Abstract
The prefrontal cortex and the frontoparietal network are associated with a variety of regulatory behaviors. Functional connections between these brain regions and the amygdala are implicated in risk for anxiety disorders. The prefrontal cortex and frontoparietal network are also linked to executive functioning, or behaviors that help orient action towards higher order goals. Where much research has been focused on deleterious effects of under-controlled behavior, a body of work suggests that over-controlled behavior may also pose a risk for internalizing problems. Indeed, while work suggests that high levels of attention shifting may still be protective against internalizing problems, there is evidence that high levels of inhibitory control may be a risk factor for socioemotional difficulties. In the ABCD sample, which offers large sample sizes as well as sociodemographic diversity, we test the interaction between frontoparietal network-amygdala resting state functional connectivity and executive functioning behaviors on longitudinal changes in internalizing symptoms from approximately 10 to 12 years of age. We found that higher proficiency in attention shifting indeed predicts fewer internalizing behaviors over time. In addition, higher proficiency in inhibitory control predicts fewer internalizing symptoms over time, but only for children showing resting state connectivity moderately above the sample average between the frontoparietal network and amygdala. This finding supports the idea that top-down control may not be adaptive for all children, and relations between executive functioning and anxiety risk may vary as a function of trait-level regulation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Data can be obtained through the Adolescent Brain Cognitive Development (ABCD) Study’s Data Exploration and Analysis Portal (DEAP).
References
Achenbach, T. M., & Edelbrock, C. S. (1983). Manual for the child behavioral checklist and revised child behavior profile. University of Vermont.
Adolphs, R. (2008). Fear, faces, and the human amygdala. Current Opinion in Neurobiology, 18, 166–172. https://doi.org/10.1016/j.conb.2008.06.006
Ansari, T. L., & Derakshan, N. (2011). The neural correlates of impaired inhibitory control in anxiety. Neuropsychologia, 49, 1146–1153. https://doi.org/10.1016/j.neuropsychologia.2011.01.019
Arán-Filippetti, V., & Richaud de Minzi, M. C. (2012). A structural analysis of executive functions and socioeconomic status in school-age children: cognitive factors as effect mediators. The Journal of Genetic Psychology, 173(4), 393–416.
Basten, U., Stelzel, C., & Fiebach, C. J. (2011). Trait anxiety modulates the neural efficiency of inhibitory control. Journal of Cognitive Neuroscience, 23(10), 3132–3145. https://doi.org/10.1162/jocn_a_00003
Basten, U., Stelzel, C., & Fiebach, C. J. (2012). Trait anxiety and the neural efficiency of manipulation in working memory. Cognitive, Affective, and Behavioral Neuroscience, 12, 571–588. https://doi.org/10.3758/s13415-012-0100-3
Beesdo, K., Bittner, A., Pine, D. S., Stein, M. B., Hofler, M., Lieb, R., & Wittchen, H. (2007). Incidence of social anxiety disorder and the consistent risk for secondary depression in the first three decades of life. Archives of General Psychiatry, 64(8), 903–912. https://doi.org/10.1001/archpsyc.64.8.903
Beesdo, K., Knappe, S., & Pine, D. S. (2009). Anxiety and anxiety disorders in children and adolescents: developmental issues and implications for DSM-V. The Psychiatric Clinics of North America, 32(3), 483–524. https://doi.org/10.1016/j.psc.2009.06.002
Blackwell, K. A., Chatham, C. H., Wiseheart, M., & Munakata, Y. (2014). A developmental window into trade-offs in executive function: The case of task switching versus response inhibition in 6-year-olds. Neuropsychologia, 62, 356–364. https://doi.org/10.1016/j.neuropsychologia.2014.04.016
