Ophthalmologic Psychophysical Tests Support OCT Findings in Mild Alzheimer's Disease

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[1] G. D. Rabinovici, W. W. Seeley, E. J. Kim et al., “Distinct MRI atrophy patterns in autopsy-proven Alzheimer’s disease and frontotemporal lobar degeneration,” The American Journal of Alzheimer’s Disease & Other Dementias, vol. 22, no. 6, pp. 474–488, 2007-2008. [2] A. London, I. Benhar, and M. Schwartz, “The retina as a window to the brain—from eye research to CNS disorders,” Nature Reviews Neurology, vol. 9, no. 1, pp. 44–53, 2013. [3] N. Patton, T. Aslam, T. MacGillivray, A. Pattie, I. J. Deary, and B. Dhillon, “Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures,” Journal of Anatomy, vol. 206, no. 4, pp. 319–348, 2005. [4] M. H. Dehabadi, B. M. Davis, T. K. Wong, and M. F. Cordeiro, “Retinal manifestations of Alzheimer’s disease,” Neurodegenerative Disease Management, vol. 4, no. 3, pp. 241–252, 2014. [5] D. R. Hinton, A. A. Sadun, J. C. Blanks, and C. A. Miller, “Opticnerve degeneration in Alzheimer’s disease,” The New England Journal of Medicine, vol. 315, no. 8, pp. 485–487, 1986. [6] J. C. Blanks, D. R. Hinton, A. A. Sadun, and C. A. Miller, “Retinal ganglion cell degeneration in Alzheimer’s disease,” Brain Research, vol. 501, no. 2, pp. 364–372, 1989. [7] J. C. Blanks, S. Y. Schmidt, Y. Torigoe, K. V. Porrello, D. R. Hinton, and R. H. I. Blanks, “Retinal pathology in Alzheimer’s disease. II. Regional neuron loss and glial changes in GCL,” Neurobiology of Aging, vol. 17, no. 3, pp. 385–395, 1996. [8] J. C. Blanks, Y. Torigoe, D. R. Hinton, and R. H. I. Blanks, “Retinal pathology in Alzheimer’s disease. I. Ganglion cell loss in foveal/parafoveal retina,” Neurobiology of Aging, vol. 17, no. 3, pp. 377–384, 1996. [9] E. S. Garcia-Martin, B. Rojas, A. I. Ramirez et al., “Macular thickness as a potential biomarker of mild Alzheimer’s disease,” Ophthalmology, vol. 121, no. 5, pp. 1149–1151, 2014. [10] P. K. Iseri, Ö. Altinas, T. Tokay, and N. Yüksel, “Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease,” Journal of Neuro-Ophthalmology, vol. 26, no. 1, pp. 18–24, 2006. [11] V. Parisi, R. Restuccia, F. Fattapposta, C. Mina, M. G. Bucci, and F. Pierelli, “Morphological and functional retinal impairment in Alzheimer’s disease patients,” Clinical Neurophysiology, vol. 112, no. 10, pp. 1860–1867, 2001. [12] C. Paquet, M. Boissonnot, F. Roger, P. Dighiero, R. Gil, and J. Hugon, “Abnormal retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease,” Neuroscience Letters, vol. 420, no. 2, pp. 97–99, 2007. [13] Y. Lu, Z. Li, X. Zhang et al., “Retinal nerve fiber layer structure abnormalities in early Alzheimer’s disease: evidence in optical coherence tomography,” Neuroscience Letters, vol. 480, no. 1, pp. 69–72, 2010. [14] F. Berisha, G. T. Feke, C. L. Trempe, J. W. McMeel, and C. L. Schepens, “Retinal abnormalities in early Alzheimer’s disease,” Investigative Ophthalmology and Visual Science, vol. 48, no. 5, pp. 2285–2289, 2007. [15] R. Kromer, N. Serbecic, L. Hausner, F. Aboul-Enein, L. Froelich, and S. C. Beutelspacher, “Detection of retinal nerve fiber layer defects in Alzheimer’s disease using SD-OCT,” Frontiers in Psychiatry, vol. 5, article 