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Visual Object Discrimination Impairment as an Early Predictor of Mild Cognitive Impairment and Alzheimer’s Disease

Published online by Cambridge University Press:  21 May 2019

Leslie S. Gaynor ,
Rosie E. Curiel Cid ,
Ailyn Penate ,
Mónica Rosselli ,
Sara N. Burke ,
Meredith Wicklund ,
David A. Loewenstein  and
Russell M. Bauer
Leslie S. Gaynor*
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA
Rosie E. Curiel Cid
Affiliation:
Department of Psychiatry and Center for Cognitive Neuroscience and Aging, University of Miami Miller School of Medicine, Miami, FL, USA Florida Alzheimer’s Disease Research Center, Gainesville, FL, USA
Ailyn Penate
Affiliation:
Wien Center for Alzheimer’s Disease and Memory Disorders, Miami Beach, FL, USA
Mónica Rosselli
Affiliation:
Florida Alzheimer’s Disease Research Center, Gainesville, FL, USA Department of Psychology, Florida Atlantic University, Boca Raton, FL, USA
Sara N. Burke
Affiliation:
Florida Alzheimer’s Disease Research Center, Gainesville, FL, USA McKnight Brain Institute and Department of Neuroscience, University of Florida, Gainesville, FL, USA
Meredith Wicklund
Affiliation:
Florida Alzheimer’s Disease Research Center, Gainesville, FL, USA Department of Neurology, University of Florida College of Medicine, University of Florida, Gainesville, FL, USA
David A. Loewenstein
Affiliation:
Department of Psychiatry and Center for Cognitive Neuroscience and Aging, University of Miami Miller School of Medicine, Miami, FL, USA Florida Alzheimer’s Disease Research Center, Gainesville, FL, USA
Russell M. Bauer
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA Florida Alzheimer’s Disease Research Center, Gainesville, FL, USA
*
Correspondence and reprint requests to: Leslie S. Gaynor, University of Florida, College of Public Health and Health Professions, P.O. Box 100165, Gainesville, FL 32610, USA, Phone (352) 273-6014, Fax (352) 273-6156. E-mail: lesliesg2@ufl.edu
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Abstract

Objective: Detection of cognitive impairment suggestive of risk for Alzheimer’s disease (AD) progression is crucial to the prevention of incipient dementia. This study was performed to determine if performance on a novel object discrimination task improved identification of earlier deficits in older adults at risk for AD. Method: In total, 135 participants from the 1Florida Alzheimer’s Disease Research Center [cognitively normal (CN), Pre-mild cognitive impairment (PreMCI), amnestic mild cognitive impairment (aMCI), and dementia] completed a test of object discrimination and traditional memory measures in the context of a larger neuropsychological and clinical evaluation. Results: The Object Recognition and Discrimination Task (ORDT) revealed significant differences between the PreMCI, aMCI, and dementia groups versus CN individuals. Moreover, relative risk of being classified as PreMCI rather than CN increased as an inverse function of ORDT score. Discussion: Overall, the obtained results suggest that a novel object discrimination task improves the detection of very early AD-related cognitive impairment, increasing the window for therapeutic intervention. (JINS, 2019, 25, 688–698)

Keywords

Dementiatemporal lobememoryperirhinal cortexvisual perceptionearly diagnosis
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 7 , August 2019 , pp. 688 - 698
Copyright
Copyright © INS. Published by Cambridge University Press, 2019. 

