Brain Structure and Function

, Volume 222, Issue 5, pp 2127–2141 | Cite as

Commonly preserved and species-specific gyral folding patterns across primate brains

  • Xiao Li
  • Hanbo Chen
  • Tuo Zhang
  • Xiang Yu
  • Xi Jiang
  • Kaiming Li
  • Longchuan Li
  • Mir Jalil Razavi
  • Xianqiao Wang
  • Xintao Hu
  • Junwei Han
  • Lei Guo
  • Xiaoping Hu
  • Tianming Liu
Original Article

Abstract

Cortical folding pattern analysis is very important to understand brain organization and development. Since previous studies mostly focus on human brain cortex, the regularity and variability of cortical folding patterns across primate brains (macaques, chimpanzees and human) remain largely unknown. This paper presents a novel computational framework to identify common or unique gyral folding patterns in macaque, chimpanzee and human brains using magnetic resonance imaging (MRI) data. We quantitatively characterize gyral folding patterns via hinge numbers with cortical surfaces constructed from MRI data, and identify 6 common three-hinge gyral folds that exhibit consistent anatomical locations across these three species as well as 2 unique three hinges in macaque, 6 ones in chimpanzee and 14 ones in human. A novel morphology descriptor is then applied to classify three-hinge gyral folds, and the increasing complexity is identified among the species analyzed. This study may provide novel insights into the regularity and variability of the cerebral cortex from developmental perspective and may potentially facilitate novel neuroimage analyses such as cortical parcellation with correspondences across species in the future.

Keywords

Cortical folding Primate brains Magnetic resonance imaging Three hinges 

Notes

Acknowledgements

T Liu was supported by the NIH Career Award EB006878 (2007–2012), NIH R01 HL087923-03S2 (2010–2012), NIH R01 DA033393 (2012–2017), NIH R01 AG-042599 (2013–2018), NSF CAREER Award IIS-1149260 (2012-2017), NSF CBET-1302089 (2013–2016), NSF BCS-1439051 (2014–2017) and NSF DBI-1564736 (2016–2019). T Zhang was supported by NSFC 31500798, the fundamental research funds for the central universities.

