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Age-related macular degeneration changes the processing of visual scenes in the brain

Published online by Cambridge University Press:  19 March 2018

STEPHEN RAMANOËL ,
SYLVIE CHOKRON ,
RUXANDRA HERA ,
LOUISE KAUFFMANN ,
CHRISTOPHE CHIQUET ,
ALEXANDRE KRAINIK  and
CAROLE PEYRIN
STEPHEN RAMANOËL
Affiliation:
Univ. Grenoble Alpes, CNRS, LPNC, 38000 Grenoble, France Univ. Grenoble Alpes, Inserm, CHU Grenoble, GIN, 38000 Grenoble, France
SYLVIE CHOKRON
Affiliation:
UMR 8242, Laboratoire de Psychologie de la Perception, Université Paris-Descartes & CNRS, Paris, France Unité Vision & Cognition, Fondation Ophtalmologique Rothschild, Paris, France
RUXANDRA HERA
Affiliation:
Alpes Retine, Montbonnot Saint Martin, France
LOUISE KAUFFMANN
Affiliation:
Univ. Grenoble Alpes, CNRS, LPNC, 38000 Grenoble, France
CHRISTOPHE CHIQUET
Affiliation:
Department of Ophthalmology, University Hospital, Grenoble, France
ALEXANDRE KRAINIK
Affiliation:
Univ. Grenoble Alpes, Inserm, CHU Grenoble, GIN, 38000 Grenoble, France Department of Neuroradiology and MRI, CHU Grenoble Alpes, Grenoble, France CHU Grenoble Alpes, University Grenoble Alpes, CNRS UMS 3552, Inserm US17, IRMaGe, Grenoble, France
CAROLE PEYRIN*
Affiliation:
Univ. Grenoble Alpes, CNRS, LPNC, 38000 Grenoble, France
*
*Address correspondence to: Carole Peyrin, Laboratoire de Psychologie et NeuroCognition (LPNC), Université Grenoble Alpes, BSHM - 1251 Av Centrale CS40700, 38058 Grenoble Cedex 9, France. E-mail: carole.peyrin@univ-grenoble-alpes.fr
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Abstract

In age-related macular degeneration (AMD), the processing of fine details in a visual scene, based on a high spatial frequency processing, is impaired, while the processing of global shapes, based on a low spatial frequency processing, is relatively well preserved. The present fMRI study aimed to investigate the residual abilities and functional brain changes of spatial frequency processing in visual scenes in AMD patients. AMD patients and normally sighted elderly participants performed a categorization task using large black and white photographs of scenes (indoors vs. outdoors) filtered in low and high spatial frequencies, and nonfiltered. The study also explored the effect of luminance contrast on the processing of high spatial frequencies. The contrast across scenes was either unmodified or equalized using a root-mean-square contrast normalization in order to increase contrast in high-pass filtered scenes. Performance was lower for high-pass filtered scenes than for low-pass and nonfiltered scenes, for both AMD patients and controls. The deficit for processing high spatial frequencies was more pronounced in AMD patients than in controls and was associated with lower activity for patients than controls not only in the occipital areas dedicated to central and peripheral visual fields but also in a distant cerebral region specialized for scene perception, the parahippocampal place area. Increasing the contrast improved the processing of high spatial frequency content and spurred activation of the occipital cortex for AMD patients. These findings may lead to new perspectives for rehabilitation procedures for AMD patients.

Keywords

RetinaOccipital cortexParahippocampal place areaSpatial frequencyContrast
Type
Research Article
Information
Visual Neuroscience , Volume 35 , 2018 , E006
Copyright
Copyright © Cambridge University Press 2018 

