Context Memory Decline in Middle Aged Adults is Related to Changes in Prefrontal Cortex Function

Cerebral Cortex

Volumn 26, Issue 6, 2016, Pages 2440-2460

  Kwon, Diana ^a   Maillet, David ^a   Pasvanis, Stamatoula ^b   Ankudowich, Elizabeth ^a   Grady, Cheryl L ^c   Rajah, M Natasha ^b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Aging; Compensation; Context memory; Middle age adults; Prefrontal cortex

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; CONTEXT MEMORY; CORRELATIONAL STUDY; ELECTROENCEPHALOGRAM; EPISODIC MEMORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; MALE; MEMORY; MIDDLE AGED; OCCIPITAL CORTEX; PARAHIPPOCAMPAL GYRUS; PREFRONTAL CORTEX; PRIORITY JOURNAL; VISUAL CORTEX; AGING; BRAIN MAPPING; MEMORY DISORDER; MENTAL HEALTH; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; REACTION TIME; SIGNAL PROCESSING; YOUNG ADULT;

ADULT; AGING; BRAIN MAPPING; HUMANS; MAGNETIC RESONANCE IMAGING; MEMORY; MEMORY DISORDERS; MENTAL STATUS SCHEDULE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; REACTION TIME; SIGNAL PROCESSING, COMPUTER-ASSISTED; YOUNG ADULT;

EID: 84974529213     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv068     Document Type: Article

References (86)

