Cortical Morphological Networks Differ Between Gyri and Sulci
Language English Country Singapore Media print-electronic
Document type Journal Article
PubMed
39044060
PubMed Central
PMC11748734
DOI
10.1007/s12264-024-01262-7
PII: 10.1007/s12264-024-01262-7
Knihovny.cz E-resources
- Keywords
- Cortical folding, Graph theory, Magnetic resonance imaging, Morphological connectivity, Test-retest reliability,
- MeSH
- Depressive Disorder, Major pathology diagnostic imaging MeSH
- Adult MeSH
- Connectome methods MeSH
- Humans MeSH
- Magnetic Resonance Imaging MeSH
- Young Adult MeSH
- Cerebral Cortex * diagnostic imaging anatomy & histology MeSH
- Nerve Net * diagnostic imaging anatomy & histology MeSH
- Neural Pathways MeSH
- Check Tag
- Adult MeSH
- Humans MeSH
- Young Adult MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
This study explored how the human cortical folding pattern composed of convex gyri and concave sulci affected single-subject morphological brain networks, which are becoming an important method for studying the human brain connectome. We found that gyri-gyri networks exhibited higher morphological similarity, lower small-world parameters, and lower long-term test-retest reliability than sulci-sulci networks for cortical thickness- and gyrification index-based networks, while opposite patterns were observed for fractal dimension-based networks. Further behavioral association analysis revealed that gyri-gyri networks and connections between gyral and sulcal regions significantly explained inter-individual variance in Cognition and Motor domains for fractal dimension- and sulcal depth-based networks. Finally, the clinical application showed that only sulci-sulci networks exhibited morphological similarity reductions in major depressive disorder for cortical thickness-, fractal dimension-, and gyrification index-based networks. Taken together, these findings provide novel insights into the constraint of the cortical folding pattern to the network organization of the human brain.
Center for Studies of Psychological Application South China Normal University Guangzhou 510631 China
Institute for Brain Research and Rehabilitation South China Normal University Guangzhou 510631 China
School of Interdisciplinary Engineering and Sciences Islamabad 44000 Pakistan
See more in PubMed
Bullmore E, Sporns O. Complex brain networks: Graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009, 10: 186–198. PubMed
Liao X, Vasilakos AV, He Y. Small-world human brain networks: Perspectives and challenges. Neurosci Biobehav Rev 2017, 77: 286–300. PubMed
van den Heuvel MP, Sporns O. Network hubs in the human brain. Trends Cogn Sci 2013, 17: 683–696. PubMed
Sporns O, Betzel RF. Modular brain networks. Annu Rev Psychol 2016, 67: 613–640. PubMed PMC
Iturria-Medina Y, Pérez Fernández A, Morris DM, Canales-Rodríguez EJ, Haroon HA, García Pentón L. Brain hemispheric structural efficiency and interconnectivity rightward asymmetry in human and nonhuman Primates. Cereb Cortex 2011, 21: 56–67. PubMed
Tian L, Wang J, Yan C, He Y. Hemisphere- and gender-related differences in small-world brain networks: A resting-state functional MRI study. Neuroimage 2011, 54: 191–202. PubMed
Choi YH, Yun JY, Kim BH, Lee MH, Song SK, Lee JM. Gender-related and hemispheric effects in cortical thickness-based hemispheric brain morphological network. Biomed Res Int 2020, 2020: 3560259. PubMed PMC
Yang S, Zhao Z, Cui H, Zhang T, Zhao L, He Z, et al. Temporal variability of cortical gyral-sulcal resting state functional activity correlates with fluid intelligence. Front Neural Circuits 2019, 13: 36. PubMed PMC
Liu H, Zhang S, Jiang X, Zhang T, Huang H, Ge F, et al. The cerebral cortex is bisectionally segregated into two fundamentally different functional units of gyri and sulci. Cereb Cortex 2019, 29: 4238–4252. PubMed PMC
Zhao L, Zhang T, Guo L, Liu T, Jiang X. Gyral-sulcal contrast in intrinsic functional brain networks across task performances. Brain Imaging Behav 2021, 15: 1483–1498. PubMed
Liu H, Jiang X, Zhang T, Ren Y, Hu X, Guo L, et al. Elucidating functional differences between cortical gyri and sulci via sparse representation HCP grayordinate fMRI data. Brain Res 2017, 1672: 81–90. PubMed PMC
Deng F, Jiang X, Zhu D, Zhang T, Li K, Guo L, et al. A functional model of cortical gyri and sulci. Brain Struct Funct 2014, 219: 1473–1491. PubMed PMC
Li X, Hu X, Jiang X, Guo L, Han J, Liu T (2013) Assessing structural organization and functional interaction in gyral, sulcal and cortical networks. In: Shen Li et al (eds) International Workshop on Multimodal Brain Image Analysis, Springer, Cham, pp 9–17.
