Abstract
Postnatal development of cerebral cortex is associated with a variety of neuronal processes and is thus critical to development of brain function and cognition. Longitudinal changes of cortical morphology and topology, such as postnatal cortical thinning and flattening have been widely studied. However, thorough and systematic investigation of such cortical change, including how to quantify it from multiple spatial directions and how to relate it to surface topology, is rarely found. In this work, based on a longitudinal macaque neuroimaging dataset, we quantified local changes in gyral white matter's surface area and sulcal depth during early development. We also investigated how these two metrics are coupled and how this coupling is linked to cortical surface topology, underlying white matter, and positions of functional areas. Semi-parametric generalized additive models were adopted to quantify the longitudinal changes of surface area (A) and sulcal depth (D), and the coupling patterns between them. This resulted in four classes of regions, according to how they change compared with global change throughout early development: slower surface area change and slower sulcal depth change (slowA_slowD), slower surface area change and faster sulcal depth change (slowA_fastD), faster surface area change and slower sulcal depth change (fastA_slowD), and faster surface area change and faster sulcal depth change (fastA_fastD). We found that cortex-related metrics, including folding pattern and cortical thickness, vary along slowA_fastD–fastA_slowD axis, and structural connection-related metrics vary along fastA_fastD–slowA_slowD axis, with which brain functional sites align better. It is also found that cortical landmarks, including sulcal pits and gyral hinges, spatially reside on the borders of the four patterns. These findings shed new lights on the relationship between cortex development, surface topology, axonal wiring pattern and brain functions.
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Availability of data and material
The UNC-Wisconsin Rhesus Macaque Neurodevelopment Database (Young et al. 2017) is available as a publicly available dataset.
Code availability
All models and code generated or used on this study are available from the corresponding author by request. (tuozhang@nwpu.edu.cn).
References
Aleman-Gomez Y, Janssen J, Schnack H, Balaban E, Pina-Camacho L, Alfaro-Almagro F, Castro-Fornieles J, Otero S, Baeza I, Moreno D, Bargallo N, Parellada M, Arango C, Desco M (2013) The human cerebral cortex flattens during adolescence. J Neurosci 33(38):15004–15010. https://doi.org/10.1523/JNEUROSCI.1459-13.2013
Amlien IK, Fjell AM, Tamnes CK, Grydeland H, Krogsrud SK, Chaplin TA, Rosa MGP, Walhovd KB (2016) Organizing principles of human cortical development—thickness and area from 4 to 30 years: insights from comparative primate neuroanatomy. Cereb Cortex 26:257–267. https://doi.org/10.1093/cercor/bhu214
Andersson JL, Skare S (2010) Image distortion and its correction in diffusion MRI. Diffus MRI Theory Methods Appl. https://doi.org/10.1093/med/9780195369779.003.0017
Andersson JL, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078. https://doi.org/10.1016/j.neuroimage.2015.10.019
Aubert-Broche B, Fonov VS, García-Lorenzo D, Mouiha A, Guizard N, Coupé P, Eskildsen SF, Collins DL (2013) A new method for structural volume analysis of longitudinal brain MRI data and its application in studying the growth trajectories of anatomical brain structures in childhood. Neuroimage 82:393–402. https://doi.org/10.1016/j.neuroimage.2013.05.065
Bakken TE, Miller JA, Ding S-L, Sunkin SM, Smith KA, Ng L, Szafer A, Dalley RA, Royall JJ, Lemon T, Shapouri S, Aiona K, Arnold J, Bennett JL, Bertagnolli D, Bickley K, Boe A, Brouner K, Butler S, Byrnes E, Caldejon S, Carey A, Cate S, Chapin M, Chen J, Dee N, Desta T, Dolbeare TA, Dotson N, Ebbert A, Fulfs E, Gee G, Gilbert TL, Goldy J, Gourley L, Gregor B, Gu G, Hall J, Haradon Z, Haynor DR, Hejazinia N, Hoerder-Suabedissen A, Howard R, Jochim J, Kinnunen M, Kriedberg A, Kuan CL, Lau C, Lee C-K, Lee F, Luong L, Mastan N, May R, Melchor J, Mosqueda N, Mott E, Ngo K, Nyhus J, Oldre A, Olson E, Parente J, Parker PD, Parry S, Pendergraft J, Potekhina L, Reding M, Riley ZL, Roberts T, Rogers B, Roll K, Rosen D, Sandman D, Sarreal M, Shapovalova N, Shi S, Sjoquist N, Sodt AJ, Townsend R, Velasquez L, Wagley U, Wakeman WB, White C, Bennett C, Wu J, Young R, Youngstrom BL, Wohnoutka P, Gibbs RA, Rogers J, Hohmann JG, Hawrylycz MJ, Hevner RF, Molnár Z, Phillips JW, Dang C, Jones AR, Amaral DG, Bernard A, Lein ES (2016) A comprehensive transcriptional map of primate brain development. Nature 535:367–375. https://doi.org/10.1038/nature18637