Bloom, P. A., VanTieghem, M., Gabard-Durnam, L., Gee, D. G., Flannery, J., Caldera, C., Goff, B., Telzer, E. H., Humphreys, K. L., Fareri, D. S., Shapiro, M., Algharazi, S., Bolger, N., Aly, M., & Tottenham, N. (2021). Age-related change in task-evoked amygdala-prefrontal circuitry: A multiverse approach with an accelerated longitudinal cohort aged 4–22 years. Human Brain Mapping. https://doi.org/10.1002/hbm.25847
Bryce, N. V., Flournoy, J. C., Moreira, J. F. G., Rosen, M. L., Sambook, K. A., Mair, P., & McLaughlin, K. A. (2021). Brain parcellation selection: An overlooked decision point with meaningful effects on individual differences in resting-state functional connectivity. NeuroImage, 243, 118487. https://doi.org/10.1016/j.neuroimage.2021.118487
Camacho, M. C., Quiñones-Camacho, L. E., & Perlman, S. B. (2020). Does the child brain rest?: An examination and interpretation of resting cognition in developmental cognitive neuroscience. Neuroimage, 212, 116688. https://doi.org/10.1016/j.neuroimage.2020.116688
Carlson, S. M., & Moses, L. J. (2001). Individual differences in inhibitory control and children’s theory of mind. Child Development, 72(4), 1032–1053. https://doi.org/10.1111/1467-8624.00333
Casey, B. J., Cannonier, T., Conley, M. I., Cohen, A. O., Barch, D. M., Heitzeh, M. M., Soules, M. E., Teslovich, T., Dellarco, D. V., Garavan, H., Orr, C. A., Wager, T. D., Banich, M. T., Speer, N. K., Sutherland, M. T., Riedel, M. C., Dick, A. S., Bjork, J. M., Thomas, K. M., & Dale, A. M. (2018). The Adolescent Brain Cognitive Development (ABCD) study: Imaging acquisition across 21 sites. Developmental Cognitive Neuroscience, 32, 43–54. https://doi.org/10.1016/j.dcn.2018.03.001
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(3), 104–110. https://doi.org/10.1016/j.tics.2005.01.011
Cheng, T. W., Magis-Weinberg, L., Guazzelli Williamson, V., Ladouceur, C. D., Whittle, S. L., Herting, M. M., Uban, K. A., Byrne, M. L., Barendse, M. E. A., Shirtcliff, E. A., & Pfeifer, J. H. (2021). A researcher’s guide to the measurement and modeling of puberty in the ABCD study at baseline. Frontiers in Endocrinology, 12, 608575. https://doi.org/10.3389/fendo.2021.608575
Cisler, J. M., & Koster, E. H. W. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: an integrative review. Clinical Psychology Review, 30(2), 203–216. https://doi.org/10.1016/j.cpr.2009.11.003
Cohodes, E. M., Kitt, E. R., Baskin-Sommers, A., & Gee, D. G. (2020). Influences of early-life tress on frontolimbic circuitry: Harnessing a dimensional approach to elucidate the effects of heterogeneity in stress exposure. Developmental Psychobiology, 1–20. https://doi.org/10.1002/dev.21969
Cole, M., Repovs, G., & Anticevic, A. (2014). The frontoparietal control system: a central role in mental health. The Neuroscientist, 20(1), 652–664. https://doi.org/10.1177/1073858414525995
Cuthbert, B. N., & Insel, T. R. (2013). Toward the future of psychiatric diagnosis: The seven pillars of RDoC. BMC Medicine, 11(1), 1–8.
Dai, J., & Scherf, K. S. (2019). Puberty and functional brain development in humans: Convergence in findings? Developmental Cognitive Neuroscience, 39, 100690. https://doi.org/10.1016/j.dcn.2019.100690
de Lijster, J. M., Dierckx, B., Utens, E. M., Verhulst, F. C., Zieldorff, C., Dieleman, G. C., & Legerstee, J. S. (2017). The age of onset of anxiety disorders. Canadian Journal of Psychiatry, 62(4), 237–246. https://doi.org/10.1177/0706743716640757
Diamond, A. (2006). The early development of executive functions. In E. Bialystok & F. Craik (Eds.), Lifespan Cognition: Mechanisms of Change (pp. 70–95). Oxford University Press.
