10.1016/j.neubiorev.2013.02.008 23438893

41. Theeuwes J. Visual selection: Usually fast and automatic; seldom slow and volitional. 2018.

42. Harris JA, Andrew BJ, Kwok DWS. Magazine approach during a signal for food depends on Pavlovian, not instrumental, conditioning. Journal of Experimental Psychology: Animal Behavior Processes. 2013;39(2):107–16. doi: 10.1037/a0031315 23421397

Článek vyšel v časopise


2019 Číslo 12