Fear not! Anxiety biases attentional enhancement of threat without impairing working memory filtering

Abstract

Individuals with anxiety have attentional biases toward threat-related distractors. This deficit in attentional control has been shown to impact visual working memory (VWM) filtering efficiency, as anxious individuals inappropriately store threatening distractors in VWM. It remains unclear, however, whether this mis-allocation of memory resources is due to inappropriate attentional enhancement of threatening distractors, or to a failure in suppression. Here, we used a systematically lateralized VWM task with fearful and neutral faces to examine event-related potentials related to attentional selection (N2pc), suppression (PD), and working memory maintenance (CDA). We found that state anxiety correlated with attentional enhancement of threat-related distractors, such that more anxious individuals had larger N2pc amplitudes toward fearful distractors than neutral distractors. However, there was no correlation between anxiety and memory storage of fearful distractors (CDA). These findings demonstrate that anxiety biases attention toward fearful distractors, but that this bias does not always guarantee increased memory storage of threat-related distractors.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Ansari, T. L., & Derakshan, N. (2011). The neural correlates of impaired inhibitory control in anxiety. Neuropsychologia, 49(5), 1146–1153.

    Article  Google Scholar 

  2. Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M. J., & Van Ijzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133(1), 1–24.

    Article  Google Scholar 

  3. Barnes, L., Harp, D., & Jung, W. (2002). Reliability generalization of scores on the Spielberger state-trait anxiety inventory. Educational and Psychological Measurement, 62(4), 603–618. https://doi.org/10.1177/0013164402062004005

    Article  Google Scholar 

  4. Beck, A. T., & Clark, D. A. (1997). An information processing model of anxiety: Automatic and strategic processes. Behaviour Research and Therapy, 35(1), 49–58. https://doi.org/10.1016/S0005-7967(96)00069-1

    Article  PubMed  Google Scholar 

  5. Bentin, S., Allison, T., Puce, A., Perez, E., & McCarthy, G. (1996). Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience, 8(6), 551–565. https://doi.org/10.1162/jocn.1996.8.6.551

    Article  PubMed  PubMed Central  Google Scholar 

  6. Berggren, N., & Derakshan, N. (2013). Attentional control deficits in trait anxiety: Why you see them and why you don’t. Biological Psychology, 92(3), 440–446.

    Article  Google Scholar 

  7. Bishop, S. J. (2007). Neurocognitive mechanisms of anxiety: An integrative account. Trends in Cognitive Sciences, 11(7), 307–316. https://doi.org/10.1016/j.tics.2007.05.008

    Article  PubMed  Google Scholar 

  8. Bishop, S. J. (2009). Trait anxiety and impoverished prefrontal control of attention. Nature Neuroscience, 12(1), 92–98. https://doi.org/10.1038/nn.2242

    Article  PubMed  Google Scholar 

  9. Bishop, S. J., Duncan, J., Brett, M., & Lawrence, A. D. (2004a). Prefrontal cortical function and anxiety: Controlling attention to threat-related stimuli. Nature Neuroscience, 7(2), 184–188. https://doi.org/10.1038/nn1173

    Article  PubMed  Google Scholar 

  10. Bishop, S. J., Duncan, J., & Lawrence, A. D. (2004b). State anxiety modulation of the amygdala response to unattended threat-related stimuli. Journal of Neuroscience, 24(46), 10364–10368. https://doi.org/10.1523/JNEUROSCI.2550-04.2004

    Article  PubMed  Google Scholar 

  11. Bishop, S. J., Jenkins, R., & Lawrence, A. D. (2007). Neural processing of fearful faces: Effects of anxiety are gated by perceptual capacity limitations. Cerebral Cortex, 17(7), 1595–1603. https://doi.org/10.1093/cercor/bhl070

    Article  PubMed  Google Scholar 

  12. Böckmann-Barthel, M. (2017). r. https://www.mathworks.com/matlabcentral/fileexchange/65377-sensitivity-index-d

  13. Bretherton, P. M., Eysenck, M. W., Richards, A., & Holmes, A. (2017). Target and distractor processing and the influence of load on the allocation of attention to task-irrelevant threat. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2017.09.009

  14. Burra, N., Barras, C., Coll, S. Y., & Kerzel, D. (2016). Electrophysiological evidence for attentional capture by irrelevant angry facial expressions. Biological Psychology, 120, 69–80. https://doi.org/10.1016/j.biopsycho.2016.08.008

    Article  PubMed  Google Scholar 

  15. Burra, N., Coll, S. Y., Barras, C., & Kerzel, D. (2017). Electrophysiological evidence for attentional capture by irrelevant angry facial expressions: Naturalistic faces. Neuroscience Letters, 637, 44–49. https://doi.org/10.1016/j.neulet.2016.11.055

