Decoding episodic memory in ageing: A Bayesian analysis of activity patterns predicting memory

NeuroImage

Volumn 59, Issue 2, 2012, Pages 1772-1782

  Morcom, Alexa M ^a,b   Friston, Karl J ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Ageing; Compensation; Decoding; Dedifferentiation; Episodic memory; FMRI; Lateralisation; Multivariate; Over recruitment; Prefrontal cortex

Indexed keywords

ADULT; AGED; AGING; ANTERIOR INFERIOR FRONTAL GYRUS; ARTICLE; BAYES THEOREM; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; EPISODIC MEMORY; FEMALE; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; LATERAL PREFRONTAL CORTEX; MALE; MIDDLE FRONTAL GYRUS; NORMAL HUMAN; PREDICTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE;

ADOLESCENT; ADULT; AGED; AGING; BAYES THEOREM; CEREBRAL CORTEX; COMPUTER SIMULATION; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; MIDDLE AGED; MODELS, NEUROLOGICAL; PATTERN RECOGNITION, AUTOMATED; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 83055181197     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.08.071     Document Type: Article

References (105)

1. Aizenstein H.J., Clark K.A., Butters M.A., Cochran J., Stenger V.A., Meltzer C.C., Reynolds C.F., Carter C.S. The BOLD hemodynamic response in healthy aging. J. Cogn. Neurosci. 2004, 16:786-793.
2. Anderson N.D., Iidaka T., Cabeza R., Kapur S., McIntosh A.R., Craik F.I. The effects of divided attention on encoding- and retrieval-related brain activity: a PET study of younger and older adults. J. Cogn. Neurosci. 2000, 12:775-792.
3. Ashburner J., Friston K.J. Nonlinear spatial normalization using basis functions. Hum. Brain Mapp. 1999, 7:254-266.
4. Backman L., Almkvist O., Andersson J., Nordberg A., Winblad B., Reineck R., Langstrom B. Brain activation in young and old adults during implicit and explicit retrieval. J. Cogn. Neurosci. 1997, 9:378-391.
5. Bamford S.A., Murray A.F., Willshaw D.J. Synaptic rewiring for topographic mapping and receptive field development. Neural Netw. 2010 2010, 517-527. Elsevier Ltd., United States.
6. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 2002, 17:85-100.
7. Cabeza R., Grady C.L., Nyberg L., McIntosh A.R., Tulving E., Kapur S., Jennings J.M., Houle S., Craik F.I.M. Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J. Neurosci. 1997, 17(1):391-400.
8. Cabeza R., Anderson N.D., Locantore J.K., McIntosh A.R. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 2002, 17:1394-1402.
9. Cabeza R., Daselaar S.M., Dolcos F., Prince S.E., Budde M., Nyberg L. Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb. Cortex 2004, 14:364-375.
10. Cappell K.A., Gmeindl L., Reuter-Lorenz P.A. Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load. Cortex 2009, 462-473. Elsevier Srl, Italy.
11. Carp J., Gmeindl L., Reuter-Lorenz P.A. Age differences in the neural representation of working memory revealed by multi-voxel pattern analysis. Front. Hum. Neurosci. 2010, 4:217.
12. Carp J., Park J., Polk T.A., Park D.C. Age differences in neural distinctiveness revealed by multi-voxel pattern analysis. Neuroimage 2010, 56:736-743.
13. Chklovskii D.B., Koulakov A.A. Maps in the brain: what can we learn from them?. Annu. Rev. Neurosci. 2004, 27:369-392.
14. Clark D., Wagner A.D. Assembling and encoding word representations: fMRI subsequent memory effects implicate a role for phonological control. Neuropsychologia 2003, 41:304-317.
15. Cruz L., Roe D.L., Urbanc B., Inglis A., Stanley H.E., Rosene D.L. Age-related reduction in microcolumnar structure correlates with cognitive decline in ventral but not dorsal area 46 of the rhesus monkey. Neuroscience 2009, 1509-1520. United States.
