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Large-scale remapping of visual cortex is absent in adult humans with macular degeneration

Abstract

The occipital lobe contains retinotopic representations of the visual field. The representation of the central retina in early visual areas (V1–3) is found at the occipital pole. When the central retina is lesioned in both eyes by macular degeneration, this region of visual cortex at the occipital pole is accordingly deprived of input. However, even when such lesions occur in adulthood, some visually driven activity in and around the occipital pole can be observed. It has been suggested that this activity is a result of remapping of this area so that it now responds to inputs from intact, peripheral retina. We evaluated whether or not remapping of visual cortex underlies this activity. Our functional magnetic resonance imaging results provide no evidence of remapping, questioning the contemporary view that early visual areas of the adult human brain have the capacity to reorganize extensively.

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Figure 1: Cortical responses to visual stimulation.
Figure 2: Mean coherences for each ROI, averaged across individuals for each group.
Figure 3: Simulating retinal lesions in a control subject.
Figure 4: Occipital lobe responses compared across groups and ROIs.
Figure 5: Receptive field characteristics.
Figure 6: Individual eccentricity maps.
Figure 7: The cortical area representing intact visual field.

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References

  1. Wandell, B.A., Dumoulin, S.O. & Brewer, A.A. Visual field maps in human cortex. Neuron 56, 366–383 (2007).

    Article  CAS  Google Scholar 

  2. Morland, A.B., Baseler, H.A., Hoffmann, M.B., Sharpe, L.T. & Wandell, B.A. Abnormal retinotopic representations in human visual cortex revealed by fMRI. Acta Psychol. (Amst.) 107, 229–247 (2001).

    Article  CAS  Google Scholar 

  3. Hoffmann, M.B., Tolhurst, D.J., Moore, A.T. & Morland, A.B. Organization of the visual cortex in human albinism. J. Neurosci. 23, 8921–8930 (2003).

    Article  CAS  Google Scholar 

  4. Muckli, L., Naumer, M.J. & Singer, W. Bilateral visual field maps in a patient with only one hemisphere. Proc. Natl. Acad. Sci. USA 106, 13034–13039 (2009).

    Article  CAS  Google Scholar 

  5. Levin, N., Dumoulin, S.O., Winawer, J., Dougherty, R.F. & Wandell, B.A. Cortical maps and white matter tracts following long period of visual deprivation and retinal image restoration. Neuron 65, 21–31 (2010).

    Article  CAS  Google Scholar 

  6. Baseler, H.A. et al. Reorganization of human cortical maps caused by inherited photoreceptor abnormalities. Nat. Neurosci. 5, 364–370 (2002).

    Article  CAS  Google Scholar 

  7. Kaas, J.H. et al. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229–231 (1990).

    Article  CAS  Google Scholar 

  8. Heinen, S.J. & Skavenski, A.A. Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey. Exp. Brain Res. 83, 670–674 (1991).

    Article  CAS  Google Scholar 

  9. Chino, Y.M., Kaas, J.H., Smith, E.L. III, Langston, A.L. & Cheng, H. Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina. Vision Res. 32, 789–796 (1992).

    Article  CAS  Google Scholar 

  10. Gilbert, C.D. & Wiesel, T.N. Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152 (1992).

    Article  CAS  Google Scholar 

  11. Darian-Smith, C. & Gilbert, C.D. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15, 1631–1647 (1995).

    Article  CAS  Google Scholar 

  12. Kaas, J.H. Sensory loss and cortical reorganization in mature primates. Prog. Brain Res. 138, 167–176 (2002).

    Article  Google Scholar 

  13. Giannikopoulos, D.V. & Eysel, U.T. Dynamics and specificity of cortical map reorganization after retinal lesions. Proc. Natl. Acad. Sci. USA 103, 10805–10810 (2006).

    Article  CAS  Google Scholar 

  14. Sunness, J.S., Liu, T. & Yantis, S. 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 (2004).

    Article  Google Scholar 

  15. Baker, C.I., Peli, E., Knouf, N. & Kanwisher, N.G. Reorganization of visual processing in macular degeneration. J. Neurosci. 25, 614–618 (2005).

