Skip to main content
Log in

Increased Error-Related Brain Activity in Six-Year-Old Children with Clinical Anxiety

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

Abstract

Anxiety disorders are the most frequently diagnosed form of psychopathology in children and often result in chronic impairment that persists into adulthood. Identifying neurobehavioral correlates of anxiety that appear relatively early in life would inform etiological models of development and allow intervention and prevention strategies to be implemented more effectively. The error-related negativity (ERN), a negative deflection in the event-related potential at fronto-central sites approximately 50 ms following the commission of errors, has been consistently found to be larger among anxious adults. The current study sought to extend these findings to even younger individuals: the ERN was elicited by a Go/NoGo task in 48 six year-old children with a clinical anxiety disorder assessed by diagnostic interview and 48 age-matched controls. In addition to child anxiety disorder, the ERN was examined in relation to maternal history of anxiety disorder, which was previously related to a smaller ERN. Anxious children were characterized by a larger (i.e., more negative) ERN and maternal history of anxiety disorder was associated with a smaller ERN. Thus, the relationship between an increased ERN and clinical anxiety is evident by age 6, and this effect appears independent from an opposing influence of maternal anxiety history on the ERN. These findings support the ERN as a promising neurobehavioral marker of anxiety, and implications are discussed.

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

Notes

  1. A follow-up Repeated-measures ANOVA suggested that the ERN was larger among children with specific phobia compared to controls, at a trend level, F(1, 66) = 3.21, p = 0.08. No other diagnostic group was large enough to perform similar analyses.

  2. The error positivity (Pe) was evaluated on error trials as the average activity at a pooling of Cz, CP1, CP2, and Pz from 200 to 500 ms following response onset. A comparable time window was also evaluated at the same sites on correct trials. Overall, there was a main effect of response type (error vs. correct), F(1, 94) = 76.35, p < 0.001, such that incorrect responses, M = 13.89, SD = 14.08, were significantly more positive than correct responses, M = 3.04, SD = 4.36. Overall electrocortical responses in this time window did not vary by group, F(1, 94) = 0.25, p = 0.25. Statistical analyses did not reveal a significant difference between the ANX and CON groups, F(1, 94) = 0.65, p = 0.42.

  3. Using children randomly chosen with no diagnoses as a control group, we performed the same analysis. Results were consistent with those reported above, the ∆ERN was larger in the ANX group, F(1, 92) = 7.32, p < 0.01, and smaller among children with a history of maternal anxiety, F(1, 92) = 4.74, p < 0.05.

References

  • Achenbach, T. M., McConaughy, S. H., & Howell, C. T. (1987). Child/adolescent behavioral and emotional problems: implications of cross-informant correlations for situational specificity. Psychological Bulletin, 101, 213–232.

    Article  PubMed  Google Scholar 

  • Adleman, N. E., Menon, V., Blasey, C. M., White, C. D., Warsofsky, I. S., Glover, G. H., et al. (2002). A Developmental fMRI study of the stroop color-word task. NeuroImage, 16, 61–75. doi:10.1006/nimg.2001.1046.

    Article  PubMed  Google Scholar 

  • Amodio, D. M., Master, S. L., Yee, C. M., & Taylor, S. E. (2008). Neurocognitive components of the behavioral inhibition and activation systems: implications for theories of self-regulation. Psychophysiology, 45, 11–19. doi:10.1111/j.1469-8986.2007.00609.x.

    PubMed  Google Scholar 

  • Anokhin, A. P., Golosheykin, S., & Heath, A. C. (2008). Heritability of frontal brain function related to action monitoring. Psychophysiology, 45, 524–534. doi:10.1111/j.1469-8986.2008.00664.x.

    Article  PubMed  Google Scholar 

  • Arbel, Y., & Donchin, E. (2011). When a child errs: the ERN and the Pe complex in children. Psychophysiology, 48, 55–63. doi:10.1111/j.1469-8986.2010.01042.x.

    Article  PubMed  Google Scholar 

  • Beesdo, K., Knappe, S., & Pine, D. S. (2009). Anxiety and anxiety disorders in children and adolescents: developmental issues and implications for DSM-V. Psychiatric Clinics of North America, 32, 483–524. doi:10.1016/j.psc.2009.06.002.

    Article  PubMed  Google Scholar 

  • Beesdo, K., Pine, D. S., Lieb, R., & Wittchen, H. (2010). Incidence and risk patterns of anxiety and depressive disorders and categorization of generalized anxiety disorder. Archives of General Psychiatry, 67, 47–57. doi:10.1001/archgenpsychiatry.2009.177.