Nie J, Guo L, Li K, Wang Y, Chen G, Li L, et al. Axonal fiber terminations concentrate on gyri. Cereb Cortex 2012, 22: 2831–2839. PubMed PMC
He Y, Chen ZJ, Evans AC. Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 2007, 17: 2407–2419. PubMed
Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A. Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 2008, 28: 9239–9248. PubMed PMC
Wang J, He Y. Toward individualized connectomes of brain morphology. Trends Neurosci 2024, 47: 106–119. PubMed
Cai M, Ma J, Wang Z, Zhao Y, Zhang Y, Wang H, et al. Individual-level brain morphological similarity networks: Current methodologies and applications. CNS Neurosci Ther 2023, 29: 3713–3724. PubMed PMC
Li Y, Wang N, Wang H, Lv Y, Zou Q, Wang J. Surface-based single-subject morphological brain networks: Effects of morphological index, brain parcellation and similarity measure, sample size-varying stability and test-retest reliability. Neuroimage 2021, 235: 118018. PubMed
Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K, et al. The WU-Minn Human Connectome Project: An overview. Neuroimage 2013, 80: 62–79. PubMed PMC
Lin Q, Dai Z, Xia M, Han Z, Huang R, Gong G, et al. A connectivity-based test-retest dataset of multi-modal magnetic resonance imaging in young healthy adults. Sci Data 2015, 2: 150056. PubMed PMC
Liu W, Wei D, Chen Q, Yang W, Meng J, Wu G, et al. Longitudinal test-retest neuroimaging data from healthy young adults in southwest China. Sci Data 2017, 4: 170017. PubMed PMC
Wu Y, Zheng Y, Li J, Liu Y, Liang X, Chen Y, et al. Subregion-specific, modality-dependent and timescale-sensitive hippocampal connectivity alterations in patients with first-episode, drug-naïve major depression disorder. J Affect Disord 2022, 305: 159–172. PubMed
Zheng Y, Wu Y, Liu Y, Li D, Liang X, Chen Y, et al. Abnormal dynamic functional connectivity of thalamic subregions in patients with first-episode, drug-naïve major depressive disorder. Front Psychiatry 2023, 14: 1152332. PubMed PMC
Li Z, Li J, Wang N, Lv Y, Zou Q, Wang J. Single-subject cortical morphological brain networks: Phenotypic associations and neurobiological substrates. Neuroimage 2023, 283: 120434. PubMed
Yu M, Linn KA, Cook PA, Phillips ML, McInnis M, Fava M, et al. Statistical harmonization corrects site effects in functional connectivity measurements from multi-site fMRI data. Hum Brain Mapp 2018, 39: 4213–4227. PubMed PMC
Güney B, Çullu N, Özdemir MY. Evaluation of olfactory bulbus volume and olfactory sulcus depth development with 3 Tesla magnetic resonance imaging in childhood. Folia Morphol 2022, 81: 307–313. PubMed
Meregalli V, Alberti F, Madan CR, Meneguzzo P, Miola A, Trevisan N, et al. Cortical complexity estimation using fractal dimension: A systematic review of the literature on clinical and nonclinical samples. Eur J Neurosci 2022, 55: 1547–1583. PubMed PMC
Sasabayashi D, Takahashi T, Takayanagi Y, Suzuki M. Anomalous brain gyrification patterns in major psychiatric disorders: A systematic review and transdiagnostic integration. Transl Psychiatry 2021, 11: 176. PubMed PMC
Suh JS, Schneider MA, Minuzzi L, MacQueen GM, Strother SC, Kennedy SH, et al. Cortical thickness in major depressive disorder: A systematic review and meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 2019, 88: 287–302. PubMed