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References

REFERENCES

Alegret, M., Boada-Rovira, M., Vinyes-Junque, G., Valero, S., Espinosa, A., Hernandez, I., & Tarraga, L. (2009). Detection of visuoperceptual deficits in preclinical and mild Alzheimer’s disease. Journal of Clinical and Experimental Neuropsychology, 31(7), 860–867. doi: 10.1080/13803390802595568CrossRefGoogle ScholarPubMed
Barense, M.D., Henson, R.N., Lee, A.C., & Graham, K.S. (2010). Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: effects of viewpoint. Hippocampus, 20(3), 389–401. doi: 10.1002/hipo.20641Google ScholarPubMed
Barense, M.D., Ngo, J.K., Hung, L.H., & Peterson, M.A. (2012). Interactions of memory and perception in amnesia: the figure-ground perspective. Cerebral Cortex, 22(11), 2680–2691. doi: 10.1093/cercor/bhr347CrossRefGoogle ScholarPubMed
Bartko, S.J., Winters, B.D., Cowell, R.A., Saksida, L.M., & Bussey, T.J. (2007). Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks. Learning & Memory, 14(12), 821–832. doi: 10.1101/lm.749207CrossRefGoogle ScholarPubMed
Benedict, R.H.B., Schretlen, D., Groninger, L., & Brandt, J. (2010). Hopkins verbal learning test—revised: normative data and analysis of inter-form and test-retest reliability. The Clinical Neuropsychologist, 12(1), 43–55. doi: 10.1076/clin.12.1.43.1726CrossRefGoogle Scholar
Bilgel, M., An, Y., Lang, A., Prince, J., Ferrucci, L., Jedynak, B., & Resnick, S.M. (2014). Trajectories of Alzheimer disease-related cognitive measures in a longitudinal sample. Alzheimer's & Dementia, 10(6), 735–742.e734. doi: 10.1016/j.jalz.2014.04.520CrossRefGoogle Scholar
Braak, H. & Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica, 82(4), 239–259.CrossRefGoogle ScholarPubMed
Brooks, L.G. & Loewenstein, D.A. (2010). Assessing the progression of mild cognitive impairment to Alzheimer’s disease: current trends and future directions. Alzheimer's Research & Therapy, 2(5), 28. doi: 10.1186/alzrt52Google ScholarPubMed
Buckley, M.J., Booth, M.C., Rolls, E.T., & Gaffan, D. (2001). Selective perceptual impairments after perirhinal cortex ablation. The Journal of Neuroscience, 21(24), 9824–9836.CrossRefGoogle ScholarPubMed
Buckley, M.J. & Gaffan, D. (1997). Impairment of visual object-discrimination learning after perirhinal cortex ablation. Behavioral Neuroscience, 111(3), 467–475.CrossRefGoogle ScholarPubMed
Burke, S.N. & Barnes, C.A. (2006). Neural plasticity in the ageing brain. Nature Reviews Neuroscience, 7(1), 30–40. Retrieved from http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16371948.CrossRefGoogle ScholarPubMed
Burke, S.N., Maurer, A.P., Nematollahi, S., Uprety, A., Wallace, J.L., & Barnes, C.A. (2014). Advanced age dissociates dual functions of the perirhinal cortex. Journal of Neuoscience, 34(2), 467–480.Google ScholarPubMed
Burke, S.N., Wallace, J.L., Hartzell, A.L., Nematollahi, S., Plange, K., & Barnes, C.A. (2011). Age-associated deficits in pattern separation functions of the perirhinal cortex: a cross-species consensus. Behavioral Neuroscience, 125(6), 836–847.CrossRefGoogle ScholarPubMed
Bussey, T.J., Saksida, L.M., & Murray, E.A. (2003). Impairments in visual discrimination after perirhinal cortex lesions: testing “declarative” vs. “perceptual-mnemonic” views of perirhinal cortex function. European Journal of Neuroscience, 17(3), 649–660.CrossRefGoogle ScholarPubMed
Caselli, R.J., Locke, D.E., Dueck, A.C., Knopman, D.S., Woodruff, B.K., Hoffman-Snyder, C., & Reiman, E.M. (2014). The neuropsychology of normal aging and preclinical Alzheimer’s disease. Alzheimer’s & Dementia, 10(1), 84–92. doi: 10.1016/j.jalz.2013.01.004CrossRefGoogle ScholarPubMed