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References

Aminoff, E., Gronau, N. & Bar, M. (2007). The parahippocampal cortex mediates spatial and nonspatial associations. Cerebral Cortex 17, 1493–1503.Google Scholar
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.CrossRefGoogle ScholarPubMed
Baker, C.I., Peli, E., Knouf, N. & Kanwisher, N.G. (2005). Reorganization of visual processing in macular degeneration. Journal of Neuroscience 25, 614–618.CrossRefGoogle ScholarPubMed
Botelho, E.P., Ceriatte, C., Soares, J.G., Gattass, R. & Fiorani, M. (2014). Quantification of early stages of cortical reorganization of the topographic map of V1 following retinal lesions in monkeys. Cerebral Cortex 24, 1–16.CrossRefGoogle ScholarPubMed
Boucart, M., Despretz, P., Hladiuk, K. & Desmettre, T. (2008a). 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. (2008b). Recognition of facial emotion in low vision: A flexible usage of facial features. Visual Neuroscience 25, 603–609.CrossRefGoogle ScholarPubMed
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
Brown, B. & Lovie-Kitchin, J. (1993). Repeated visual acuity measurement: Establishing the patient’s own criterion for change. Optometry and Vision Science 70, 45–53.Google Scholar
Bullimore, M.A., Bailey, I.L. & Wacker, R.T. (1991). Face recognition in age-related maculopathy. Investigative Ophthalmology & Visual Science 32, 2020–2029.Google ScholarPubMed
Burge, W.K., Griffis, J.C., Nenert, R., Elkhetali, A., DeCarlo, D.K., ver Hoef, L.W., Rosse, L.A. & Visscher, K.M. (2016). Cortical thickness in human V1 associated with central vision loss. Scientific Reports 6, 23268.Google Scholar
Cheung, S.H. & Legge, G.E. (2005). Functional and cortical adaptations to central vision loss. Visual Neuroscience 22, 187–201.CrossRefGoogle ScholarPubMed
Chino, Y.M., Smith, E.L. 3rd, Kaas, J.H., Sasaki, Y. & Cheng, H. (1995). Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats. Journal of Neuroscience 15, 2417–2433.CrossRefGoogle ScholarPubMed
Crawford, J.R., Garthwaite, P.H. & Porter, S. (2010). Point and interval estimates of effect sizes for the case-controls design in neuropsychology: Rationale, methods, implementations, and proposed reporting standards. Cognitive Neuropsychology 27, 245–260.Google Scholar
Crawford, J.R. & Howell, D.C. (1998). Regression equations in clinical neuropsychology: An evaluation of statistical methods for comparing predicted and obtained scores. Journal of Clinical and Experimental Neuropsychology 20, 755–762.Google Scholar
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 292, 497–523.CrossRefGoogle ScholarPubMed
Delcourt, C., Lacroux, A., Carriere, I. & Group, P.S. (2005). The three-year incidence of age-related macular degeneration: The “Pathologies Oculaires Liees a l’Age” (POLA) prospective study. American Journal of Ophthalmology 140, 924–926.Google Scholar
Dilks, D.D., Julian, J.B., Peli, E. & Kanwisher, N. (2014). Reorganization of visual processing in age-related macular degeneration depends on foveal loss. Optometry and Vision Science 91, e199–206.Google Scholar
Elliott, D.B. (1987). Contrast sensitivity decline with ageing: A neural or optical phenomenon? Ophthalmic and Physiological Optics 7, 415–419.Google Scholar
Elliott, S.L. & Werner, J.S. (2010). Age-related changes in contrast gain related to the M and P pathways. Journal of Vision 10, 1-15.Google Scholar
Elliott, D., Whitaker, D. & MacVeigh, D. (1990). Neural contribution to spatiotemporal contrast sensitivity decline in healthy ageing eyes. Vision Research 30, 541–547. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/2339508.Google Scholar
Elliott, D.B., Yang, K.C. & Whitaker, D. (1995). Visual acuity changes throughout adulthood in normal, healthy eyes: Seeing beyond 6/6. Optometry and Vision Science 72, 186–191.Google Scholar
Epstein, R., Harris, A., Stanley, D. & Kanwisher, N. (1999). The parahippocampal place area: Recognition, navigation, or encoding? Neuron 23, 115–125.Google Scholar
Epstein, R. & Kanwisher, N. (1998). A cortical representation of the local visual environment. Nature 392, 598–601.Google Scholar