Dick, A. S., Garcia, N. L., Pruden, S. M., Thompson, W. K., Hawes, S. W., Sutherland, M. T., Reidel, M. C., Laird, A. R., & Gonzalez, R. (2019). No evidence for a bilingual executive function advantage in the ABCD study. Nature Human Behaviour, 3(7), 692–701. https://doi.org/10.1038/s41562-019-0609-3
Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D. (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Archives of general psychiatry, 66(12), 1361–1372. https://doi.org/10.1001/archgenpsychiatry.2009.104
Fields, A., Bloom, P. A., VanTieghem, M., Harmon, C., Choy, T., Camacho, N. L., Gibson, L., Umbach, R., Heleniak, C., & Tottenham, N. (2021). Adaptation in the face of adversity: Decrements and enhancements in children’s cognitive control behavior following early caregiving instability. Developmental Science, 24(6), e13133. https://doi.org/10.1111/desc.13133
Filippi, C. A., Suber, A., Ravi, S., Haas, S., Troller-Renfree, S. V., Fox, N. A., Leibenluft, E., & Pine, D. S. (2021). Developmental changes in the association between cognitive control and anxiety. Child Psychiatry and Human Development. https://doi.org/10.1007/s10578-021-01150-5
Fitzpatrick, C., McKinnon, R. D., Blair, C. B., & Willoughby, M. T. (2014). Do preschool executive function skills explain the school readiness gap between advantaged and disadvantaged children? Learning and Instruction, 30, 25–31. https://doi.org/10.1016/j.learninstruc.2013.11.003
Fox, N. A., Buzzell, G. A., Morales, S., Valadez, E. A., Wilson, M., & Henderson, H. A. (2020). Understanding the emergence of social anxiety in children with behavioral inhibition. Biological Psychiatry, 89, 681–689. https://doi.org/10.1016/j.biopsych.2020.10.004
Franz, L., Angold, A., Copeland, W., Costello, E. J., Towe-Goodman, N., & Egger, H. (2013). Preschool anxiety disorders in pediatric primary care: prevalence and comorbidity. Journal of the American Academy of Child and Adolescent Psychiatry, 52(12), 1294–1303. https://doi.org/10.1016/j.jaac/2013.09.008
Gaffrey, M. S., Barch, D. M., Luby, J. L., & Petersen, S. E. (2021). Amygdala functional connectivity is associated with emotion regulation and amygdala reactivity in 4-to 6-year-olds. Journal of the American Academy of Child & Adolescent Psychiatry, 60(1), 176–185.
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., Hare, T. A., Bookheimer, S. Y., & Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience, 33(10), 4584–4593. https://doi.org/10.1523/JNEUROSCI.3446-12.2013
Geiger, M. J., Domschke, K., Isper, J., Hattingh, C., Baldwin, D. S., Lochner, C., & Stein, D. J. (2015). Altered executive control network resting-state connectivity in social anxiety disorder. The World Journal of Biological Psychiatry, 17(1), 47–57. https://doi.org/10.3109/15622975.2015.1083613
Gordon, E. M., Laumann, T. O., Adeyemo, B., Huckins, J. F., Kelley, W. M., & Petersen, S. E. (2016). Generation and evaluation of a cortical area parcellation from resting-state correlations. Cerebral Cortex, 26, 288–303. https://doi.org/10.1093/cercor/bhu239
Gunther, K. E., & Pérez-Edgar, K. (2021). Dopaminergic associations between behavioral inhibition, executive functioning, and anxiety in development. Developmental Review, 60, 100966. https://doi.org/10.1016/j.dr.2021.100966
Hagler, D. J., Hatton, S. N., Cornejo, M. D., Makowski, C., Fair, D. A., Dick, A. S., Sutherland, M. T., Casey, B. J., Barch, D. M., Harms, M. P., Watts, R., Bjork, J. M., Garavan, H. P., Hilmer, L., Pung, C. J., Sicat, C. S., Kuperman, J., Bartsch, H., Xue, F., & Dale, A. M. (2019). Image processing and analysis methods for the Adolescent Brain Cognitive Development Study. NeuroImage, 202, 116091. https://doi.org/10.1016/j.neuroimage.2019.116091
He, Y., Xu, T., Zhang, W., & Zuo, X. (2016). Lifespan anxiety is reflected in human amygdala cortical connectivity. Human Brain Mapping, 37, 1178–1193. https://doi.org/10.1002/hbm.23094
Henderson, H. A., Pine, D. S., & Fox, N. A. (2015). Behavioral inhibition and developmental risk: A dual-processing perspective. Neuropsychopharmacology, 40, 207–224. https://doi.org/10.1038/npp.2014.189
Henderson, H. A., & Wilson, M. J. G. (2017). Attention processes underlying risk and resilience in behaviorally inhibited children. Current Behavioral Neuroscience Reports, 4, 99–106. https://doi.org/10.1007/s40473-017-0111-z
Kooijmans, R., Scheres, A., & Oosterlaan, J. (2000). Response inhibition and measures of psychopathology: A dimensional analysis. Child Neuropsychology, 6(3), 145–184. https://doi.org/10.1076/chin.6.3.175.3154
Lengua, L. J. (2003). Associations among emotionality, self-regulation, adjustment problems, and positive adjustment in middle childhood. Applied Developmental Psychology, 24, 595–618. https://doi.org/10.1016/j.appdev.2003.08.002
Li, W., Yang, P., Ngetich, R. K., Zhang, J., Jin, Z., & Li, L. (2021). Differential involvement of frontoparietal network and insula cortex in emotion regulation. Neuropsychologia, 161, 107991. https://doi.org/10.1016/j.neuropsychologia.2021.107991
Luciana, M., Bjork, J. M., Nagel, B. J., Barch, D. M., Gonzalez, R., Nixon, S. J., & Banick, M. T. (2018). Adolescent neurocognitive development and impacts of substance use: Overview of the adolescent brain cognitive development (ABCD) baseline neurocognition battery. Developmental Cognitive Neuroscience, 32, 67–79. https://doi.org/10.1016/j.dcn.2018.02.006
Marek, S., Tervo-Clemmens, B., Calabro, F. J., Montez, D. F., Kay, B. P., Hatoum, A. S., Donohue, M. R., Foran, W., Miller, R. L., Hendrickson, T. J., Malone, S. M., Kandala, S., Feczko, E., Miranda-Dominguez, O., Graham, A. M., Earl, E. A., Perrone, A. J., Cordova, M., Doyle, O., & Dosenbach, N. U. (2022). Reproducible brain-wide association studies require thousands of individuals. Nature, 603, 654–660. https://doi.org/10.1038/s41586-022-04492-9
McLaughlin, K. A., & Nolen-Hoeksema, S. (2011). Rumination as a transdiagnostic factor in depression and anxiety. Behaviour Research and Therapy, 49(3), 186–193. https://doi.org/10.1016/j.brat.2010.12.006
McTeague, L. M., Goodkind, M. S., & Etkin, A. (2016). Transdiagnostic impairment of cognitive control in mental illness. Journal of Psychiatric Research, 83, 37–46. https://doi.org/10.1016/j.jpsychires.2016.08.001
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.
Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., & Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cognitive Psychology, 41(1), 49–100. https://doi.org/10.1006/cogp.1999.0734
Moran, T. P. (2016). Anxiety and working memory capacity: A meta-analysis and narrative review. Psychological Bulletin, 142(8), 1–34. https://doi.org/10.1037/bul0000051
NIH Toolbox. (n.d.). Health measures. https://www.healthmeasures.net/score-and-interpret/interpret-scores/nih-toolbox
Northoff, G., & Tumati, S. (2016). Average is good, extremes are bad - Non-linear inverted U-shaped relationship between neural mechanisms and functionality of mental features. Neuroscience and Biobehavioral Reviews, 104, 11–25. https://doi.org/10.1016/j.neubiorev.2019.06.030
Pérez-Edgar, K., Vallorani, A., Buss, K. A., & LoBue, V. (2020). Individual differences in infancy research: Letting the baby stand out from the crowd. Infancy, 25, 438–457. https://doi.org/10.1111/infa.12338
Petersen, A.C., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: reliability, validity, and initial norms. Journal of Youth and Adolescence, 17(2), 117–33. https://doi.org/10.1007/BF01537962
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2022). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–155. https://CRAN.R-project.org/package=nlme
Qin, S., Young, C. B., Duan, X., Chen, T., Supekar, K., & Menon, V. (2014). Amygdala subregional structure and intrinsic functional connectivity predicts individual differences in anxiety during early childhood. Biological Psychiatry, 75, 892–900. https://doi.org/10.1016/j.biopsych.2013.10.006
Raver, C. C., Blair, C., Willoughby, M., & The Family Life Project Key Investigators. (2013). Poverty as a predictor of 4-year-olds’ executive function: new perspectives on models of differential susceptibility. Developmental Psychology, 49(2), 292–304.
Regier, D. A., Rae, D. S., Narrow, W. E., Kaelber, C. T., & Schatzberg, A. F. (1998). Prevalence of anxiety disorders and their comorbidity with mood and addictive disorders. British Journal of Psychiatry, 173, 24–28. https://doi.org/10.1192/S0007125000293483
Rhebergen, D., Aderka, I. M., van der Steenstraten, I. M., van Balkom, A. L. J. M., van Oppen, P., Stek, M. L., Comijs, H. C., & Batelaan, N. M. (2017). Admixture analysis of age of onset in generalized anxiety disorder. Journal of Anxiety Disorders, 50, 47–51. https://doi.org/10.1016/j.janxdis.2017.05.003
Rodman, A. M., Jenness, J. L., Weissman, D. G., Pine, D. S., & McLaughlin, K. A. (2019). Neurobiological Markers of Resilience to Depression Following Childhood Maltreatment: The Role of Neural Circuits Supporting the Cognitive Control of Emotion. Biological Psychiatry, 86, 464–473. https://doi.org/10.1016/j.biopsych.2019.04.033
Schmid, P. C., Kleiman, T., & Amodio, D. M. (2015). Neural mechanisms of proactive and reactive cognitive control in social anxiety. Cortex, 70, 137–145. https://doi.org/10.1016/j.cortex.2015.05.030
Snijders, T. A., & Bosker, R. J. (2011). Multilevel analysis: An introduction to basic and advanced multilevel modeling. Sage.
