Regional heterogeneity in limbic maturational changes: Evidence from integrating cortical thickness, volumetric and diffusion tensor imaging measures

NeuroImage

Volumn 55, Issue 3, 2011, Pages 868-879

  Grieve, Stuart M ^a,b,c,d   Korgaonkar, Mayuresh S ^a   Clark, C Richard ^e   Williams, Leanne M ^a,c,d  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^c Brain Resource Company   (Australia)

^d Flinders University and Brain Health Clinics ^*  (United States)

^e FLINDERS UNIVERSITY   (Australia)

Author keywords

Aging; Cortical thickness; Diffusion tensor imaging; Limbic; Magnetic resonance imaging; Regional heterogeneity

Indexed keywords

ADOLESCENT; ADULT; AGE; AGED; AGING; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN MATURATION; BRAIN REGION; BRAIN SIZE; CHILD; COGNITION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; ENTORHINAL CORTEX; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; LIMBIC SYSTEM; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTERIOR CINGULATE; PRIORITY JOURNAL; RHOMBENCEPHALIC ISTHMUS; SCHOOL CHILD; VOLUNTEER; WHITE MATTER;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ANISOTROPY; CEREBRAL CORTEX; CHILD; DATABASES, FACTUAL; DIFFUSION TENSOR IMAGING; ENTORHINAL CORTEX; FEMALE; FORNIX, BRAIN; GYRUS CINGULI; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LIMBIC SYSTEM; MALE; MIDDLE AGED; NEURAL PATHWAYS; YOUNG ADULT;

EID: 79952070999     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.12.087     Document Type: Article

References (79)

