Abstract
The anatomical structure of the human brain varies widely, as does individual cognitive behavior. It is important and interesting to study the relationship between brain structure and cognitive behavior. There has however been little previous work on the relationship between inhibitory control and brain structure. The goal of this study was to elucidate possible cortical markers related to inhibitory control using structural magnetic resonance imaging (sMRI) data. In this study, we analyzed sMRI data and inhibitory control behavior measurement values from 361 healthy adults from the Human Connectome Project (HCP). The data of all participants were divided into two datasets. In the first dataset, we first constructed individual brain morphometric similarity networks by calculating the inter-regional statistical similarity relationship of nine cortical characteristic measures (such as volume) for each brain area obtained from sMRI data. Areas that covary in their morphology are termed ‘connected’. After that, we used a brain connectome-based predictive model (CPM) to search for ‘connected’ brain areas that were significantly related to inhibitory control. This is a purely data-driven method with built-in cross-validation. Two different ‘connected’ patterns were observed for high and low inhibitory control networks. The high inhibitory control network comprised 25 ‘connections’ (edges between nodes), mostly involving nodes in the prefrontal and especially orbitofrontal cortex and inferior frontal gyrus. In the low inhibitory control network, nodes were scattered between parietal, occipital and limbic areas. Furthermore, these ‘connections’ were verified as reliable and generalizable in a cross-validation dataset. Two regions of interest, the right ventromedial prefrontal cortex including a part of medial area 10 (R.OFCmed) and left middle temporal gyrus (L.MTG) were crucial nodes in the two networks, respectively, which suggests that these two regions may be fundamentally involved in inhibitory control. Our findings potentially help to understand the relationship between areas with a correlated cortical structure and inhibitory control, and further help to reveal the brain systems related to inhibition and its disorders.
Similar content being viewed by others
Abbreviations
- CPM:
-
connectome-based predictive model
- L.MTG:
-
left middle temporal gyrus
- MAPE:
-
mean absolute percentage error
- R.OFCmed:
-
right medial orbitofrontal
- sMRI:
-
structural magnetic resonance imaging
References
Abé, C., Ekman, C.-J., Sellgren, C., Petrovic, P., Ingvar, M., & Landén, M. (2016). Cortical thickness, volume and surface area in patients with bipolar disorder types I and II. Journal of Psychiatry & Neuroscience, 41(4), 240–250.
Beaty, R. E., Kenett, Y. N., Christensen, A. P., Rosenberg, M. D., Benedek, M., Chen, Q., et al. (2018). Robust prediction of individual creative ability from brain functional connectivity. Proceedings of the National Academy of Sciences, 115(5), 1087–1092.
Colzato, L. S., Ruiz, M. J., van den Wildenberg, W. P. M., Bajo, M. T., & Hommel, B. (2011). Long-term effects of chronic khat use: Impaired inhibitory control. Frontiers in Psychology, 1.
Crossley, N. A., Mechelli, A., Vertes, P. E., Winton-Brown, T. T., Patel, A. X., Ginestet, C. E., et al. (2013). Cognitive relevance of the community structure of the human brain functional coactivation network. Proceedings of the National Academy of Sciences, 110(28), 11583–11588.
Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. NeuroImage, 9(2), 179–194.
Deng, W., Rolls, E. T., Ji, X., Robbins, T. W., Banaschewski, T., Bokde, A. L. W., et al. (2017). Separate neural systems for behavioral change and for emotional responses to failure during behavioral inhibition. Human Brain Mapping, 38, 3527–3537.
Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980.
Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64(1), 135–168.
Dong, G., DeVito, E. E., Du, X., & Cui, Z. (2012). Impaired inhibitory control in “internet addiction disorder”: A functional magnetic resonance imaging study. Psychiatry Research: Neuroimaging, 203(2–3), 153–158.
Durston, S., Hulshoff Pol, H. E., Casey, B. J., Giedd, J. N., Buitelaar, J. K., & Vanengeland, H. (2001). Anatomical MRI of the developing human brain: What have we learned? Journal of the American Academy of Child and Adolescent Psychiatry, 40(9), 1012–1020.
Filbey, F., & Yezhuvath, U. (2013). Functional connectivity in inhibitory control networks and severity of cannabis use disorder. The American Journal of Drug and Alcohol Abuse, 39(6), 382–391.
Fillmore, M. T., & Rush, C. R. (2002). Impaired inhibitory control of behavior in chronic cocaine users. Drug and Alcohol Dependence, 66(3), 265–273.
Fischl, B. (2012). Freesurfer. Neuroimage, 62(2), 774–781.
Fuster, J. M. (2001). The prefrontal cortex—An update: Time is of the essence. Neuron, 30(2), 319–333.
