Brain cortical characteristics of lifetime cognitive ageing

Brain Structure and Function

Volumn 223, Issue 1, 2018, Pages 509-518

  Cox, Simon R ^a,b   Bastin, Mark E ^a,b   Ritchie, Stuart J ^a   Dickie, David Alexander ^a,b   Liewald, Dave C ^a   Muñoz Maniega, Susana ^a,b   Redmond, Paul ^a   Royle, Natalie A ^a,b   Pattie, Alison ^a   Valdés Hernández, Maria ^a,b   Corley, Janie ^a   Aribisala, Benjamin S ^a,c   McIntosh, Andrew M ^a   Wardlaw, Joanna M ^a,b   Deary, Ian J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Scottish Imaging Network   (United Kingdom)

^c LAGOS STATE UNIVERSITY   (Nigeria)

Author keywords

Ageing; Cortex; Intelligence; MRI; Surface area; Thickness

Indexed keywords

ADOLESCENT; ADULT; AGED; ANTERIOR CINGULATE; ARTICLE; BRAIN CORTEX; BRAIN SIZE; CHILD; COGNITIVE AGING; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DORSOLATERAL PREFRONTAL CORTEX; ENTORHINAL CORTEX; FEMALE; FRONTAL CORTEX; FUSIFORM GYRUS; HUMAN; INFERIOR FRONTAL GYRUS; INFERIOR TEMPORAL CORTEX; INTELLIGENCE; MAJOR CLINICAL STUDY; MALE; MEDIAL TEMPORAL LOBE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PARIETAL CORTEX; PHENOTYPE; PRIORITY JOURNAL; SURFACE AREA; TEMPORAL CORTEX; AGING; BRAIN MAPPING; COGNITION; DIAGNOSTIC IMAGING; IMAGE PROCESSING; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGING; BRAIN MAPPING; CEREBRAL CORTEX; CHILD; COGNITION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; YOUNG ADULT;

EID: 85028831818     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-017-1505-0     Document Type: Article

References (70)