    Article  PubMed  Google Scholar 

  • Beidel, D. C., & Turner, S. M. (1997). At risk for anxiety: I. Psychopathology in the offspring of anxious parents. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 918–924. doi:10.1097/00004583-199707000-00013.

    Article  PubMed  Google Scholar 

  • Bijl, R. V., Cuijpers, P., & Smit, F. (2002). Psychiatric disorders in adult children of parents with a history of psychopathology. Social Psychiatry And Psychiatric Epidemiology, 37, 7–12.

    Article  PubMed  Google Scholar 

  • Bird, H. R., Gould, M. S., & Staghezza, B. (1992). Aggregating data from multiple informants in child psychiatry epidemiological research. Journal of the American Academy of Child and Adolescent Psychiatry, 31, 78–85.

    Article  PubMed  Google Scholar 

  • Bittner, A., Egger, H. L., Erkanli, A., Jane Costello, E., Foley, D. L., & Angold, A. (2007). What do childhood anxiety disorders predict? Journal of Child Psychology and Psychiatry, 48, 1174–1183.

    Article  PubMed  Google Scholar 

  • Boksem, M. A. S., Tops, M., Wester, A. E., Meijman, T. F., & Lorist, M. M. (2006). Error-related ERP components and individual differences in punishment and reward sensitivity. Brain Research, 1101, 92–101. doi:10.1016/j.brainres.2006.05.004.

    Article  PubMed  Google Scholar 

  • Brooker, R. J., Buss, K. A., & Dennis, T. A. (2011). Error-monitoring brain activity is associated with affective behaviors in young children. Developmental Cognitive Neuroscience, 1, 141–152. doi:10.1016/j.dcn.2010.12.002.

    Article  PubMed  Google Scholar 

  • Carrasco, M., Harbin, S. M., Nienhuis, J. K., Fitzgerald, K. D., Gehring, W. J., & Hanna, G. L. (2013). Increased error-related brain activity in youth with obsessive-compulsive disorder and unaffected siblingseased error–related brain activity in youth with obsessive–compulsive disorder and unaffected siblings. Depression and Anxiety, 30, 39–46.

    Article  PubMed  Google Scholar 

  • Casey, B. J., Tottenham, N., Liston, C., & Durston, S. (2005). Imaging the developing brain: what have we learned about cognitive development? Trends in Cognitive Sciences, 9, 104–110. doi:10.1016/j.tics.2005.01.011.

    Article  PubMed  Google Scholar 

  • Crozier, W. R., & Burnham, M. (1990). Age-related differences in children’s understanding of shyness. British Journal of Developmental Psychology, 8, 179–185. doi:10.1111/j.2044-835X.1990.tb00832.x.

    Article  Google Scholar 

  • Cunningham, M. G., Bhattacharyya, S., & Benes, F. M. (2002). Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. The Journal of Comparative Neurology, 453, 116–130. doi:10.1002/cne.10376.

    Article  PubMed  Google Scholar 

  • Davies, P. L., Segalowitz, S. J., & Gavin, W. J. (2004). Development of response-monitoring ERPs in 7- to 25-year-olds. Developmental Neuropsychology, 25, 355–376.

    Article  PubMed  Google Scholar 

  • Debener, S., Ullsperger, M., Siegel, M., Fiehler, K., von Cramon, D. Y., & Engel, A. K. (2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. The Journal of Neuroscience, 25, 11730–11737. doi:10.1523/jneurosci.3286-05.2005.

    Article  PubMed  Google Scholar 

  • Dehaene, S., Posner, M. I., & Don, M. T. (1994). Localization of a neural system for error detection and compensation. Psychological Science, 5, 303–305.

    Article  Google Scholar 

  • Egger, H. L., Ascher, B. H., & Angold, A. (1999). The preschool age psychiatric assessment: Version 1.1. Durham, NC: Center for Developmental Epidemiology, Department of Psychiatry and Behavioral Sciences, Duke University Medical Center.

  • Egger, Erkanli, A., Keeler, G., Potts, E., Walter, B. K., & Angold, A. (2006). Test-retest reliability of the Preschool Age Psychiatric Assessment (PAPA). Journal of the American Academy of Child and Adolescent Psychiatry, 45, 538–549.

    Article  PubMed  Google Scholar 

  • Emmelkamp, P. M. G., & Wittchen, H. U. (2009). Specific Phobias. In G. Andrews, D. S. Charney, & P. J. Sirovatka (Eds.), Stress-induced and fear circuitry disorders. Refining the research agenda for DSM-V (pp. 77–101). Arlington, VA: APA.