    Article  CAS  Google Scholar 

  16. Schumacher, E.H. et al. Reorganization of visual processing is related to eccentric viewing in patients with macular degeneration. Restor. Neurol. Neurosci. 26, 391–402 (2008).

    PubMed  Google Scholar 

  17. Cowey, A. & Walsh, V. Magnetically induced phosphenes in sighted, blind and blindsighted observers. Neuroreport 11, 3269–3273 (2000).

    Article  CAS  Google Scholar 

  18. Masuda, Y., Dumoulin, S.O., Nakadomari, S. & Wandell, B.A. V1 projection zone signals in human macular degeneration depend on task, not stimulus. Cereb. Cortex 18, 2483–2493 (2008).

    Article  Google Scholar 

  19. Wandell, B.A. & Smirnakis, S.M. Plasticity and stability of visual field maps in adult primary visual cortex. Nat. Rev. Neurosci. 10, 873–884 (2009).

    Article  CAS  Google Scholar 

  20. Masuda, Y. et al. Task-dependent V1 responses in human retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 51, 5356–5364 (2010).

    Article  Google Scholar 

  21. DeYoe, E.A. et al. Mapping striate and extrastriate visual areas in human cerebral cortex. Proc. Natl. Acad. Sci. USA 93, 2382–2386 (1996).

    Article  CAS  Google Scholar 

  22. Engel, S.A., Glover, G.H. & Wandell, B.A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7, 181–192 (1997).

    Article  CAS  Google Scholar 

  23. Engel, S.A. et al. fMri of human visual cortex. Nature 369, 525 (1994).

    Article  CAS  Google Scholar 

  24. Sereno, M.I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).

    Article  CAS  Google Scholar 

  25. Smirnakis, S.M. et al. Lack of long-term cortical reorganization after macaque retinal lesions. Nature 435, 300–307 (2005).

    Article  CAS  Google Scholar 

  26. Baker, C.I., Dilks, D.D., Peli, E. & Kanwisher, N. Reorganization of visual processing in macular degeneration: replication and clues about the role of foveal loss. Vision Res. 48, 1910–1919 (2008).

    Article  Google Scholar 

  27. Crossland, M.D., Morland, A.B., Feely, M.P., von dem Hagen, E. & Rubin, G.S. The effect of age and fixation instability on retinotopic mapping of primary visual cortex. Invest. Ophthalmol. Vis. Sci. 49, 3734–3739 (2008).

    Article  Google Scholar 

  28. Parrish, T.B., Gitelman, D.R., LaBar, K.S. & Mesulam, M.M. Impact of signal-to-noise on functional MRI. Magn. Reson. Med. 44, 925–932 (2000).

    Article  CAS  Google Scholar 

  29. Cavanaugh, J.R., Bair, W. & Movshon, J.A. Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J. Neurophysiol. 88, 2530–2546 (2002).

    Article  Google Scholar 

  30. Dumoulin, S.O. & Wandell, B.A. Population receptive field estimates in human visual cortex. Neuroimage 39, 647–660 (2008).

    Article  Google Scholar 

  31. Andrews, T.J., Halpern, S.D. & Purves, D. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 17, 2859–2868 (1997).

    Article  CAS  Google Scholar 

  32. Hubel, D.H. & Wiesel, T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206, 419–436 (1970).

    Article  CAS  Google Scholar 

  33. Hubel, D.H., Wiesel, T.N. & LeVay, S. Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. R. Soc. Lond. B 278, 377–409 (1977).

    Article  CAS  Google Scholar 

  34. Le Vay, S., Wiesel, T.N. & Hubel, D.H. The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191, 1–51 (1980).

    Article  CAS  Google Scholar 

  35. Horton, J.C. & Hocking, D.R. Timing of the critical period for plasticity of ocular dominance columns in macaque striate cortex. J. Neurosci. 17, 3684–3709 (1997).

    Article  CAS  Google Scholar 

  36. Williams, M.A. et al. Feedback of visual object information to foveal retinotopic cortex. Nat. Neurosci. 11, 1439–1445 (2008).

    Article  CAS  Google Scholar 

  37. Angelucci, A. & Bullier, J. Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? J. Physiol. (Paris) 97, 141–154 (2003).