22, 2014. [16] A. Kesler, V. Vakhapova, A. D. Korczyn, E. Naftaliev, and M. Neudorfer, “Retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease,” Clinical Neurology and Neurosurgery, vol. 113, no. 7, pp. 523–526, 2011. [17] C. Y. Cheung, Y. T. Ong, S. Hilal et al., “Retinal ganglion cell analysis using high-definition optical coherence tomography in patients with mild cognitive impairment and Alzheimer’s disease,” Journal of Alzheimer’s Disease, vol. 45, no. 1, pp. 45–56, 2015. [18] E. O. Oktem, E. Derle, S. Kibaroglu, C. Oktem, I. Akkoyun, and U. Can, “The relationship between the degree of cognitive impairment and retinal nerve fiber layer thickness,” Neurological Sciences, 2015. [19] D. Liu, L. Zhang, Z. Li et al., “Thinner changes of the retinal nerve fiber layer in patients with mild cognitive impairment and Alzheimer’s disease,” BMC Neurology, vol. 15, article 14, 2015. [20] M. Koronyo-Hamaoui, Y. Koronyo, A. V. Ljubimov et al., “Identification of amyloid plaques in retinas from Alzheimer’s patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model,” NeuroImage, vol. 54, no. 1, pp. S204–S217, 2011. [21] Y. Tsai, B. Lu, A. V. Ljubimov et al., “Ocular changes in TGF344-AD rat model of Alzheimer’s disease,” Investigative Ophthalmology and Visual Science, vol. 55, no. 1, pp. 523–534, 2014. [22] B. Liu, S. Rasool, Z. Yang et al., “Amyloid-peptide vaccinations reduce β-amyloid plaques but exacerbate vascular deposition and inflammation in the retina of Alzheimer’s transgenic mice,” The American Journal of Pathology, vol. 175, no. 5, pp. 2099–2110, 2009. [23] U. Kayabasi, R. Sergott, and M. Rispoli, “Retinal examination for the diagnosis of Alzheimer’s disease,” Journal of Clinical Ophthalmology and Research, vol. 3, article 4, 2014. [24] M. C. Campbell, D. DeVries, L. Emptage et al., “Polarization properties of amyloid beta in the retina of the eye as a biomarker of Alzheimer’s disease,” in Bio-Optics: Design and Application, p. BM3A.4, OSA Publishing, 2015. [25] Y. Koronyo, B. C. Salumbides, K. L. Black, and M. KoronyoHamaoui, “Alzheimer’s disease in the retina: Imaging retinal aβ plaques for early diagnosis and therapy assessment,” Neurodegenerative Diseases, vol. 10, no. 1–4, pp. 285–293, 2012. [26] P. R. Hof and J. H. Morrison, “Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: II. Primary and secondary visual cortex,” Journal of Comparative Neurology, vol. 301, no. 1, pp. 55–64, 1990. [27] G. L. Trick, L. R. Trick, P. Morris, and M. Wolf, “Visual field loss in senile dementia of the Alzheimer’s type,” Neurology, vol. 45, no. 1, pp. 68–74, 1995. [28] R. Steffes and J. Thralow, “Visual field limitation in the patient with dementia of the Alzheimer’s type,” Journal of the American Geriatrics Society, vol. 35, no. 3, pp. 198–204, 1987. [29] S. L. Risacher, D. WuDunn, S. M. Pepin et al., “Visual contrast sensitivity in Alzheimer’s disease, mild cognitive impairment, and older adults with cognitive complaints,” Neurobiology of Aging, vol. 34, no. 4, pp. 1133–1144, 2013. [30] A. Cronin-Golomb, R. Sugiura, S. Corkin, and J. H. Growdon, “Incomplete Achromatopsia in Alzheimer’s disease,” Neurobiology of Aging, vol. 14, no. 5, pp. 471–477, 1993. [31] M. Pache, C. H. W. Smeets, P. F. Gasio