Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Neural evidence for attentional capture by salient distractors

Abstract

Salient objects often capture our attention, serving as distractors and hindering our current goals. It remains unclear when and how salient distractors interact with our goals, and our knowledge on the neural mechanisms responsible for attentional capture is limited to a few brain regions recorded from non-human primates. Here we conducted a multivariate analysis on human intracranial signals covering most brain regions and successfully dissociated distractor-specific representations from target-arousal signals in the high-frequency (60–100 Hz) activity. We found that salient distractors were processed rapidly around 220 ms, while target-tuning attention was attenuated simultaneously, supporting initial capture by distractors. Notably, neuronal activity specific to the distractor representation was strongest in the superior and middle temporal gyrus, amygdala and anterior cingulate cortex, while there were smaller contributions from the parietal and frontal cortices. These results provide neural evidence for attentional capture by salient distractors engaging a much larger network than previously appreciated.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Stimuli, behavioural results and HF activity.
Fig. 2: Signal reconstruction with the IEM.
Fig. 3: Contribution to salient distractor processing of different brain regions.
Fig. 4: Comparisons between different brain regions when reacting to salient distractors.

Similar content being viewed by others

Data availability

As the iEEG data are being used in ongoing studies, we are unable to share them at this time. However, should researchers express interest in replicating our study, we will share the derived iEEG data upon request.

Code availability

The code we used can be accessed through https://github.com/wangbenchi/Shared_data (ref. 78).

References

  1. Theeuwes, J. Top-down and bottom-up control of visual selection. Acta Psychol. 135, 77–99 (2010).

    Article  Google Scholar 

  2. Itti, L. & Koch, C. Computational modelling of visual attention. Nat. Rev. Neurosci. 2, 194–203 (2001).

    Article  CAS  PubMed  Google Scholar 

  3. Theeuwes, J. Perceptual selectivity for color and form. Percept. Psychophys. 51, 599–606 (1992).

    Article  CAS  PubMed  Google Scholar 

  4. Theeuwes, J. Exogenous and endogenous control of attention: the effect of visual onsets and offsets. Percept. Psychophys. 49, 83–90 (1991).

    Article  CAS  PubMed  Google Scholar 

  5. Anderson, B. A., Laurent, P. A. & Yantis, S. Value-driven attentional capture. Proc. Natl Acad. Sci. USA 108, 10367–10371 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schmidt, L. J., Belopolsky, A. V. & Theeuwes, J. Attentional capture by signals of threat. Cogn. Emot. 29, 687–694 (2015).

    Article  PubMed  Google Scholar 

  7. Luck, S. J., Gaspelin, N., Folk, C. L., Remington, R. W. & Theeuwes, J. Progress toward resolving the attentional capture debate. Vis. Cogn. 29, 1–21 (2021).

    Article  PubMed  Google Scholar 

  8. Constantinidis, C. & Steinmetz, M. A. Neuronal responses in Area 7a to multiple-stimulus displays: I. Neurons encode the location of the salient stimulus. Cereb. Cortex 11, 581–591 (2001).

    Article  CAS  PubMed  Google Scholar 

  9. Constantinidis, C. Posterior parietal cortex automatically encodes the location of salient stimuli. J. Neurosci. 25, 233–238 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Katsuki, F. & Constantinidis, C. Early involvement of prefrontal cortex in visual bottom-up attention. Nat. Neurosci. 15, 1160–1166 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bichot, N. P., Schall, J. D. & Thompson, K. G. Visual feature selectivity in frontal eye fields induced by experience in mature macaques. Nature 381, 697–699 (1996).

    Article  CAS  PubMed  Google Scholar 

  12. Schall, J. D. & Hanes, D. P. Neural basis of saccade target selection in frontal eye field during visual search. Nature 366, 467–469 (1993).

