Abstract
Reading disorder (RD) is characterized by deficient phonological processing, but children with RD also have cognitive control deficits, the neural correlates of which are not fully understood. We used fMRI to assess neural activity during the resolution of cognitive conflict on the Simon Spatial Incompatibility task and patterns of resting-state functional connectivity (RSFC) from task control (TC) regions in 7–12-year-old children with RD compared to their typically developing (TD) peers. Relative to TD children (n = 17), those with RD (n = 16) over-engaged a right superior/medial frontal cluster during the resolution of conflict (p = .05). Relative to TD children (n = 18), those with RD (n = 17) also showed reduced RSFC (voxel-wise p < .001; cluster-size p < .05, FDR corrected) from cingulo-opercular seeds to left hemisphere fronto-parietal and temporo-parietal reading-related regions, perhaps reflecting reduced organization of TC circuits and reduced integration with reading-related regions. Children with RD additionally showed reduced RSFC between fronto-parietal and default mode network regions. Follow-up analyses in a subset of children with both useable task and resting state data (RD = 13; TD = 17) revealed that greater conflict-related activation of the right frontal Simon task ROI associated with better word-reading, perhaps suggesting a compensatory role for this over-engagement. Connectivity from fronto-parietal seeds significantly associated with Simon task performance and word-reading accuracy in RD children. These findings suggest that altered functioning and connectivity of control circuits may contribute to cognitive control deficits in children with RD. Future studies should assess the utility of adding cognitive control training to reading remediation programs.
Similar content being viewed by others
References
Bednarek, D. B., Saldana, D., Quintero-Gallego, E., Garcia, I., Grabowska, A., & Gomez, C. M. (2004). Attentional deficit in dyslexia: a general or specific impairment? Neuroreport, 15(11), 1787–1790.
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage, 37(1), 90–101. https://doi.org/10.1016/j.neuroimage.2007.04.042.
Booth, J. N., Boyle, J. M., & Kelly, S. W. (2010). Do tasks make a difference? Accounting for heterogeneity of performance of children with reading difficulties on tasks of executive function: findings from a meta-analysis. British Journal of Developmental Psychology, 28(Pt 1, 133–176.
Borella, E., Carretti, B., & Pelegrina, S. (2010). The specific role of inhibition in reading comprehension in good and poor comprehenders. Journal of Learning Disabilities, 43(6), 541–552. https://doi.org/10.1177/0022219410371676.
Brett, M., Anton, J., Valabregue, R., & Poline, J. B. (2002, June 2–6, 2002). Region of interest analysis using an SPM toolbox (MARSBAR). Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.
Brosnan, M., Demetre, J., Hamill, S., Robson, K., Shepherd, H., & Cody, G. (2002). Executive functioning in adults and children with developmental dyslexia. Neuropsychologia, 40(12), 2144–2155.
Chai, X. J., Ofen, N., Gabrieli, J. D., & Whitfield-Gabrieli, S. (2014). Selective development of anticorrelated networks in the intrinsic functional organization of the human brain. Journal of Cognitive Neuroscience, 26(3), 501–513. https://doi.org/10.1162/jocn_a_00517.
Ciric, R., Wolf, D. H., Power, J. D., Roalf, D. R., Baum, G. L., Ruparel, K., et al. (2017). Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity. Neuroimage, 154, 174–187. https://doi.org/10.1016/j.neuroimage.2017.03.020.
Dosenbach, N. U. F., Visscher, K. M., Palmer, E. D., Miezin, F. M., Wenger, K. K., Kang, H. C., et al. (2006). A Core system for the implementation of task sets. Neuron, 50(5), 799–812. https://doi.org/10.1016/j.neuron.2006.04.031.
Dosenbach, N. U., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A., et al. (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences of the United States of America, 104(26), 11073–11078. https://doi.org/10.1073/pnas.0704320104.
Dosenbach, N. U., Fair, D. A., Cohen, A. L., Schlaggar, B. L., & Petersen, S. E. (2008). A dual-networks architecture of top-down control. Trends in Cognitive Sciences, 12(3), 99–105. https://doi.org/10.1016/j.tics.2008.01.001.
Facoetti, A., & Turatto, M. (2000). Asymmetrical visual fields distribution of attention in dyslexic children: a neuropsychological study. Neuroscience Letters, 290(3), 216–218.
