Publication Cover
Aging, Neuropsychology, and Cognition
A Journal on Normal and Dysfunctional Development
Volume 30, 2023 - Issue 5
1,878
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Procedural learning and retention relative to explicit learning and retention in mild cognitive impairment and Alzheimer’s disease using a modification of the trail making test

, , , , , , , , , , , & show all
Pages 669-686 | Received 07 Dec 2021, Accepted 09 May 2022, Published online: 22 May 2022

References

  • Albert, M. S., DeKosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., Phelps, C. H., Holtzman, D. M., Jagust, W. J., Petersen, R. C., Snyder, P. J., Carrillo, M. C., Thies, B., & Phelps, C. H. (2013). The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the national institute on aging-Alzheimer’s association workgroups on diagnostic guidelines for Alzheimer’s disease. Focus, 11(1), 96–106. doi:https://doi.org/10.1176/appi.focus.11.1.96
  • Allain, H., Lieury, A., Quemener, V., Thomas, V., Reymann, J. M., & Gandon, J. M. (1995). Procedural memory and Parkinson’s disease. Dementia and Geriatric Cognitive Disorders, 6(3), 174–178. doi:https://doi.org/10.1159/000106942
  • Baker, R., Bentham, P., & Kourtzi, Z. (2015). Learning to predict is spared in mild cognitive impairment due to Alzheimer’s disease. Experimental Brain Research, 233(10), 2859–2867. doi:https://doi.org/10.1007/s00221-015-4356-z
  • Beaunieux, H., Eustache, F., Busson, P., De La Sayette, V., Viader, F., & Desgranges, B. (2012). Cognitive procedural learning in early Alzheimer’s disease: Impaired processes and compensatory mechanisms. Journal of Neuropsychology, 6(1), 31–42. doi:https://doi.org/10.1111/j.1748-6653.2011.02002.x
  • Bondi, M. W., & Kaszniak, A. W. (1991). Implicit and explicit memory in Alzheimer’s disease and Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 13(2), 339–358. doi:https://doi.org/10.1080/01688639108401048
  • 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 & Therapy, 7(1), 1–10 doi:10.1186/s13195-015-0147-9.
  • Cobia, D., Rich, C., Smith, M. J., Mamah, D., Csernansky, J. G., & Wang, L. (2021). Basal ganglia shape features differentiate schizoaffective disorder from schizophrenia. Psychiatry Research: Neuroimaging, 317, 111352. doi:https://doi.org/10.1016/j.pscychresns.2021.111352
  • Cohen, N. J., & Squire, L. R. (1980). Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science, 210(4466), 207–210. doi:https://doi.org/10.1126/science.7414331
  • De Wit, L., Marsiske, M., O’Shea, D., Kessels, R. P., Kurasz, A. M., DeFeis, B., Smith, G. E., & Smith, G. E. (2021). Procedural learning in individuals with amnestic mild cognitive Impairment and Alzheimer’s dementia: A systematic review and meta-analysis. Neuropsychology Review, 31(1), 103–114. doi:https://doi.org/10.1007/s11065-020-09449-1
  • Delis, D. C., Kramer, J. H., Kaplan, E. (2000). California verbal learning test - second edition. Adult Version. Manual.
  • Devanand, D. P., Bansal, R., Liu, J., Hao, X., Pradhaban, G., & Peterson, B. S. (2012). MRI hippocampal and entorhinal cortex mapping in predicting conversion to Alzheimer’s disease. Neuroimage, 60(3), 1622–1629. doi:https://doi.org/10.1016/j.neuroimage.2012.01.075
  • Deweer, B., Pillon, B., Michon, A., & Dubois, B. (1993). Mirror reading in AlzheimerAlzheimer’s disease: normal skill learning and acquisition of item-specific information. Journal of Clinical and Experimental Neuropsychology, 15(5), 789–804. doi:https://doi.org/10.1080/01688639308402596
  • Deweer, B., Ergis, A. M., Fossati, P., Pillon, B., Boller, F., Agid, Y., & Dubois, B. (1994). Explicit memory, procedural learning and lexical priming in Alzheimer’s disease. Cortex, 30(1), 113–126. doi:https://doi.org/10.1016/S0010-9452(13)80327-9
  • Di Paola, M., Macaluso, E., Carlesimo, G. A., Tomaiuolo, F., Worsley, K. J., Fadda, L., & Caltagirone, C. (2007). Episodic memory impairment in patients with Alzheimer’s disease is correlated with entorhinal cortex atrophy. Journal of Neurology, 254(6), 774–781. doi:https://doi.org/10.1007/s00415-006-0435-1
