Abstract
Diffusion tensor imaging (DTI) and high angular resolution diffusion imaging (HARDI) have been broadly used in the neuroimaging field to investigate the macro-scale fiber connection patterns in the cerebral cortex. Our recent analyses of DTI and HARDI data demonstrated that gyri are connected by denser, streamlined fibers than sulci are. Inspired by this finding and motivated by the fact that DTI-derived fibers provide the structural substrates for functional connectivity, we hypothesize that gyri are global functional connection centers and sulci are local functional units. To test this functional model of gyri and sulci, we examined the structural and functional connectivity among the landmarks on the selected gyral/sulcal areas in the frontal/parietal lobe and in the whole cerebral cortex via multimodal DTI and resting state fMRI (R-fMRI) datasets. Our results demonstrate that functional connectivity is strong among gyri, weak among sulci, and moderate between gyri and sulci. These results suggest that gyri are functional connection centers that exchange information among remote structurally connected gyri and neighboring sulci, while sulci communicate directly with their neighboring gyri and indirectly with other cortical regions through gyri. This functional model of gyri and sulci has been supported by a series of experiments, and provides novel perspectives on the functional architecture of the cerebral cortex.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andersson JL, Skare S, Ashburner J (2003) How to correct image distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 20:870–888
Asanuma H (1989) The motor cortex. Raven Press, New York
Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson, Ser B 111(3):209–219
Bassett DS, Wymbs NF, Porter MA, Mucha PJ, Carlson JM, Grafton ST (2011) Dynamic reconfiguration of human brain networks during learning. PNAS 108(18):7641–7646
Brett M, Johnsrude IS, Owen AM (2002) The problem of functional localization in the human brain. Nat Rev Neurosci 3(3):243–249
Broman SH, Fletcher JM (eds) (1999) The changing nervous system: Neurobehavioral consequences of early brain disorders. Oxford University Press, New York, pp 100–101
Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186–198
Chang C, Glover G (2010) Time-frequency dynamics of resting-state brain connectivity measured with fMRI. NeuroImage 50(1):81–98
Chen H, Zhang T, Guo L, Li K, Yu X, Li L, Hu X, Han J, Hu X, Liu T (2012) Coevolution of gyral folding and structural connection patterns in primate brains. Cereb Cortex, in press
Deco G, Jirsa VK (2012) Ongoing cortical activity at rest: criticality, multistability, and ghost attractors. J Neurosci 32:3366–3375
Deligianni F, Robinson E, Beckmann CF, Sharp D, Edwards AD, Rueckert D (2011) Inference of functional connectivity from direct and indirect structural brain connections. ISBI
Fischl B, Sereno M, Dale AM (1999) Cortical surface-based analysis II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9(2):195–207
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711
Ghosh S, Fyffe RE, Porter R (1988) Morphology of neurons in area 4 gamma of the cat’s cortex studied with intracellular injection of HRP. J Comp Neurol 277:290–312
Hasson U, Malach R, Heeger DJ (2010) Reliability of cortical activity during natural stimulation. Trends Cogn Sci 14(1):40–48
Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P (2009) Predicting human resting-state functional connectivity from structural connectivity. PNAS 106(6):2035–2040
Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science, 4th edn
Keller A, Asanuma H (1993) Synaptic relationships involving local axon collaterals of pyramidal neurons in the cat motor cortex. J Comp Neurol 336:229–242
Li G, Guo L, Nie J, Liu T (2009) Automatic cortical sulcal parcellation based on surface principal direction flow field tracking. Neuroimage 46(4):923–937
Li G, Guo L, Nie J, Liu T (2010) An automated pipeline for sulci fundi extraction. Med Image Anal 14(3):343–359
Li K, Guo L, Zhu D, Hu X, Han J, Liu T (2012a) Individual functional ROI optimization via maximization of group-wise consistency of structural and functional profiles. Neuroinformatics, in press
Li X, Lim C, Li K, Guo L, Liu T (2012b) Detecting brain state changes via fiber-centered functional connectivity analysis. Neuroinformatics, in press
