ISSN : 1226-9654
According to the cognitive reserve hypothesis, more educated older adults are less susceptible to age-related or pathological cognitive changes due to accumulated resources necessary for various cognitive tasks. Although previous studies have validated the concept of cognitive reserve, it remains elusive how the early experience of education alters the relationship between regional gray matter volume and episodic memory performance. The present work examined Elderly Verbal Learning Test (EVLT) and structural Magnetic Resonance Imaging within 54 healthy older women. Education groups were divided into low (n = 27, mean education = 2.44) and middle (n = 27, mean education = 8.48) groups. We tested each group’s correlations between regional gray matter volume and memory performances using the voxel-based morphometry (VBM) method and compared whether the correlations between the two groups differ. We found that regional volumes of the medial temporal lobe and orbitofrontal cortex highly correlated with EVLT performance among low education group, whereas the precuneus and inferior parietal lobule volumes were specifically associated with better memory performance among the middle education group. These results indicate that the neuroanatomical substrates contributing to better memory performance differ depending on the years of education, in concert with the protective effect of cognitive reserve.
Amieva, H., Mokri, H., Le Goff, M., Meillon, C., Jacqmin-Gadda, H., Foubert-Samier, A., ..., & Dartigues, J. F. (2014). Compensatory mechanisms in higher-educated subjects with Alzheimer’s disease: A study of 20 years of cognitive decline. Brain, 137, 1167-1175.
Ardila, A., Bertolucci, P. H., Braga, L. W., Castro-Caldas, A., Judd, T., Kosmidis, M. H., ..., & Rosselli, M. (2010). Illiteracy: The neuropsychology of cognition without reading. Archives of Clinical Neuropsychology, 25, 689-712.
Ardila, A, Ostrosky-Solis, F., Rosselli, M., & Gómez, C. (2000). Age-related cognitive decline during normal aging: the complex effect of education. Archives of Clinical Neuropsychology, 15, 495-513.
Arenaza-Urquijo, E. M., Landeau, B., La Joie, R., Mevel, K., Mézenge, F., Perrotin, A., ..., & Chételat, G. (2013). Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. NeuroImage, 83, 450-457.
Ashburner, J., & Friston, K. J. (2005). Unified segmentation. NeuroImage, 26, 839-851.
Baltes, P. B. (1969). Cohort Effects in Cognitive Development of Children as Revealed by Cross-Sectional Sequences 1. Developmental Psychology, 1, 169-177.
Bennett, D. a., Wilson, R. S., Schneider, J. a., Evans, D. a., Aggarwal, N. T., Arnold, S. E., ..., & Bienias, J. L. (2003). Apolipoprotein E 4 allele, AD pathology, and the clinical expression of Alzheimer’s disease. Neurology, 60, 246-252.
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624.
Brayne, C., Ince, P. G., Keage, H. a D., McKeith, I. G., Matthews, F. E., Polvikoski, T., & Sulkava, R. (2010). Education, the brain and dementia: Neuroprotection or compensation?. Brain, 133, 2210-2216.
Cabeza, R. (2008). Role of parietal regions in episodic memory retrieval: The dual attentional processes hypothesis. Neuropsychologia, 46, 1813-1827.
Capitani, E., Barbarotto, R., & Laiacona, M. (1996). Developmental Neuropsychology Does education influence the age related cognitive decline? A further inquiry. Developmental Neuropsychology, 12, 231-240.
Chey, J. (2007). Elderly Memory disorder Scale. Seoul:Hakjisa.
Chey, J. (2011). Korean Dementia Rating Scale 2. Seoul: Hakjisa.
Chey, J., Lee, J., Kim, M., & Kim, H. (2006). Development and Standardization of the Elderly Verbal Learning Test (EVLT). Korean Journal of Psychology: General, 25, 141-173.
Christensen, K. J., Multhaup, K. S., Nordstrom, S., & Voss, K. (1991). A cognitive battery for dementia: Development and measurement characteristics. Psychological Assessment, 3, 168-174.
Craik, F. I. (1986). A functional account of age differences in memory. In F. Klix & H. Hagendorf (Eds.), Human memory and cognitive capabilities, mechanisms, and performance (pp. 409–422). Amsterdam: Elsevier, North-Holland.
Deary, I. J., & Johnson, W. (2010). Intelligence and education: Causal perceptions drive analytic processes and therefore conclusions. International Journal of Epidemiology, 39, 1362-1369.
Delis, D. C., Kramer, J. H., Kaplan, E., & Thompkins, B. A. O. (1987). CVLT:California Verbal Learning Test-Adult Version:Manual. San Antonio, TX: Psychological Corporation.
Fjell, A. M., Walhovd, K. B., Westlye, L. T., Østby, Y., Tamnes, C. K., Jernigan, T. L., ..., & Dale, A. M. (2010). When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies. NeuroImage, 50, 1376-1383.
