Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-06-02T08:34:19.243Z Has data issue: false hasContentIssue false
  • English
  • Français

Story Memory Impairment Rates and Association with Hippocampal Volumes in a Memory Clinic Population

Published online by Cambridge University Press:  30 June 2021

Christina G. Wong Open the ORCID record for Christina G. Wong [Opens in a new window] ,
Sharlene L. Jeffers ,
Samantha A. Bell ,
Jessica Z.K. Caldwell ,
Sarah J. Banks  and
Justin B. Miller Open the ORCID record for Justin B. Miller [Opens in a new window]
Christina G. Wong*
Affiliation:
Department of Neuropsychology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA
Sharlene L. Jeffers
Affiliation:
Department of Neuropsychology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA
Samantha A. Bell
Affiliation:
Department of Neuropsychology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA
Jessica Z.K. Caldwell
Affiliation:
Department of Neuropsychology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA
Sarah J. Banks
Affiliation:
Department of Neurosciences and Psychiatry, University of California, San Diego, San Diego, CA, USA
Justin B. Miller
Affiliation:
Department of Neuropsychology, Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA
*
*Correspondence and reprint requests to: Christina G. Wong, PhD, Department of Neuropsychology, Cleveland Clinic Lou Ruvo Center for Brain Health, 888 W. Bonneville Ave, Las Vegas, NV89106, USA., Fax: 702-438-6007. E-mail: wongc7@ccf.org
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

Story memory tasks are among the most commonly used memory tests; however, research suggests they may be less sensitive to memory decline and have a weaker association with hippocampal volumes than list learning tasks. To examine its utility, we compared story memory to other memory tests on impairment rates and association with hippocampal volumes.

Method:

Archival records from 1617 older adults (Mage = 74.41, range = 65–93) who completed the Wechsler Memory Scale – 4th edition (WMS-IV) Logical Memory (LM), Hopkins Verbal Learning Test – Revised (HVLT-R), and Brief Visuospatial Memory Test – Revised (BVMT-R) as part of a clinical neuropsychological evaluation were reviewed. Scores >1.5 SD below age-adjusted means were considered impaired, and frequency distributions were used to examine impairment rates. A subset of participants (n = 179) had magnetic resonance imaging (MRI) data that underwent image quality assessment. Partial correlations and linear regression analyses, accounting for age, education, and total intracranial volume (TIV), examined associations between memory raw scores and hippocampal volumes.

Results:

For delayed recall, nearly half of the sample was impaired on HVLT-R (48.8%) and BVMT-R (46.1%), whereas a little more than a third was impaired on LM (35.7%). Better performance on all three measures was related to larger hippocampal volumes (r’s =. 26–.43, p’s < .001). Individually adding memory scores to regression models predicting hippocampal volumes improved the model fit for all measures.

Conclusions:

Despite findings suggesting that story memory is less sensitive to memory dysfunction, it was not differentially associated with hippocampal volumes compared to other memory measures. Results support assessing memory using different formats and modalities in older adults.

