Skip to main content
Log in

Neural Correlates of Attentional Processing of Threat in Youth with and without Anxiety Disorders

  • Published:
Journal of Abnormal Child Psychology Aims and scope Submit manuscript

Abstract

Late-stage attentional processing of threatening stimuli, quantified through event-related potentials (ERPs), differentiates youth with and without anxiety disorders. It is unknown whether early-stage attentional processing of threatening stimuli differentiates these groups. Examining both early and late stage attentional processes in youth may advance knowledge and enhance efforts to identify biomarkers for translational prevention and treatment research. Twenty-one youth with primary DSM-IV-TR anxiety disorders (10 males, ages 8–15 years) and 21 typically developing Controls (15 males, ages 8–16 years) completed a dot probe task while electroencephalography (EEG) was recorded, and ERPs were examined. Youth with anxiety disorders showed significantly larger (more positive) P1 amplitudes for threatening stimuli than for neutral stimuli, and Controls showed the opposite pattern. Youth with anxiety showed larger (more negative) N170 amplitudes compared with Controls. Controls showed significantly larger (more positive) P2 and P3 amplitudes, regardless of stimuli valence, compared with youth with anxiety disorders. ERPs observed during the dot probe task indicate youth with anxiety disorders display distinct neural processing during early stage attentional orienting and processing of faces; this was not the case for Controls. Such results suggest these ERP components may have potential as biomarkers of anxiety disorders in youth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

DSM-IV-TR:

Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision

ADIS for DSM-IV: C/P:

Anxiety Disorders Interview Schedule for DSM-IV: Child and Parent Versions

ERPs:

event-related potentials

EEG:

electroencephalogram

References

  • Association, A. P. (2000). Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition (text revision).

  • Balconi, M., & Lucchiari, C. (2005). Event-related potentials related to normal and morphed emotional faces. The Journal of Psychology, 139(2), 176–192.

    Article  PubMed  Google Scholar 

  • Bar-Haim, Y. (2010). Research review: Attention bias modification (ADM): A novel treatment for anxiety disorders (Vol. 51, pp. 859–870). United Kingdom United Kingdom: Wiley-Blackwell Publishing Ltd. Blackwell Publishing.

    Google Scholar 

  • Bar-Haim, Y., Lamy, D., & Glickman, S. (2005). Attentional bias in anxiety: A behavioral and ERP study. Brain and Cognition, 59(1), 11–22 http://dx.doi.org.ezproxy.fiu.edu/10.1016/j.bandc.2005.03.005.

    Article  PubMed  Google Scholar 

  • Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M., & van Ijzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133(1), 1–1-24. https://doi.org/10.1037/0033-2909.133.1.1.

    Article  PubMed  Google Scholar 

  • Batty, M., & Taylor, M. J. (2003). Early processing of the six basic facial emotional expressions. Cognitive Brain Research, 17(3), 613–620.

    Article  PubMed  Google Scholar 

  • Batty, M., & Taylor, M. J. (2006). The development of emotional face processing during childhood. Developmental Science, 9(2), 207–220.

    Article  PubMed  Google Scholar 

  • Benoit, K. E., McNally, R. J., Rapee, R. M., Gamble, A. L., & Wiseman, A. L. (2007). Processing of emotional faces in children and adolescents with anxiety disorders. Behaviour Change, 24(4), 183–194 http://dx.doi.org.ezproxy.fiu.edu/10.1375/bech.24.4.183.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. (1997). The screen for child anxiety related emotional disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child & Adolescent Psychiatry, 36(4), 545–553.

    Article  Google Scholar 

  • Birmaher, B., Brent, D. A., Chiappetta, L., Bridge, J., Monga, S., & Baugher, M. (1999). Psychometric properties of the screen for child anxiety related emotional disorders (SCARED): A replication study. Journal of the American Academy of Child & Adolescent Psychiatry, 38(10), 1230–1236.

    Article  Google Scholar 

  • Bruin, K., Kenemans, J., Verbaten, M., & Van der Heijden, A. (2000). Habituation: An event-related potential and dipole source analysis study. International Journal of Psychophysiology, 36(3), 199–209.

    Article  PubMed  Google Scholar 

  • Carretié, L., Mercado, F., Hinojosa, J. A. J. A., Martín-Loeches, M., & Sotillo, M. (2004). Valence-related vigilance biases in anxiety studied through event-related potentials. Journal of Affective Disorders, 78(2), 119–130. https://doi.org/10.1016/S0165-0327(02)00242-2.