    Google Scholar 

  • Endrass, T., Klawohn, J., Schuster, F., & Kathmann, N. (2008). Overactive performance monitoring in obsessive-compulsive disorder: ERP evidence from correct and erroneous reactions. Neuropsychologia, 46, 1877–1887. doi:10.1016/j.neuropsychologia.2007.12.001.

    Article  PubMed  Google Scholar 

  • Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. The American Journal of Psychiatry, 164, 1476–1488.

    Article  PubMed  Google Scholar 

  • Falkenstein, M., Hohnsbein, J., Hoormann, J., & Blanke, L. (1991). Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. Electroencephalography and Clinical Neurophysiology, 78, 447–455. doi:10.1016/0013-4694(91)90062-9.

    Article  PubMed  Google Scholar 

  • First, M. B., Spitzer, R. L., Gibbon, M., Williams, J. B. W., Davies, M., Borus, J., et al. (1995). The structured clinical interview for DSM-III-R personality disorders (SCID-II). Part II: Multi-site test-retest reliability study. Journal of Personality Disorders, 9, 92–104.

    Article  Google Scholar 

  • Fitzgerald, K. D., Welsh, R. C., Gehring, W. J., Abelson, J. L., Himle, J. A., Liberzon, I., et al. (2005). Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder. Biological Psychiatry, 57, 287–294. doi:10.1016/j.biopsych.2004.10.038.

    Article  PubMed  Google Scholar 

  • Gehring, W. J., Goss, B., Coles, M. G. H., Meyer, D. E., & Donchin, E. (1993). A neural system for error detection and compensation. Psychological Science, 4, 385–390.

    Article  Google Scholar 

  • Gehring, W. J., Himle, J., & Nisenson, L. G. (2000). Action-monitoring dysfunction in obsessive-compulsive disorder. Psychological Science, 11, 1–6.

    Article  PubMed  Google Scholar 

  • Gratton, G., Coles, M. G. H., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55, 468–484. doi:10.1016/0013-4694(83)90135-9.

    Article  PubMed  Google Scholar 

  • Hajcak, G. (2012). What we’ve learned from mistakes. Current Directions in Psychological Science, 21, 101–106. doi:10.1177/0963721412436809.

    Article  Google Scholar 

  • Hajcak, G., McDonald, N., & Simons, R. F. (2003). Anxiety and error-related brain activity. Biological Psychology, 64, 77–90. doi:10.1016/s0301-0511(03)00103-0.

    Article  PubMed  Google Scholar 

  • Hajcak, G., McDonald, N., & Simons, R. F. (2004). Error-related psychophysiology and negative affect. Brain and Cognition, 56, 189–197. doi:10.1016/j.bandc.2003.11.001.

    Article  PubMed  Google Scholar 

  • Hajcak, G., Franklin, M. E., Foa, E. B., & Simons, R. F. (2008). Increased error-related brain activity in pediatric obsessive-compulsive disorder before and after treatment. Amercian Journal of Psychiatry, 165, 116–123. doi:10.1176/appi.ajp.2007.07010143.

    Article  Google Scholar 

  • Hall, J. R., Bernat, E. M., & Patrick, C. J. (2007). Externalizing psychopathology and the error-related negativity. Psychological Science, 18, 326–333.

    Article  PubMed  Google Scholar 

  • Hanna, G. L., Carrasco, M., Harbin, S. M., Nienhuis, J. K., LaRosa, C. E., Chen, P., Gehring, W. J. (2012). Error-related negativity and tic history in pediatric obsessive-compulsive disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 902–910. doi:10.1016/j.jaac.2012.06.019.

    Google Scholar 

  • Holroyd, C. B., Dien, J., & Coles, M. G. H. (1998). Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans. Neuroscience Letters, 242, 65–68. doi:10.1016/s0304-3940(98)00035-4.

    Article  PubMed  Google Scholar 

  • Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 593–602.

    Article  PubMed  Google Scholar 

  • Ladouceur, C. D., Dahl, R. E., Birmaher, B., Axelson, D. A., & Ryan, N. D. (2006). Increased error–related negativity (ERN) in childhood anxiety disorders: ERP and source localization. Journal of Child Psychology and Psychiatry, 47, 1073–1082.

    Article  PubMed  Google Scholar 

  • Last, C. G., Hersen, M., Kazdin, A., Orvaschel, H., & Perrin, S. (1991). Anxiety disorders in children and their families. Archives of General Psychiatry, 48, 928–934.

    Article  PubMed  Google Scholar 

  • Last, C. G., Perrin, S., Hersen, M., & Kazdin, A. E. (1996). A prospective study of childhood anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 35, 1502–1510.