  • Dick, M. B., Nielson, K. A., Beth, R. E., Shankle, W. R., & Cotman, C. W. (1995). Acquisition and long-term retention of a fine motor skill in Alzheimer's-disease. Brain and Cognition, 29(3), 294–306. doi:https://doi.org/10.1006/brcg.1995.1283
  • Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., Benali, H., & Benali, H. (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behavioural Brain Research, 199(1), 61–75. doi:https://doi.org/10.1016/j.bbr.2008.11.012
  • Du, A. T., Schuff, N., Amend, D., Laakso, M. P., Hsu, Y. Y., Jagust, W. J., … Weiner, M. W. (2001). Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 71(4), 441–447. doi:https://doi.org/10.1136/jnnp.71.4.441
  • Duara, R., Loewenstein, D. A., et-al, P. E., Appel, J., Greig, M. T., Urs, R., Shen, Q., Raj, A., Small, B., Barker, W., Schofield, E., Wu, Y., & Potter, H. (2008). Medial temporal lobe atrophy on MRI scans and the diagnosis of Alzheimer disease. Neurology, 71(24), 1986–1992. doi:https://doi.org/10.1212/01.wnl.0000336925.79704.9f
  • Eslinger, P. J., & Damasio, A. R. (1986). Preserved motor learning in Alzheimer’s disease: implications for anatomy and behavior. Journal of Neuroscience, 6(10), 3006–3009. doi:https://doi.org/10.1523/JNEUROSCI.06-10-03006.1986
  • Ezzati, A., Zammit, A. R., Habeck, C., Hall, C. B., & Lipton, R. B. (2020). Detecting biological heterogeneity patterns in ADNI amnestic mild cognitive impairment based on volumetric MRI. Brain Imaging and Behavior, 14(5), 1792–1804. doi:https://doi.org/10.1007/s11682-019-00115-6
  • 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(2), 351–356. doi:https://doi.org/10.2214/ajr.149.2.351
  • Folstein, M., McHugh, P., & 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), 189–198. doi:https://doi.org/10.1016/0022-3956(75)90026-6
  • Gabrieli, J. D. E., Corkin, S., Mickel, S. F., & Growdon, J. H. (1993). Intact acquisition and long-term retention of mirror-tracing in Alzheimer’s disease and global amnesia. Behavioral Neuroscience, 107(6), 899–910. doi:https://doi.org/10.1037/0735-7044.107.6.899
  • Gobel, E. W., Blomeke, K., Zadikoff, C., Simuni, T., Weintraub, S., & Reber, P. J. (2013). Implicit perceptual-motor skill learning in mild cognitive impairment and Parkinson’s disease. Neuropsychology, 27(3), 314. doi:https://doi.org/10.1037/a0032305
  • Graf, P., Squire, L. R., & Mandler, G. (1984). The information that amnesic patients do not forget. Journal of Experimental Psychology. Learning, Memory, and Cognition, 10(1), 164. doi:https://doi.org/10.1037//0278-7393.https://doi.org/10.1.164
  • Grober, E., Ausubel, R., Sliwinski, M., & Gordon, B. (1992). Skill learning and repetition priming in Alzheimer’s disease. Neuropsychologia, 30(10), 849–858. doi:https://doi.org/10.1016/0028-3932(92)90030-P
  • Haut, M. W., Hogg, J. P., Marshalek, P. J., Suter, B. C., & Miller, L. E. (2017). Amnesia associated with bilateral hippocampal and bilateral basal ganglia lesions in anoxia with stimulant use. Frontiers in Neurology, 8, 27. doi:https://doi.org/10.3389/fneur.2017.00027
  • Hays, C. C., Zlatar, Z. Z., Meloy, M. J., Bondi, M. B., Gilbert, P. E., Lui, T. H., L, J., & Wierenga, C. W. (2020). Interaction of APOE, cerebral blood flow, and cortical thickness in the entorhinal cortex predicts memory decline. Brain Imaging and Behavior, 14(2), 369–382. doi:https://doi.org/10.1007/s11682-019-00245-x
  • Hong, Y., Alvarado, R. L., Jog, A., Greve, D. N., & Salat, D. H. (2020). Serial reaction time task performance in older adults with neuropsychologically defined mild cognitive impairment. Journal of Alzheimer’s Disease, 74(2), 491–500. doi:https://doi.org/10.3233/JAD-191323
  • Huo, Y., Zhoubing, X., Aboud, K., Parvathaneni, P., Bao, S., Bermudez, C., Resnick, S. M., Cutting, L. E., & Landman, B. A. 2018“Spatially localized atlas network tiles enables 3D whole brain segmentation” In International Conference on Medical Image Computing and Computer-Assisted Intervention, MICCAI (Cham: Springer) .