    Article  PubMed  Google Scholar 

  16. Burra, N., & Kerzel, D. (2014). The distractor positivity (Pd) signals lowering of attentional priority: Evidence from event-related potentials and individual differences. Psychophysiology, 51(7), 685–696. https://doi.org/10.1111/psyp.12215

    Article  PubMed  Google Scholar 

  17. Burra, N., Pittet, C., Barras, C., & Kerzel, D. (2019). Attentional suppression is delayed for threatening distractors. Visual Cognition, 27(3–4), 185–198. https://doi.org/10.1080/13506285.2019.1593272

    Article  Google Scholar 

  18. Cauquil, A. S., Edmonds, G. E., & Taylor, M. J. (2000). Is the face-sensitive N170 the only ERP not affected by selective attention? NeuroReport, 11(10), 2167–2171.

    Article  Google Scholar 

  19. Curby, K. M., & Gauthier, I. (2007). A visual short-term memory advantage for faces. Psychonomic Bulletin & Review, 14(4), 620–628. https://doi.org/10.3758/BF03196811

    Article  Google Scholar 

  20. Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009

    Article  Google Scholar 

  21. Derakshan, N., & Eysenck, M. W. (2009). Anxiety, processing efficiency, and cognitive performance. European Psychologist, 14(2), 168–176. https://doi.org/10.1027/1016-9040.14.2.168

    Article  Google Scholar 

  22. Dube, B., Emrich, S. M., & Al-Aidroos, N. (2017). More than a filter: Feature-based attention regulates the distribution of visual working memory resources. Journal of Experimental Psychology. Human Perception and Performance, 43(10), 1843–1854. https://doi.org/10.1037/xhp0000428

    Article  PubMed  Google Scholar 

  23. Eimer. (1996). The N2pc component as an indicator of attentional selectivity. Electroencephalography and Clinical Neurophysiology, 99(3), 225–234.

    Article  Google Scholar 

  24. Eimer, & Kiss, M. (2007). Attentional capture by task-irrelevant fearful faces is revealed by the N2pc component. Biological Psychology, 74(1), 108–112. https://doi.org/10.1016/j.biopsycho.2006.06.008

    Article  PubMed  PubMed Central  Google Scholar 

  25. Eimer, M. (2000). The face-specific N170 component reflects late stages in the structural encoding of faces. NeuroReport, 11(10), 2319.

    Article  Google Scholar 

  26. Emrich, S. M., & Busseri, M. A. (2015). Re-evaluating the relationships among filtering activity, unnecessary storage, and visual working memory capacity. Cognitive, Affective, & Behavioral Neuroscience, 15(3), 589–597. https://doi.org/10.3758/s13415-015-0341-z

    Article  Google Scholar 

  27. Emrich, S. M., Lockhart, H. A., & Al-Aidroos, N. (2017). Attention mediates the flexible allocation of visual working memory resources. Journal of Experimental Psychology. Human Perception and Performance, 43(7), 1454–1465. https://doi.org/10.1037/xhp0000398

    Article  PubMed  Google Scholar 

  28. Eysenck, M. W., Derakshan, N., Santos, R., & Calvo, M. G. (2007). Anxiety and cognitive performance: Attentional control theory. Emotion, 7(2), 336–353.

    Article  Google Scholar 

  29. Feldmann-Wüstefeld, T., Schmidt-Daffy, M., & Schubö, A. (2011). Neural evidence for the threat detection advantage: Differential attention allocation to angry and happy faces: Neural evidence for threat detection. Psychophysiology, 48(5), 697–707. https://doi.org/10.1111/j.1469-8986.2010.01130.x

    Article  PubMed  Google Scholar 

  30. Feldmann-Wüstefeld, T., & Vogel, E. K. (2019). Neural evidence for the contribution of active suppression during working memory filtering. Cerebral Cortex, 29(2), 529–543. https://doi.org/10.1093/cercor/bhx336

    Article  PubMed  Google Scholar 

  31. Fortier-Gauthier, U., Moffat, N., Dell’Acqua, R., McDonald, J. J., & Jolicœur, P. (2012). Contralateral cortical organisation of information in visual short-term memory: Evidence from lateralized brain activity during retrieval. Neuropsychologia, 50(8), 1748–1758. https://doi.org/10.1016/j.neuropsychologia.2012.03.032

    Article  PubMed  Google Scholar 

  32. Fox, E., Derakshan, N., & Shoker, L. (2008). Trait anxiety modulates the electrophysiological indices of rapid spatial orienting towards angry faces. Neuroreport, 19(3), 259–263.