Fair, D. A., Dosenbach, N. U., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., et al. (2007). Development of distinct control networks through segregation and integration. Proceedings of the National Academy of Sciences of the United States of America, 104(33), 13507–13512. https://doi.org/10.1073/pnas.0705843104.
Fair, D. A., Cohen, A. L., Dosenbach, N. U., Church, J. A., Miezin, F. M., Barch, D. M., et al. (2008). The maturing architecture of the brain's default network. Proceedings of the National Academy of Sciences of the United States of America, 105(10), 4028–4032. https://doi.org/10.1073/pnas.0800376105.
Finn, E. S., Shen, X., Holahan, J. M., Scheinost, D., Lacadie, C., Papademetris, X., et al. (2014). Disruption of functional networks in dyslexia: a whole-brain, data-driven analysis of connectivity. Biological Psychiatry, 76(5), 397–404. https://doi.org/10.1016/j.biopsych.2013.08.031.
Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9673–9678. https://doi.org/10.1073/pnas.0504136102.
Friston, K. J., Ashburner, J., Frith, C. D., Poline, J.-B., Heather, J. D., & Frackowiak, R. S. J. (1995). Spatial registration and normalization of images. Human Brain Mapping, 2, 165–189.
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 (New York, N.Y. : 1991), 26(1), 288–303. https://doi.org/10.1093/cercor/bhu239.
Henson, R. N., Price, C. J., Rugg, M. D., Turner, R., & Friston, K. J. (2002). Detecting latency differences in event-related BOLD responses: application to words versus nonwords and initial versus repeated face presentations. Neuroimage, 15(1), 83–97. https://doi.org/10.1006/nimg.2001.0940.
Hoeft, F., Meyler, A., Hernandez, A., Juel, C., Taylor-Hill, H., Martindale, J. L., et al. (2007). Functional and morphometric brain dissociation between dyslexia and reading ability. Proceedings of the National Academy of Sciences of the United States of America, 104(10), 4234–4239. https://doi.org/10.1073/pnas.0609399104.
Hoeft, F., McCandliss, B. D., Black, J. M., Gantman, A., Zakerani, N., Hulme, C., et al. (2011a). Neural systems predicting long-term outcome in dyslexia. Proceedings of the National Academy of Sciences of the United States of America, 108(1), 361–366. https://doi.org/10.1073/pnas.1008950108.
Hoeft, F., Walter, E., Lightbody, A. A., Hazlett, H. C., Chang, C., Piven, J., & Reiss, A. L. (2011b). Neuroanatomical differences in toddler boys with fragile x syndrome and idiopathic autism. Archives of General Psychiatry, 68(3), 295–305. https://doi.org/10.1001/archgenpsychiatry.2010.153.
Horga, G., Maia, T. V., Wang, P., Wang, Z., Marsh, R., & Peterson, B. S. (2011). Adaptation to conflict via context-driven anticipatory signals in the dorsomedial prefrontal cortex. Journal of Neuroscience, 31(45), 16208–16216. https://doi.org/10.1523/JNEUROSCI.2783-11.2011.
Horowitz-Kraus, T., Toro-Serey, C., & DiFrancesco, M. (2015). Increased resting-state functional connectivity in the Cingulo-Opercular cognitive-control network after intervention in children with Reading difficulties. PLoS One, 10(7), e0133762. https://doi.org/10.1371/journal.pone.0133762.
Horowitz-Kraus, T., Hershey, A., Kay, B., & DiFrancesco, M. (2019). Differential effect of reading training on functional connectivity in children with reading difficulties with and without ADHD comorbidity. Journal of Neurolinguistics, 49, 93–108. https://doi.org/10.1016/j.jneuroling.2018.09.002.
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 and Adolescent Psychiatry, 36(7), 980–988. https://doi.org/10.1097/00004583-199707000-00021.
Kibby, M. Y., Lee, S. E., & Dyer, S. M. (2014). Reading performance is predicted by more than phonological processing. Frontiers in Psychology, 5, 960. https://doi.org/10.3389/fpsyg.2014.00960.
Koyama, M. S., Di Martino, A., Zuo, X. N., Kelly, C., Mennes, M., Jutagir, D. R., et al. (2011). Resting-state functional connectivity indexes reading competence in children and adults. Journal of Neuroscience, 31(23), 8617–8624. https://doi.org/10.1523/JNEUROSCI.4865-10.2011.
