Skip to main content
Log in

Quantitative diffusion tensor fiber tracking of age-related changes in the limbic system

  • Neuro
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Cerebral white matter is known to undergo degradation with aging, and diffusion tensor imaging (DTI) is capable of revealing the white matter integrity. We assessed age-related changes of quantitative diffusivity parameters and fiber characteristics within the fornix and the cingulum. Thirty-eight healthy subjects aged 18–88 years were examined at 3 Tesla using a 1.9-mm isotropic DTI sequence. Quantitative fiber tracking was performed for 3D-segmentation of the fornix and the cingulum to determine fractional anisotropy (FA), mean diffusivity (MD), eigenvalues (λ1, λ2, and λ3), number of fibers (NoF), and mean NoF/voxel (FpV). In the fornix, all diffusivity parameters (FA, MD, and eigenvalues) were moderately correlated with age. Strong and moderate negative correlations for NoF and FpV were found, respectively. In the cingulum, no correlation was observed between FA and age, and only weak correlations for the other quantitative parameters. Differences in correlations between the fornix and the cingulum were significant for all diffusivity parameters and for NoF, but not for FpV. The strongest relative changes per decade of age were found in the fornix: FA −2.1%, MD 4.2%, NoF −10.6%, and FpV −4.6%. Our quantitative 3D fiber tracking approach shows that the cingulum is resistant to aging while the fornix is not.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Tisserand DJ, Pruessner JC, Sanz Arigita EJ, van Boxtel MP, Evans AC, Jolles J, Uylings HB (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 17:657–669

    Article  PubMed  Google Scholar 

  2. Tisserand DJ, Visser PJ, van Boxtel MP, Jolles J (2000) The relation between global and limbic brain volumes on MRI and cognitive performance in healthy individuals across the age range. Neurobiol Aging 21:569–576

    Article  PubMed  CAS  Google Scholar 

  3. Ylikoski R, Salonen O, Mantyla R, Ylikoski A, Keskivaara P, Leskela M, Erkinjuntti T (2000) Hippocampal and temporal lobe atrophy and age-related decline in memory. Acta Neurol Scand 101:273–278

    Article  PubMed  CAS  Google Scholar 

  4. Bigler ED, Blatter DD, Anderson CV, Johnson SC, Gale SD, Hopkins RO, Burnett B (1997) Hippocampal volume in normal aging and traumatic brain injury. AJNR Am J Neuroradiol 18:11–23

    PubMed  CAS  Google Scholar 

  5. Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, Loken WJ, Thornton AE, Acker JD (1997) Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex 7:268–282

    Article  PubMed  CAS  Google Scholar 

  6. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546

    Article  PubMed  Google Scholar 

  7. Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 21:1174–1181

    Article  PubMed  Google Scholar 

  8. Bhagat YA, Beaulieu C (2004) Diffusion anisotropy in subcortical white matter and cortical gray matter: changes with aging and the role of CSF-suppression. J Magn Reson Imaging 20:216–227

    Article  PubMed  Google Scholar 

  9. Pfefferbaum A, Adalsteinsson E, Sullivan EV (2005) Frontal circuitry degradation marks healthy adult aging: Evidence from diffusion tensor imaging. Neuroimage 26:891–899

    Article  PubMed  Google Scholar 

  10. Pfefferbaum A, Sullivan EV (2003) Increased brain white matter diffusivity in normal adult aging: relationship to anisotropy and partial voluming. Magn Reson Med 49:953–961

    Article  PubMed  Google Scholar 

  11. Sullivan EV, Adalsteinsson E, Pfefferbaum A (2006) Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb Cortex 16:1030–1039

    Article  PubMed  Google Scholar 

  12. Salat DH, Tuch DS, Hevelone ND, Fischl B, Corkin S, Rosas HD, Dale AM (2005) Age-related changes in prefrontal white matter measured by diffusion tensor imaging. Ann N Y Acad Sci 1064:37–49

    Article  PubMed  CAS  Google Scholar 

  13. Abe O, Aoki S, Hayashi N, Yamada H, Kunimatsu A, Mori H, Yoshikawa T, Okubo T, Ohtomo K (2002) Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 23:433–441

    Article  PubMed  Google Scholar 

  14. Sijens PE, Irwan R, Potze JH, Mostert JP, De Keyser J, Oudkerk M (2006) Relationships between brain water content and diffusion tensor imaging parameters (apparent diffusion coefficient and fractional anisotropy) in multiple sclerosis. Eur Radiol 16:898–904

    Article  PubMed  Google Scholar 

  15. Poupon C, Clark CA, Frouin V, Regis J, Bloch I, Le Bihan D, Mangin J (2000) Regularization of diffusion-based direction maps for the tracking of brain white matter fascicles. Neuroimage 12:184–195

    Article  PubMed  CAS  Google Scholar 

  16. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625–632

    Article  PubMed  CAS  Google Scholar 

  17. Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies- a technical review. NMR Biomed 15:468–480

    Article  PubMed  Google Scholar 

  18. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S (2004) Fiber tract-based atlas of human white matter anatomy. Radiology 230:77–87

    Article  PubMed  Google Scholar 

  19. Concha L, Beaulieu C, Gross DW (2005) Bilateral limbic diffusion abnormalities in unilateral temporal lobe epilepsy. Ann Neurol 57:188–196

    Article  PubMed  Google Scholar 

  20. Roberts TP, Liu F, Kassner A, Mori S, Guha A (2005) Fiber density index correlates with reduced fractional anisotropy in white matter of patients with glioblastoma. AJNR Am J Neuroradiol 26:2183–2186

