Hostname: page-component-76d6cb85b7-pn7tm Total loading time: 0 Render date: 2026-07-16T08:17:31.048Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental pathways to social anxiety and irritability: The role of the ERN

Published online by Cambridge University Press:  28 October 2019

Courtney A. Filippi ,
Anni R. Subar ,
Jessica F. Sachs ,
Katharina Kircanski ,
George Buzzell ,
David Pagliaccio ,
Rany Abend ,
Nathan A. Fox ,
Ellen Leibenluft  and
Daniel S. Pine
Courtney A. Filippi*
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
Anni R. Subar
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
Jessica F. Sachs
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
Katharina Kircanski
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
George Buzzell
Affiliation:
Department of Human Development and Quantitative Methodology, University of Maryland, College Park, MD20742, USA
David Pagliaccio
Affiliation:
Division of Child & Adolescent Psychiatry, New York State Psychiatric Institute, Columbia University, New York, NY10032, USA
Rany Abend
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
Nathan A. Fox
Affiliation:
Department of Human Development and Quantitative Methodology, University of Maryland, College Park, MD20742, USA
Ellen Leibenluft
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
Daniel S. Pine
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD20892, USA
*
Author for Correspondence: Courtney Filippi, 9000 Rockville Pike, Bethesda, MD, 20892. E-mail: courtney.filippi@nih.gov
Get access Rights & Permissions [Opens in a new window]

Abstract

Early behaviors that differentiate later biomarkers for psychopathology can guide preventive efforts while also facilitating pathophysiological research. We tested whether error-related negativity (ERN) moderates the link between early behavior and later psychopathology in two early childhood phenotypes: behavioral inhibition and irritability. From ages 2 to 7 years, children (n = 291) were assessed longitudinally for behavioral inhibition (BI) and irritability. Behavioral inhibition was assessed via maternal report and behavioral responses to novelty. Childhood irritability was assessed using the Child Behavior Checklist. At age 12, an electroencephalogram (EEG) was recorded while children performed a flanker task to measure ERN, a neural indicator of error monitoring. Clinical assessments of anxiety and irritability were conducted using questionnaires (i.e., Screen for Child Anxiety Related Disorders and Affective Reactivity Index) and clinical interviews. Error monitoring interacted with early BI and early irritability to predict later psychopathology. Among children with high BI, an enhanced ERN predicted greater social anxiety at age 12. In contrast, children with high childhood irritability and blunted ERN predicted greater irritability at age 12. This converges with previous work and provides novel insight into the specificity of pathways associated with psychopathology.