Bakker R, Wachtler T, Diesmann M (2012) CoCoMac 2.0 and the future of tract-tracing databases. Front Neuroinform 6:30. https://doi.org/10.3389/fninf.2012.00030
Ball G, Seal ML (2019) Individual variation in longitudinal postnatal development of the primate brain. Brain Struct Funct 224(3):1185–1201. https://doi.org/10.1101/396887
Batalle D, Edwards AD, O’Muircheartaigh J (2018) Annual research review: not just a small adult brain: understanding later neurodevelopment through imaging the neonatal brain. J Child Psychol Psychiatry 59(4):350–371. https://doi.org/10.1111/jcpp.12838
Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50(5):1077–1088. https://doi.org/10.1002/mrm.10609
Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34(1):144–155. https://doi.org/10.1016/j.neuroimage.2006.09.018
Benkarim OM, Sanroma G, Zimmer VA, Muñoz-Moreno E, Hahner N, Eixarch E, Camara O, Ballester M, Piella G (2017) Toward the automatic quantification of in utero brain development in 3D structural MRI: a review. Hum Brain Mapp 38(5):2772–2787. https://doi.org/10.1002/hbm.23536
Blakemore SJ (2012) Imaging brain development: the adolescent brain. Neuroimage 61:397–406. https://doi.org/10.1016/j.neuroimage.2011.11.080
Bourgeois JP, Rakic P (1993) Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13(7):2801–2820. https://doi.org/10.1523/JNEUROSCI.13-07-02801.1993
Bourgeois JP, Goldman-Rakic PS, Rakic P (1994) Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4(1):78–96. https://doi.org/10.1093/cercor/4.1.78
Breier A, Buchanan RW, Elkashef A, Munson RC, Kirkpatrick B, Gellad F (1992) Brain morphology and schizophrenia: a magnetic resonance imaging study of limbic, prefrontal cortex, and caudate structures. Arch Gen Psychiatry 49(12):921. https://doi.org/10.1111/j.1600-0447.1992.tb03306.x
Brody BA, Kinney HC, Kloman AS, Gilles FH (1987) Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301. https://doi.org/10.1097/00005072-198805000-00003
Brown TT, Kuperman JM, Chung Y, Erhart M, McCabe C, Hagler DJ Jr, Venkatraman VK, Akshoomoff N, Amaral DG, Bloss CS, Casey BJ, Chang L, Ernst TM, Frazier JA, Gruen JR, Kaufmann WE, Kenet T, Kennedy DN, Murray SS, Sowell ER, Jernigan TL, Dale AM (2012) Neuroanatomical assessment of biological maturity. Curr Biol 22:1693–1698. https://doi.org/10.1016/j.cub.2012.07.002
Budde MD, Annese J (2013) Quantification of anisotropy and fiber orientation in human brain histological sections. Front Integr Neurosci 7:3. https://doi.org/10.3389/fnint.2013.00003
Chen H, Zhang T, Guo L, Li K, Yu X, Li L, Hu X, Han J, Hu X, Liu T (2013) Coevolution of gyral folding and structural connection patterns in primate brains. Cereb Cortex 23:1208–1217. https://doi.org/10.1093/cercor/bhs113
Chen H, Li Y, Ge F, Li G, Shen D, Liu T (2017) Gyral net: a new representation of cortical folding organization. Med Image Anal 42:14–25. https://doi.org/10.1016/j.media.2017.07.001
Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol off J Am Neurol Assoc Child Neurol Soc 1(1):86–93. https://doi.org/10.1002/ana.410010109
Chiapponi C, Piras F, Fagioli S, Piras F, Caltagirone C, Spalletta G (2013) Age-related brain trajectories in schizophrenia: a systematic review of structural MRI studies. Psychiatry Res Neuroimaging 214(2):83–93. https://doi.org/10.1016/j.pscychresns.2013.05.003
Choe MS, Ortiz-Mantilla S, Makris N, Gregas M, Bacic J, Haehn D, Kennedy D, Pienaar R, Caviness VS, Benasich AA, Grant PE (2013) Regional infant brain development: an MRI-based morphometric analysis in 3 to 13 month olds. Cereb Cortex 23(9):2100–2117. https://doi.org/10.1093/cercor/bhs197
Clouchoux C, Kudelski D, Gholipour A, Warfield SK, Viseur S, Bouyssi-Kobar M, Mari J, Evans AC, Plessis AJ, Limperopoulos C (2012) Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Struct Funct 217(1):127–139. https://doi.org/10.1007/s00429-011-0325-x
Cordero ME, D’Acuña E, Benveniste S, Prado R, Nuñez JA, Colombo M (1993) Dendritic development in neocortex of infants with early postnatal life undernutrition. Pediatr Neurol 9(6):457–464. https://doi.org/10.1016/0887-8994(93)90025-8
Courchesne E, Carper R, Akshoomoff N (2003) Evidence of brain overgrowth in the first year of life in autism. JAMA 290(3):337–344. https://doi.org/10.1001/jama.290.3.337
Counsell SJ, Maalouf EF, Fletcher AM, Duggan P, Battin M, Lewis HJ, Herlihy AH, Edwards AD, Bydder GM, Rutherford MA (2002) MR imaging assessment of myelination in the very preterm brain. Am J Neuroradiol 23(5):872–881. https://doi.org/10.1016/S1076-6332(03)80421-X