Geisler, D., Walton, E., Naylor, M., Roessner, V., Lim, K. O., Charles Schulz, S., et al. (2015). Brain structure and function correlates of cognitive subtypes in schizophrenia. Psychiatry Research: Neuroimaging, 234(1), 74–83.
Gershon, R. C., Wagster, M. V., Hendrie, H. C., Fox, N. A., Cook, K. F., & Nowinski, C. J. (2013). NIH toolbox for assessment of neurological and behavioral function. Neurology, 80(issue 11, supplement 3), S2–S6.
Giedd, J. N. (2004). Structural magnetic resonance imaging of the adolescent brain. Annals of the New York Academy of Sciences, 1021(1), 77–85.
Glasser, M. F., & Van Essen, D. C. (2011). Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI. Journal of Neuroscience, 31(32), 11597–11616.
Hampshire, A., & Sharp, D. J. (2015). Contrasting network and modular perspectives on inhibitory control. Trends in Cognitive Sciences, 19(8), 445–452.
He, Y., Chen, Z. J., & Evans, A. C. (2007). Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cerebral Cortex, 17(10), 2407–2419.
Heaton, R. K., Akshoomoff, N., Tulsky, D., Mungas, D., Weintraub, S., Dikmen, S., et al. (2014). Reliability and validity of composite scores from the NIH toolbox cognition battery in adults. Journal of the International Neuropsychological Society, 20(06), 588–598.
Hoekzema, E., Barba-Müller, E., Pozzobon, C., Picado, M., Lucco, F., García-García, D., et al. (2016). Pregnancy leads to long-lasting changes in human brain structure. Nature Neuroscience, 20(2), 287–296.
Hummer, T. A., Wang, Y., Kronenberger, W. G., Mosier, K. M., Kalnin, A. J., Dunn, D. W., & Mathews, V. P. (2010). Short-term violent video game play by adolescents alters prefrontal activity during cognitive inhibition. Media Psychology, 13(2), 136–154.
Ilieva, I. P., Hook, C. J., & Farah, M. J. (2015). Prescription stimulants’ effects on healthy inhibitory control, working memory, and episodic memory: A meta-analysis. Journal of Cognitive Neuroscience, 27(6), 1069–1089.
Izquierdo, A., & Jentsch, J. D. (2012). Reversal learning as a measure of impulsive and compulsive behavior in addictions. Psychopharmacology, 219(2), 607–620.
Koob, G. F., & Volkow, N. D. (2010). Neurocircuitry of addiction. Neuropsychopharmacology., 35(1), 217–238.
Lerman-Sinkoff, D. B., Sui, J., Rachakonda, S., Kandala, S., Calhoun, V. D., & Barch, D. M. (2017). Multimodal neural correlates of cognitive control in the human connectome project. NeuroImage, 163, 41–54.
Li, S., Yuan, X., Pu, F., Li, D., Fan, Y., Wu, L., et al. (2014). Abnormal changes of multidimensional surface features using multivariate pattern classification in amnestic mild cognitive impairment patients. Journal of Neuroscience, 34(32), 10541–10553.
Li, W., Yang, C., Shi, F., Wu, S., Wang, Q., Nie, Y., & Zhang, X. (2017). Construction of individual morphological brain networks with multiple morphometric features. Frontiers in Neuroanatomy, 11–34.
Liddle, E. B., Hollis, C., Batty, M. J., Groom, M. J., Totman, J. J., Liotti, M., et al. (2010). Task-related default mode network modulation and inhibitory control in ADHD: Effects of motivation and methylphenidate. Journal of Child Psychology and Psychiatry, 52(7), 761–771.
Lim, H. K., Jung, W. S., Ahn, K. J., Won, W. Y., Hahn, C., Lee, S. Y., et al. (2012). Regional cortical thickness and subcortical volume changes are associated with cognitive impairments in the drug-naive patients with late-onset depression. Neuropsychopharmacology, 37(3), 838–849.
Luo, X.. (2001). Basic neuroscience. Central South University Press.
Maij, D. L., van de Wetering, B. J., & Franken, I. H. (2017). Cognitive control in young adults with cannabis use disorder: An event-related brain potential study. Journal of Psychopharmacology, 31(8), 1015–1026.
Metzuyanim-Gorlick, S., & Mashal, N. (2016). The effects of transcranial direct current stimulation over the dorsolateral prefrontal cortex on cognitive inhibition. Experimental Brain Research, 234(6), 1537–1544.
Morasch, K. C., & Bell, M. A. (2011). The role of inhibitory control in behavioral and physiological expressions of toddler executive function. Journal of Experimental Child Psychology, 108(3), 593–606.
Mostofsky, S. H., Newschaffer, C. J., & Denckla, M. B. (2003). Overflow movements predict impaired response inhibition in children with ADHD. Perceptual and Motor Skills, 97(3_suppl), 1315–1331.