Keywords

behavioral inhibitiondevelopmental pathwaysERNirritabilitypsychopathology

Information

Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Issue 3 , August 2020 , pp. 897 - 907
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Amodio, D. M., Jost, J. T., Master, S. L., & Yee, C. M. (2007). Neurocognitive correlates of liberalism and conservatism. Nature neuroscience, 10, 1246–1247. https://doi.org/10.1038/nn1979CrossRefGoogle ScholarPubMed
Barker, T. V. (2016). Social influences of error monitoring (Doctoral dissertation, University of Maryland, College Park, Maryland, United States, 2016). Available from ProQuest Dissertations and Theses. (AAT U10128666).Google Scholar
Barker, T. V., Troller-Renfree, S., Pine, D. S., & Fox, N. A. (2015). Individual differences in social anxiety affect the salience of errors in social contexts. Cognitive, Affective, & Behavioral Neuroscience, 15, 723–735. https://doi.org/10.3758/s13415-015-0360-9Google Scholar
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624–652.CrossRefGoogle ScholarPubMed
Brotman, M. A., Kircanski, K., Stringaris, A., Pine, D. S., & Leibenluft, E. (2017). Irritability in youths: A translational model. American Journal of Psychiatry, 174, 520–532. https://doi.org//10.1176/appi.ajp.2016.16070839CrossRefGoogle ScholarPubMed
Buzzell, G. A., Richards, J. E., White, L. K., Barker, T. V., Pine, D. S., & Fox, N. A. (2017). Development of the error-monitoring system from ages 9–35: Unique insight provided by MRI-constrained source localization of EEG. NeuroImage, 157,13–26. https://doi.org/10.1016/j.neuroimage.2017.05.045CrossRefGoogle ScholarPubMed
Buzzell, G. A., Troller-Renfree, S. V., Barker, T. V., Bowman, L. C., Chronis-Tuscano, A., Henderson, H. A., … Fox, N. A. (2017). A neurobehavioral mechanism linking behaviorally inhibited temperament and later adolescent social anxiety. Journal of the American Academy of Child & Adolescent Psychiatry, 56, 1097–1105. https://doi.org/10.1016/j.jaac.2017.10.007CrossRefGoogle ScholarPubMed
Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., … & Fox, N. A. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 928–935. https://doi.org/10.1097/CHI.0b013e3181ae09dfCrossRefGoogle ScholarPubMed
Clauss, J. A., & Blackford, J. U. (2012). Behavioral inhibition and risk for developing social anxiety disorder: A meta-analytic study. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 1066–1075. https://doi.org/10.1016/j.jaac.2012.08.002CrossRefGoogle ScholarPubMed
Debener, S. (2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. Journal of Neuroscience, 25, 11730–11737. https://doi.org/10.1523/JNEUROSCI.3286-05.2005CrossRefGoogle ScholarPubMed
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, 9–21.CrossRefGoogle ScholarPubMed
Dougherty, L. R., Smith, V. C., Bufferd, S. J., Stringaris, A., Leibenluft, E., Carlson, G. A., & Klein, D. N. (2013). Preschool irritability: Longitudinal associations with psychiatric disorders at age 6 and parental psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 1304–1313. https://doi.org/10.1016/j.jaac.2013.09.007CrossRefGoogle ScholarPubMed
Fox, N.A., Henderson, H.A., Rubin, K.H., Calkins, S.D., Schmidt, L.A. (2001). Continuity and discontinuity of behavioral inhibition and exuberance: Psychophysiological and behavioral influences across the first four years of life. Child Development, 72, 1–21. https://doi.org/10.1111/1467-8624.00262CrossRefGoogle ScholarPubMed
Fox, N. A., & Pine, D. S. (2012). Temperament and the emergence of anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 125–128. http://doi.org/10.1016/j.jaac.2011.10.006CrossRefGoogle ScholarPubMed
Fox, N. A., Snidman, N., Haas, S. A., Degnan, K. A., & Kagan, J. (2015). The relations between reactivity at 4 months and behavioral inhibition in the second year: Replication across three independent samples. Infancy, 20, 98–114. https://doi.org/10.1111/infa.12063CrossRefGoogle ScholarPubMed
Franken, I. H., van Strien, J. W., Franzek, E. J., & van de Wetering, B. J. (2007). Error-processing deficits in patients with cocaine dependence. Biological Psychology, 75, 45–51. https://doi.org/10.1016/j.biopsycho.2006.11.003CrossRefGoogle ScholarPubMed
Gehring, W. J., Goss, B., Coles, M. G., Meyer, D. E., & Donchin, E. (1993). A neural system for error detection and compensation. Psychological science, 4, 385–390. https://doi.org/10.1111/j.1467-9280.1993.tb00586.xCrossRefGoogle Scholar
Hajcak, G., McDonald, N., & Simons, R.F. (2003). To err is autonomic: Error-related brain potentials, ANS activity, and post-error compensatory behavior. Psychophysiology, 40, 895–903. https://doi.org/10.1111/1469-8986.00107CrossRefGoogle ScholarPubMed
Hajcak, G., & Simons, R. F. (2002). Error-related brain activity in obsessive–compulsive undergraduates. Psychiatry Research, 110, 63–72. https://doi.org/10.1016/S0165-1781(02)00034-3CrossRefGoogle ScholarPubMed