1. Andersson J.L.R., Jenkinson M., Smith S.M. Non-linear optimisation FMRIB technical report TR07JA1 from. http://www.fmrib.ox.ac.uk/analysis/techrep.
2. Andersson J.L.R., Jenkinson M., Smith S.M. Non-linear registration, aka Spatial normalisation FMRIB technical report TR07JA2 from. http://www.fmrib.ox.ac.uk/analysis/techrep.
3. Apostolova L.G., Thompson P.M. Mapping progressive brain structural changes in early Alzheimer's disease and mild cognitive impairment. Neuropsychologia 2008, 46:1597-1612.
4. Ashburner J., Friston K.J. Voxel-based morphometry - the methods. Neuroimage 2000, 11:805-821.
5. Basser P.J., Mattiello J., LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B 1994, 103:247-254.
6. Beckmann M., Johansen-Berg H., Rushworth M.F. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 2009, 29:1175-1190.
7. Behrens T.E., Woolrich M.W., Jenkinson M., Johansen-Berg H., Nunes R.G., Clare S., Matthews P.M., Brady J.M., Smith S.M. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 2003, 50:1077-1088.
8. Bennett I.J., Madden D.J., Vaidya C.J., Howard D.V., Howard J.H. Age-related differences in multiple measures of white matter integrity: a diffusion tensor imaging study of healthy aging. Hum. Brain Mapp. 2010, 31:378-390.
9. Brickman A.M., Zimmerman M.E., Paul R.H., Grieve S.M., Tate D.F., Cohen R.A., Williams L.M., Clark C.R., Gordon E. Regional white matter and neuropsychological functioning across the adult lifespan. Biol. Psychiatry 2006, 60:444-453.
10. Cohen R.A., Grieve S., Hoth K.F., Paul R.H., Sweet L., Tate D., Gunstad J., Stroud L., McCaffery J., Hitsman B., Niaura R., Clark C.R., McFarlane A., Bryant R., Gordon E., Williams L.M. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol. Psychiatry 2006, 59:975-982.
11. Dale A.M., Sereno M.I. Improved Localization of Cortical Activity by Combining Eeg and Meg with Mri Cortical Surface Reconstruction - a Linear-Approach. J. Cogn. Neurosci. 1993, 5:162-176.
12. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194.
13. Desikan R.S., Segonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Buckner R.L., Dale A.M., Maguire R.P., Hyman B.T., Albert M.S., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
14. deToledo-Morrell L., Stoub T.R., Bulgakova M., Wilson R.S., Bennett D.A., Leurgans S., Wuu J., Turner D.A. MRI-derived entorhinal volume is a good predictor of conversion from MCI to AD. Neurobiol. Aging 2004, 25:1197-1203.
15. Dobson-Stone C., Gatt J.M., Kuan S.A., Grieve S.M., Gordon E., Williams L.M., Schofield P.R. Investigation of MCPH1 G37995C and ASPM A44871G polymorphisms and brain size in a healthy cohort. Neuroimage 2007, 37:394-400.
16. Fennema-Notestine C., McEvoy L.K., Hagler D.J., Jacobson M.W., Dale A.M., The Alzheimer's Disease Neuroimaging I. Structural neuroimaging in the detection and prognosis of pre-clinical and early AD. Behav. Neurol. 2009, 21:3-12.
17. Fischl B., Dale A.M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl Acad. Sci. USA 2000, 97:11050-11055.
18. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 1999, 9:195-207.
19. Fischl B., Sereno M.I., Tootell R.B., Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 1999, 8:272-284.
20. Fischl B., Liu A., Dale A.M. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans. Med. Imaging 2001, 20:70-80.
21. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., van der Kouwe A., Killiany R., Kennedy D., Klaveness S., Montillo A., Makris N., Rosen B., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
22. Fischl B., Salat D.H., van der Kouwe A.J., Makris N., Segonne F., Quinn B.T., Dale A.M. Sequence-independent segmentation of magnetic resonance images. Neuroimage 2004, 23(Suppl 1):S69-S84.
23. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D.H., Busa E., Seidman L.J., Goldstein J., Kennedy D., Caviness V., Makris N., Rosen B., Dale A.M. Automatically parcellating the human cerebral cortex. Cereb. Cortex 2004, 14:11-22.
24. Fjell A.M., Walhovd K.B., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Holland D., Brewer J.B., Dale A.M. One-year brain atrophy evident in healthy aging. J. Neurosci. 2009, 29(48):15223-15231.
25. Gatt J.M., Nemeroff C.B., Dobson-Stone C., Paul R.H., Bryant R.A., Schofield P.R., Gordon E., Kemp A.H., Williams L.M. Interactions between BDNF Val66Met polymorphism and early life stress predict brain and arousal pathways to syndromal depression and anxiety. Mol. Psychiatry 2009, 14:681-695.
26. Giorgio A., Watkins K.E., Douaud G., James A.C., James S., De Stefano N., Matthews P.M., Smith S.M., Johansen-Berg H. Changes in white matter microstructure during adolescence. Neuroimage 2008, 39:52-61.
27. Giorgio A., Watkins K.E., Chadwick M., James S., Winmill L., Douaud G., De Stefano N., Matthews P.M., Smith S.M., Johansen-Berg H., James A.C. Longitudinal changes in grey and white matter during adolescence. Neuroimage 2010, 49:94-103.
28. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl Acad. Sci. USA 2004, 101:8174-8179.
29. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