Koyama, M. S., Di Martino, A., Kelly, C., Jutagir, D. R., Sunshine, J., Schwartz, S. J., et al. (2013). Cortical signatures of dyslexia and remediation: an intrinsic functional connectivity approach. PLoS One, 8(2), e55454. https://doi.org/10.1371/journal.pone.0055454.
Mahe, G., Doignon-Camus, N., Dufour, A., & Bonnefond, A. (2014). Conflict control processing in adults with developmental dyslexia: an event related potentials study. Clinical Neurophysiology, 125(1), 69–76. https://doi.org/10.1016/j.clinph.2013.06.005.
Maisog, J. M., Einbinder, E. R., Flowers, D. L., Turkeltaub, P. E., & Eden, G. F. (2008). A meta-analysis of functional neuroimaging studies of dyslexia. Annals of the New York Academy of Sciences, 1145, 237–259. https://doi.org/10.1196/annals.1416.024.
Marek, S., Hwang, K., Foran, W., Hallquist, M. N., & Luna, B. (2015). The contribution of network organization and integration to the development of cognitive control. PLoS Biology, 13(12), e1002328. https://doi.org/10.1371/journal.pbio.1002328.
Margolis, A. E., Davis, K. S., Pao, L. S., Lewis, A., Yang, X., Tau, G., et al. (2017). Verbal-spatial IQ discrepancies impact brain activation associated with the resolution of cognitive conflict in children and adolescents. Developmental Science, 21. https://doi.org/10.1111/desc.12550.
Melby-Lervag, M., Lyster, S. A., & Hulme, C. (2012). Phonological skills and their role in learning to read: a meta-analytic review. Psychological Bulletin, 138(2), 322–352. https://doi.org/10.1037/a0026744.
Nee, D. E., Wager, T. D., & Jonides, J. (2007). Interference resolution: insights from a meta-analysis of neuroimaging tasks. Cognitive, Affective, & Behavioral Neuroscience, 7(1), 1–17.
Power, J. D., Cohen, A. L., Nelson, S. M., Wig, G. S., Barnes, K. A., Church, J. A., et al. (2011). Functional network organization of the human brain. Neuron, 72(4), 665–678. https://doi.org/10.1016/j.neuron.2011.09.006.
Purvis, K. L., & Tannock, R. (2000). Phonological processing, not inhibitory control, differentiates ADHD and reading disability. Journal of the American Academy of Child and Adolescent Psychiatry, 39(4), 485–494. https://doi.org/10.1097/00004583-200004000-00018.
Reiter, A., Tucha, O., & Lange, K. W. (2005). Executive functions in children with dyslexia. Dyslexia, 11(2), 116–131. https://doi.org/10.1002/dys.289.
Richlan, F. (2012). Developmental dyslexia: dysfunction of a left hemisphere reading network. Frontiers in Human Neuroscience, 6, 120. https://doi.org/10.3389/fnhum.2012.00120.
Richlan, F., Kronbichler, M., & Wimmer, H. (2009). Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies. Human Brain Mapping, 30(10), 3299–3308. https://doi.org/10.1002/hbm.20752.
Richlan, F., Sturm, D., Schurz, M., Kronbichler, M., Ladurner, G., & Wimmer, H. (2010). A common left occipito-temporal dysfunction in developmental dyslexia and acquired letter-by-letter reading? PLoS One, 5(8), e12073. https://doi.org/10.1371/journal.pone.0012073.
Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., & Brammer, M. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27(12), 973–993. https://doi.org/10.1002/hbm.20237.
Satterthwaite, T. D., Wolf, D. H., Loughead, J., Ruparel, K., Elliott, M. A., Hakonarson, H., et al. (2012). Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage, 60(1), 623–632. https://doi.org/10.1016/j.neuroimage.2011.12.063.
Schurz, M., Wimmer, H., Richlan, F., Ludersdorfer, P., Klackl, J., & Kronbichler, M. (2015). Resting-state and task-based functional brain connectivity in developmental dyslexia. Cerebral Cortex, 25(10), 3502–3514. https://doi.org/10.1093/cercor/bhu184.
