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Dilksetal09_JN_PRL_Supplemental.pdf1.pdf2.pdf3.pdf4.pdfBrief CommunicationsReorganization of Visual Processing in MacularDegeneration Is Not Specific to the “Preferred Retinal Locus”Daniel D. Dilks,1Chris I. Baker,2Eli Peli,3and Nancy Kanwisher11McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, and2Laboratory of Brain and Cognition,National Institute of Mental Health–National Institutes of Health, Bethesda, Maryland 20892, and3Schepens Eye Research Institute, Harvard MedicalSchool, Boston, Massachusetts 02114Recent work has shown that foveal cortex, deprived of its normal bottom-up input as a result of macular degeneration (MD), beginsresponding to stimuli presented to a peripheral retinal location. However, these studies have only presented stimuli to the “preferredretinal location,” or PRL, a spared part of the peripheral retina used by individuals with MD for fixating, face recognition, reading, andother visual tasks. Thus, previous research has not yet answered a question critical for understanding the mechanisms underlying thisreorganization: Does formerly foveal cortex respond only to stimuli presented at the PRL, or does it also respond to other peripherallocations of similar eccentricity? If foveal cortex responds to stimuli at PRL because it is the long-term habitual use of this region as afunctional fovea that drives the formerly foveal cortex to respond to stimuli presented at the PRL (the “use-dependent reorganization”hypothesis), then foveal cortex will not respond to stimuli presented at other locations. Alternatively, it may be that foveal cortex respondsto any peripheral retinal input, independent of whether input at that retinal location has been chronically attended for months or years(the “use-independent reorganization” hypothesis). Using fMRI, we found clear activation of formerly foveal cortex to stimuli presentedat either the PRL or an isoeccentric non-PRL location in two individuals with MD, supporting the use-independent reorganizationhypothesis. This finding suggests that reorganization is driven by passive, not use-dependent mechanisms.IntroductionRecent studies have demonstrated reorganization of visual pro-cessing in individuals with loss of foveal vision, and consequentloss of bottom-up input to “foveal” cortex, due to macular de-generation (MD). Specifically, in these individuals, stimuli pre-sented to a peripheral retinal location elicited responses in thedeprived cortex that would normally be responsive only to stim-uli presented to the fovea (Baker et al., 2005, 2008; Masuda et al.,2008). However, these previous studies presented stimuli only tothe “preferred retinal locus”, or PRL, which is the part of thesurviving peripheral retina chronically used as a “new fixation”center by people with MD. To test hypotheses about the mecha-nisms underlying reorganization, we ask here whether activationof formerly foveal cortex occurs only when stimuli are presentedat the PRL, or whether it is also found for stimuli presented atother peripheral locations of similar eccentricity.In individuals with MD, the PRL assumes the functional roleof the former fovea: it is the part of the retina preferentially usedfor active, attention-demanding visual tasks such as reading andface recognition (Timberlake et al., 1987). Thus, according to onehypothesis (the “use-dependent reorganization” hypothesis),formerly foveal cortex responds in MD individuals when stimuliare presented at the PRL because the PRL has become the func-tional equivalent of the fovea. In other words, it is the long-termhabitual use of this region as a functional fovea over months oryears with persistent attentional focus to stimuli at this retinallocation that drives the formerly foveal cortex to respond to stim-uli presented at the PRL. Thus, the “use-dependent reorganiza-tion” hypothesis predicts that formerly foveal cortex will not beresponsive to stimuli presented at an isoeccentric non-PRL loca-tion. However, the chronic fovea-like use of the PRL is not theonly possible cause of the observed activation of formerly fovealcortex by stimuli presented at the PRL. According to the alternate“use-independent reorganization” hypothesis, formerly fovealcortex responds to peripheral stimuli simply because the fovealregion gets no bottom-up input of its own, and peripheral regionsdo, leading the deprived foveal cortex to take any available inputfrom cortex responding to peripheral stimuli. This hypothesispredicts that stimuli presented to both PRL and non-PRL loca-tions will activate formerly foveal cortex.To distinguish between these two accounts, we tested whetherthe deprived foveal cortex responds only to stimuli presented atthe PRL (as predicted by the use-dependent reorganization hy-pothesis), or also to stimuli presented at an isoeccentric non-PRLlocation abutting the scotoma (as predicted by the use-independent reorganization hypothesis). Using functional mag-netic resonance imaging (fMRI), we found robust activation ofReceived Oct. 31, 2008; revised Jan. 9, 2009; accepted Jan. 27, 2009.This work was supported by National Institutes of Health Grants EY016559 (N.K.) and EY005957 (E.P.), by Kir-schstein National Research Service Award EY017507 (D.D.D.), by the National Institute of Mental Health IntramuralResearch Program (C.I.B.), and by Dr. Joseph Byrne and Nancy Byrne. We express our sincere thanks to the partici-pants with macular degeneration and to Bradley Berk and Jonas Kubilius for help with data collection and analyses.We also thank the Athinoula A. Martinos Imaging Center at the McGovern Institute for Brain Research, Massachu-setts Institute of Technology.Correspondence should be addressed to Daniel D. Dilks, McGovern Institute for Brain Research, MassachusettsInstitute of Technology, 46-4141, Cambridge, MA 02139. E-mail: [email protected]:10.1523/JNEUROSCI.5258-08.2009Copyright © 2009 Society for Neuroscience 0270-6474/09/292768-06$15.00/02768 • The Journal of Neuroscience, March 4, 2009 • 29(9):2768 –2773formerly foveal cortex to stimuli presented at either peripherallocation in two individuals with bilateral MD. These findings aremore consistent with the use-independent reorganization hy-pothesis than the use-dependent hypothesis, and suggest thatreorganization is driven by passive, not use-dependentmechanisms.Materials and MethodsParticipants. We tested two individuals with MD:


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