Gray matter responsiveness to adaptive working memory training: a surface-based morphometry study

Brain Structure and Function

Volumn 221, Issue 9, 2016, Pages 4369-4382

  Román, Francisco J ^a   Lewis, Lindsay B ^b   Chen, Chi Hua ^c   Karama, Sherif ^b   Burgaleta, Miguel ^d   Martínez, Kenia ^a,e   Lepage, Claude ^b   Jaeggi, Susanne M ^f   Evans, Alan C ^b   Kremen, William S ^c   Colom, Roberto ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain plasticity; Cognitive training; Cortical surface area; Cortical thickness; Surface based morphometry

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BRAIN CORTEX; COGNITIVE FUNCTION TEST; CONTROLLED STUDY; CORTICAL SURFACE AREA; CORTICAL THICKNESS (BRAIN); FEMALE; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; INFERIOR PARIETAL CORTEX; INTELLIGENCE; MIDDLE TEMPORAL CORTEX; MORPHOMETRICS; NERVOUS SYSTEM PARAMETERS; PARS OPERCULARIS; PRIORITY JOURNAL; TEMPORAL CORTEX; VENTRAL FRONTAL CORTEX; WORKING MEMORY; ANATOMY AND HISTOLOGY; BRAIN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; SHORT TERM MEMORY; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN; FEMALE; GRAY MATTER; HUMANS; INTELLIGENCE; MAGNETIC RESONANCE IMAGING; MEMORY, SHORT-TERM; YOUNG ADULT;

EID: 84951746933     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-015-1168-7     Document Type: Article

References (85)