    Article  CAS  PubMed  Google Scholar 

  13. Bichot, N. P. & Schall, J. D. Priming in macaque frontal cortex during popout visual search: feature-based facilitation and location-based inhibition of return. J. Neurosci. 22, 4675–4685 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Klink, P. C., Teeuwen, R. R. M., Lorteije, J. A. M. & Roelfsema, P. R. Inversion of pop-out for a distracting feature dimension in monkey visual cortex. Proc. Natl Acad. Sci. USA 120, e2210839120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ipata, A. E., Gee, A. L., Gottlieb, J., Bisley, J. W. & Goldberg, M. E. LIP responses to a popout stimulus are reduced if it is overtly ignored. Nat. Neurosci. 9, 1071–1076 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cosman, J. D., Lowe, K. A., Zinke, W., Woodman, G. F. & Schall, J. D. Prefrontal control of visual distraction. Curr. Biol. 28, 414–420 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).

    Article  CAS  PubMed  Google Scholar 

  18. Treue, S. & Trujillo, J. C. M. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999).

    Article  CAS  PubMed  Google Scholar 

  19. Hickey, C., McDonald, J. J. & Theeuwes, J. Electrophysiological evidence of the capture of visual attention. J. Cogn. Neurosci. 18, 604–613 (2006).

    Article  PubMed  Google Scholar 

  20. Brouwer, G. J. & Heeger, D. J. Decoding and reconstructing color from responses in human visual cortex. J. Neurosci. 29, 13992–14003 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sprague, T. C. & Serences, J. T. Attention modulates spatial priority maps in the human occipital, parietal and frontal cortices. Nat. Neurosci. 16, 1879–1887 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Foster, J. J., Sutterer, D. W., Serences, J. T., Vogel, E. K. & Awh, E. Alpha-band oscillations enable spatially and temporally resolved tracking of covert spatial attention. Psychol. Sci. 28, 929–941 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Sprague, T. C., Saproo, S. & Serences, J. T. Visual attention mitigates information loss in small- and large-scale neural codes. Trends Cogn. Sci. 19, 215–226 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ossandon, T. et al. Efficient ‘pop-out’ visual search elicits sustained broadband gamma activity in the dorsal attention network. J. Neurosci. 32, 3414–3421 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Clayton, M. S., Yeung, N. & Cohen Kadosh, R. The roles of cortical oscillations in sustained attention. Trends Cogn. Sci. 19, 188–195 (2015).

    Article  PubMed  Google Scholar 

  26. Yeo, B. T. et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125–1165 (2011).

    Article  PubMed  Google Scholar 

  27. Kunz, L. et al. Hippocampal theta phases organize the reactivation of large-scale electrophysiological representations during goal-directed navigation. Sci. Adv. 5, eaav8192 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Buschman, T. J. & Miller, E. K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860–1862 (2007).

    Article  CAS  PubMed  Google Scholar 

  29. Chen, X. et al. Parietal cortex regulates visual salience and salience-driven behavior. Neuron 106, 177–187 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Norman, Y. et al. Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. Science 365, eaax1030 (2019).

    Article  CAS  PubMed  Google Scholar 

  31. Solomon, E. A. et al. Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition. Nat. Commun. 8, 1704 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Banaie Boroujeni, K., Oemisch, M., Hassani, S. A. & Womelsdorf, T. Fast spiking interneuron activity in primate striatum tracks learning of attention cues. Proc. Natl Acad. Sci. USA 117, 18049–18058 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Gueguen, M. C. et al. Anatomical dissociation of intracerebral signals for reward and punishment prediction errors in humans. Nat. Commun. 12, 3344 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Goldstein, A. et al. Shared computational principles for language processing in humans and deep language models. Nat. Neurosci. 25, 369–380 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Khalighinejad, B., Herrero, J. L., Mehta, A. D. & Mesgarani, N. Adaptation of the human auditory cortex to changing background noise. Nat. Commun. 10, 2509 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Gaspelin, N. & Luck, S. J. Inhibition as a potential resolution to the attentional capture debate. Curr. Opin. Psychol. 29, 12–18 (2019).

    Article  PubMed  Google Scholar 

  37. Geng, J. J. Attentional mechanisms of distractor suppression. Curr. Dir. Psychol. Sci. 23, 147–153 (2014).

    Article  Google Scholar 

  38. Theeuwes, J., Bogaerts, L. & van Moorselaar, D. What to expect where and when: how statistical learning drives visual selection. Trends Cogn. Sci. 26, 860–872 (2022).

