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

  • Michele Bechor
  • Michelle L. Ramos
  • Michael J. Crowley
  • Wendy K. Silverman
  • Jeremy W. Pettit
  • Bethany C. Reeb-Sutherland
Article

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.

Keywords

Event-related potential Youth Anxiety Attention 

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

Notes

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.

Compliance with Ethical Standards

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.

References

  1. Association, A. P. (2000). Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition (text revision).Google Scholar
  2. Balconi, M., & Lucchiari, C. (2005). Event-related potentials related to normal and morphed emotional faces. The Journal of Psychology, 139(2), 176–192.CrossRefPubMedGoogle Scholar
  3. 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
  4. 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.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. Batty, M., & Taylor, M. J. (2003). Early processing of the six basic facial emotional expressions. Cognitive Brain Research, 17(3), 613–620.CrossRefPubMedGoogle Scholar
  7. Batty, M., & Taylor, M. J. (2006). The development of emotional face processing during childhood. Developmental Science, 9(2), 207–220.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. Dennis, T. A., & Chen, C. C. (2009). Trait anxiety and conflict monitoring following threat: An ERP study. Psychophysiology, 46(1), 122–131.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. Eimer, M. (2000). The face-specific N170 component reflects late stages in the structural encoding of faces. Neuroreport, 11(10), 2319–2324.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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
  22. Falkenstein, M., Hoormann, J., & Hohnsbein, J. (1999). ERP components in Go/Nogo tasks and their relation to inhibition. Acta psychologica, 101(2), 267–291.CrossRefPubMedGoogle Scholar
  23. 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.
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Kolassa, I.-T., & Miltner, W. H. (2006). Psychophysiological correlates of face processing in social phobia. Brain Research, 1118(1), 130–141.Google Scholar
  30. 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
  31. 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.CrossRefPubMedGoogle Scholar
  32. Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: An open-source toolbox for the analysis of event-related potentials. Frontiers in Human Neuroscience, 8.Google Scholar
  33. MacLeod, C., Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95(1), 15–20.CrossRefPubMedGoogle Scholar
  34. 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
  35. Mathews, A., & MacLeod, C. (2002). Induced processing biases have causal effects on anxiety. Cognition and Emotion, 16(3), 331–354.CrossRefGoogle Scholar
  36. Mogg, K., & Bradley, B. P. (1998). A cognitive-motivational analysis of anxiety. Behaviour Research and Therapy, 36(9), 809–848.CrossRefPubMedGoogle Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pine, D. S. (2011). The brain and behavior in childhood and adolescent anxiety disorders. In Anxiety disorders in children and adolescents (pp. 179–197).CrossRefGoogle Scholar
  43. Pourtois, G., Grandjean, D., Sander, D., & Vuilleumier, P. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14(6), 619–633.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefPubMedGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar
  49. Segalowitz, S. J., Santesso, D. L., & Jetha, M. K. (2010). Electrophysiological changes during adolescence: A review. Brain and Cognition, 72(1), 86–100.CrossRefPubMedGoogle Scholar
  50. Silverman, & Albano, A. M. (1996). Anxiety Disorders Interview Schedule for DSM-IV.: Parent interview schedule (Vol. 1): Oxford University Press.Google Scholar
  51. 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.CrossRefPubMedGoogle Scholar
  52. SPSS, I. (2013). IBM SPSS statistics 22. IBM SPSS Inc: Algorithms. Chicago.Google Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. Verleger, R. (1997). On the utility of P3 latency as an index of mental chronometry. Psychophysiology, 34(2), 131–156.CrossRefPubMedGoogle Scholar
  60. 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.CrossRefPubMedGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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.CrossRefPubMedGoogle Scholar
  63. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of PsychologyFlorida International UniversityMiamiUSA
  2. 2.Yale Child Study CenterYale UniversityNew HavenUSA

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