Neurobiology of Aging
Volume 33, Issue 1 , Pages 200.e23-200.e31 , January 2012

Age-related effects on cortical thickness patterns of the Rhesus monkey brain

  • Bang-Bon Koo

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
    • Center for Biomedical Imaging, Boston University School of Medicine, Boston, MA, USA
  • ,
  • Steven P. Schettler

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
  • ,
  • Donna E. Murray

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
  • ,
  • Jong-Min Lee

      Affiliations

    • Department of Biomedical Engineering, Hanyang University, Seoul, South Korea
  • ,
  • Ronald J. Killiany

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
  • ,
  • Douglas L. Rosene

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
    • Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA
  • ,
  • Dae-Shik Kim

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
    • Center for Biomedical Imaging, Boston University School of Medicine, Boston, MA, USA
    • Department of Electrical Engineering, Korea Advanced Institute of Science and Technology, Daejeon, South Korea
  • ,
  • Itamar Ronen

      Affiliations

    • Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA
    • Center for Biomedical Imaging, Boston University School of Medicine, Boston, MA, USA
    • Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
    • Corresponding Author InformationCorresponding author: Tel.: +31 71 526 5479

Received 6 October 2009 ,Revised 2 July 2010 ,Accepted 11 July 2010.

References 

  1. Alexander GE, Chen K, Aschenbrenner M, Merkley TL, Santerre-Lemmon LE, Shamy JL, et al. Age-related regional network of magnetic resonance imaging gray matter in the rhesus macaque. J. Neurosci. 2008;28:2710–2718
  2. Allen JS, Bruss J, Brown CK, Damasio H. Normal neuroanatomical variation due to age: The major lobes and a parcellation of the temporal region. Neurobiol. Aging. 2005;26:1245–1260
  3. Anderson MJ, Robinson J. Permutation tests for linear models. Aust. N Z J. Stat. 2001;43:75–88
  4. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans. Med. Imaging. 1999;18:32–42
  5. Cocosco CA, Zijdenbos AP, Evans AC. A fully automatic and robust brain MRI tissue classification method. Med. Image Anal. 2003;7:513–527
  6. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994;18:192–205
  7. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis (I. Segmentation and surface reconstruction). Neuroimage. 1999;9:179–194
  8. Dickerson BC, Fenstermacher E, Salat DH, Wolk DA, Maguire RP, Desikan R, et al. Detection of cortical thickness correlates of cognitive performance: Reliability across MRI scan sessions, scanners, and field strengths. Neuroimage. 2008;39:10–18
  9. Dickstein DL, Kabaso D, Rocher AB, Luebke JI, Wearne SL, Hof PR. Changes in the structural complexity of the aged brain. Aging Cell. 2007;6:275–284
  10. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. USA. 2000;97:11050–11055
  11. Fjell AM, Walhovd KB, Reinvang I, Lundervold A, Salat D, Quinn BT, et al. Selective increase of cortical thickness in high-performing elderly − structural indices of optimal cognitive aging. Neuroimage. 2006;29:984–994
  12. Franklin MS, Kraemer GW, Shelton SE, Baker E, Kalin NH, Uno H. Gender differences in brain volume and size of corpus callosum and amygdala of rhesus monkey measured from MRI images. Brain Res. 2000;852:263–267
  13. Ge Y, Grossman RI, Babb JS, Rabin ML, Mannon LJ, Kolson DL. Age-related total gray matter and white matter changes in normal adult brain (Part I: volumetric MR imaging analysis). AJNR Am. J. Neuroradiol. 2002;23:1327–1333
  14. Herculano-Houzel S, Collins CE, Wong P, Kaas JH, Lent R. The basic nonuniformity of the cerebral cortex. Proc. Natl. Acad. Sci. U S A. 2008;105:12593–12598
  15. Herndon JG, Moss MB, Rosene DL, Killiany RJ. Patterns of cognitive decline in aged rhesus monkeys. Behav. Brain Res. 1997;87:25–34
  16. Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, et al. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging. 2001;22:581–594
  17. Kim JS, Singh V, Lee JK, Lerch J, Ad-Dab'Bagh Y, MacDonald D, et al. Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage. 2005;27:210–221
  18. Kochunov P, Thompson PM, Coyle TR, Lancaster JL, Kochunov V, Royall D, et al. Relationship among neuroimaging indices of cerebral health during normal aging. Hum Brain Mapp. 2008;29:36–45
  19. Lee J, Lee JM, Kim JH, Kim IY, Evans AC, Kim SI. A novel quantitative validation of the cortical surface reconstruction algorithm using MRI phantom: issues on local geometric accuracy and cortical thickness. In: Medical Image Computing and Computer-Assisted Intervention: MICCAI International Conference on Medical Image Computing and Computer-Assisted Intervention. 2006;p. 183–1909, (Pt 1)