16. Dahl C.D., Logothetis N.K., Kayser C. Spatial organization of multisensory responses in temporal association cortex. J. Neurosci. 2009, 11924-11932. United States.
17. Davis S.W., Dennis N.A., Daselaar S.M., Fleck M.S., Cabeza R. Que PASA? The posterior -anterior shift in aging. Cereb. Cortex 2008, 18:1201-1209.
18. Dennis N.A., Hayes S.M., Prince S.E., Madden D.J., Huettel S.A., Cabeza R. Effects of aging on the neural correlates of successful item and source memory encoding. J. Exp. Psychol. Learn. Mem. Cogn. 2008, 34:791-808.
19. D'Esposito M., Zarahn E., Aguirre G.K., Rypma B. The effect of normal aging on the coupling of neural activity to the bold hemodynamic response. Neuroimage 1999, 10:6-14.
20. Duncan J. An adaptive coding model of neural function in prefrontal cortex. Nat. Rev. Neurosci. 2001, 820-829. England.
21. Duverne S., Habibi A., Rugg M.D. Regional specificity of age effects on the neural correlates of episodic retrieval. Neurobiol. Aging 2008, 29:1902-1916.
22. Duverne S., Motamedinia S., Rugg M.D. The relationship between aging, performance, and the neural correlates of successful memory encoding. Cereb. Cortex 2009, 19:733-744.
23. Fernandes M.A., Pacurar A., Moscovitch M., Grady C. Neural correlates of auditory recognition under full and divided attention in younger and older adults. Neuropsychologia 2006, 44:2452-2464.
24. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S.J. Comparing functional (PET) images: the assessment of significant change. J. Cereb. Blood Flow Metab. 1991, 11:690-699.
25. Friston K.J., Glaser D.E., Henson R.N., Kiebel S., Phillips C., Ashburner J. Classical and Bayesian inference in neuroimaging: applications. Neuroimage 2002, 16:484-512.
26. Friston K., Mattout J., Trujillo-Barreto N., Ashburner J., Penny W. Variational free energy and the Laplace approximation. Neuroimage 2007, 220-234. United States.
27. Friston K., Chu C., Mourao-Miranda J., Hulme O., Rees G., Penny W., Ashburner J. Bayesian decoding of brain images. Neuroimage 2008, 39:181-205.
28. Goh J.O., Suzuki A., Park D.C. Reduced neural selectivity increases fMRI adaptation with age during face discrimination. Neuroimage 2010, 51:336-344.
29. Grady C.L., Haxby J.V. Functional neuroimaging of the aging brain. Handbook of Neuropsychology 1995, 467-481. Elsevier Sciences, Amsterdam. F. Boller, J. Grafman (Eds.).
30. Grady C.L., Maisog J.M., Horwitz B., Ungerleider L.G., Mentis M.J., Salerno J.A., Pietrini P., Wagner E., Haxby J.V. Age-related changes in cortical blood flow activation during visual processing of faces and location. Journal of Neuroscience 1994, 14:1450-1462.
31. Grady C.L., McIntosh A.R., Rajah M.N., Beig S., Craik F.I. The effects of age on the neural correlates of episodic encoding. Cereb. Cortex 1999, 9:805-814.
32. Grady C.L., Bernstein L.J., Beig S., Siegenthaler A.L. The effects of encoding task on age-related differences in the functional neuroanatomy of face memory. Psychol. Aging 2002, 17:7-23.
33. Grady C.L., McIntosh A.R., Craik F.I. Task-related activity in prefrontal cortex and its relation to recognition memory performance in young and old adults. Neuropsychologia 2005, 43:1466-1481.
34. Greenhouse G.W., Geisser S. On methods in the analysis of repeated measures designs. Psychometrika 1959, 49:95-112.
35. Gur R.E., Chin S. Laterality in functional brain imaging studies of schizophrenia. Schizophr. Bull. 1999, 25:141-156.