    Article  Google Scholar 

  33. Fox, E., Russo, R., Bowles, R., & Dutton, K. (2001). Do threatening stimuli draw or hold visual attention in subclinical anxiety? Journal of Experimental Psychology: General, 130(4), 681–700. https://doi.org/10.1037/0096-3445.130.4.681

    Article  Google Scholar 

  34. Gambarota, F., & Sessa, P. (2019). Visual working memory for faces and facial expressions as a useful “tool” for understanding social and affective cognition. Frontiers in Psychology, 10. https://doi.org/10.3389/fpsyg.2019.02392

  35. Gaspar, J. M., & McDonald, J. J. (2014). Suppression of salient objects prevents distraction in visual search. Journal of Neuroscience, 34(16), 5658–5666. https://doi.org/10.1523/JNEUROSCI.4161-13.2014

    Article  PubMed  Google Scholar 

  36. Gaspar, J. M., & McDonald, J. J. (2018). High level of trait anxiety leads to salience-driven distraction and compensation. Psychological Science, 29(12), 2020–2030. https://doi.org/10.1177/0956797618807166

    Article  Google Scholar 

  37. Gaspelin, N., & Luck, S. J. (2018). Combined electrophysiological and behavioral evidence for the suppression of salient distractors. Journal of Cognitive Neuroscience, 30(9), 1265–1280. https://doi.org/10.1162/jocn_a_01279

    Article  PubMed  PubMed Central  Google Scholar 

  38. Guzman-Martinez, E., Leung, P., Franconeri, S., Grabowecky, M., & Suzuki, S. (2009). Rapid eye-fixation training without eyetracking. Psychonomic Bulletin & Review, 16(3), 491–496. https://doi.org/10.3758/PBR.16.3.491

    Article  Google Scholar 

  39. Hickey, C., Di Lollo, V., & McDonald, J. J. (2009). Electrophysiological indices of target and distractor processing in visual search. Journal of Cognitive Neuroscience, 21(4), 760–775. https://doi.org/10.1162/jocn.2009.21039

  40. Hickey, C., McDonald, J. J., & Theeuwes, J. (2006). Electrophysiological evidence of the capture of visual attention. Journal of Cognitive Neuroscience, 18(4), 604–613. https://doi.org/10.1162/jocn.2006.18.4.604

    Article  PubMed  Google Scholar 

  41. Hodsoll, S., Viding, E., & Lavie, N. (2011). Attentional capture by irrelevant emotional distractor faces. Emotion, 11(2), 346–353. https://doi.org/10.1037/a0022771

    Article  PubMed  Google Scholar 

  42. Holmes, A., Bradley, B. P., Nielsen, M. K., & Mogg, K. (2009). Attentional selectivity for emotional faces: Evidence from human electrophysiology. Psychophysiology, 46(1), 62–68. https://doi.org/10.1111/j.1469-8986.2008.00750.x

    Article  PubMed  Google Scholar 

  43. IBM SPSS Statistics for Macintosh (25.0). (2017). [Computer software]. IBM Corp.

  44. Ikkai, A., McCollough, A., & Vogel, E. (2010). Contralateral delay activity provides a neural measure of the number of representations in visual working memory. Journal of Neurophysiology, 103(4), 1963–1968.

    Article  Google Scholar 

  45. Jannati, A., Gaspar, J. M., & McDonald, J. J. (2013). Tracking target and distractor processing in fixed-feature visual search: Evidence from human electrophysiology. Journal of Experimental Psychology: Human Perception and Performance, 39(6), 1713–1730. https://doi.org/10.1037/a0032251

    Article  PubMed  Google Scholar 

  46. Kappenman, E. S., MacNamara, A., & Proudfit, G. H. (2015). Electrocortical evidence for rapid allocation of attention to threat in the dot-probe task. Social Cognitive and Affective Neuroscience, 10(4), 577–583. https://doi.org/10.1093/scan/nsu098

    Article  PubMed  Google Scholar 

  47. Kiss, M., & Eimer, M. (2008). ERPs reveal subliminal processing of fearful faces. Psychophysiology, 45(2), 318–326. https://doi.org/10.1111/j.1469-8986.2007.00634.x

    Article  PubMed  Google Scholar 

  48. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23(1), 155–184. https://doi.org/10.1146/annurev.neuro.23.1.155

    Article  PubMed  Google Scholar 

  49. Liesefeld, A. M., Liesefeld, H. R., & Zimmer, H. D. (2014). Intercommunication between prefrontal and posterior brain regions for protecting visual working memory from distractor interference. Psychological Science, 25(2), 325–333. https://doi.org/10.1177/0956797613501170

