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Medial Temporal Lobe Atrophy is Related to Learning Strategy Changes in Amnestic Mild Cognitive Impairment

Published online by Cambridge University Press:  26 April 2019

Liling Zhang
Affiliation:
Department of Neurology, Tianjin Medical University General Hospital, Tianjin Neurological Institute, 154, Anshan Road, Tianjin 300052, China Department of Neurology, Heji Hospital Affiliated to Changzhi Medical College, 271, Taihang East Street, Changzhi, Shanxi 046000, China
Wen-hao Sun
Affiliation:
Department of Neurology, Tianjin Medical University General Hospital, Tianjin Neurological Institute, 154, Anshan Road, Tianjin 300052, China
Mengya Xing
Affiliation:
Department of Neurology, Tianjin Medical University General Hospital, Tianjin Neurological Institute, 154, Anshan Road, Tianjin 300052, China
Yue Wang
Affiliation:
Department of Neurology, Tianjin Medical University General Hospital, Tianjin Neurological Institute, 154, Anshan Road, Tianjin 300052, China
Yuanyuan Zhang
Affiliation:
Department of Radiology, Tianjin Medical University General Hospital, 154, Anshan Road, Tianjin 300052, China
Qingna Sun
Affiliation:
Department of Neurology, Baoding No. 1 Central Hospital, 320, Changcheng Bei Street, Baoding, Hebei 071000, China
Yan Cheng
Affiliation:
Department of Neurology, Tianjin Medical University General Hospital, Tianjin Neurological Institute, 154, Anshan Road, Tianjin 300052, China
Chuan Shi
Affiliation:
Psychological Assessment Center, Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health, Ministry of Health (Peking University), The National Clinical Research Center for Mental Health Disorders (Peking University Sixth Hospital), 51, Hua Yuan Bei Road, Beijing 100191, China
Nan Zhang*
Affiliation:
Department of Neurology, Tianjin Medical University General Hospital, Tianjin Neurological Institute, 154, Anshan Road, Tianjin 300052, China Department of Neurology, Tianjin Medical University General Hospital Airport Hospital, 85, Dongliu Road, Airport Economic Area, Tianjin 300308, China
*
Correspondence and reprint requests to: Nan Zhang, Department of Neurology, Tianjin Medical University General Hospital, 154, Anshan Road, Tianjin 300052, China. E-mail: nkzhangnan@yeah.net

Abstract

Objective: Deficits in the semantic learning strategy were observed in subjects with amnestic mild cognitive impairment (aMCI) in our previous study. In the present study, we explored the contributions of executive function and brain structure changes to the decline in the semantic learning strategy in aMCI. Methods: A neuropsychological battery was used to test memory and executive function in 96 aMCI subjects and 90 age- and gender-matched healthy controls (HCs). The semantic clustering ratio on the verbal learning test was calculated to evaluate learning strategy. Medial temporal lobe atrophy (MTA) and white matter hyperintensities (WMH) were measured on MRI with the MTA and Fazekas visual rating scales, respectively. Results: Compared to HCs, aMCI subjects had poorer performance in terms of memory, executive function, and the semantic clustering ratio (P < .001). In aMCI subjects, no significant correlation between learning strategy and executive function was observed. aMCI subjects with obvious MTA demonstrated a lower semantic clustering ratio than those without MTA (P < .001). There was no significant difference in the learning strategies between subjects with high-grade WMH and subjects with low-grade WMH. Conclusion: aMCI subjects showed obvious impairment in the semantic learning strategy, which was attributable to MTA but independent of executive dysfunction and subcortical WMH. These findings need to be further validated in large cohorts with biomarkers identified using volumetric brain measurements. (JINS, 2019, 25, 706–717)

Type
Regular Research
Copyright
Copyright © INS. Published by Cambridge University Press, 2019. 

