Abstract
It is thought that brain structure is the primary determinant of functions of brain regions. For example, cortical areas with functional differences also have different structural connectivity (SC) patterns. We used SCs derived from diffusion tensor imaging (DTI) data in 100 healthy adults included in the Human Connectome Project (HCP) to successfully predict cortical activation responses across distinct cognitive tasks and found that predictive performance varied among tasks. We also observed that predictive performance could be used to characterize task load in both relational reasoning and N-back working memory tasks and was significantly positively associated with behavioral performance. Moreover, we found that the default mode network (DMN) played a more dominant role in both activation prediction and behavioral performance than was found for other functional networks. These results support our hypothesis that individuals who performed tasks better might exhibit a more accurate predicted activation pattern as task-evoked activities are more inclined to flow over inherent structural networks than over more flexible paths. In the high difficulty condition, the decreased correlation between predicted and empirical activation may be associated with the more random brain activity in these conditions/participants due to the lack of engagement. Together, our findings highlight the feasibility of using SCs to estimate various cognitive task activations and thus further facilitate the exploration of the relationship between the brain and behavior by providing strong evidence for the relevance of structure to function in the human brain.
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Availability of data and material
All the imaging data used in this study are available in the Human Connectome Project’s Connectome DB repository (https://db.humanconnectome.org) under the identifiers ‘WU-Minn HCP Data’ and ‘100 Unrelated Subjects’.
Code availability
Codes are availiable in the GitHub repository (https://github.com/Tiantianhub/Activityflow_dti).
References
Alders GL et al (2019) Reduced accuracy accompanied by reduced neural activity during the performance of an emotional conflict task by unmedicated patients with major depression: A CAN-BIND fMRI study. J Affect Disord 257:765–773. https://doi.org/10.1016/j.jad.2019.07.037
Andrews-Hanna JR, Smallwood J, Spreng RN (2014) The default network and self-generated thought: component processes, dynamic control, and clinical relevance Year in Cognitive. Neuroscience 1316:29–52. https://doi.org/10.1111/nyas.12360
Barch DM et al (2013) Function in the human connectome: Task-fMRI and individual differences in behavior. Neuroimage 80:169–189. https://doi.org/10.1016/j.neuroimage.2013.05.033
Bassett DS, Wymbs NF, Porter MA, Mucha PJ, Carlson JM, Grafton ST (2011) Dynamic reconfiguration of human brain networks during learning. Proc Natl Acad Sci USA 108:7641–7646. https://doi.org/10.1073/pnas.1018985108
Berron D et al (2019) Higher CSF Tau levels are related to hippocampal hyperactivity and object mnemonic discrimination in older adults. J Neurosci 39:8788–8797. https://doi.org/10.1523/Jneurosci.1279-19.2019
Binder JR et al (2011) Mapping anterior temporal lobe language areas with fMRI: a multicenter normative study. Neuroimage 54:1465–1475. https://doi.org/10.1016/j.neuroimage.2010.09.048
Bluhm RL et al (2007) Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: Anomalies in the default network. Schizophr Bull 33:1004–1012. https://doi.org/10.1093/schbul/sbm052
Braun U et al (2015) Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proc Natl Acad Sci USA 112:11678–11683. https://doi.org/10.1073/pnas.1422487112
Buckner RL, Andrews-Hanna JR (2008) Schacter DL (2008) The brain’s default network—anatomy, function, and relevance to disease year in cognitive. Neuroscience 1124:1–38. https://doi.org/10.1196/annals.1440.011
Cabeza R, Nyberg L (2000) Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12:1–47. https://doi.org/10.1162/08989290051137585
Cao L, Liu Z (2020) How IQ depends on the running mode of brain network? Chaos. https://doi.org/10.1063/5.0008289
Cole MW, Pathak S, Schneider W (2010) Identifying the brain’s most globally connected regions. Neuroimage 49:3132–3148. https://doi.org/10.1016/j.neuroimage.2009.11.001
Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS (2012) Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32:8988–8999. https://doi.org/10.1523/jneurosci.0536-12.2012
Cole MW, Ito T, Bassett DS, Schultz DH (2016) Activity flow over resting-state networks shapes cognitive task activations. Nat Neurosci 19:1718–1726. https://doi.org/10.1038/nn.4406
Correia AI, Branco P, Martins M, Reis AM, Martins N, Castro SL, Lima CF (2019) Resting-state connectivity reveals a role for sensorimotor systems in vocal emotional processing in children. Neuroimage 201:10. https://doi.org/10.1016/j.neuroimage.2019.116052
Cui ZX, Zhong SY, Xu PF, He Y, Gong GL (2013) PANDA: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci 7:16. https://doi.org/10.3389/fnhum.2013.00042
Cullum A, Hodgetts WE, Milburn TF, Cummine J (2019) Cerebellar activation during reading tasks: exploring the dichotomy between motor vs. language functions in adults of varying reading proficiency. Cerebellum 18:688–704. https://doi.org/10.1007/s12311-019-01024-6
Drobyshevsky A, Baumann SB, Schneider W (2006) A rapid fMRI task battery for mapping of visual, motor, cognitive, and emotional function Neuroimage 31:732–744 doi:https://doi.org/10.1016/j.neuroimage.2005.12.016
Edde M et al (2020) Age-related change in episodic memory: role of functional and structural connectivity between the ventral posterior cingulate and the parietal cortex. Brain Struct Funct 225:2203–2218. https://doi.org/10.1007/s00429-020-02121-7
Elton A, Gao W (2015) Task-positive Functional Connectivity of the Default Mode Network Transcends Task Domain. J Cogn Neurosci 27:2369–2381. https://doi.org/10.1162/jocn_a_00859
Evangelisti S et al (2019) L-Dopa modulation of brain connectivity in parkinson’s disease patients: a Pilot EEG-fMRI Study. Front Neurosci 13:10. https://doi.org/10.3389/fnins.2019.00611
Falakshahi H et al (2020) Meta-modal information flow: a method for capturing multimodal modular disconnectivity in schizophrenia ieee transactions. Biomed Eng 67:2572–2584. https://doi.org/10.1109/tbme.2020.2964724
Genc E, Fraenz C, Schluter C, Friedrich P, Voelkle MC, Hossiep R, Gunturkun O (2019) The neural architecture of general knowledge. Eur J Personal 33:589–605. https://doi.org/10.1002/per.2217
Glasser MF et al (2013) The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage 80:105–124. https://doi.org/10.1016/j.neuroimage.2013.04.127
Gong GL, He Y, Concha L, Lebel C, Gross DW, Evans AC, Beaulieu C (2009) Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb Cortex 19:524–536. https://doi.org/10.1093/cercor/bhn102
Hammer R, Paul EJ, Hillman CH, Kramer AF, Cohen NJ, Barbey AK (2019) Individual differences in analogical reasoning revealed by multivariate task-based functional brain imaging. Neuroimage 184:993–1004. https://doi.org/10.1016/j.neuroimage.2018.09.011
Hariri AR, Tessitore A, Mattay VS, Fera F, Weinberger DR (2002) The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 17:317–323. https://doi.org/10.1006/nimg.2002.1179
Hearne LJ, Cocchi L, Zalesky A, Mattingley JB (2017) Reconfiguration of brain network architectures between resting-state and complexity-dependent cognitive reasoning. J Neurosci 37:8399–8411. https://doi.org/10.1523/Jneurosci.0485-17.2017
Huang AS, Rogers BP, Anticevic A, Blackford JU, Heckers S (2019) Woodward ND (2019) Brain function during stages of working memory in schizophrenia and psychotic bipolar disorder (vol 44, pg 2136. Neuropsychopharmacology 44:2143–2143. https://doi.org/10.1038/s41386-019-0488-3
Jang JH et al (2011) Reduced prefrontal functional connectivity in the default mode network is related to greater psychopathology in subjects with high genetic loading for schizophrenia. Schizophr Res 127:58–65. https://doi.org/10.1016/j.schres.2010.12.022
Kim Y-K, Han K-M (2021) Neural substrates for late-life depression: A selective review of structural neuroimaging studies. Prog Neuro-Psychopharmacol Biol Psychiatry 104:28. https://doi.org/10.1016/j.pnpbp.2020.110010
Kochunov P et al (2015) Heritability of fractional anisotropy in human white matter: a comparison of human connectome Project and ENIGMA-DTI data. Neuroimage 111:300–311. https://doi.org/10.1016/j.neuroimage.2015.02.050
Kurth S, Bahri MA, Collette F, Phillips C, Majerus S, Bastin C, Salmon E (2019) Alzheimer’s disease patients activate attention networks in a short-term memory task. Neuroimage Clin 23:15. https://doi.org/10.1016/j.nicl.2019.101892