30. Gordon E., Cooper N., Rennie C., Hermens D., Williams L.M. Integrative neuroscience: the role of a standardized database. Clin. EEG Neurosci. 2005, 36:64-75.
31. Grieve S.M., Clark C.R., Williams L.M., Peduto A.J., Gordon E. Preservation of limbic and paralimbic structures in aging. Hum. Brain Mapp. 2005, 25:391-401.
32. Grieve S.M., Williams L.M., Paul R.H., Clark C.R., Gordon E. Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor MR imaging study. AJNR Am. J. Neuroradiol. 2007, 28:226-235.
33. Gunstad J., Paul R.H., Cohen R.A., Tate D.F., Spitznagel M.B., Grieve S., Gordon E. Relationship between body mass index and brain volume in healthy adults. Int. J. Neurosci. 2008, 118:1582-1593.
34. Han X., Jovicich J., Salat D., van der Kouwe A., Quinn B., Czanner S., Busa E., Pacheco J., Albert M., Killiany R., Maguire P., Rosas D., Makris N., Dale A., Dickerson B., Fischl B. Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 2006, 32:180-194.
35. Hickie I.B., Davenport T.A., Hadzi-Pavlovic D., Koschera A., Naismith S.L., Scott E.M., Wilhelm K.A. Development of a simple screening tool for common mental disorders in general practice. Med. J. Aust. 2001, 175(Suppl):S10-S17.
36. Jernigan T.L., Archibald S.L., Fennema-Notestine C., Gamst A.C., Stout J.C., Bonner J., Hesselink J.R. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging 2001, 22:581-594.
37. Joffe R.T., Gatt J.M., Kemp A.H., Grieve S., Dobson-Stone C., Kuan S.A., Schofield P.R., Gordon E., Williams L.M. Brain derived neurotrophic factor Val66Met polymorphism, the five factor model of personality and hippocampal volume: implications for depressive illness. Hum. Brain Mapp. 2009, 30:1246-1256.
38. Jones B.F., Barnes J., Uylings H.B., Fox N.C., Frost C., Witter M.P., Scheltens P. Differential regional atrophy of the cingulate gyrus in Alzheimer disease: a volumetric MRI study. Cereb. Cortex 2006, 16:1701-1708.
39. Jovicich J., Czanner S., Greve D., Haley E., van der Kouwe A., Gollub R., Kennedy D., Schmitt F., Brown G., Macfall J., Fischl B., Dale A. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage 2006, 30:436-443.
40. Lebel C., Walker L., Leemans A., Phillips L., Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 2008, 40:1044-1055.
41. Margulies D.S., Kelly A.M., Uddin L.Q., Biswal B.B., Castellanos F.X., Milham M.P. Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 2007, 37:579-588.
42. Marsh R., Gerber A.J., Peterson B.S. Neuroimaging studies of normal brain development and their relevance for understanding childhood neuropsychiatric disorders. J. Am. Acad. Child Adolesc. Psychiatry 2008, 47:1233-1251.
43. McLaughlin N.C., Paul R.H., Grieve S.M., Williams L.M., Laidlaw D., DiCarlo M., Clark C.R., Whelihan W., Cohen R.A., Whitford T.J., Gordon E. Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan. Int. J. Dev. Neurosci. 2007, 25:215-221.
44. Mori S., Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006, 51:527-539.
45. Mori S., Oishi K., Jiang H., Jiang L., Li X., Akhter K., Hua K., Faria A.V., Mahmood A., Woods R., Toga A.W., Pike G.B., Neto P.R., Evans A., Zhang J., Huang H., Miller M.I., van Zijl P., Mazziotta J. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008, 40:570-582.
46. Mu Q., Xie J., Wen Z., Weng Y., Shuyun Z. A quantitative MR study of the hippocampal formation, the amygdala, and the temporal horn of the lateral ventricle in healthy subjects 40 to 90years of age. AJNR Am. J. Neuroradiol. 1999, 20:207-211.
47. Paul R.H., Grieve S.M., Niaura R., David S.P., Laidlaw D.H., Cohen R., Sweet L., Taylor G., Clark R.C., Pogun S., Gordon E. Chronic cigarette smoking and the microstructural integrity of white matter in healthy adults: a diffusion tensor imaging study. Nicotine Tob. Res. 2008, 10:137-147.
48. Paul R., Grieve S.M., Chaudary B., Gordon N., Lawrence J., Cooper N., Clark C.R., Kukla M., Mulligan R., Gordon E. Relative contributions of the cerebellar vermis and prefrontal lobe volumes on cognitive function across the adult lifespan. Neurobiol. Aging 2009, 30:457-465.
49. Pennanen C., Kivipelto M., Tuomainen S., Hartikainen P., Hanninen T., Laakso M.P., Hallikainen M., Vanhanen M., Nissinen A., Helkala E.L., Vainio P., Vanninen R., Partanen K., Soininen H. Hippocampus and entorhinal cortex in mild cognitive impairment and early AD. Neurobiol. Aging 2004, 25:303-310.
50. Raz N., Gunning F.M., Head D., Dupuis J.H., McQuain J., Briggs S.D., Loken W.J., Thornton A.E., Acker J.D. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal grey matter. Cereb. Cortex 1997, 7:268-282.
51. Salat D.H., Kaye J.A., Janowsky J.S. Prefrontal grey and white matter volumes in healthy aging and Alzheimer disease. Arch. Neurol. 1999, 56:338-344.
52. Salat D.H., Kaye J.A., Janowsky J.S. Selective preservation and degeneration within the prefrontal cortex in aging and Alzheimer disease. Arch. Neurol. 2001, 58:1403-1408.
53. Salat D.H., Buckner R.L., Snyder A.Z., Greve D.N., Desikan R.S., Busa E., Morris J.C., Dale A.M., Fischl B. Thinning of the cerebral cortex in aging. Cereb. Cortex 2004, 14:721-730.