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References

Anderson, S.W. & Tranel, D. (2002). Neuropsychological consequences of dysfunction in human dorsolateral pre-frontal cortex, In J. Grafman (Ed.), Handbook of Neuropsychology (pp. 145–156). New York: Elsevier.Google Scholar
Apostolova, L.G., Morra, J.H., Green, A.E., Hwang, K.S., Avedissian, C., Woo, E., … Alzheimer’s Disease Neuroimaging Initiative. (2010). Automated 3D mapping of baseline and 12-month associations between three verbal memory measures and hippocampal atrophy in 490 ADNI subjects. Neuroimage, 51(1), 488499.CrossRefGoogle ScholarPubMed
Appel, J., Potter, E., Bhatia, N., Shen, Q., Zhao, W., Greig, M.T., … Duara, R. (2009). Association of white matter hyperintensity measurements on brain MR imaging with cognitive status, medial temporal atrophy, and cardiovascular risk factors. AJNR American Journal of Neuroradiology, 30(10), 18701876.CrossRefGoogle ScholarPubMed
Baddeley, A.D. (2001). Is working memory still working? American Psychologist, 56(11), 851.CrossRefGoogle ScholarPubMed
Baker, J.T., Sanders, A.L., Maccotta, L., & Buckner, R.L. (2001). Neural correlates of verbal memory encoding during semantic and structural processing tasks. Neuroreport, 12(6), 12511256.CrossRefGoogle ScholarPubMed
Becker, S. & Lim, J. (2003). A computational model of prefrontal control in free recall: Strategic memory use in the California verbal learning task. Journal of Cognitive Neuroscience, 15(6), 821832.CrossRefGoogle ScholarPubMed
Bell, C.C. (1994). DSM-IV: Diagnostic and statistical manual of mental disorders. JAMA the Journal of the American Medical Association, 272(10), 828829.CrossRefGoogle Scholar
Berg, L. (1988). Clinical dementia rating (CDR). Psychopharmacology Bulletin, 24(4), 637639.Google Scholar
Binder, J.R., Desai, R.H., Graves, W.W., & Conant, L.L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebral Cortex, 19(12), 27672796.CrossRefGoogle ScholarPubMed
Braak, H. & Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica, 82(4), 239259.CrossRefGoogle ScholarPubMed
Bronnick, K., Alves, G., Aarsland, D., Tysnes, O.B., & Larsen, J.P. (2011). Verbal memory in drug-naive, newly diagnosed Parkinson’s disease. The retrieval deficit hypothesis revisited. Neuropsychology, 25(1), 114124.CrossRefGoogle ScholarPubMed
Burns, J.M., Church, J.A., Johnson, D.K., Xiong, C., Marcus, D., Fotenos, A.F., … Buckner, R.L. (2005). White matter lesions are prevalent but differentially related with cognition in aging and early Alzheimer disease. Archives of Neurology, 62(12), 1870.CrossRefGoogle ScholarPubMed
Carlesimo, G.A., Mauri, M., Graceffa, A.M., Fadda, L., Loasses, A., Lorusso, S., & Caltagirone, C. (1998). Memory performances in young, elderly, and very old healthy individuals versus patients with Alzheimer’s disease: Evidence for discontinuity between normal and pathological aging. Journal of Clinical & Experimental Neuropsychology, 20(4), 1429.CrossRefGoogle ScholarPubMed
Chan, A.S., Kwok, I.C., Chiu, H., Lam, L., Pang, A., & Chow, L.Y. (2000). Memory and organizational strategies in chronic and acute schizophrenic patients. Schizophrenia Research, 41(3), 431445.CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Journal of the American Statistical Association, 2(4), 1974.Google Scholar
Daly, E., Zaitchik, D., Copeland, M., Schmahmann, J., Gunther, J., & Albert, M. (2000). Predicting conversion to Alzheimer disease using standardized clinical information. Archives of Neurology, 57(5), 675680.CrossRefGoogle ScholarPubMed
Das, S.R., Mancuso, L., Olson, I.R., Arnold, S.E., & Wolk, D.A. (2016). Short-term memory depends on dissociable medial temporal lobe regions in amnestic mild cognitive impairment. Cerebral Cortex, 26(5), 20062017.CrossRefGoogle ScholarPubMed