et al., “Colour vision deficiencies in Alzheimer’s disease,” Age and Ageing, vol. 32, no. 4, pp. 422–426, 2003. [32] G. Salamone, C. Di Lorenzo, S. Mosti et al., “Color discrimination performance in patients with Alzheimer’s disease,” Dementia and Geriatric Cognitive Disorders, vol. 27, no. 6, pp. 501–507, 2009. [33] K. Krasodomska, W. Lubinski, A. Potemkowski, and K. Honczarenko, “Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease,” Documenta Ophthalmologica, vol. 121, no. 2, pp. 111–121, 2010. [34] G. L. Trick, M. C. Barris, and M. Bickler-Bluth, “Abnormal pattern electroretinograms in patients with senile dementia of the Alzheimer type,” Annals of Neurology, vol. 26, no. 2, pp. 226–231, 1989. [35] A. Cronin-Golomb, J. F. Rizzo, S. Corkin, and J. H. Growdon, “Visual function in Alzheimer’s disease and normal aging,” Annals of the New York Academy of Sciences, vol. 640, pp. 28–35, 1991. [36] V. Lakshminarayanan, J. Lagrave, M. L. Kean, M. Dick, and R. Shankle, “Vision in dementia: contrast effects,” Neurological Research, vol. 18, no. 1, pp. 9–15, 1996. [37] S. A. Neargarder, E. R. Stone, A. Cronin-Golomb, and S. Oross, “The impact of acuity on performance of four clinical measures of contrast sensitivity in Alzheimer’s disease,” Journals of Gerontology, Series B: Psychological Sciences and Social Sciences, vol. 58, no. 1, pp. P54–P62, 2003. [38] D. A. Valenti, “Alzheimer’s disease: visual system review,” Optometry, vol. 81, no. 1, pp. 12–21, 2010. [39] I. B. Wollner and S. P. Diamond, “The measurement of spatial contrast sensitivity in cases of blurred vision associated with cerebral lesions,” Brain, vol. 99, no. 4, pp. 695–710, 1976. [40] G. Schlotterer, M. Moscovitch, and D. Crapper-McLachlan, “Visual processing deficits as assessed by spatial frequency contrast sensitivity and backward masking in normal ageing and Alzheimer’s disease,” Brain, vol. 107, no. 1, pp. 309–324, 1984. [41] C. E. Wright, N. Drasdo, and G. F. A. Harding, “Pathology of the optic nerve and visual association areas. Information given by the flash and pattern visual evoked potential, and the temporal and spatial contrast sensitivity function,” Brain, vol. 110, no. 1, pp. 107–120, 1987. [42] A. Cronin-Golomb, S. Corkin, and J. H. Growdon, “Contrast sensitivity in Alzheimer’s disease,” Journal of the Optical Society of America A, vol. 4, p. 7, 1987. [43] L. Gao, Y. Liu, X. Li, Q. Bai, and P. Liu, “Abnormal retinal nerve fiber layer thickness and macula lutea in patients with mild cognitive impairment and Alzheimer’s disease,” Archives of Gerontology and Geriatrics, vol. 60, no. 1, pp. 162–167, 2015. [44] E. Marziani, S. Pomati, P. Ramolfo et al., “Evaluation of retinal nerve fiber layer and ganglion cell layer thickness in Alzheimer’s disease using spectral-domain optical coherence tomography,” Investigative Ophthalmology & Visual Science, vol. 54, no. 9, pp. 5953–5958, 2013. [45] B. Reisberg, S. H. Ferris, M. J. de Leon, and T. Crook, “The global deterioration scale for assessment of primary degenerative dementia,” The American Journal of Psychiatry, vol. 139, no. 9, pp. 1136–1139, 1982. [46] L. Rami, M. Serradell, B. Bosch, A. Villar, and J. L. Molinuevo, “Perception Digital Test (PDT) for the