    Article  PubMed  Google Scholar 

  • Mathalon, D. H., Whitfield, S. L., & Ford, J. M. (2003). Anatomy of an error: ERP and fMRI. Biological Psychology, 64, 119–141. doi:10.1016/s0301-0511(03)00105-4.

    Article  PubMed  Google Scholar 

  • McClure, E. B., Monk, C. S., & Nelson, E. E. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64, 97–106. doi:10.1001/archpsyc.64.1.97.

    Article  PubMed  Google Scholar 

  • McDermott, J. M., Perez-Edgar, K., Henderson, H. A., Chronis-Tuscano, A., Pine, D. S., & Fox, N. A. (2009). A history of childhood behavioral inhibition and enhanced response monitoring in adolescence are linked to clinical anxiety. Biological Psychiatry, 65, 445–448. doi:10.1016/j.biopsych.2008.10.043.

    Article  PubMed  Google Scholar 

  • Merikangas, K. R., Dierker, L. C., & Szatmari, P. (1998). Psychopathology among offspring of parents with substance abuse and/or anxiety disorders: a high-risk study. Journal of Child Psychology and Psychiatry, 39, 711–720.

    Article  PubMed  Google Scholar 

  • Meyer, Klein, D. N., Torpey, D. C., Kujawa, A. J., Hayden, E. P., & Sheikh, H. I. (2012a). Additive effects of the dopamine D2 receptor and dopamine transporter genes on the error–related negativity in young children. Genes, Brain, and Behavior, 11, 695–703.

    Article  PubMed  Google Scholar 

  • Meyer, Weinberg, A., Klein, D. N., & Hajcak, G. (2012b). The development of the error-related negativity (ERN) and its relationship with anxiety: Evidence from 8 to 13 year-olds. Developmental Cognitive Neuroscience, 2, 152–161. doi:10.1016/j.dcn.2011.09.005.

    Article  PubMed  Google Scholar 

  • Moser, J. S., Moran, T. P., & Jendrusina, A. A. (2012). Parsing relationships between dimensions of anxiety and action monitoring brain potentials in female undergraduates. Psychophysiology, 49, 3–10. doi:10.1111/j.1469-8986.2011.01279.x.

    Article  PubMed  Google Scholar 

  • Nieuwenhuis, S., Ridderinkhof, K. R., Blom, J., Band, G. P., & Kok, A. (2001). Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. Psychophysiology, 38, 752–760.

    Article  PubMed  Google Scholar 

  • Pailing, P. E., Segalowitz, S. J., Dywan, J., & Davies, P. L. (2002). Error negativity and response control. Psychophysiology, 39, 198–206.

    Article  PubMed  Google Scholar 

  • Paulus, M. P., Hozack, N., Frank, L., & Brown, G. G. (2002). Error rate and outcome predictability affect neural activation in prefrontal cortex and anterior cingulate during decision-making. NeuroImage, 15, 836–846. doi:10.1006/nimg.2001.1031.

    Article  PubMed  Google Scholar 

  • Pine, D. S. (2007). Research review: a neuroscience framework for pediatric anxiety disorders. Journal of Child Psychology and Psychiatry, 48, 631–648.

    Article  PubMed  Google Scholar 

  • Pine, D. S., Cohen, P., Gurley, D., Brook, J., & Ma, Y. (1998). The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Archives of General Psychiatry, 55, 56–64.

    Article  PubMed  Google Scholar 

  • Potts, G. F., George, M. R. M., Martin, L. E., & Barratt, E. S. (2006). Reduced punishment sensitivity in neural systems of behavior monitoring in impulsive individuals. Neuroscience Letters, 397, 130–134.

    Article  PubMed  Google Scholar 

  • Riesel, A., Endrass, T., Kaufmann, C., & Kathmann, N. (2011). Overactive error-related brain activity as a candidate endophenotype for Obsessive-Compulsive Disorder: Evidence from unaffected first-degree relatives. The American Journal of Psychiatry, 168, 317–324. doi:10.1176/appi.ajp.2010.10030416.

    Article  PubMed  Google Scholar 

  • Santesso, D. L., Segalowitz, S. J., & Schmidt, L. A. (2006). Error-related electrocortical responses are enhanced in children with obsessive-compulsive behaviors. Developmental Neuropsychology, 29, 431–445.

    Article  PubMed  Google Scholar 

  • Spence, S. H., Rapee, R., McDonald, C., & Ingram, M. (2001). The structure of anxiety symptoms among preschoolers. Behaviour Research and Therapy, 39, 1293–1316. doi:10.1016/s0005-7967(00)00098-x.