36. Gutchess A.H., Welsh R.C., Hedden T., Bangert A., Minear M., Liu L.L., Park D.C. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial -temporal activity. J. Cogn. Neurosci. 2005, 17:84-96.
37. Haynes J.D., Rees G. Decoding mental states from brain activity in humans. Nat. Rev. Neurosci. 2006, 7:523-534.
38. Henson R. What can functional neuroimaging tell the experimental psychologist?. Q. J. Exp. Psychol. A 2005, 58:193-233.
39. Holmes N.P., Spence C. Multisensory integration: space, time and superadditivity. Curr. Biol. 2005, R762-R764. England.
40. Horton J.C., Adams D.L. The cortical column: a structure without a function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 837-862. England.
41. Hubel D.H., Wiesel T.N. Receptive fields, binocular interaction and functional architecture in cats visual cortex. J. Physiol. 1962, 160:106. London.
42. Hubel, D.H., Wiesel, T.N., 1968. Functional architecture of the striate cortex mammal. Functional Architecture of the Striate Cortex Mammal, 153-161.
43. Huettel S.A., Singerman J.D., McCarthy G. The effects of aging upon the hemodynamic response measured by functional MRI. Neuroimage 2001, 13:161-175.
44. Kamitani Y., Tong F. Decoding the visual and subjective contents of the human brain. Nat. Neurosci. 2005, 8:679-685.
45. Kriegeskorte N., Bandettini P. The neuroscientific exploitation of high-resolution functional magnetic resonance imaging. 2006 28th Annual International Conference of the IEEE Engineering in Medicine and Biology Society 2006, Vols. 1-15:6228-6231.
46. Kriegeskorte N., Goebel R., Bandettini P. Information-based functional brain mapping. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3863-3868.
47. Kucera H., Francis W.N. Computational analysis of present-day American English 1967, Brown University Press, Providence RI.
48. Kusunoki M., Sigala N., Nili H., Gaffan D., Duncan J. Target detection by opponent coding in monkey prefrontal cortex. J. Cogn. Neurosci. 2010, 22:751-760.
49. Li S.C., Lindenberger U., Sikstrom S. Aging cognition: from neuromodulation to representation. Trends Cogn. Sci. 2001, 5:479-486.
50. Li S.C., Naveh-Benjamin M., Lindenberger U. Aging neuromodulation impairs associative binding: a neurocomputational account. Psychol. Sci. 2005, 16:445-450.
51. Logan J.M., Sanders A.L., Snyder A.Z., Morris J.C., Buckner R.L. Under-recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging. Neuron 2002, 33:827-840.
52. Madden D.J., Turkington T.G., Provenzale J.M., Denny L.L., Hawk T.C., Gottlob L.R., Coleman R.E. Adult age differences in the functional neuroanatomy of verbal recognition memory. Hum. Brain Mapp. 1999, 7:115-135.
53. Maguire E.A., Frith C.D. Aging affects the engagement of the hippocampus during autobiographical memory retrieval. Brain 2003, 126:1511-1523.
54. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
55. McIntosh A.R., Bookstein F.L., Haxby J.V., Grady C.L. Spatial pattern analysis of functional brain images using partial least squares. Neuroimage 1996, 3:143-157.
56. Miezin F.M., Maccotta L., Ollinger J.M., Petersen S.E., Buckner R.L. Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 2000, 11:735-759.
57. Miller K.D., Keller J.B., Stryker M.P. Ocular dominance column development: analysis and simulation. Science 1989, 245:605-615.
58. Miller S.L., Celone K., DePeau K., Diamond E., Dickerson B.C., Rentz D., Pihlajamaki M., Sperling R.A. Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2181-2186.
59. Morcom A.M., Good C.D., Frackowiak R.S., Rugg M.D. Age effects on the neural correlates of successful memory encoding. Brain 2003, 126:213-229.
60. Morcom A.M., Li J., Rugg M.D. Age effects on the neural correlates of episodic retrieval: increased cortical recruitment with matched performance. Cereb. Cortex 2007, 17:2491-2506.