Field, D.J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. Journal of the Optical Society of America A 4, 2379–2394.CrossRefGoogle ScholarPubMed
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. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7500210.CrossRefGoogle 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 ScholarPubMed
Frezzotti, P., Giorgio, A., Motolese, I., De Leucio, A., Lester, M., Motolese, E., Frederico, A. & De Stefano, N. (2014). Structural and functional brain changes beyond visual system in patients with advanced glaucoma. PLoS One 9, e105931.CrossRefGoogle ScholarPubMed
Friedman, D.S., O’Colmain, B.J., Munoz, B., Tomany, S.C., McCarty, C., de Jong, P.T., Nemesure, B., Mitchell, P., Kempen, J. & Eye Diseases Prevalence Research Group (2004). Prevalence of age-related macular degeneration in the United States. Archives of Ophthalmology 122, 564–572.Google Scholar
Friston, K.J., Holmes, A.P., Poline, J.B., Grasby, P.J., Williams, S.C., Frackowiak, R.S. & Turner, R. (1995). Analysis of fMRI time-series revisited. NeuroImage 2, 45–53.CrossRefGoogle ScholarPubMed
Gittings, N.S. & Fozard, J.L. (1986). Age related changes in visual acuity. Experimental Gerontology 21, 423–433.Google Scholar
Grill-Spector, K. & Malach, R. (2004). The human visual cortex. Annual Review of Neuroscience 27, 649–677.CrossRefGoogle ScholarPubMed
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
Henriksson, L., Nurminen, L., Hyvarinen, A. & Vanni, S. (2008). Spatial frequency tuning in human retinotopic visual areas. Journal of Vision 8, 1–13.CrossRefGoogle ScholarPubMed
Higgins, K.E., Jaffe, M.J., Caruso, R.C. & deMonasterio, F.M. (1988). Spatial contrast sensitivity: Effects of age, test-retest, and psychophysical method. Journal of the Optical Society of America A 5, 2173–2180.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. Journal of Neuroscience 18, 5433–5455.CrossRefGoogle ScholarPubMed
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
Kauffmann, L., Ramanoël, S., Guyader, N., Chauvin, A. & Peyrin, C. (2015). Spatial frequency processing in scene-selective cortical regions. NeuroImage 112, 86–95.CrossRefGoogle ScholarPubMed
Klein, R., Klein, B.E., Jensen, S.C. & Meuer, S.M. (1997). The five-year incidence and progression of age-related maculopathy: The beaver dam eye study. Ophthalmology 104, 7–21.Google Scholar
Legge, G.E., Ross, J.A., Isenberg, L.M. & LaMay, J.M. (1992). Psychophysics of reading. Clinical predictors of low-vision reading speed. Investigative Ophthalmology & Visual Science 33, 677–687.Google Scholar
Liu, T., Cheung, S.H., Schuchard, R.A., Glielmi, C.B., Hu, X., He, S. & Legge, G.E. (2010). Incomplete cortical reorganization in macular degeneration. Investigative Ophthalmology & Visual Science 51, 6826–6834.Google Scholar
Martins Rosa, A., Silva, M.F., Ferreira, S., Murta, J. & Castelo-Branco, M. (2013). Plasticity in the human visual cortex: An ophthalmology-based perspective. BioMed Research International 2013, 568354.Google ScholarPubMed
Masuda, Y., Dumoulin, S.O., Nakadomari, S. & Wandell, B.A. (2008). V1 projection zone signals in human macular degeneration depend on task, not stimulus. Cerebral Cortex 18, 2483–2493.Google Scholar
Moshtael, H., Aslam, T., Underwood, I. & Dhillon, B. (2015). High tech aids low vision: A review of image processing for the visually impaired. Translational Vision Science & Technology 4, 6.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 14, 89–101.Google Scholar
Musel, B., Bordier, C., Dojat, M., Pichat, C., Chokron, S., Le Bas, J.F. & Peyrin, C. (2013). Retinotopic and lateralized processing of spatial frequencies in human visual cortex during scene categorization. Journal of Cognitive Neuroscience 25, 1315–1331.Google Scholar
Musel, B., Hera, R., Chokron, S., Alleysson, D., Chiquet, C., Romanet, J.P., Guyader, N. & Peyrin, C. (2011). Residual abilities in age-related macular degeneration to process spatial frequencies during natural scene categorization. Visual Neuroscience 28, 529–541.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