Liu T (2011) A few thoughts on brain ROIs. Brain Imaging Behav 5(3):189–202
Liu T, Li H, Wong K, Tarokh A, Guo L, Wong S (2007) Brain tissue segmentation based on DTI data. NeuroImage 38(1):114–123
Liu T, Nie J, Tarokh A, Guo L, Wong S (2008) Reconstruction of central cortical surface from MRI brain images: method and application. NeuroImage 40(3):991–1002
Logothetis NK (2008) What we can do and what we cannot do with fMRI. Nature 453:869–878
Lohmann G, von Cramon DY (2000) Automatic labelling of the human cortical surface using sulcal basins. Med Image Anal 4(3):179–188
Majeed W, Magnuson M, Hasenkamp W, Schwarb H, Schumacher EH, Barsalou L, Keilholz SD (2011) Spatiotemporal dynamics of low frequency BOLD fluctuations in rats and humans. NeuroImage 54:1140–1150
Miller JSG (1988) Motor areas of the cerebral cortex. CIBA foundation symposium 132. J Neurol Neurosurg Psychiatry 51(9):1245–1246
Mori S (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51(5):527–539
Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722
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(12):2831–2839
Passingham RE, Stephan KE, Kötter R (2002) The anatomical basis of functional localization in the cortex. Nat Rev Neurosci 3(8):606–616
Ragan T, Kadiri LR, Venkataraju KU, Bahlmann K, Sutin J, Taranda J, Arganda-Carreras I, Kim Y, Seung HS, Osten P (2012) Serial two-photon tomography for automated ex vivo mouse brain imaging. Nat Methods 9(3):255–258. doi:10.1038/nmeth.1854
Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176
Rettmann ME, Han X, Xu C, Prince JL (2002) Automated sulcal segmentation using watersheds on the cortical surface. NeuroImage 15(2):329–344
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 11:426–428
Scannell JW (1997) Determining cortical landscapes. Nature 386(6624):452
Schmahmann J, Pandya D (2006) Fiber pathways of the brain. Oxford University Press, Oxford
Shi Y, Thompson P, Dinov I, Toga A (2008) Hamilton–Jacobi skeleton on cortical surfaces. IEEE Trans Med Imaging 27(5):664–673
Smith SM, Miller KL, Moeller S, Xu J, Auerbach EJ, Woolrich MW, Beckmann CF, Jenkinson M, Andersson J, Glasser MF, Van Essen DC, Feinberg DA, Yacoub ES, Ugurbil K (2012) Temporally-independent functional modes of spontaneous brain activity. PNAS, in press
Stephan KE, Tittgemeyer M, Knoesche TR, Moran RJ, Friston KJ (2009) Tractography-based priors for dynamic causal models. NeuroImage 47(4):1628–1638
Sun J, Hu X, Huang X, Liu Y, Li K, Li X, Han J, Guo L, Liu T, Zhang J (2012) Inferring consistent functional interaction patterns from natural stimulus FMRI data. NeuroImage, in press
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical Publishers, Inc., New York
Thirion JP (1996) The extremal mesh and understanding of 3D surfaces. Int J Comput Vis 19(2):115–128
Thomson AM, Lamy C (2007) Functional maps of neocortical local circuitry. Front Neurosci 1(1):19–42
Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME (2007) Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447:83–86
Zhu D, Li K, Faraco C, Deng F, Zhang D, Jiang X, Chen H, Guo L, Miller LS, Liu T (2011) Optimization of functional brain ROIs via maximization of consistency of structural connectivity profiles. NeuroImage 59(2):1382–1393
Zhu D, Li K, Guo L, Jiang X, Zhang T, Zhang D, Chen H, Deng F, Faraco C, Jin C, Wee CY, Yuan Y, Lv P, Yin Y, Hu X, Duan L, Hu X, Han J, Wang L, Shen D, Miller LS, Li L, Liu T (2012) DICCCOL: dense individualized and common connectivity-based cortical landmarks. Cereb Cortex, in press
Zilles K, Amunts K (2009) Centenary of Brodmann’s map—conception and fate. Nat Rev Neurosci 11(2):139–145
Acknowledgments
TL was supported by the NIH Career Award (EB 006878), NSF CAREER Award IIS-1149260, NIH R01 DA033393, and The University of Georgia start-up. KL and LG were supported by The Northwestern Polytechnic University Foundation for Fundamental Research. The HARDI dataset was obtained from our prior studies in Nie et al. (2012). The authors would like to thank the anonymous reviewers for their constructive comments.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Deng, F., Jiang, X., Zhu, D. et al. A functional model of cortical gyri and sulci. Brain Struct Funct 219, 1473–1491 (2014). https://doi.org/10.1007/s00429-013-0581-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-013-0581-z