Decarli, C. (2004). Vascular factors in dementia: An overview. Journal of the Neurological Sciences, 226(1–2), 1923.CrossRefGoogle ScholarPubMed
Delanowood, L., Bondi, M.W., Sacco, J., Abeles, N., Jak, A.J., Libon, D.J., & Bozoki, A. (2009). Heterogeneity in mild cognitive impairment: Differences in neuropsychological profile and associated white matter lesion pathology. Journal of the International Neuropsychological Society, 15(6), 906914.CrossRefGoogle Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). California verbal learning test–II (2nd ed). New York: The Psychological Corporation.Google Scholar
Delis, D.C. & Massman, P.J. (1991). Profiles of demented and amnesic patients on the California Verbal Learning Test: Implications for the assessment of memory disorders. Psychological Assessment, 3(1), 1926.CrossRefGoogle Scholar
Dong, A., Toledo, J.B., Honnorat, N., Doshi, J., Varol, E., Sotiras, A., … Davatzikos, C. (2017). Heterogeneity of neuroanatomical patterns in prodromal Alzheimer’s disease: Links to cognition, progression and biomarkers. Brain: A Journal of Neurology, 140(3), 735747.Google ScholarPubMed
England, H.B., Gillis, M.M., & Hampstead, B.M. (2014). RBANS memory indices are related to medial temporal lobe volumetrics in healthy older adults and those with mild cognitive impairment. Archives of Clinical Neuropsychology, 29(4), 322328.CrossRefGoogle ScholarPubMed
Fazekas, F., Chawluk, J.B., Alavi, A., Hurtig, H.I., & Zimmerman, R.A. (1987). MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. American Journal of Roentgenology, 149(3), 421426.CrossRefGoogle Scholar
Folstein, M.F., Folstein, S.E., & Mchugh, P.R. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189198.CrossRefGoogle ScholarPubMed
Fox, N.C., Warrington, E.K., Freeborough, P.A., Hartikainen, P., Kennedy, A.M., Stevens, J.M., & Rossor, M.N. (1996). Presymptomatic hippocampal atrophy in Alzheimer’s disease. A longitudinal MRI study. Brain, 119(Pt 6), 20012007.CrossRefGoogle ScholarPubMed
Fujishima, M., Maikusa, N., Nakamura, K., Nakatsuka, M., Matsuda, H., & Meguro, K. (2014). Mild cognitive impairment, poor episodic memory, and late-life depression are associated with cerebral cortical thinning and increased white matter hyperintensities. Frontiers in Aging Neuroscience, 6, 306.CrossRefGoogle ScholarPubMed
Gaines, J.J., Shapiro, A., Alt, M., & Benedict, R.H. (2006). Semantic clustering indexes for the Hopkins Verbal Learning Test-Revised: Initial exploration in elder control and dementia groups. Applied Neuropsychology, 105(13), 213222.CrossRefGoogle Scholar
Gao, F.Q., Swartz, R.H., Scheltens, P., Leibovitch, F.S., Kiss, A., Honjo, K., & Black, S.E. (2011). Complexity of MRI white matter hyperintensity assessments in relation to cognition in aging and dementia from the Sunnybrook Dementia Study. Journal of Alzheimer’s Disease, 26(Suppl 3), 379388.CrossRefGoogle ScholarPubMed
Geary, E.K., Kraus, M.F., Rubin, L.H., Pliskin, N.H., & Little, D.M. (2011). Verbal learning strategy following mild traumatic brain injury. Journal of the International Neuropsychological Society, 17(4), 709719.CrossRefGoogle ScholarPubMed
Geschwind, N. (1965). Disconnexion syndromes in animal and man. Brain, 88(2), 237294.CrossRefGoogle ScholarPubMed
Glosser, G., Gallo, J.L., Clark, C.M., & Grossman, M. (2002). Memory encoding and retrieval in frontotemporal dementia and Alzheimer’s disease. Neuropsychology, 16(2), 190196.CrossRefGoogle ScholarPubMed
Gong, Y. (1989). Handbook of Wechsler memory scale-revised. Changsha, China: Hunan Medical University.Google Scholar