    Article  PubMed  Google Scholar 

  50. Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: An open-source toolbox for the analysis of event-related potentials. Frontiers in Human Neuroscience, 8. https://doi.org/10.3389/fnhum.2014.00213

  51. Luck, S. J., & Hillyard, S. A. (1994a). Spatial filtering during visual search: Evidence from human electrophysiology. Journal of Experimental Psychology: Human Perception and Performance, 20(5), 1000–1014. https://doi.org/10.1037/0096-1523.20.5.1000

    Article  PubMed  Google Scholar 

  52. Luck, S. J., & Hillyard, S. A. (1994b). Electrophysiological correlates of feature analysis during visual search. Psychophysiology, 31(3), 291–308. https://doi.org/10.1111/j.1469-8986.1994.tb02218.x

    Article  PubMed  Google Scholar 

  53. Luck, S. J., & Vogel, E. K. (1997). The capacity of visual working memory for features and conjunctions. Nature, 390(6657), 279–281. https://doi.org/10.1038/36846

    Article  PubMed  PubMed Central  Google Scholar 

  54. Mathews, A., & Mackintosh, B. (1998). A cognitive model of selective processing in anxiety. Cognitive Therapy and Research, 22(6), 539–560. https://doi.org/10.1023/A:1018738019346

    Article  Google Scholar 

  55. McCollough, A. W., Machizawa, M. G., & Vogel, E. K. (2007). Electrophysiological measures of maintaining representations in visual working memory. Cortex, 43(1), 77–94.

    Article  Google Scholar 

  56. McNab, F., & Klingberg, T. (2008). Prefrontal cortex and basal ganglia control access to working memory. Nature Neuroscience, 11(1), 103–107. https://doi.org/10.1038/nn2024

    Article  PubMed  Google Scholar 

  57. Mogg, K., & Bradley, B. P. (1999). Orienting of attention to threatening facial expressions presented under conditions of restricted awareness. Cognition and Emotion, 13(6), 713–740. https://doi.org/10.1080/026999399379050

    Article  Google Scholar 

  58. Moran, T. P., & Moser, J. S. (2015). The color of anxiety: Neurobehavioral evidence for distraction by perceptually salient stimuli in anxiety. Cognitive, Affective, & Behavioral Neuroscience, 15(1), 169–179. https://doi.org/10.3758/s13415-014-0314-7

    Article  Google Scholar 

  59. Öhman, A. (2005). The role of the amygdala in human fear: Automatic detection of threat. Psychoneuroendocrinology, 30(10), 953–958. https://doi.org/10.1016/j.psyneuen.2005.03.019

    Article  PubMed  Google Scholar 

  60. Öhman, A., Flykt, A., & Esteves, F. (2001). Emotion drives attention: Detecting the snake in the grass. Journal of Experimental Psychology: General, 130(3), 466–478. https://doi.org/10.1037/0096-3445.130.3.466

    Article  Google Scholar 

  61. Öhman, A., & Mineka, S. (2001). Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review, 108(3), 483–522. https://doi.org/10.1037//0033-295X.108.3.483

    Article  PubMed  Google Scholar 

  62. Peirce, J. (2009). Generating stimuli for neuroscience using PsychoPy. Frontiers in Neuroinformatics, 2, 10. https://doi.org/10.3389/neuro.11.010.2008

    Article  PubMed  PubMed Central  Google Scholar 

  63. Pessoa, L. (2005). To what extent are emotional visual stimuli processed without attention and awareness? Current Opinion in Neurobiology, 15(2), 188–196. https://doi.org/10.1016/j.conb.2005.03.002

    Article  PubMed  Google Scholar 

  64. Qi, S., Ding, C., & Li, H. (2014). Neural correlates of inefficient filtering of emotionally neutral distractors from working memory in trait anxiety. Cognitive, Affective, & Behavioral Neuroscience, 14(1), 253–265. https://doi.org/10.3758/s13415-013-0203-5

    Article  Google Scholar 

  65. Salahub, C., Lockhart, H. A., Dube, B., Al-Aidroos, N., & Emrich, S. M. (2019). Electrophysiological correlates of the flexible allocation of visual working memory resources. Scientific Reports, 9:19428. https://doi.org/10.1101/746164

    Article  PubMed  PubMed Central  Google Scholar 

  66. Sawaki, R., Geng, J. J., & Luck, S. J. (2012). A common neural mechanism for preventing and terminating the allocation of attention. The Journal of Neuroscience, 32(31), 10725–10736. https://doi.org/10.1523/JNEUROSCI.1864-12.2012