Cowell, R.A., Bussey, T.J., & Saksida, L.M. (2006). Why does brain damage impair memory? A connectionist model of object recognition memory in perirhinal cortex. The Journal of Neuroscience, 26(47), 12186–12197. doi: 10.1523/JNEUROSCI.2818-06.2006CrossRefGoogle ScholarPubMed
Devlin, J.T. & Price, C.J. (2007). Perirhinal contributions to human visual perception. Current Biology, 17(17), 1484–1488. doi: 10.1016/j.cub.2007.07.066CrossRefGoogle ScholarPubMed
Duara, R., Loewenstein, D.A., Greig, M.T., Potter, E., Barker, W., Raj, A., & Potter, H. (2011). Pre-MCI and MCI: neuropsychological, clinical, and imaging features and progression rates. The American Journal of Geriatric Psychiatry, 19(11), 951–960. doi: 10.1097/JGP.0b013e3182107c69CrossRefGoogle ScholarPubMed
Duara, R., Loewenstein, D.A., Shen, Q., Barker, W., Potter, E., Varon, D., & Buckley, C. (2013). Amyloid positron emission tomography with (18)F-flutemetamol and structural magnetic resonance imaging in the classification of mild cognitive impairment and Alzheimer’s disease. Alzheimer’s & Dementia, 9(3), 295–301. doi: 10.1016/j.jalz.2012.01.006CrossRefGoogle ScholarPubMed
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 & Dementia, 11(4), 415–424. doi: 10.1016/j.jalz.2014.03.005CrossRefGoogle ScholarPubMed
Edmonds, E.C., Delano-Wood, L., Jak, A.J., Galasko, D.R., Salmon, D.P., & Bondi, M.W. (2016). “Missed” mild cognitive impairment: high false-negative error rate based on conventional diagnostic criteria. Journal of Alzheimer’s Disease, 52(2), 685–691. doi: 10.3233/jad-150986CrossRefGoogle ScholarPubMed
Elwood, R.W. (1991). The Wechsler Memory Scale-Revised: psychometric characteristics and clinical application. Neuropsychology Review, 2(2), 179–201.CrossRefGoogle ScholarPubMed
Fidalgo, C.O., Changoor, A.T., Page-Gould, E., Lee, A.C., & Barense, M.D. (2016). Early cognitive decline in older adults better predicts object than scene recognition performance. Hippocampus, 26(12), 1579–1592. doi: 10.1002/hipo.22658CrossRefGoogle ScholarPubMed
Gaynor, L.S., Johnson, S.A., Mizell, J.M., Campos, K.T., Maurer, A.P., Bauer, R.M., & Burke, S.N. (2018). Impaired discrimination with intact crossmodal association in aged rats: a dissociation of perirhinal cortical-dependent behaviors. Behavioral Neuroscience, 132, 138–151.CrossRefGoogle ScholarPubMed
Harris, I.M., Egan, G.F., Sonkkila, C., Tochon-Danguy, H.J., Paxinos, G., & Watson, J.D.G. (2018). Selective right parietal lobe activation during mental rotationA parametric PET study. Brain , 123(1), 65–73. doi: 10.1093/brain/123.1.65CrossRefGoogle Scholar
Huber, C.M., Yee, C., May, T., Dhanala, A., & Mitchell, C.S. (2017). Cognitive decline in preclinical Alzheimer’s disease: amyloid-beta versus tauopathy. Journal of Alzheimer’s Disease, 61(1), 265–281. doi: 10.3233/jad-170490CrossRefGoogle Scholar
Johnson, S.A., Sacks, P.K., Turner, S.M., Gaynor, L.S., Ormerod, B.K., Maurer, A.P., & Burke, S.N. (2016). Discrimination performance in aging is vulnerable to interference and dissociable from spatial memory. Learning & Memory, 23, 339–348.CrossRefGoogle ScholarPubMed
Johnson, S.A., Turner, S.M., Santacroce, L.A., Carty, K.N., Shafiq, L., Bizon, J.L., & Burke, S.N. (2017). Rodent age-related impairments in discriminating perceptually similar objects parallel those observed in humans. Hippocampus, 27(7), 759–776. doi: 10.1002/hipo.22729CrossRefGoogle ScholarPubMed
Khan, U.A., Liu, L., Provenzano, F.A., Berman, D.E., Profaci, C.P., Sloan, R., & Small, S.A. (2014). Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer’s disease. Nature Neuroscience, 17(2), 304–311. doi: 10.1038/nn.3606CrossRefGoogle ScholarPubMed