Li YH, Liu Y, Li J, Qin W, Li KC, Yu CS, Jiang TZ (2009) Brain anatomical network and intelligence. PLoS Comput Biol 5:17. https://doi.org/10.1371/journal.pcbi.1000395
Li CH et al (2017) Impaired topological architecture of brain structural networks in idiopathic Parkinson’s disease: a DTI study. Brain Imaging Behav 11:113–128. https://doi.org/10.1007/s11682-015-9501-6
Liu X et al (2020) Disrupted rich-club network organization and individualized identification of patients with major depressive disorder. Prog Neuro-Psychopharmacol Biol Psychiatry 12:110074–110074. https://doi.org/10.1016/j.pnpbp.2020.110074
Mori S, van Zijl PCM (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480. https://doi.org/10.1002/nbm.781
Mori S, Crain BJ, Chacko VP, van Zijl PCM (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269. https://doi.org/10.1002/1531-8249(199902)45:2%3c265::Aid-Ana21%3e3.0.Co;2-3
Moseley M (2002) Diffusion tensor imaging and aging—a review. NMR Biomed 15:553–560. https://doi.org/10.1002/nbm.785
Newton AT, Morgan VL, Rogers BP, Gore JC (2011) Modulation of steady state functional connectivity in the default mode and working memory networks by cognitive load. Hum Brain Mapp 32:1649–1659. https://doi.org/10.1002/hbm.21138
Osher DE, Saxe RR, Koldewyn K, Gabrieli JDE, Kanwisher N, Saygin ZM (2016) Structural connectivity fingerprints predict cortical selectivity for multiple visual categories across cortex. Cereb Cortex 26:1668–1683. https://doi.org/10.1093/cercor/bhu303
Phillips ML, Swartz HA (2014) A critical appraisal of neuroimaging studies of bipolar disorder: toward a new conceptualization of underlying neural circuitry and a road map for future research. Am J Psychiatry 171:829–843. https://doi.org/10.1176/appi.ajp.2014.13081008
Rigotti M, Barak O, Warden MR, Wang XJ, Daw ND, Miller EK, Fusi S (2013) The importance of mixed selectivity in complex cognitive tasks. Nature 497:585–590. https://doi.org/10.1038/nature12160
Sala-Llonch R, Pena-Gomez C, Arenaza-Urquijo EM, Vidal-Pineiro D, Bargallo N, Junque C, Bartres-Faz D (2012) Brain connectivity during resting state and subsequent working memory task predicts behavioural performance. Cortex 48:1187–1196. https://doi.org/10.1016/j.cortex.2011.07.006
Salami A et al (2019) Dopamine D-2/3 binding potential modulates neural signatures of working memory in a load-dependent fashion. J Neurosci 39:537–547. https://doi.org/10.1523/Jneurosci.1493-18.2018
Sami S, Robertson EM, Miall RC (2014) The time course of task-specific memory consolidation effects in resting state networks. J Neurosci 34:3982–3992. https://doi.org/10.1523/Jneurosci.4341-13.2014
Saygin ZM, Osher DE, Koldewyn K, Reynolds G, Gabrieli JDE, Saxe RR (2012) Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat Neurosci 15:321–327. https://doi.org/10.1038/nn.3001
Shine JM et al (2016) The Dynamics of Functional Brain Networks: Integrated Network States during Cognitive Task Performance. Neuron 92:544–554. https://doi.org/10.1016/j.neuron.2016.09.018
Sitaram R et al (2017) Closed-loop brain training: the science of neurofeedback Nature reviews. Neuroscience 18:86–100. https://doi.org/10.1038/nrn.2016.164
Smith R, Keramatian K, Christoff K (2007) Localizing the rostrolateral prefrontal cortex at the individual level. Neuroimage 36:1387–1396. https://doi.org/10.1016/j.neuroimage.2007.04.032
Smith SM et al (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045. https://doi.org/10.1073/pnas.0905267106
Sole-Casals J et al (2019) Structural brain network of gifted children has a more integrated and versatile topology. Brain Struct Funct 224:2373–2383. https://doi.org/10.1007/s00429-019-01914-9
Straathof M et al (2019) A systematic review on the quantitative relationship between structural and functional network connectivity strength in mammalian brains. J Cereb Blood Flow Metab 39:189–209. https://doi.org/10.1177/0271678x18809547
Tagliazucchi E, Laufs H (2014) Decoding wakefulness levels from typical fmri resting-state data reveals reliable drifts between wakefulness and sleep. Neuron 82:695–708. https://doi.org/10.1016/j.neuron.2014.03.020
Tavor I, Jones OP, Mars RB, Smith SM, Behrens TE, Jbabdi S (2016) Task-free MRI predicts individual differences in brain activity during task performance. Science 352:216–220. https://doi.org/10.1126/science.aad8127