1. Addis DR, Giovanello KS, Vu MA, Schacter DL. 2014. Age-related changes in prefrontal and hippocampal contributions to relational encoding. Neuroimage. 84:19-26.
2. Aminoff E, Kveraga K, Bar M. 2013. The role of the parahippocampal cortex in cognition. Trends Cogn Sci. 17 (8):379-390.
3. Badre D, D'Esposito M. 2007. Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J Cogn Neurosci. 19 (12):2082-2099.
4. Badre D, Wagner AD. 2007. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia. 45 (13):2883-2901.
5. Bar M, Aminoff E, Ishai A. 2008. Famous faces activate contextual associations in the parahippocampal cortex. Cereb Cortex. 18 (6):1233-1238.
6. Barbalat G, Chambon V, Franck N, Koechlin E, Farrer C. 2009. Organization of cognitive control within the lateral prefrontal cortex in schizophrenia. Arch Gen Psychiatry. 66 (4):377-386.
7. Beck AT. 1987. Beck depression inventroy. TX: The Psychological Corporation.
8. Bender R, Lange S. 2001. Adjusting for multiple testing-when and how? J Clin Epidemiol. 54 (4):343-349.
9. Bucur B, Madden DJ, Spaniol J, Provenzale JM, Cabeza R, White LE, Huettel SA. 2008. Age-related slowing of memory retrieval: contributions of perceptual speed and cerebral white matter integrity. Neurobiol Aging. 29 (7):1070-1079.
10. Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L. 2000. Agerelated differences in neural activity during item and temporal-order memory retrieval: A positron emission tomography study. J Cogn Neurosci. 12 (1):197-206.
11. Cabeza R, Anderson ND, Locantore JK, McIntosh AR. 2002. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage. 17 (3):1394-1402.
12. Cansino S, Estrada-Manilla C, Trejo-Morales P, Pasaye-Alcaraz EH, Aguilar-Castaneda E, Salgado-Lujambio P, Sosa-Ortiz AL. 2015. fMRI subsequent source memory effects in young, middleaged and old adults. Behav Brain Res. 280:24-35.
13. Cansino S, Hernandez-Ramos E, Trejo-Morales P. 2012. Neural correlates of source memory retrieval in young, middle-aged and elderly adults. Biol Psychol. 90 (1):33-49.
14. Cansino S, Maquet P, Dolan RJ, Rugg MD. 2002. Brain activity underlying encoding and retrieval of source memory. Cereb Cortex. 12 (10):1048-1056.
15. Cansino S, Trejo-Morales P, Hernandez-Ramos E. 2010. Age-related changes in neural activity during source memory encoding in young, middle-aged and elderly adults. Neuropsychologia. 48 (9):2537-2549.
16. Cappell KA, Gmeindl L, Reuter-Lorenz PA. 2010. Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load. Cortex. 46 (4):462-473.
17. Christoff K, Prabhakaran V, Dorfman J, Zhao Z, Kroger JK, Holyoak KJ, Gabrieli JD. 2001. Rostrolateral prefrontal cortex involvement in relational integration during reasoning. Neuroimage. 14 (5):1136-1149.
18. Crane D, Maillet D, Floden D, Valiquette L, Rajah MN. 2011. Similarities in the patterns of prefrontal cortex activity during spatial and temporal context memory retrieval after equating for task structure and performance. Neuroimage. 54 (2): 1549-1564.
19. Davachi L. 2006. Item, context and relational episodic encoding in humans. Curr Opin Neurobiol. 16 (6):693-700.
20. Davachi L, Mitchell JP, WagnerAD. 2003. Multiple routes tomemory: distinct medial temporal lobe processes build item and source memories. Proc Natl Acad Sci USA. 100 (4):2157-2162.
21. DavisSW, Dennis NA, Daselaar SM, Fleck MS, Cabeza R. 2008. Que PASA? The posterior-anterior shift in aging. Cereb Cortex. 18 (5):1201-1209.
22. Dennis NA, Cabeza R. 2012. Frontal lobes and aging: deterioration and compensation. In: Stuss D, Knight R, editors. Principles of frontal lobe function, 2nd ed. New York: Oxford University Press.
23. Dobbins IG, Foley H, Schacter DL, Wagner AD. 2002. Executive control during episodic retrieval: multiple prefrontal processes subserve source memory. Neuron. 35 (5):989-996.
24. Dobbins IG, Simons JS, Schacter DL. 2004. fMRI evidence for separable and lateralized prefrontal memory monitoring processes. J Cogn Neurosci. 16 (6):908-920.
25. Dove A, Brett M, Cusack R, Owen AM. 2006. Dissociable contributions of the mid-ventrolateral frontal cortex and the medial temporal lobe system to human memory. Neuroimage. 31 (4):1790-1801.
26. Duarte A, Henson RN, Graham KS. 2008. The effects of aging on the neural correlates of subjective and objective recollection. Cereb Cortex. 18 (9):2169-2180.
27. Dulas MR, Duarte A. 2011. The effects of aging on material-independent and material-dependent neural correlates of contextual binding. Neuroimage. 57 (3):1192-1204.
28. Dulas MR, Duarte A. 2012. The effects of aging on material-independent and material-dependent neural correlates of source memory retrieval. Cereb Cortex. 22 (1):37-50.
29. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. 2009. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: A random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp. 30 (9):2907-2926.