Griffith, H.R., Hollander, J.A.D., Okonkwo, O., Evanochko, W.T., Harrell, L.E., Zamrini, E.Y., … Marson, D.C. (2007). Executive function is associated with brain proton magnetic resonance spectroscopy in amnestic mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 29(6), 599609.CrossRefGoogle ScholarPubMed
Gronwall, D.M. (2011). Paced auditory serial-addition task: A measure of recovery from concussion. Perceptual & Motor Skills, 44(2), 367373.CrossRefGoogle Scholar
Gsottschneider, A., Keller, Z., Pitschel-Walz, G., Frobose, T., Bauml, J., & Jahn, T. (2011). The role of encoding strategies in the verbal memory performance in patients with schizophrenia. Journal of Neuropsychology, 5(Pt 1), 5672.CrossRefGoogle ScholarPubMed
Harper, L., Barkhof, F., Fox, N.C., & Schott, J.M. (2015). Using visual rating to diagnose dementia: A critical evaluation of MRI atrophy scales. Journal of Neurology, Neurosurgery, and Psychiatry, 86(11), 12251233.CrossRefGoogle ScholarPubMed
He, Y., Qu, G., Xiong, X., Chi, Y., Zhang, M., & Zhang, M. (1990). The assessment of activities of daily living in the elderly. Journal of Gerontology (5), 266269.Google Scholar
Hildebrandt, H., Brand, A., & Sachsenheimer, W. (1998). Profiles of patients with left prefrontal and left temporal lobe lesions after cerebrovascular infarcations on california verbal learning test-like indices. Journal of Clinical & Experimental Neuropsychology, 20(5), 673683.CrossRefGoogle ScholarPubMed
Hutchens, R.L., Kinsella, G.J., Ong, B., Pike, K.E., Parsons, S., Storey, E., … Clare, L. (2012). Knowledge and use of memory strategies in amnestic mild cognitive impairment. Psychology and Aging, 27(3), 768777.CrossRefGoogle ScholarPubMed
Jackson, O. & Schacter, D.L. (2004). Encoding activity in anterior medial temporal lobe supports subsequent associative recognition. NeuroImage, 21(1), 456462.CrossRefGoogle ScholarPubMed
Jack, C.R. Jr., Petersen, R.C., Xu, Y.C., O’Brien, P.C., Smith, G.E., Ivnik, R.J., … Kokmen, E. (1999). Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology, 52(7), 13971403.CrossRefGoogle ScholarPubMed
Kirchhoff, B.A., Gordon, B.A., & Head, D. (2014). Prefrontal gray matter volume mediates age effects on memory strategies. Neuroimage, 90, 326334.CrossRefGoogle ScholarPubMed
La, V.D.P., Korf, E.S., Wm, V.D.F., Brashear, H.R., Fox, N.C., Barkhof, F., & Scheltens, P. (2007). Magnetic resonance imaging predictors of cognition in mild cognitive impairment. Archives of Neurology, 64(7), 10231028.Google Scholar
Lawton, M.P. & Brody, E.M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist, 9(3), 179186.CrossRefGoogle ScholarPubMed
Luchsinger, J.A., Brickman, A.M., Reitz, C., Cho, S.J., Schupf, N., Manly, J.J., … Decarli, C. (2009). Subclinical cerebrovascular disease in mild cognitive impairment. Neurology, 73(6), 450456.CrossRefGoogle ScholarPubMed
Malek-Ahmadi, M., Raj, A., & Small, B.J. (2011). Semantic clustering as a neuropsychological predictor for amnestic-MCI. Aging, Neuropsychology, and Cognition, 18(3), 280292.CrossRefGoogle ScholarPubMed
Manning, J.R., Sperling, M.R., Sharan, A., Rosenberg, E.A., & Kahana, M.J. (2012). Spontaneously reactivated patterns in frontal and temporal lobe predict semantic clustering during memory search. Journal of Neuroscience, 32(26), 88718878.CrossRefGoogle ScholarPubMed
McLaughlin, P.M., Wright, M.J., Larocca, M., Nguyen, P.T., Teng, E., Apostolova, L.G., … Woo, E. (2014). The “Alzheimer’s type” profile of semantic clustering in amnestic mild cognitive impairment. Journal of the International Neuropsychological Society, 20(4), 402412.CrossRefGoogle ScholarPubMed