54. Salat D.H., Greve D.N., Pacheco J.L., Quinn B.T., Helmer K.G., Buckner R.L., Fischl B. Regional white matter volume differences in nondemented aging and Alzheimer's disease. Neuroimage 2009, 44:1247-1258.
55. Scahill R.I., Frost C., Jenkins R., Whitwell J.L., Rossor M.N., Fox N.C. A longitudinal study of brain volume changes in normal aging using serial registered Magnetic Resonance Imaging. Arch. Neurol. 2003, 60:989-994.
56. Schneider J.F., Vergesslich K. Maturation of the limbic system revealed by MR FLAIR imaging. Pediatr. Radiol. 2007, 37:351-355.
57. Schofield P.R., Williams L.M., Paul R.H., Gatt J.M., Brown K., Luty A., Cooper N., Grieve S., Dobson-Stone C., Morris C., Kuan S.A., Gordon E. Disturbances in selective information processing associated with the BDNF Val66Met polymorphism: evidence from cognition, the P300 and fronto-hippocampal systems. Biol. Psychol. 2009, 80:176-188.
58. Segonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., Fischl B. A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004, 22:1060-1075.
59. Shaw P., Kabani N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein D., Clasen L., Evans A., Rapoport J.L., Giedd J.N., Wise S.P. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 2008, 28:3586-3594.
60. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl 1):S208-S219.
61. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006, 31:1487-1505.
62. Sowell E.R., Thompson P.M., Tessner K.D., Toga A.W. Mapping continued brain growth and grey matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J. Neurosci. 2001, 21:8819-8829.
63. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nat. Neurosci. 2003, 6:309-315.
64. Sowell E.R., Thompson P.M., Toga A.W. Mapping changes in the human cortex throughout the span of life. Neuroscientist 2004, 10:372-392.
65. Sowell E.R., Peterson B.S., Kan E., Woods R.P., Yoshii J., Bansal R., Xu D., Zhu H., Thompson P.M., Toga A.W. Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87years of age. Cereb. Cortex 2007, 17:1550-1560.
66. Stadlbauer A., Salomonowitz E., Strunk G., Hammen T., Ganslandt O. Quantitative diffusion tensor fiber tracking of age-related changes in the limbic system. Eur. Radiol. 2008, 18:130-137.
67. Stadlbauer A., Salomonowitz E., Strunk G., Hammen T., Ganslandt O. Age-related degradation in the central nervous system: assessment with diffusion-tensor imaging and quantitative fiber tracking. Radiology 2008, 247(1):179-188.
68. Tamnes C.K., Ostby Y., Fjell A.M., Westlye L.T., Due-Tonnessen P., Walhovd K.B. Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 2010, 20:534-548.
69. Tapiola T., Pennanen C., Tapiola M., Tervo S., Kivipelto M., Hanninen T., Pihlajamaki M., Laakso M.P., Hallikainen M., Hamalainen A., Vanhanen M., Helkala E.L., Vanninen R., Nissinen A., Rossi R., Frisoni G.B., Soininen H. MRI of hippocampus and entorhinal cortex in mild cognitive impairment: a follow-up study. Neurobiol. Aging 2008, 29:31-38.
70. Tisserand D.J., Pruessner J.C., Sanz Arigita E.J., van Boxtel M.P., Evans A.C., Jolles J., Uylings H.B. Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 2002, 17:657-669.
71. Vogt B.A., Finch D.M., Olson C.R. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb. Cortex 1992, 2:435-443.
72. Whitford T.J., Rennie C.J., Grieve S.M., Clark C.R., Gordon E., Williams L.M. Brain maturation in adolescence: concurrent changes in neuroanatomy and neurophysiology. Hum. Brain Mapp. 2007, 28:228-237.
73. Williams L.M., Brown K.J., Palmer D., Liddell B.J., Kemp A.H., Olivieri G., Peduto A., Gordon E. The mellow years?: neural basis of improving emotional stability over age. J. Neurosci. 2006, 26:6422-6430.
74. Williams L.M., Das P., Liddell B.J., Kemp A.H., Rennie C.J., Gordon E. Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. J. Neurosci. 2006, 26:9264-9271.
75. Williams L.M., Gatt J.M., Hatch A., Palmer D.M., Nagy M., Rennie C., Cooper N.J., Morris C., Grieve S., Dobson-Stone C., Schofield P., Clark C.R., Gordon E., Arns M., Paul R.H. The integrate model of emotion, thinking and self regulation: an application to the "paradox of aging". J. Integr. Neurosci. 2008, 7:367-404.
76. Wolf H., Jelic V., Gertz H.J., Nordberg A., Julin P., Wahlund L.O. A critical discussion of the role of neuroimaging in mild cognitive impairment. Acta Neurol. Scand. Suppl. 2003, 179:52-76.
77. Yoshiura T., Noguchi T., Hiwatashi A., Togao O., Yamashita K., Nakao T., Nagao E., Kumazawa S., Arimura H., Honda H. Age-related microstructural changes in subcortical white matter during postadolescent periods in men revealed by diffusion-weighted MR imaging. Hum. Brain Mapp. 2009, 30:3142-3150.
78. Yuan W., Mangano F.T., Air E.L., Holland S.K., Jones B.V., Altaye M., Bierbrauer K. Anisotropic diffusion properties in infants with hydrocephalus: a diffusion tensor imaging study. AJNR Am. J. Neuroradiol. 2009, 30:1792-1798.
79. Zimmerman M.E., Brickman A.M., Paul R.H., Grieve S.M., Tate D.F., Gunstad J., Cohen R.A., Aloia M.S., Williams L.M., Clark C.R., Whitford T.J., Gordon E. The relationship between frontal grey matter volume and cognition varies across the healthy adult lifespan. Am. J. Geriatr. Psychiatry 2006, 14:823-833.