Owsley, C. (2011). Aging and vision. Vision Research 51, 1610–1622.Google Scholar
Owsley, C., Sekuler, R. & Siemsen, D. (1983). Contrast sensitivity throughout adulthood. Vision Research 23, 689–699.Google Scholar
Peli, E., Lee, E., Trempe, C.L. & Buzney, S. (1994). Image enhancement for the visually impaired: The effects of enhancement on face recognition. Journal of the Optical Society of America A: Optics, Image Science, and Vision 11, 1929–1939.Google Scholar
Peyrin, C., Ramanoël, S., Roux-Sibilon, A., Chokron, S. & Hera, R. (2017). Scene perception in age-related macular degeneration: Effect of spatial frequencies and contrast in residual vision. Vision Research 130, 36–47.CrossRefGoogle ScholarPubMed
Prins, D., Plank, T., Baseler, H.A., Gouws, A.D., Beer, A., Morland, A.B., Greenlee, M.W. & Cornelissen, F.W. (2016). Surface-based analyses of anatomical properties of the visual cortex in macular degeneration. PLoS One 11, e0146684.Google Scholar
Rajimehr, R., Devaney, K.J., Bilenko, N.Y., Young, J.C. & Tootell, R.B. (2011). The “parahippocampal place area” responds preferentially to high spatial frequencies in humans and monkeys. PLoS Biology 9, e1000608.Google Scholar
Ramanoël, S., Kauffmann, L., Cousin, E., Dojat, M. & Peyrin, C. (2015). Age-related differences in spatial frequency processing during scene categorization. PLoS One 10, e0134554.Google Scholar
Rovner, B.W. & Casten, R.J. (2002). Activity loss and depression in age-related macular degeneration. American Journal of Geriatric Psychiatry 10, 305–310. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11994218.Google Scholar
Rubin, G.S., West, S.K., Munoz, B., Bandeen-Roche, K., Zeger, S., Schein, O. & Fried, L.P. (1997). A comprehensive assessment of visual impairment in a population of older Americans. The SEE Study. Salisbury Eye Evaluation Project. Investigative Ophthalmology & Visual Science 38, 557–568.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 physical function. Journal of the American Geriatrics Society 42, 287–292.Google Scholar
Sasaki, Y., Hadjikhani, N., Fischl, B., Liu, A.K., Marrett, S., Dale, A.M. & Tootell, R.B. (2001). Local and global attention are mapped retinotopically in human occipital cortex. Proceedings of the National Academy of Sciences of the United States of America 98, 2077–2082.CrossRefGoogle ScholarPubMed
Schumacher, E.H., Jacko, J.A., Primo, S.A., Main, K.L., Moloney, K.P., Kinzel, E.N. & Ginn, J. (2008). Reorganization of visual processing is related to eccentric viewing in patients with macular degeneration. Restorative Neurology and Neuroscience 26, 391–402.Google Scholar
Sekuler, R., Hutman, L.P. & Owsley, C.J. (1980). Human aging and spatial vision. Science 209, 1255–1256. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/7403884.Google Scholar
Smirnakis, S.M., Brewer, A.A., Schmid, M.C., Tolias, A.S., Schuz, 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.CrossRefGoogle ScholarPubMed
Sunness, J.S., 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. British Journal of Ophthalmology 86, 1019–1026.CrossRefGoogle ScholarPubMed
Thibaut, M., Tran, T.H., Szaffarczyk, S. & Boucart, M. (2014). The contribution of central and peripheral vision in scene categorization: A study on people with central vision loss. Vision Research 98, 46–53.Google Scholar
Tran, T.H., Despretz, P. & Boucart, M. (2012). Scene perception in age-related macular degeneration: The effect of contrast. Optometry and Vision Science 89, 419–425.Google Scholar
Tran, T.H., Guyader, N., Guerin, A., Despretz, P. & Boucart, M. (2011). Figure ground discrimination in age-related macular degeneration. Investigative Ophthalmology & Visual Science 52, 1655–1660.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
Wandell, B.A., Dumoulin, S.O. & Brewer, A.A. (2007). Visual field maps in human cortex. Neuron 56, 366–383.Google Scholar
Young, R.W. (1987). Pathophysiology of age-related macular degeneration. Survey of Ophthalmology 31, 291–306.Google Scholar
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