Kivisaari, S.L., Tyler, L.K., Monsch, A.U., & Taylor, K.I. (2012). Medial perirhinal cortex disambiguates confusable objects. Brain, 135(Pt 12), 3757–3769. doi: 10.1093/brain/aws277CrossRefGoogle ScholarPubMed
Krueger, K.R., Lam, C.S., & Wilson, R.S. (2006). The word accentuation test—Chicago. Journal of Clinical and Experimental Neuropsychology, 28(7), 1201–1207. doi: 10.1080/13803390500346603CrossRefGoogle ScholarPubMed
Krumm, S., Kivisaari, S.L., Probst, A., Monsch, A.U., Reinhardt, J., Ulmer, S., & Taylor, K.I. (2016). Cortical thinning of parahippocampal subregions in very early Alzheimer’s disease. Neurobiology of Aging, 38, 188–196. doi: 10.1016/j.neurobiolaging.2015.11.001CrossRefGoogle ScholarPubMed
Kurylo, D.D., Corkin, S., Rizzo Iii, J.F., & Growdon, J.H. (1996). Greater relative impairment of object recognition than of visuospatial abilities in Alzheimer’s disease. Neuropsychology, 10(1), 74–81. doi: 10.1037/0894-4105.10.1.74CrossRefGoogle Scholar
Lee, A.C., Barense, M.D., & Graham, K.S. (2005). The contribution of the human medial temporal lobe to perception: bridging the gap between animal and human studies. The Quarterly Journal of Experimental Psychology. B, Comparative and Physiological Psychology, 58(3–4), 300–325. doi: 10.1080/02724990444000168CrossRefGoogle ScholarPubMed
Lezak, M.D., Howieson, D.B., Loring, D.W., & Fischer, J.S. (2004). Neuropsychological assessment. New York, NY, USA: Oxford University Press.Google Scholar
Loewenstein, D.A., Curiel, R.E., DeKosky, S., Bauer, R.M., Rosselli, M., Guinjoan, S.M., & Duara, R. (2018). Utilizing semantic intrusions to identify amyloid positivity in mild cognitive impairment. Neurology, 91(10), e976–e984. doi: 10.1212/wnl.0000000000006128CrossRefGoogle ScholarPubMed
Loewenstein, D.A., Curiel, R.E., Greig, M.T., Bauer, R.M., Rosado, M., Bowers, D., & Duara, R. (2016). A novel cognitive stress test for the detection of preclinical Alzheimer disease: discriminative properties and relation to amyloid load. The American Journal of Geriatric Psychiatry, 24(10), 804–813. doi: 10.1016/j.jagp.2016.02.056CrossRefGoogle ScholarPubMed
Loewenstein, D.A., Greig, M.T., Schinka, J.A., Barker, W., Shen, Q., Potter, E., & Duara, R. (2012). An investigation of PreMCI: subtypes and longitudinal outcomes. Alzheimer’s & Dementia, 8(3), 172–179. doi: 10.1016/j.jalz.2011.03.002CrossRefGoogle ScholarPubMed
Loonstra, A.S., Tarlow, A.R., & Sellers, A.H. (2001). COWAT metanorms across age, education, and gender. Applied Neuropsychology, 8(3), 161–166. doi: 10.1207/s15324826an0803_5CrossRefGoogle ScholarPubMed
Mason, E.J., Hussey, E.P., Molitor, R.J., Ko, P.C., Donahue, M.J., & Ally, B.A. (2017). Family history of Alzheimer’s disease is associated with impaired perceptual discrimination of novel objects. Journal of Alzheimer’s Disease, 57(3), 735–745. doi: 10.3233/jad-160772CrossRefGoogle ScholarPubMed
Maurer, A.P., Burke, S.N., Diba, K., & Barnes, C.A. (2017). Attenuated activity across multiple cell types and reduced monosynaptic connectivity in the aged perirhinal cortex. The Journal of Neuroscience, 37(37), 8965–8974. doi: 10.1523/jneurosci.0531-17.2017CrossRefGoogle ScholarPubMed
Moyer, J.R. Jr., Furtak, S.C., McGann, J.P., & Brown, T.H. (2011). Aging-related changes in calcium-binding proteins in rat perirhinal cortex. Neurobiology of Aging, 32(9), 1693–1706. doi: 10.1016/j.neurobiolaging.2009.10.001CrossRefGoogle ScholarPubMed
Murray, E.A. & Bussey, T.J. (1999). Perceptual-mnemonic functions of the perirhinal cortex. Trends in Cognitive Sciences, 3(4), 142–151.CrossRefGoogle ScholarPubMed
Newsome, R.N., Duarte, A., & Barense, M.D. (2012). Reducing perceptual interference improves visual discrimination in mild cognitive impairment: implications for a model of perirhinal cortex function. Hippocampus, 22(10), 1990–1999. doi: 10.1002/hipo.22071CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Qiu, W.Y., Yang, Q., Zhang, W., Wang, N., Zhang, D., Huang, Y., & Ma, C. (2017). The correlations between postmortem brain pathologies and cognitive dysfunction in aging and Alzheimer’s disease. Current Alzheimer Research, 15(5), 462–473. doi: 10.2174/1567205014666171106150915CrossRefGoogle Scholar
Rockwood, K., Strang, D., MacKnight, C., Downer, R., & Morris, J.C. (2000). Interrater reliability of the Clinical Dementia Rating in a multicenter trial. Journal of the American Geriatrics Society, 48(5), 558–559.CrossRefGoogle Scholar
Ryan, L., Cardoza, J.A., Barense, M.D., Kawa, K.H., Wallentin-Flores, J., Arnold, W.T., & Alexander, G.E. (2012). Age-related impairment in a complex object discrimination task that engages perirhinal cortex. Hippocampus, 22(10), 1978–1989. doi: 10.1002/hipo.22069CrossRefGoogle Scholar
Schneider, L.S., Mangialasche, F., Andreasen, N., Feldman, H., Giacobini, E., Jones, R., & Kivipelto, M. (2014). Clinical trials and late-stage drug development for Alzheimer’s disease: an appraisal from 1984 to 2014. Journal of Internal Medicine, 275(3), 251–283. doi: 10.1111/joim.12191CrossRefGoogle ScholarPubMed
Snow, W.G., Tierney, M.C., Zorzitto, M.L., Fisher, R.H., & Reid, D.W. (1989). WAIS-R test-retest reliability in a normal elderly sample. Journal of Clinical and Experimental Neuropsychology, 11(4), 423–428. doi: 10.1080/01688638908400903CrossRefGoogle Scholar
Snyder, P.J., Kahle-Wrobleski, K., Brannan, S., Miller, D.S., Schindler, R.J., DeSanti, S., & Carrillo, M.C. (2014). Assessing cognition and function in Alzheimer’s disease clinical trials: do we have the right tools?: Alzheimer’s & Dementia, 10(6), 853–860. doi: 10.1016/j.jalz.2014.07.158CrossRefGoogle ScholarPubMed
Sone, D., Imabayashi, E., Maikusa, N., Okamura, N., Furumoto, S., Kudo, Y., & Matsuda, H. (2017). Regional tau deposition and subregion atrophy of medial temporal structures in early Alzheimer’s disease: a combined positron emission tomography/magnetic resonance imaging study. Alzheimer’s & Dementia (Amst), 9, 35–40. doi: 10.1016/j.dadm.2017.07.001Google ScholarPubMed
Tombaugh, T.N. (2004). Trail Making Test A and B: normative data stratified by age and education. Archives of Clinical Neuropsychology, 19(2), 203–214. doi: 10.1016/s0887-6177(03)00039-8CrossRefGoogle Scholar
Weintraub, S., Salmon, D., Mercaldo, N., Ferris, S., Graff-Radford, N.R., Chui, H., & Morris, J.C. (2009). The Alzheimer’s Disease Centers’ Uniform Data Set (UDS): the neuropsychological test battery. Alzheimer Disease and Associated Disorders, 23(2), 91–101. doi: 10.1097/WAD.0b013e318191c7ddCrossRefGoogle Scholar
Weissberger, G.H., Strong, J.V., Stefanidis, K.B., Summers, M.J., Bondi, M.W., & Stricker, N.H. (2017). Diagnostic accuracy of memory measures in Alzheimer’s dementia and mild cognitive impairment: a systematic review and meta-analysis. Neuropsychology Review, 27(4), 354–388. doi: 10.1007/s11065-017-9360-6CrossRefGoogle ScholarPubMed
Wilkinson, G.S. & Robertson, G. (2006). Wide Range Achievement Test (4th ed.). Lutz, FL: Psychological Assessment Resources.Google Scholar
Woodcock, R.W., Muñoz-Sandoval, A.F., Ruef, M.L., & Alvarado, C.G. (2005). Woodcock language proficiency battery—Revised. Itasca, IL: Riverside.Google Scholar
Yeung, L.K., Ryan, J.D., Cowell, R.A., & Barense, M.D. (2013). Recognition memory impairments caused by false recognition of novel objects. Journal of Experimental Psychology: General, 142(4), 1384–1397. doi: 10.1037/a0034021CrossRefGoogle ScholarPubMed