    Article  PubMed  Google Scholar 

  39. Wang, B. & Theeuwes, J. Statistical regularities modulate attentional capture. J. Exp. Psychol. Hum. Percept. Perform. 44, 13–17 (2018).

    Article  PubMed  Google Scholar 

  40. Jonides, J. & Yantis, S. Uniqueness of abrupt visual onset in capturing attention. Percept. Psychophys. 43, 346–354 (1988).

    Article  CAS  PubMed  Google Scholar 

  41. Folk, C. L., Remington, R. W. & Johnston, J. C. Involuntary covert orienting is contingent on attentional control settings. J. Exp. Psychol. Hum. Percept. Perform. 18, 1030–1044 (1992).

    Article  CAS  PubMed  Google Scholar 

  42. Gaspelin, N., Leonard, C. J. & Luck, S. J. Direct evidence for active suppression of salient-but-irrelevant sensory inputs. Psychol. Sci. 26, 1740–1750 (2015).

    Article  PubMed  Google Scholar 

  43. Wang, B., Van Driel, J., Ort, E. & Theeuwes, J. Anticipatory distractor suppression elicited by statistical regularities in visual search. J. Cogn. Neurosci. 31, 1535–1548 (2019).

    Article  PubMed  Google Scholar 

  44. Baudena, P., Halgren, E., Heit, G. & Clarke, J. M. Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. Electroencephalogr. Clin. Neurophysiol. 94, 251–264 (1995).

    Article  CAS  PubMed  Google Scholar 

  45. Clark, V. P., Fannon, S., Lai, S., Benson, R. & Bauer, L. Responses to rare visual target and distractor stimuli using event-related fMRI. J. Neurophysiol. 83, 3133–3139 (2000).

    Article  CAS  PubMed  Google Scholar 

  46. Kiehl, K. A., Laurens, K. R., Duty, T. L., Forster, B. B. & Liddle, P. F. Neural sources involved in auditory target detection and novelty processing: an event-related fMRI study. Psychophysiology 38, 133–142 (2001).

    CAS  PubMed  Google Scholar 

  47. Uddin, L. Q. Salience processing and insular cortical function and dysfunction. Nat. Rev. Neurosci. 16, 55–61 (2015).

    Article  CAS  PubMed  Google Scholar 

  48. Menon, V. & Uddin, L. Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214, 655–667 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Sani, I. et al. The human endogenous attentional control network includes a ventro-temporal cortical node. Nat. Commun. 12, 360 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Stemmann, H. & Freiwald, W. A. Evidence for an attentional priority map in inferotemporal cortex. Proc. Natl Acad. Sci. USA 116, 23797–23805 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bogadhi, A. R., Bollimunta, A., Leopold, D. A. & Krauzlis, R. J. Spatial attention deficits are causally linked to an area in macaque temporal cortex. Curr. Biol. 29, 726–736 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ramezanpour, H. & Fallah, M. The role of temporal cortex in the control of attention. Curr. Res. Neurobiol. 3, 100038 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Peck, C. J., Lau, B. & Salzman, C. D. The primate amygdala combines information about space and value. Nat. Neurosci. 16, 340–348 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Knight, R. T. Contribution of human hippocampal region to novelty detection. Nature 383, 256–259 (1996).

    Article  CAS  PubMed  Google Scholar 

  55. Rao, H., Zhou, T., Zhuo, Y., Fan, S. & Chen, L. Spatiotemporal activation of the two visual pathways in form discrimination and spatial location: a brain mapping study. Hum. Brain Mapp. 18, 79–89 (2003).

    Article  PubMed  Google Scholar 

  56. Posner, M. I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).

    Article  CAS  PubMed  Google Scholar 

  57. Corbetta, M. & Shulman, G. L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).

    Article  CAS  PubMed  Google Scholar 

  58. Vossel, S., Geng, J. J. & Fink, G. R. Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist 20, 150–159 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Van Rossum, G. & Drake, F. L. Python Reference Manual http://docs.python.org (2006).