References

  1. Barkovich AJ (2010) Current concepts of polymicrogyria. Neuroradiology 52:479–487CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barton RA (2006) Primate brain evolution: integrating comparative, neurophysiological, and ethological data. Evol Anthropol Issues News Rev 15:224–236CrossRefGoogle Scholar
  3. Bayly PV, Taber LA, Kroenke CD (2014) Mechanical forces in cerebral cortical folding: a review of measurements and models. J Mech Behav Biomed Mater 29:568–581CrossRefPubMedGoogle Scholar
  4. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198CrossRefPubMedGoogle Scholar
  5. Buxhoeveden DP, Switala AE, Roy E, Litaker M, Casanova MF (2001) Morphological differences between minicolumns in human and nonhuman primate cortex. Am J Phys Anthropol 115:361–371CrossRefPubMedGoogle Scholar
  6. 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 23:1208–1217CrossRefPubMedGoogle Scholar
  7. Chen H, Yu X, Jiang X, Li K, Li L, Hu X, Han J, Guo L, Hu X, Liu T (2014) Evolutionarily-preserved consistent gyral folding patterns across primate brains. In: ISBI. IEEE. p 1218–1221Google Scholar
  8. Dubois J, Benders M, Borradori-Tolsa C, Cachia A, Lazeyras F, Leuchter HV, Sizonenko SV, Warfield SK, Mangin JF, Hüppi PS (2008) Primary cortical folding in the human newborn: an early marker of later functional development. Brain A J Neurol 131:2028–2041CrossRefGoogle Scholar
  9. Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347CrossRefPubMedGoogle Scholar
  10. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis: II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207CrossRefPubMedGoogle Scholar
  11. Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BTT, Mohlberg H, Amunts K, Zilles K (2008) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18:1973–1980CrossRefPubMedGoogle Scholar
  12. Giedd JN, Rapoport JL (2010) Structural MRI of pediatric brain development: What have we learned and where are we going? Neuron 67:728–734CrossRefPubMedPubMedCentralGoogle Scholar
  13. Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253–258CrossRefPubMedGoogle Scholar
  14. Hardan AY, Jou RJ, Keshavan MS, Varma R, Minshew NJ (2004) Increased frontal cortical folding in autism: a preliminary MRI study. Psychiatry Res 131:263–268CrossRefPubMedGoogle Scholar
  15. Harris JM, Whalley H, Yates S, Miller P, Johnstone EC, Lawrie SM (2004) Abnormal cortical folding in high-risk individuals: a predictor of the development of schizophrenia? Biol Psychiatry 56:182–189CrossRefPubMedGoogle Scholar
  16. Heimann T, Meinzer H-P (2009) Statistical shape models for 3D medical image segmentation: a review. Med Image Anal 13:543–563CrossRefPubMedGoogle Scholar
  17. Hilgetag CC, Barbas H (2005) Developmental mechanics of the primate cerebral cortex. Anat Embryol (Berl) 210:411–417CrossRefGoogle Scholar
  18. Hilgetag CC, Barbas H (2006) Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex. PLoS Comput Biol 2:e22CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 USA 106:2035–2040CrossRefPubMedPubMedCentralGoogle Scholar
  20. Honey CJ, Thivierge J-P, Sporns O (2010) Can structure predict function in the human brain? Neuroimage 52:766–776CrossRefPubMedGoogle Scholar
  21. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156CrossRefPubMedGoogle Scholar
  22. 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 17:825–841CrossRefPubMedGoogle Scholar
  23. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790CrossRefPubMedGoogle Scholar
  24. King R, Brown B, Hwang MSH, Jeon T, George AT (2010) Fractal dimension analysis of the cortical ribbon in mild Alzheimer’s disease. Neuroimage 53:471–479CrossRefPubMedPubMedCentralGoogle Scholar
  25. Landrieu P, Husson B, Pariente D, Lacroix C (1998) MRI-neuropathological correlations in type 1 lissencephaly. Neuroradiology 40:173–176CrossRefPubMedGoogle Scholar
  26. 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 52:1202–1214CrossRefPubMedPubMedCentralGoogle Scholar
  27. Li G, Wang L, Shi F, Lyall AE, Lin W, Gilmore JH, Shen D (2014) Mapping longitudinal development of local cortical gyrification in infants from birth to 2 years of age. J Neurosci 34:4228–4238CrossRefPubMedPubMedCentralGoogle Scholar