Neubert, F.-X., Mars, R. B., Thomas, A. G., Sallet, J., & Rushworth, M. F. S. (2014). Comparison of human ventral frontal cortex areas for cognitive control and language with areas in monkey frontal cortex. Neuron, 81(3), 700–713.
Niendam, T. A., Laird, A. R., Ray, K. L., Dean, Y. M., Glahn, D. C., & Carter, C. S. (2012). Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective, & Behavioral Neuroscience, 12(2), 241–268.
Noonan, M. P., Chau, B. K. H., Rushworth, M. F. S., & Fellows, L. K. (2017). Contrasting effects of medial and lateral orbitofrontal cortex lesions on credit assignment and decision-making in humans. The Journal of Neuroscience, 37(29), 7023–7035.
Norman, A. L., Pulido, C., Squeglia, L. M., Spadoni, A. D., Paulus, M. P., & Tapert, S. F. (2011). Neural activation during inhibition predicts initiation of substance use in adolescence. Drug and Alcohol Dependence, 119(3), 216–223.
Öngür, D., Ferry, A. T., & Price, J. L. (2003). Architectonic subdivision of the human orbital and medial prefrontal cortex. The Journal of Comparative Neurology, 460(3), 425–449.
Panizzon, M. S., Fennema-Notestine, C., Eyler, L. T., Jernigan, T. L., Prom-Wormley, E., Neale, M., et al. (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex, 19(11), 2728–2735.
Pienaar, R., Fischl, B., Caviness, V., Makris, N., & Grant, P. E. (2008). A methodology for analyzing curvature in the developing brain from preterm to adult. International Journal of Imaging Systems and Technology, 18(1), 42–68.
Pires, L., Leitão, J., Guerrini, C., & Simões, M. R. (2014). Event-related brain potentials in the study of inhibition: Cognitive control, source localization and age-related modulations. Neuropsychology Review, 24(4), 461–490.
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.
Qi, X., Xu, F., & Fan, Z. (2017). Analysis of sMRI features of mild cognitive impairment and Alzheimer disease. China Modern Medicine.
Rimol, L. M., Nesvåg, R., Hagler, D. J., Bergmann, Ø., Fennema-Notestine, C., Hartberg, C. B., et al. (2012). Cortical volume, surface area, and thickness in schizophrenia and bipolar disorder. Biological Psychiatry, 71(6), 552–560.
Rolls, E. T. (2016). Cerebral cortex: Principles of operation. Oxford: Oxford University Press.
Rolls, E. T. (2017) The orbitofrontal cortex and emotion in health and disease, including depression. Neuropsychologia, S0028-3932(17)30347–0.
Rolls, E. T. (2018). The brain, emotion, and depression. Oxford: Oxford University Press.
Rolls, E. T. (2019). The orbitofrontal cortex. Oxford University Press.
Rosenberg, M. D., Hsu, W.-T., Scheinost, D., Todd Constable, R., & Chun, M. M. (2018). Connectome-based models predict separable components of attention in novel individuals. Journal of Cognitive Neuroscience, 30(2), 160–173.
Sabuncu, M. R., Ge, T., Holmes, A. J., Smoller, J. W., Buckner, R. L., & Fischl, B. (2016). Morphometricity as a measure of the neuroanatomical signature of a trait. Proceedings of the National Academy of Sciences, 113(39), E5749–E5756.
Schaer, M., Cuadra, M. B., Tamarit, L., Lazeyras, F., Eliez, S., & Thiran, J.-P. (2008). A surface-based approach to quantify local cortical gyrification. IEEE Transactions on Medical Imaging, 27(2), 161–170.
Schaer, M., Cuadra, M. B., Schmansky, N., Fischl, B., Thiran, J.-P., & Eliez, S. (2012). How to measure cortical folding from MR images: A step-by-step tutorial to compute local gyrification index. Journal of Visualized Experiments, 59.
Seidlitz, J., Váša, F., Shinn, M., Romero-Garcia, R., Whitaker, K. J., Vértes, P. E., et al. (2018). Morphometric similarity networks detect microscale cortical organization and predict inter-individual cognitive variation. Neuron, 97(1), 231–247.e7.
Sellitto, M., Ciaramelli, E., & di Pellegrino, G. (2010). Myopic discounting of future rewards after medial orbitofrontal damage in humans. Journal of Neuroscience, 30(49), 16429–16436.
Shen, X., Finn, E. S., Scheinost, D., Rosenberg, M. D., Chun, M. M., Papademetris, X., & Constable, R. T. (2017). Using connectome-based predictive modeling to predict individual behavior from brain connectivity. Nature Protocols, 12(3), 506–518.