61. Nelson H.E. The National Adult Reading Test (NART) 1982, NFER-Nelson, Windsor, Berkshire.
62. Norman K.A., Polyn S.M., Detre G.J., Haxby J.V. Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn. Sci. 2006, 10:424-430.
63. Obler L.K., Woodward S., Albert M.L. Changes in cerebral lateralization in aging. Neuropsychologia 1984, 22:235-240.
64. Op de Beeck H.P., Haushofer J., Kanwisher N.G. Interpreting fMRI data: maps, modules and dimensions. Nat. Rev. Neurosci. 2008, 9:123-135.
65. Otten L.J., Henson R.N., Rugg M.D. Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. Brain 2001, 124:399-412.
66. Park D.C., Reuter-Lorenz P. The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 2009, 60:173-196.
67. Park D.C., Polk T.A., Mikels J.A., Taylor S.F., Marshuetz C. Cerebral aging: integration of brain and behavioral models of cognitive function. Dialogues Clin. Neurosci. 2001, 3:16.
68. Park D.C., Welsh R.C., Marshuetz C., Gutchess A.H., Mikels J., Polk T.A., Noll D.C., Taylor S.F. Working memory for complex scenes: age differences in frontal and hippocampal activations. J. Cogn. Neurosci. 2003, 15:1122-1134.
69. Park D.C., Polk T.A., Park R., Minear M., Savage A., Smith M.R. Aging reduces neural specialization in ventral visual cortex. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13091-13095.
70. Payer D., Marshuetz C., Sutton B., Hebrank A., Welsh R.C., Park D.C. Decreased neural specialization in old adults on a working memory task. Neuroreport 2006, 17:487-491.
71. Penny W., Mattout J., Trujillo-Barreto N. Bayesian model selection and averaging. Statistical Parametric Mapping: The Analysis of Functional Brain Images 2006, 454-470. Elsevier, London. K. Friston, J. Ashburner, S. Kiebel, T. Nichols, W. Penny (Eds.).
72. Persson J., Nyberg L., Lind J., Larsson A., Nilsson L.G., Ingvar M., Buckner R.L. Structure-function correlates of cognitive decline in aging. Cereb. Cortex 2006, 16:907-915.
73. Rajah M.N., D'Esposito M. Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. Brain 2005, 128:1964-1983.
74. Raven J.C., Raven J., Court J.H. Manual for Raven's Progressive Matrices and Vocabulary 1994, Oxford University Press, Oxford.
75. Reddy L., Kanwisher N. Coding of visual objects in the ventral stream. Curr. Opin. Neurobiol. 2006, 16:408-414.
76. Reuter-Lorenz P. New visions of the aging mind and brain. Trends Cogn. Sci. 2002, 6:394.
77. Reuter-Lorenz P.A., Cappell K.A. Neurocognitive aging and the compensation hypothesis. Curr. Dir. Psychol. Sci. 2008, 17:177-182.
78. Reuter-Lorenz P.A., Lustig C. Brain aging: reorganizing discoveries about the aging mind. Curr. Opin. Neurobiol. 2005, 15:245-251.
79. Reuter-Lorenz P.A., Jonides J., Smith E.E., Hartley A., Miller A., Marshuetz C., Koeppe R.A. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J. Cogn. Neurosci. 2000, 12:174-187.
80. Roe A.W. Optical imaging of short-term working memory in prefrontal cortex of the Macaque monkey. Imaging the Brain with Optical Methods 2009, 119-133. Springer, New York. A.W. Roe (Ed.).
81. Rosen A.C., Prull M.W., O'Hara R., Race E.A., Desmond J.E., Glover G.H., Yesavage J.A., Gabrieli J.D.E. Variable effects of aging on frontal lobe contributions to memory. Neuroreport 2002, 13:2425-2428.