Cascino G, Canna A, Monteleone AM, Russo AG, Prinster A, Aiello M, et al. Cortical thickness, local gyrification index and fractal dimensionality in people with acute and recovered Anorexia Nervosa and in people with Bulimia Nervosa. Psychiatry Res Neuroimaging 2020, 299: 111069. PubMed
Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM. The structure of the cerebral cortex across adult life: Age-related patterns of surface area, thickness, and gyrification. Cereb Cortex 2013, 23: 2521–2530. PubMed
Lv Y, Wei W, Han X, Song Y, Han Y, Zhou C, et al. Multiparametric and multilevel characterization of morphological alterations in patients with transient ischemic attack. Hum Brain Mapp 2021, 42: 2045–2060. PubMed PMC
Podgórski P, Bladowska J, Sasiadek M, Zimny A. Novel volumetric and surface-based magnetic resonance indices of the aging brain - does male and female brain age in the same way? Front Neurol 2021, 12: 645729. PubMed PMC
Yin G, Li T, Jin S, Wang N, Li J, Wu C, et al. A comprehensive evaluation of multicentric reliability of single-subject cortical morphological networks on traveling subjects. Cereb Cortex 2023, 33: 9003–9019. PubMed
Ruan J, Wang N, Li J, Wang J, Zou Q, Lv Y, et al. Single-subject cortical morphological brain networks across the adult lifespan. Hum Brain Mapp 2023, 44: 5429–5449. PubMed PMC
Destrieux C, Fischl B, Dale A, Halgren E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 2010, 53: 1–15. PubMed PMC
Yang Y, Li J, Li T, Li Z, Zhuo Z, Han X, et al. Cerebellar connectome alterations and associated genetic signatures in multiple sclerosis and neuromyelitis optica spectrum disorder. J Transl Med 2023, 21: 352. PubMed PMC
Wang H, Jin X, Zhang Y, Wang J. Single-subject morphological brain networks: Connectivity mapping, topological characterization and test-retest reliability. Brain Behav 2016, 6: e00448. PubMed PMC
Wang J, Wang L, Zang Y, Yang H, Tang H, Gong Q, et al. Parcellation-dependent small-world brain functional networks: A resting-state fMRI study. Hum Brain Mapp 2009, 30: 1511–1523. PubMed PMC
Watts DJ, Strogatz SH. Collective dynamics of ‘small-world’ networks. Nature 1998, 393: 440–442. PubMed
Achard S, Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol 2007, 3: e17. PubMed PMC
Wang J, Wang X, Xia M, Liao X, Evans A, He Y. GRETNA: A graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci 2015, 9: 386. PubMed PMC
Maslov S, Sneppen K. Specificity and stability in topology of protein networks. Science 2002, 296: 910–913. PubMed
Zhang J, Wang J, Wu Q, Kuang W, Huang X, He Y, et al. Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biol Psychiatry 2011, 70: 334–342. PubMed
Shrout PE, Fleiss JL. Intraclass correlations: Uses in assessing rater reliability. Psychol Bull 1979, 86: 420–428. PubMed
Wang JH, Zuo XN, Gohel S, Milham MP, Biswal BB, He Y. Graph theoretical analysis of functional brain networks: Test-retest evaluation on short- and long-term resting-state functional MRI data. PLoS One 2011, 6: e21976. PubMed PMC
Ge T, Reuter M, Winkler AM, Holmes AJ, Lee PH, Tirrell LS, et al. Multidimensional heritability analysis of neuroanatomical shape. Nat Commun 2016, 7: 13291. PubMed PMC
Liégeois R, Li J, Kong R, Orban C, van De Ville D, Ge T, et al. Resting brain dynamics at different timescales capture distinct aspects of human behavior. Nat Commun 2019, 10: 2317. PubMed PMC