Teng J, Massar SAA, Tandi J, Lim J (2019) Pace yourself: neural activation and connectivity changes over time vary by task type and pacing. Brain Cogn 137:11. https://doi.org/10.1016/j.bandc.2019.103629
Thompson GJ et al (2013) Short-time windows of correlation between large-scale functional brain networks predict vigilance intraindividually and interindividually. Hum Brain Mapp 34:3280–3298. https://doi.org/10.1002/hbm.22140
Tung KC, Uh J, Mao D, Xu F, Xiao GH, Lu HZ (2013) Alterations in resting functional connectivity due to recent motor task. Neuroimage 78:316–324. https://doi.org/10.1016/j.neuroimage.2013.04.006
Tzourio-Mazoyer N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289. https://doi.org/10.1006/nimg.2001.0978
Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K, Consortium W-MH (2013) The WU-Minn Human Connectome Project: An overview Neuroimage 80:62-79 doi:https://doi.org/10.1016/j.neuroimage.2013.05.041
Wang JH, Wang XD, Xia MR, Liao XH, Evans A, He Y (2015) GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci 9:16. https://doi.org/10.3389/fnhum.2015.00386
Wang K et al (2019) GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Dev Cogn Neurosci 37:10. https://doi.org/10.1016/j.dcn.2019.100647
Wang Z, Yuan Y, You J, Zhang Z (2020) Disrupted structural brain connectome underlying the cognitive deficits in remitted late-onset depression. Brain Imag Behav 14:1600–1611. https://doi.org/10.1007/s11682-019-00091-x
Xie YY et al (2019) Changes in centrality frequency of the default mode network in individuals with subjective cognitive decline. Front Aging Neurosci 11:11. https://doi.org/10.3389/fnagi.2019.00118
Yan CG, Wang XD, Zuo XN, Zang YF (2016) DPABI: data processing & analysis for (Resting-State). Brain Imag Neuroinf 14:339–351. https://doi.org/10.1007/s12021-016-9299-4
Yan TY et al (2019) Early-stage identification and pathological development of Alzheimer’s disease using multimodal MRI. J Alzheimers Dis 68:1013–1027. https://doi.org/10.3233/Jad-181049
Yang FPG, Bal SS, Lee J-F, Chen C-C (2020) White matter differences in networks in elders with mild cognitive impairment and Alzheimer’s disease. Brain Connect. https://doi.org/10.1089/brain.2020.0767
Zhang RB et al (2015) Disrupted brain anatomical connectivity in medication-na < ve patients with first-episode schizophrenia. Brain Struct Funct 220:1145–1159. https://doi.org/10.1007/s00429-014-0706-z
Zhang ZF et al (2018) Polymorphism in schizophrenia risk gene MIR137 is associated with the posterior cingulate Cortex’s activation and functional and structural connectivity in healthy controls. Neuroimage-Clinical 19:160–166. https://doi.org/10.1016/j.nicl.2018.03.039
Zhong M et al (2019) Effects of levodopa therapy on voxel-based degree centrality in Parkinson’s disease. Brain Imaging Behav 13:1202–1219. https://doi.org/10.1007/s11682-018-9936-7
Zuo NM, Salami A, Yang YH, Yang ZY, Sui J, Jiang TZ (2019) Activation-based association profiles differentiate network roles across cognitive loads. Hum Brain Mapp 40:2800–2812. https://doi.org/10.1002/hbm.24561
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We gratefully acknowledge all the participants. We thank Yan Yan for her help and contribution during data processing.
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This work was supported by the National Key R&D Program of China (Grant Number 2018YFC0115400), the National Natural Science Foundation of China (Grant Numbers U20A20191, 61727807), and the Beijing Municipal Science & Technology Commission (Grant Number Z191100010618004).
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TY conceptualized and designed the study; TL wrote the paper; JA performed the data analysis; ZS downloaded the data; JZ revised the paper; GP and JW interpreted the data. All authors agree to be accountable for all aspects of the work.
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Yan, T., Liu, T., Ai, J. et al. Task-induced activation transmitted by structural connectivity is associated with behavioral performance. Brain Struct Funct 226, 1437–1452 (2021). https://doi.org/10.1007/s00429-021-02249-0
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DOI: https://doi.org/10.1007/s00429-021-02249-0