  28. Liu T (2011) A few thoughts on brain ROIs. Brain Imaging Behav 5:189–202CrossRefPubMedPubMedCentralGoogle Scholar
  29. Liu T, Nie J, Tarokh A, Guo L, Wong STC (2008) Reconstruction of central cortical surface from brain MRI images: method and application. Neuroimage 40:991–1002CrossRefPubMedGoogle Scholar
  30. Luders E, Thompson PM, Narr KL, Toga AW, Jancke L, Gaser C (2006) A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage 29:1224–1230CrossRefPubMedGoogle Scholar
  31. MacLeod CE, Zilles K, Zilles K, Schleicher A, Rilling JK, Gibson KR (2003) Expansion of the neocerebellum in Hominoidea. J Hum Evol 44:401–429CrossRefPubMedGoogle Scholar
  32. Mantini D, Gerits A, Nelissen K, Durand J-B, Joly O, Simone L, Sawamura H, Wardak C, Orban GA, Buckner RL, Vanduffel W (2011) Default mode of brain function in monkeys. J Neurosci 31:12954–12962CrossRefPubMedPubMedCentralGoogle Scholar
  33. Marquardt D (1963) An algorithm for least-squares estimation of nonlinear parameters. J Soc Ind Appl Math 11:431–441CrossRefGoogle Scholar
  34. Neal J, Takahashi M, Silva M, Tiao G, Walsh CA, Sheen VL (2007) Insights into the gyrification of developing ferret brain by magnetic resonance imaging. J Anat 210:66–77CrossRefPubMedPubMedCentralGoogle Scholar
  35. Nie J, Guo L, Li G, Faraco C, Stephen Miller L, Liu T (2010) A computational model of cerebral cortex folding. J Theor Biol 264:467–478CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 P-T, 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 22:2831–2839CrossRefPubMedGoogle Scholar
  37. Nishikuni K, Ribas GC (2013) Study of fetal and postnatal morphological development of the brain sulci: laboratory investigation. J Neurosurg: Pediatr 11(1):1–11Google Scholar
  38. Nordahl CW, Dierker D, Mostafavi I, Schumann CM, Rivera SM, Amaral DG, Van Essen DC (2007) Cortical folding abnormalities in autism revealed by surface-based morphometry. J Neurosci 27:11725–11735CrossRefPubMedGoogle Scholar
  39. Orban GA, Van Essen D, Vanduffel W (2004) Comparative mapping of higher visual areas in monkeys and humans. Trends Cogn Sci 8:315–324CrossRefPubMedGoogle Scholar
  40. Passingham R (2009) How good is the macaque monkey model of the human brain? Curr Opin Neurobiol 19:6–11CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pereira JB, Ibarretxe-Bilbao N, Marti MJ, Compta Y, Junqué C, Bargallo N, Tolosa E (2012) Assessment of cortical degeneration in patients with Parkinson’s disease by voxel-based morphometry, cortical folding, and cortical thickness. Hum Brain Mapp 33:2521–2534CrossRefPubMedGoogle Scholar
  42. Richman DP, Stewart RM, Hutchinson JW, Caviness VS (1975) Mechanical model of brain convolutional development. Science 189:18–21CrossRefPubMedGoogle Scholar
  43. Rilling JK (2006) Human and nonhuman primate brains: are they allometrically scaled versions of the same design? Evol Anthropol Issues. News Rev 15:65–77Google Scholar
  44. Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223CrossRefPubMedGoogle Scholar
  45. Rilling JK, Seligman RA (2002) A quantitative morphometric comparative analysis of the primate temporal lobe. J Hum Evol 42:505–533CrossRefPubMedGoogle Scholar
  46. Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TEJ (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:426–428CrossRefPubMedGoogle Scholar
  47. Roland PE, Zilles K (1996) Functions and structures of the motor cortices in humans. Curr Opin Neurobiol 6:773–781CrossRefPubMedGoogle Scholar
  48. Ronan L, Voets NL, Rua C, Alexanderbloch A, Hough M, Mackay CE, Crow TJ, James AC, Giedd JN, Fletcher PC (2013) Differential tangential expansion as a mechanism for cortical gyrification. Cereb Cortex 24:2219CrossRefPubMedPubMedCentralGoogle Scholar
  49. Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH, van der Kouwe A, Jenkins BG, Dale AM, Fischl B (2002) Regional and progressive thinning of the cortical ribbon in Huntington’s disease. Neurology 58:695–701CrossRefPubMedGoogle Scholar
  50. Sallet PC, Elkis H, Alves TM, Oliveira JR, Sassi E, Campi de Castro C, Busatto GF, Gattaz WF (2003) Reduced cortical folding in schizophrenia: an MRI morphometric study. Am J Psychiatry 160:1606–1613CrossRefPubMedGoogle Scholar
  51. Schoenemann PT (2006) Evolution of the size and functional areas of the human brain. Annu Rev Anthropol 35:379–406CrossRefGoogle Scholar