Keywords

Memory disordersNeuropsychological testsHippocampusMagnetic resonance imagingAgedAlzheimer disease
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 6 , July 2022 , pp. 611 - 619
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, E., De Jager, C., & Iversen, S. (2006). The placing test: Preliminary investigations of a quick and simple memory test designed to be sensitive to pre-dementia Alzheimer’s disease but not to normal ageing. Journal of Clinical and Experimental Neuropsychology, 28(6), 843–858. https://doi.org/10.1080/13803390591001016 CrossRefGoogle ScholarPubMed
Belleville, S., Fouquet, C., Hudon, C., Zomahoun, H.T.V., & Croteau, J. (2017). Neuropsychological Measures that Predict Progression from Mild Cognitive Impairment to Alzheimer’s type dementia in Older Adults: a Systematic Review and Meta-Analysis. Neuropsychology Review, 27, 328–353. https://doi.org/10.1007/s11065-017-9361-5 CrossRefGoogle ScholarPubMed
Benedict, R.H.B. (1997). Brief Visuospatial Memory Test-Revised. Lutz, FL: Psychological Assessment Resources.Google Scholar
Bondi, M.W., Edmonds, E.C., Jak, A.J., Clark, L.R., Delano-Wood, L., McDonald, C.R., … Salmon, D.P. (2014). Neuropsychological Criteria for Mild Cognitive Impairment Improves Diagnostic Precision, Biomarker Associations, and Progression Rates. Journal of Alzheimer’s Disease, 42(1), 275–289. https://doi.org/10.3233/JAD-140276 CrossRefGoogle ScholarPubMed
Bonner-Jackson, A., Mahmoud, S., Miller, J., & Banks, S.J. (2015). Verbal and non-verbal memory and hippocampal volumes in a memory clinic population. Alzheimer’s Research and Therapy, 7(1). https://doi.org/10.1186/s13195-015-0147-9 Google Scholar
Brandt, J., & Benedict, R.H.B. (2001). Hopkins Verbal Learning Test–Revised: Professional manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Brooks, B.L., Weaver, L.E., & Scialfa, C.T. (2006). Does impaired executive functioning differentially impact verbal memory measures in older adults with suspected dementia? Clinical Neuropsychologist, 20(2), 230–242. https://doi.org/10.1080/13854040590947461 CrossRefGoogle ScholarPubMed
Contador, I., Fernández-Calvo, B., Cacho, J., Ramos, F., & Lopez-Rolon, A. (2010). Nonverbal memory tasks in early differential diagnosis of alzheimer’s disease and unipolar depression. Applied Neuropsychology, 17(4), 251–261. https://doi.org/10.1080/09084282.2010.525098 CrossRefGoogle ScholarPubMed
Dale, A.M., & Sereno, M.I. (1993). Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: A linear approach. Journal of Cognitive Neuroscience, 5(2), 162–176. https://doi.org/10.1162/jocn.1993.5.2.162 CrossRefGoogle Scholar
Dale, A.M., Fischl, B., & Sereno, M.I. (1999). Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194. https://doi.org/10.1006/nimg.1998.0395 CrossRefGoogle ScholarPubMed
De Toledo-Morrell, L., Dickerson, B., Sullivan, M.P., Spanovic, C., Wilson, R., & Bennett, D A. (2000). Hemispheric differences in hippocampal volume predict verbal and spatial memory performance in patients with Alzheimer’s disease. Hippocampus, 10(2), 136–142. https://doi.org/10.1002/(SICI)1098-1063(2000)10:2<136:AID-HIPO2>3.0.CO;2-J 3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Delis, D.C., Cullum, C.M., Butters, N., Cairns, P., & Prifitera, A. (1988). Wechsler memory scale-revised and california verbal learning test: Convergence and divergence. Clinical Neuropsychologist, 2(2), 188–196. https://doi.org/10.1080/13854048808520100 CrossRefGoogle Scholar
Edmonds, E.C., Delano-Wood, L., Clark, L.R., Jak, A.J., Nation, D.A., McDonald, C.R., … Bondi, M.W. (2015). Susceptibility of the conventional criteria for mild cognitive impairment to false-positive diagnostic errors. Alzheimer’s and Dementia, 11(4), 415–424. https://doi.org/10.1016/j.jalz.2014.03.005 CrossRefGoogle ScholarPubMed
Ezzati, A., Katz, M.J., Zammit, A.R., Lipton, M.L., Zimmerman, M.E., Sliwinski, M.J., & Lipton, R.B. (2016). Differential association of left and right hippocampal volumes with verbal episodic and spatial memory in older adults. Neuropsychologia, 93, 380–385. https://doi.org/10.1016/j.neuropsychologia.2016.08.016 CrossRefGoogle ScholarPubMed