1. Barbey AK, Colom R, Solomon J, Krueger F, Forbes C, Grafman J (2012) An integrative architecture for general intelligence and executive function revealed by lesion mapping. Brain 135:1145–1164
2. Bárrios H, Narciso S, Guerreiro M, Maroco J, Logsdon R, de Mendonça A (2013) Quality of life in patients with mild cognitive impairment. Aging Ment Health 17:287–292
3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
4. Chen C-H, Pen Q, Schork AJ, Lo M-T, Fan C-C, Wang Y, Desikan RS, Bettella F, Pediatric Imaging, Neurocognition and Genetics Study, Alzheimer’s Disease Neuroimaging Initiative, Hagler DJ, Westlye LT, Kremen WS, Jernigan TL, Le Hellard S, Steen VM, Espeseth T, Huentelman M, Håberg AK, Agartz I, Djurovic S, Andreassen OE, Schork N, Dale AM (2015) Large-scale genomics unveil polygenic architecture of human cortical surface area. Nat Commun 6:7549
5. Colom R, Karama S, Jung RE, Haier RJ (2010) Human intelligence and brain networks. Dialogues Clin Neurosci 12:489–501
6. Cox SR, Ferguson KJ, Royle NA, Shenkin SD, MacPherson SE, MacLullich AMJ, Deary IJ, Wardlaw JM (2014) A systematic review of brain frontal lobe parcellation techniques in Magnetic Resonance Imaging. Brain Struct Funct 219:1–22
7. Cox SR, Ritchie SJ, Tucker-Drob EM, Liewald DC, Hagenaars SP, Davies G, Wardlaw JM, Gale CR, Bastin ME, Deary IJ (2016a) Ageing and brain white matter structure in 3513 UK Biobank participants. Nat Commun 7:13629
8. Cox SR, Dickie DA, Ritchie SJ, Karama S, Pattie A, Royle NA, Corley J, Aribisala BS, Valdés Hernández MC, Muñoz Maniega S, Starr JM, Bastin ME, Evans AC, Wardlaw JM, Deary IJ (2016b) Associations between education and brain structure at age 73 years, adjusted for age 11 IQ. Neurology 87:1820–1826
9. Deary IJ (2014) The stability of intelligence from childhood to old age. Curr Dir Psychol Sci 23:239–245
10. Deary IJ, Whalley LJ, Lemmon H, Crawford JR, Starr JM (2000) The stability of individual differences in mental ability from childhood to old age: follow-up of the 1932 Scottish Mental Survey. Intelligence 28:49–55
11. Deary IJ, Gow AJ, Taylor MD, Corley J, Brett C, Wilson V, Campbell H, Whalley LJ, Visscher PM, Porteous DJ, Starr JM (2007) The Lothian Birth Cohort 1936: a study to examine influences on cognitive ageing from age 11 to age 70 and beyond. BMC Geriatr 7:28
12. Deary IJ, Penke L, Johnson W (2010) The neuroscience of human intelligence differences. Nat Rev Neurosci 11:201–211
13. Deary IJ, Gow AJ, Pattie A, Starr JM (2012) Cohort profile: the Lothian Birth Cohorts of 1921 and 1936. Int J Epidemiol 41:1576–1584
14. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980
15. Dickerson BC, Feczko E, Augustinack JC, Pacheco J, Morris JC, Fischl B, Buckner RL (2009) Differential effects of aging and Alzheimer’s disease on medial temporal lobe cortical thickness and surface area. Neurobiol Aging 30:432–440
16. Dickie DA, Mikhael S, Job DE, Wardlaw JM, Laidlaw DH, Bastin ME (2015) Permutation and parametric tests for effect sizes in voxel-based morphometry of gray matter volume in structural MRI. Magn Reson Imaging 33:1299–1305
17. Dickie DA, Karama S, Ritchie SJ, Cox SR, Sakka E, Royle NA, Aribisala BS, Valdés Hernández MC, Muñoz Maniega S, Pattie A, Corley J, Starr JM, Bastin ME, Evans AC, Deary IJ, Wardlaw JM (2016) Progression of white matter disease and cortical thinning are not related in older community-dwelling subjects. Stroke 47:410–416
18. Dotson VM, Szymkowitz SM, Sozda CN, Kirton JW, Green ML, O’Shea A, McLaren ME, Anton SD, Manini TM, Woods AJ (2015) Age differences in prefrontal surface area and thickness in middle aged to older adults. Font Aging Neurosci 7:250
19. Eyler LT, Chen CH, Panizzon MS, Fennema-Notestine C, Neale MC, Jak A, Jernigan TL, Fischl B, Franz CE, Lyons MJ, Grant M, Prom-Wormley E, Seidman LJ, Tsuang MT, Fiecas MJ, Dale AM, Kremen WS (2012) A comparison of heritability maps of cortical surface area and thickness and the influence of adjustment for whole brain measures: a magnetic resonance imaging twin study. Twin Res Hum Genet 15:304–314
20. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci 97:11050–11055
21. Fischl B, Sereno MI, Dale AM (1999a) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207
22. Fischl B, Sereno MI, Tootell RB, Dale AM (1999b) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272–284
23. Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20:70–80
24. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22
25. Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB (2009) High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19:2001–2012
26. Fjell AM, Westlye LT, Grydeland H, Amlien I, Espeseth T, Reinvang I, Raz N, Dale AM, Walhovd KB, Alzheimer Disease Neuroimaging Initiative (2014) Accelerating cortical thinning: unique to dementia or universal in aging? Cereb Cortex 24:919–934
27. Fleischman DA, Leurgans S, Arfanakis K, Arvanitakis Z, Barnes LL, Boyle PA, Han SD, Bennett DA (2014) Gray-matter macrostructure in cognitively healthy older persons: associations with age and cognition. Brain Struct Funct 219:2029–2049
28. Folstein MF, Folstein SE, McHugh PR (1975) Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiat Res 12:189–198
29. Hedden T, Gabrieli JD (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci 5:87–96
30. Hedman AM, van Haren NEM, van Baal CM, Brouwer RM, Brans RGH, Schnack HG, Kahn RS, Hulshoff Pol HE (2016) Heritability of cortical thickness changes over time in twin pairs discordant for schizophrenia. Schizophr Res 173:192–199
31. Hofer SM, Sliwinski MJ (2001) Understanding ageing. An evaluation of research designs for assessing the interdependence of ageing-related changes. Gerontology 47:341–352
32. Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM (2013) The structure of the cerebral cortex across adult life: age related patterns of surface area, thickness and gyrification. Cereb Cortex 23:2521–2530
33. Im K, Lee J-M, Lyttelton O, Kim SH, Evans AC, Kim SI (2008) Brain size and cortical structure in the adult human brain. Cereb Cortex 18:2181–2191
34. Jensen A (1998) The g factor. Praeger, Westpost
35. Jiang J, Sachdev P, Lipnicki DM, Zhang H, Liu T, Zhu W, Suo C, Zhuang L, Crawford J, Reppermund S, Trollor J, Brodaty H, Wen W (2014) A longitudinal study of brain atrophy over two years in community-dwelling older individuals. Neuroimage 86:203–211
36. Johnson W, te Nijenhuis J, Bouchard TJ Jr (2008) Still just 1 g: consistent results from five test batteries. Intelligence 36:81–95
37. Jung RE, Haier RJ (2007) The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30:135–154
38. Karama S, Bastin ME, Murray C, Royle NA, Penke L, Muñoz Maniega S, Gow AJ, Corley J, Valdés Hernández MC, Lewis JD, Rousseau M-É, Lepage C, Fonov V, Collins SL, Booth T, Rioux P, Sherif T, Adalat R, Starr JM, Evans AC, Wardlaw JM, Deary IJ (2014) Childhood cognitive ability accounts for associations between cognitive ability and brain cortical thickness in old age. Mol Psychiatry 19:555–559
39. Lemaitre H, Goldman AL, Sambataro F, Verchinski BA, Meyer-Lindberg A, Weinberger DR, Mattay VS (2012) Normal age-related brain morphometric changes: nonuniformity across cortical thickness, surface area and gray matter volume? Neurobiol Aging 33:617. e1–9
40. Matthews F, Brayne C (2005) The incidence of dementia in England and Wales: findings from the five identical sites of the MRC CFA Study. PLoS Med 2:e193
41. McGinnis SM, Brickhouse M, Pascual B, Dickerson BC (2011) Age-related changes in the thickness of cortical zones in humans. Brain Topogr 24:279–291
42. Nygaard GO, Walhovd KB, Sowa P, Chepkoech J-L, Björnerud A, Due-Tönnessen P, Landrø NI, Damangir S, Spulber G, Storsve AB, Beyer MK, Fjell AM, Celuis EG, Harbo HF (2015) Cortical thickness and surface area relate to specific symptoms in early relapsing-remitting multiple sclerosis. Mult Scler 21:402–414
43. Pakkenberg G, Gunderson HJ (1997) Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 384:312–320
44. Panizzon MS, Fennema-Notestine C, Eyler LT, Jernigan TL, Prom-Wormley E, Neale M, Jacobson K, Lyons MJ, Grant MD, Franz CE, Xian H, Tsuang M, Fischl B, Seidman L, Dale AM, Kremen WS (2009) Distinct genetic influences on cortical surface area and cortical thickness. Cereb Cortex 19:2728–2735
45. Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Osftedal MB, Burke JR, Hurd MD, Potter GG, Rodgers WL, Steffens DC, McArdle JJ, Willis RJ, Wallace RB (2008) Prevalence of cognitive impairment without dementia in the United States. Ann Intern Med 148:427–434
46. Raz N, Rodrigue KM (2006) Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev 30:730–748