    Article  PubMed  PubMed Central  Google Scholar 

  67. Sawaki, R., & Luck, S. J. (2010). Capture versus suppression of attention by salient singletons: Electrophysiological evidence for an automatic attend-to-me signal. Attention, Perception, & Psychophysics, 72(6), 1455–1470. https://doi.org/10.3758/APP.72.6.1455

    Article  Google Scholar 

  68. Sawaki, R., & Luck, S. J. (2013). Active suppression after involuntary capture of attention. Psychonomic Bulletin & Review, 20(2), 296–301. https://doi.org/10.3758/s13423-012-0353-4

    Article  Google Scholar 

  69. Sessa, P., Luria, R., Gotler, A., Jolicœur, P., & Dell’acqua, R. (2011). Interhemispheric ERP asymmetries over inferior parietal cortex reveal differential visual working memory maintenance for fearful versus neutral facial identities. Psychophysiology, 48(2), 187–197. https://doi.org/10.1111/j.1469-8986.2010.01046.x

    Article  PubMed  Google Scholar 

  70. Shackman, A. J., Stockbridge, M. D., Tillman, R. M., Kaplan, C. M., Tromp, D. P. M., Fox, A. S., & Gamer, M. (2016). The neurobiology of dispositional negativity and attentional biases to threat: Implications for understanding anxiety disorders in adults and youth. Journal of Experimental Psychopathology, 7(3), 311–342. https://doi.org/10.5127/jep.054015

    Article  PubMed  PubMed Central  Google Scholar 

  71. Spielberger, C. D., Gorsuch, R. L., Lushene, R., & Vagg, P. R. (1983). Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press.

  72. Stout, D. M., Shackman, A. J., & Larson, C. L. (2013). Failure to filter: Anxious individuals show inefficient gating of threat from working memory. Frontiers in Human Neuroscience, 7, 58. https://doi.org/10.3389/fnhum.2013.00058

    Article  PubMed  PubMed Central  Google Scholar 

  73. Stout, D. M., Shackman, A. J., Pedersen, W. S., Miskovich, T. A., & Larson, C. L. (2017). Neural circuitry governing anxious individuals’ mis-allocation of working memory to threat. Scientific Reports, 7(1), 8742. https://doi.org/10.1038/s41598-017-08443-7

    Article  PubMed  PubMed Central  Google Scholar 

  74. JASP Team. (2020). JASP (0.12) [Computer software].

  75. Vogel, E. K., McCollough, A. W., & Machizawa, M. G. (2005). Neural measures reveal individual differences in controlling access to working memory. Nature, 438(7067), 500–503. https://doi.org/10.1038/nature04171

    Article  PubMed  Google Scholar 

  76. Weaver, M. D., van Zoest, W., & Hickey, C. (2017). A temporal dependency account of attentional inhibition in oculomotor control. NeuroImage, 147, 880–894. https://doi.org/10.1016/j.neuroimage.2016.11.004

  77. Weymar, M., Löw, A., Öhman, A., & Hamm, A. O. (2011). The face is more than its parts—Brain dynamics of enhanced spatial attention to schematic threat. NeuroImage, 58(3), 946–954. https://doi.org/10.1016/j.neuroimage.2011.06.061

    Article  PubMed  PubMed Central  Google Scholar 

  78. Woodman, G. F., & Luck, S. J. (2003). Serial deployment of attention during visual search. Journal of Experimental Psychology: Human Perception and Performance, 29(1), 121–138. https://doi.org/10.1037/0096-1523.29.1.121

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery (#2019-435945) and Research Tools and Instruments (#458707) Grants awarded to SME, and a NSERC post-graduate scholarship awarded to CS. We thank Joseph Capozza (experiment programming/data collection) and Brenda de Wit (data collection).

Open practices statement

The methods and analyses in the present study were pre-registered at https://aspredicted.org/cf7jn.pdf. The data from this experiment are not available online due to the absence of participant consent. Task and data analysis scripts are available upon request.

Author information

Affiliations

Authors

Contributions

CS and SME contributed equally to the experimental design, data analysis, and manuscript preparation. CS collected the data.

Corresponding author

Correspondence to Christine Salahub.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 49 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Salahub, C., Emrich, S.M. Fear not! Anxiety biases attentional enhancement of threat without impairing working memory filtering. Cogn Affect Behav Neurosci 20, 1248–1260 (2020). https://doi.org/10.3758/s13415-020-00831-3

Download citation

Keywords

  • Attention
  • Working memory
  • Cognitive control
  • ERP
  • Anxiety