Table of Contents Author Guidelines Submit a Manuscript
Journal of Ophthalmology
Volume 2015, Article ID 736949, 10 pages
http://dx.doi.org/10.1155/2015/736949
Research Article

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

1Instituto de Investigaciones Oftalmológicas Ramón Castroviejo, Universidad Complutense de Madrid, Madrid, Spain
2Facultad de Óptica, Universidad Complutense de Madrid, Madrid, Spain
3Facultad de Medicina, Universidad Complutense de Madrid, Madrid, Spain
4Hospital Clínico San Carlos, Madrid, Spain

Received 19 February 2015; Accepted 20 May 2015

Academic Editor: Hermann Mucke

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.

Linked References

  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  5. D. R. Hinton, A. A. Sadun, J. C. Blanks, and C. A. Miller, “Optic-nerve degeneration in Alzheimer's disease,” The New England Journal of Medicine, vol. 315, no. 8, pp. 485–487, 1986. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  10. P. K. Iseri, Ö. Altinaş, 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Google Scholar
  25. Y. Koronyo, B. C. Salumbides, K. L. Black, and M. Koronyo-Hamaoui, “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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Krasodomska, W. Lubiński, 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  38. D. A. Valenti, “Alzheimer's disease: visual system review,” Optometry, vol. 81, no. 1, pp. 12–21, 2010. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  53. M. F. Mendez, R. L. Tomsak, and B. Remler, “Disorders of the visual system in Alzheimer's disease,” Journal of Clinical Neuro-Ophthalmology, vol. 10, no. 1, pp. 62–69, 1990. View at Google Scholar · View at Scopus
  54. M. Rizzo and M. Nawrot, “Perception of movement and shape in Alzheimer's disease,” Brain, vol. 121, no. 12, pp. 2259–2270, 1998. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  71. K. L. Possin, “Visual spatial cognition in neurodegenerative disease,” Neurocase, vol. 16, no. 6, pp. 466–487, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. A. L. Benton, Contributions to Neuropsychological Assessment: A Clinical Manual, Oxford University Press, Oxford, UK, 1994.