Dean DC III, O’Muircheartaigh J, Dirks H, Waskiewicz N, Lehman K, Walker L, Han M, Deoni SC (2014) Modeling healthy male white matter and myelin development: 3 through 60 months of age. Neuroimage 84:742–752. https://doi.org/10.1016/j.neuroimage.2013.09.058
Douaud G, Behrens TE, Poupon C, Cointepas Y, Jbabdi S, Gaura V, Golestani N, Krystkowiak P, Verny C, Damier P, Bachoud-Lévi A, Hantraye P, Remy P (2009) In vivo evidence for the selective subcortical degeneration in Huntington’s disease. Neuroimage 46(4):958–966. https://doi.org/10.1016/j.neuroimage.2009.03.044
Duan D, Xia S, Rekik I, Meng Y, Wu Z, Wang L, Lin W, Gilmore J, Shen D, Li G (2019) Exploring folding patterns of infant cerebral cortex based on multi-view curvature features: methods and applications. Neuroimage 185:575–592. https://doi.org/10.1016/j.neuroimage.2018.08.041
Dubois J, Benders M, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Borradori-Tolsa C, Mangin JF, Hüppi PS (2008) Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex 18(6):1444–1454. https://doi.org/10.1093/cercor/bhm180
Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Hüppi PS, Hertz-Pannier L (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71. https://doi.org/10.1016/j.neuroscience.2013.12.044
Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis: II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9(2):195–207. https://doi.org/10.1006/nimg.1998.0396
Fischl B, Wald LL (2007) Phase maps reveal cortical architecture. Proc Natl Acad Sci 104(28):11513–11514. https://doi.org/10.1073/pnas.0704515104
Fischl B (2012) FreeSurfer. Neuroimage 62(2):774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021
Gao W, Lin W, Chen Y, Gerig G, Smith JK, Jewells V, Gilmore JH (2009) Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. Am J Neuroradiol 30(2):290–296. https://doi.org/10.1016/j.neuroimage.2009.03.044
Ge F, Li X, Razavi MJ, Chen H, Zhang T, Zhang S, Guo L, Hu X, Wang X, Liu T (2018) Denser growing fiber connections induce 3-hinge gyral folding. Cereb Cortex 28(3):1064–1075. https://doi.org/10.1093/cercor/bhx227
Geng X, Gouttard S, Sharma A, Gu H, Styner M, Lin W, Gerig G, Gilmore JH (2012) Quantitative tract-based white matter development from birth to age 2 years. Neuroimage 61(3):542–557. https://doi.org/10.1016/j.neuroimage.2012.03.057
Ghashghaei HT, Lai C, Anton ES (2007) Neuronal migration in the adult brain: are we there yet? Nat Rev Neurosci 8(2):141. https://doi.org/10.1038/nrn2074
Gibson KR (1991) Myelination and behavioral development: a comparative perspective on questions of neoteny, altriciality and intelligence. In: Gibson KR, Petersen AC (eds) Brain maturation and cognitive development: comparative and cross-cultural perspectives. Aldine de Gruyter, New York, pp 29–63
Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2(10):861–863. https://doi.org/10.1038/13158
Gilmore JH, Shi F, Woolson SL, Knickmeyer RC, Short SJ, Lin W, Zhu H, Hamer RM, Styner M, Shen D (2012) Longitudinal development of cortical and subcortical gray matter from birth to 2 years. Cereb Cortex 22(11):2478–2485. https://doi.org/10.1093/cercor/bhr327
Glasser MF, Goyal MS, Preuss TM, Raichle ME, Van Essen DC (2014) Trends and properties of human cerebral cortex: correlations with cortical myelin content. Neuroimage 93(2):165–175. https://doi.org/10.1016/j.neuroimage.2013.03.060
Gulani V, Webb AG, Duncan ID, Lauterbur PC (2001) Apparent diffusion tensor measurements in myelin-deficient rat spinal cords. Magn Reson Med 45(2):191–195. https://doi.org/10.1002/1522-2594(200102)45:2%3c191::aid-mrm1025%3e3.0.co;2-9
Hayakawa K, Konishi Y, Kuriyama M, Konishi K, Matsuda T (1991) Normal brain maturation in MRI. Eur J Radiol 12:208–215. https://doi.org/10.1016/0720-048X(91)90074-6
Hazlett HC, Gu H, Munsell BC, Kim SH, Styner M, Wolff JJ, Elison JT, Swanson MR, Zhu H, Botteron KN, Collins DL, Constantino JN, Dager SR, Estes AM, Evans AC, Fonov VS, Gerig G, Kostopoulos P, McKinstry RC, Pandey J, Paterson S, Pruett JR, Schultz RT, Shaw DW, Zwaigenbaum L, Piven J, Network IBIS (2017) Early brain development in infants at high risk for autism spectrum disorder. Nature 542(7641):348–351. https://doi.org/10.1038/nature21369
He Y, Chen ZJ, Evans AC (2007) Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 10:2407–2419. https://doi.org/10.1093/cercor/bhl149
Heuvel M, Mandl R, Kahn RS, Pol H (2010) Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30(10):3127–3141. https://doi.org/10.1002/hbm.20737
Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2(3):e22. https://doi.org/10.1371/journal.pcbi.0020022
Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, Coalson T, Van Essen D (2010) A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants. J Neurosci 30(6):2268–2276. https://doi.org/10.1523/JNEUROSCI.4682-09.2010
Holland D, Chang L, Ernst TM, Curran M, Buchthal SD, Alicata D, Skranes J, Johansen H, Hernandez A, Yamakawa R, Kuperman JM, Dale AM (2014) Structural growth trajectories and rates of change in the first 3 months of infant brain development. JAMA Neurol 71(10):1266–1274. https://doi.org/10.1001/jamaneurol.2014.1638
Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci 106(6):2035–2040. https://doi.org/10.1016/10.1073/pnas.0811168106
Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387(2):167–178. https://doi.org/10.1002/(SICI)1096-9861(19971020)387:2%3c167::AID-CNE1%3e3.0.C
Im K, Jo HJ, Mangin JF, Evans AC, Kim SI, Lee JM (2010) Spatial distribution of deep sulcal landmarks and hemispherical asymmetry on the cortical surface. Cereb Cortex 20(3):602–611. https://doi.org/10.1093/cercor/bhp127
Im K, Yu YC, Yang JJ, Lee KH, Sun IK, Grant PE, Lee JM (2011) The relationship between the presence of sulcal pits and intelligence in human brains. Neuroimage 55(4):1490–1496. https://doi.org/10.1016/j.neuroimage.2010.12.080
Im K, Grant PE (2019) Sulcal pits and patterns in developing human brains. Neuroimage 185:881–890. https://doi.org/10.1016/j.neuroimage.2018.03.057
Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17(2):825–841. https://doi.org/10.1006/nimg.2002.1132
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015
Jernigan TL, Baaré WF, Stiles J, Madsen KS (2011) Postnatal brain development: structural imaging of dynamic neurodevelopmental processes. Prog Brain Res 189:77–92. https://doi.org/10.1016/B978-0-444-53884-0.00019-1
Jouvent E, Reyes S, Mangin JF, Roca P, Perrot M, Thyreau B, Hervé D, Dich-gans M, Chabriat H (2011) Apathy is related to cortex morphology in CADASIL A sulcal-based morphometry study. Neurology 76:1472–1477. https://doi.org/10.1212/WNL.0b013e31821810a4
Keightley ML, Winocur G, Graham SJ, Mayberg HS, Hevenor SJ, Grady CL (2003) An fmri study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli. Neuropsychologia 41(5):585–596. https://doi.org/10.1016/S0028-3932(02)00199-9
Kinney HC, Brody BA, Kloman AS, Gilles FH (1988) Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47:217–234. https://doi.org/10.1097/00005072-198805000-00003
Klingberg T, Vaidya CJ, Gabrieli JD, Moseley ME, Hedehus M (1999) Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. NeuroReport 10:2817–2821. https://doi.org/10.1097/00001756-199909090-00022
Knickmeyer RC, Gouttard S, Kang C, Evans D, Wilber K, Smith JK, Hamer RM, Lin W, Gerig G, Gilmore JH (2008) A structural MRI study of human brain development from birth to 2 years. J Neurosci 28(47):12176–12182. https://doi.org/10.1523/JNEUROSCI.3479-08.2008
Kochunov P, Rogers W, Mangin JF, Lancaster J (2012) A library of cortical morphology analysis tools to study development, aging and genetics of cerebral cortex. Neuroinformatics 10:81–96. https://doi.org/10.1007/s12021-011-9127-9
Kolasinski J, Takahashi E, Stevens AA, Benner T, Fischl B, Zöllei L, Grant PE (2013) Radial and tangential neuronal migration pathways in the human fetal brain: anatomically distinct patterns of diffusion MRI coherence. Neuroimage 79:412–422. https://doi.org/10.1016/j.neuroimage.2013.04.125
Kostović I, Jovanov-Milošević N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med 11(6):415–422. https://doi.org/10.1016/j.siny.2006.07.001
Kötter R, Wanke E (2005) Mapping brains without coordinates. Philos Trans R Soc B 360(1456):751–766. https://doi.org/10.1098/rstb.2005.1625
Lampi KM, Lehtonen L, Tran PL, Suominen A, Lehti V, Banerjee PN, MSocSC MG, Brown AS, Sourander A (2012) Risk of autism spectrum disorders in low birth weight and small for gestational age infants. J Pediatr 161(5):830–836. https://doi.org/10.1016/j.jpeds.2012.04.058
Le Guen Y, Auzias G, Leroy F, Noulhiane M, Dehaene-Lambertz G, Duchesnay E, Mangin J, Coulon O, Frouin V (2018) Genetic influence on the sulcal pits: on the origin of the first cortical folds. Cereb Cortex 28(6):1922–1933. https://doi.org/10.1093/cercor/bhx098
Lebel C, Beaulieu C (2011) Longitudinal development of human brain wiring continues from childhood into adulthood. J Neurosci 31(30):10937–10947. https://doi.org/10.1523/jneurosci.5302-10.2011