47. Raznahan A, Shaw P, Lalonde F, Stockman M, Wallace GL, Greenstein D, Clasen L, Gogtay N, Giedd JN (2011) How does your cortex grow? J Neurosci 31:7174–7177
48. Ritchie SJ, Dickie DA, Cox SR, Valdés Hernández MC, Corley J, Royle NA, Pattie A, Aribisala BS, Redmond P, Muñoz Maniega S, Taylor AM, Sibbett R, Gow AJ, Starr JM, Bastin ME, Wardlaw JM, Deary IJ (2015a) Hum Brain Mapp 36:4910–4925
49. Ritchie SJ, Bastin ME, Tucker-Drob EM, Muñoz Maniega S, Engelhardt LE, Cox SR, Royle NA, Gow AJ, Corley J, Pattie A, Taylor AM, Valdés Hernández MC, Starr JM, Wardlaw JM, Deary IJ (2015b) Coupled changes in brain white matter microstructure and fluid intelligence in later life. J Neurosci 35:8672–8682
50. Royle NA, Booth T, Valdés Hernández MC, Penke L, Murray C, Gow AJ, Muñoz Maniega S, Starr JM, Bastin ME, Deary IJ, Wardlaw JM (2013) Estimated maximal and current brain volume predict cognitive ability in old age. Neurobiol Aging 34:2726–2733
51. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RSR, Busa E, Morris JC, Dale AM, Fischl B (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14:721–730
52. Salthouse TA (2004) Localizing age-related individual differences in a hierarchical structure. Intelligence. doi:10.1016/j.intell.2004.07.003
53. Salthouse TA (2011) Neuroanatomical substrates of age-related cognitive decline. Psychol Bull 137:753–784
54. Schnack HG, van Haren NEM, Brouwer RM, Evans AC, Durston S, Boomsma DI, Kahn RS, Hulshoff Pol HE (2015) Changes in thickness and surface area of the human cortex and their relationship with intelligence. Cereb Cortex 25:1608–1617
55. Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22:1060–1075
56. Segonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26:518–529
57. Singh-Manoux A, Kivimaki M, Glymour MM, Elbaz A, Berr C, Ebmeier KP, Ferrie JE, Dugravot A (2012) Timing of onset of cognitive decline: results from Whitehall II prospective cohort study. BMJ 344:d7622
58. Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97
59. Storsve AB, Fjell AM, Tamnes CK, Westlye LT, Overbye K, Aasland HW, Walhovd KB (2014) Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change. J Neurosci 34:8488–8498
60. Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534–548
61. Tucker-Drob EM (2011) Neurocognitive functions and everyday functions change together in old age. Neuropsychology 25:368–377
62. Tucker-Drob EM, Briley DA, Starr JM, Deary IJ (2014) Structure and correlates of cognitive aging in a narrow age cohort. Psychol Aging 29:236–249
63. Valdés Hernández MC, Ferguson KJ, Chappell FM, Wardlaw JM (2010) New multispectral MRI data fusion technique for white matter lesion segmentation: method and comparison with thresholding in FLAIR images. Eur Radiol 20:1684–1691
64. Vuoksimaa E, Panizzon MS, Chen CH, Fiecas M, Eyler LT, Fennema-Notestine C, Hagler DJ, Fischl B, Franz CE, Jak A, Lyons MJ, Neale MC, Rinker DA, Thompson WK, Tsuang MT, Dale AM, Kremen WS (2015) The genetic association between neocortical volume and general cognitive ability is driven by global surface area rather than thickness. Cereb Cortex 25:2127–2137
65. Walhovd KB, Krogsrud SK, Amlien IK, Bartsch H, Bjornerud A, Due-Tonnessen P, Grydeland H, Hagler DJ Jr, Haberg AK, Kremen WS, Ferschmann L, Nyberg L, Panizzon MS, Rohani DA, Skranes J, Storsve AB, Solsnes AE, Tamnes CK, Thompson WK, Reuter C, Dale AM, Fjell AM (2016) Neurodevelopmental origins of lifespan changes in brain and cognition. Proc Natl Acad Sci USA 113:9357–9362
66. Wang X, Valdés Hernández MC, Doubal F, Chappell FM, Wardlaw JM (2012) How much do focal infarcts distort white matter lesions and global cerebral atrophy measures? Cerebrovasc Dis 34:336–342
67. Wardlaw JM, Bastin ME, Valdés Hernández MC, Maniega SM, Royle NA, Morris Z, Clayden JD, Sandeman EM, Eadie E, Murray C, Starr JM, Deary IJ (2011) Brain aging, cognition in youth and old age and vascular disease in the Lothian Birth Cohort 1936: rationale, design and methodology of the imaging protocol. Int J Stroke 6:547–559
68. Wechsler D (1998) WAIS-III-UK Administration and Scoring Manual. Psychological Corporation, London
69. Winkler AM, Kochunov P, Blangero J, Almasy L, Zilles K, Fox PT, Duggirala R, Glahn DC (2010) Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 53:1135–1146
70. Ziegler G, Dahnke R, Jänke L, Yotter RA, May A, Gaser C (2012) Brain structural trajectories over the adult lifespan. Hum Brain Mapp 33:2377–2389