Meijs, C.J., Hurks, P.P., Kalff, A.C., Slaats-Willemse, D.I., Rozendaal, N., & Jolles, J. (2009). Differential development of learning strategies on a Pictorial Verbal Learning Test (PVLT) in primary-school children. Child Neuropsychology: A Journal on Normal & Abnormal Development in Childhood & Adolescence, 15(3), 247261.CrossRefGoogle Scholar
Mendonça, A.D., Ribeiro, F., Guerreiro, M., Palma, T., & Garcia, C. (2005). Clinical significance of subcortical vascular disease in patients with mild cognitive impairment. European Journal of Neurology, 12(2), 125130.CrossRefGoogle ScholarPubMed
Mok, V.C., Wong, A., Yim, P., Fu, M., Lam, W.W., Hui, A.C., … Wong, K.S. (2004). The validity and reliability of chinese frontal assessment battery in evaluating executive dysfunction among Chinese patients with small subcortical infarct. Alzheimer Disease & Associated Disorders, 18(2), 6874.CrossRefGoogle ScholarPubMed
Naya, Y. (2016). Declarative association in the perirhinal cortex. Neuroscience Research, 113, 1218.CrossRefGoogle ScholarPubMed
Nitzburg, G.C., Cuesta-Diaz, A., Ospina, L.H., Russo, M., Shanahan, M., Perez-Rodriguez, M., … Burdick, K.E. (2017). Organizational learning strategies and verbal memory deficits in bipolar disorder. Journal of the International Neuropsychological Society, 23(4), 358366.CrossRefGoogle ScholarPubMed
Overdorp, E.J., Kessels, R.P., Claassen, J.A., & Oosterman, J.M. (2014). Cognitive impairments associated with medial temporal atrophy and white matter hyperintensities: An MRI study in memory clinic patients. Frontiers in Aging Neuroscience, 6, 98.CrossRefGoogle ScholarPubMed
Pantel, J., Schönknecht, P., Essig, M., & Schröder, J. (2004). Distribution of cerebral atrophy assessed by magnetic resonance imaging reflects patterns of neuropsychological deficits in Alzheimer’s dementia. Neuroscience Letters, 361(1–3), 1720.CrossRefGoogle ScholarPubMed
Perri, R., Carlesimo, G.A., Serra, L., & Caltagirone, C. (2005). Characterization of memory profile in subjects with amnestic mild cognitive impairment. Journal of Clinical & Experimental Neuropsychology, 27(8), 10331055.CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183194.CrossRefGoogle ScholarPubMed
Petersen, R.C. & Morris, J.C. (2005). Mild cognitive impairment as a clinical entity and treatment target. Archives of Neurology, 62(7), 11601163; discussion 1167.CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E.G., & Kokmen, E. (1999). Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology, 56(3), 303.CrossRefGoogle ScholarPubMed
Price, S.E., Kinsella, G.J., Ong, B., Mullaly, E., Phillips, M., Pangnadasa-Fox, L., … Storey, E. (2010). Learning and memory in amnestic mild cognitive impairment: Contribution of working memory. Journal of the International Neuropsychological Society, 16(2), 342351.CrossRefGoogle ScholarPubMed
Petersen, R. C., Doody, R., Kurz, A., Mohs, R.C., Morris, J.C., Rabins, P.V., … Winblad, B. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58(12), 19851992.CrossRefGoogle ScholarPubMed
Ribeiro, F., Guerreiro, M., & De Mendonca, A. (2007). Verbal learning and memory deficits in Mild Cognitive Impairment. Journal of Clinical and Experimental Neuropsychology, 29(2), 187197.CrossRefGoogle ScholarPubMed
Rossini, E.D. & Karl, M.A. (1994). The Trail Making Test A and B: A technical note on structural nonequivalence. Perceptual & Motor Skills, 78(2), 625626.CrossRefGoogle Scholar
Sanchez-Benavides, G., Gomez-Anson, B., Molinuevo, J.L., Blesa, R., Monte, G.C., Buschke, H., & Pena-Casanova, J. (2010). Medial temporal lobe correlates of memory screening measures in normal aging, MCI, and AD. Journal of Geriatric Psychiatry and Neurology, 23(2), 100108.CrossRefGoogle ScholarPubMed