  52. Smaers JB, Soligo C (2013) Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution. Proc Biol Sci 280:20130269CrossRefPubMedPubMedCentralGoogle Scholar
  53. Smart IH, McSherry GM (1986a) Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes. J Anat 146:141–152PubMedPubMedCentralGoogle Scholar
  54. Smart IH, McSherry GM (1986b) Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes. J Anat 147:27–43PubMedPubMedCentralGoogle Scholar
  55. Tallinen T, Chung JY, Rousseau F, Girard N, Lefevre J, Mahadevan L (2016) On the growth and form of cortical convolutions. Nat Phys 12:588–593CrossRefGoogle Scholar
  56. Thompson PM, Hayashi KM, Sowell ER, Gogtay N, Giedd JN, Rapoport JL, de Zubicaray GI, Janke AL, Rose SE, Semple J, Doddrell DM, Wang Y, van Erp TGM, Cannon TD, Toga AW (2004) Mapping cortical change in Alzheimer’s disease, brain development, and schizophrenia. Neuroimage 23(Suppl):S2–S18CrossRefPubMedGoogle Scholar
  57. Toro R (2012) On the Possible Shapes of the Brain. Evol Biol 39:600–612CrossRefGoogle Scholar
  58. Toro R, Burnod Y (2005) A morphogenetic model for the development of cortical convolutions. Cereb Cortex 15:1900–1913CrossRefPubMedGoogle Scholar
  59. Tortori-Donati P, Rossi A, Biancheri R (2005) Brain Malformations. Springer, Berlin HeidelbergCrossRefGoogle Scholar
  60. Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313CrossRefPubMedGoogle Scholar
  61. Van Essen DC (2002) Surface-based atlases of cerebellar cortex in the human, macaque, and mouse. Ann N Y Acad Sci 978:468–479CrossRefPubMedGoogle Scholar
  62. Van Essen DC, Lewis JW, Drury HA, Hadjikhani N, Tootell RBH, Bakircioglu M, Miller MI (2001) Mapping visual cortex in monkeys and humans using surface-based atlases. Vision Res 41:1359–1378CrossRefPubMedGoogle Scholar
  63. Van Essen DC, Ugurbil K, Auerbach E, Barch D, Behrens TEJ, Bucholz R, Chang A, Chen L, Corbetta M, Curtiss SW, Della Penna S, Feinberg D, Glasser MF, Harel N, Heath AC, Larson-Prior L, Marcus D, Michalareas G, Moeller S, Oostenveld R, Petersen SE, Prior F, Schlaggar BL, Smith SM, Snyder AZ, Xu J, Yacoub E (2012) The human connectome project: a data acquisition perspective. Neuroimage 62:2222–2231CrossRefPubMedPubMedCentralGoogle Scholar
  64. Welker W (1990) Why does cerebral cortex fissure and fold?. A review of determinants of gyri and sulci, Cereb Cortex, p 8Google Scholar
  65. Yeo BTT, Yu P, Grant PE, Fischl B, Golland P (2008) Shape Analysis with Overcomplete Spherical Wavelets. MICCAI LNCS Lect Notes Comput Sci 5241:468–476CrossRefGoogle Scholar
  66. Yu P, Han X, Ségonne F, Pienaar R, Buckner RL, Golland P, Grant PE, Fischl B (2006) Cortical Surface Shape Analysis Based on Spherical Wavelet Transformation. Conf Comput Vis Pattern Recognit WorkshopsGoogle Scholar
  67. Yu X, Chen H, Zhang T, Hu X, Guo L, Liu T (2013) Joint analysis of gyral folding and fiber shape patterns. In: ISBI. IEEE. p 85–88Google Scholar
  68. Zhang D, Guo L, Zhu D, Li K, Li L, Chen H, Zhao Q, Hu X, Liu T (2013) Diffusion tensor imaging reveals evolution of primate brain architectures. Brain Struct Funct 218:1429–1450CrossRefPubMedGoogle Scholar
  69. Zilles K, Armstrong E, Schleicher A, Kretschmann H-J (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol (Berl) 179:173–179CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Xiao Li
    • 1
  • Hanbo Chen
    • 2
  • Tuo Zhang
    • 1
    • 5
  • Xiang Yu
    • 1
  • Xi Jiang
    • 2
  • Kaiming Li
    • 3
    • 7
  • Longchuan Li
    • 4
  • Mir Jalil Razavi
    • 6
  • Xianqiao Wang
    • 6
  • Xintao Hu
    • 1
  • Junwei Han
    • 1
  • Lei Guo
    • 1
  • Xiaoping Hu
    • 3
  • Tianming Liu
    • 2
  1. 1.School of AutomationNorthwestern Polytechnical UniversityXi’anChina
  2. 2.Cortical Architecture Imaging and Discovery Lab, Department of Computer Science and Bioimaging Research CenterThe University of GeorgiaAthensUSA
  3. 3.Department of BioengineeringUC RiversideRiversideUSA
  4. 4.Marcus Autism CenterEmory UniversityAtlantaUSA
  5. 5.Brain Decoding Research CenterNorthwestern Polytechnical UniversityXi’anChina
  6. 6.College of EngineeringThe University of GeorgiaAthensUSA
  7. 7.West China Hospital of Sichuan UniversityChengduChina

Personalised recommendations