Foubert-Samier, A., Catheline, G., Amieva, H., Dilharreguy, B., Helmer, C., Allard, M., & Dartigues, J. F. (2012). Education, occupation, leisure activities, and brain reserve: a population-based study. Neurobiology of Aging, 33, 423. e15-423.e25.
Freeman, S. H., Kandel, R., Cruz, L., Rozkalne, A., Newell, K., Frosch, M. P., ..., & Hyman, B. T. (2008). Preservation of neuronal number despite age-related cortical brain atrophy in elderly subjects without Alzheimer disease. Journal of Neuropathology & Experimental Neurology, 67, 1205-1212.
Glymour, M. M., Kawachi, I., Jencks, C. S., & Berkman, L. F. (2008). Does childhood schooling affect old age memory or mental status? Using state schooling laws as natural experiments. Journal of Epidemiology and Community Health, 62, 532-537.
Habeck, C., Razlighi, Q., Gazes, Y., Barulli, D., Steffener, J., & Stern, Y. (2016). Cognitive Reserve and Brain Maintenance: Orthogonal Concepts in Theory and Practice. Cerebral Cortex, 27, 3962-3969.
Hall, C. B., Derby, C., LeValley, A., Katz, M. J., Verghese, J., & Lipton, R. B. (2007). Education delays accelerated decline on a memory test in persons who develop dementia. Neurology, 69, 1657-1664.
Head, D., Rodrigue, K. M., Kennedy, K. M., & Raz, N. (2008). Neuroanatomical and cognitive mediators of age-related differences in episodic memory. Neuropsychology, 22, 491-507.
Hedden, T., Schultz, A. P., Rieckmann, A., Mormino, E. C., Johnson, K. a, Sperling, R. a, & Buckner, R. L. (2014). Multiple Brain Markers are Linked to Age-Related Variation in Cognition. Cerebral Cortex, 26, 1388-1400.
Hwang, S., Kim, J., Park, K., Chey, J., & Hong, S. (2011). Korean Wechsler Adult Intelligence Test (4th ed.). Daegu: Korean Psychology.
Jung, J., Min, S., Han, S., & Yi, D. (2012). The Effects of Categorical Relationship Between Memory Items on Hippocampal Activation in a Long-term Associative Memory Task. The Korean Journal of Cognitive and Biological Psychology, 24, 453-470.
Kanai, R., & Rees, G. (2011). The structural basis of inter-individual differences in human behaviour and cognition. Nature Reviews Neuroscience, 12, 231-242.
Kim, H., & Chey, J. (2010). Effects of education, literacy, and dementia on the Clock Drawing Test performance. Journal of the International Neuropsychological Society, 16, 1138-1146.
Kim, H., Kim, Y. S., & Kim, T. (2011). Effects of Age, Education and Gender on Multiple Cognitive Measures of Korean Older Adults. Korean Journal of Clinical Psychology, 3, 681-701.
Kim, J., & Kang, E. (2013). Individual differences in feedback learning and regional gray matter volume. The Korean Journal of Cognitive and Biological Psychology, 25, 517-538.
Kim, S. G., Lee, E. H., Hwang, S. T., Park, K., Chey, J., Hong, S. H., & Kim, J. H. (2015). Estimation of K-WAIS-IV Premorbid Intelligence in South Korea: Development of the KPIE-IV. The Clinical Neuropsychologist, 4046, 1-11.
Liu, Y., Julkunen, V., Paajanen, T., Westman, E., Wahlund, L. O., Aitken, A., ..., & Soininen, H. (2012). Education increases reserve against Alzheimer’s disease-Evidence from structural MRI analysis. Neuroradiology, 54, 929-938.
Lockhart, S. N., & DeCarli, C. (2014). Structural Imaging Measures of Brain Aging. Neuropsychology Review, 24, 271-289.
Marques, P., Soares, J. M., Magalhães, R., Santos, N. C., & Sousa, N. (2015). The Bounds Of Education In The Human Brain Connectome. Scientific Reports, 5, 12812.
Naveh-Benjamin, M. (2000). Adult age differences in memory performance: tests of an associative deficit hypothesis. Journal of Experimental Psychology: Learning, Memory, and Cognition, 26, 1170.
Park, H., Chey, J., & Lee, J. (2017). Vocabulary Knowledge is Not a Predictor of General Cognitive Functioning in Elderly People with Very Low Educational Attainment. Dementia and Neurocognitive Disorders, 16, 20-25.
Pillai, J. A., McEvoy, L. K., Hagler, D. J., Holland, D., Dale, A. M., Salmon, D. P., ..., & Fennema-Notestine, C. (2012). Higher education is not associated with greater cortical thickness in brain areas related to literacy or intelligence in normal aging or mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 34, 925-935.
Poldrack, R. A. (2015). Is “efficiency” a useful concept in cognitive neuroscience?. Developmental Cognitive Neuroscience, 11, 12-17.
Prull, M. W., Dawes, L. L., Martin III, A. M., Rosenberg, H. F., & Light, L. L. (2006). Recollection and familiarity in recognition memory: Adult age differences and neuropsychological test correlates. Psychology and Aging, 21, 107-118.
