Neural Correlates of Attentional Processing of Threat in Youth with and without Anxiety Disorders
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.
KeywordsEvent-related potential Youth Anxiety Attention
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
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.
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 was obtained from all individual participants included in the study.
- Association, A. P. (2000). Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition (text revision).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.CrossRefPubMedGoogle 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.CrossRefPubMedGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefPubMedGoogle 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
- 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.
- 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
- 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
- Kolassa, I.-T., & Miltner, W. H. (2006). Psychophysiological correlates of face processing in social phobia. Brain Research, 1118(1), 130–141.Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Silverman, & Albano, A. M. (1996). Anxiety Disorders Interview Schedule for DSM-IV.: Parent interview schedule (Vol. 1): Oxford University Press.Google Scholar
- 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
- 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.CrossRefPubMedGoogle 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.CrossRefPubMedGoogle 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.CrossRefPubMedGoogle 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.CrossRefPubMedGoogle 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.CrossRefGoogle Scholar