Baggio HC, Abos A, Segura B, Campabadal A, Garcia-Diaz A, Uribe C, et al. Statistical inference in brain graphs using threshold-free network-based statistics. Hum Brain Mapp 2018, 39: 2289–2302. PubMed PMC
Hilgetag CC, Barbas H. Developmental mechanics of the primate cerebral cortex. Anat Embryol 2005, 210: 411–417. PubMed
Bassett DS, Bullmore E. Small-world brain networks. Neuroscientist 2006, 12: 512–523. PubMed
Jiang X, Zhang T, Zhang S, Kendrick KM, Liu T. Fundamental functional differences between gyri and sulci: Implications for brain function, cognition, and behavior. Psychoradiology 2021, 1: 23–41. PubMed PMC
Sun BB, Loomis SJ, Pizzagalli F, Shatokhina N, Painter JN, Foley CN, et al. Genetic map of regional sulcal morphology in the human brain from UK biobank data. Nat Commun 2022, 13: 6071. PubMed PMC
Pizzagalli F, Auzias G, Yang Q, Mathias SR, Faskowitz J, Boyd JD, et al. The reliability and heritability of cortical folds and their genetic correlations across hemispheres. Commun Biol 2020, 3: 510. PubMed PMC
van der Meer D, Kaufmann T, Shadrin AA, Makowski C, Frei O, Roelfs D, et al. The genetic architecture of human cortical folding. Sci Adv 2021, 7: eabj9446. PubMed PMC
Lin HY, Huang CC, Chou KH, Yang AC, Lo CYZ, Tsai SJ, et al. Differential patterns of gyral and sulcal morphological changes during normal aging process. Front Aging Neurosci 2021, 13: 625931. PubMed PMC
Jiang M, Chen Y, Yan J, Xiao Z, Mao W, Zhao B, et al. Anatomy-guided spatio-temporal graph convolutional networks (AG-STGCNs) for modeling functional connectivity between gyri and sulci across multiple task domains. IEEE Trans Neural Netw Learn Syst 2024, 35: 7435–7445. PubMed
Jiang X, Li X, Lv J, Zhang T, Zhang S, Guo L, et al. Sparse representation of HCP grayordinate data reveals novel functional architecture of cerebral cortex. Hum Brain Mapp 2015, 36: 5301–5319. PubMed PMC
Jiang X, Li X, Lv J, Zhao S, Zhang S, Zhang W, et al. Temporal dynamics assessment of spatial overlap pattern of functional brain networks reveals novel functional architecture of cerebral cortex. IEEE Trans Biomed Eng 2018, 65: 1183–1192. PubMed PMC
Beauchamp MS, Lee KE, Haxby JV, Martin A. Parallel visual motion processing streams for manipulable objects and human movements. Neuron 2002, 34: 149–159. PubMed
Han Z, Bi Y, Chen J, Chen Q, He Y, Caramazza A. Distinct regions of right temporal cortex are associated with biological and human-agent motion: Functional magnetic resonance imaging and neuropsychological evidence. J Neurosci 2013, 33: 15442–15453. PubMed PMC
Szendi I, Kiss M, Racsmány M, Boda K, Cimmer C, Vörös E, et al. Correlations between clinical symptoms, working memory functions and structural brain abnormalities in men with schizophrenia. Psychiatry Res 2006, 147: 47–55. PubMed
Matsui M, Suzuki M, Zhou SY, Takahashi T, Kawasaki Y, Yuuki H, et al. The relationship between prefrontal brain volume and characteristics of memory strategy in schizophrenia spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32: 1854–1862. PubMed
Wood JL, Murko V, Nopoulos P. Ventral frontal cortex in children: Morphology, social cognition and femininity/masculinity. Soc Cogn Affect Neurosci 2008, 3: 168–176. PubMed PMC