assessment of incipient visual disorder in initial Alzheimer’s disease,” Neurologia, vol. 22, no. 6, pp. 342–347, 2007. [47] A. Roth, Test-28 hue de Roth selon Farnsworth-Munsell (Manual), Luneau, Paris, France, 1966. [48] D. Farnsworth and M. Color, The Farnsworth-Munsell 100-Hue Test for the Examination of Color Discrimination, Munsell Color Company, 1957. [49] A. Cronin-Golomb, G. C. Gilmore, S. Neargarder, S. R. Morrison, and T. M. Laudate, “Enhanced stimulus strength improves visual cognition in aging and Alzheimer’s disease,” Cortex, vol. 43, no. 7, pp. 952–966, 2007. [50] A. Cronin-Golomb, S. Corkin, J. F. Rizzo, J. Cohen, J. H. Growdon, and K. S. Banks, “Visual dysfunction in Alzheimer’s disease: relation to normal aging,” Annals of Neurology, vol. 29, no. 1, pp. 41–52, 1991. [51] G. C. Gilmore and P. J. Whitehouse, “Contrast sensitivity in Alzheimer’s disease: a 1-year longitudinal analysis,” Optometry & Vision Science, vol. 72, no. 2, pp. 83–91, 1995. [52] D. N. Levine, J. M. Lee, and C. M. Fisher, “The visual variant of Alzheimer’s disease: a clinicopathologic case study,” Neurology, vol. 43, no. 2, pp. 305–313, 1993. [53] M. F. Mendez, R. L. Tomsak, and B. Remler, “Disorders of the visual system in Alzheimer’s disease,” Journal of Clinical NeuroOphthalmology, vol. 10, no. 1, pp. 62–69, 1990. [54] M. Rizzo and M. Nawrot, “Perception of movement and shape in Alzheimer’s disease,” Brain, vol. 121, no. 12, pp. 2259–2270, 1998. [55] A. A. Sadun, M. Borchert, E. DeVita, D. R. Hinton, and C. J. Bassi, “Assessment of visual impairment in patients with Alzheimer’s disease,” The American Journal of Ophthalmology, vol. 104, no. 2, pp. 113–120, 1987. [56] C. Murgatroyd and R. Prettyman, “An investigation of visual hallucinosis and visual sensory status in dementia,” International Journal of Geriatric Psychiatry, vol. 16, no. 7, pp. 709–713, 2001. [57] M. S. Livingstone and D. H. Hubel, “Psychophysical evidence for separate channels for the perception of form, color, movement, and depth,” The Journal of Neuroscience, vol. 7, no. 11, pp. 3416–3468, 1987. [58] C. J. Bassi, K. Solomon, and D. Young, “Vision in aging and dementia,” Optometry & Vision Science, vol. 70, no. 10, pp. 809–813, 1993. [59] R. W. Crow, L. B. Levin, L. LaBree, R. Rubin, and S. E. Feldon, “Sweep visual evoked potential evaluation of contrast sensitivity in Alzheimer’s dementia,” Investigative Ophthalmology& Visual Science, vol. 44, no. 2, pp. 875–878, 2003. [60] F. K. Cormack, M. Tovee, and C. Ballard, “Contrast sensitivity and visual acuity in patients with Alzheimer’s disease,” International Journal of Geriatric Psychiatry, vol. 15, no. 7, pp. 614–620, 2000. [61] J. T. Hutton, J. L. Morris, J. W. Elias, and J. N. Poston, “Contrast sensitivity dysfunction in Alzheimer’s disease,” Neurology, vol. 43, no. 11, pp. 2328–2330, 1993. [62] D. R. Baker, M. F. Mendez, J. C. Townsend, P. F. Ilsen, and D. C. Bright, “Optometric management of patients with Alzheimer’s disease,” Journal of the American Optometric Association, vol. 68, no. 8, pp. 483–494, 1997. [63] G. C. Gilmore, A. Cronin-Golomb, S. A. Neargarder, and S. R. Morrison, “Enhanced stimulus contrast normalizes visual processing of rapidly presented letters in Alzheimer’s