Raz, N., Gunning-Dixon, F., Head, D., Rodrigue, K. M., Williamson, A., & Acker, J. D.(2004). Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex:Replicability of regional differences in volume. Neurobiology of Aging, 25, 377-396.
Raz, N., & Kennedy, K. M. (2009). A systems approach to the aging brain: Neuroanatomic changes, their modifiers, and cognitive correlates. In W. Jagust & M. D’Esposito (Eds.), Imaging the aging brain (pp. 43-70). New York: Oxford University Press.
Reed, B. R., Mungas, D., Farias, S. T., Harvey, D., Beckett, L., Widaman, K., ..., & DeCarli, C. (2010). Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain, 133, 2196-2209.
Rentz, D. M., Locascio, J. J., Becker, J. A., Moran, E. K., Eng, E., Buckner, R. L., ..., & Johnson, K. A. (2010). Cognition, reserve, and amyloid deposition in normal aging. Annals of Neurology, 67, 353-364.
Reuter-Lorenz, P. A., & Cappell, K. A. (2008). Neurocognitive aging and the compensation hypothesis. Current Directions in Psychological Science, 17, 177-182.
Rzezak, P., Squarzoni, P., Duran, F. L., De Toledo Ferraz Alves, T., Tamashiro-Duran, J., Bottino, C. M., ..., & Busatto, G. F. (2015). Relationship between brain age-related reduction in gray matter and educational attainment. PLoS ONE, 10, 1-15.
Rönnlund, M., Nyberg, L., Bäckman, L., & Nilsson, L. G. (2005). Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychology of Aging, 20, 3-18.
Seghier, M. (2012). The Angular Gyrus: Multiple Functions and Multiple Subdivisions. The Neuroscientist, 19, 43-61.
Shin M., & Chey, J. (2016). Literacy and cognitive aging in the elderly Korean population. Korean Journal of Psychology: General, 35, 435- 453.
Shing, Y. L., Werkle-Bergner, M., Brehmer, Y., Moller, V., Li, S. C., & Lindenberger, U. (2010). Episodic memory across the lifespan:The contributions of associative and strategic components. Neuroscience and Biobehavioral Reviews, 34, 1080-1091.
Siedlecki, K. L., Stern, Y., Reuben, A., Sacco, R. L., Elkind, M. S. V, & Wright, C. B. (2009). Construct validity of cognitive reserve in a multiethnic cohort: The Northern Manhattan Study. Journal of the International Neuropsychological Society, 15, 558-569.
Steffener, J., Barulli, D., Habeck, C., O’Shea, D., Razlighi, Q., & Stern, Y. (2014). The role of education and verbal abilities in altering the effect of age-related gray matter differences on cognition. PLoS ONE, 9, e91196.
Steffener, J., Reuben, A., Rakitin, B. C., & Stern, Y. (2011). Supporting performance in the face of age-related neural changes:testing mechanistic roles of cognitive reserve. Brain Imaging and Behavior, 5, 212-221.
Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society, 8, 448-460.
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47, 2015-2028.
Stern, Y., Zarahn, E., Habeck, C., Holtzer, R., Rakitin, B. C., Kumar, A., ..., & Brown, T. (2008). A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cerebral Cortex, 18, 959-967.
Suk, J., Chey, J., & Kim, H. (2010). An Additional Normative Study of the Korean-Dementia Rating Scale. Korean Journal of Clinical Psychology, 29, 559-572.
Tark, K., Lee, H., & Yi, D. (2014). Memory Encoding and Consolidation in the Default Mode Networks. The Korean Journal of Cognitive and Biological Psychology, 26, 343-367.
Valenzuela, M. J., & Sachdev, P. (2006). Brain reserve and dementia: a systematic review. Psychological Medicine, 36(4), 441-454.
van Kesteren, M. T. R., Fernández, G., Norris, D. G., & Hermans, E. J. (2010). Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proceedings of the National Academy of Sciences of the United States of America, 107, 7550-7555.
Van Petten, C., Plante, E., Davidson, P. S. R., Kuo, T. Y., Bajuscak, L., & Glisky, E. L. (2004). Memory and executive function in older adults: Relationships with temporal and prefrontal gray matter volumes and white matter hyperintensities. Neuropsychologia, 42, 1313-1335.
Vygotsky, L. (1978). Interaction between learning and development. Readings on the Development of Children, 23(3), 34-41.
Whitfield-Gabrieli, S. (2009). Region of interest extraction (REX) toolbox. Boston, MA, 497.
Zahodne, L. B., Manly, J. J., Brickman, A. M., Siedlecki, K. L., Decarli, C., & Stern, Y. (2013). Quantifying cognitive reserve in older adults by decomposing episodic memory variance: replication and extension. Journal of the International Neuropsychological Society, 19, 854-862.
Zahodne, L. B., Stern, Y., & Manly, J. J. (2015). Differing effects of education on cognitive decline in diverse elders with low versus high educational attainment. Neuropsychology, 29, 649-657.