Li K, Guo L, Li G, Nie J, Faraco C, Cui G, Zhao Q, Miller LS, Liu T (2010) Gyral folding pattern analysis via surface profiling. Neuroimage 52(4):1202–1214. https://doi.org/10.1016/j.neuroimage.2010.04.263
Li G, Nie J, Wang L, Shi F, Lin W, Gilmore JH, Shen D (2013) Mapping region-specific longitudinal cortical surface expansion from birth to 2 years of age. Cereb Cortex 23(11):2724–2733. https://doi.org/10.1093/cercor/bhs265
Li G, Wang L, Shi F, Lyall AE, Lin W, Gilmore JH, Shen D (2014a) Mapping longitudinal development of local cortical gyrification in infants from birth to 2 years of age. J Neurosci 34(12):4228–4238. https://doi.org/10.1523/JNEUROSCI.3976-13.2014
Li G, Nie J, Wang L, Shi F, Gilmore JH, Lin W, Shen D (2014b) Measuring the dynamic longitudinal cortex development in infants by reconstruction of temporally consistent cortical surfaces. Neuroimage 90:266–279. https://doi.org/10.1016/j.neuroimage.2013.12.038
Li G, Liu T, Ni D, Lin W, Gilmore JH, Shen D (2015) Spatiotemporal patterns of cortical fiber density in developing infants, and their relationship with cortical thickness. Hum Brain Mapp 36(12):5183–5195. https://doi.org/10.1002/hbm.23003
Liu T, Wen W, Zhu W, Kochan NA, Trollor JN, Reppermund S, Jin JS, Luo S, Brodaty H, Sachdev PS (2011) The relationship between cortical sulcal variability and cognitive performance in the elderly. Neuroimage 56:865–873. https://doi.org/10.1016/j.neuroimage.2011.03.015
Li X, Chen H, Zhang T, Yu X, Jiang X, Li K, Li L, Razavi MJ, Wang X, Hu X, Han J, Guo L, Hu X, Liu T (2017) Commonly preserved and species-specific gyral folding patterns across primate brains. Brain Struct Funct 222(5):2127–2141. https://doi.org/10.1007/s00429-016-1329-3
Lohmann G, Von Cramon DY, Colchester AC (2008) Deep sulcal landmarks provide an organizing framework for human cortical folding. Cereb Cortex 18(6):1415–1420. https://doi.org/10.1093/cercor/bhm174
McGraw P, Liang L, Provenzale JM (2002) Evaluation of normal age-related changes in anisotropy during infancy and childhood as shown by diffusion tensor imaging. Am J Roentgenol 179(6):1515–1522. https://doi.org/10.2214/ajr.179.6.1791515
Malkova L, Heuer E, Saunders RC (2006) Longitudinal magnetic resonance imaging study of rhesus monkey brain development. Eur J Neurosci 24(11):3204–3212. https://doi.org/10.1111/j.1460-9568.2006.05175.x
Mantini D, Gerits A, Nelissen K, Durand JB, Joly O, Simone L, Sawamura H, Wardak C, Orban GA, Buckner RL, Vanduffel W (2011) Default mode of brain function in monkeys. J Neurosci 31(36):12954–12962. https://doi.org/10.1523/JNEUROSCI.2318-11.2011
Margulies DS, Ghosh SS, Goulas A, Falkiewicz M, Huntenburg JM, Langs G, Bezgin G, Eickhoff SB, Castellanos FX, Petrides M, Jefferies E, Smallwood J (2016) Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci 113(44):12574–12579. https://doi.org/10.1073/pnas.1608282113
Meng Y, Li G, Lin W, Gilmore JH, Shen D (2014) Spatial distribution and longitudinal development of deep cortical sulcal landmarks in infants. Neuroimage 100:206–218. https://doi.org/10.1016/j.neuroimage.2014.06.004
Mills KL, Goddings AL, Herting MM, Meuwese R, Blakemore SJ, Crone EA, Dahl RE, Güroğlu B, Raznahan A, Sowell ER, Tamnes CK (2016) Structural brain development between childhood and adulthood: convergence across four longitudinal samples. Neuroimage 141:273–281. https://doi.org/10.1016/j.neuroimage.2016.07.044
Miller JH, McKinstry RC, Philip JV, Mukherjee P, Neil JJ (2003) Diffusion-tensor MR imaging of normal brain maturation: a guide to structural development and myelination. Am J Roentgenol 180(3):851–859. https://doi.org/10.2214/ajr.180.3.1800851
Morsing E, Åsard M, Ley D, Stjernqvist K, Maršál K (2011) Cognitive function after intrauterine growth restriction and very preterm birth. Pediatrics 127(4):874–882. https://doi.org/10.1542/peds.2010-1821
Mukherjee P, Miller JH, Shimony JS, Philip JV, Nehra D, Snyder AZ, Conturo TE, Neil JJ, McKinstry RC (2002) Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. Am J Neuroradiol 23(9):1445–1456. https://doi.org/10.1097/00002093-200210000-00011
Natu VS, Arcaro MJ, Barnett MA, Jesse G, Margaret L, Kalanit GS, Weiner KS (2021) Sulcal depth in the medial ventral temporal cortex predicts the location of a place-selective region in macaques, children, and adults. Cereb Cortex 31:48–61. https://doi.org/10.1093/cercor/bhaa203
Nie J, Guo L, Li K, Wang Y, Chen G, Li L, Chen H, Deng F, Jiang X, Zhang T, Huang L, Faraco C, Zhang D, Guo C, Yap PT, Hu X, Li G, Lv J, Yuan Y, Zhu D, Han J, Sabatinelli D, Zhao Q, Miller LS, Xu B, Shen P, Platt S, Shen D, Hu X, Liu T (2012) Axonal fiber terminations concentrate on gyri. Cereb Cortex 22:2831–2839. https://doi.org/10.1093/cercor/bhr361