  • Huo, Y., Xu, Z., Xiong, Y., Aboud, K., Parvathaneni, P., Bao, S., Landman, B. A., Resnick, S. M., Cutting, L. E., & Landman, B. A. (2019). 3D whole brain segmentation using spatially localized atlas network tiles. NeuroImage, 194, 105–119. doi:https://doi.org/10.1016/j.neuroimage.2019.03.041
  • Kaplan, E., Goodglass, H., & Weintraub, S. (2001). Boston naming test. PRO-ED Inc.
  • Killiany, R. J., Hyman, B. T., t, G.-I., Moss, M. B., Kikinis, R., Jolesz, F., Tanzi, R., Jones, K., & Albert, M. S. (2002). MRI measures of entorhinal cortex vs. hippocampus in preclinical AD. Neurology, 58(8), 1188–1196. doi:https://doi.org/10.1212/WNL.58.8.1188
  • Knopman, D. (1991). Long-term retention of implicitly acquired learning in patients with Alzheimer’s disease. Journal of Clinical and Experimental Neuropsychology, 13(6), 880–894 doi:10.1080/01688639108405105.
  • Knowlton, B. J., Mangels, J. A., & Squire, L. R. (1996). A neostriatal habit learning system in humans. Science, 273(5280), 1399–1402. doi:https://doi.org/10.1126/science.273.5280.1399
  • Koedam, E. L., Lehmann, M., van der Flier, W. M., Scheltens, P., Pijnenburg, Y. A. L., Fox, N., Barkhof, F., & Wattjes, M. P. (2011). Visual assessment of posterior atrophy development of a MRI rating scale. European Radiology, 21(12), 2618–2625. doi:https://doi.org/10.1007/s00330-011-2205-4
  • Laakso, M. P., Soininen, H., Partanen, K., Helkala, E. L., Hartikainen, P., Vainio, P., Riekkinen, P. J., Sr, Hänninen, T., & Riekkinen Sr, P. J. (1995). Volumes of hippocampus, amygdala and frontal lobes in the MRI-based diagnosis of early Alzheimer’s disease: Correlation with memory functions. Journal of Neural transmission-Parkinson’s Disease and Dementia Section, 9(1), 73–86. doi:https://doi.org/10.1007/BF02252964
  • Lehmann, M., Koedam, E. L., et-al, B. J., Bartlett, J. W., Ryan, N. S., Pijnenburg, Y. A. L., Barkhof, F., Wattjes, M. P., Scheltens, P., & Fox, N. C. (2012). Posterior cerebral atrophy in the absence of medial temporal lobe atrophy in pathologically-confirmed Alzheimer’s disease. Neurobiology of Aging, 33(3), 627.e1–627.e12. doi:https://doi.org/10.1016/j.neurobiolaging.2011.04.003
  • Libon, D. J., Bogdanoff, B., Cloud, B. S., Skalina, S., Giovannetti, T., Gitlin, H. L., & Bonavita, J. (1998). Declarative and procedural learning, quantitative measures of the hippocampus, and subcortical white alterations in Alzheimer’s disease and ischaemic vascular dementia. Journal of Clinical and Experimental Neuropsychology, 20(1), 30–41. doi:https://doi.org/10.1076/jcen.20.1.30.1490
  • Luft, C. D. B., Baker, R., Bentham, P., & Kourtzi, Z. (2015). Learning temporal statistics for sensory predictions in mild cognitive impairment. Neuropsychologia, 75, 368–380. doi:https://doi.org/10.1016/j.neuropsychologia.2015.06.002
  • McKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R., Jr, Kawas, C. H., Klunk, W. E., Koroshetz, W. J., Manly, J. J., Mayeux, R., Mohs, R. C., Morris, J. C., Rossor, M. N., Scheltens, P., Carrillo, M. C., Thies, B., Weintraub, S., & Phelps, C. H. (2011). The diagnosis of dementia due to Alzheimer’s disease: recommendations from the national institute on aging‐Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 263–269. doi:https://doi.org/10.1016/j.jalz.2011.03.005
  • Merbah, S., Salmon, E., & Meulemans, T. (2011). Impaired acquisition of a mirror-reading skill in Alzheimer’s disease. Cortex, 47(2), 157–165. doi:https://doi.org/10.1016/j.cortex.2009.11.006
  • Milner, B., Corkin, S., & Teuber, H. L. (1968). Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of HM. Neuropsychologia, 6(3), 215–234. doi:https://doi.org/10.1016/0028-3932(68)90021-3
  • Mochizuki-Kawai, H., Kawamura, M., Hasegawa, Y., Mochizuki, S., Oeda, R., Yamanaka, K., & Tagaya, H. (2004). Deficits in long-term retention of learned motor skills in patients with cortical or subcortical degeneration. Neuropsychologia, 42(13), 1858–1863. doi:https://doi.org/10.1016/j.neuropsychologia.2004.03.012
  • Nettiksimmons, J., DeCarli, C., Landau, S., & Beckett, L., & Alzheimer’s Disease Neuroimaging Initiative. (2014). Biological heterogeneity in ADNI amnestic mild cognitive impairment. Alzheimer’s & Dementia, 10(5), 511–521. doi:https://doi.org/10.1016/j.jalz.2013.09.003
  • Oudman, E., Nijboer, T. C., Postma, A., Wijnia, J. W., & Van der Stigchel, S. (2015). Procedural learning and memory rehabilitation in Korsakoff’s syndrome-a review of the literature. Neuropsychology Review, 25(2), 134–148. doi:https://doi.org/10.1007/s11065-015-9288-7
  • Pfeffer, R. I., Kurosaki, T. T., Harrah, C. H., Chance, J. M., & Filos, S. (1982). Measurement of functional activities in older adults in the community. Journal of Gerontology, 37(3), 323–329. doi: https://doi.org/10.1093/geronj/37.3.323
  • Reitan, R. M., & Wolfson, D. (1985). The Halstead–Reitan Neuropsycholgical Test Battery: Therapy and clinical interpretation. Tucson, AZ: Neuropsychological Press.