disease,” Vision Research, vol. 45, no. 8, pp. 1013–1020, 2005. [64] S. Wood, K. F. Mortel, M. Hiscock, B. G. Breitmeyer, and J. S. Caroselli, “Adaptive and maladaptive utilization of color cues by patients with mild to moderate Alzheimer’s disease,” Archives of Clinical Neuropsychology, vol. 12, no. 5, pp. 483–489, 1997. [65] F. Massoud, H. Chertkow, V. Whitehead, O. Overbury, and H. Bergman, “Word-reading thresholds in Alzheimer disease and mild memory loss: a pilot study,” Alzheimer Disease & Associated Disorders, vol. 16, no. 1, pp. 31–39, 2002. [66] A. Cronin-Golomb, S. Corkin, and J. H. Growdon, “Visual dysfunction predicts cognitive deficits in Alzheimer’s disease,” Optometry & Vision Science, vol. 72, no. 3, pp. 168–176, 1995. [67] J. F. Rizzo III, A. Cronin-Golomb, J. H. Growdon et al., “Retinocalcarine function in Alzheimer’s disease: a clinical and electrophysiological study,” Archives of Neurology, vol. 49, no. 1, pp. 93–101, 1992. [68] A. Cronin-Golomb, S. Corkin, and J. H. Growdon, “Visual dysfunction predicts cognitive deficits in Alzheimer’s disease,” Optometry and Vision Science, vol. 72, no. 3, pp. 168–176, 1995. [69] P. R. Martin, A. J. R. White, A. K. Goodchild, H. D. Wilder, and A. E. Sefton, “Evidence that blue-on cells are part of the third geniculocortical pathway in primates,” European Journal of Neuroscience, vol. 9, no. 7, pp. 1536–1541, 1997. [70] D. M. Dacey and B. B. Lee, “The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type,” Nature, vol. 367, no. 6465, pp. 731–735, 1994. [71] K. L. Possin, “Visual spatial cognition in neurodegenerative disease,” Neurocase, vol. 16, no. 6, pp. 466–487, 2010. [72] A. L. Benton, Contributions to Neuropsychological Assessment: A Clinical Manual, Oxford University Press, Oxford, UK, 1994.
Abstract
Purpose. To analyze in mild Alzheimer's disease (MAD) patients, GDS-4 (Reisberg Scale), whether or not some psychophysical tests (PTs) support OCT macular findings in the same group of MAD patients reported previously. Methods. Twenty-three MAD patients and 28 age-matched control subjects with mean Mini Mental State Examination of 23.3 and 28.2, respectively, with no ocular disease or systemic disorders affecting vision were included. Best-corrected visual acuity (VA), contrast sensitivity (CS) (3, 6, 12, and 18 cpds), color perception (CP), and perception digital test (PDT) were tested in one eye of each patient. Results. In comparison with the controls, MAD patients presented (i) a significant decrease in VA, PDT, and CS for all spatial frequencies analyzed, especially the higher ones, and (ii) a significant increase in unspecific errors on the blue axis (P < 0.05 in all instances). In MAD patients, a wide a ROC curve was plotted in all PTs. Conclusions. In MAD, CS, VA, and the tritan axis in CP were impaired. The PTs with the greatest predictive value are the higher spatial frequencies in CS and tritan unspecific errors in CP. PT abnormalities are consistent with the structural findings reported in the same MAD patients using OCT.
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Copyright © 2015 Elena Salobrar-Garcia et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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