    Article  PubMed  Google Scholar 

  • Cisler, J. M., & Koster, E. H. W. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clinical Psychology Review, 30, 203–216.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Dennis, T. A., & Chen, C. C. (2009). Trait anxiety and conflict monitoring following threat: An ERP study. Psychophysiology, 46(1), 122–131.

    Article  PubMed  Google Scholar 

  • Dudeney, J., Sharpe, L., & Hunt, C. (2015). Attentional bias towards threatening stimuli in children with anxiety: A meta-analysis. Clinical Psychology Review, 40, 66–75.

    Article  PubMed  Google Scholar 

  • Eimer, M. (2000). The face-specific N170 component reflects late stages in the structural encoding of faces. Neuroreport, 11(10), 2319–2324.

    Article  PubMed  Google Scholar 

  • Éismont, E., Lutsyuk, N., & Pavlenko, V. (2009). Reflection of anxiety in the characteristics of evoked EEG potentials in 10-to 11-year-old children. Neurophysiology, 41(6), 435–442.

    Article  Google Scholar 

  • Eldar, S., Yankelevitch, R., Lamy, D., & Bar-Haim, Y. (2010). Enhanced neural reactivity and selective attention to threat in anxiety. Biological Psychology, 85(2), 252–257. https://doi.org/10.1016/j.biopsycho.2010.07.010.

    Article  PubMed  Google Scholar 

  • Falkenstein, M., Hohnsbein, J., & Hoormann, J. (1994). Event-related potential correlates of errors in reaction tasks. Electroencephalography and Clinical Neurophysiology. Supplement, 44, 287–296.

    Google Scholar 

  • Falkenstein, M., Hoormann, J., & Hohnsbein, J. (1999). ERP components in Go/Nogo tasks and their relation to inhibition. Acta psychologica, 101(2), 267–291.

    Article  PubMed  Google Scholar 

  • Helfinstein, S. M., White, L. K., Bar-Haim, Y., & Fox, N. A. (2008). Affective primes suppress attention bias to threat in socially anxious individuals. Behaviour Research and Therapy, 46(7), 799–810 https://doi.org/10.1016/j.brat.2008.03.011.

  • Holmes, A., Nielsen, M. K., & Green, S. (2008). Effects of anxiety on the processing of fearful and happy faces: An event-related potential study. Biological Psychology, 77(2), 159–173.

    Article  PubMed  Google Scholar 

  • Hum, K. M., Manassis, K., & Lewis, M. D. (2013). Neural mechanisms of emotion regulation in childhood anxiety. Journal of Child Psychology and Psychiatry, 54(5), 552–564 http://dx.doi.org.ezproxy.fiu.edu/10.1111/j.1469-7610.2012.02609.x.

    Article  PubMed  Google Scholar 

  • Huster, R. J., Enriquez-Geppert, S., Lavallee, C. F., Falkenstein, M., & Herrmann, C. S. (2013). Electroencephalography of response inhibition tasks: Functional networks and cognitive contributions. International Journal of Psychophysiology, 87(3), 217–233.

    Article  PubMed  Google Scholar 

  • Kappenman, E. S., Farrens, J. L., Luck, S. J., & Proudfit, G. H. (2014). Behavioral and ERP measures of attentional bias to threat in the dot-probe task: Poor reliability and lack of correlation with anxiety. Frontiers in Psychology, 5, 1368.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., et al. (1997). Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry, 36(7), 980–988.

    Article  Google Scholar 

  • Kolassa, I.-T., & Miltner, W. H. (2006). Psychophysiological correlates of face processing in social phobia. Brain Research, 1118(1), 130–141.

  • Kujawa, A., MacNamara, A., Fitzgerald, K. D., Monk, C. S., & Phan, K. L. (2015). Enhanced neural reactivity to threatening faces in anxious youth: Evidence from event-related potentials. Journal of Abnormal Child Psychology. https://doi.org/10.1007/s10802-015-0029-4

  • Lonigan, C. J., Vasey, M. W., Phillips, B. M., & Hazen, R. A. (2004). Temperament, anxiety, and the processing of threat-relevant stimuli. Journal of Clinical Child and Adolescent Psychology, 33(1), 8–20.

    Article  PubMed  Google Scholar 

  • Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: An open-source toolbox for the analysis of event-related potentials. Frontiers in Human Neuroscience, 8.

  • MacLeod, C., Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95(1), 15–20.

    Article  PubMed  Google Scholar 

  • MacNamara, A., Kappenman, E. S., Black, S. R., Bress, J. N., & Hajcak, G. (2013). Integratived behavioral and electrocortical measures of attentional bias toward threat. In K. C. Barrett, N. A. Fox, G. A. Morgan, D. J. Fidler, & L. A. Daunhauer (Eds.), Handbook of self-regulatory processes in development: New directions and international perspectives (pp. 215–243). New York: Psychology Press.