Sylvester, C. M., Corbetta, M., Raichle, M. E., Rodebaugh, T. L., Schlaggar, B. L., Sheline, Y. I., Zorumski, C. F., & Lenze, E. J. (2012). Fumctional network dysfunction in anxiety and anxiety disorders. Trends in Neurosciences, 35(9), 527–535. https://doi.org/10.1016/j.tins.2012.04.012
Taber-Thomas, B., & Pérez-Edgar, K. (2015). Brain development in emerging adulthood. In J. Arnett (Ed.), Oxford Handbook of Emerging Adulthood (pp. 126–141). Oxford University Press.
Thorell, L. B., Bohlin, G., & Rydell, A. (2004). Two types of inhibitory control: Predictive relations to social functioning. International Journal of Behavioral Development, 28(3), 193–203. https://doi.org/10.1080/01650250344000389
Tottenham, N., & Gabard-Durnam, L. J. (2017). The developing amygdala: A student of the world and a teacher of the cortex. Current Opinion in Psychology, 17, 55–60. https://doi.org/10.1016/j.copsyc.2017.06.012
Ulfig, N., Setzer, M., & Bohl, J. (2003). Ontogeny of the human amygdala. Annals of the New York Academy of Sciences, 985(1), 22–33.
Valadez, E. A., Morales, S., Buzzell, G. A., Troller-Renfree, S. V., Henderson, H. A., Chronis-Tuscano, A., Pine, D. S., & Fox, N. A. (2022). Development of Proactive Control and Anxiety Among Behaviorally Inhibited Adolescents. Journal of the American Academy of Child and Adolescent Psychiatry. https://doi.org/10.1016/j.jaac.2022.04.012
Weintraub, S., Dikmen, S. S., Heaton, R. K., Tulsky, D. S., Zelazo, P. D., Bauer, P. J., Carlozzi, N. E., Slotkin, J., Blitz, D., Wallner-Allen, K., Fox, N. A., Beaumont, J. L., Mungas, D., Nowinski, C. J., Richler, J., Deocampo, J. A., Anderson, J. E., Manly, J. J., Borosh, B., … Gershon, R. C. (2013). Cognition assessment using the NIH Toolbox. Neurology, 80(11 Suppl 3), S54–S64. https://doi.org/10.1212/WNL.0b013e3182872ded
Welsh, M. C., Pennington, B. F., & Groisser, D. B. (1991). A normative-developmental study of executive function: A window on prefrontal function in children. Developmental Neuropsychology, 7(2), 131–149. https://doi.org/10.1080/87565649109540483
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. https://doi.org/10.1007/s10802-011-9490-x
Wolfe, C. D., & Bell, M. A. (2014). Brain electrical activity of shy and non-shy preschool-aged children during executive function tasks. Infant and Child Development, 23(3), 259–272. https://doi.org/10.1002/icd.1858
Xiao, T., Zhang, S., Lee, L., Chao, H. H., van Dyck, C., & Li, C. R. (2019). Exploring Age-Related Changes in Resting State Functional Connectivity of the Amygdala: From Young to Middle Adulthood. Frontiers in Aging Neuroscience, 10, 209. https://doi.org/10.3389/fnagi.2018.00209
Xie, L., Ren, M., Cao, B., & Li, F. (2017). Distinct brain responses to different inhibitions: Evidence from a modified Flanker Task. Nature Scientific Reports, 7, 6657. https://doi.org/10.1038/s41598-017-04907-y
Zanto, T. P., & Gazzaley, A. (2013). Fronto-parietal network: Flexible hub of cognitive control. Trends in Cognitive Sciences, 17(12), 602–603.
Zelazo, P. D., Anderson, J. E., Richler, J., Wallner‐Allen, K., Beaumont, J. L., & Weintraub, S. (2013). II. NIH Toolbox Cognition Battery (CB): Measuring executive function and attention. Monographs of the Society for Research in Child Development, 78(4), 16–33.
Funding
This study was funded by the National Science Foundation Graduate Research Fellowship Grant No. DGE1255832 (to KEG) and the National Institute on Drug Abuse T32 DA017629 (to DP). The content is the sole responsibility of the authors and does not necessarily represent the official position of any funding agencies.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors have no conflicts of interest to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gunther, K.E., Petrie, D., Pérez-Edgar, K. et al. Relations Between Executive Functioning and Internalizing Symptoms Vary as a Function of Frontoparietal-amygdala Resting State Connectivity. Res Child Adolesc Psychopathol 51, 775–788 (2023). https://doi.org/10.1007/s10802-023-01025-4
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10802-023-01025-4