1. Ad-Dab’bagh Y, Lyttelton O, Muehlboeck JS, Lepage C, Einarson D, Mok K, Ivanov O, Vincent RD, Lerch J, Fombonne E, Evans AC (2006) The CIVET image processing environment: A fully automated comprehensive pipeline for anatomical neuroimaging research. In: Corbetta M (ed) Proceedings of the 12th Annual Meeting of the Organization for Human Brain Mapping NeuroImage. Florence, Italy
2. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends in cognitive sciences 8:170–177
3. Au J, Sheehan E, Tsai N, Duncan GJ, Buschkuehl M, Jaeggi SM (2014) Improving fluid intelligence with training on working memory: a meta-analysis. Psychonomic bulletin and review, pp 1–12
4. Blanton RE, Levitt JG, Thompson PM, Narr KL, Capetillo-Cunliffe L, Nobel A, Toga AW (2001) Mapping cortical asymmetry and complexity patterns in normal children. Psychiatry Res Neuroimag 107:29–43
5. Bueti D, Lasaponara S, Cercignani M, Macaluso E (2012) Learning about time: plastic changes and interindividual brain differences. Neuron 75:725–737
6. Burgaleta M, Johnson W, Waber DP, Colom R, Karama S (2014) Cognitive ability changes and dynamics of cortical thickness development in healthy children and adolescents. NeuroImage 84:810–819
7. Burgess GC, Gray JR, Conway AR, Braver TS (2011) Neural mechanisms of interference control underlie the relationship between fluid intelligence and working memory span. J Exp Psychol Gen 140:674–692
8. Buschman TJ, Siegel M, Roy JE, Miller EK (2011) Neural substrates of cognitive capacity limitations. Proc Natl Acad Sci 108:11252–11255
9. Cabeza R (2002) Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging 17:85–100
10. Chance SA, Casanova MF, Switala AE, Crow TJ (2008) Auditory cortex asymmetry, altered minicolumn spacing and absence of ageing effects in schizophrenia. Brain 131:3178–3192
11. Chen CH, Gutierrez ED, Thompson W, Panizzon MS, Jernigan TL, Eyler LT, Dale AM (2012) Hierarchical genetic organization of human cortical surface area. Science 335:1634–1636
12. Chen CH, Fiecas M, Gutiérrez ED, Panizzon MS, Eyler LT, Vuoksimaa E, Kremen WS (2013) Genetic topography of brain morphology. Proc Natl Acad Sci 110:17089–17094
13. Chklovskii DB, Mel BW, Svoboda K (2004) Cortical rewiring and information storage. Nature 431:782–788
14. Cohen J (1992) A power primer. Psychol Bull 112:155–159
15. Colom R, Jung RE, Haier RJ (2007) General intelligence and memory span: evidence for a common neuroanatomic framework. Cognit Neuropsychol 24:867–878
16. Colom R, Quiroga M, Solana AB, Burgaleta M, Román FJ, Privado J, Karama S (2012) Structural changes after videogame practice related to a brain network associated with intelligence. Intelligence 40:479–489
17. Colom R, Burgaleta M, Román FJ, Karama S, Álvarez-Linera J, Abad FJ, Haier RJ (2013a) Neuroanatomic overlap between intelligence and cognitive factors: morphometry methods provide support for the key role of the frontal lobes. Neuroimage 72:143–152
18. Colom R, Román FJ, Abad FJ, Shih PC, Privado J, Froufe M, Jaeggi SM (2013b) Adaptive n-back training does not improve fluid intelligence at the construct level: Gains on individual tests suggest that training may enhance visuospatial processing. Intelligence 41:712–727
19. Deary IJ, Weiss A, Batty GD (2010) Intelligence and personality as predictors of illness and death how researchers in differential psychology and chronic disease epidemiology are collaborating to understand and address health inequalities. Psychol Sci Publ Interest 11:53–79
20. Draganski B, Kherif F (2013) In vivo assessment of use-dependent brain plasticity—beyond the “one trick pony” imaging strategy. NeuroImage 73:255–259
21. Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A (2004) Neuroplasticity: changes in grey matter induced by training. Nature 427:311–312
22. Draganski B, Gaser C, Kempermann G, Kuhn HG, Winkler J, Büchel C, May A (2006) Temporal and spatial dynamics of brain structure changes during extensive learning. J Neurosci 26(23):6314–6317
23. Duncan J, Owen AM (2000) Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475–483
24. Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth Ø, Larsen VA, Walhovd KB (2010) Effects of memory training on cortical thickness in the elderly. Neuroimage 52:1667–1676
25. Erickson KI (2013) Evidence for structural plasticity in humans: comment on Thomas and Baker (2012). NeuroImage 73:237–238