O’Rourke NA, Dailey ME, Smith SJ, McConnell SK (1992) Diverse migratory pathways in the developing cerebral cortex. Science 258:299–302
Park HJ, Friston K (2013) Structural and functional brain networks: from connections to cognition. Science 342(6158):579. https://doi.org/10.1126/science.1238411
Paxinos G, Huang XF, Toga AW (2000) The rhesus monkey brain in stereotaxic coordinates. Rhesus Monkey Brain in Stereotaxic Coordinates 1(2):6. https://doi.org/10.1016/0165-0270(80)90021-7
Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232(4747):232–235. https://doi.org/10.1126/science.3952506
Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145(1):61–83. https://doi.org/10.1002/cne.901450105
Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176. https://doi.org/10.1126/science.3291116
Razavi MJ, Zhang T, Liu T, Wang X (2015a) Cortical folding pattern and its consistency induced by biological growth. Sci Rep 5:14477. https://doi.org/10.1038/srep14477
Razavi MJ, Zhang T, Li X, Liu T, Wang X (2015b) Role of mechanical factors in cortical folding development. Phys Rev E Stat Nonlin Soft Matter Phys 92(3):032701. https://doi.org/10.1103/PhysRevE.92.032701
Raznahan A, Shaw PW, Lerch JP, Clasen LS, Greenstein D, Berman R, Pipitone J, Chakravarty MM, Giedd JN (2014) Longitudinal four-dimensional mapping of subcortical anatomy in human development. Proc Natl Acad Sci 111(4):1592–1597. https://doi.org/10.1073/pnas.1316911111
Reardon PK, Seidlitz J, Vandekar S, Liu S, Patel R, Park MTM, Alexander-Bloch A, Clasen LS, Blumenthal JD, Lalonde FM, Giedd JN, Gur RC, Gur RE, Lerch JP, Chakravarty MM, Scatterthwaite TD, Shinohara RT, Raznahan A (2018) Normative brain size variation and brain shape diversity in humans. Science 360(6394):1222–1227. https://doi.org/10.1126/science.aar2578
Reid AT, Lewis J, Bezgin G, Khundrakpam B, Evans AC (2016) A cross-modal, cross-species comparison of connectivity measures in the primate brain. Neuroimage 125:311–331. https://doi.org/10.1016/j.neuroimage.2015.10.057
Reillo I, de Juan RC, Garcia-Cabezas MA, Borrell V (2011) A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 21:1674–1694. https://doi.org/10.1093/cercor/bhq238
Ronan L, Voets N, Rua C, Alexander-Bloch A, Hough M, Mackay C, Crow TJ, James A, Giedd JN, Fletcher PC (2013) Differential tangential expansion as a mechanism for cortical gyrification. Cereb Cortex 24:2219–2228. https://doi.org/10.1093/cercor/bht082
Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RS, Busa E, Morris JC, Dale AM, Fischl B (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14(7):721–730. https://doi.org/10.1093/cercor/bhh032
Salzer JL, Zalc B (2016) Myelination. Curr Biol 26(20):971–975. https://doi.org/10.1016/j.cub.2016.07.074
Schaer M, Cuadra MB, Tamarit L, Lazeyras F, Eliez S, Thiran JP (2008) A surface-based approach to quantify local cortical gyrification. IEEE Trans Med Imaging 27(2):161–170. https://doi.org/10.1109/TMI.2007.903576
Scott JA, Grayson D, Fletcher E, Lee A, Bauman MD, Schumann CM, Buonocore MH, Amaral DG (2016) Longitudinal analysis of the developing rhesus monkey brain using magnetic resonance imaging: birth to adulthood. Brain Struct Funct 221(5):2847–2871. https://doi.org/10.1007/s00429-015-1076-x
Semendeferi K, Teffer K, Buxhoeveden DP, Park MS, Bludau S, Amunts K, Travis K, Buckwalter J (2011) Spatial organization of neurons in the frontal pole sets humans apart from great apes. Cereb Cortex 21(7):1485–1497. https://doi.org/10.1093/cercor/bhq191
Shaw P, Lerch JP, Pruessner JC, Taylor KN, Giedd JN (2007) Cortical morphology in children and adolescents with different apolipoprotein e gene polymorphisms: an observational study. Lancet Neurol 6(6):494–500. https://doi.org/10.1016/S1474-4422(07)70106-0
Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL, Giedd JN, Wise SP (2008) Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28(14):3586–3594. https://doi.org/10.1523/jneurosci.5309-07.2008
Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1–35. https://doi.org/10.1016/0006-8993(73)90617-3
Sie LT, Van der Knaap MS, van Wezel-Meijler G, Valk J (1997) MRI assessment of myelination of motor and sensory pathways in the brain of preterm and term-born infants. Neuropediatrics 28(02):97–105. https://doi.org/10.1055/s-2007-973680
Song SK, Sun SW, Ramsbottom MJ, Chen C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17(3):1429–1436. https://doi.org/10.1006/nimg.2002.1267
Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW (2004) Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24(38):8223–8231. https://doi.org/10.1523/JNEUROSCI.1798-04.2004
Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17(3):143–155. https://doi.org/10.1002/hbm.10062
Smart I, Mcsherry GM (1986) Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes. J Anat 146:141–152. https://doi.org/10.1109/ETFA.1999.815391
Stasinopoulos DM, Rigby RA (2007) Generalized additive models for location scale and shape (GAMLSS) in R. J Stat Softw 23(7):1–46. https://doi.org/10.18637/jss.v023.i07
Striedter GF, Srinivasan S, Monuki ES (2015) Cortical folding: when, where, how, and why? Annu Rev Neurosci 38:291–307. https://doi.org/10.1146/annurev-neuro-071714-034128
Sun L, Zhang D, Lian C, Wang L, Wu Z, Shao W, Lin W, Shen D, Li G, UNC/UMN Baby Connectome Project Consortium (2019) Topological correction of infant white matter surfaces using anatomically constrained convolutional neural network. Neuroimage 198:114–124. https://doi.org/10.1016/j.neuroimage.2019.05.037
Takahashi E, Folkerth RD, Galaburda AM, Grant PE (2012) Emerging cerebral connectivity in the human fetal brain: an MR tractography study. Cereb Cortex 22(2):455–464. https://doi.org/10.1093/cercor/bhr126
Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534–548. https://doi.org/10.1093/cercor/bhp118
Tamnes CK, Herting MM, Goddings AL, Meuwese R, Blakemore SJ, Dahl RE, Guroglu B, Raznahan A, Sowell ER, Crone EA, Mills KL (2017) Development of the cerebral cortex across adolescence: a multisample study of inter-related longitudinal changes in cortical volume, surface area, and thickness. J Neurosci 37(12):3402–3412. https://doi.org/10.1523/JNEUROSCI.3302-16.2017
Toro R, Burnod Y (2005) A morphogenetic model for the development of cortical convolutions. Cereb Cortex 15:1900–1913. https://doi.org/10.1093/cercor/bhi068
Van der Knaap MS, Valk J, Bakker CJ, Schooneveld M, Faber JAJ, Willemse J, Gooskens RHJM (1991) Myelination as an expression of the functional maturity of the brain. Dev Med Child Neurol 33(10):849–857. https://doi.org/10.1111/j.1469-8749.1991.tb14793.x
Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313. https://doi.org/10.1038/385313a0
Van Essen DC (2002) Windows on the brain: the emerging role of atlases and databases in neuroscience. Curr Opin Neurobiol 12:574–579. https://doi.org/10.1016/s0959-4388(02)00361-6
Van Essen DC, Dierker DL (2007) Surface-based and probabilistic atlases of primate cerebral cortex. Neuron 56:209–225. https://doi.org/10.1016/j.neuron.2007.10.015
Vandekar SN, Shinohara RT, Raznahan A, Hopson RD, Roalf DR, Ruparel K, Gur RC, Gur RE, Satterthwaite TD (2016) Subject-level measurement of local cortical coupling. Neuroimage 133:88–97. https://doi.org/10.1016/j.neuroimage.2016.03.002
Wang F, Lian C, Xia J, Wu Z, Duan D, Wang L, Shen D, Li G (2018) Construction of spatiotemporal infant cortical surface atlas of rhesus macaque. In: 2018 IEEE 15th International symposium on biomedical imaging (ISBI 2018), pp 704–707. https://doi.org/10.1109/ISBI.2018.8363671
Wang L, Shi F, Li G, Gao Y, Lin W, Gilmore JH, Shen D (2014) Segmentation of neonatal brain MR images using patch-driven level sets. Neuroimage 84:141–158. https://doi.org/10.1016/j.neuroimage.2013.08.008
Wang L, Gao Y, Shi F, Li G, Gilmore JH, Lin W, Shen D (2015) LINKS: Learning-based multi-source IntegratioN frameworK for Segmentation of infant brain images. Neuroimage 108:160–172. https://doi.org/10.1007/978-3-319-13972-2_3
Welker KM, Patton A (2012) Assessment of normal myelination with magnetic resonance imaging. Semin Neurol 32(01):015–028. https://doi.org/10.1055/s-0032-1306382
Westlye LT, Walhovd KB, Dale AM, Bjørnerud A, Due-Tønnessen P, Engvig A, Grydeland H, Tamnes CK, Østby Y, Fjell AM (2010) Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cereb Cortex 20(9):2055–2068. https://doi.org/10.1093/cercor/bhp280
Wierenga L, Langen M, Ambrosino S, van Dijk S, Oranje B, Durston S (2014) Typical development of basal ganglia, hippocampus, amygdala and cerebellum from age 7 to 24. Neuroimage 96:67–72. https://doi.org/10.1016/j.neuroimage.2014.03.072
Xia J, Wang F, Wu Z, Wang L, Zhang C, Shen D, Li G (2020) Mapping hemispheric asymmetries of the macaque cerebral cortex during early brain development. Hum Brain Mapp 41(1):95–106. https://doi.org/10.1002/hbm.24789
Xu G, Knutsen AK, Dikranian K, Kroenke CD, Bayly PV, Taber LA (2010) Axons pull on the brain, but tension does not drive cortical folding. J Biomech Eng 132(7):071013. https://doi.org/10.1115/1.4001683
Yakovlev PI, Lecours AR (1967) The myelogenetic cycles of regional maturation of the brain. Regional development of the brain in early life, 3-70.