  • Rouleau, I., Salmon, D. P., & Vrbancic, M. (2002). Learning, retention and generalization of a mirror tracing skill in Alzheimer’s disease. Journal of Clinical and Experimental Neuropsychology, 24(2), 239–250. doi:https://doi.org/10.1076/jcen.24.2.239.997
  • Sarazin, M., Deweer, B., Merkl, A., Von Poser, N., Pillon, B., & Dubois, B. (2002). Procedural learning and striatofrontal dysfunction in Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 17(2), 265–273. doi:https://doi.org/10.1002/mds.10018
  • Sheikh, J. I., & Yesavage, J. A. (1986). Geriatric depression scale (GDS): recent evidence and development of a shorter version. Clinical Gerontologist: The Journal of Aging and Mental Health, 5(1–2), 165–173. doi: https://doi.org/10.1300/J018v05n01_09
  • Smith, M. J., Cobia, D. J., Wang, L., Alpert, K. I., Cronenwett, W. J., Goldman, M. B., and Csernansky, J. G. (2014). Cannabis-related working memory deficits and associated subcortical morphological differences in healthy individuals and schizophrenia subjects. Schizophrenia Bulletin, 40(2), 287–299.
  • Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171–177. doi:https://doi.org/10.1016/j.nlm.2004.06.005
  • Tulving, E. (1985). How many memory systems are there? American Psychologist, 40(4), 385. doi:https://doi.org/10.1037/0003-066X.40.4.385
  • Vakil, E., Kahan, S., Huberman, M., & Osimani, A. (2000). Motor and non-motor sequence learning in patients with basal ganglia lesions: The case of serial reaction time (SRT). Neuropsychologia, 38(1), 1–10. doi:https://doi.org/10.1016/S0028-3932(99)00058-5
  • van Halteren-van Tilborg, I. A., Scherder, E. J., & Hulstijn, W. (2007). Motor-skill learning in Alzheimer’s disease: A review with an eye to the clinical practice. Neuropsychology Review, 17(3), 203–212. doi:https://doi.org/10.1007/s11065-007-9030-1
  • Wahlund, L. O., Julin, P., Johansson, S. E., & Scheltens, P. (2000). Visual rating and volumetry of the medial temporal lobe on magnetic resonance imaging in dementia: A comparative study. Journal of Neurology Neurosurgery Psychiatry, 69(5), 630–635. doi:https://doi.org/10.1136/jnnp.69.5.630
  • Wechsler, D. (2008). Wechsler adult intelligence scale - fourth edition. Psychological Corporation: San Antonio, TX, USA.
  • Wilkinson, G. S., & Robertson, G. J. (2006). WRAT 4: wide range achievement test. Lutz, FL: Psychological Assessment Resources.
  • Ystad, M. A., Lundervold, A. J., Wehling, E., Espeseth, T., Rootwelt, H., Westlye, L. T., & Lundervold, A. (2009). Hippocampal volumes are important predictors for memory function in elderly women. BMC Medical Imaging, 9(1), 1–15. doi:https://doi.org/10.1186/1471–2342-9-17
  • Zanetti, O., Zanieri, G., Giovanni, G. D., De Vreese, L. P., Pezzini, A., Metitieri, T., & Trabucchi, M. (2001). Effectiveness of procedural memory stimulation in mild Alzheimer’s disease patients: A controlled study. Neuropsychological Rehabilitation, 11(3–4), 263–272. doi:https://doi.org/10.1080/09602010042000088