26. Feczko E, Augustinack JC, Fischl B, Dickerson BC (2009) An MRI-based method for measuring volume, thickness and surface area of entorhinal, perirhinal, and posterior parahippocampal cortex. Neurobiol Aging 30:420–431
27. Fields RD (2013) Changes in brain structure during learning: fact or artifact? Reply to Thomas and Baker. NeuroImage 73:260–264
28. Forstmann B, van den Wildenberg W, Ridderinkhof K (2008) Neural mechanisms, temporal dynamics, and individual differences in interference control. J Cogn Neurosci 20:1854–1865
29. Fu M, Zuo Y (2011) Experience-dependent structural plasticity in the cortex. Trends Neurosci 34:177–187
30. Haier RJ, Karama S, Leyba L, Jung RE (2009) MRI assessment of cortical thickness and functional activity changes in adolescent girls following three months of practice on a visual-spatial task. BMC Res Notes 2:174
31. Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT (2006) Brain connectivity related to working memory performance. J Neurosci 26:13338–13343
32. Hensch TK (2004) Critical period regulation. Ann Rev Neurosci 27:549–579
33. Hill J, Inder T, Neil J, Dierker D, Harwell J, Van Essen D (2010) Similar patterns of cortical expansion during human development and evolution. Proc Natl Acad Sci 107:13135–13140
34. Hsu NS, Buschkuehl M, Jonides J, Jaeggi SM (2013) Potential Mechanisms Underlying Working Memory Training and Transfer. Poster presented at the Psychonomic Society Annual Meeting, Toronto, Ontario
35. Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167–178
36. Jack CR, Bernstein MA, Fox NC, Thompson P, Alexander G, Harvey D, Weiner MW (2008) The Alzheimer’s disease neuroimaging initiative (ADNI): MRI methods. J Magn Reson Imaging 27:685–691
37. Jaeggi SM, Buschkuehl M, Jonides J, Perrig WJ (2008) Improving fluid intelligence with training on working memory. Proc Natl Acad Sci 105:6829–6833
38. Jaeggi SM, Buschkuehl M, Perrig WJ, Meier B (2010) The concurrent validity of the N-back task as a working memory measure. Memory 18:394–412
39. Jaeggi SM, Buschkuehl M, Jonides J, Shah P (2011) Short-and long-term benefits of cognitive training. Proc Natl Acad Sci 108:10081–10086
40. Jaeggi SM, Buschkuehl M, Shah P, Jonides J (2014) The role of individual differences in cognitive training and transfer. Memory Cognition 42:464–480
41. Jung RE, Haier RJ (2007) The Parieto-frontal integration theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30:135–154
42. Karama S, Bastin ME, Murray C, Royle NA, Penke L, Maniega SM, Deary IJ (2014) Childhood cognitive ability accounts for associations between cognitive ability and brain cortical thickness in old age. Molecular psychiatry 19:555–559
43. Karnath HO (2001) New insights into the functions of the superior temporal cortex. Nat Rev Neurosci 2:568–576
44. Kim JS, Singh V, Lee JK, Lerch J, Ad-Dab’bagh Y, MacDonald D, Evans AC (2005) Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage 27:210–221
45. Kirkwood T, Bond J, May C, McKeith I, Teh M (2008) Foresight mental capital and wellbeing project. Mental capital through life: Future challenges. The Government Office for Science, London
46. Kirwan CB, Stark CE (2007) Overcoming interference: An fMRI investigation of pattern separation in the medial temporal lobe. Learn Memory 14:625–633
47. Knudsen E (2004) Sensitive periods in the development of the brain and behavior. Cognit Neurosci J 16:1412–1425
48. Kwok V, Niu Z, Kay P, Zhou K, Mo L, Jin Z, Tan LH (2011) Learning new color names produces rapid increase in gray matter in the intact adult human cortex. Proc Natl Acad Sci 108:6686–6688
49. 18F] flumazenil-PET. Neuroimage 56:951–960
50. Landi SM, Baguear F, Della-Maggiore V (2011) One week of motor adaptation induces structural changes in primary motor cortex that predict long-term memory 1 year later. J Neurosci 31:11808–11813
51. Lerch JP, Yiu AP, Martinez-Canabal A, Pekar T, Bohbot VD, Frankland PW, Sled JG (2011) Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. Neuroimage 54:2086–2095
52. Lustig C, Shah P, Seidler R, Reuter-Lorenz PA (2009) Aging, training, and the brain: a review and future directions. Neuropsychol Rev 19:504–522
53. Lyttelton OC, Karama S, Ad-Dab’bagh Y, Zatorre RJ, Carbonell F, Worsley K, Evans AC (2009) Positional and surface area asymmetry of the human cerebral cortex. Neuroimage 46:895–903
54. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
55. Østby Y, Tamnes CK, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2009) Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J Neurosci 29:11772–11782