Fischl, B., Liu, A., & Dale, A.M. (2001). Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Imaging, 20(1), 70–80. https://doi.org/10.1109/42.906426 CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., … Dale, A.M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355. https://doi.org/10.1016/S0896-6273(02)00569-X CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Van Der Kouwe, A.J.W., Makris, N., Ségonne, F., Quinn, B.T., & Dale, A.M. (2004). Sequence-independent segmentation of magnetic resonance images. NeuroImage, 23(SUPPL. 1). https://doi.org/10.1016/j.neuroimage.2004.07.016 CrossRefGoogle Scholar
Hackert, V.H., Den Heijer, T., Oudkerk, M., Koudstaal, P.J., Hofman, A., & Breteler, M.M.B. (2002). Hippocampal head size associated with verbal memory performance in nondemented elderly. NeuroImage, 17(3), 1365–1372. https://doi.org/10.1006/nimg.2002.1248 CrossRefGoogle ScholarPubMed
IBM Corp. (2019). SPSS Statistics 26.0. Armonk, NY: IMB Corp.Google Scholar
Iglesias, J.E., Augustinack, J.C., Nguyen, K., Player, C.M., Player, A., Wright, M., … Van Leemput, K. (2015). A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI. NeuroImage, 115, 117–137. https://doi.org/10.1016/j.neuroimage.2015.04.042 CrossRefGoogle ScholarPubMed
Jak, A.J., Bondi, M.W., Delano-Wood, L., Wierenga, C., Corey-Bloom, J., Salmon, D.P., & Delis, D.C. (2009). Quantification of five neuropsychological approaches to defining mild cognitive impairment. American Journal of Geriatric Psychiatry, 17(5), 368–375. https://doi.org/10.1097/JGP.0b013e31819431d5 Google ScholarPubMed
Lee, I.A., & Preacher, K.J. (2013). Calculation for the test of the difference between two dependent correlations with one varaible in common. Retrieved from http://quantpsy.org Google Scholar
Marchiani, N.C.P., Balthazar, M.L.F., Cendes, F., & Damasceno, B.P. (2008). Hippocampal atrophy and verbal episodic memory performance in amnestic mild cognitive impairment and mild Alzheimer’s disease: A preliminary study. Dementia & Neuropsychologia, 2(1), 37–41. https://doi.org/10.1590/s1980-57642009dn20100008 CrossRefGoogle ScholarPubMed
Marquis, S., Milar Moore, M., Howieson, D.B., Sexton, G., Payami, H., Kaye, J.A., & Camicioli, R. (2002). Independent predictors of cognitive decline in healthy elderly persons. Archives of Neurology, 59(4), 601–606. https://doi.org/10.1001/archneur.59.4.601 CrossRefGoogle ScholarPubMed
Peng, G.P., Feng, Z., He, F.P., Chen, Z.Q., Liu, X.Y., Liu, P., & Luo, B.Y. (2015). Correlation of Hippocampal Volume and Cognitive Performances in Patients with Either Mild Cognitive Impairment or Alzheimer’s disease. CNS Neuroscience and Therapeutics, 21(1), 15–22. https://doi.org/10.1111/cns.12317 CrossRefGoogle ScholarPubMed
Petersen, R.C., Jack, C.R., Xu, Y.C., Waring, S.C., O’Brien, P.C., Smith, G.E., … Kokmen, E. (2000). Memory and MRI-based hippocampal volumes in aging and AD. Neurology, 54(3), 581–587. https://doi.org/10.1212/wnl.54.3.581 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), 303–308. https://doi.org/10.1001/archneur.56.3.303 CrossRefGoogle ScholarPubMed
Prince, M., Bryce, R., Albanese, E., Wimo, A., Ribeiro, W., & Ferri, C.P. (2013). The global prevalence of dementia: A systematic review and metaanalysis. Alzheimer’s and Dementia, 9, 63–75.e2. https://doi.org/10.1016/j.jalz.2012.11.007 CrossRefGoogle ScholarPubMed
Putcha, D., Brickhouse, M., Wolk, D.A., & Dickerson, B.C. (2019). Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer’s disease. Neuropsychologia, 129, 83–92. https://doi.org/10.1016/j.neuropsychologia.2019.03.015 CrossRefGoogle ScholarPubMed
Rabin, L.A., Paré, N., Saykin, A.J., Brown, M.J., Wishart, H.A., Flashman, L.A., & Santulli, R.B. (2009). Differential memory test sensitivity for diagnosing amnestic mild cognitive impairment and predicting conversion to Alzheimer’s disease. Aging, Neuropsychology, and Cognition, 16(3), 357–376. https://doi.org/10.1080/13825580902825220 CrossRefGoogle ScholarPubMed