Szatkowska I, Szymańska O, Grabowska A. The role of the human ventromedial prefrontal cortex in memory for contextual information. Neurosci Lett 2004, 364: 71–75. PubMed
Cloots RJH, Gervaise HMT, van Dommelen JAW, Geers MGD. Biomechanics of traumatic brain injury: Influences of the morphologic heterogeneities of the cerebral cortex. Ann Biomed Eng 2008, 36: 1203–1215. PubMed PMC
Ghajari M, Hellyer PJ, Sharp DJ. Computational modelling of traumatic brain injury predicts the location of chronic traumatic encephalopathy pathology. Brain 2017, 140: 333–343. PubMed PMC
Goldstein LE, Fisher AM, Tagge CA, Zhang XL, Velisek L, Sullivan JA, et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci Transl Med 2012, 4: 134ra60. PubMed PMC
Cole JH, Jolly A, de Simoni S, Bourke N, Patel MC, Scott G, et al. Spatial patterns of progressive brain volume loss after moderate-severe traumatic brain injury. Brain 2018, 141: 822–836. PubMed PMC
Johnson VE, Stewart W, Smith DH. Widespread τ and amyloid-β pathology many years after a single traumatic brain injury in humans. Brain Pathol 2012, 22: 142–149. PubMed PMC
McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013, 136: 43–64. PubMed PMC
Van Essen DC. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997, 385: 313–318. PubMed
Sebenius I, Seidlitz J, Warrier V, Bethlehem RAI, Alexander-Bloch A, Mallard TT, et al. Robust estimation of cortical similarity networks from brain MRI. Nat Neurosci 2023, 26: 1461–1471. PubMed PMC
Seidlitz J, Váša F, Shinn M, Romero-Garcia R, Whitaker KJ, Vértes PE, et al. Morphometric similarity networks detect microscale cortical organization and predict inter-individual cognitive variation. Neuron 2018, 97: 231-247.e7. PubMed PMC
Auzias G, Viellard M, Takerkart S, Villeneuve N, Poinso F, Fonséca DD, et al. Atypical sulcal anatomy in young children with autism spectrum disorder. Neuroimage Clin 2014, 4: 593–603. PubMed PMC
Levitt JG, Blanton RE, Smalley S, Thompson PM, Guthrie D, McCracken JT, et al. Cortical sulcal maps in autism. Cereb Cortex 2003, 13: 728–735. PubMed
Coyle TR, Kochunov P, Patel RD, Nery FG, Lancaster JL, Mangin JF, et al. Cortical sulci and bipolar disorder. Neuroreport 2006, 17: 1739–1742. PubMed
Cachia A, Paillère-Martinot ML, Galinowski A, Januel D, de Beaurepaire R, Bellivier F, et al. Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations. Neuroimage 2008, 39: 927–935. PubMed
Im K, Lee JM, Seo SW, Hyung Kim S, Kim SI, Na DL. Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer’s disease. Neuroimage 2008, 43: 103–113. PubMed
Wagstyl K, Lerch JP (2018) Cortical thickness, Brain Morphometry. Humana Press, New York, pp 35–49.
Marzi C, Giannelli M, Tessa C, Mascalchi M, Diciotti S. Toward a more reliable characterization of fractal properties of the cerebral cortex of healthy subjects during the lifespan. Sci Rep 2020, 10: 16957. PubMed PMC
Madan CR, Kensinger EA. Cortical complexity as a measure of age-related brain atrophy. Neuroimage 2016, 134: 617–629. PubMed PMC
Li W, Yang C, Shi F, Wu S, Wang Q, Nie Y, et al. Construction of individual morphological brain networks with multiple morphometric features. Front Neuroanat 2017, 11: 34. PubMed PMC
Yu K, Wang X, Li Q, Zhang X, Li X, Li S. Individual morphological brain network construction based on multivariate euclidean distances between brain regions. Front Hum Neurosci 2018, 12: 204. PubMed PMC