Yeh F, Wedeen VJ, Tseng WI (2010) Generalized q-sampling imaging. IEEE Trans Med Imaging 29:1626–1635. https://doi.org/10.1109/TMI.2010.2045126
Yeh F, Verstynen TD, Wang Y, Fernández-Miranda JC, Tseng WI (2013) Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE. https://doi.org/10.1371/journal.pone.0080713
Yeo BT, Sabuncu MR, Vercauteren T, Ayache N, Fischl B, Golland P (2009) Spherical demons: fast diffeomorphic landmark-free surface registration. IEEE Trans Med Imaging 29(3):650–668. https://doi.org/10.1109/TMI.2009.2030797
Young JT, Shi Y, Niethammer M, Grauer M, Coe CL, Lubach GR, Davis B, Budin F, Knickmeyer RC, Alexander AL, Styner MA (2017) The UNC-Wisconsin rhesus macaque neurodevelopment database: a structural MRI and DTI database of early postnatal development. Front Neurosci 11:29. https://doi.org/10.3389/fnins.2017.00029
Yun HJ, Im K, Yang J-J, Yoon U, Lee JM (2013) Automated sulcal depth measurement on cortical surface reflecting geometrical properties of sulci. PLoS ONE 8(2):e55977. https://doi.org/10.1109/TMI.2009.2030797
Zecevic N, Rakic P (1991) Synaptogenesis in monkey somatosensory cortex. Cereb Cortex 1(6):510–523. https://doi.org/10.1093/cercor/1.6.510
Zhang T, Chen H, Guo L, Li K, Li L, Zhang S, Shen D, Hu X, Liu T (2014) Characterization of U-shape streamline fibers: methods and applications. Med Image Anal 18:795–807. https://doi.org/10.1016/j.media.2014.04.005
Zhang T, Razavi MJ, Li X, Chen H, Liu T, Wang X (2016) Mechanism of consistent gyrus formation: an experimental and computational study. Sci Rep 6:37272. https://doi.org/10.1038/srep37272
Zhang T, Razavi MJ, Chen H, Li Y, Li X, Li L, Guo L, Hu X, Liu T, Wang X (2017) Mechanisms of circumferential gyral convolution in primate brains. J Comput Neurosci 42(3):217–229. https://doi.org/10.1007/s10827-017-0637-9
Zhang T, Chen H, Razavi MJ, Li Y, Ge F, Guo L, Wang X, Liu T (2018) Exploring 3-hinge gyral folding patterns among HCP Q3 868 human subjects. Hum Brain Mapp 39(10):4134–4149. https://doi.org/10.1002/hbm.24237
Zhang T, Huang Y, Zhao L, He Z, Jiang X, Guo L, Hu X, Liu T (2020a) Identifying cross-individual correspondences of 3-hinge gyri. Med Image Anal 63:101700. https://doi.org/10.1016/j.media.2020.101700
Zhang T, Li X, Jiang X, Ge F, Zhang S, Zhao L, Liu H, Huang Y, Wang X, Yang J, Guo L, Hu X, Liu T (2020b) Cortical 3-hinges could serve as hubs in cortico-cortical connective network. Brain Imaging Behav. https://doi.org/10.1007/s11682-019-00204-6
Zhong T, Zhao F, Pei Y, Ning Z, Liao L, Wu Z, Niu Y, Wang L, Shen D, Zhang Y, Li G (2021) DIKA-nets: domain-invariant knowledge-guided attention networks for brain skull stripping of early developing macaques. Neuroimage 227:117649. https://doi.org/10.1016/j.neuroimage.2020.117649
Zilles K, Armstrong E, Schleicher A, KreTchmann HJ (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol (berl) 179:173–179. https://doi.org/10.1007/BF00304699
Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36(5):275–284. https://doi.org/10.1016/j.tins.2013.01.006
Acknowledgements
T Zhang was supported by the National Natural Science Foundation of China (31971288, 31671005). L Guo was supported by the National Natural Science Foundation of China (61936007). X Jiang was supported by the National Natural Science Foundation of China (61976045) and Sichuan Science and Technology Program (2021YJ0247). S Zhang was supported by National Natural Science Foundation of China (62006194), The Fundamental Research Funds for the Central Universities (3102019QD005) and High-level researcher start-up projects (06100-20GH020161).
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XL: conceptualization, methodology, software, and writing—original draft. SZ: investigation and software. XJ: methodology. SZ: visualization. JH: supervision. LG: supervision and funding acquisition. TZ: data curation, conceptualization, supervision, methodology, writing—review and editing, and funding acquisition.
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Li, X., Zhang, S., Jiang, X. et al. Cortical development coupling between surface area and sulcal depth on macaque brains. Brain Struct Funct 227, 1013–1029 (2022). https://doi.org/10.1007/s00429-021-02444-z
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DOI: https://doi.org/10.1007/s00429-021-02444-z