82. Salthouse T.A. The processing-speed theory of adult age differences in cognition. Psychol. Rev. 1996, 103:403-428.
83. Samanez-Larkin G.R., D'Esposito M. Group comparisons: imaging the aging brain. Soc. Cogn. Affect. Neurosci. 2008, 290-297. England.
84. Schneider-Garces N.J., Gordon B.A., Brumback-Peltz C.R., Shin E., Lee Y., Sutton B.P., Maclin E.L., Gratton G., Fabiani M. Span, CRUNCH, and beyond: working memory capacity and the aging brain. J. Cogn. Neurosci. 2010, 22:655-669.
85. Snodgrass J.G., Corwin J. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J. Exp. Psychol. 1988, 117:34-50.
86. Sokunbi M.O., Staff R.T., Waiter G.D., Ahearn T.S., Fox H.C., Deary I.J., Starr J.M., Whalley L.J., Murray A.D. Inter-individual differences in fMRI entropy measurements in old age 2011, IEEE Trans Biomed Eng.
87. Solbakk A.K., Fuhrmann Alpert G., Furst A.J., Hale L.A., Oga T., Chetty S., Pickard N., Knight R.T. Altered prefrontal function with aging: insights into age-associated performance decline 2008, Brain Res, Netherlands, pp. 30-47.
88. Spearman C. The Abilities of Man 1927, MacMillan, London.
89. Stern Y. Cognitive reserve. Neuropsychologia 2009, 47:2015-2028.
90. Tanaka K. Columns for complex visual object features in the inferotemporal cortex: clustering of cells with similar but slightly different stimulus selectivities. Cereb. Cortex 2003, 13:90-99.
91. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 788-794. England.
92. Tsunoda K., Yamane Y., Nishizaki M., Tanifuji M. Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns. Nat. Neurosci. 2001, 832-838. United States.
93. Tulving E. Elements of episodic memory 1983, Oxford University Press, Oxford.
94. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
95. Vallesi A., McIntosh A.R., Stuss D.T. Overrecruitment in the aging brain as a function of task demands: evidence for a compensatory view. J. Cogn. Neurosci. 2010, 23:801-815.
96. Voss M.W., Erickson K.I., Chaddock L., Prakash R.S., Colcombe S.J., Morris K.S., Doerksen S., Hu L., McAuley E., Kramer A.F. Dedifferentiation in the visual cortex: an fMRI investigation of individual differences in older adults. Brain Res. 2008, 1244:121-131.
97. Wagner A.D., Schacter D.L., Rotte M., Koustaal W., Maril A., Dale A.M., Rosen B.R., Buckner R.L. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 1998, 21:188-191.
98. Wagner A.D., Schacter D.L., Rotte M., Koutstaal W., Maril A., Dale A.M., Rosen B.R., Buckner R.L. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 1998, 281:1188-1191.
99. West R.L. An application of prefrontal cortex function theory to cognitive aging. Psychol. Bull. 1996, 120:272-292.
100. Willshaw D. Analysis of mouse EphA knockins and knockouts suggests that retinal axons programme target cells to form ordered retinotopic maps. Development 2006, 2705-2717. England.
101. Willshaw D.J., von der Malsburg C. How patterned neural connections can be set up by self-organization. Proc. R. Soc. Lond. B Biol. Sci. 1976, 194:431-445.
102. Worsley K.J., Poline J.B., Friston K.J., Evans A.C. Characterizing the response of PET and fMRI data using multivariate linear models. Neuroimage 1997, 6:305-319.
103. Yonelinas A.P. The nature of recollection and familiarity: a review of 30 years of research. Journal of Memory and Language 2002, 46:441-517.
104. Zarahn E., Rakitin B., Abela D., Flynn J., Stern Y. Age-related changes in brain activation during a delayed item recognition task. Neurobiol. Aging 2007, 28:784-798.
105. Zeki S. The motion pathways of the visual cortex. Vision: Coding and Efficiency 1990, 321-345. Cambridge University Press, Cambridge. C. Blakemore (Ed.).