30. Epstein R, Kanwisher N. 1998. A cortical representation of the local visual environment. Nature. 392 (6676):598-601.
31. Fletcher PC, Shallice T, Dolan RJ. 1998. The functional roles of prefrontal cortex in episodic memory. I. Encoding. Brain. 121 (Pt 7):1239-1248.
32. Folstein MF, Folstein SE, McHugh PR. 1975. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 12 (3):189-198.
33. Friston K. 2004. Experimental design and statistical parametric mapping. In Frackowiak RS, Friston K, Frith CD, Dolan RJ, Price CJ, Zeki S, Ashburner J, Penny W editors Human Brain Function. 2nd ed. London: Elsevier Academic Press. p. 599-634.
34. Grady CL. 2002. Age-related differences in face processing: A meta-analysis of three functional neuroimaging experiments. Can J Exp Psychol. 56 (3):208-220.
35. Grady CL, Maisog JM, Horwitz B, Ungerleider LG, Mentis MJ, Salerno JA, Wagner E, Haxby JV. 1994. Age-related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci. 14 (3 Pt 2):1450-1462.
36. Grady CL, Springer MV, Hongwanishkul D, McIntosh AR, Winocur G. 2006. Age-related changes in brain activity across the adult lifespan. J Cogn Neurosci. 18 (2):227-241.
37. Habib R, Nyberg L, Tulving E. 2003. Hemispheric asymmetries of memory: the HERA model revisited. Trends Cogn Sci. 7 (6):241-245.
38. Kennedy KM, Raz N. 2009. Pattern of normal age-related regional differences in white matter microstructure is modified by vascular risk. Brain Res. 1297:41-56.
39. Kennedy KM, Rodrigue KM, Devous MD Sr, Hebrank AC, Bischof GN, Park DC. 2012. Effects of beta-amyloid accumulation on neural function during encoding across the adult lifespan. Neuroimage. 62 (1):1-8.
40. Koechlin E, Ody C, Kouneiher F. 2003. The architecture of cognitive control in the human prefrontal cortex. Science. 302 (5648):1181-1185.
41. Kriegeskorte N, Formisano E, Sorger B, Goebel R. 2007. Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc Natl Acad Sci USA. 104 (51):20600-20605.
42. Kukolja J, Thiel CM, Wilms M, Mirzazade S, Fink GR. 2009. Ageingrelated changes of neural activity associated with spatial contextual memory. Neurobiol Aging. 30 (4):630-645.
43. Lancaster JL, Tordesillas-Gutierrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT. 2007. Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp. 28 (11):1194-1205.
44. Lebel C, Gee M, Camicioli R, Wieler M, MartinW, Beaulieu C. 2012. Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage. 60 (1):340-352.
45. Lighthall NR, Huettel SA, Cabeza R. 2014. Functional compensation in the ventromedial prefrontal cortex improves memory-dependent decisions in older adults. J Neurosci. 34 (47):15648-15657.
46. Logan JM, Sanders AL, Snyder AZ, Morris JC, Buckner RL. 2002. Under-recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging. Neuron. 33 (5):827-840.
47. Long NM, Oztekin I, Badre D. 2010. Separable prefrontal cortex contributions to free recall. J Neurosci. 30 (33):10967-10976.
48. Maguire EA, Frith CD, Burgess N, Donnett JG, O'Keefe J. 1998. Knowing where things are parahippocampal involvement in encoding object locations in virtual large-scale space. J Cogn Neurosci. 10 (1):61-76.
49. Maillet D, Rajah MN. 2011. Age-related changes in the three-way correlation between anterior hippocampus volume, wholebrain patterns of encoding activity and subsequent context retrieval. Brain Res. 1420:68-79.
50. Maillet D, Rajah MN. 2013. Association between prefrontal activity and volume change in prefrontal and medial temporal lobes in aging and dementia: A review. Ageing Res Rev. 12 (2): 479-489.
51. Martin CB, McLean DA, O'Neil EB, Kohler S. 2013. Distinct familiarity-based response patterns for faces and buildings in perirhinal and parahippocampal cortex. J Neurosci. 33 (26):10915-10923.
52. Mason CH, Perreault WD. 1991. Collinearity, power, and interpretation of multiple regression analysis. J Marketing Res. 28 (3):268-280.
53. McIntosh AR, Chau WK, Protzner AB. 2004. Spatiotemporal analysis of event-related fMRI data using partial least squares. Neuroimage. 23 (2):764-775.
54. McIntosh AR, Lobaugh NJ. 2004. Partial least squares analysis of neuroimaging data: Applications and advances. Neuroimage. 23 (Suppl 1):S250-S263.
55. Morcom AM, Li J, Rugg MD. 2007. Age effects on the neural correlates of episodic retrieval: increased cortical recruitment with matched performance. Cereb Cortex. 17 (11):2491-2506.
56. Murray LJ, Ranganath C. 2007. The dorsolateral prefrontal cortex contributes to successful relational memory encoding. J Neurosci. 27 (20):5515-5522.
57. Norman MA, Evans JD, Miller WS, Heaton RK. 2000. Demographically corrected norms for the California Verbal Learning Test. J Clin Exp Neuropsychol. 22 (1):80-94.
58. O'Brien RM. 2007. A caution regarding rules of thumb for variance inflation factors. Qual Quant. 41 (5):673-690.
59. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9 (1):97-113.
60. Park DC, Polk TA, Park R, Minear M, Savage A, Smith MR. 2004. Aging reduces neural specialization in ventral visual cortex. Proc Natl Acad Sci USA. 101 (35):13091-13095.
61. Park DC, Reuter-Lorenz P. 2009. The adaptive brain: Aging and neurocognitive scaffolding. Annu Rev Psychol. 60:173-196.
62. Park H, Kennedy KM, Rodrigue KM, Hebrank A, Park DC. 2013. An fMRI study of episodic encoding across the lifespan: changes in subsequent memory effects are evident by middle-age. Neuropsychologia. 51 (3):448-456.
63. Parkin AJ, Walter BM, Hunkin NM. 1995. Relationships between normal aging, frontal lobe function, and memory for temporal and spatial information. Neuropsychology. 9 (3):304-312.
64. Rajah MN, Ames B, D'Esposito M. 2008. Prefrontal contributions to domain-general executive control processes during temporal context retrieval. Neuropsychologia. 46 (4):1088-1103.
65. Rajah MN, D'Esposito M. 2005. Region-specific changes in prefrontal function with age: A review of PET and fMRI studies on working and episodic memory. Brain. 128 (Pt 9):1964-1983.
66. Rajah MN, Kromas M, Han JE, Pruessner JC. 2010. Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults. Neuropsychologia. 48 (14):4020-4030.
67. Rajah MN, Languay R, Grady CL. 2011. Age-related changes in right middle frontal gyrus volumes correlate with altered episodic retrieval activity. J Neurosci. 31:17941-17954.
68. Rajah MN, Languay R, Valiquette L. 2010. Age-related changes in prefrontal cortex activity are associated with behavioural deficits in both temporal and spatial context memory retrieval in older adults. Cortex. 46 (4):535-549.
69. Rajah MN, McIntosh AR. 2008. Age-related differences in brain activity during verbal recency memory. Brain Res. 1199: 111-125.
70. Reuter-Lorenz PA, Cappell KA. 2008. Neurocognitive aging and the compensation hypothesis. Curr Dir Psychol Sci. 17 (3): 177-182.
71. Rogers TT, Hocking J, Noppeney U, Mechelli A, Gorno-Tempini ML, Patterson K, Price CJ. 2006. Anterior temporal cortex and semantic memory: reconciling findings from neuropsychology and functional imaging. Cogn Affect Behav Neurosci. 6 (3):201-213.
72. Salthouse TA. 1996. The processing-speed theory of adult age differences in cognition. Psychol Rev. 103 (3):403-428.
73. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC. 1998. The Mini-InternationalNeuropsychiatric Interview (M. I. N. I.): the development and validation of a structured diagnostic psychiatric interviewfor DSM-IVand ICD-10. J Clin Psychiatry. 59 (Suppl 20): 22-33; quiz 34-57.
74. Shimamura AP, Wickens TD. 2009. Superadditive memory strength for item and source recognition: the role of hierarchical relational binding in the medial temporal lobe. Psychol Rev. 116 (1):1-19.
75. Shing YL, Werkle-Bergner M, Brehmer Y, Muller V, Li SC, Lindenberger U. 2010. Episodic memory across the lifespan: the contributions of associative and strategic components. Neurosci Biobehav Rev. 34 (7):1080-1091.
76. Small SA, Tsai WY, DeLaPaz R, Mayeux R, Stern Y. 2002. Imaging hippocampal function across the human life span: is memory decline normal or not? Ann Neurol. 51 (3):290-295.
77. Slotnick SD, Moo LR, Segal JB, Hart J Jr. 2003. Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Res Cogn Brain Res. 17 (1):75-82.
78. Spaniol J, Davidson PS, Kim AS, Han H, Moscovitch M, Grady CL. 2009. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia. 47 (8-9):1765-1779.
79. Spaniol J, Grady C. 2010. Aging and the neural correlates of source memory: over-recruitment and functional reorganization. Neurobiol Aging. doi:10. 1016/j. neurobiolaging. 2010. 10. 005
80. Sperling R. 2007. Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer's disease. Ann N Y Acad Sci. 1097:146-155.
81. Spreen O, Strauss E. 1997. A compendium of neuropsychological tests: Administration, norms, and commentary. New York: Oxford University Press.
82. Talairach J, Tournoux P. 1988. Co-planar stereotaxic atlas of the human brain (M. Rayport, Trans.). New York: Thieme Medical Publishers, Inc.
83. VanPetten C. 2004. Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia. 42 (10):1394-1413.
84. Verhaeghen P, Salthouse TA. 1997. Meta-analyses of age-cognition relations inadulthood: estimates of linearand nonlinear age effects and structural models. Psychol Bull. 122 (3):231-249.
85. Vuoksimaa E, Panizzon MS, Chen CH, Eyler LT, Fennema-Notestine C, Fiecas MJ, Fischl B, Franz CE, Grant MD, Jak AJ, et al. 2013. Cognitive reserve moderates the association between hippocampal volume and episodic memory in middle age. Neuropsychologia. 51 (6):1124-1131.
86. Wang WC, Yonelinas AP, Ranganath C. 2013. Dissociable neural correlates of item and context retrieval in the medial temporal lobes. Behav Brain Res. 254:102-107.