Hall, J. R., Bernat, E. M., & Patrick, C. J. (2007). Externalizing psychopathology and the error-related negativity. Psychological science, 18, 326–333.CrossRefGoogle ScholarPubMed
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 (OCD). Journal of the American Academy of Child and Adolescent Psychiatry, 51, 902–910. http://doi.org/10.1016/j.jaac.2012.06.019CrossRefGoogle Scholar
Hayes, A.F. (2018). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach (2nd edition). New York: Guilford Press.Google Scholar
Henderson, H. A., Pine, D. S., & Fox, N. A. (2015). Behavioral inhibition and developmental risk: A dual-processing perspective. Neuropsychopharmacology, 40, 207. https://doi.org/10.1038/npp.2014.189CrossRefGoogle ScholarPubMed
Holmes, A. J., & Pizzagalli, D. A. (2008). Response conflict and frontocingulate dysfunction in unmedicated participants with major depression. Neuropsychologia, 46, 2904–2913. http://doi.org/10.1016/j.neuropsychologia.2008.05.028CrossRefGoogle ScholarPubMed
Hommer, R. E., Meyer, A., Stoddard, J., Connolly, M. E., Mogg, K., Bradley, B. P., … & Brotman, M. A. (2014). Attention bias to threat faces in severe mood dysregulation. Depression and Anxiety, 31, 559–565. https://doi.org/10.1002/da.22145CrossRefGoogle ScholarPubMed
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-SADSPL): Initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980–988. https://doi.org/10.1097/00004583-199707000-00021CrossRefGoogle Scholar
Kessel, E. M., Meyer, A., Hajcak, G., Dougherty, L. R., Torpey-Newman, D. C., Carlson, G. A., & Klein, D. N. (2016). Transdiagnostic factors and pathways to multifinality: The error-related negativity predicts whether preschool irritability is associated with internalizing versus externalizing symptoms at age 9. Development and Psychopathology, 28, 913–926.CrossRefGoogle ScholarPubMed
Kircanski, K., Zhang, S., Stringaris, A., Wiggins, J. L., Towbin, K. E., Pine, D. S., … & Brotman, M. A. (2017). Empirically derived patterns of psychiatric symptoms in youth: A latent profile analysis. Journal of Affective Disorders, 216, 109–116. https://doi.org/10.1016/j.jad.2016.09.016CrossRefGoogle ScholarPubMed
Ladouceur, C. D., Dahl, R. E., Birmaher, B., Axelson, D. A., & Yan, 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.CrossRefGoogle ScholarPubMed
Lahat, A., Lamm, C., Chronis-Tuscano, A., Pine, D. S., Henderson, H. A., & Fox, N. A. (2014). Early behavioral inhibition and increased error monitoring predict later social phobia symptoms in childhood. Journal of the American Academy of Child and Adolescent Psychiatry, 53, 447–455. http://doi.org/10.1016/j.jaac.2013.12.019CrossRefGoogle ScholarPubMed
Lahat, A., Walker, O. L., Lamm, C., Degnan, K. A., Henderson, H. A., & Fox, N. A. (2014). Cognitive conflict links behavioral inhibition and social problem solving during social exclusion in childhood. Infant and Child Development, 23, 273–282. http://doi.org/10.1002/icd.1845CrossRefGoogle ScholarPubMed
Leibenluft, E. (2017). Pediatric irritability: A systems neuroscience approach. Trends in Cognitive Sciences, 21, 277–289. https://doi.org/10.1016/j.tics.2017.02.002CrossRefGoogle ScholarPubMed
Leibenluft, E., Cohen, P., Gorrindo, T., Brook, J. S., & Pine, D. S. (2006). Chronic versus episodic irritability in youth: A community-based, longitudinal study of clinical and diagnostic associations. Journal of Child & Adolescent Psychopharmacology, 16, 456–466. https://doi.org/10.1089/cap.2006.16.456CrossRefGoogle ScholarPubMed
Leibenluft, E., & Stoddard, J. (2013). The developmental psychopathology of irritability. Development and Psychopathology, 25, 1473–1487. https://doi.org/10.1017/S0954579413000722CrossRefGoogle ScholarPubMed
Luu, P., Collins, P., & Tucker, D. M. (2000). Mood, personality, and self-monitoring: Negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. Journal of Experimental Psychology: General, 129, 43–60.CrossRefGoogle ScholarPubMed
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. http://doi.org/10.1016/j.biopsych.2008.10.043CrossRefGoogle ScholarPubMed
Meyer, A., Weinberg, A., Klein, D. N., & Hajcak, G. (2012). 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. https://doi.org/10.1016/j.dcn.2011.09.005CrossRefGoogle ScholarPubMed
Moffitt, T. E., Arseneault, L., Belsky, D., Dickson, N., Hancox, R. J., Harrington, H., … & Sears, M. R. (2011). A gradient of childhood self-control predicts health, wealth, and public safety. Proceedings of the National Academy of Sciences, 108, 2693–2698. https://doi.org/10.1073/pnas.1010076108CrossRefGoogle ScholarPubMed
Mognon, A., Jovicich, J., Bruzzone, L., & Buiatti, M. (2011). ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. Psychophysiology, 48, 229–240.CrossRefGoogle ScholarPubMed
Muris, P, Dreessen, L, Bögels, S, Weckx, M, van Melick, M. (2004). A questionnaire for screening a broad range of DSM-defined anxiety disorder symptoms in clinically referred children and adolescents. Journal of Child Psychology and Psychiatry. 45, 813–820. https://doi.org/10.1111/j.1469-7610.2004.00274.xCrossRefGoogle ScholarPubMed