Reuter, M., Rosas, H.D., & Fischl, B. (2010). Highly accurate inverse consistent registration: A robust approach. NeuroImage, 53(4), 1181–1196. https://doi.org/10.1016/j.neuroimage.2010.07.020 CrossRefGoogle ScholarPubMed
Rodrigue, K.M., & Raz, N. (2004). Shrinkage of the Entorhinal Cortex over Five Years Predicts Memory Performance in Healthy Adults. Journal of Neuroscience, 24(4), 956–963. https://doi.org/10.1523/JNEUROSCI.4166-03.2004 CrossRefGoogle ScholarPubMed
Rosen, A.C., Prull, M.W., Gabrieli, J.D.E., Stoub, T., O’Hara, R., Friedman, L., … DeToledo-Morrell, L. (2003). Differential Associations between Entorhinal and Hippocampal Volumes and Memory Performance in Older Adults. Behavioral Neuroscience, 117(6), 1150–1160. https://doi.org/10.1037/0735-7044.117.6.1150 CrossRefGoogle ScholarPubMed
Sarazin, M., Chauviré, V., Gerardin, E., Colliot, O., Kinkingnéhun, S., De Souza, L.C., … Dubois, B. (2010). The amnestic syndrome of hippocampal type in Alzheimer’s disease: An MRI study. Journal of Alzheimer’s Disease, 22(1), 285–294. https://doi.org/10.3233/JAD-2010-091150 CrossRefGoogle ScholarPubMed
Ségonne, F., Dale, A.M., Busa, E., Glessner, M., Salat, D., Hahn, H.K., & Fischl, B. (2004). A hybrid approach to the skull stripping problem in MRI. NeuroImage, 22(3), 1060–1075. https://doi.org/10.1016/j.neuroimage.2004.03.032 CrossRefGoogle Scholar
Ségonne, F., Pacheco, J., & Fischl, B. (2007). Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Transactions on Medical Imaging, 26(4), 518–529. https://doi.org/10.1109/TMI.2006.887364 CrossRefGoogle ScholarPubMed
Slachevsky, A., Barraza, P., Hornberger, M., Muñoz-Neira, C., Flanagan, E., Henríquez, F., … Delgado, C. (2017). Neuroanatomical Comparison of the “word” and “picture” Versions of the Free and Cued Selective Reminding Test in Alzheimer’s Disease. Journal of Alzheimer’s Disease, 61(2), 589–600. https://doi.org/10.3233/JAD-160973 CrossRefGoogle Scholar
Sled, J.G., Zijdenbos, A.P., & Evans, A.C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in mri data. IEEE Transactions on Medical Imaging, 17(1), 87–97. https://doi.org/10.1109/42.668698 CrossRefGoogle ScholarPubMed
Tremont, G., Halpert, S., Javorsky, D.J., & Stern, R.A. (2000). Differential impact of executive dysfunction on verbal list learning and story recall. Clinical Neuropsychologist, 14(3), 295–302. https://doi.org/10.1076/1385-4046(200008)14:3;1-P;FT295 CrossRefGoogle ScholarPubMed
Tremont, G., Miele, A., Smith, M.M., & Westervelt, H.J. (2010). Comparison of verbal memory impairment rates in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 32(6), 630–636. https://doi.org/10.1080/13803390903401328 CrossRefGoogle ScholarPubMed
Van Petten, C. (2004). Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: Review and meta-analysis. Neuropsychologia, 42, 1394–1413. https://doi.org/10.1016/j.neuropsychologia.2004.04.006 CrossRefGoogle ScholarPubMed
Wechsler, D. (1945). A standardized memory scale for clinical use. Journal of Psychology, (19), 87–95.CrossRefGoogle Scholar
Wechsler, D. (2009). Wechsler Memory Scale-4th Edition. San San Antonio, TX: The Psychological Corporation.Google Scholar
Wolk, D.A., & Dickerson, B.C. (2011). Fractionating verbal episodic memory in Alzheimer’s disease. NeuroImage, 54(2), 1530–1539. https://doi.org/10.1016/j.neuroimage.2010.09.005 CrossRefGoogle ScholarPubMed
Zahodne, L.B., Bowers, D., Price, C.C., Bauer, R.M., Nisenzon, A., Foote, K.D., & Okun, M.S. (2011). The case for testing memory with both stories and word lists prior to DBS surgery for Parkinson’s disease. Clinical Neuropsychologist, 25(3), 348–358. https://doi.org/10.1080/13854046.2011.562869 CrossRefGoogle ScholarPubMed
Zimmerman, M.E., Pan, J.W., Hetherington, H.P., Katz, M.J., Verghese, J., Buschke, H., … Lipton, R.B. (2008). Hippocampal neurochemistry, neuromorphometry, and verbal memory in nondemented older adults. Neurology, 70(18), 1594–1600. https://doi.org/10.1212/01.wnl.0000306314.77311.be CrossRefGoogle ScholarPubMed