    Google Scholar 

  • Mathews, A., & MacLeod, C. (2002). Induced processing biases have causal effects on anxiety. Cognition and Emotion, 16(3), 331–354.

    Article  Google Scholar 

  • Mogg, K., & Bradley, B. P. (1998). A cognitive-motivational analysis of anxiety. Behaviour Research and Therapy, 36(9), 809–848.

    Article  PubMed  Google Scholar 

  • Moser, J. S., Huppert, J. D., Duval, E., & Simons, R. F. (2008). Face processing biases in social anxiety: An electrophysiological study. Biological Psychology, 78(1), 93–103.

    Article  PubMed  Google Scholar 

  • Mueller, E. M., Hofmann, S. G., Santesso, D. L., Meuret, A. E., Bitran, S., & Pizzagalli, D. A. (2009). Electrophysiological evidence of attentional biases in social anxiety disorder. Psychological Medicine, 39(7), 1141–1152. https://doi.org/10.1017/S0033291708004820.

    Article  PubMed  Google Scholar 

  • Mühlberger, A., Wieser, M. J., Herrmann, M. J., Weyers, P., Tröger, C., & Pauli, P. (2009). Early cortical processing of natural and artificial emotional faces differs between lower and higher socially anxious persons. Journal of Neural Transmission, 116(6), 735–746.

    Article  PubMed  Google Scholar 

  • O’Toole, L., & Dennis, T. A. (2012). Attention training and the threat bias: An ERP study. Brain and Cognition, 78(1), 63–73 http://dx.doi.org.ezproxy.fiu.edu/10.1016/j.bandc.2011.10.007.

    Article  PubMed  Google Scholar 

  • O'Toole, L. J., DeCicco, J. M., Berthod, S., & Dennis, T. A. (2013). The N170 to angry faces predicts anxiety in typically developing children over a two-year period. Developmental Neuropsychology, 38(5), 352–363.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pine, D. S. (2011). The brain and behavior in childhood and adolescent anxiety disorders. In Anxiety disorders in children and adolescents (pp. 179–197).

    Chapter  Google Scholar 

  • Pourtois, G., Grandjean, D., Sander, D., & Vuilleumier, P. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14(6), 619–633.

    Article  PubMed  Google Scholar 

  • Pourtois, G., Dan, E. S., Grandjean, D., Sander, D., & Vuilleumier, P. (2005). Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked-potentials mapping. Human Brain Mapping, 26(1), 65–79 http://dx.doi.org.ezproxy.fiu.edu/10.1002/hbm.20130.

    Article  PubMed  Google Scholar 

  • Price, R. B., Siegle, G. J., Silk, J. S., Ladouceur, C., McFarland, A., Dahl, R. E., & Ryan, N. D. (2013). Sustained neural alterations in anxious youth performing an attentional bias task: A pupilometry study. Depression and Anxiety, 30(1), 22–30 http://dx.doi.org.ezproxy.fiu.edu/10.1002/da.21966.

    Article  PubMed  Google Scholar 

  • Rossignol, M., Campanella, S., Maurage, P., Heeren, A., Falbo, L., & Philippot, P. (2012). Enhanced perceptual responses during visual processing of facial stimuli in young socially anxious individuals. Neuroscience letters, 526(1), 68–73.

    Article  PubMed  Google Scholar 

  • Roy, A. K., Fudge, J. L., Kelly, C., Perry, J. S., Daniele, T., Carlisi, C., et al. (2013). Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 52(3), 290–299 e292.

    Article  Google Scholar 

  • Salum, G., Mogg, K., Bradley, B., Gadelha, A., Pan, P., Tamanaha, A., . . . Polanczyk, G. (2013). Threat bias in attention orienting: Evidence of specificity in a large community-based study. Psychological Medicine, 43(04), 733–745.

    Article  PubMed  Google Scholar 

  • Segalowitz, S. J., Santesso, D. L., & Jetha, M. K. (2010). Electrophysiological changes during adolescence: A review. Brain and Cognition, 72(1), 86–100.

    Article  PubMed  Google Scholar 

  • Silverman, & Albano, A. M. (1996). Anxiety Disorders Interview Schedule for DSM-IV.: Parent interview schedule (Vol. 1): Oxford University Press.