    Article  PubMed  Google Scholar 

  • Torpey, D. C., Hajcak, G., Kim, J., Kujawa, A., & Klein, D. N. (2011). Electrocortical and behavioral measures of response monitoring in young children during a Go/No-Go task. Developmental Psychobiology, 54, 139–150. doi:10.1002/dev.20590.

  • Torpey, D. C., Hajcak, G., Kim, J., Kujawa, A. J., Dyson, M. W., Olino, T. M., & Klein, D. N. (2013). Error-related brain activity in young children: associations with parental anxiety and child temperamental negative emotionality. Journal of Child Psychology and Psychiatry. doi:10.1111/jcpp.12041.

  • Ursu, S., Stenger, V. A., Shear, M. K., Jones, M. R., & Cameron, S. C. (2003). Overactive action monitoring in obsessive-compulsive disorder: evidence from functional magnetic resonance imaging. Psychological Science, 14, 347–353.

    Article  PubMed  Google Scholar 

  • Van Bogaert, P., Wikler, D., Damhaut, P., Szliwowski, H. B., & Goldman, S. (1998). Regional changes in glucose metabolism during brain development from the age of 6 years. NeuroImage, 8, 62–68. doi:10.1006/nimg.1998.0346.

    Article  PubMed  Google Scholar 

  • Van den Bergh, B. R., & Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8–and 9–year–olds. Child Development, 75, 1085–1097.

    Article  PubMed  Google Scholar 

  • Van den Bergh, B. R., Mulder, E. J., Mennes, M., & Glover, V. (2005). Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neuroscience and Biobehavioral Reviews, 29, 237–258.

    Article  PubMed  Google Scholar 

  • Van Der Toorn, S. L. M., Huizink, A. C., Utens, E. M. W. J., Verhulst, F. C., Ormel, J., & Ferdinand, R. F. (2010). Maternal depressive symptoms, and not anxiety symptoms, are associated with positive mother–child reporting discrepancies of internalizing problems in children: a report on the TRAILS Study. European Child & Adolescent Psychiatry, 19, 379–388.

    Article  Google Scholar 

  • Vasey, M., Crnic, K., & Carter, W. (1994). Worry in childhood: a developmental perspective. Cognitive Therapy and Research, 18, 529–549. doi:10.1007/bf02355667.

    Article  Google Scholar 

  • Weinberg, A., & Hajcak, G. (2011a). Electrocortical evidence for vigilance-avoidance in Generalized Anxiety Disorder. Psychophysiology, 48, 842–851. doi:10.1111/j.1469-8986.2010.01149.x.

    Article  PubMed  Google Scholar 

  • Weinberg, A., & Hajcak, G. (2011b). Longer term test–retest reliability of error-related brain activity. Psychophysiology, 48, 1420–1425. doi:10.1111/j.1469-8986.2011.01206.x.

    Article  PubMed  Google Scholar 

  • Weinberg, A., Olvet, D. M., & Hajcak, G. (2010). Increased error-related brain activity in generalized anxiety disorder. Biological Psychology, 85, 472–480. doi:10.1016/j.biopsycho.2010.09.011.

    Article  PubMed  Google Scholar 

  • Weinberg, A., Klein, D. N., & Hajcak, G. (2012). Increased error-related brain activity distinguishes generalized anxiety disorder with and without comorbid major depressive disorder. Journal of Abnormal Psychology, 121, 885–896. doi:10.1037/a0028270.

    Article  PubMed  Google Scholar 

  • Wiersema, J. R., van der Meere, J. J., & Roeyers, H. (2007). Developmental changes in error monitoring: an event-related potential study. Neuropsychologia, 45, 1649–1657. doi:10.1016/j.neuropsychologia.2007.01.004.

    Article  PubMed  Google Scholar 

  • Wittchen, H. U., Lieb, R., Pfister, H., & Schuster, P. (2000). The waxing and waning of mental disorders: evaluating the stability of syndromes of mental disorders in the population. Comprehensive Psychiatry, 41(2 Suppl 1), 122–132.

    Article  PubMed  Google Scholar 

  • Xiao, Z., Wang, J., Zhang, M., Li, H., Tang, Y., Wang, Y., et al. (2011). Error-related negativity abnormalities in generalized anxiety disorder and obsessive–compulsive disorder. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 35, 265–272. doi:10.1016/j.pnpbp.2010.11.022.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexandria Meyer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meyer, A., Hajcak, G., Torpey, D.C. et al. Increased Error-Related Brain Activity in Six-Year-Old Children with Clinical Anxiety. J Abnorm Child Psychol 41, 1257–1266 (2013). https://doi.org/10.1007/s10802-013-9762-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10802-013-9762-8

Keywords

Navigation