Nolan, H., Whelan, R., & Reilly, R. B. (2010). FASTER: Fully automated statistical thresholding for EEG artifact rejection. Journal of Neuroscience Methods, 192, 152–162. https://doi.org/10.1016/j.jneumeth.2010.07.015CrossRefGoogle ScholarPubMed
Olvet, D. M., & Hajcak, G. (2008). The error-related negativity (ERN) and psychopathology: Toward an Endophenotype. Clinical Psychology Review, 28, 1343–1354. http://doi.org/10.1016/j.cpr.2008.07.003CrossRefGoogle ScholarPubMed
Pagliaccio, D., Pine, D. S., Barch, D. M., Luby, J. L., & Leibenluft, E. (2018). Irritability trajectories, cortical thickness, and clinical outcomes in a sample enriched for preschool depression. Journal of the American Academy of Child & Adolescent Psychiatry, 57, 336–342.e6. https://doi.org/10.1016/j.jaac.2018.02.010.CrossRefGoogle Scholar
Pailing, P. E., Segalowitz, S. J., Dywan, J., & Davies, P. L. (2002). Error negativity and response control. Psychophysiology, 39, 198–206. https://doi.org/10.1017/S0048577202010247CrossRefGoogle ScholarPubMed
Pérez-Edgar, K., Reeb-Sutherland, B. C., McDermott, J. M., White, L. K., Henderson, H. A., Degnan, K. A., … Fox, N. A. (2011). Attention biases to threat link behavioral inhibition to social withdrawal over time in very young children. Journal of Abnormal Child Psychology, 39, 885–895. http://doi.org/10.1007/s10802-011-9495-5CrossRefGoogle ScholarPubMed
Pontifex, M. B., Scudder, M. R., Brown, M. L., O'Leary, K. C., Wu, C.-T., Themanson, J. R., & Hillman, C. H. (2010). On the number of trials necessary for stabilization of error-related brain activity across the life span. Psychophysiology, 47, 767–773.Google ScholarPubMed
Salum, G. A., Mogg, K., Bradley, B. P., Stringaris, A., Gadelha, A., Pan, P. M., & Leibenluft, E. (2017). Association between irritability and bias in attention orienting to threat in children and adolescents. Journal of Child Psychology and Psychiatry, 58, 595–602.CrossRefGoogle ScholarPubMed
Savage, J., Verhulst, B., Copeland, W., Althoff, R. R., Lichtenstein, P., & Roberson-Nay, R. (2015). A genetically informed study of the longitudinal relation between irritability and anxious/depressed symptoms. Journal of the American Academy of Child & Adolescent Psychiatry, 54, 377–384. https://doi.org/10.1016/j.jaac.2015.02.010CrossRefGoogle ScholarPubMed
Snyder, H. R., Miyake, A., & Hankin, B. L. (2015). Advancing understanding of executive function impairments and psychopathology: Bridging the gap between clinical and cognitive approaches. Frontiers in Psychology, 6, 328. http://doi.org/10.3389/fpsyg.2015.00328CrossRefGoogle ScholarPubMed
Steele, V. R., Anderson, N. E., Claus, E. D., Bernat, E. M., Rao, V., Assaf, M., … Kiehl, K. A. (2016). Neuroimaging measures of error-processing: Extracting reliable signals from event-related potentials and functional magnetic resonance imaging. NeuroImage, 132, 247–260.CrossRefGoogle ScholarPubMed
Stoddard, J., Stringaris, A., Brotman, M. A., Montville, D., Pine, D. S., & Leibenluft, E. (2014). Irritability in child and adolescent anxiety disorders. Depression and Anxiety, 31, 566–573. https://doi.org/10.1002/da.22151CrossRefGoogle ScholarPubMed
Stringaris, A., Goodman, R., Ferdinando, S., Razdan, V., Muhrer, E., Leibenluft, E., & Brotman, M. A. (2012). The Affective Reactivity Index: A concise irritability scale for clinical and research settings. Journal of Child Psychology and Psychiatry, 53, 1109–1117. https://doi.org/10.1111/j.1469-7610.2012.02561.xCrossRefGoogle ScholarPubMed
Velez, C. N., Johnson, J. I. M., & Cohen, P. (1989). A longitudinal analysis of selected risk factors for childhood psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 28, 861–864. https://doi.org/10.1097/00004583-198911000-00009CrossRefGoogle ScholarPubMed
Vidal-Ribas, P., Brotman, M. A., Valdivieso, I., Leibenluft, E., & Stringaris, A. (2016). The status of irritability in psychiatry: A conceptual and quantitative review. Journal of the American Academy of Child & Adolescent Psychiatry, 55, 556–570. https://doi.org/10.1016/j.jaac.2016.04.014CrossRefGoogle ScholarPubMed
White, L. K., McDermott, J. M., Degnan, K. A., Henderson, H. A., & Fox, N. A. (2011). Behavioral inhibition and anxiety: The moderating roles of inhibitory control and attention shifting. Journal of Abnormal Child Psychology, 39, 735–747. http://doi.org/10.1007/s10802-011-9490-xCrossRefGoogle ScholarPubMed
Wiggins, J. L., Mitchell, C., Stringaris, A., & Leibenluft, E. (2014). Developmental trajectories of irritability and bidirectional associations with maternal depression. Journal of the American Academy of Child and Adolescent Psychiatry, 53, 1191–1205.e4. http://doi.org/10.1016/j.jaac.2014.08.005CrossRefGoogle ScholarPubMed
Supplementary material: File

Filippi et al. supplementary material

Filippi et al. supplementary material

Download Filippi et al. supplementary material(File)
File 193.1 KB