  20. Lerch JP, Evans AC. Cortical thickness analysis examined through power analysis and a population simulation. Neuroimage. 2005;24:163–173
  21. Lyttelton O, Boucher M, Robbins S, Evans A. An unbiased iterative group registration template for cortical surface analysis. Neuroimage. 2007;34:1535–1544
  22. Matochik JA, Chefer SI, Lane MA, Woolf RI, Morris ED, Ingram DK, et al. Age-related decline in striatal volume in monkeys as measured by magnetic resonance imaging. Neurobiol. Aging. 2000;21:591–598
  23. McLaren DG, Kosmatka KJ, Oakes TR, Kroenke CD, Kohama SG, Matochik JA, et al. A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage. 2009;45:52–59
  24. Moss MB, Killiany RJ, Lai ZC, Rosene DL, Herndon JG. Recognition memory span in rhesus monkeys of advanced age. Neurobiol. Aging. 1997;18:13–19
  25. Moss MB, Rosene DL, Peters A. Effects of aging on visual recognition memory in the rhesus monkey. Neurobiol. Aging. 1988;9:495–502
  26. Narayan VM, Narr KL, Kumari V, Woods RP, Thompson PM, Toga AW, et al. Regional cortical thinning in subjects with violent antisocial personality disorder or schizophrenia. Am. J. Psychiatry. 2007;164:1418–1427
  27. Peters A, Moss MB, Sethares C. The effects of aging on layer 1 of primary visual cortex in the rhesus monkey. Cereb. Cortex. 2001;11:93–103
  28. Peters A, Sethares C. The effects of age on the cells in layer 1 of primate cerebral cortex. Cereb. Cortex. 2002;12:27–36
  29. Peters A, Sethares C, Moss MB. The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey. Cereb. Cortex. 1998;8:671–684
  30. Rakic P. Confusing cortical columns. Proc. Natl. Acad. Sci. U S A. 2008;105:12099–12100
  31. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex. 2005;15:1676–1689
  32. Raz N, Rodrigue KM. Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci. Biobehav. Rev. 2006;30:730–748
  33. Robbins S, Evans AC, Collins DL, Whitesides S. Tuning and comparing spatial normalization methods. Med. Image Anal. 2004;8:311–323
  34. Roth GS, Mattison JA, Ottinger MA, Chachich ME, Lane MA, Ingram DK. Aging in rhesus monkeys: relevance to human health interventions. Science. 2004;305:1423–1426
  35. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RS, Busa E, et al. Thinning of the cerebral cortex in aging. Cereb. Cortex. 2004;14:721–730
  36. Salat DH, Kaye JA, Janowsky JS. Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease. Arch. Neurol. 1999;56:338–344
  37. Salat DH, Lee SY, van der Kouwe AJ, Greve DN, Fischl B, Rosas HD. Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast. Neuroimage. 2009;48:21–28
  38. Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging. 1998;17:87–97
  39. Smith SM. Fast robust automated brain extraction. Hum. Brain Mapp. 2002;17:143–155
  40. Sowell ER, Peterson BS, Kan E, Woods RP, Yoshii J. Sex Differences in Cortical Thickness Mapped in 176 Healthy Individuals between 7 and 87 Years of age. Cereb. Cortex. 2007;17:1550–1560
  41. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW. Mapping cortical change across the human life span. Nat. Neurosci. 2003;6:309–315
  42. Styner M, Knickmeyer R, Joshi S, Coe C, Short SJ. Automatic Brain Segmentation in Rhesus Monkeys. Proceedings of the SPIE Medical Imaging. 2007;65:122;L1-8
  43. Tigges J, Gordon TP, McClure HM, Hall EC, Peters A. Survival rate and life span of rhesus monkeys at the Yerkes regional primate Research Center. Am. J. Primatol. 1988;15:263–273
  44. Van Essen DC, Lewis JW, Drury HA, Hadjikhani N, Tootell RB, Bakircioglu M, et al. Mapping visual cortex in monkeys and humans using surface-based atlases. Vis. Res. 2001;41:1359–1378
  45. Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT. Intrinsic functional architecture in the anaesthetized monkey brain. Nature. 2007;447:83–86
  46. Walhovd KB, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, et al. Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiol. Aging. 2009;June 29 [Epub ahead of print]
  47. Wisco JJ, Killiany RJ, Guttmann CR, Warfield SK, Moss MB, Rosene DL. An MRI study of age-related white and gray matter volume changes in the rhesus monkey. Neurobiol. Aging. 2008;29:1563–1575
  48. Zhang K, Sejnowski TJ. A universal scaling law between gray matter and white matter of cerebral cortex. Proc. Natl. Acad. Sci. U S A. 2000;97:5621–5626
  49. Ziegler DA, Piguet O, Salat DH, Prince K, Connally E, Corkin S. Cognition in healthy aging is related to regional white matter integrity, but not cortical thickness. Neurobiol. Aging. 2008;Dec 15 [Epub ahead of print]

PII: S0197-4580(10)00318-0

doi: 10.1016/j.neurobiolaging.2010.07.010

Neurobiology of Aging
Volume 33, Issue 1 , Pages 200.e23-200.e31 , January 2012