    PubMed  Google Scholar 

  21. Berman JI, Mukherjee P, Partridge SC, Miller SP, Ferriero DM, Barkovich AJ, Vigneron DB, Henry RG (2005) Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants. Neuroimage 27:862–871

    Article  PubMed  Google Scholar 

  22. Schonberg T, Pianka P, Hendler T, Pasternak O, Assaf Y (2006) Characterization of displaced white matter by brain tumors using combined DTI and fMRI. Neuroimage 30:1100–1111

    Article  PubMed  Google Scholar 

  23. Benson AD, Slavin MJ, Tran TT, Petrella JR, Doraiswamy PM (2005) Screening for early Alzheimer’s disease: is there still a role for the mini-mental state examination? Prim Care Companion J Clin Psychiatry 7:62–69

    PubMed  Google Scholar 

  24. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  PubMed  CAS  Google Scholar 

  25. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210

    Article  PubMed  Google Scholar 

  26. Jiang H, van Zijl PC, Kim J, Pearlson GD, Mori S (2006) DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed 81:106–116

    Article  PubMed  Google Scholar 

  27. Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247–254

    Article  PubMed  CAS  Google Scholar 

  28. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267

    Article  PubMed  CAS  Google Scholar 

  29. Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906

    Article  PubMed  CAS  Google Scholar 

  30. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269

    Article  PubMed  CAS  Google Scholar 

  31. Xue R, van Zijl PC, Crain BJ, Solaiyappan M, Mori S (1999) In vivo three-dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging. Magn Reson Med 42:1123–1127

    Article  PubMed  CAS  Google Scholar 

  32. Concha L, Gross DW, Beaulieu C (2005) Diffusion tensor tractography of the limbic system. AJNR Am J Neuroradiol 26:2267–2274

    PubMed  Google Scholar 

  33. Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, Solaiyappan M, Mori S (2001) Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 14:723–735

    Article  PubMed  CAS  Google Scholar 

  34. Williams EJ (1959) The comparision of regression variables. J R Stat Soc Ser B 21:395–399

    Google Scholar 

  35. Zou KH, Tuncali K, Silverman SG (2003) Correlation and simple linear regression. Radiology 227:617–622

    Article  PubMed  Google Scholar 

  36. Meier-Ruge W, Ulrich J, Bruhlmann M, Meier E (1992) Age-related white matter atrophy in the human brain. Ann N Y Acad Sci 673:260–269

    Article  PubMed  CAS  Google Scholar 

  37. Moseley M (2002) Diffusion tensor imaging and aging- a review. NMR Biomed 15:553–560

    Article  PubMed  Google Scholar 

  38. Nusbaum AO, Tang CY, Buchsbaum MS, Wei TC, Atlas SW (2001) Regional and global changes in cerebral diffusion with normal aging. AJNR Am J Neuroradiol 22:136–142

    PubMed  CAS  Google Scholar 

  39. 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. AJR Am J Roentgenol 179:1515–1522

    PubMed  Google Scholar 

  40. Zhai G, Lin W, Wilber KP, Gerig G, Gilmore JH (2003) Comparisons of regional white matter diffusion in healthy neonates and adults performed with a 3.0-T head-only MR imaging unit. Radiology 229:673–681

    Article  PubMed  Google Scholar 

  41. Suzuki Y, Matsuzawa H, Kwee IL, Nakada T (2003) Absolute eigenvalue diffusion tensor analysis for human brain maturation. NMR Biomed 16:257–260

    Article  PubMed  Google Scholar 

  42. 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. AJNR Am J Neuroradiol 23:1445–1456

    PubMed  Google Scholar 

  43. Schmithorst VJ, Wilke M, Dardzinski BJ, Holland SK (2002) Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-tensor MR imaging study. Radiology 222:212–218

    Article  PubMed  Google Scholar 

  44. Papanikolaou N, Karampekios S, Papadaki E, Malamas M, Maris T, Gourtsoyiannis N (2006) Fractional anisotropy and mean diffusivity measurements on normal human brain: comparison between low-and high-resolution diffusion tensor imaging sequences. Eur Radiol 16:187–192

    Article  PubMed  Google Scholar 

  45. Jack CR Jr, Petersen RC, O’Brien PC, Tangalos EG (1992) MR-based hippocampal volumetry in the diagnosis of Alzheimer’s disease. Neurology 42:183–188

    PubMed  Google Scholar 

  46. Convit A, de Leon MJ, Hoptman MJ, Tarshish C, De Santi S, Rusinek H (1995) Age-related changes in brain: I. Magnetic resonance imaging measures of temporal lobe volumes in normal subjects. Psychiatr Q 66:343–355

    Article  PubMed  CAS  Google Scholar 

  47. Huisman TA, Loenneker T, Barta G, Bellemann ME, Hennig J, Fischer JE, Il’yasov KA (2006) Quantitative diffusion tensor MR imaging of the brain: field strength related variance of apparent diffusion coefficient (ADC) and fractional anisotropy (FA) scalars. Eur Radiol 16:1651–1658

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erich Salomonowitz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stadlbauer, A., Salomonowitz, E., Strunk, G. et al. Quantitative diffusion tensor fiber tracking of age-related changes in the limbic system. Eur Radiol 18, 130–137 (2008). https://doi.org/10.1007/s00330-007-0733-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-007-0733-8

Keywords

Navigation