Shimoda, K., Kimura, M., Yokota, M., & Okubo, Y. (2015). Comparison of regional gray matter volume abnormalities in Alzheimer′s disease and late life depression with hippocampal atrophy using VSRAD analysis: A voxel-based morphometry study. Psychiatry Research: Neuroimaging, 232(1), 71–75.
Smid, H. G., Böcker, K. B., van Touw, D. A., Mulder, G., & Brunia, C. H. (1996). A psychophysiological investigation of the selection and the use of partial stimulus information in response choice. Journal of Experimental Psychology: Human Perception and Performance, 22(1), 3–24.
Sowell, E. R., Trauner, D. A., Gamst, A., & Jernigan, T. L. (2007). Development of cortical and subcortical brain structures in childhood and adolescence: A structural MRI study. Developmental Medicine & Child Neurology, 44(1), 4–16.
Stange, J. P., Bessette, K. L., Jenkins, L. M., Peters, A. T., Feldhaus, C., Crane, N. A., et al. (2017). Attenuated intrinsic connectivity within cognitive control network among individuals with remitted depression: Temporal stability and association with negative cognitive styles. Human Brain Mapping, 38(6), 2939–2954.
Szatkowska, I., Szymańska, O., Bojarski, P., & Grabowska, A. (2007). Cognitive inhibition in patients with medial orbitofrontal damage. Experimental Brain Research, 181(1), 109–115.
Tofallis, C. (2015). A better measure of relative prediction accuracy for model selection and model estimation. Journal of the Operational Research Society, 66(8), 1352–1362.
Van Essen, D. C., Smith, S. M., Barch, D. M., Behrens, T. E. J., Yacoub, E., & Ugurbil, K. (2013). The WU-Minn human connectome project: An overview. NeuroImage, 80, 62–79.
Vandekar, S. N., Shinohara, R. T., Raznahan, A., Hopson, R. D., Roalf, D. R., Ruparel, K., et al. (2016). Subject-level measurement of local cortical coupling. NeuroImage, 133, 88–97.
Walton, M. E., Behrens, T. E. J., Buckley, M. J., Rudebeck, P. H., & Rushworth, M. F. S. (2010). Separable learning Systems in the Macaque Brain and the role of orbitofrontal cortex in contingent learning. Neuron, 65(6), 927–939.
Watson, A. J., & Bell, M. A. (2013). Individual differences in inhibitory control skills at three years of age. Developmental Neuropsychology, 38(1), 1–21.
Weintraub, S., Dikmen, S. S., Heaton, R. K., Tulsky, D. S., Zelazo, P. D., Bauer, P. J., … Gershon, R. C. (2013). Cognition assessment using the NIH toolbox. Neurology, 80(issue 11, supplement 3), S54–S64.
Whitaker, K., Vértes, P., Romero-Garcia, R., Váša, F., Moutoussis, M., Prabhub, G., et al. (2017). Adolescence is associated with genomically patterned consolidation of the hubs of the human brain connectome. Biological Psychiatry, 81(10), S152–S153.
Wong, A. W. K., Chen, C., Baum, M. C., Heaton, R. K., Goodman, B., & Heinemann, A. W. (2019). Cognitive, emotional, and physical functioning as predictors of paid employment in people with stroke, traumatic brain injury, and spinal cord injury. American Journal of Occupational Therapy, 73(2), 7302205010p1–7302205010p15.
Yokota, S., Takeuchi, H., Hashimoto, T., Hashizume, H., Asano, K., Asano, M., et al. (2015). Individual differences in cognitive performance and brain structure in typically developing children. Developmental Cognitive Neuroscience, 14, 1–7.
Yu, K., Wang, X., Li, Q., Zhang, X., Li, X., & Li, S. (2018). Individual morphological brain network construction based on multivariate euclidean distances between brain regions. Frontiers in Human Neuroscience, 12.
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.
Zelazo, P. D., Anderson, J. E., Richler, J., Wallner-Allen, K., Beaumont, J. L., Conway, K. P., et al. (2014). NIH toolbox cognition battery (CB): Validation of executive function measures in adults. Journal of the International Neuropsychological Society, 20(06), 620–629.
Acknowledgements
Use of the Human Connectome Project (https://www.humanconnectome.org/) dataset is acknowledged. Shuixia Guo is supported by the National Natural Science Foundation of China (NSFC) grant (No.11671129). All work of the study was done by the authors. The authors were responsible for the authenticity of the data and related results.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no competing interests.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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
(DOC 3376 kb)
Rights and permissions
About this article
Cite this article
He, N., Rolls, E.T., Zhao, W. et al. Predicting human inhibitory control from brain structural MRI. Brain Imaging and Behavior 14, 2148–2158 (2020). https://doi.org/10.1007/s11682-019-00166-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-019-00166-9