  • Silverman, W. K., Saavedra, L. M., & Pina, A. A. (2001). Test-retest reliability of anxiety symptoms and diagnoses with the anxiety disorders interview schedule for DSM-IV: Child and parent versions. Journal of the American Academy of Child and Adolescent Psychiatry, 40(8), 937–944. https://doi.org/10.1097/00004583-200108000-00016.

    Article  PubMed  Google Scholar 

  • SPSS, I. (2013). IBM SPSS statistics 22. IBM SPSS Inc: Algorithms. Chicago.

    Google Scholar 

  • Susa, G., Pitică, I., Benga, O., & Miclea, M. (2012). The self regulatory effect of attentional control in modulating the relationship between attentional biases toward threat and anxiety symptoms in children. Cognition and Emotion, 26(6), 1069–1083. http://dx.doi.org.ezproxy.fiu.edu/10.1080/02699931.2011.638910.

    Article  PubMed  Google Scholar 

  • Suway, J. G., White, L. K., Vanderwert, R. E., Bar-Haim, Y., Pine, D. S., & Fox, N. A. (2013). Modification of threat-processing in non-anxious individuals: A preliminary behavioral and ERP study. Journal of Behavior Therapy and Experimental Psychiatry, 44(3), 285–292 http://dx.doi.org.ezproxy.fiu.edu/10.1016/j.jbtep.2012.11.006.

    Article  PubMed  Google Scholar 

  • Taylor, M. J., Edmonds, G. E., McCarthy, G., & Allison, T. (2001). Eyes first! Eye processing develops before face processing in children. Neuroreport, 12(8), 1671–1676.

    Article  PubMed  Google Scholar 

  • Thai, N., Taber-Thomas, B. C., & Pérez-Edgar, K. E. (2016). Neural correlates of attention biases, behavioral inhibition, and social anxiety in children: An ERP study. Developmental Cognitive Neuroscience, 19, 200–210.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., et al. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242–249.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vasey, M. W., Daleiden, E. L., Williams, L. L., & Brown, L. M. (1995). Biased attention in childhood anxiety disorders: A preliminary study. Journal of Abnormal Child Psychology, 23(2), 267–279 http://dx.doi.org.ezproxy.fiu.edu/10.1007/BF01447092.

    Article  PubMed  Google Scholar 

  • Verleger, R. (1997). On the utility of P3 latency as an index of mental chronometry. Psychophysiology, 34(2), 131–156.

    Article  PubMed  Google Scholar 

  • Waters, A. M., Lipp, O. V., & Spence, S. H. (2004). Attentional bias toward fear-related stimuli: An investigation with nonselected children and adults and children with anxiety disorders. Journal of Experimental Child Psychology, 89(4), 320–337.

    Article  PubMed  Google Scholar 

  • Waters, A. M., Mogg, K., Bradley, B. P., & Pine, D. S. (2008). Attentional bias for emotional faces in children with generalized anxiety disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 47(4), 435–442.

    Article  Google Scholar 

  • Weissman, A. S., Chu, B. C., Reddy, L. A., & Mohlman, J. (2012). Attention mechanisms in children with anxiety disorders and in children with attention deficit hyperactivity disorder: Implications for research and practice. Journal of Clinical Child and Adolescent Psychology, 41(2), 117–126 http://dx.doi.org.ezproxy.fiu.edu/10.1080/15374416.2012.651993.

    Article  PubMed  Google Scholar 

  • White, L. K., Britton, J. C., Sequeira, S., Ronkin, E. G., Chen, G., Bar-Haim, Y., et al. (2016). Behavioral and neural stability of attention bias to threat in healthy adolescents. Neuroimage, 136, 84–93.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wren, F. J., Berg, E. A., Heiden, L. A., Kinnamon, C. J., Ohlson, L. A., Bridge, J. A., . . . Bernal, M. P. (2007). Childhood anxiety in a diverse primary care population: parent-child reports, ethnicity and SCARED factor structure. Journal of the American Academy of Child & Adolescent Psychiatry, 46(3), 332–340.

    Article  Google Scholar 

Download references

Acknowledgements

Work on this project was supported by National Institute of Mental Health grants R34 MH097931 and R01 MH079943 to Jeremy W. Pettit and Wendy K. Silverman, a National Institute of Mental Health grant F31 MH105144-01A1 to Michele Bechor and a National Institute on Drug Abuse K01DA034125 grant to Michael J. Crowley. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michele Bechor.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bechor, M., Ramos, M.L., Crowley, M.J. et al. Neural Correlates of Attentional Processing of Threat in Youth with and without Anxiety Disorders. J Abnorm Child Psychol 47, 119–129 (2019). https://doi.org/10.1007/s10802-018-0424-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10802-018-0424-8

Keywords

Navigation