Sestieri, C., Corbetta, M., Spadone, S., Romani, G. L., & Shulman, G. L. (2014). Domain-general signals in the cingulo-opercular network for visuospatial attention and episodic memory. Journal of Cognitive Neuroscience, 26(3), 551–568. https://doi.org/10.1162/jocn_a_00504.
Shaywitz, S. E., Shaywitz, B. A., Pugh, K. R., Fulbright, R. K., Constable, R. T., Mencl, W. E., et al. (1998). Functional disruption in the organization of the brain for reading in dyslexia. Proceedings of the National Academy of Sciences of the United States of America, 95(5), 2636–2641.
Shaywitz, B. A., Shaywitz, S. E., Pugh, K. R., Mencl, W. E., Fulbright, R. K., Skudlarski, P., et al. (2002). Disruption of posterior brain systems for reading in children with developmental dyslexia. Biological Psychiatry, 52(2), 101–110.
Sheridan, M., Kharitonova, M., Martin, R. E., Chatterjee, A., & Gabrieli, J. D. (2014). Neural substrates of the development of cognitive control in children ages 5-10 years. Journal of Cognitive Neuroscience, 26(8), 1840–1850. https://doi.org/10.1162/jocn_a_00597.
Temple, E., Deutsch, G. K., Poldrack, R. A., Miller, S. L., Tallal, P., Merzenich, M. M., & Gabrieli, J. D. (2003). Neural deficits in children with dyslexia ameliorated by behavioral remediation: evidence from functional MRI. Proceedings of the National Academy of Sciences of the United States of America, 100(5), 2860–2865. https://doi.org/10.1073/pnas.0030098100.
Vaidya, C. J., Bunge, S. A., Dudukovic, N. M., Zalecki, C. A., Elliott, G. R., & Gabrieli, J. D. (2005). Altered neural substrates of cognitive control in childhood ADHD: evidence from functional magnetic resonance imaging. The American Journal of Psychiatry, 162(9), 1605–1613. https://doi.org/10.1176/appi.ajp.162.9.1605.
Varvara, P., Varuzza, C., Sorrentino, A. C., Vicari, S., & Menghini, D. (2014). Executive functions in developmental dyslexia. Frontiers in Human Neuroscience, 8, 120. https://doi.org/10.3389/fnhum.2014.00120.
Vellutino, F. R., & Fletcher, J. M. (2005). Developmental dyslexia. In M. J. Snowling & C. J. Hulme (Eds.), The science of reading: A handbook (pp. 362–378). Oxford: Blackwell.
Willcutt, E. G., & Pennington, B. F. (2000). Psychiatric comorbidity in children and adolescents with reading disability. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 41(8), 1039–1048.
Willcutt, E. G., Pennington, B. F., Boada, R., Ogline, J. S., Tunick, R. A., Chhabildas, N. A., & Olson, R. K. (2001). A comparison of the cognitive deficits in reading disability and attention-deficit/hyperactivity disorder. Journal of Abnormal Psychology, 110(1), 157–172.
Willcutt, E. G., Pennington, B. F., Olson, R. K., Chhabildas, N., & Hulslander, J. (2005). Neuropsychological analyses of comorbidity between reading disability and attention deficit hyperactivity disorder: in search of the common deficit. Developmental Neuropsychology, 27(1), 35–78. https://doi.org/10.1207/s15326942dn2701_3.
Wimmer, H., Schurz, M., Sturm, D., Richlan, F., Klackl, J., Kronbichler, M., & Ladurner, G. (2010). A dual-route perspective on poor reading in a regular orthography: an fMRI study. Cortex, 46(10), 1284–1298. https://doi.org/10.1016/j.cortex.2010.06.004.
Funding
This work was supported by NIEHS K23ES026239, Promise Project at Columbia, and the NVLD Project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors (Amy E. Margolis, David Pagliaccio, Katie S. Davis, Lauren Thomas, Sarah M. Banker, Marilyn Cyr, Rachel Marsh) declare that they have no conflict of interest.
Ethical approval
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation.
Informed consent
Informed consent and assent was obtained from all legal guardians and participants in the study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 2080 kb)
Rights and permissions
About this article
Cite this article
Margolis, A.E., Pagliaccio, D., Davis, K.S. et al. Neural correlates of cognitive control deficits in children with reading disorder. Brain Imaging and Behavior 14, 1531–1542 (2020). https://doi.org/10.1007/s11682-019-00083-x
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-019-00083-x