Savage, C.R., Deckersbach, T., Heckers, S., Wagner, A.D., Schacter, D.L., Alpert, N.M., … Rauch, S.L. (2001). Prefrontal regions supporting spontaneous and directed application of verbal learning strategies: Evidence from PET. Brain A Journal of Neurology, 124(Pt 1), 219231.CrossRefGoogle ScholarPubMed
Scheltens, P., Leys, D., Barkhof, F., Huglo, D., Weinstein, H.C., Vermersch, P., … Valk, J. (1992). Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: Diagnostic value and neuropsychological correlates. Journal of Neurology Neurosurgery & Psychiatry, 55(10), 967972.CrossRefGoogle ScholarPubMed
Shi, C., Kang, L., Yao, S., Ma, Y., Li, T., Liang, Y., … Yu, X. (2015). The MATRICS Consensus Cognitive Battery (MCCB): Co-norming and standardization in China. Schizophrenia Research, 169(1–3), 109115.CrossRefGoogle Scholar
Shim, Y.S., Youn, Y.C., Na, D.L., Kim, S.Y., Cheong, H.K., Moon, S.Y., … Seo, S.W. (2011). Effects of medial temporal atrophy and white matter hyperintensities on the cognitive functions in patients with Alzheimer’s disease. European Neurology, 66(2), 7582.CrossRefGoogle ScholarPubMed
Smith, A. (1982). Symbol digit modalities test. 2444–2444. Los Angeles, CA: Western Psychological Services.Google Scholar
Sorianoraya, J.J., Miralbell, J., Lópezcancio, E., Bargalló, N., Arenillas, J.F., Barrios, M., … Dávalos, A. (2012). Deep versus periventricular white matter lesions and cognitive function in a community sample of middle-aged participants. Journal of the International Neuropsychological Society JINS, 18(5), 874885.CrossRefGoogle Scholar
Stelmokas, J., Yassay, L., Giordani, B., Dodge, H.H., Dinov, I.D., Bhaumik, A., … Hampstead, B.M. (2017). Translational MRI volumetry with neuroquant: Effects of version and normative data on relationships with memory performance in healthy older adults and patients with mild cognitive impairment. Journal of Alzheimer’s Disease, 60(4), 14991510.CrossRefGoogle ScholarPubMed
Strangman, G.E., O’Neil-Pirozzi, T.M., Goldstein, R., Kelkar, K., Katz, D.I., Burke, D., … Glenn, M.B. (2008). Prediction of memory rehabilitation outcomes in traumatic brain injury by using functional magnetic resonance imaging. Archives of Physical Medicine and Rehabilitation, 89(5), 974981.CrossRefGoogle ScholarPubMed
Sun, Q., Luo, L., Ren, H., Wei, C., Xing, M., Cheng, Y., & Zhang, N. (2016). Semantic clustering and sleep in patients with amnestic mild cognitive impairment or with vascular cognitive impairment-no dementia. International Psychogeriatrics, 28(9), 14931502.CrossRefGoogle ScholarPubMed
Sunderaraman, P., Blumen, H.M., DeMatteo, D., Apa, Z.L., & Cosentino, S. (2013). Task demand influences relationships among sex, clustering strategy, and recall: 16-word versus 9-word list learning tests. Cognitive and Behavioral Neurology, 26(2), 7884.CrossRefGoogle ScholarPubMed
Wechsler, D. (1987). Wechsler memory scale–revised manual. San Antonio, TX: Psychological Corporation.Google Scholar
Weidemann, C.T., Kragel, J.E., Lega, B.C., Worrell, G.A., Sperling, M.R., Sharan, A.D., … Kahana, M.J. (2019). Neural activity reveals interactions between episodic and semantic memory systems during retrieval. Journal of Experimental Psychology: General, 148(1), 112.CrossRefGoogle ScholarPubMed
Zheng, D., Sun, H., Dong, X., Liu, B., Xu, Y., Chen, S., … Wang, X. (2014). Executive dysfunction and gray matter atrophy in amnestic mild cognitive impairment. Neurobiol Aging, 35(3), 548555.CrossRefGoogle ScholarPubMed
Zheng, Y.P. & Lin, K.M. (1991). Comparison of the Chinese Depression Inventory and the Chinese version of the Beck Depression Inventory. Acta Psychiatrica Scandinavica, 84(6), 531536.CrossRefGoogle ScholarPubMed
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