    Article  Google Scholar 

  38. Angelucci, A. & Sainsbury, K. Contribution of feedforward thalamic afferents and corticogeniculate feedback to the spatial summation area of macaque V1 and LGN. J. Comp. Neurol. 498, 330–351 (2006).

    Article  Google Scholar 

  39. Lund, J.S. Anatomical organization of macaque monkey striate visual cortex. Annu. Rev. Neurosci. 11, 253–288 (1988).

    Article  CAS  Google Scholar 

  40. Gilbert, C.D. & Wiesel, T.N. Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120–125 (1979).

    Article  CAS  Google Scholar 

  41. Dougherty, R.F. et al. Visual field representations and locations of visual areas V1/2/3 in human visual cortex. J. Vis. 3, 586–598 (2003).

    Article  Google Scholar 

  42. Horton, J.C. & Hocking, D.R. 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. J. Neurosci. 18, 5433–5455 (1998).

    Article  CAS  Google Scholar 

  43. Liu, T. et al. Incomplete cortical reorganization in macular degeneration. Invest. Ophthalmol. Vis. Sci. 51, 6826–6834 (2010).

    Article  Google Scholar 

  44. Boucard, C.C. et al. Changes in cortical grey matter density associated with long-standing retinal visual field defects. Brain 132, 1898–1906 (2009).

    Article  Google Scholar 

  45. Teo, P.C., Sapiro, G. & Wandell, B.A. Creating connected representations of cortical gray matter for functional MRI visualization. IEEE Trans. Med. Imaging 16, 852–863 (1997).

    Article  CAS  Google Scholar 

  46. Wandell, B.A., Chial, S. & Backus, B.T. Visualization and measurement of the cortical surface. J. Cogn. Neurosci. 12, 739–752 (2000).

    Article  CAS  Google Scholar 

  47. Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825–841 (2002).

    Article  Google Scholar 

  48. Wandell, B.A., Brewer, A.A. & Dougherty, R.F. Visual field map clusters in human cortex. Phil. Trans. R. Soc. Lond. B 360, 693–707 (2005).

    Article  Google Scholar 

  49. Lewis, S.M. et al. Logarithmic transformation for high-field BOLD fMRI data. Exp. Brain Res. 165, 447–453 (2005).

    Article  Google Scholar 

  50. Winawer, J., Horiguchi, H., Sayres, R.A., Amano, K. & Wandell, B.A. Mapping hV4 and ventral occipital cortex: the venous eclipse. J. Vis. 10, 1–22 (2010).

    Article  Google Scholar 

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Acknowledgements

We would like to thank all of our participants. We thank Edward Silson for constructive discussion of the manuscript. We are also grateful to the Medical Research Council for funding this study (G0401339). K.V.H. and F.W.C. were supported by a grant from Stichting Nederlands Oogheelkundig Onderzoek and by European Union grants #043157 (Syntex) and #043261 (Percept). A.T., G.S.R. and M.D.C. also received financial support from the Department of Health through an award made by the National Institute for Health Research to Moorfields Eye Hospital National Health Service (NHS) Foundation Trust and University College London Institute of Ophthalmology for a Specialist Biomedical Research Centre for Ophthalmology. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research, the Department of Health or the EU commission.

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H.A.B. and A.G. acquired and analyzed the neuroimaging data and prepared the manuscript. K.V.H. designed and implemented an analysis to determine the population receptive field characteristics and prepared the manuscript. C.R. acquired neuroimaging data. M.D.C. recruited patients, acquired and analyzed clinical data. A.T. recruited and assessed patients. G.S.R. jointly designed the study, recruited patients and acquired and analyzed clinical data. F.W.C. designed an analysis to determine the population receptive field characteristics and prepared the manuscript. A.B.M. jointly designed the study, acquired and analyzed the neuroimaging data and prepared the manuscript. All authors contributed to drafts of the manuscript.

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Correspondence to Antony B Morland.

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Baseler, H., Gouws, A., Haak, K. et al. Large-scale remapping of visual cortex is absent in adult humans with macular degeneration. Nat Neurosci 14, 649–655 (2011). https://doi.org/10.1038/nn.2793

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