56. Panizzon MS, Fennema-Notestine C, Eyler LT, Jernigan TL, Prom-Wormley E, Neale M, Kremen WS (2009) Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex, bhp026
57. Paus T (2010) Growth of white matter in the adolescent brain: myelin or axon? Brain Cogn 72:26–35
58. Petanjek Z, Judaš M, Kostović I, Uylings HB (2008) Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. Cereb Cortex 18:915–929
59. Prabhakaran V, Rypma B, Narayanan NS, Meier TB, Austin BP, Nair VA, Gabrieli JD (2011) Capacity-speed relationships in prefrontal cortex. PLoS One 6:e27504
60. Rakic P (1988) Specification of cerebral cortical areas. Science 24:170–176
61. Raznahan A, Shaw P, Lalonde F, Stockman M, Wallace GL, Greenstein D, Giedd JN (2011) How does your cortex grow? J Neurosci 31:7174–7177
62. Reuter-Lorenz PA, Jonides J, Smith EE, Hartley A, Miller A, Marshuetz C, Koeppe RA (2000) Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci 12:174–187
63. Rimol LM, Panizzon MS, Fennema-Notestine C, Eyler LT, Fischl B, Franz CE, Dale AM (2010) Cortical thickness is influenced by regionally specific genetic factors. Biol Psychiatry 67:493–499
64. Román FJ, Abad FJ, Escorial S, Burgaleta M, Martínez K, Álvarez-Linera J, Colom R (2014) Reversed hierarchy in the brain for general and specific cognitive abilities: A morphometric analysis. Hum Brain Mapp 35:3805–3818
65. Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Eickhoff SB (2012) Modelling neural correlates of working memory: a coordinate-based meta-analysis. Neuroimage 60:830–846
66. Schnack HG, van Haren NEM, Brouwer RM, Evans A, Durston S, Hulshoff Pol HH (2015) Changes in thickness and surface area of the human cortex and their relationship with intelligence. Cereb Cortex 25:1608–1617
67. Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Giedd J (2006) Intellectual ability and cortical development in children and adolescents. Nature 440:676–679
68. Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310:805–810
69. Takeuchi H, Sekiguchi A, Taki Y, Yokoyama S, Yomogida Y, Komuro N, Kawashima R (2010) Training of working memory impacts structural connectivity. J Neurosci 30:3297–3303
70. Thomas C, Baker CI (2013a) Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans. Neuroimage 73:225–236
71. Thomas C, Baker CI (2013b) On evidence, biases and confounding factors: Response to commentaries. NeuroImage 73:265–267
72. Thomas AG, Marrett S, Saad ZS, Ruff DA, Martin A, Bandettini PA (2009) Functional but not structural changes associated with learning: an exploration of longitudinal voxel-based morphometry (VBM). Neuroimage 48:117–125
73. Thompson PM, Hayashi KM, Dutton RA, Chiang MC, Leow AD, Sowell ER, Toga AW (2007) Tracking Alzheimer’s disease. Ann N Y Acad Sci 1097:183–214
74. Vendetti MS, Bunge SA (2014) Evolutionary and developmental changes in the lateral frontoparietal network: a little goes a long way for higher-level cognition. Neuron 84:906–917
75. Vuoksimaa E, Panizzon MS, Chen CH, Fiecas M, Eyler LT, Fennema-Notestine C, 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
76. Wierenga LM, Langen M, Oranje B, Durston S (2014) Unique developmental trajectories of cortical thickness and surface area. NeuroImage 87:120–126
77. Woollett K, Maguire EA (2011) Acquiring “the Knowledge” of London’s layout drives structural brain changes. Curr Biol 21:2109–2114
78. World Medical Association (2008) Declaration of Helsinki—ethical principles for medical research involving human subjects, 59th WMA General Assembly. Seoul, Korea
79. Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515–525
80. Yassa MA, Mattfeld AT, Stark SM, Stark CE (2011) Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proc Natl Acad Sci 108:8873–8878
81. Zhang Q, Buschkuehl M, Bernat E, Jaeggi SM (2014) EEG power changes as a function of working memory training. Poster presented at the 26th Annual Convention of the Association for Psychological Science, San Francisco
82. Zhou D, Lebel C, Evans A, Beaulieu C (2013) Cortical thickness asymmetry from childhood to older adulthood. NeuroImage 83:66–74
83. Zhou D, Lebel C, Treit S, Evans A, Beaulieu C (2015) Accelerated longitudinal cortical thinning in adolescence. NeuroImage 104:138–145
84. Zilles K, Amunts K (2012) Segregation and wiring in the brain. Science 335:1582–1584
85. Zou Q, Ross TJ, Gu H, Geng X, Zuo XN, Hong LE, Yang Y (2013) Intrinsic resting-state activity predicts working memory brain activation and behavioral performance. Hum Brain Mapp 34:3204–3215