  60. Delorme, A. & Makeig, S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9–21 (2004).

    Article  PubMed  Google Scholar 

  61. Lopez-Calderon, J. & Luck, S. J. ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front. Hum. Neurosci. 8, 213 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Liu, J. et al. Stable maintenance of multiple representational formats in human visual short-term memory. Proc. Natl Acad. Sci. USA 117, 32329–32339 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Bijanzadeh, M. et al. Decoding naturalistic affective behaviour from spectro-spatial features in multiday human iEEG. Nat. Hum. Behav. 6, 823–836 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Grossman, S. et al. Convergent evolution of face spaces across human face-selective neuronal groups and deep convolutional networks. Nat. Commun. 10, 4934 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Feldmann-Wüstefeld, T., Weinberger, M. & Awh, E. Spatially guided distractor suppression during visual search. J. Neurosci. 41, 3180–3191 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Gaspelin, N., Leonard, C. J. & Luck, S. J. Suppression of overt attentional capture by salient-but-irrelevant color singletons. Atten. Percept. Psychophys. 79, 45–62 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Wang, B., Samara, I. & Theeuwes, J. Statistical regularities bias overt attention. Atten. Percept. Psychophys. 81, 1813–1821 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Fischl, B., Sereno, M. I. & Dale, A. M. Cortical surface-based analysis: II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195–207 (1999).

    Article  CAS  PubMed  Google Scholar 

  69. Groppe, D. M. et al. iELVis: an open source MATLAB toolbox for localizing and visualizing human intracranial electrode data. J. Neurosci. Methods 281, 40–48 (2017).

    Article  CAS  PubMed  Google Scholar 

  70. Mukamel, R. et al. Coupling between neuronal firing, field potentials, and fMRI in human auditory cortex. Science 309, 951–954 (2005).

    Article  CAS  PubMed  Google Scholar 

  71. Parvizi, J. & Kastner, S. Promises and limitations of human intracranial electroencephalography. Nat. Neurosci. 21, 474–483 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Watson, B. O., Ding, M. & Buzsáki, G. Temporal coupling of field potentials and action potentials in the neocortex. Eur. J. Neurosci. 48, 2482–2497 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Jensen, O., Kaiser, J. & Lachaux, J.-P. Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 30, 317–324 (2007).

    Article  CAS  PubMed  Google Scholar 

  74. Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188 (2001).

    Article  Google Scholar 

  75. Norman, Y., Yeagle, E. M., Harel, M., Mehta, A. D. & Malach, R. Neuronal baseline shifts underlying boundary setting during free recall. Nat. Commun. 8, 1301 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Miller, J., Patterson, T. & Ulrich, R. Jackknife-based method for measuring LRP onset latency differences. Psychophysiology 35, 99–115 (1998).

    Article  CAS  PubMed  Google Scholar 

  77. Wang, L., Kuperberg, G. & Jensen, O. Specific lexico-semantic predictions are associated with unique spatial and temporal patterns of neural activity. eLife 7, e39061 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Wang, B. Shared_data, GitHub, https://github.com/wangbenchi/Shared_data (2024).

Download references

Acknowledgements

This research was supported by the National Science and Technology Innovation 2030 Major Program (grant no. 2022ZD0204802 to B.W.), the National Natural Science Foundation of China (grant no. 32000738 to B.W.) and the Sanming Project of Medicine in Shenzhen (grant no. SZSM202003006 to X.M.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

R.L., X.M., F.C., X.L. and B.W. designed the experiment. R.L., X.M. and F.C. collected the data. R.L. and B.W. analysed the data. R.L., O.J., J.T. and B.W. wrote the paper.

Corresponding author

Correspondence to Benchi Wang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Human Behaviour thanks Jacqueline Gottlieb and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

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

Supplementary information

Supplementary Information

Supplementary results (including ten figures).

Reporting Summary

Peer Review File

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, R., Meng, X., Chen, F. et al. Neural evidence for attentional capture by salient distractors. Nat Hum Behav (2024). https://doi.org/10.1038/s41562-024-01852-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41562-024-01852-5

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing