Hostname: page-component-cb9f654ff-mnl9s Total loading time: 0 Render date: 2025-08-11T03:59:30.998Z Has data issue: false hasContentIssue false
  • English
  • Français

Residual abilities in age-related macular degeneration to process spatial frequencies during natural scene categorization

Published online by Cambridge University Press:  22 December 2011

BENOIT MUSEL ,
RUXANDRA HERA ,
SYLVIE CHOKRON ,
DAVID ALLEYSSON ,
CHRISTOPHE CHIQUET ,
JEAN-PAUL ROMANET ,
NATHALIE GUYADER  and
CAROLE PEYRIN
BENOIT MUSEL*
Affiliation:
Laboratoire de Psychologie et NeuroCognition, Centre National de la Recherche Scientifique UMR 5105, Université Pierre Mendès France, Grenoble, France
RUXANDRA HERA
Affiliation:
Service d’ophtalmologie, CHU Albert Michalon, Grenoble, France
SYLVIE CHOKRON
Affiliation:
Laboratoire de Psychologie et NeuroCognition, Centre National de la Recherche Scientifique UMR 5105, Université Pierre Mendès France, Grenoble, France Unité Fonctionnelle Vision et Cognition, Fondation Ophtalmologique Rothschild, Paris, France
DAVID ALLEYSSON
Affiliation:
Laboratoire de Psychologie et NeuroCognition, Centre National de la Recherche Scientifique UMR 5105, Université Pierre Mendès France, Grenoble, France
CHRISTOPHE CHIQUET
Affiliation:
Service d’ophtalmologie, CHU Albert Michalon, Grenoble, France
JEAN-PAUL ROMANET
Affiliation:
Service d’ophtalmologie, CHU Albert Michalon, Grenoble, France
NATHALIE GUYADER
Affiliation:
Grenoble-Image-Parole-Signal-Automatique (GIPSA-lab), CNRS UMR 5216, Grenoble, France
CAROLE PEYRIN
Affiliation:
Laboratoire de Psychologie et NeuroCognition, Centre National de la Recherche Scientifique UMR 5105, Université Pierre Mendès France, Grenoble, France
*
*Address correspondence and reprint requests to: Benoit Musel, Laboratoire de Psychologie et NeuroCognition, CNRS UMR 5105, Université Pierre Mendès France, BP 47 38040 Grenoble Cedex, France. E-mail: benoit.musel@upmf-grenoble.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

Age-related macular degeneration (AMD) is characterized by a central vision loss. We explored the relationship between the retinal lesions in AMD patients and the processing of spatial frequencies in natural scene categorization. Since the lesion on the retina is central, we expected preservation of low spatial frequency (LSF) processing and the impairment of high spatial frequency (HSF) processing. We conducted two experiments that differed in the set of scene stimuli used and their exposure duration. Twelve AMD patients and 12 healthy age-matched participants in Experiment 1 and 10 different AMD patients and 10 healthy age-matched participants in Experiment 2 performed categorization tasks of natural scenes (Indoors vs. Outdoors) filtered in LSF and HSF. Experiment 1 revealed that AMD patients made more no-responses to categorize HSF than LSF scenes, irrespective of the scene category. In addition, AMD patients had longer reaction times to categorize HSF than LSF scenes only for indoors. Healthy participants’ performance was not differentially affected by spatial frequency content of the scenes. In Experiment 2, AMD patients demonstrated the same pattern of errors as in Experiment 1. Furthermore, AMD patients had longer reaction times to categorize HSF than LSF scenes, irrespective of the scene category. Again, spatial frequency processing was equivalent for healthy participants. The present findings point to a specific deficit in the processing of HSF information contained in photographs of natural scenes in AMD patients. The processing of LSF information is relatively preserved. Moreover, the fact that the deficit is more important when categorizing HSF indoors, may lead to new perspectives for rehabilitation procedures in AMD.

Keywords

Low visionIndoor/OutdoorLow spatial frequencyHigh spatial frequencyVisual categorization

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 6 , November 2011 , pp. 529 - 541
Copyright
Copyright © Cambridge University Press 2011

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.)

Article purchase

Temporarily unavailable

References

Baker, C.I., Dilks, D.D., Peli, E. & Kanwisher, N. (2008). Reorganization of visual processing in macular degeneration: Replication and clues about the role of foveal loss. Vision Research 48, 1910–1919.Google Scholar
Baker, C.I., Peli, E., Knouf, N. & Kanwisher, N.G. (2005). Reorganization of visual processing in macular degeneration. The Journal of Neuroscience 25, 614–618.Google Scholar
Boucard, C.C., Hernowo, A.T., Maguire, R.P., Jansonius, N.M., Roerdink, J.B., Hooymans, J.M. & Cornelissen, F.W. (2009). Changes in cortical grey matter density associated with long-standing retinal visual field defects. Brain 132, 1898–1906.Google Scholar
Boucart, M., Despretz, P., Hladiuk, K. & Desmettre, T. (2008 a). Does context or color improve object recognition in patients with low vision? Visual Neuroscience 25, 685–691.Google Scholar
Boucart, M., Dinon, J.F., Despretz, P., Desmettre, T., Hladiuk, K. & Oliva, A. (2008 b). Recognition of facial emotion in age related macular degeneration (AMD): A flexible usage of facial features. Visual Neuroscience 25, 1–7.Google Scholar
Brody, B.L., Gamst, A.C., Williams, R.A., Smith, A.R., Lau, P.W., Dolnak, D., Rapaport, M.H., Kaplan, R.M. & Brown, S.I. (2001). Depression, visual acuity, comorbidity, and disability associated with age-related macular degeneration. Ophthalmology 108, 1893–1900.Google Scholar
Brown, M.M., Brown, G.C., Sharma, S., Landy, J. & Bakal, J. (2002). Quality of life with visual acuity loss from diabetic retinopathy and age-related macular degeneration. Archives of Ophthalmology 120, 481–484.Google Scholar
Bullimore, M.A., Bailey, I.L. & Wacker, R.T. (1991). Face recognition in age-related maculopathy. Investigative Ophthalmology and Visual Science 32, 2020–2029.Google Scholar
Calford, M.B., Wright, L.L., Metha, A.B. & Taglianetti, V. (2003). Topographic plasticity in primary visual cortex is mediated by local corticocortical connections. The Journal of Neuroscience 23, 6434–6442.Google Scholar
Callaway, E.M. (2005). Neural substrates within primary visual cortex for interactions between parallel visual pathways. Progress in Brain Research 149, 59–64.Google Scholar
Campbell, F.W. & Green, D.G. (1965). Optical and retinal factors affecting visual resolution. The Journal of Physiology 181, 576–593.Google Scholar
Cavézian, C., Gaudy, I., Perez, C., Coubard, O., Doucet, G., Peyrin, C., Marendaz, C., Obadia, M., Gout, O. & Chokron, S. (2010). Specific impairments in visual processing following lesion side in hemianopic patients. Cortex 46, 1123–1131.Google Scholar
Cheung, S.H. & Legge, G.E. (2005). Functional and cortical adaptations to central vision loss. Visual Neuroscience 22, 187–201.Google Scholar
Chino, Y.M., Smith, E.L., Kaas, J.H., Sasaki, Y. & Cheng, H. (1995). Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats. The Journal of Neuroscience 15, 2417–2433.Google Scholar
Curcio, A.C., Kenneth, R.S. & Robert, E.K. (1990). Human receptor topography. The Journal of Comparative Neurology 292, 497–523.Google Scholar
Dacey, D. & Packer, O. (2003). Colour coding in the primate retina: Diverse cell types and cone-specific circuitry. Current Opinion in Neurobiology 13, 421–427.Google Scholar
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545–559.Google Scholar
Faubert, J. & Overbury, O. (2000). Binocular vision in older people with adventitious visual impairment: Sometimes one eye is better than two. Journal of the American Geriatrics Society 48, 375–380.Google Scholar
Fine, E.M. & Peli, E. (1995). Scrolled and rapid serial visual presentation texts are read at similar rates by the visually impaired. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 12, 2286–2292.Google Scholar
Fletcher, D.C., Schuchard, R.A. & Watson, G. (1999). Relative locations of macular scotomas near the PRL: Effect on low vision reading. Journal of Rehabilitation Research and Development 36, 356–364.Google Scholar
Friedman, D.S., O’Colmain, B.J., Munoz, B., Tomany, S.C., McCarty, C., de Jong, P.T., Nemesure, B., Mitchell, P. & Kempen, J. (2004). Prevalence of age-related macular degeneration in the United States. Archives of Ophthalmology 122, 565–572.Google Scholar
Gilbert, C.D. & Wiesel, T.N. (1992). Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152.Google Scholar
Ginsburg, A.P. (1986). Spatial filtering and visual form perception. In Handbook of Perception and Human Performance, Vol. 2, ed. Boff, K., Kauman, L. & Thomas, J. New York: Wiley.Google Scholar
Guyader, N., Chauvin, A., Peyrin, C., Herault, J. & Marendaz, C. (2004). Image phase or amplitude? Rapid scene categorization is an amplitude-based process. Comptes Rendus Biologies 327, 313–318.Google Scholar
Hassan, S.E., Lovie-Kitchin, J.E. & Woods, R.L. (2002). Vision and mobility performance of subjects with age-related macular degeneration. Optometry and Vision Science 79, 697–707.Google Scholar
Heinen, S.J. & Skavenski, A.A. (1991). Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey. Experimental Brain Research 83, 670–674.Google Scholar
Hera, R., Keramidas, M., Peoc’H, M., Mouillon, M., Romanet, J.P. & Feige, J. (2005). Expression of VEGF and angiopoietins in subfoveal membranes from patients with age-related macular degeneration. American Journal of Ophthalmology 139, 589–596.Google Scholar
Horton, J.C. & Hocking, D.R. (1998). Monocular core zones and binocular border strips in primate striate cortex revealed by the contrasting effects of enucleation, eyelid suture and retinal laser lesions on cytochrome oxidase activity. The Journal of Neuroscience 18, 5433–5455.Google Scholar
Hughes, H.C., Nozawa, G. & Kitterle, F.L. (1996). Global precedence, spatial frequency channels, and the statistic of the natural image. Journal of Cognitive Neuroscience 8, 197–230.Google Scholar
Kaas, J.H., Krubitzer, L.A., Chino, Y.M., Langston, A.L., Polley, E.H. & Blair, N. (1990). Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229–231.Google Scholar
Keck, T., Mrsic-flogel, T.D., Afonso, M.V., Eysel, U.T., Bonhoeffer, T. & Hübener, M. (2008). Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nature Neuroscience 11, 1162–1167.Google Scholar
Klein, R., Klein, B.E. & Linton, K.L. (1992). Prevalence of age-related maculopathy. The Beaver Dam Eye Study. Ophthalmology 99, 933–943.Google Scholar
Klein, R., Peto, T., Bird, A. & Vannewkirk, M. (2004). The epidemiology of age-related macular degeneration. American Journal of Ophthalmology 137, 486–495.Google Scholar
Kleiner, R.C., Enger, C., Alexander, M.E. & Fine, S.L. (1988). Contrast sensitivity in age-related macular degeneration. Archives of Ophthalmology 106, 55–57.Google Scholar
Kulkarni, A.D. & Kuppermann, B.D. (2005). Wet age-related macular degeneration. Advanced Drug Delivery Reviews 57, 1994–2009.Google Scholar
Lee, S.C., Telkes, I. & Grünert, U. (2005). S-cones do not contribute to the OFF-midget pathway in the retina of the marmoset, Callithrix jacchus. The European Journal of Neuroscience 22, 437–447.Google Scholar
Legge, G.E., Ross, J.A., Isenberg, L.M. & LaMay, J.M. (1992). Psychophysics of reading. XII. Clinical predictors of low vision reading speed. Investigative Ophthalmology and Visual Science 33, 677–687.Google Scholar
Legge, G.E., Rubin, G.S., Pelli, D.G. & Schleske, M.M. (1985). Psychophysics of reading II. Vision Research 25, 253–265.Google Scholar
Mangione, C.M., Gutierrez, P.R., Lowe, G., Orav, E.J. & Seddon, J.M. (1999). Influence of age-related maculopathy on visual functioning and health-related quality of life. American Journal of Ophthalmology 128, 45–53.Google Scholar
Midena, E., Degli Angeli, C., Blarzino, M.C., Valenti, M. & Segato, T. (1997). Macular function impairment in eyes with early age-related macular degeneration. Investigative Ophthalmology and Visual Science 38, 469–477.Google Scholar
Mitchell, J. & Bradley, C. (2006). Quality of life in age-related macular degeneration: A review of the literature. Health and Quality of Life Outcomes 4, 97.Google Scholar
Murakami, I., Komatsu, H. & Kinoshita, M. (1997). Perceptual filling in at the scotoma following a monocular retinal lesion in the monkey. Visual Neuroscience 4, 89–101.Google Scholar
Osterberg, G.A. (1935). Topography of the layer of rods and cones in the human retina. Acta Ophthalmologica 13, 1–97.Google Scholar
Peli, E. (1994). Image enhancement for the visually impaired: The effect of enhancement on face recognition. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 11, 1029–1039.Google Scholar
Penfold, P.L., Madigan, M.C., Gillies, M.C. & Provis, J.M. (2001). Immunological and aetiological aspects of macular degeneration. Progress in Retinal and Eye Research 20, 385–414.Google Scholar
Peyrin, C., Baciu, M., Segebarth, C. & Marendaz, C. (2004). Cerebral regions and hemispheric specialization for processing spatial frequencies during natural scene recognition, an event-related fMRI study. NeuroImage 23, 698–707.Google Scholar
Peyrin, C., Chauvin, A., Chokron, S. & Marendaz, C. (2003). Hemispheric specialization for spatial frequency processing in the analysis of natural scenes. Brain and Cognition 53, 278–282.Google Scholar
Peyrin, C., Chokron, S., Guyader, N., Gout, O., Moret, J. & Marendaz, C. (2006 a). Neural correlates of spatial frequency processing: A neuropsychological approach. Brain Research 74, 1–10.Google Scholar
Peyrin, C., Mermillod, M., Chokron, S. & Marendaz, C. (2006 b). Effect of temporal constraints on hemispheric asymmetries during spatial frequency processing. Brain and Cognition 62, 214–220.Google Scholar
Peyrin, C., Michel, C.M., Schwartz, S., Thut, G., Seghier, M., Landis, T., Marendaz, C. & Vuilleumier, P. (2010). The neural substrates and timing of top-down processes during coarse-to-fine categorization of visual scenes: A combined fMRI and ERP study. Journal of Cognitive Neuroscience 22, 2768–2780.Google Scholar
Rosenholtz, R., Li, Y. & Nakano, L. (2007. Measuring visual clutter. Journal of Vision 7, 1–22.Google Scholar
Rovner, B.W. & Casten, R.J. (2002). Activity loss and depression in age-related macular degeneration. The American Journal of Geriatric Psychiatry 10, 305–310.Google Scholar
Salive, M.E., Guralnik, J., Glynn, R.J., Christen, W., Wallace, R.B. & Ostfeld, A.M. (1994). Association of visual impairment with mobility and visual function. Journal of the American Geriatrics Society 42, 287–292.Google Scholar
Schyns, P.G. & Oliva, A. (1999). Dr. Angry and Mr. Smile: When categorization flexibly modifies the perception of faces in rapid visual presentations. Cognition 69, 243–265.Google Scholar
Seiple, W., Szlyk, J.P., McMahon, T., Pulido, J.S. & Fishman, G.A. (2005). Eye movement training for reading in patients with age-related macular degeneration. Investigative Ophthalmology and Visual Science 46, 2886–2896.Google Scholar
Shams, L. & von der Malsburg, C. (2002). The role of complex cells in object recognition. Vision Research 42, 2547–2554.Google Scholar
Smirnakis, S.M., Brewer, A.A., Schmid, M.C., Tolias, A.S., Schüz, A., Augath, M., Inhoffen, W., Wandell, B.A. & Logothetis, N.K. (2005). Lack of long-term cortical reorganization after macaque retinal lesions. Nature 435, 300–307.Google Scholar
Sunness, J., Liu, T. & Yantis, S. (2004). Retinotopic mapping of the visual cortex using functional magnetic resonance imaging in a patient with central scotomas from atrophic macular degeneration. Ophthalmology 111, 1595–1598.Google Scholar
Tejeria, L., Harper, R.A., Artes, P.H. & Dickinson, C.M. (2002). Face recognition in age related macular degeneration: Perceived disability, measured disability, and performance with a bioptic device. The British Journal of Ophthalmology 86, 1019–1026.Google Scholar
Torralba, A. & Oliva, A. (2003). Statistics of natural images categories. Network: Computation in Neural Systems 14, 391–412.Google Scholar
Tran, T.H.C., Rambaud, C., Despretz, P. & Boucart, M. (2010). Scene perception in age-related macular degeneration (AMD). Investigative Ophthalmology and Visual Science 51, 6868–6874.Google Scholar
Van Essen, D.C. & DeYoe, E.A. (1995). Concurrent processing in the primate visual cortex. In The Cognitive Neurosciences, ed. Gazzaniga, M., pp. 383–400. Cambridge: Bradford Book.Google Scholar
Vingerling, J.R., Dielemans, I., Hofman, A., Grobbee, D.E., Hijmering, M., Kramer, C.F. & de Jong, P.T. (1995). The prevalence of age-related maculopathy in the Rotterdam study. Ophthalmology 102, 205–210.Google Scholar
Wang, Y., Wilson, E., Locke, K.G. & Edwards, A.O. (2002). Shape discrimination in age-related macular degeneration. Investigative Ophthalmology and Visual Science 43, 2055–2062.Google Scholar
West, S.K., Munoz, B. & Rubin, G.S. (1997). Function and visual impairment in a population-based study of older adults. The SEE project. Salisbury Eye Evaluation. Investigative Ophthalmology and Visual Science 38, 72–84.Google Scholar
Williams, R.A., Brody, B.L., Thomas, R.G., Kaplan, R.M. & Brown, S.J. (1998). The psychosocial impact of macular degeneration. Archives of Ophthalmology 116, 514–520.Google Scholar
Wright, V. & Watson, G.R. (1995). Learning to Use Your Vision for Reading: Workbook. Lilburn, Georgia: Bear Consultants.Google Scholar
Young, W. (1987). Pathophysiology of age-related macular degeneration. Survey of Ophthalmology 31, 291–306.Google Scholar