Skip to main content Accessibility help
×
Home

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

  • Courtney A. Filippi (a1), Anni R. Subar (a1), Jessica F. Sachs (a1), Katharina Kircanski (a1), George Buzzell (a2), David Pagliaccio (a3), Rany Abend (a1), Nathan A. Fox (a2), Ellen Leibenluft (a1) and Daniel S. Pine (a1)...

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.

Copyright

Corresponding author

Author for Correspondence:Courtney Filippi, 9000 Rockville Pike, Bethesda, MD, 20892. E-mail: courtney.filippi@nih.gov

References

Hide All
Amodio, D. M., Jost, J. T., Master, S. L., & Yee, C. M. (2007). Neurocognitive correlates of liberalism and conservatism. Nature neuroscience, 10, 12461247. https://doi.org/10.1038/nn1979
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).
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, 723735. https://doi.org/10.3758/s13415-015-0360-9
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624652.
Brotman, M. A., Kircanski, K., Stringaris, A., Pine, D. S., & Leibenluft, E. (2017). Irritability in youths: A translational model. American Journal of Psychiatry, 174, 520532. https://doi.org//10.1176/appi.ajp.2016.16070839
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, 157,1326. https://doi.org/10.1016/j.neuroimage.2017.05.045
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, 10971105. https://doi.org/10.1016/j.jaac.2017.10.007
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, 928935. https://doi.org/10.1097/CHI.0b013e3181ae09df
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, 10661075. https://doi.org/10.1016/j.jaac.2012.08.002
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, 1173011737. https://doi.org/10.1523/JNEUROSCI.3286-05.2005
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, 921.
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, 13041313. https://doi.org/10.1016/j.jaac.2013.09.007
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, 121. https://doi.org/10.1111/1467-8624.00262
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, 125128. http://doi.org/10.1016/j.jaac.2011.10.006
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, 98114. https://doi.org/10.1111/infa.12063
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, 4551. https://doi.org/10.1016/j.biopsycho.2006.11.003
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, 385390. https://doi.org/10.1111/j.1467-9280.1993.tb00586.x
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, 895903. https://doi.org/10.1111/1469-8986.00107
Hajcak, G., & Simons, R. F. (2002). Error-related brain activity in obsessive–compulsive undergraduates. Psychiatry Research, 110, 6372. https://doi.org/10.1016/S0165-1781(02)00034-3
Hall, J. R., Bernat, E. M., & Patrick, C. J. (2007). Externalizing psychopathology and the error-related negativity. Psychological science, 18, 326333.
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, 902910. http://doi.org/10.1016/j.jaac.2012.06.019
Hayes, A.F. (2018). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach (2nd edition). New York: Guilford Press.
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.2014.189
Holmes, A. J., & Pizzagalli, D. A. (2008). Response conflict and frontocingulate dysfunction in unmedicated participants with major depression. Neuropsychologia, 46, 29042913. http://doi.org/10.1016/j.neuropsychologia.2008.05.028
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, 559565. https://doi.org/10.1002/da.22145
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, 980988. https://doi.org/10.1097/00004583-199707000-00021
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, 913926.
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, 109116. https://doi.org/10.1016/j.jad.2016.09.016
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, 10731082.
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, 447455. http://doi.org/10.1016/j.jaac.2013.12.019
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, 273282. http://doi.org/10.1002/icd.1845
Leibenluft, E. (2017). Pediatric irritability: A systems neuroscience approach. Trends in Cognitive Sciences, 21, 277289. https://doi.org/10.1016/j.tics.2017.02.002
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, 456466. https://doi.org/10.1089/cap.2006.16.456
Leibenluft, E., & Stoddard, J. (2013). The developmental psychopathology of irritability. Development and Psychopathology, 25, 14731487. https://doi.org/10.1017/S0954579413000722
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, 4360.
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, 445448. http://doi.org/10.1016/j.biopsych.2008.10.043
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, 152161. https://doi.org/10.1016/j.dcn.2011.09.005
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, 26932698. https://doi.org/10.1073/pnas.1010076108
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, 229240.
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, 813820. https://doi.org/10.1111/j.1469-7610.2004.00274.x
Nolan, H., Whelan, R., & Reilly, R. B. (2010). FASTER: Fully automated statistical thresholding for EEG artifact rejection. Journal of Neuroscience Methods, 192, 152162. https://doi.org/10.1016/j.jneumeth.2010.07.015
Olvet, D. M., & Hajcak, G. (2008). The error-related negativity (ERN) and psychopathology: Toward an Endophenotype. Clinical Psychology Review, 28, 13431354. http://doi.org/10.1016/j.cpr.2008.07.003
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, 336342.e6. https://doi.org/10.1016/j.jaac.2018.02.010.
Pailing, P. E., Segalowitz, S. J., Dywan, J., & Davies, P. L. (2002). Error negativity and response control. Psychophysiology, 39, 198206. https://doi.org/10.1017/S0048577202010247
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, 885895. http://doi.org/10.1007/s10802-011-9495-5
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, 767773.
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, 595602.
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, 377384. https://doi.org/10.1016/j.jaac.2015.02.010
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.2015.00328
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, 247260.
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, 566573. https://doi.org/10.1002/da.22151
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, 11091117. https://doi.org/10.1111/j.1469-7610.2012.02561.x
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, 861864. https://doi.org/10.1097/00004583-198911000-00009
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, 556570. https://doi.org/10.1016/j.jaac.2016.04.014
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, 735747. http://doi.org/10.1007/s10802-011-9490-x
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, 11911205.e4. http://doi.org/10.1016/j.jaac.2014.08.005

Keywords

Type Description Title
WORD
Supplementary materials

Filippi et al. supplementary material
Filippi et al. supplementary material

 Word (193 KB)
193 KB

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

  • Courtney A. Filippi (a1), Anni R. Subar (a1), Jessica F. Sachs (a1), Katharina Kircanski (a1), George Buzzell (a2), David Pagliaccio (a3), Rany Abend (a1), Nathan A. Fox (a2), Ellen Leibenluft (a1) and Daniel S. Pine (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed