Summary

Sådan måler du Kortikal Folding fra MR-billeder: en trin-for-trin introduktion til at beregne Lokal Gyrification Index

Published: January 02, 2012
doi:

Summary

Measuring gyrification (cortical folding) at any age represents a window into early brain development. Hence, we previously developed an algorithm to measure local gyrification at thousands of points over the hemisphere1. In this paper, we detail the computation of this local gyrification index.

Abstract

Cortical folding (gyrification) is determined during the first months of life, so that adverse events occurring during this period leave traces that will be identifiable at any age. As recently reviewed by Mangin and colleagues2, several methods exist to quantify different characteristics of gyrification. For instance, sulcal morphometry can be used to measure shape descriptors such as the depth, length or indices of inter-hemispheric asymmetry3. These geometrical properties have the advantage of being easy to interpret. However, sulcal morphometry tightly relies on the accurate identification of a given set of sulci and hence provides a fragmented description of gyrification. A more fine-grained quantification of gyrification can be achieved with curvature-based measurements, where smoothed absolute mean curvature is typically computed at thousands of points over the cortical surface4. The curvature is however not straightforward to comprehend, as it remains unclear if there is any direct relationship between the curvedness and a biologically meaningful correlate such as cortical volume or surface. To address the diverse issues raised by the measurement of cortical folding, we previously developed an algorithm to quantify local gyrification with an exquisite spatial resolution and of simple interpretation. Our method is inspired of the Gyrification Index5, a method originally used in comparative neuroanatomy to evaluate the cortical folding differences across species. In our implementation, which we name local Gyrification Index (lGI1), we measure the amount of cortex buried within the sulcal folds as compared with the amount of visible cortex in circular regions of interest. Given that the cortex grows primarily through radial expansion6, our method was specifically designed to identify early defects of cortical development.

In this article, we detail the computation of local Gyrification Index, which is now freely distributed as a part of the FreeSurfer Software (http://surfer.nmr.mgh.harvard.edu/, Martinos Center for Biomedical Imaging, Massachusetts General Hospital). FreeSurfer provides a set of automated reconstruction tools of the brain’s cortical surface from structural MRI data. The cortical surface extracted in the native space of the images with sub-millimeter accuracy is then further used for the creation of an outer surface, which will serve as a basis for the lGI calculation. A circular region of interest is then delineated on the outer surface, and its corresponding region of interest on the cortical surface is identified using a matching algorithm as described in our validation study1. This process is repeatedly iterated with largely overlapping regions of interest, resulting in cortical maps of gyrification for subsequent statistical comparisons (Fig. 1). Of note, another measurement of local gyrification with a similar inspiration was proposed by Toro and colleagues7, where the folding index at each point is computed as the ratio of the cortical area contained in a sphere divided by the area of a disc with the same radius. The two implementations differ in that the one by Toro et al. is based on Euclidian distances and thus considers discontinuous patches of cortical area, whereas ours uses a strict geodesic algorithm and include only the continuous patch of cortical area opening at the brain surface in a circular region of interest.

Protocol

1. Rekonstruere 3D kortikale overflader Denne første del af protokollen bruger standard FreeSurfer rørledningen som beskrevet i Wiki ( http://surfer.nmr.mgh.harvard.edu/fswiki ). Bemærk, at kommandoerne detaljerede her beskrive en måde at opnå det kortikale overfladen rekonstruktioner, men tilsvarende kommandoer kan også anvendes. Importer rå MRI DICOM ind FreeSurfer og kontrollere kvali…

Discussion

The protocol above describes how to measure local Gyrification Index based on cerebral T1-weighted MRI and conduct statistical group comparisons. Our method has been specifically designed to localize early disruption in the cortical expansion process and as such is of particular interest in many neurodevelopmental or psychiatric conditions. Examples of group comparisons in clinical samples can be found in publications by our group1,12 or by others13-16. The process is fully automated and requ…

Disclosures

The authors have nothing to disclose.

Acknowledgements

This research was supported by the National Center of Competence in Research (NCCR) “SYNAPSY – The Synaptic Bases of Mental Diseases” financed by the Swiss National Science Foundation (n° 51AU40_125759). Development of the local Gyrification Index was supported by grants from the Swiss National Research Fund to Dr. Marie Schaer (323500-111165) and to Dr. Stephan Eliez (3200-063135.00/1, 3232-063134.00/1, PP0033-102864 and 32473B-121996) and by the Center for Biomedical Imaging (CIBM) of the Geneva-Lausanne Universities and the EPFL, as well as the foundations Leenaards and Louis-Jeantet. Support for the development of FreeSurfer software was provided in part by the National Center for Research Resources (P41-RR14075, and the NCRR BIRN Morphometric Project BIRN002, U24 RR021382), the National Institute for Biomedical Imaging and Bioengineering (R01 EB001550, R01EB006758), the National Institute for Neurological Disorders and Stroke (R01 NS052585-01) as well as the Mental Illness and Neuroscience Discovery (MIND) Institute, and is part of the National Alliance for Medical Image Computing (NAMIC), funded by the National Institutes of Health through the NIH Roadmap for Medical Research, Grant U54 EB005149. Additional support was provided by The Autism & Dyslexia Project funded by the Ellison Medical Foundation.

Materials

Material: a Unix or Mac workstation with a processor of 2GHz or faster and a minimum of 4GB of RAM, with FreeSurfer installed (http://surfer.nmr.mgh.harvard.edu/fswiki, preferably the latest version, but no older than version 4.0.3). In order to compute the local Gyrification Index, MATLAB is also required (http://www.mathworks.com/) along with the Image Processing Toolbox.

Data: A sample of good quality (high-resolution, high contrast) cerebral MRI T1-weighted dataset. Your group of subjects must be preferably matched for age and gender. Given the normal inter-individual variability in cerebral morphology, the number of subjects in each group should be sufficient to identify an existing group difference (the more – the better). A reasonable minimum sample size would be around 20 subjects per group (although you can probably go for less if the intensity of changes is large and if your groups are tightly matched for gender and age).

Name of the equipment Company Catalogue number Comments
FreeSurfer Martinos Center for Biomedical Imaging, MGH   Version newer than 4.0.3
Matlab Mathworks   Image Processing Toolbox

References

  1. Schaer, M. A surface-based approach to quantify local cortical gyrification. IEEE. Trans. Med. Imaging. 27, 161-170 (2008).
  2. Mangin, J. F., Jouvent, E., Cachia, A. In-vivo measurement of cortical morphology: means and meanings. Curr. Opin. Neurol. 23, 359-367 (2010).
  3. Mangin, J. F. A framework to study the cortical folding patterns. Neuroimage. 23, S129-S138 (2004).
  4. Luders, E. A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage. 29, 1224-1230 (2006).
  5. Zilles, K., Armstrong, E., Schleicher, A., Kretschmann, H. J. The human pattern of gyrification in the cerebral cortex. Anat. Embryol. (Berl). 179, 173-179 (1988).
  6. Rakic, P. Specification of cerebral cortical areas. Science. 241, 170-176 (1988).
  7. Toro, R. Brain size and folding of the human cerebral cortex. Cereb. Cortex. 18, 2352-2357 (2008).
  8. Fischl, B., Sereno, M. I., Dale, A. M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage. 9, 195-207 (1999).
  9. Dale, A. M., Fischl, B., Sereno, M. I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 9, 179-194 (1999).
  10. Genovese, C. R., Lazar, N. A., Nichols, T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage. 15, 870-878 (2002).
  11. Desikan, R. S. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 31, 968-980 (2006).
  12. Schaer, M. Congenital heart disease affects local gyrification in 22q11.2 deletion syndrome. Dev. Med. Child. Neurol. 51, 746-753 (2009).
  13. Palaniyappan, L., Mallikarjun, P., Joseph, V., White, T. P., Liddle, P. F. Folding of the Prefrontal Cortex in Schizophrenia: Regional Differences in Gyrification. Biol. Psychiatry. , (2011).
  14. Zhang, Y. Decreased gyrification in major depressive disorder. Neuroreport. 20, 378-380 (2009).
  15. Juranek, J., Salman, M. S. Anomalous development of brain structure and function in spina bifida myelomeningocele. Dev. Disabil. Res. Rev. 16, 23-30 (2010).
  16. Zhang, Y. Reduced cortical folding in mental retardation. AJNR. Am. J. Neuroradiol. 31, 1063-1067 (2010).
  17. Kuperberg, G. R. Regionally localized thinning of the cerebral cortex in schizophrenia. Archives of general psychiatry. 60, 878-888 (2003).
  18. Milad, M. R. Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc. Natl. Acad. Sci. U. S. A. 102, 10706-10711 (2005).
  19. Rauch, S. L. A magnetic resonance imaging study of cortical thickness in animal phobia. Biol. Psychiatry. 55, 946-952 (2004).
  20. Fjell, A. M. Selective increase of cortical thickness in high-performing elderly–structural indices of optimal cognitive aging. Neuroimage. 29, 984-994 (2006).
  21. Walhovd, K. B. Regional cortical thickness matters in recall after months more than minutes. Neuroimage. 31, 1343-1351 (2006).
  22. Gold, B. T. Differing neuropsychological and neuroanatomical correlates of abnormal reading in early-stage semantic dementia and dementia of the Alzheimer type. Neuropsychologia. 43, 833-846 (2005).
  23. Salat, D. H. Thinning of the cerebral cortex in aging. Cereb. Cortex. 14, 721-730 (2004).
  24. Schaer, M., Eliez, S. Contribution of structural brain imaging to our understanding of cortical development process. European Psychiatry Reviews. 2, 13-16 (2009).
  25. Shaw, P. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 28, 3586-3594 (2008).
check_url/3417?article_type=t

Play Video

Cite This Article
Schaer, M., Cuadra, M. B., Schmansky, N., Fischl, B., Thiran, J., Eliez, S. How to Measure Cortical Folding from MR Images: a Step-by-Step Tutorial to Compute Local Gyrification Index. J. Vis. Exp. (59), e3417, doi:10.3791/3417 (2012).

View Video